A Monograph of Paris (Melanthiaceae): Morphology, Biology, Systematics and Taxonomy 9789811579028

Table of contents :
Preface
Acknowledgements
Contents
Chapter 1: Introduction: Taxonomic History
1.1 Establishment of the Genus
1.2 Affinities
1.3 History of Species Discoveries
1.4 Generic Circumscription and Subdivision
1.5 Issues to Be Resolved
References
Chapter 2: Morphology
2.1 Gross Morphology
2.1.1 Rhizome
2.1.2 Mycorrhiza
2.1.3 Leaves
2.1.4 Flower
2.1.5 Fruit
2.1.6 Seeds
2.1.7 Taxonomic Significance
2.2 Pollen Morphology
2.2.1 Pollen Size, Shape, and Ornamentation
2.2.2 Taxonomic Implications
References
Chapter 3: Biology
3.1 Distribution and Habitat
3.2 Phenology
3.3 Propagation and Growth
3.3.1 Pollination
3.3.2 Seed Production
3.3.3 Seed Dispersal
3.3.4 Life Cycle
3.4 Chromosomes
3.4.1 Karyotype
3.4.2 B Chromosomes
3.4.3 Chromosome Evolution
3.5 Genomes
3.5.1 Genome Size
3.5.2 Possible Mechanisms Underlying the Formation of Large Genomes
3.5.3 Plastid Genomes
3.5.3.1 General Features
3.5.3.2 Pseudogenization of Plastid cemA
3.5.3.3 Hotspots of Sequence Variation
References
Chapter 4: Economic Importance
4.1 Medicinal Importance
4.1.1 Overall Information
4.1.2 Traditional Uses and Ethnopharmacological Properties
4.2 Horticultural Potential
4.2.1 P. cronquistii (Takht.) H. Li
4.2.2 P. delavayi Franch
4.2.3 P. lancifolia Hayata
4.2.4 P. luquanensis H. Li
4.2.5 P. marmorata Stearn
4.2.6 P. yunnanensis Franch
4.3 Phytochemistry
4.3.1 Steroidal Saponins
4.3.2 Phytoecdysones
4.3.3 Phytosterols
4.3.4 Flavonoids
4.3.5 Triterpenoid Saponins
4.3.6 Others
4.4 Pharmaceutical Prospects
4.4.1 Anti-Tumor
4.4.2 Hemostatic Activity
4.4.3 Uterine Contractile Agonistic Activity
4.4.4 Antimicrobial
4.4.5 Other Activities
References
Chapter 5: Phylogeny, Classification, Biogeography, and Evolution
5.1 Ancient and Recent Hybridization
5.2 Generic Circumscription
5.3 Infrageneric Classification
5.4 Historical Biogeography
5.5 Species Diversification
5.6 Origin and Evolution of Genomic Gigantism
References
Chapter 6: Taxonomic Revision
6.1 Section Paris
6.2 Section Kinugasa
6.3 Section Thibeticae
6.4 Section Axiparis
6.5 Section Euthyra
References
Chapter 7: Conservation Considerations
7.1 Conservation Status
7.1.1 Species Rarity
7.1.2 Extinction Risk
7.2 Principal Threats
7.2.1 Commercial Collecting
7.2.2 Arbitrary Introduction
7.2.3 Habitat Degradation
7.3 Conservation Priorities
7.4 Conservation Strategies
7.4.1 Commercial Cultivation
7.4.2 In situ Conservation
7.4.3 Ex situ Conservation
References

Citation preview

Yunheng Ji

A Monograph of Paris (Melanthiaceae) Morphology, Biology, Systematics and Taxonomy

A Monograph of Paris (Melanthiaceae)

Yunheng Ji

A Monograph of Paris (Melanthiaceae) Morphology, Biology, Systematics and Taxonomy

Yunheng Ji Kunming Institute of Botany Chinese Academy of Sciences Kunming, Yunnan, China In association with: Zhenyan Yang, Jin Yang, Lingling Yu, Haiyang Liu, Junbo Yang, Lifang Yang, Changkun Liu, Min Shen, Lei Jin and Shuying Wang.

ISBN 978-981-15-7902-8 ISBN 978-981-15-7903-5 https://doi.org/10.1007/978-981-15-7903-5

(eBook)

# Science Press 2021 The print edition is not for sale in the Mainland of China. Customers from the Mainland of China please order the print book from: Science Press. Jointly published with Science Press. This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore

Dedicated to my professors, Heng Li, Shengji Pei, and Zhekun Zhou, as well as to my family.

Preface

Paris Linn. is a morphologically distinctive genus belonging to the monocotyledonous family Melanthiaceae (Liliales), according to the updated classification of the Angiosperm Phylogeny Group. Species of this genus are widely distributed throughout Eurasia, entering the Arctic at the northernmost limit and reaching Hainan Island and Indochina at the southernmost limit. Nearly all Paris species with a thick rhizome (medicinal Paris) are traditionally used as medicinal herbs in China, Bhutan, India, Myanmar, Nepal, and Vietnam, owing to their analgesic, hemostatic, anti-tumor, and anti-inflammatory activities. To date, approximately 90 commercial drugs and health products have been developed in China using the rhizomes of medicinal Paris as raw materials. It is estimated that the income generated by the sale of these drugs and products is approximately 10 billion CNY (ca. 1.6 billion USD) per year. Despite the great economic importance of the Paris species, the taxonomy of the genus Paris remains controversial. First, the circumscription of this genus, long in dispute, has not been satisfactorily resolved. Historically, Paris was recognized as either a single genus or divided into three narrowly defined genera (Daiswa, Kinugasa, and Paris s.s.) by different researchers. Similarly, previous phylogenetic analyses of Paris based on different DNA sequence datasets have yielded conflicting results. Second, the infrageneric classification of Paris is still questionable and controversial. To date, five infrageneric systems have been outlined, in which a total of two subgenera and eight sections have been recognized. It remains unclear how many subgenera and sections should be recognized within this genus, and what are the evolutionary relationships among them. Third, the taxonomy of Paris is very complicated because of the diversity and plasticity of morphological characteristics at the species level. Approximately 95 taxa have been described to date. Although four major taxonomical revisions have been done on Paris since 1888, they are greatly contradictory in delineating species. As a result, the alpha taxonomy of Paris remains uncertain. To understand the true species diversity in this genus, a comprehensive taxonomic revision is urgently needed. Under the supervision of Prof. Heng Li, who has carried out the most recent and comprehensive taxonomic revision on this genus, my monographic study on the genus Paris was initiated in 2002 when I was a Ph.D. student. During the past 18 years, I have conducted extensive field observations and collections in China and neighboring countries and have examined thousands of specimens (and specimen photos) from 88 herbaria worldwide. I have investigated the general morphology, pollen morphology, and genome size of Paris species. With the advent of next-generation DNA sequencing technologies, I generated complete plastid genomes and nuclear ribosomal DNA sequences, to reconstruct phylogenies and to assess the species delineation in this genus. Consequently, most of the taxonomic issues mentioned above have been satisfactorily elucidated. This monograph outlines a revised infrageneric system of Paris that includes five sections. Based on infrageneric evolutionary relationships and molecular dating, the biogeographic scenario of genus Paris is proposed. This book, which includes seven chapters, provides essential knowledge on the taxonomic history, morphology, biology, economic importance, phytochemistry, pharmaceutical

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Preface

prospects, origin, evolution, lineage diversification, biogeography, taxonomy, and conservation of the genus Paris, as well as the description, characteristics, illustration, and distribution of each species. Given the great economic importance of this genus, such knowledge will be conducive to the exploration and protection of Paris species. Kunming, China December 12, 2019

Yunheng Ji

Acknowledgements

This monographic study of Paris was jointly supported by the National Natural Science Foundation of China (30670312, 31070297, 31770391, and 31872683); the NSFC-Joint Foundation of Yunnan Province (U1802287); the Major Program of National Natural Science Foundation of China (31590820 and 31590823); a grant from the Large-Scale Scientific Facilities of the Chinese Academy of Sciences (No. 2017-LSF-GBOWS-02); and the open research project of “Cross-Cooperative Team” of the Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences. The present work was accomplished with the assistance of many people. First, I should express my sincere thanks to Chengjin Yang, Guohua Zhou, Rong Li, Zhiling Dao, Sirong Yi, Qiliang Gan, Tingzhou Zhao, Ren Zhao, Zhangming Wang, Yongxing Xiong, Tai Su, Yuling Huang, Xiaochun Shi, Qiuping Tan, Liangxue Sun, Shaotian Chen, Wenyun Chen, Tao Su, Yongjiang Huang, Ying Yang, Yanhong Zhai, Haicheng An, Yuhua Li, Yulong Li, and Benxi Liu for their invaluable help with the field observations and specimen collections. My sincere thanks also go out to Royal Botanic Garden (Edinburg), P. Bruggeman, J. Marata, J. McClments, and W. B. Zomlefer for providing DNA samples of Paris and related plant taxa. Deserving special thanks are Zhirong Zhang, Jing Yang, and Zhengshan He for their help with the molecular experiments, Drs. Jianjun Jin, Jiahui Chen, and Hongtao Li for their assistance in data analysis, Zhijia Gu for helping with the microscopic investigation of pollen morphology, and Yanxia Jia for measuring the genome sizes of Paris species. I would like to thank all staff at the herbaria BJM, CDBI, HIB, HITBC, HWA, IBK, IGA, IMC, IMDY, KUN, LBG, LZU, NAS, PE, SYS, SZ, WUK, and YUKU for accommodating my examination of their specimens and to curators of the herbaria B, BN, E, GH, K, and MO for providing specimens on loan or specimen photographs. Finally, during the last 10 years, my students have made great contributions to this book, without their assistance and comments, this book would never have been written.

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Contents

1

Introduction: Taxonomic History . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1 Establishment of the Genus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 Affinities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3 History of Species Discoveries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.4 Generic Circumscription and Subdivision . . . . . . . . . . . . . . . . . . . . . . . . . 1.5 Issues to Be Resolved . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1 1 1 3 8 9 10

2

Morphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Gross Morphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.1 Rhizome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.2 Mycorrhiza . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.3 Leaves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.4 Flower . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.5 Fruit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.6 Seeds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.7 Taxonomic Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Pollen Morphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.1 Pollen Size, Shape, and Ornamentation . . . . . . . . . . . . . . . . . . . . . 2.2.2 Taxonomic Implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

13 13 13 14 14 14 16 17 17 19 19 30 30

3

Biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Distribution and Habitat . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Phenology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Propagation and Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.1 Pollination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.2 Seed Production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.3 Seed Dispersal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.4 Life Cycle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4 Chromosomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.1 Karyotype . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.2 B Chromosomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.3 Chromosome Evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5 Genomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5.1 Genome Size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5.2 Possible Mechanisms Underlying the Formation of Large Genomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5.3 Plastid Genomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

33 33 33 34 34 35 35 36 36 37 37 40 42 42 45 45 51

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4

Economic Importance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 Medicinal Importance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.1 Overall Information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.2 Traditional Uses and Ethnopharmacological Properties . . . . . . . . . 4.2 Horticultural Potential . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.1 P. cronquistii (Takht.) H. Li . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.2 P. delavayi Franch . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.3 P. lancifolia Hayata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.4 P. luquanensis H. Li . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.5 P. marmorata Stearn . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.6 P. yunnanensis Franch . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3 Phytochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.1 Steroidal Saponins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.2 Phytoecdysones . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.3 Phytosterols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.4 Flavonoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.5 Triterpenoid Saponins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.6 Others . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4 Pharmaceutical Prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4.1 Anti-Tumor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4.2 Hemostatic Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4.3 Uterine Contractile Agonistic Activity . . . . . . . . . . . . . . . . . . . . . 4.4.4 Antimicrobial . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4.5 Other Activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . .

55 55 55 55 56 56 56 56 58 58 60 61 62 63 63 63 63 64 64 64 64 65 65 65 65

5

Phylogeny, Classification, Biogeography, and Evolution . . . . . . . . . . . . . . . 5.1 Ancient and Recent Hybridization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2 Generic Circumscription . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3 Infrageneric Classification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4 Historical Biogeography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5 Species Diversification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.6 Origin and Evolution of Genomic Gigantism . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . .

69 69 72 72 74 77 77 79

6

Taxonomic Revision . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1 Section Paris . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2 Section Kinugasa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.3 Section Thibeticae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.4 Section Axiparis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.5 Section Euthyra . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . .

83 84 105 106 111 122 192

7

Conservation Considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1 Conservation Status . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1.1 Species Rarity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1.2 Extinction Risk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2 Principal Threats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2.1 Commercial Collecting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2.2 Arbitrary Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2.3 Habitat Degradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3 Conservation Priorities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.4 Conservation Strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . .

193 193 193 194 195 195 197 199 199 199

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7.4.1 7.4.2 7.4.3 References .

Commercial Cultivation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . In situ Conservation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ex situ Conservation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .................................................

. . . .

199 201 202 202

1

Introduction: Taxonomic History

1.1

Establishment of the Genus

Linnaeus (1753) established Paris as a genus, and described Paris quadrifolia (Fig. 1.1) as the type species. Paris is a morphologically distinctive lineage in flowering plants. All species in the genus share the morphological characters of a whorl of 4 to 15 net-veined leaves and a solitary flower developing at the apex of the stem. These morphological features make it easy to distinguish Paris from other plant groups. The genus name, Paris, is derived from the Latin root “par-” and refers to whorled sepals parallel to a whorl of leaves. In China, the genus Paris had the name Chonglou, which was given by Mao Lan (1397–1470), a Ming-era

scholar, in his book South Yunnan Herbals, and this description similarly refers to parallel sepals and leaves. Paris species are also called Qi-Ye-Yi-Zhi-Hua in China, which refers to a solitary flower emerging from a whorl of leaves at the apex of the stem. These names precisely represent the unique morphologies of Paris species (Fig. 1.2).

1.2

Affinities

Due to its distinctive morphology, Paris is easy to recognize but difficult to place. After the initial recognition of the genus by Linnaeus in 1753, it has been placed in five families and

Fig. 1.1 Image of Paris quadrifolia # Science Press 2021 Y. Ji, A Monograph of Paris (Melanthiaceae), https://doi.org/10.1007/978-981-15-7903-5_1

1

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1 Introduction: Taxonomic History

Fig. 1.2 Representative Paris species in China: Paris chinensis (a), P. polyphylla (b), and P. yunnanensis (c)

been considered a member of seven orders in the major classifications of flowering plants. First, Paris was placed in Liliaceae by De-Jusseau (1789). Du-Mortier (1829) compared the morphological characteristics of all lilioid genera known at that time. He found that the genera Paris, Trillium Linn., and Medeola Linn. share similar morphological features of whorled leaves and flower (or flowers) developing at the top of stem, which are significantly different from all other lilioids. He thus described a new family, Paridaceae, which included Paris, Trillium, and Medeola. Based on Paridaceae, the monotypic order Paridales was established. However, Endlicher (1836– 1840) considered that Paris, Trillium, and Medeola have broad and net-veined leaves, which may indicate that they belong to Smilacaceae. He reduced the family Paridaceae to the tribe Parideae and moved it into Smilacaceae. This classification was adopted by Kunth (1850). However, Lindley (1846) pointed out that the two tiers of whorled leaves and multiple flowers in Medeola are different from the whorled leaves and single flower in Paris and Trillium. Therefore, he established a new family, Trilliaceae, which included Paris and Trillium; in this classification, Trilliaceae was treated as a member of Dioscorales. Watson (1879) investigated the morphologies of Paris, Trillium, Medeola, and Scoliopus. He proposed that these genera are characterized by their opposite or whorled leaves and a flower developing at the stem apex, and he thus grouped them into a new tribe, Trilleae, in Liliaceae. Similarly, Bentham and Hooker (1883) placed Paris in Liliaceae. However, they described a new tribe, Medeoleae, to accommodate the genera Medeola, Paris, Trillium, Scoliopus, and Clintonia. Because Clintonia species have 2–6 basal leaves and an inflorescence arising from the rhizome crown (vs. two basal leaves and a flower at the top of rhizome in Scoliopus), it was proposed that is closely related to Scoliopus. Although Engler (1888) retained Paris in Liliaceae and reduced both

tribes Trilleae and Medeoleae to synonyms of Parideae, he moved both Scoliopus and Clintonia out of this tribe. Hutchinson (1926) adopted the family Trilliaceae, recognized by Lindley (1846), which included Paris and Trillium. However, the circumscription of the family was enlarged to accommodate two more genera, Medeola and Scoliopus. In this classification, Trilliaceae was put in Liliales. This delineation of Trilliaceae was adopted by Willis (1973), Huber (1969), Dahlgren (1975), and Watson and Dallwitz (1991). However, the family Trilliaceae was placed in Stemonales by Huber (1977) and Dahlgren (1975) but in Dioscorales by Watson and Dallwitz (1991). In the classifications of Rendle (1930) and Cronquist (1968), Paris was regarded as part of Liliaceae. By contrast, Takhtajan (1959, 1980, 1987, 1997) followed the circumscription of Trilliaceae by Lindley (1846), in which Paris and Trillium were included in it. The family was placed in either Dioscorales (Takhtajan 1980), Smilicales (Takhtajan 1959, 1987), or Trillales (Takhtajan 1997). The family Trilliaceae, as recognized by Thorne (1992), includes Paris and Trillium, which matches the taxonomic treatment of Lindley (1846) and Takhtajan (1959, 1980, 1987, 1997). However, Thorne (1992) placed Trilliaceae in Liliales. Recent phylogenetic analyses using DNA sequences have indicated that the most closely related genus to Paris is Trillium, and the two genera are phylogenetically distinct from Medeola, Scoliopus, and Clintonia. These studies have indicated that Paris and Trillium are not part of Liliaceae or Smilacaceae, and under the principle of monophyly the two genera should be placed in Melanthiaceae (Zomlefer et al. 2001, 2006). The Angiosperm Phylogeny Group (1998, 2003, 2009, 2016) followed this treatment to place Paris and Trillium in Melanthiaceae. Recent molecular phylogenetic studies indicated that Paris is a sister genus to Trillium, forming a well-supported lineage, Parideae in Melanthiaceae (Zomlefer et al. 2001, 2006; Kim et al. 2013, 2016, 2019; Huang et al. 2016; Ji et al. 2006a, 2019; Yang et al. 2019a).

1.3 History of Species Discoveries

1.3

History of Species Discoveries

Linnaeus (1753) described the first species in the genus, Paris quadrifolia, which is found in Europe. Based on collections from France, Renault (1804) described two species, P. trifolia and P. pentafolia. Both were treated as synonyms of P. quadrifolia by Franchet (1888a, b). Bieberstein (1808) described Paris incompleta as a new species from the Caucasus. It is distinctive in the genus in its 6–12 leaves, absent petals, and globose berry. Hoffman described Paris apetala and P. octophylla as new species from Armenia. Both species were reduced to synonyms of P. incompleta by Franchet (1888a). Bieberstein (1819) described P. verticillata as a new species based on collections from Siberia. The species is morphologically similar to P. incompleta but can be distinguished by its obovate to obovate-lanceolate leaves, presence of petals, and the long (5.0–8.0 mm) free portion of connective. P. polyphylla was described by Smith (1819), based on collection from Nepal. It is one of the most taxonomically difficult species in the genus, due to its high levels of morphological variation. The species is distinct from other Paris species known at that time in having thick rhizome and producing capsule fruit. Ledebour (1828) described P. obovata as a new species from the Russian Far East. Regel and Tiling (1888) treated it as a conspecific variety of P. quadrifolia, while Hara (1969) considered it a variety of P. verticillata. However, Wang and Tang (1978) reduced it to a synonym of P. verticillata. Subsequently, von Chamisso (1831) described a new species from Siberia, Paris hexaphylla. Franchet (1888b) reduced it to a synonym of P. verticillata. Fedtschenko (1912) combined it with P. quadrifolia as a conspecific variety, which was treated as a synonym of P. verticillata by Hara (1969). Fischer (1854) described Paris dahurica as a new species from Stanovoy. Franchet (1888a) combined it to P. quadrifolia as a conspecific variety, while Hara (1969) reduced it to a synonym of P. verticillata. Gray described P. tetraphylla as a new species from Japan. Morphologically, it is close to P. quadrifolia in its 4merous phyllotaxy, but it differs in that its petals are usually absent. Franchet and Salisbury described Trillidium japonicum based on collections from Japan, and it was transferred to Paris (P. japonica) by Franchet (1888a). These two distinct species are endemic to Japan. Based on specimens collected by J. M. Delavay, and A. David in southwest China, Franchet (1888c) described three new species, P. chinensis, P. thibetica, P. yunnanensis, and a conspecific variety of P. polyphylla (P. polyphylla var. stenophylla). P. yunnanensis was transferred to P. polyphylla as a variety by Handel-Mazzetti (1936), while Takhtajan recovered its status as a species and transferred it to Daiswa.

3

P. chinensis was also treated as a variety of P. polyphylla by Hara (1969). Similarly, Takhtajan (1983) recovered its status as a species and combined it with Daiswa. Although P. thibetica was recognized as a variety of P. polyphylla by Hara (1969), this treatment was not accepted by Li (1984a, 1986, 1998). Takhtajan (1983), however, transferred it to Daiswa, and reduced P. polyphylla var. stenophylla as a synonym of P. lancefolia and transferred it to Daiswa. Franchet (1898) examined collections by J. M. Delavay, R. P. Farges, and A. David from China and recognized two new species, P. delavayi and P. fargesii, as well as three varieties, P. polyphylla var. branchystemon, P. polyphylla var. platypetala, and P. quadrifolia var. setchuanensis. P. polyphylla var. platypetala was reduced to P. polyphylla var. chinensis by Hara (1969). P. fargesii was recognized as a subspecies of P. polyphylla by Hara (1969), while Wang and Tang (1978), Takhtajan (1983), and Li (1984a, 1986, 1998) recovered its status as a species. P. polyphylla var. branchystemon and P. quadrifolia var. setchuanensis were treated as synonyms of P. polyphylla var. stenophylla and P. bashanensis by Wang and Tang (1978). Diels (1900) described P. bockiana and P. henryi as new from China. These were reduced to P. polyphylla var. chinensis and P. polyphylla subsp. fargesii by Hara (1969). Takhtajan (1983) argued that P. bockiana should be recognized as a distinct species (Daiswa bockiana) and reduced P. henryi to P. delavayi. Li (1986) reduced P. bockana (= D. bockiana) to P. polyphylla var. stenophylla, whereas I found that it should be conspecific with P. delavayi. Wright (1903) recognized a new species, P. petiolata, with the variety P. petiolata var. membranacea, from China. These were reduced to P. polyphylla subsp. fargesii by Hara (1969). Wang and Tang (1978) recognized P. petiolate var. membranacea as a synonym of P. fargesii, and treated P. petiolata as a variety of P. fargesii. However, Li (1998) combined P. petiolata with P. delavayi as a conspecific variety. Léveillé (1903, 1906, 1909, 1910, 1913) described 16 new species in Paris (P. christii, P. franchetiana, P. mercieri, P. cavalerier, P. debeauxii, P. gigas, P. vaniotii, P. aprica, P. hookeri, P. pinfaensis, P. dunniana, P. mairei, P. violacea, P. atrata, P. hamifer, and P. marchandii). Hara (1969) reviewed Leveille’s publications and relevant specimens and reduced P. debeauxii, P. vaniotii, P. dunniana, and P. mairei to P. polyphylla var. polyphylla; P. christii, P. franchetiana, P. mercieri, P. cavalerier, P. gigas, P. aprica, P. pinfaensis, P. atrata, and P. marchandii to P. polyphylla var. yunnanensis; P. hamifer to P. polyphylla var. stenophylla; and P. hookeri to P. polyphylla subsp. fargesii. However, the status of P. dunniana, P. mairei, P. vaniotii, and P. violacea remains controversial. Takhtajan (1983) recovered P. dunniana as a distinctive species; Li (1984a, 1986) retained the species in Paris and presented a supplemental

4

description. Also, there has been much debate over whether P. vaniotii, which was synonymized by Hara (1969), Wang and Tang (1978), and Takhtajan (1983), is a distinct species. However, Li (1984a, 1986, 1998) argued that it should be a distinct species due to its possession of a four- to sevenloculed ovary, axile placentation, and oblong to oblanceolate leaf blade. Likewise, there is dispute over the taxonomic treatment of P. mairei and P. violacea, whose types were collected from the same locality (Dongchuan, Yunnan, China) and with successive collection numbers (E. E. Maire 7457 for P. mairei and E. E. Maire 7458 for P. violacea). It is noteworthy that Li (1986) found that the types had similar floral and vegetative morphologies, and the unique character that the leaves have short hair abaxially, suggesting that they represent the same species; therefore, she reduced P. violacea to a synonym of P. mairei. Although Wang and Tang (1978) also recognized P. violacea as a distinct species, and Takhtajan (1983) accepted the treatment and transferred it to Daiswa, they, unfortunately, did not treat P. mairei as a synonym. Here, I follow the treatment of Li (1986) and recognize P. violacea as a synonym of P. mairei. Hayata (1906) recognized P. lancifolia, based on specimens collected from China, which was reduced to the third synonym of P. polyphylla var. stenophylla by Hara (1969). Takhtajan (1983) recovered its taxonomic rank as a species and then transferred it to Daiswa. This species is distinctive in the genus in its linear or narrowly lanceolate (or oblanceolate) leaves. Based on a specimen from Hubei, central China, Pampanini (1919) published P. biondii, which was treated as a synonym of P. polyphylla by Hara (1969). Hayata (1911) recognized P. formosana from China as a new species, but it was reduced to a synonym of P. polyphylla var. chinensis by Hara (1969). Pampanini (1915) described P. brachysepala based on a specimen collected from Hubei, China. The species was ignored by most later authors, except for Takhtajan (1983), who reduced it to P. chinensis. Hayata (1920) described P. arisanensis as a new species, based on a specimen collected from China. This species was treated as a synonym of P. polyphylla var. stenophylla by Hara (1969). Merrill (1923) published P. hainanensis as a new species, based on a specimen from Hainan Island, south China. Hara (1969) reduced it to a synonym of P. polyphylla var. chinensis. Takhtajan (1983) retained its status as a species, while Li (1986) reduced it to a synonym of P. dunniana. I critically examined collections from Hainan Island and found that they exhibited high levels of morphological similarity to P. dunniana, justifying the propose that P. hainanensis is conspecific with P. dunniana (Li 1986, 1998). Handel-Mazzetti (1925) described two new varieties, P. polyphylla var. pubescens and P. thibetica var. apetala. The former was raised to the specific rank by Wang and Tang (1978). Li (1986), however, reduced it to a synonym of P. mairei. I found that the characteristic absence (or presence) of petals is not always present during the life history of a given

1 Introduction: Taxonomic History

P. thibetica individual, suggesting that P. thibetica var. apetala should be reduced as a synonym of P. thibetica. Komarov and Alissova-Klobukova published Paris manshurica as a new species from the Russian Far East. Hara (1969) and Voroschilov (1972) combined it with P. verticillata and P. hexaphylla, respectively, as a variety. However, Wang and Tang (1978) reduced it to P. verticillata. This treatment was followed by Li (1984a, 1986, 1998). I examined the original description of P. hexaphylla to confirm that it is conspecific with P. verticillata. Based on a specimen from Butan, Stearn (1956) described P. marmorata as a new species. It was combined with P. polyphylla as a subspecies by Hara (1969), while Wang and Tang (1978) reduced it to a synonym of P. violacea. Li (1986) recovered it as a distinct species. This treatment was supported by the molecular phylogenetic analyses by Ji et al. (2019). Hara (1966) described P. polyphylla var. appendiculata as a new variety, while it was reduced to P. thibetica by Takhtajan (1983). Ying published P. taitungensis as a new species. However, Li (1986) reduced it to a synonym of P. polyphylla var. stenophylla. Wang and Tang (1978) described a new species, P. bashanensis, based on collections from Sichuan, China, and they reduced P. quadrifolia var. setchuanensis to its synonym. They published a new variety, as well, P. polyphylla var. latifolia, which was recognized as a form under P. polyphylla var. stenophylla by Li (1986). Based on collections from central Yunnan, southwest China, Li (1982) described P. luquanensis as a new species. It is unique in the genus in its small plant size, and green or adaxially deep green and abaxially dark purple leaf blades, tinged with pale green along the veins. Miao (1982) described Paris kwantungensis as a new species based on a specimen collected from Guangdong, south China. The species was reduced to P. polyphylla (Daiswa polyphylla) by Takhtajan (1983), while Chen and Liang (1995) combined it with P. polyphylla as a variety. After careful examination of type specimens, I found that it should be conspecific with P. chinensis. In the comprehensive taxonomic revision of Daiswa, Takhtajan (1983) recognized four novel taxa, namely, Daiswa hainanensis subsp. vietnamensis, D. birmanica, D. cronquistii, and D. forrestii. These taxa were combined into Paris (Li 1984a; Li and Noltie 1997), and the taxonomic rank of D. hainanensis subsp. vietnamensis was raised to a species (P. vietnamensis). However, Liang and Soukup (2000) reduced P. birmanica (D. birmanica) to P. polyphylla var. yunnanensis. Li (1984a) published two new species from Yunnan: P. axialis and P. longistigmata. In the same year, she reduced P. longistigmata to D. forrestii and recognized a new combination P. forrestii (Li 1984b). Here, P. axialis is reduced to a synonym of P. vaniotii.

1.3 History of Species Discoveries

Wang (1985) described P. polyandra as a new species in Sichuan, southwest China. It was reduced to P. cronquistii by Li (1986). Li (1986) revised the taxonomy of Paris, recognizing 19 species and eight varieties, of which four were recognized as new. Among them, P. polyphylla var. nana was reduced to P. polyphylla var. yunnanensis by Mitchell (1988). Ji et al. (2006b) raised P. cronquistii var. xichouensis to the status of a species and reduced P. polyphylla var. pseudothibetica to P. delavayi. After carefully examining the types and specimens of related taxa, I here treat P. polyphylla var. alba as a synonym of P. polyphylla. Peng and Zhao (1986) described P. wenxianensis as a new species, based on collections from Wenxian, Southern Gansu, China. Wang (1988) described P. polyphylla var. minor as a new variety. These two taxa were reduced to P. thibetica and P. delavayi by Ji et al. (2007). Huang and Yang (1988) published a new variety, Daiswa fargesii var. brevipetalata. Subsequently, they combined it with Paris. Here, I treated it as a synonym of P. fargesii. He (1990) recognized P. guizhouensis as a new species. Zhou et al. (1991) published P. axialis var. rubra as a new variety. The two taxa here are reduced to synonyms of P. vaniotii. Li (1992) described P. daliensis, P. dulongensis, P. rugosa, and P. undulatis as new species, as well as the new variety P. fargesii var. latipetala. Here, P. daliensis is reduced to P. yunnanensis; P. dulongensis and P. rugosa are treated as synonyms of P. forrestii; P. undulatis is reduced to P. vaniotii; and P. fargesii var. latipetala is reduced to P. fargesii. Ji et al. (2006c) published a new species, P. caobangensis, which is distinctive in its ovate-lanceolate and triplinerved leaf blade. Wang et al. (2017) published P. nitida as a new species. It is proposed that this species is closely related to P. caobangensis, but it is distinct from the latter species in its number of leaves, four to five, as well as their leathery and adaxially lustrous quality. Actually, these features are possessed by not only P. nitida but also P. caobangensis, suggesting that they are the same species. Yin et al. (2007) described P. polyphylla var. emeiensis as a new variety. I reviewed the description and examined species collected from the type locality. I found that except for a shortened pedicel, its leaf and flower morphologies are almost identical to P. yunnanensis. Accordingly, here P. polyphylla var. emeiensis is reduced to P. yunnanensis. Zhang et al. (2008) described P. stigmatosa as new. I carefully examined the holotype, reviewed the description, and found that the leaf shape of P. stigmatosa is largely similar to that of P. mairei. In addition, its second pair of lateral veins on the leaf blade curved and collected at the leaf apex; this feature is highly homologous to P. mairei.

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Therefore, I reduce P. stigmatosa to P. mairei, although its stem and leaves are glabrous. Liu (2009) described P. polyphylla var. panxiensis as new to southwest Sichuan, China. However, its leaf and flower morphologies are quite close to P. lancifolia. Accordingly, I treat it as a synonym of the latter. Yin and Zhang (2013) described P. cronquistii var. brevipetalata as a new variety. They believed that it differs from the proto-variety in its petals, which are shorter than its sepals. I carefully examined the holotype of P. cronquistii and found that its petal length (ca. 4 cm) is also shorter than its sepal length (ca. 5.5 cm). In addition, the petal length of P. cronquistii varies from 2 to 12 cm, so it thus cannot be used as a character for taxa delimitation. Therefore, here P. cronquistii var. brevipetalata is treated as a synonym of P. cronquistii. Ji et al. (2017) described P. tengchongensis as a new species. Except for its petal colors, leaf morphologies, flower and fruit of P. tengchongensis are almost identical to that of P. forrestii. Here, I treat it as a synonym of P. forrestii. Li et al. (2017) described P. yanchii as new, based on collection from Yulong, Yunnan, southwest China. Its morphological features and our molecular phylogenetic analyses (Ji et al. 2019) indicated that it is a distinct species. Subsequently, Liu et al. (2017) described a new species, P. caojianensis, whose types were also collected from Yunlong. I found the morphologies of the two species to be largely similar, with the exception that P. caojianensis has a slightly shorter free portion of connective; this difference is not robust enough to recognize P. caojianensis as a distinct species. Accordingly, it is reduced to a synonym of P. yanchii. Yang et al. (2017) described a new species, Paris qiliangiana. Molecular evidence suggested that it could be a hybrid between P. delavayi/P. cronquistii and P. chinensis (Ji et al. 2019). Here, it is treated as a distinct taxon. Xu et al. (2019) described Paris lihengiana as a new species, based on collection from Weixin, Yunnan, southwest China. Yang et al. (2019b) published a new species, P. variabilis. However, morphological evidence indicated that both P. lihengiana and P. variabilis are closely related to P. vaniotii, and the morphological difference between these two species is not significant enough to recognize them as different species. Therefore, I here reduce them to synonyms of P. vaniotii. Ji et al. (2020) identified a genetically distinct lineage (cryptic species) within P. yunnanensis based on phylogenetic analyses of complete plastomes and ribosomal DNA sequences. With distinct morphologies and distribution, the cryptic species was proposed as a previously unrecognized taxon. Accordingly, it was described as a new species, Paris liiana. Overall, since the establishment of the genus Paris by Linnaeus (1753), 71 Paris species and 24 subspecific taxa have been described (Table 1.1), resulting in considerable

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1 Introduction: Taxonomic History

Table 1.1 List of taxa discribed in the genus Paris Taxa Paris quadrifolia Linn. Paris trifolia Renault Paris pentafolia Renault Paris incompleta M. Bieb. Paris apetala Hoffm. Paris octophylla Hoffm. Paris polyphylla Smith Paris verticillata M. Bieb. Paris obovata Ledeb. Paris hexaphylla Cham. Paris dahurica Fisch. ex Turcz. Paris tetraphylla A. Gray. Paris japonica (Franch. et Sav.) Franch. Paris chinensis Franch. Paris thibetica Franch. Paris yunnanensis Franch. Paris polyphylla Smith var. stenophylla Franch. Paris delavayi Franch. Paris fargesii Franch. Paris polyphylla Smith var. brachystemon Franch. Paris polyphylla Smith var. platipetala Franch. Paris quadrifolia Linn. var. setchuanensis Franch. Paris bockiana Diels Paris henryi Diels Paris petiolata Baker ex C. H. Wright Paris petiolata Baker ex C. H. Wright var. membranacea C. H. Wright Paris christii Lévl. Paris franchetiana Lévl. Paris mercieri Lévl. Paris cavaleriei Lévl. et Vaniot Paris debeauxii Lévl. Paris gigas Lévl. Paris vaniotii Lévl. Paris aprica Lévl. Paris hookeri Lévl. Paris pinfaensis Lévl. Paris dunniana Lévl. Paris mairei Lévl. Paris violacea Lévl. Paris atrata Lévl. Paris hamifer Lévl. Paris lancifolia Hayata Paris biondii Pamp. Paris formosana Hayata Paris brachysepala Pamp. Paris arisanensis Hayata Paris hainanensis Merr. Paris polyphylla Smith var. pubescens Hand. -Mazz. Paris thibetica Franch. var. apetala Hand. -Mazz.

Types George Clifford s. n. (Holotype, BM) Not assigned Not assigned Not assigned Not assigned Not assigned F. Buchanan s. n. (Holotype, LINN; Isotype, BM, GH) Not assigned Not assigned Not assigned Not assigned C. Wright s. n. (Holotye, GH) Rein 2945 (Holotype, P) David s. n. (Holotype, P) David s. n. (Holotype, P; Isotype, K, LE) J. M. Delavay 2227 (Holotype, P) David s. n. (Holotype, P) J. M. Delavay s. n. (Holotype, P; Isotype, P) R. Paris Farges 573 (Holotype, P) Farges s. n. (Holotype, P) Farges 573 (Holotype, P) R. Paris Farges 414 (Holotype, P; Isotype, PE) Rosthorn A. V. & Bock C. 642 (B) Henry A 5380 (Lectotype, B; Isotype, B, E). Prat 572 (Holotype, K) A. Henry 5385 (Holotype, K) Bodinier s. n. (Holotype, E) Bodinier 712 (Holotype, E) Bodinier 1635 (Holotype, E) Cavalerie 1310 (Holotype, E) Cavalerie 533 (Holotype, E) Cavalerie 729 (Holotype, E) Cavalerie & Pierre Julien 1309 (Holotype, E) Cavalerie 3023 (Holotyp, Isotype, E) Cavalerie s. n. (Holotype, E) Cavalerie 2023 (Holotype, E; Isotype, GH, K) Cavalerie 3652 (Holotype, E; Isotype, E, PE) Maire 7457 (Holotype, E) Maire 7458 (Holotype, E) Maire s. n. (Holotyp, E) Maire s. n. (Holotype, E) S. Nagasawa 693 C. Silvestri 211 (Holotype, FI) T. Kawakami & U. Mori 3573 (Holotype, GH) C. Silvestri 3384 (Holotype, FI) B. Hayata s. n. McClure 9347 (Lectotype, PNH; Isotype, GH) Handel-Mazzetti 2489 (Isotype, E) Handel-Mazzetti 9383 (Holotype, E)

Type locality Netherlands France France Caucasus Armenia Armenia Naraianhetty, Nepal Siberia Irkutsk, Russia Siberia Stanovoy, Russia Japan Japan Baoxing, Sichuan, China Baoxing, Sichuan, China Eryuan, Yunnan, China Baoxing, Sichuan, China Yanjin, Yunnan, China Chengkou, Chongqing, China Chengkou, Chongqing, China Chengkou, Chongqing, China Chengkou, Chongqing, China Nanchuan, Chongqing, China Hubei, China Sichuan, China Hubei, China Guizhou, China Guizhou, China Guiyang, Guizhou, China Longli, Guizhou, China Guiding, Guizhou, China Guiding, Guizhou, China Guiding, Guizhou, China Guiding, Guizhou, China Guiding, Guizhou, China Guiding, Guizhou, China Luodian, Guizhou, China Dongchuan, Yunnan, China Yunnan, China Ninglang, Yunnan, China Ninglang, Yunnan, China Taiwan, China Hubei, China Taiwan, China Hubei, China Taiwan, China Hainan, China Sichuan, China Yunnnan, China (continued)

1.3 History of Species Discoveries

7

Table 1.1 (continued) Taxa Paris manshurica Kom. Paris marmorata Stearn Paris polyphylla Smith var. appendiculata Hara Paris taitungensis S. S. Ying Paris bashanensis Wang et Tang Paris polyphylla Smith var. latifolia Wang et Tang Paris luquanensis H. Li Paris kwantungensis Miao Paris vietnamensis (Takha.) H. Li Paris birmanica (Takht.) H. Li et H. Noltie Paris cronquistii (Takht.) H. Li Paris forrestii (Takht.) H. Li Paris axialis H. Li Paris longistigmata H. Li Paris polyandra S. F. Wang Paris polyphylla Smith var. nana H. Li Paris cronquistii Takht. var. xichouensis H. Li Paris polyphylla Smith var. pseudothibetica H. Li Paris polyphylla Smith var. alba H. Li & R. J. Mitchell Paris polyphylla Smith var. pseudothibetica H. Li f. macrosepala H. Li Paris delavayi Franch. var. ovalifolia H. Li Paris wenxianensis Z. X. Peng & R. N. Zhao Paris polyphylla Smith var. minor S. F. Wang Paris fargesii Franch. var. brevipetalata (T. C. Huang & K. C. Yang) T. C. Huang & K. C. Yang Paris guizhouensis S. Z. He Paris axialis H. Li var. rubra H. H. Zhou, K. Y. Wu & R. Tao Paris daliensis H. Li et V. G. Soukup Paris dulongensis H. Li & Kurita Paris rugosa H. Li & Kurita Paris undulatis H. Li et V. G. Soukup Paris fargesii Franch. var. latipetala H. Li & V. G. Soukup Paris caobangensis Y. H. Ji, H. Li & Z. K. Zhou Paris polyphylla Smith var. emeiensis X. H. Yin, H. Zhang & D. Xue Paris stigmatosa S.-D. Zhang Paris polyphylla Smith var. panxiensis J. L. Liu Paris cronquistii (Takht.) H. Li var. brevipetalata H. X. Yin et H. Zhang Paris nitida G. W. Hu, Z. Wang & Q. F. Wang Paris tengchongensis Y. H. Ji, C. J. Yang & Y. L. Huang Paris yanchii H. Li, L. G. Lei & Y. M. Yang

Types Not seen Ludlow, Sheriff & Hicks 16213 (Holotype, BM) Hara 366 (Holotype, TI) Sangyang 1037 (NTUF) Song ZP 38238 (Holotype, SZ) Xia WY 4426 (PE) Zhu WM 671 (Holotype, HGUY) C. Wang 32199 (holotype, SYS) G. Yakovlev et al. 860a (Holotype, LE; Isotype, HNV) Lace John Henry 6233 (Holotype, E; Isotype, E) A. N. Steward & H. C. Cheo 187 (Holotype, NY; Isotype, PE, GH). G. Forrest 29602 (Holotype, E; Isotype, BM). Li H, Chen Y, & Yu HY 1322 (Holotype; Isotype, KUN) J. S. Yang 63-1590 (Holotype, KUN). Xiao JX 48491 (SZ) Yibin Drug Inspection Institute Yi428 (KUN) Wang SZ 483 (Holotype, KUN) Li H, Chen Y & Yu HY 1275 (Holotype, KUN) Sino-Germany Expedition 403 (KUN). Li H 1275 (KUN)

Baoshan, Yunnan, China Mt. Emei, Sichuan, China Yibin, Sichuan, China Xichou, Yunnan, China Yi+, Yunnan, China Dali, Yunnan, China Yiliang, Yunnan, China

Li H 1324 L (KUN) Zhao RN 550291 (LZU). Wang SF 6512 (SZ) Huang TC & Yang KC 10803 (Holotype, TAI)

Yiliang, Yunnan, China Wenxian, Gansu, China Mt. Emei, Sichuan, China Yilan, Taiwan, China

He SZ 293 (HGCM) Zhou HH 9031 (Holotype, KUN) H. Li & V. G. Soukup 1098 (Holotype, KUN; Isotype, CINC) Dulongjiang Botany Expedition 6765 (Holotype, KUN) Dulongjiang Expedition 5388 (Holotype, KUN) Li H 88168 (Holotype, KUN) Li H 87-167 (Holotype, KUN) Ji YH 0127 (Holotype, KUN) Yin XH et al. 06121 (Holotype, SZ; Isotype, CDBI) Wang H et al. 03-1372 (Holotype, KUN; Isotype, MO, PE, YUKU) Liu JL & Yang JM 4 935 (Holotype, XIAS) Yin XH et al. 0427001 (Holotype, WCU)

Zhenning, Guizhou, China Shuicheng, Guizhou, China Yunnan, China

G. W. Hu & Z. Xu HGW-01060 (Holotype, HIB; Isotypes, HIB, HNNU) Ji YH 1341 (Holotype, KUN; Isotype, KUN, PE) Wang YH et al. 009 (Holotype, KUN)

Type locality Russian Far East Drugye Dzong, Bhutan Bakkim-Jongri Taiwan, China Baoxing, Sichuan, China Huayin, Shaanxi, China Luquan, Yunnan, China Xinyi, Guangdong, China Tam Dao, Vietnam Maymyo, Myanmar Lingyun, Guangxi, China Tengchong, Yunnan, China Yiliang, Yunnan, China

Gongshan, Yunnan, China Gongshan, Yunnan, China Mt. Emei, Sichuan, China Guiding, Guizhou, China Yan Lac, Cao Bang, Vietnam Mt. Emei, Sichuan, China Qiaojia, Yunnan, China Puge, Sichuan, China Chongzhou, Sichuan, China Tongshan, Hubei, China Tengchong, Yunnan, China Yunlong, Yunnan, China (continued)

8

1 Introduction: Taxonomic History

Table 1.1 (continued) Taxa Paris caojianensis B. Z. Duan & Y. Y. Liu Paris qiliangiana H. Li, J. Yang & Y. H. Wang Paris lihengiana G. W. Hu & Q. F. Wang Paris variabilis Z. Y. Yang, C. J. Yang & Y. H. Ji Paris liiana Y. H. Ji

Types Duan BZ & Liu YY 055 (Holotype, DLU) Li & Yang 053-03 (Holotype, KUN; Isotype, KUN) Hu, Wang & Zhao HGW-00655 (Holotype; Isotype, HIB) Ji & Yang 039 (Holotype; Isotypes: KUN) Ji YH 2016457 (Holotype, KUN), Huang YL 006 (Paratype, KUN)

Type locality Yunlong, Yunnan, China Zhuxi, Hubei, China Weixin, Yunnan, China Shuifu, Yunnan, China Yuanyang, Yunnan, China; Qiubei, Yunan, China

Fig. 1.3 Relationships among subdivisions of Paris in the classification of Hara (1969) and Takhtajan (1983)

confusion in species delimitation. Although the genus has been subjected to four major revisions (Franchet 1888a; Hara 1969; Takhtajan 1983; Li 1998), there remain many controversies in species delineation. Even for the taxa commonly recognized by Franchet (1888a, b), Hara (1966), Takhtajan (1983), and Li (1998), for instance, P. chinensis and P. yunnanensis, their taxonomic status as a species or a variety (or subspecies) has never been satisfactorily resolved. In addition, several taxa described in the 1980s, for instance, P. guizhouensis and P. wenxianensis, were ignored by the most recent and comprehensive revision by Li (1998). It is noteworthy that a total of 35 new taxa (23 species and 12 varieties) have been described in the past 40 years. The discovery of some of these taxa is most likely based on some plastic characters, such as leaf shape and size, petal color, length and width of pedicel, petals, stigma, and free portion of connectives, which are usually variable within a given species. This has resulted in individually different plants, ecotypes, and phenotypes being recognized as new taxa. As a result, the alpha taxonomy of Paris remains uncertain despite its great economic importance, hindering its effective conservation and the exploration of Paris species. Therefore, a further comprehensive taxonomic revision is urgently needed.

1.4

Generic Circumscription and Subdivision

Paris species are morphologically distinctive in their single whorl of leaves (>3) and solitary apical 4- to 15-merous flower. However, the rhizome, leaf, flower, stamens, ovary,

fruit, and seeds, which are widely used to construct classifications, are highly divergent among species, making overall classification complex (Hara 1969; Li 1998). Since the establishment of the genus by Linnaeus (1753), it has been subject to numerous critical revisions (Rafinesque 1838; Salisbury 1866; Franchet 1888a; Tatewaki and Suto 1935; Hara 1969; Wang and Tang 1978; Takhtajan 1983; Li 1998). However, the circumscription of the genus and its subdivisions are unresolved questions in the taxonomy of Paris. Rafinesque (1838) examined the morphorlogy of Paris polyphylla and proposed it to be different from other Paris species known at that time in its thick rhizome and capsule fruit. Based on these differences, Rafinesque (1838) established a new genus, Daiswa, and assigned P. polyphylla as the type species. Subsequently, using the same species as the type, Salisbury (1866) defined another genus, Euthyra, which is of course a synonym of Daiswa. Franchet (1888a), who carried out the first comprehensive taxonomic revision on this genus, argued that there is no substantially morphological difference between Paris and Daiswa to support recognizing them as distinct genera. Therefore, the genus Euthyra was reduced to a section under Paris to accommodate species with thick rhizomes (Franchet 1888a). Kinugasa was established as a monotypic genus by Tatewaki and Suto (1935), based on P. japonica. However, its generic status was not recognized by Hara (1969), who reduced Kinugasa to a section under Paris and divided the 14 species known at the time into three sections: Paris sect. Paris, P. sect. Kinugasa, and P. sect. Euthyra based on the characters of their fruit and seed (Fig. 1.3a). Instead, Takhtajan (1983) recognized these three sections as separate

1.5 Issues to Be Resolved

9

Fig. 1.4 Infrageneric relationships proposed by Li (1998)

genera (Fig. 1.3b), Paris s. s. (= P. sect. Paris), Daiswa (= P. sect. Euthyra), and Kinugasa (= P. sect. Kinugasa). In the most recent comprehensive taxonomic revision, Li (1998) likewise recognized Paris as a genus but divided it into two subgenera, Paris subg. Daiswa and P. subg. Paris (Fig. 1.4). The subgenus Daiswa was further divided into P. sect. Dunnianae, Euthyra, Marmoratae, Fargesianae, and Thibeticae; P. subgenus Paris was divided into the sections Kinugasa, Paris, and Axiparis. The advantage of this classification is that it takes into account both the morphological diversity and uniqueness of the genus. As a result, five more sections, P. sect. Axiparis, Dunnianae, Fargesianae, Marmoratae, and Thibeticae were subdivided from the collective section Euthyra defined by Franchet (1888a) and Hara (1969). However, there are also many problems with this. For instance, P. sect. Axiparis can be closely related to P. sect. Thibeticae because their seeds are incompletely covered by arils. It might not make sense to put them in two different subgenera. In this sense, the subgenus Paris circumscribed by Li (1998) seems to be heterogeneous. In addition, for these sections, P. sect. Dunnianae, Euthyra, Fargesianae, and Marmoratae, the rhizome, ovary fruit, and seed morphology are almost identical; however, there are only slight differences in the number of stamens, the color of leaves, and the shape of the free portion of connective. The division of them into four distinct sections may be artificial. It is clear that for elucidation of generic circumscription and relationships within the genus, evidence from a number of different approaches is needed. Based on molecular and morphological evidence, an updated classification of Li (1998) was suggested by combining P. sect. Dunnianae, Fargesianae, and Marmoratae with Euthyra (Ji 2006; Ji et al. 2006a). However, the monophyly of the five sections

proposed by Ji et al. (2006a) was not robustly supported by molecular phylogeny. In addition, due to insufficient sequence variation and significant cytonuclear discordance, the phylogenetic analyses did not provide satisfactory resolution or support for infrageneric relationships in Paris. Several recent studies have attempted to resolve the enigmatic relationships within Paris based on molecular evidences. An analysis by Kato et al. (1995) using the plastid rbcL region resolved Paris as a monophyletic lineage which is sister to the Trillium. However, phylogenetic analyses of nuclear 18S ribosomal DNA sequence by Osaloo and Kawano (1999) and the combination analyses of plastid rbcL and matK and nuclear ITS DNA regions by Farmer and Schilling (2002) did not resolve Paris as monophyletic. By contrast, two independent phylogenies based on the chloroplast psbA-trnH and trnL-F and nuclear ITS sequence data (Ji et al. 2006a), and the combination of five chloroplast sequences (atpB, rbcL, matK, ndhF, and trnL-F) (Kim et al. 2016), resolved Paris as a monophyletic group. As such, the relationships of Paris to related genera remain unresolved.

1.5

Issues to Be Resolved

According to the above review of the taxonomic history, the main objectives of my monographic study on Paris are: (1) to resolve the long-standing taxonomic and phylogenetic controversies within the genus based on multi-disciplinary evidences; (2) to reconstruct a natural classification; (3) to elucidate the real species diversity within the genus by conducting a comprehensive taxonomic revision; and (4) to explore biogeographic history and species diversification for the genus.

10

References Angiosperm Phylogeny Group (1998) An ordinal classification for the families of flowering plants. Ann Mo Bot Gard 85:531–553. https:// doi.org/10.2307/2992015 Angiosperm Phylogeny Group (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc 141:399–436. https://doi. org/10.1046/j.1095-8339.2003.t01-1-00158.x Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121. https:// doi.org/10.1111/j.1095-8339.2009.00996.x Angiosperm Phylogeny Group (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20. https://doi. org/10.1111/boj.12385 Bentham GJD, Hooker H (1883) Genera plantarum. Reeve & Co, London Bieberstein M (1808) Flora Taurico-Caucasica, vol 1. Typis Academicis, Charkouiae Bieberstein M (1819) Flora Taurico-Caucasica, vol 3. Typis Academicis, Charkouiae Chen SC, Liang SY (1995) A new combination of Paris. Acta Phytotaxon Sin 33:490 Cronquist A (1968) The evolution and classification of flowering plants. Nelson, London Dahlgren RMT (1975) A system of classification to be used to demonstrate the distribution of characters. Bot Not 128:119–147 De-Jusseau AL (1789) Genera plantarum secundum ordines naturales disposita. Viduam Herissan, Paris Diels (1900) Die flora von central-China. In: HGA E (ed) Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie, vol 25. Leipzig, pp 251–253 Du-Mortier BC (1829) Analyse des families des plantes avec l’indication des principaus cenres que s’y battachent. J. Casterman, Touray Endlicher S (1836–1840) Genera plantarum. Apud Fr. Beck Universitatis Bibliopol, Vindobonae Engler A (1888) Die naturlichen pflanzenfamilien II. W. Engelmann, Leipzig Farmer SB, Schilling EE (2002) Phylogenetic analyses of Trilliaceae based on morphological and molecular data. Syst Bot 27:674–692. https://doi.org/10.2307/3093915 Fedtschenko BA (1912) Trudy Imperatorskago S.-Peterburgskago Botaničeskago Sada 31:121 Fischer FEL (1854) Bulletin de la Société Impériale des Naturalistes de Moscou 27:105 Franchet A (1888a) Monographie du genere Paris. Gauthiers-Villars, Paris Franchet A (1888b) Monographie du genre Paris. Mémoires Publiés par la Société Philomathique 24:267–324 Franchet A (1888c) Nouvelles archives du Muséum d’histoire naturelle 2:96, 97, 184 Franchet A (1898) Plantarum sinensium. ecloge secunda. J Bot (Morot) 12:190–191 Handel-Mazzetti H (1925) Anzeiger der Akademie der Wissenschaften in Wien. Mathematische-naturwissenschaftliche Klasse. Vienna 62:145–149 Handel-Mazzetti H (1936) Symbolae Sinicae. J. Springer, Wien Hara H (1966) Flora of Eastern Himalaya, vol 1. University of Tokyo Press, Tokyo, pp 410–411 Hara H (1969) Variation in Paris polyphylla Smith, with reference to other Asiatic species. J Fac Sci Univ Tokyo 10(10):141–180 Hayata B (1906) Contributions to the Flora of Mt. Morrison. Bot Mag 20:52

1 Introduction: Taxonomic History Hayata B (1911) J Coll Sci, Imperial University of Tokyo 30:367–369 Hayata B (1920) Icones Plantarum Formosanarum nec non et Contributiones ad Floram Formosanam 9:141–142 He SZ (1990) A new medicinal species of Paris from Guizhou province, China. Guizhou Sci 3:16 Huang TC, Yang KC (1988) Notes on the Flora of Taiwan (1)-The Daiswa (Trilliaceae) of Taiwan. Taiwania 33:123 Huang YL, Li XJ, Yang ZY et al (2016) Analysis of complete chloroplast genome sequences improves phylogenetic resolution of Paris (Melanthiaceae). Front Plant Sci 7:1797. https://doi.org/10.3389/ fpls.2016.01797 Huber H (1969) Die samenmerkmale und verwandtschaftsver haltnisse der Liliiflorae. Mitt Bot Staatssam Munchen 8:219–253 Huber H (1977) The treatment of the monocotyledons in an evolutionary system of classification. Plant Syst Ecol Suppl 1:285–298. https:// doi.org/10.1007/978-3-7091-7076-2_18 Hutchinson J (1926) The families of flowering plants, vol 2. Monocotyledons. Clarendon P, London Ji YH (2006) Phylogeny and biogeography of Paris (Melanthiaceae). Ph.D. Dissertation. Graduate University of Chinese Academy of Sciences, Beijing Ji YH, Fritsch PW, Li H, Xiao TJ, Zhou ZK (2006a) Phylogeny and classification of Paris (Melanthiaceae) inferred from DNA sequence data. Ann Bot 98:245–256. https://doi.org/10.1046/j.1365-2885. 2002.00426.x Ji YH, Zhou ZK, Li H (2006b) Paris xichouensis, a new combination of Trilliaceae from China. Acta Phytotaxon Sin 44:612–613 Ji YH, Li H, Zhou ZK (2006c) Paris caobangensis Y. H. Ji, Li H. & Z. K. Zhou (Trilliaceae), A new species from northern Vietnam. Acta Phytotaxon Sin 44:700–703 Ji YH, Zhou ZK, Li H (2007) Four new synonyms in the genus Paris (Trilliaceae). Acta Phytotaxon Sin 46:388–390 Ji YH, Yang CJ, Huang YL (2017) A new species of Paris sect. Axiparis (Melanthiaceae) from Yunnan, China. Phytotaxa 306:234–236 Ji YH, Yang LF, Chase MW et al (2019) Plastome phylogenomics, biogeography and clade diversification of Paris (Melanthiaceae). BMC Plant Biol 19:543. https://doi.org/10.1186/s12870-019-2147-6 Ji YH, Liu CK, Yang J et al (2020) Ultra-Barcoding discovers a cryptic species in Paris yunnanensis (Melanthiaceae), a medicinally important plant. Front Plant Sci 11:411. https://doi.org/10.3389/fpls.2020. 00411 Kato H, Terauchi R, Utech FH, Kawano S (1995) Molecular systematics of the Trilliaceae sensu lato as inferred from rbcL sequence data. Mol Phylogenet Evol 4:184–193. https://doi.org/10.1006/mpev.1995.1018 Kim JS, Hong JK, Chase MW et al (2013) Familial relationships of the monocot order Liliales based on a molecular phylogenetic analysis using four plastid loci: matK, rbcL, atpB and atpF-H. Bot J Linn Soc 172:5–21. https://doi.org/10.1111/boj.12039 Kim S, Kim JS, Chase MW et al (2016) Molecular phylogenetic relationships of Melanthiaceae (Liliales) based on plastid DNA sequences. Bot J Linn Soc 181:567–584. https://doi.org/10.1111/ boj.12405 Kim C, Kim SC, Kim JH (2019) Historical biogeography of Melanthiaceae: a case of out-of-North America through the Bering land bridge. Front Plant Sci 10:396. https://doi.org/10.3389/fpls. 2019.00396 Kunth CS (1850) Enumeratio Plantarum, vol 2. Sumtibus J. G. Cottae, Stutgardiae Ledebour KF (1828) Icones Plantarum Novarum vel Imperfecte Cognitarum Floram Rossicam 1:16 Léveillé H (1903) Bulletin de l’Académie Internationale de Géographie Botanique, vol 12. Au siège de la Société, Le Mans Léveillé H (1906) Memorie della Pontificia Accademia Romana dei Nuovi Lincei 24:21, 354, 355 Léveillé H (1909) Decades plantarum novarum. XIII-XIV. Repert Spec Nov Regni Veg 6(119–124):265. https://doi.org/10.1002/fedr. 19090061509

References Léveillé H (1910) Decades plantarum novarum. XLVII-XLVIII. Repert Spec Nov Regni Veg 9:78. https://doi.org/10.1002/fedr.19100090406 Léveillé H (1913) Decades plantarum novarum. CXIX-CXXIV. Repert Spec Nov Regni Veg 12:288. https://doi.org/10.1002/fedr. 19130121707 Li H (1982) A new species of the genus Paris. Act Bot Yunnan 4:353– 354 Li H (1984a) The phylogeny of the genus Paris L. Act Bot Yunnan 6:351–362 Li H (1984b) Two new species of the genus Paris. Act Bot Yunnan 6:273–276 Li H (1986) A study on the taxonomy of the genus Paris L. Bull Bot Res 6:111–146 Li H (1992) New taxa of the genus Paris L. Act Bot Yunnan Suppl 5:13–18 Li H (1998) The Genus Paris (Trilliaceae). Science Press, Beijing Li H, Noltie HJ (1997) Miscellaneous notes on the genus Paris. Edinburgh J Bot 54:351–353 Li H, Lei LG, Yang YM (2017) Paris yanchii, a new species of Paris Linnaeus (Melanthiaceae) from Yunnan, China. J West China For Sci 46:1–5 Liang SY, Soukup VG (2000) Paris L. In: Wu ZY, Raven PH (eds) Flora of China, vol 24. Science Press/Missouri Botanical Garden Press, Beijing/St. Louis, pp 88–95 Lindley J (1846) The vegetable kingdom, 3rd edn. Bradley and Evan, London Linneaus C (1753) Species plantarum. Salvius, Stockholm Liu JL (2009) Paris polyphylla var. panxiensis (Trilliaceae), a new variety from Sichuan, China. Acta Bot Boreali-Occident Sin 29:1697–1700 Liu YY, Luo DD, Yao H et al (2017) New species of Paris (Melanthiaceae) from Yunnan, China. Phytotaxa 326:297 Merrill ED (1923) Diagnoses of Hainan plants II. Philipp J Crop Sci 23:238–239 Miao RH (1982) New taxa of Liliaceae from China. Acta Sci Nat Univ Nankaiensis 3:74 Mitchell B (1988) Paris—Part II. Daiswa. Plantsman 10:167–190 Osaloo SK, Kawano S (1999) Molecular systematics of Trilliaceae II. Phylogenetic analyses of Trillium and its allies using sequences of rbcL and matK genes of cpDNA and internal transcribed spacers of 18S–26S nrDNA. Plant Spec Biol 14:75–94. https://doi.org/10. 1046/j.1442-1984.1999.00009.x Pampanini R (1915) Nuovo Giornale Botanico Italiano, Nuova Serie 22:266 Pampanini R (1919) Nuovo Giornale Botanico Italiano, Nuova Serie 17:241 Peng ZX, Zhao RN (1986) A new species of Paris from Gansu province, China. Acta Bot Boreali-Occident Sin 6:133–134 Rafinesque CS (1838) Flora Telluriana, vol 4. Probasco, Philadelphia Regel ED, Tiling HST (1888) Memoire de la Societe Philomathique Centaire 24:282 Renault PA (1804) Flore du Département de l’Orne. Imprimerie de Malassis le jeune, Alcncon, p 26 Rendle AB (1930) The classification of flowering plants, vol 1. Gymnosperms and monocotyledons, 2nd edn. Cambridge University Press, Cambridge Salisbury RA (1866) Genera Plantarum. John Van Voorst, London Smith JE (1819) In: Rees A (ed) The cyclopædia: or, universal dictionary of arts, sciences, and literature, vol 26. Longman, Hurst, Rees, Orme & Brown etc., London Stearn WT (1956) Novitates Himalaicae I. Bull Br Mus (Nat Hist) Bot 2:79–81 Takhtajan A (1959) Die evolution der angiospermen. G. Fischer, Jena Takhtajan A (1980) Outline of the classification of flowering plants. Bot Rev 46:225–359. https://doi.org/10.2307/4353970 Takhtajan A (1983) A revision of Daiswa (Trilliaceae). Brittonia 35:255–270. https://doi.org/10.2307/2806025

11 Takhtajan A (1987) Systema magnoliophytorum. Soviet Sciences Press, Leningrad Takhtajan A (1997) Diversity and classification of flowering plants. Columbia University Press, New York Tatewaki M, Suto K (1935) In: Sapporo HG (ed) Transactions of the Sapporo Natural History Society, vol 14. Sapporo, Hokkaido Imperial University Thorne RF (1992) Classification and geography of the flowering plants. Bot Rev 58:225–234. https://doi.org/10.2307/4354190 von Chamisso LKA (1831) Linnaea, vol 6. F. Dümmler, Berlin, pp 586– 587 Voroschilov VN (1972) Byulleten Glavnogo Botanicheskogo Sada 84:31 Wang SF (1985) A new species of the genus Paris. Bull Bot Res 5:169– 172 Wang SF (1988) A new variety of Paris from Sichuan. Bull Bot Res 8:139–142 Wang FZ, Tang J (1978) Flora Reipubicae Popularis Sinicae, vol 15. Science Press, Beijing, pp 86–96 Wang Z, Cai XZ, Zhong ZX et al (2017) Paris nitida (Melanthiaceae), A new species from Hubei and Hunan, China. Phytotaxa 314:145–149 Watson S (1879) Contributions to American botany: revision of the North American Liliaceae. Proc Am Acad Arts Sci 14:2. https:// doi.org/10.2307/25138538 Watson L, Dallwitz MJ (1991) The families of angiosperms: automated descriptions with interactive identification and information retrieval. Aust Syst Bot 4:681–695. https://doi.org/10.1071/sb9910681 Willis JC (1973) A dictionary of flowering plants and ferns, 8th edn. Cambridge University, Cambridge Wright CH (1903) In: Forbes FB, Hemsley WB (eds) An Enumeration of all the Plants known from China Proper, Formosa, Hainan, Corea, the Luchu Archipelago, and the Island of Hongkong, together with their Distribution and Synonymy (Part—XIV). Bot J Linn Soc 36:145 Xu Z, Wei N, Tan Y et al (2019) Paris lihengiana (Melanthiaceae: Parideae), a new species from Yunnan, China. Phytotaxa 392:045– 053 Yang J, Wang YH, Li H (2017) Paris qiliangiana (Melanthiaceae), a new species from Hubei, China. Phytotaxa 329:193–196 Yang LF, Yang ZY, Liu CK, He ZS, Zhang ZR, Yang J et al (2019a) Chloroplast phylogenomic analysis provides insights into the evolution of the largest eukaryotic genome holder, Paris japonica (Melanthiaceae). BMC Plant Biol 19:293. https://doi.org/10.1186/ s12870-019-1879-7 Yang ZY, Yang CJ, Ji YH (2019b) Paris variabilis (Melanthiaceae), a new species from southwestern China. Phytotaxa 401:190–198 Yin HX, Zhang H (2013) Paris cronquistii (Takht.) Li H. var. brevipetalata H. X. Yin et H. Zhang, a new variety of Paris (Trilliaceae) form Sichuan, China. Acta Bot Boreali-Occident Sin 33:0190–0193 Yin HX, Zhang H, Xue D (2007) Paris polyphylla var. emeiensis H. X. Yin, H. Zhang & D. Xue, a new variety of Trilliaceae from Sichuan, China. Acta Phytotaxon Sin 45:823–824 Zhang SD, Wang H, Li DZ (2008) A new species of Paris (Melanthiaceae) from northeastern Yunnan, China. Novon 18:550– 554 Zhou HH, Wu KY, Tao R (1991) A variety of Paris axialis. Act Bot Yunnan 13:424 Zomlefer WB, Williams NH, Judd WS (2001) Generic circumscription and relationships in the Tribe Melanthieae (Liliales, Melanthiaceae), with emphasis on Zigadenus: evidence from ITS and trnL-F sequence data. Am J Bot 88:1657–1669 Zomlefer WB, Judd WS, Whitten WM et al (2006) A synopsis of Melanthiaceae (Liliales) with focus on character evolution in Tribe Melanthieae. Aliso 22:566–578. https://doi.org/10.5642/aliso. 20062201.44

2

Morphology

2.1

Gross Morphology

Paris species are perennial rhizomatous herbs. A grown plant (Fig. 2.1) comprises adventitious roots, rhizome, stem, leaves, and flower (fruit and seeds). The rhizome grows underground, bearing many adventitious roots and one or several apical buds. The aerial organs (stem, leaves, and flower) die each winter, and underground rhizome produces new shoots in the next spring. After dormancy, the aerial stem withers, which forms a scar on the rhizome. Based on the number of scars on the rhizome, it is easy to estimate the approximate age of the plant. The stem of Paris species is erect, cylindrical, and smooth or pubescent. A whorl of 4–15 net-veined leaves and a solitary flower develop at the stem apex; these characters are highly distinctive in angiosperms (Hara 1969; Li 1998). Flowers of Paris species are bisexual and mostly 4- to15-merous. Compared with the trimerous condition of Trillium Linn. (Fig. 2.2), a sister genus of Paris, the floral and phyllotaxy merosity are likely the morphological synapomorphies that differentiate the two genera.

2.1.1

Rhizome

Rhizome is an important underground storage organ. In grown plants of Paris species, rhizomes are usually found within the upper 10–15 cm soil layer. Aerial shoots are terminated by an apical bud, which either develops into a flower or aborts, depending on the rhizome biomass. Annual increments in rhizome biomass usually consist of 3–5 cylindrical internodes, surrounded by leaf-like and parallel-veined scales (Yang 1998). Scales generally fall off early (after approximately 3 months), but when the plant is in good nutritional condition, scales develop into cordate leaves. At the end of the growing season, rhizome growth terminates upon the senescence of the aerial shoot. Annual rhizome increments, which can be influenced by such factors as different species, growth stage, and nutritional status, account

for approximately 15–50% of the total underground rhizome biomass. My personal observations indicate that the rhizome volume of Paris chinensis, P. dunniana, P. forrestii, P. vietnamensis, and P. yunnanensis, shows positive correlation with plant height, stem diameter, and leaf area. In addition, volume of the latest rhizome increment depends on fruit production and seed yield; in general, the latest rhizome increments of abortive individuals are greater than those of reproductive plants. On the basis of the results of a previous study (Jacquemyn et al. 2008), I speculate that a threshold rhizome volume is necessary in Paris species for an aerial shoot to initiate flowering. Jacquemyn et al. (2008) proposed that old and new rhizome segments in Paris species perform different functions; old segments function only in the storage of nutrients, whereas young segments are involved in the acquisition of carbon and other nutrients. In addition, Zhao et al. (2014) found that the steroidal saponin contents of young segments of P. yunnanensis rhizomes are significantly higher than those of old segments, suggesting that young segments are also active in the storage of secondary metabolites. I found that the removal of old rhizome segments always results in the abortion of aerial shoots in P. yunnanensis and P. chinensis, further supporting the critical function of old segments in nutrient storage (Jacquemyn et al. 2008). Rhizome morphology is diverse in Paris. Two types of rhizomes have been identified within this genus. The rhizomes of the five species belonging to Paris sect. Paris, namely, P. bashanensis, P. incompleta, P. quadrifolia, P. tetraphylla, and P. verticillata, are long (>10 cm), slender (2–5 mm diameter), creeping, and usually branched (Fig. 2.3a). The remaining species of this genus have thick (1–10 cm diameter), cylindrical or conical, and yellow-brown rhizomes of variable length (3–20 cm) (Fig. 2.3b). Such thick rhizomes show seldom branching, although physical damage to the apical bud or gibberellin treatment removes apical dominance, thus inducing the initiation of numerous adventitious buds on the rhizome (Fig. 2.4). This approach can be

# Science Press 2021 Y. Ji, A Monograph of Paris (Melanthiaceae), https://doi.org/10.1007/978-981-15-7903-5_2

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14

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Morphology

within colonized roots. This morphological type of mycorrhiza is referred to as “Paris-type,” which is distinct from the “Arum-type” mycorrhiza (presence of intercellular hyphae within colonized roots), named after Arum maculatum in which it was first described (Gallaud 1905). However, studies show that not all P. quadrifolia individuals are colonized by AM fungi (Harley and Harley 1987; Smith and Read 1997). In recent years, AM colonization has been observed in P. yunnanensis, with the infection rate ranging from 35.3% to 98.6% (Zhou et al. 2009). Also, infection of AM fungi in P. yunnanensis could improve its photosynthetic capacity, rhizome steroidal saponin content, and enzyme activity in leaves as well as the level of functional gene expression in roots (Zhou et al. 2014; Wei et al. 2015; Ou et al. 2016; Zhang et al. 2018, 2019). However, it remains unclear whether all Paris species are colonized by AM fungi. The diversity of AM fungi that infect Paris species is needed to be further characterized.

2.1.3

Fig. 2.1 Grown plant of Paris

used for the rapid propagation of seedlings and increase in the biomass of rhizomes in the plantation of medicinal Paris. Within the Paris genus, species with slender or thick rhizomes represent two evolutionarily distinct lineages (Ji et al. 2019). Therefore, rhizome morphology can be used to construct infrageneric classification. For instance, Franchet (1888) established P. sect. Euparis (syn. P. sect. Paris) to accommodate species with slender rhizomes; this classification was followed by Hara (1969), Li (1998), and Ji (2006). Recent phylogenetic analyses based on single or multiple DNA loci (Farmer and Schilling 2002; Ji et al. 2006) and complete plastomes (Huang et al. 2016; Ji et al. 2019; Yang et al. 2019) recovered the section as a well-supported monophyletic clade.

2.1.2

Mycorrhiza

It is estimated that 80% of the angiosperms have the potential to form symbiotic association with arbuscular mycorrhiza (AM) under normal growth conditions (Bonfante-Fasolo 1984). Roots of Paris species can be infected by AM fungi. Gallaud (1904) first reported AM infection in P. quadrifolia, which is characterized by the absence of intercellular hyphae

Leaves

Leaves of Paris species are simple. Compared with most monocotyledons with parallel-veined leaves, Paris species are very distinctive in having net-veined leaves (Fig. 2.5). The phyllotaxy merosity, shape, and size are often used to distinguish species within the genus Paris. For instance, P. bashanensis, P. quadrifolia, and P. tetraphylla similarly have 4-merous leaves (rarely 5 or 6) and flowers. However, the leaf shapes of these species are divergent enough to discriminate among the four species. On the contrary, species delimitation based on leaf morphology sometimes leads to significant contradictions. For instance, P. polyphylla is often incorrectly identified as P. lancifolia because of their lanceolate leaves. In addition, the infraspecific variation in leaf morphologies may have caused taxonomic over-splitting of species in this genus. For example, based on leaf shape and size, three species, namely, P. dulongensis (oblanceolate or oblong leaves), P. rugosa (obovate leaves), and P. tengchongensis (oblong to elliptic leaves), which are morphologically similar to P. forrestii, have been described in recent years (Li 1992; Ji et al. 2017). Notably, all of these forms of leaves can be found in the “typical” P. forrestii (Fig. 2.6), suggesting that P. dulongensis, P. rugosa, and P. tengchongensis should be treated as the synonym of P. forrestii.

2.1.4

Flower

Flowers of Paris species are perfect and actinomorphic, with sepals, linear or filiform petals (occasionally absent), multiple stamens, and a pistil (Fig. 2.7). Paris species are unique in

2.1 Gross Morphology

Fig. 2.2 Comparison of floral and phyllotaxy merosity between Paris (a) and Trillium (b)

Fig. 2.3 Two types of rhizomes in Paris

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2

Morphology

Fig. 2.4 Rhizome with numerous adventitious buds

Fig. 2.6 Variation of leaf shape and size in Paris forrestii

P. chinensis and P. delavayi are shorter than their sepals, and P. fargesii can be easily recognized for its purple-black and ellipsoid (or subglobose) free portion of connective tissue. The number of stamens varies among Paris species (Fig. 2.9). Although the stamen number of most species is twice the petal number (2-whorled stamens), a few species, such as P. dunniana, P. vaniotii, and Paris xichouensis, possess 3- or 4-whorled stamens. Li (1998) hypothesized that the presence of more than two whorls of stamens represents the plesiomorphic state in Paris, and species with 3- or 4-whorled stamens represent early diverging lineages of this genus. Accordingly, Paris may have originated in the tropics. However, based on the framework of molecular phylogenies, optimization of stamen number suggests that the presence of 3- or 4-whorled stamens could be an apomorphic character in Paris (Ji et al. 2006). Two types of ovaries have been identified in Paris species (Fig. 2.10). The first type, 4- to 7-loculicidal ovary with axile placentation, is shared by species of P. sect. Euthyra and P. sect. Thibeticae, while the second type, single-loculicidal ovary with parietal placentation, is characteristic of species in P. sect. Axiparis, P. sect. Kinugasa, and P. sect. Paris.

2.1.5 Fig. 2.5 Net-veined leaves of Paris species

monocotyledons in their leaf-like and net-veined sepals (Fig. 2.8), and possess diverse floral characters (Table 2.1). The shape and size of sepals and free portion of connective tissue, relative length of sepals and petals, and ovary placentation are often used to define species. For instance, petals of

Fruit

Fruit morphology is also an important basis for classification in Paris. Paris species produce morphologically diverse fruits, including rounded and angular berries as well as berry-like capsules (Table 2.2). Species of P. sect. Paris have globose and purplish-black berries (Fig. 2.11a). Although both P. sect. Axiparis and Kinugasa produce angular berries (Fig. 2.11b), those of P. sect. Kinugasa are juicy and edible. Fruits of P. sect. Euthyra and Thibeticae are

2.1 Gross Morphology

17

Fig. 2.7 Flower (a), stamen (b), and pistil (c) of Paris

berry-like capsules (Fig. 2.11c), angular in shape, usually ribbed on the outside, and irregularly dehiscent at maturity. The size of capsules is relatively larger than that of berries.

2.1.6

Seeds

Like fruits, seeds show greatly divergent morphologies among Paris species (Table 2.2). Four major types of seeds have been recognized in this genus. Species of P. sect. Paris and Kinugasa produce “dry” seeds, characterized by the absence of sarcotesta or aril (Fig. 2.12a). Seeds of P. sect. Axiparis (Fig. 2.12b) and P. sect. Thibetiacae (Fig. 2.12c) are

enveloped by an imperfect aril. However, the aril in P. sect. Thibeticae is red and juicy, which is quite different from the white (or white-yellow) and spongy aril in P. sect. Axiparis. By contrast, seeds of P. sect. Euthyra are wholly covered with red (or orange), fresh, and juicy sarcotesta (Fig. 2.12d). Thus, seed morphology is also an important trait used to determine sub-generic classification in Paris.

2.1.7

Taxonomic Significance

Paris is a morphologically distinct genus among monocotyledons. However, the rhizomes, leaves, flowers,

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2

Morphology

Fig. 2.8 Flower of Paris showing the leaf-like and net-veined sepals

stamens, ovaries, fruits, and seeds, which have been widely used to determine classification, are highly divergent among Paris species. Therefore, establishing a natural classification based on only one or few morphological traits would be unreasonable. For instance, Franchet (1888) placed the species known at that time into two sections: P. sect. Euthyra and P. sect. Euparis (syn. P. sect. Paris). Subsequently, Hara (1969) circumscribed P. sect. Kinugasa as the third section within the genus. The section Euthyra recognized by Franchet (1888) and Hara (1969) is characterized only by parietal placentation ovary and capsule fruit. However, this classification is inaccurate because species with distinct seed morphology (covered by juicy sarcotesta and aril) are included in this section. Because of the high level of morphological divergence within the genus, Takhtajan (1983) proposed that Paris is a collective genus, and recognized the three sections sensu Hara (1969) as segregate genera, namely, Paris s.s., Daiswa Rafinesque-Schmaltz, and Kinugasa Tatewaki et Suto.

However, he most possibly ignored that Paris is morphologically distinctive with a single whorl of leaves (>3) and solitary 4- to15-merous apical flower; this character can be the morphological synapomorphy to recognize Paris as an independent plant lineage (Franchet 1888; Hara 1969; Li 1998; Ji 2006; Ji et al. 2006). On the basis of ovary and fruit characters, Li (1998) recognized two subgenera within this genus: Paris subgen. Daiswa (parietal placentation ovary, capsule fruit) and P. subgen. Paris (axile placentation ovary, berry fruit). It is notable that seeds of P. sect. Thibeticae and P. sect. Axiparis are similarly enveloped by an incomplete aril (Fig. 2.13). It could be unnatural to place these sections into independent subgenera. Consequently, none of the previous molecular phylogenies (Kazempour-Osaloo and Kawano 1999; Farmer and Schilling 2002; Ji et al. 2006, 2019; Huang et al. 2016; Yang et al. 2019) resolved the two subgenera defined by Li (1998) as monophyletic. Therefore, to establish a natural classification in Paris, the features of rhizomes, leaves,

2.2 Pollen Morphology

19

Table 2.1 Comparison of floral characteristics among Paris species Species P. tetraphylla P. incompleta P. quadrifolia P. verticillata P. bashanensis P. japonica P. thibetica P. vaniotii P. forrestii P. dunniana P. vietnamensis P. xichouensis P. chinensis P. caobangensis P. qiliangiana P. fargesii P. cronquistii P. delavayi P. liiana P. yunnanensis P. luquanensis P. lancifolia P. yanchii P. marmorata P. polyphylla P. mairei

Floral merosity 4 4–6 4 4–6 4 (rarely 5) 6–10 4–7 4–7 4–7 5–8 4–7 4–7 4–8 4–6 4–7 4–6 4–7 4–7 4–8 4–7 4–7 4–7 4–7 4–7 4–7 4–8

Sepals Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like White Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like Leaf-like

Petals Absent Absent Present Present Present Present Present or absent Present Present Present Present Present Present Present Present Present Present Present Present Present Present Present Present Present Present Present

flowers, stamens, ovaries, fruits, and seeds must be taken into account comprehensively.

2.2

Pollen Morphology

Pollen morphology is an evolutionarily conserved feature that is less affected by environmental conditions; thus, it has been widely used for species identification and classification, particularly at the genus or species level (Erdtman 1952, 1969; Takahashi and Kawano 1989). Studies of pollen grains in the genus Paris were initiated by Ikuse (1956) and expanded by Huang (1972), Takahashi (1984), Takahashi and Kawano (1989), Wei (1988, 1998), and Furness et al. (2015). Ikuse (1956) found that the exine ornamentation of pollen grains in P. japonica and P. tetraphylla is gemmate. Takahashi (1984) and Takahashi and Kawano (1989) examined six Paris species, and showed that their pollen grains are monosulcate, with three types of ornamentation: foveolate, reticulate, and gemmate. Wei (1988, 1998) analyzed 18 Chinese taxa, and concluded that pollen morphology is highly consistent with the gross morphology of Paris, thus

Stamens 2-whorled 2-whorled 2-whorled 2-whorled 2-whorled 2-whorled 2-whorled 3 (rarely 2 or 4)-whorled 2-whorled 3- or 4-whorled 2- or 3-whorled 3-whorled 2-whorled 2-whorled 2-whorled 2-whorled 2- or 3-whorled 2-whorled 2-whorled 2-whorled 2-whorled 2-whorled 2-whorled 2-whorled 2-whorled 2-whorled

Ovary Axile placentation Axile placentation Axile placentation Axile placentation Axile placentation Axile placentation Parietal placentation Axile placentation Axile placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation Parietal placentation

providing palynological evidence to support the classification of Li (1998). However, these studies either sampled only a limited number of taxa or restricted their target taxa to a given area, thus providing limited information to determine whether the pollen morphology correlates with the gross morphological features. To better understand the taxonomic significance of pollen morphology, we presented the most comprehensive palynological observation in Paris by sampling 23 out of 26 species recognized by my taxonomic revision (see Chap. 6) and taking into account the pollen morphology of P. incompleta (Furness et al. 2015) and P. japonica (Ikuse 1956; Takahashi 1984; Takahashi and Kawano 1989).

2.2.1

Pollen Size, Shape, and Ornamentation

Paris species produce medium-sized pollen, with some differences among species. Lengths of polar and equatorial axes range from 12.34
0.34 to 35.20
3.20 μm and from 36.50
0.50 to 54.70
3.30 μm, respectively. Within the genus, P. japonica has the largest pollen grains

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Morphology

Fig. 2.9 Two-whorled stamens in Paris liiana (a), 3-whorled stamens in P. vaniotii (b), and 4-whorled stamens in P. dunniana (c)

(54.70
3.30  35.20
3.20 μm), while P. marmorata has the smallest pollen size (36.50
0.50  12.34
0.34 μm). The majority of pollen grains of Paris species are oblatespheroidal at the polar view, with a narrow and deep monosulcate, consistent with previous observations reported by Ikuse (1956), Huang (1972), Takahashi (1984), Takahashi and Kawano (1989), and Wei (1988, 1998). Additionally, three types of pollen ornamentation have been identified in Paris, namely, foveolate, reticulate, and gemmate. Figure 2.14 shows the distribution of pollen ornamentation

in the phylogenetic tree generated by analyses of complete plastome DNA sequences (see Chap. 5). I also investigated the pollen morphology of Paris species as described below: (1) Paris quadrifolia L. (Fig. 2.15a)

Mean length of polar axis ¼ 19.50
0.50 μm; mean length of equatorial axis ¼ 43.50
0.50 μm; pollen grains

2.2 Pollen Morphology

21

Fig. 2.10 Transverse section (left column) and longitudinal section (right column) of Paris ovary showing parietal (upper row) and axile (below row) placentation

oblate-spheroidal, elliptic at polar view, with a narrow and deep monosulcate; exine ornamentation reticulate.

oblate-spheroidal, elliptic at polar view, with a narrow and deep monosulcate; exine ornamentation reticulate.

(2) P. verticillata M. Bieb. (Fig. 2.15b)

(4) P. tetraphylla A. Gray (Fig. 2.15d)

Mean length of polar axis ¼ 15.75
0.25 μm; mean length of equatorial axis ¼ 37.00
0.50 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a narrow and deep monosulcate; exine ornamentation reticulate.

Mean length of polar axis ¼ 18.50
0.50 μm; mean length of equatorial axis ¼ 39.00
0.50 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation gemmate with sessile pila.

(3) P. bashanensis F. T. Wang & Tang (Fig. 2.15c)

(5) P. forrestii (Takht.) H. Li (Fig. 2.16a)

Mean length of polar axis ¼ 13.75
0.25 μm; mean length of equatorial axis ¼ 38.75
0.75 μm; pollen grains

Mean length of polar axis ¼ 18.00
1.00 μm; mean length of equatorial axis ¼ 40.75
0.75 μm; pollen grains

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Morphology

Table 2.2 Comparison of fruit and seed features among Paris species Species P. tetraphylla P. imcompleta P. quadrifolia P. verticillata P. bashanensis P. japonica P. thibetica P. vaniotii P. forrestii P. dunniana P. vietnamensis P. xichouensis P. chinensis P. caobangensis P. qiliangiana P. fargesii P. cronquistii P. delavayi P. liiana P. yunnanensis P. luquanensis P. lancifolia P. yanchii P. marmorata P. polyphylla P. mairei

Fruit type Berry Berry Berry Berry Berry Berry Capsule Berry Berry Capsule Capsule Capsule Capsule Capsule Capsule Capsule Capsule Capsule Capsule Capsule Capsule Capsule Capsule Capsule Capsule Capsule

Fruit shape Globose Globose Globose Globose Globose Angular Angular Angular Angular Angular Angular Angular Angular Angular Angular Angular Angular Angular Angular Angular Angular Angular Angular Angular Angular Angular

Fruit size 4.0–15.0 mm in diameter 5.0–12.0 mm in diameter 4.0–15.0 mm in diameter 7.0–10.0 mm in diameter 8.0–12.0 mm in diameter 8.0–25.0 mm in diameter 1.5–4.0 cm in diameter 1.0–2.5 cm in diameter 1.0–4.0 cm in diameter 2.5–4.0 cm in diameter 2.5–4.0 cm in diameter 1.5–3.0 cm in diameter 2.0–5.0 cm in diameter 2.0–2.5 cm in diameter 2.0–3.0 cm in diameter 1.5–3.5 cm in diameter 1.5–3.0 cm in diameter 2.0–3.5 cm in diameter 1.5–7.5 cm in diameter 1.5–6.5 cm in diameter 1.0–2.5 cm in diameter 2.0–4.5 cm in diameter 2.0–4.0 cm in diameter 1.0–3.0 cm in diameter 1.0–4.0 cm in diameter 2.0–4.5 cm in diameter

Seeds Without sarcotesta or aril Without sarcotesta or aril Without sarcotesta or aril Without sarcotesta or aril Without sarcotesta or aril Without sarcotesta or aril Enveloped by an imperfect aril (juicy) Enveloped by an imperfect aril (spongy) Enveloped by an imperfect aril (spongy) Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta Wholly covered by sarcotesta

Fig. 2.11 Three types of fruits of Paris species. (a) Globose berry; (b) angular berry; and (c) berrylike capsule

Fig. 2.13 Comparison of fruit and seed morphology between Paris sect. Thibeticae (a) and P. sect. Axiparis (b) Fig. 2.12 Four types of seeds identified in Paris. (a) Dry seed; (b) seed partially enveloped by spongy aril; (c) seed partially enveloped by juicy aril; and (d) seed wholly covered with juicy sarcotesta

2.2 Pollen Morphology

23

oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation foveolate. (11) P. qiliangiana H. Li, J. Yang & Y. H. Wang (Fig. 2.17d) Mean length of polar axis ¼ 19.34
0.67 μm; mean length of equatorial axis ¼ 40.50
0.50 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation reticulate. (12) P. mairei H. Lév. (Fig. 2.18a)

Fig. 2.14 Distribution of three types of pollen ornamentations in Paris species in the plastome-based phylogenetic tree

oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation reticulate.

Mean length of polar axis ¼ 18.34
0.34 μm; mean length of equatorial axis ¼ 37.50
0.50 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation reticulate. (13) P. marmorata Stearn (Fig. 2.18b)

(6) P. vanioti H. Lév. (Fig. 2.16b) Mean length of polar axis ¼ 20.00
1.00 μm; mean length of equatorial axis ¼ 43.50
2.00 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation reticulate.

Mean length of polar axis ¼ 12.34
0.34 μm; mean length of equatorial axis ¼ 36.50
0.50 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a narrow and deep monosulcate; exine ornamentation reticulate. (14) P. luquanensis H. Li (Fig. 2.18c)

(7) P. thibetica Franch. (Fig. 2.16c) Mean length of polar axis ¼ 19.25
0.25 μm; mean length of equatorial axis ¼ 44.40
0.90 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a narrow and deep monosulcate; exine ornamentation foveolate.

Mean length of polar axis ¼ 21.34
1.67 μm; mean length of equatorial axis ¼ 37.00
1.00 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation reticulate. (15) P. cronquistii (Takht.) H. Li (Fig. 2.18d)

(8) P. yunnanensis Franch. (Fig. 2.17a)

Mean length of polar axis ¼ 19.65
0.35 μm; mean length of equatorial axis ¼ 48.65
0.65 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a narrow and deep monosulcate; exine ornamentation foveolate. (9) P. chinensis Franch. (Fig. 2.17b) Mean length of polar axis ¼ 21.34
1.34 μm; mean length of equatorial axis ¼ 41.15
0.15 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation foveolate.

Mean length of polar axis ¼ 16.63
0.88 μm; mean length of equatorial axis ¼ 39.50
2.50 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a narrow and deep monosulcate; exine ornamentation foveolate. (16) P. dunniana H. Lév. (Fig. 2.19a)

Mean length of polar axis ¼ 25.25
0.25 μm; mean length of equatorial axis ¼ 46.25
0.75 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation foveolate.

(10) P. delavayi Franch. (Fig. 2.17c)

(17) P. xichouensis (H. Li) Y. H. Ji, H. Li & Z. K. Zhou (Fig. 2.19b)

Mean length of polar axis ¼ 16.50
1.50 μm; mean length of equatorial axis ¼ 40.34
2.34 μm; pollen grains

Mean length of polar axis ¼ 22.34
3.67 μm; mean length of equatorial axis ¼ 44.75
2.75 μm; pollen grains

2

Fig. 2.15 Pollen morphology of Paris quadrifolia (a), P. verticillata (b), P. bashanensis (c), and P. tetraphylla (d)

24 Morphology

Fig. 2.16 Pollen morphology of Paris forrestii (a), P. vaniotii (b), and P. thibetica (c)

2.2 Pollen Morphology 25

2

Fig. 2.17 Pollen morphology of Paris yunnanensis (a), P. chinensis (b), P. delavayi (c), and P. qiliangiana (d)

26 Morphology

Fig. 2.18 Pollen morphology of Paris mairei (a), P. marmorata (b), P. luquanensis (c), and P. cronquistii (d)

2.2 Pollen Morphology 27

2

Fig. 2.19 Pollen morphology of Paris dunniana (a), P. xichouensis (b), P. vietnamensis (c), and P. caobangensis (d)

28 Morphology

Fig. 2.20 Pollen morphology of Paris polyphylla (a), P. lancifolia (b), P. yanchii (c), and P. fargesii (d)

2.2 Pollen Morphology 29

30

2

oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation foveolate. (18) P. vietnamensis (Takht.) H. Li (Fig. 2.19c) Mean length of polar axis ¼ 21.50
1.50 μm; mean length of equatorial axis ¼ 47.09
0.42 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation foveolate. (19) P. caobangensis Y. H. Ji, H. Li & Z. K. Zhou (Fig. 2.19d) Mean length of polar axis ¼ 19.50
0.50 μm; mean length of equatorial axis ¼ 38.84
1.84 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation foveolate. (20) P. polyphylla Sm. (Fig. 2.20a)

Mean length of polar axis ¼ 21.00
1.50 μm; mean length of equatorial axis ¼ 42.40
1.10 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation reticulate. (21) P. lancifolia Hayata (Fig. 2.20b) Mean length of polar axis ¼ 17.67
1.00 μm; mean length of equatorial axis ¼ 39.75
0.25 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation foveolate. (22) P. yanchii H. Li, L. G. Lei & Y. M. Yang (Fig. 2.20c) Mean length of polar axis ¼ 19.34
0.67 μm; mean length of equatorial axis ¼ 44.00
2.50 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation foveolate. (23) P. fargesii Franch. (Fig. 2.20d) Mean length of polar axis ¼ 16.34
0.34 μm; mean length of equatorial axis ¼ 37.00
0.50 μm; pollen grains oblate-spheroidal, elliptic at polar view, with a deep monosulcate; exine ornamentation foveolate.

2.2.2

Taxonomic Implications

It has been proven that morphological characters of pollen grains are useful in the exploration of the intergeneric relationships in Melanthiaceae (Takahashi and Kawano

Morphology

1989). Generic circumscription of Paris is a long-standing issue in taxonomy. Franchet (1888), Hara (1969), Li (1998), and Ji (2006) recognized Paris as a genus, while Takhtajan (1983) divided it into three separate genera, Paris s.s., Daiswa, and Kinugasa. Phylogenetic studies based on complete plastomes (Ji et al. 2019; Yang et al. 2019) suggested that Paris should be recognized as a single genus. Interestingly, the currently most comprehensive analysis of pollen morphology provides further evidence to justify this assumption. It is noteworthy that pollen grains of Paris species are similar in size, shape, and structure but significantly different from the spherical pollen grains of Trillium species (Takahashi 1982, 1984; Wei 1988, 1998; Wei and Wang 2001), suggesting that all Paris species should be placed in the same genus. Wei (1988, 1998) proposed that pollen characteristics may provide insights into the subdivision of the genus Paris. However, I found that many species assigned to different sections in Paris exhibit similar pollen morphology (Fig. 2.14). For instance, P. japonica and P. tetraphylla have similar pollen ornamentation (gemmate) but belong to two different sections (P. sect. Kinugasa and P. sect. Paris). A total of 12 Paris species exhibit reticulate pollen ornamentation; however, these are assigned to distinct subgenera or sections, according to the classification of Franchet (1888), Hara (1969), Li (1998), and Ji (2006). This suggests that pollen morphology of Paris is inconsistent with gross morphological features. Consequently, none of previous infrageneric classifications outlined by Franchet (1888), Hara (1969), Li (1998), and Ji (2006) are supported by pollen characteristics. Therefore, pollen morphology alone is insufficient to determine the classification in Paris at either sub-generic or sectional level. Nevertheless, I also found that some sister species, with highly similar gross morphological characters, possess greatly distinct pollen morphology; examples of pairs of sister species include P. forrestii and P. vaniotii, P. luquanensis and P. marmorata, and P. vietnamensis and P. xichouensis. Reliable identification of these closely related species is possible based on pollen characters. Therefore, interspecific variation in pollen morphology can provide useful information for solving species-level taxonomic disputes in Paris.

References Bonfante-Fasolo P (1984) Anatomy and morphology of V. A. mycorrhizae. In: Powell CL, Bagyaraj DJ (eds) VA Mycorrhizae. CRC Press, Boca Raton, pp 5–33 Erdtman G (1952) Pollen morphology and plant taxonomy. Almqvist and Wiksell, Stockholm Erdtman G (1969) Handbook of palynology—an introduction to the study of pollen grains and spores. Munksgaard, Copenhagen

References Farmer SB, Schilling EE (2002) Phylogenetic analyses of Trilliaceae based on morphological and molecular data. Syst Bot 27:674–692. https://doi.org/10.2307/3093915 Franchet A (1888) Monographie du genre Paris. Mem Soc Philom Cent 24:267–291 Furness CA, Gregory T, Rudall PJ (2015) Pollen structure and diversity in Liliales. Int J Plant Sci 176:697–723 Gallaud I (1904) Etudes sur les mycorrhizes endotrophs. Le Biggot Frères, France Gallaud I (1905) Etudes sur les mycorrhizes endotrophs. Rev Gen Bot 17:5–500 Hara H (1969) Variations in Paris polyphylla Smith with reference to other Asiatic species. J Fac Sci Univ Tokyo Sect 3(10):141–180 Harley JL, Harley EL (1987) A check-list of mycorrhiza in the British flora. New Phytol 105:1–102. https://doi.org/10.1111/j.1469-8137. 1987.tb00674.x Huang TC (1972) Pollen flora of Taiwan. Taiwan University, Taipei Huang YL, Li XJ, Yang ZY, Yang CJ, Yang JB, Ji YH (2016) Analysis of complete chloroplast genome sequences improves phylogenetic resolution of Paris (Melanthiaceae). Front Plant Sci 7:1797. https:// doi.org/10.3389/fpls.2016.01797 Ikuse M (1956) Pollen grains of Japan. Hirokawa Pub, Tokyo, Co. 48 Jacquemyn H, Brys R, Hutchins M (2008) Biological flora of the British Isles: Paris quadrifolia L. J Ecol 96:833–844. https://doi.org/10. 1111/j.1365-2745.2008.01397.x Ji YH (2006) Phylogeny and biogeography of Paris (Melanthiaceae). Ph.D. Dissertation. Graduate University of Chinese Academy of Sciences, Beijing Ji YH, Fritsch PW, Li H, Xiao TJ, Zhou ZK (2006) Phylogeny and classification of Paris (Melanthiaceae) inferred from DNA sequence data. Ann Bot 98:245–256. https://doi.org/10.1046/j.1365-2885. 2002.00426.x Ji YH, Yang CJ, Huang YL (2017) A new species of Paris sect. Axiparis (Melanthiaceae) from Yunnan, China. Phytotaxa 306:234–236 Ji YH, Yang LF, Chase MW et al (2019) Plastome phylogenomics, biogeography, and clade diversification of Paris (Melanthiaceae). BMC Plant Biol 19:543. https://doi.org/10.1186/s12870-019-2147-6 Kazempour-Osaloo S, Kawano S (1999) Molecular systematics of the Trilliaceae. II. Phylogenetic analyses of Trillium and its allies using sequences of rbcL and matK genes of cpDNA and internal transcribed spacers of 18S-26S nrDNA. Plant Spec Biol 14:75–94 Li H (1992) New taxa of the genus Paris L. Act Bot Yunnan 5:13–18 Li H (1998) The genus Paris (Trilliaceae). Science Press, Beijing Ou H, Guo DQ, Lin JJ et al (2016) Effects of different AM fungi on quantity and enzyme activity of rhizosphere soil microorganism of Paris polyphylla var. yunnanensis. J Chin Med Mater 39:948–955 Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, London

31 Takahashi M (1982) Pollen morphology in North American species of Trillium. Am J Bot 69:1185–1195 Takahashi M (1984) Pollen morphology in Paris and its related genera. Bot Mag 97:233–245 Takahashi M, Kawano S (1989) Pollen morphology of the Melanthiaceae and its systematic implications. Ann Mo Bot Gard 76:863–876. https://doi.org/10.2307/2399650 Takhtajan A (1983) A revision of Daiswa (Trilliaceae). Brittonia 35:255–270. https://doi.org/10.2307/2806025 Wei ZX (1988) Studies on the pollen morphology of Paris. Act Bot Yunnan 10:147–153 Wei ZX (1998) Pollen morphology of Paris and the implication in systematics. In: Li H (ed) The genus Paris (Trilliaceae). Science Press, Beijing, pp 96–99 Wei ZX, Wang H (2001) Studies of pollen morphology of four genera of Trilliaceae. Act Bota Yunnan 23:451–456 Wei ZX, Guo DQ, Li HF et al (2015) Photosynthetic parameters and physiological indexes of Paris polyphylla var. yunnanensis influenced by arbuscular mycorrhizal fungi. China J Chin Mater Med 40:3945–3952. https://doi.org/10.4268/cjcmm20152010 Yang XH (1998) Morphology of Paris. In: Li H (ed) The genus Paris (Trilliaceae). Science Press, Beijing, pp 66–87 Yang LF, Yang ZY, Liu CK, He ZS, Zhang ZR, Yang J et al (2019) Chloroplast phylogenomic analysis provides insights into the evolution of the largest eukaryotic genome holder, Paris japonica (Melanthiaceae). BMC Plant Biol 19:293. https://doi.org/10.1186/ s12870-019-1879-7 Zhang J, Zhou N, Pan XJ et al (2018) Screening of preponderant arbuscular mycorrhizal fungi species from Paris polyphylla var. yunnanensis seedlings based on biomass and active components. Chin Tradit Herb Drugs 49:1897–1906. https://doi.org/10.7501/j. issn.0253-2670.2018.08.025 Zhang H, Du HH, Guo DQ, Yang M, Wang MJ, Zhou N (2019) Effects of inoculation with different AM fungi on functional gene expression in seedlings of Paris polyphylla var. yunnanensis. Nat Prod Res Dev 31:318–324. https://doi.org/10.16333/j.1001-6880.2019.2.022 Zhao TZ, Wang BQ, Ma Q, Fan QL (2014) Study on best harvesting time of Paris polyphylla var. yunnanensis. Chin Wild Plant Resour 33:61–66 Zhou N, Xia CL, Jiang B, Bai ZC, Liu GM, Ma XK (2009) Arbuscular mycorrhizae in Paris polyphylla var. yunnanensis. China J Chin Mater Med 34:1768–1772 Zhou N, Zhang DW, Guo DQ, Ding B, Zhang DQ, Wang X (2014) Effect of the arbuscular mycorrhiza fungi on heavy metals in Paris polyphylla var. yunnanensis by artificial cultivation. Chin Tradit Pat Med 36:2583–2586. https://doi.org/10.3969/j.issn.1001-1528.2014. 12.031

3

Biology

3.1

Distribution and Habitat

Paris is a temperate genus with broad distribution in East Asia and Europe (Fig. 3.1), entering the Arctic at the northernmost limit (~70
N) and reaching Hainan Island and Indochina at the southernmost limit (~18
N). Given this widespread distribution, species of this genus grow in five distinct climate zones (frigid, cold temperate, temperate, subtropical, and tropical) in Eurasia, with the elevation ranging from 50 to 3500 m above the sea level (Table 3.1). Overall, species with long and slender rhizomes mainly grow in frigid, cold temperate, and temperate areas above 35
N, whereas species with thick rhizomes are restricted to subtropical and tropical areas. Based on current taxonomic revision (see Chap. 6), the Paris genus contains 26 species. Among these, two species (P. quadrifolia and P. incompleta) occur in Europe; P. quadrifolia is widely distributed from Siberia to West Europe, while P. incompleta is endemic to Caucasian forests between the Black Sea and Caspian Sea. The remaining 24 species are species restricted to East Asia, mainly China. In general, species diversity increases with the decrease in latitude. Subtropical areas of East Asia (between 20
N and 30
N) harbor the highest species richness. Except two Japanese species (P. japonica and P. tetraphylla), the remaining 22 out of 24 Asian Paris species occur in this region, with significant species diversification (Table 3.1). Although the distribution range of Paris has extended to Indochina (Vietnam, Laos, Myanmar, and Thailand) and Himalayas (Nepal, Bhutan, and India), none of the species are native to these areas. A total of 22 species are found in China, of which 8 species are endemic to China (P. bashanensis, P. delavayi, P. dunniana, P. lancifolia, P. mairei, P. qiliangiana, P. vaniotii, and P. yanchii), with southwest China (Yunnan, Sichuan, Guizhou, and Chongqing) as the center of distribution. Paris species mainly grow as understory herbs in evergreen broad-leaved forests, deciduous broad-leaved forests,

coniferous forests, bamboo thickets, and scrubs (Li 1998). Based on herbarium specimen information, it was showed that species with long and slender rhizomes (Paris sect. Paris) are restricted to deciduous broad-leaved forests and coniferous (Taiga) forests, whereas P. dunniana, P. vietnamensis, and P. xichouensis exclusively grow in evergreen broad-leaved forests (Table 3.2). The remaining species can be found in deciduous broad-leaved forests (23/26) and warm coniferous forests (17/26), the zonal forests in temperate regions. This suggests that the primary habitat for Paris species is not evergreen broad-leaved forests, although the genus exhibits highest species diversity in subtropical areas. Thus, it is reasonable to hypothesize that the most recent common ancestor (MRCA) of the genus occurs in temperate areas.

3.2

Phenology

Aerial portions of Paris species are developed from apical buds on the rhizome. Apical buds are usually produced in winter (October to December), which synchronizes with the dormancy of aerial shoots. The growth rate of apical buds is greatly affected by soil temperature. Generally, higher soil temperature accelerates the development of apical buds, and vice versa. Shoots of Paris species start to develop in spring (February to May) and produce flowers from March to June (Fig. 3.2). However, the timings of shoot emergence, flower production, and fruit maturity is greatly divergent cross species (Table 3.3). In general, species at low latitudes sprout and flower earlier than those at high latitudes. For species distributed in tropical areas, such as P. dunniana, P. vietnamensis, and P. xichouensis, shoots emerge from underground rhizomes in November–December and produce flowers in January. By contrast, P. quadrifolia, a species occurring at high latitudes, produces shoots in April–May, which usually blossom in May–June, according to the

# Science Press 2021 Y. Ji, A Monograph of Paris (Melanthiaceae), https://doi.org/10.1007/978-981-15-7903-5_3

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Fig. 3.1 Distribution map of Paris

observations of Eriksson and Ehrlén (1991) and Diekmann (1996). However, there are exceptions; for example, P. thibetica, a species distributed at high elevations, always sprouts and flowers in March–April, when snow has not yet melted and the air temperature is lower than 5
C. Flowers of Paris species remain open for approximately 2–3 weeks, and stamens begin to wither at this time (Fig. 3.3). Development of fruits largely differs across species (Table 3.3). In species occurring at high latitudes or altitudes, for example, P. quadrifolia (Diekmann 1996; Ehrlén et al. 2006) and P. thibetica (Y. Ji, personal observation), fruits are produced in August–September. By contrast, for species distributed in subtropical areas, such as P. chinensis and P. yunnanensis, development of fruits lasts until September–November. Although P. dunniana, P. vietnamensis, and P. xichouensis flower significantly earlier than other species in this genus, their fruits do not ripen until November–December. Aerial shoots of Paris species generally begin to wither 2–6 weeks after the maturity of fruits. Most species of the genus survive the winter with underground rhizomes. However, it is observed that new shoots of P. dunniana, P. vietnamensis, and P. xichouensis usually sprout in November–December, while their old shoots die in January– March the following year. Because of the overlap between old and new shoots over two successive years, plants of these

species form an “evergreen” habit (Fig. 3.4). Compared with those “deciduous” congeneric relatives, “evergreen” species have relatively higher rhizome biomass.

3.3

Propagation and Growth

3.3.1

Pollination

Most species of Paris flower in spring over a duration of approximately 1–3 weeks. According to my personal observation, flowers of such species as P. chinensis, P. delavayi, P. dunniana, P. fargesii, P. forrestii, P. lanceolata, P. liiana, P. luquanensis, P. mairei, P. marmorata, P. thibetica, P. verticillata, and P. vietnamensis are probably protogynous, as their anthers open 2–7 days after the maturity of stigmas. A similar phenomenon was reported in P. quadrifolia by Daumann (1959). Since stigmas stay fresh and receptive for approximately 7–10 days, viable anthers and stigmas overlap for a brief period, leading to selfpollination. Experimental pollination indicates that these species are capable of producing fruit via self-pollination, suggesting that they are self-compatible. The flowers of Paris species (Fig. 3.5) are not bright and showy (except for those of P. japonica) and do not produce a scent or nectar (Knuth 1898; Daumann 1959; Yang 1998). A

3.3 Propagation and Growth

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Table 3.1 Spatial distribution and elevation ranges of Paris species Species P. tetraphylla P. incompleta P. quadrifolia P. verticillata P. bashanensis P. japonica P. thibetica P. vaniotii P. forrestii P. dunniana P. vietnamensis P. xichouensis P. chinensis P. caobangensis P. qiliangiana P. fargesii P. cronquistii P. delavayi P. liiana P. yunnanensis P. luquanensis P. lancifolia P. yanchii P. marmorata P. polyphylla P. mairei

Longitude range (
E) 129.960–143.310 38.080–45.720 0.266–108.000 85.364–145.855 101.762–110.812 136.771–139.966 85.266–104.395 102.111–112.691 82.183–101.718 106.699–109.732 98.420–111.547 104.679–105.115 98.835–122.402 98.998–114.603 103.628–110.812 103.018–121.639 101.632–108.812 102.111–115.866 98.835–108.316 94.006–109.997 102.585–102.733 101.744–121.639 99.305 86.730–101.992 81.760–110.041 87.904–106.291

bag masking experiment showed that pollen vector is not indispensable for fruiting in P. yunnanensis and P. chinensis (Y. Ji, personal observation). As proposed by Daumann (1959), autonomous pollination or windpollination is likely prevalent in Paris species. Strikingly, I found that flowers of several Paris species are frequently visited by honey bees (Fig. 3.6). However, because of the lack of biological observation, it remains unclear whether honey bees serve as potential pollinators or pollen robbers.

3.3.2

Latitude range (
N) 32.000–44.820 40.830–45.050 40.066–70.366 29.138–60.716 29.138–32.880 35.616–38.785 25.275–35.717 24.998–31.590 20.783–30.120 18.591–25.416 20.667–24.900 22.750–23.391 18.579–39.079 18.795–29.553 31.034–34.145 22.049–31.884 22.679–29.138 24.161–32.332 21.734–25.137 20.783–30.075 25.940–26.569 22.484–36.921 25.891 25.744–28.958 23.360–36.061 24.509–33.313

Elevation range (m) 200–1400 600–2000 50–1600 600–3600 1400–2750 1000–2100 1600–3600 700–3000 600–3200 400–1100 600–2000 1200–1500 150–2800 300–2900 720–1140 500–2100 200–1950 700–2900 1200–2200 1000–3200 2300–2800 1100–2300 2300–2800 1500–3100 1100–2800 1800–3500

The fruit size and consequently the number of seeds per fruit vary greatly among Paris species. Eriksson and Ehrlén (1991) reported an average of 33.6  11.2 seeds per berry in P. quadrifolia. A similar seed number per berry was investigated in P. verticillata. By contrast, species of P. sect. Euthyra exhibit higher seed yield. For example, the highest number of seeds per fruit was found in P. yunnanensis (average of 216.4  18.8 seeds in artificially pollinated flowers). In P. chinensis and P. yunnanensis, I found that individuals with high rhizome biomass always produce more seeds than those with low rhizome biomass.

Seed Production

The timing of fruit maturity differs greatly among Paris species (Table 3.3). Fruits of P. quadrifolia need approximately 68 days to develop fully and then persist on the plant for about 45 days (Eriksson and Ehrlén 1991, 1992); fruits of P. verticillata behave similarly. However, the development and maturity of fruits in P. thibetica, P. forrestii, P. chinensis, and P. yunnanensis take approximately 120, 130, 140, and 150 days, respectively (Y. Ji, personal observation). In species growing in tropical areas, such as P. dunniana, P. vietnamensis, and P. xichouensis, fruits ripen in November–December.

3.3.3

Seed Dispersal

Seeds dispersal is an interesting issue in Paris. It is generally accepted that seed of species that produce berries is dispersed by birds (Salisbury 1942). However, Eriksson and Ehrlén (1991) proposed that small mammals are the main seed dispersal agent for P. quadrifolia, whose fruits are berries. Therefore, seed dispersal distances in this species are very small (~0.21–0.33 m per year) (Brunet and Von-Oheimb 1998; Honnay et al. 1998). Population genetic studies detected strong genetic differentiation among P. quadrifolia

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Table 3.2 Occurrence of Paris species in different habitats Taxa P. tetraphylla P. incompleta P. quadrifolia P. verticillata P. bashanensis P. japonica P. thibetica P. vaniotii P. forrestii P. dunniana P. vietnamensis P. xichouensis P. chinensis P. caobangensis P. qiliangiana P. fargesii P. cronquistii P. delavayi P. liiana P. yunnanensis P. luquanensis P. lancifolia P. yanchii P. marmorata P. polyphylla P. mairei

Evergreen broad-leaved forests        + + + + + + +  + +  + + + +    

Deciduous broad-leaved forests + + + + + + + + +    + + + + + + + + + + + + + +

Coniferous forests + + + +  + + + +    +  +  + +  + + + + + + +

Bamboo thickets     +  + + +    +       +  + + + + +

Scrubs      +  +    +       +  + + + + +

Presence (+); Absence ()

populations, suggesting that limited gene flow between populations is caused by limited seed dispersal (Jacquemyn et al. 2005, 2006). It is noteworthy that P. quadrifolia shows the largest distribution range in the genus. Given its short seed dispersal distances, it is still unclear how this species spread over a wide geographical area after the Pleistocene glaciations. In addition to berries, species of P. sect. Euthyra and Thibeticae produce capsules, which dehisce at maturity to expose seeds (Fig. 3.7). These seeds are covered by red (or orange) and juicy sarcotesta (or aril). Such seeds are likely to be dispersed by birds (Brunet and Von-Oheimb 1998; Ehrlén and Eriksson 2000; Ehrlén et al. 2006). However, most species in these two sections show very narrow and restricted distribution range, whereas species with birdmediated seed dispersal show a relatively wide distribution range (Brunet and Von-Oheimb 1998). This raises another question: is seed dispersal in these species an unusual event?

3.3.4

Life Cycle

The natural propagation and growth of Paris species progress at a very slow rate (He et al. 2006; Li et al. 2015;

Cunninghamia et al. 2018). According to my observation of P. yunnanensis, the entire life cycle of this species takes at least 4 or 5 years (Fig. 3.8). The seeds of P. yunnanensis germinate (radicle emergence) after a dormancy period of 3–8 months. After another 6–10 months, the sprouting seeds develop into seedlings with a cordate leaf (develops from cotyledons). Altogether, the single-leaf seedlings are formed in approximately 9–18 months. These seedlings usually go through two stages to develop into adult (flowering) individuals. In the first stage (approximately 1–2 years long), single-leaf seedlings become sterile plants, which bear a whorl of leaves (3–5) at the stem apex. In the second stage (1–2 years), sterile individuals with whorled leaves transform into flowering plants.

3.4

Chromosomes

Changes in chromosome number (e.g., polyploidy and dysploidy) and structure have long been recognized as important drivers of plant speciation and evolution (Grant 1981; Levin 2002; Schubert and Lysak 2011). Therefore, karyotyping, i.e., characterizing the chromosome number, size, and shape, of individuals offers a primary framework

3.4 Chromosomes

37

in subtropical and tropical areas of East Asia, contain six metacentric and four telomeric chromosomes (2n ¼ 6m + 4t). On the other hand, species of P. sect. Paris and Kinugasa, which are mainly distributed in temperate regions of Eurasia, contain six metacentric, two telomeric, and two sub-telomeric chromosomes (2n ¼ 6m + 2t + 2st) or six metacentric and four sub-telomeric chromosomes (2n ¼ 6m + 4st). According to the indices of asymmetry, the “tropical” karyotype of P. sect. Thibeticae, Axiparis, and Euthyra is more asymmetric than the “temperate” karyotype of P. sect. Paris and Kinugasa. Although the octoploid species, P. japonica, has the highest chromosome number (8x ¼ 40), the most frequent chromosome number in this genus is 2n ¼ 10, suggesting that Paris species mainly consist of diploids. Additionally, infraspecific variation in ploidy level has been reported in Paris. For instance, diploid (2x ¼ 10) and tetraploid (4x ¼ 20) individuals have been identified in P. lancifolia and P. marmorata, diploid (2x ¼ 10), triploid (3x ¼ 15), tetraploid (4x ¼ 20) individuals in P. verticillata, and diploid (2x ¼ 10), triploid (3x ¼ 15), tetraploid (4x ¼ 20), and hexaploid (6x ¼ 30) individuals in P. quadrifolia.

3.4.2 Fig. 3.2 Processes of aerial shoot development in Paris chinensis. Emergence of shoot (a) in March, unfolding of leaves (b, c), and flowering (d) in April

to investigate evolutionary relationships among plant taxa at different taxonomic levels (Levin 2002). Here, chromosomal data of Paris species, including their chromosome number, ploidy level, karyotype asymmetry, and the presence of B chromosomes, are reviewed to analyze chromosome evolution patterns in the genus.

3.4.1

Karyotype

Cytological studies have been performed on 21 out of 26 Paris species to date (Table 3.4), showing that chromosome numbers in the genus vary from 10 to 40. Five different chromosome numbers (2n ¼ 10, 15, 20, 30, and 40) have been documented in Paris, revealing that basic chromosome number (x) is 5 (Gu and Li 1988). Despite the relatively small chromosome number, Paris species possess giant chromosomes, with a total haploid chromosome length of more than 90 μm (Gu and Li 1988; Pellicer et al. 2014). Based on the chromosome arm ratio and centromere index, Gu and Li (1988) identified three basic karyotypes within the genus. Diploid cells of species belonging to P. sect. Thibeticae, Axiparis, and Euthyra, which exclusively occur

B Chromosomes

B chromosomes, also known as supernumerary or accessory chromosomes, coexist with normal chromosomes, are dispensable, and exhibit non-Mendelian inheritance (Houben et al. 2014). These chromosomes are found in numerous taxa including fungi, plants, and animals (Jones and Rees 1982; Jones et al. 2008; Houben et al. 2014). In the genus Paris, 13 out of 26 species harbor B chromosomes (Table 3.4), and the prevalence of B chromosomes is proposed as a distinctive feature of Paris genomes (Gu and Li 1988; Li et al. 1988). However, our knowledge on the origin and accumulation mechanism of B chromosomes in Paris is still limited. The distribution of B chromosomes among plants is non-random. Among angiosperms, the presence of B chromosomes is positively correlated with genome size (Palestis et al. 2004; Trivers et al. 2004; Levin et al. 2005). Notably, Paris is a unique angiosperm genus with large genomes. The high frequency of B chromosomes in this genus is the evidence that justifies the assumption that B chromosomes are likely to be found in taxa with a large genome size (Trivers et al. 2004). Therefore, the prevalence of B chromosome in Paris can be explained on the grounds that taxa with large genomes are able to tolerate extra chromosomes more easily than taxa with small genomes (Puertas 2002) or that the greater amount of non-coding DNA, which is mostly what constitutes large genomes, is

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Table 3.3 Phenology of Paris species Species P. tetraphylla P. incompleta P. quadrifolia P. verticillata P. bashanensis P. japonica P. thibetica P. vaniotii P. forrestii P. dunniana P. vietnamensis P. xichouensis P. chinensis P. caobangensis P. qiliangiana P. fargesii P. cronquistii P. delavayi P. liiana P. yunnanensis P. luquanensis P. lancifolia P. yanchii P. marmorata P. polyphylla P. mairei

Shoot emergence April–May April April–May May–June May–June May–June March–April March–April March–April November–December November–December November–December March–April March March–April March–April March–April March–April March–May April–May April–May March–April April–May April–May April–May April–May

Flowering April–May April–May April–June May–June May–June June–July March–April April March–May March–April January–March February–April March–May March–May March–May March–May April–June April–June April–June April–May April–June April–June April–June April–June April–June April–June

Fig. 3.3 Flower in bloom (a) and flower with withered stamens (b)

Fruit maturity September September August–September September September September–October August–September September September–October December November–December November August–October September–November September–October September–October September–October September–October October–December September–October October September–October October October September–October October

Withering of aerial organs September–October September–October September September–October September–October October August–September September–October October February–March January–February January–February September–October October–November September–November September–November October October December November October October October October September–October October–November

Dormancy October–April October–April October–April October–May October–May October–May September–March October–March October–March N/A N/A N/A October–March October–March October–March October–March October–March October–March December–March November–April October–April October–March October–April October–April October–April October–April

Fig. 3.4 The overlap between old and new shoots over two successive years observed in Paris dunniana (a), and P. vietnamensis (b)

3.4 Chromosomes

Fig. 3.5 Flower of Paris tetraphylla (a), P. incompleta (b), P. quadrifolia (c), P. verticillata (d), P. bashanensis (e), P. japonica (f), P. thibetica (g), P. vaniotii (h), P. forrestii (i), P. dunniana (j), P. vietnamensis (k), P. xichouensis (l), P. chinensis (m), P. caobangensis

39

(n), P. qiliangiana (o), P. fargesii (p), P. cronquistii (q), P. delavayi (r), P. yunnanensis (s), P. luquanensis (t), P. lancifolia (u), P. yanchii (v), P. marmorata (w), P. polyphylla (x), and P. mairei (y)

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Fig. 3.6 Flowers of Paris vietnamensis (a), P. yanchii (b), and P. yunnanensis (c) being visited by Chinese honey bees (Apis cerana)

itself a trigger for the formation of B chromosomes (Levin et al. 2005). B chromosomes are most possibly derived from the A chromosome complement (Camacho et al. 2000; Jones and Houben 2003; Camacho 2005). It is widely accepted that B chromosomes are initially formed by segmental or whole genome duplication (Houben et al. 2014), followed by a series of chromosomal arrangements (Zhou et al. 2012). According to previous studies, Paris has undergone significant genome expansion during evolution (Pellicer et al. 2014; Yang et al. 2019). Thus, B chromosomes in Paris could be a by-product of genome expansion and chromosomal rearrangements. In addition, B chromosomes can arise infra-specifically from the A genome of the host species or from the genome of closely related species through hybridization (Camacho et al. 2000; Camacho 2005). It is interesting to note that interspecific hybridization occurs frequently in Paris (Ji et al. 2006, 2019), which might play an important role in triggering the formation of B chromosomes in this genus.

3.4.3

Chromosome Evolution

To evaluate the karyological relationships within Paris, refer to Fig. 3.9, which shows the phylogenetic tree generated analyses of complete plastome DNA sequences (see Chap. 5). The combination of karyological data with phylogeny offers the opportunity to investigate the direction of karyotypic evolution in the genus. At the sectional level, P. sect. Thibeticae, Axiparis, and Euthyra, which possess the “tropical” karyotype, are karyologically more similar to each other and distinct from P. sect. Paris and Kinugasa, which possess the “temperate” karyotype. Within this genus, the karyotypic asymmetry is associated with phylogenetic position of analyzed taxa. Briefly, species of P. sect. Paris and

Kinugasa have more symmetrical “temperate” karyotype, and these two sections occupy the early branched position in the phylogenetic tree, suggesting that karyotypic evolution in Paris is characterized by an increasing trend towards asymmetry. The evolutionary direction of karyotypic asymmetry in Paris highly coincides with the theoretical prediction that asymmetrical karyotypes are derivatives of ancestral cytotypes that were more symmetrical (Stebbins 1971). Another major process responsible for generating karyotypic diversity in Paris is polyploidization. A total of six Paris species have been identified as polyploids (Fig. 3.9, Table 3.4). The phylogenetically disparate placement of these species in tree topologies implies that polyploidization (or whole genome duplication) occurred independently during the evolution of Paris. Thus, the occurrence of polyploid in this genus may not provide systematic information. P. japonica was supposed to be an allo-octaploid resulted from hybridization between Paris and Trillium (Haga 1937). A previous study revealed that there could have been hybridization between section Paris and Trillium after the section Paris split from the rest of the genus; this suggests that ancient hybridization is likely responsible for the speciation of P. japonica (Ji et al. 2019), providing molecular evidence to the assumption of Haga (1937). By contrast, no cytonuclear discordance was detected in P. sect. Paris (Ji et al. 2019), and species in this section are not sympatric with congeneric species. Therefore, tetraploids or hexaploids found in P. verticillata (2n ¼ 20) and P. quadrifolia (2n ¼ 20, 30) are most likely autopolyploids. The occurrence of triploids in these two species implies the lack of reproductive isolation between infraspecific diploid and tetraploid individuals. Given that natural hybridization occurs between frequently sympatric species of P. sect. Euthyra (Ji et al. 2006, 2019), tetraploid individuals detected in P. lancifolia, P. marmorata, and P. polyphylla are likely allopolyploids that arose from interspecific hybridization.

3.4 Chromosomes

Fig. 3.7 Dehisced capsule and seeds in representative species of Paris sect. Thibeticae: Paris thibetica (a); and P. sect. Euthyra: P. chinensis (b), P. dunniana (c), P. fargesii (d), P. lancifolia (e), P. luquanensis (f),

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P. mairei (g), P. polyphylla (h), P. qiliangiana (i), P. yanchii (j), P. yunnanensis (k), and P. liiana (L)

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Fig. 3.8 Life cycle of Paris species, represented by Paris yunnanensis

3.5

Genomes

3.5.1

Genome Size

Genome size, defined as the haploid nuclear DNA content (1C value), exhibits extreme diversity in angiosperms, varying by approximately 2400-fold between the smallest and largest genomes (Leitch et al. 1998, 2010; Pellicer et al. 2010, 2013, 2014; Dodsworth et al. 2015). Although the distribution of genome size in angiosperms is significantly skewed towards small sizes (with a mean value of 1C  3.5 pg), large genomes (1C  35 pg) occur in only a few lineages (Kelly and Leitch 2011; Dodsworth et al. 2015). To date, five angiosperm species possessing the genome size 1C > 100 pg have been documented in the monocotyledonous families Melanthiaceae (one Paris species and two

Trillium species) and Liliaceae (one Fritillaria species), as well as the eudicot family Viscaceae (one Viscum species) (Leitch et al. 1998, 2010; Bennetzen et al. 2005; Leitch and Leitch 2013; Zonneveld et al. 2005; Hidalgo et al. 2017), suggesting that genomic gigantism may have originated and evolved independently angiosperms. In addition to its distinct morphological features, Paris is unique in angiosperms in possessing large genomes. Previously, C-value estimates were reported for only a few taxa of Paris (Zonneveld et al. 2005; Leitch et al. 2010; Pellicer et al. 2010, 2014). It is noteworthy that the minimum documented genome size in the genus (P. bashanensis, 1C ¼ 29.38 pg) is much larger than the mean genome size of angiosperms (Pellicer et al. 2010, 2014). Moreover, the largest known eukaryotic genome belongs to this genus (P. japonica, 1 C ¼ 148.88 Gb) (Pellicer et al. 2010; Dodsworth et al. 2015). To better understand the genomic diversity and

3.5 Genomes

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Table 3.4 Chromosome data of Paris species Taxa P. tetraphylla

Chromosome number (2n) 10; 10 + (1, 5, 6, 7, 8) B

P. incompleta P. quadrifolia

10 10; 3x ¼ 15; 4x ¼ 20, 20 + (1, 2, 10) B; 6x ¼ 30

P. verticillata

10; 3x ¼ 15; 4x ¼ 20

P. bashanensis P. japonica

10 8x ¼ 40

P. thibetica P. vaniotii P. forrestii P. dunniana P. vietnamensis P. chinensis P. fargesii P. cronquistii P. delavayi P. yunnanensis P. luquanensis P. lancifolia

10 10 10, 10 + 2B 10, 10 + 1B 10 10, 10 + 2B 10 10, 10 + (1, 2) B 10, 10 + 1B 10 10 10; 4x ¼ 20

P. marmorata P. polyphylla

10 10, 10 + (1, 2) B; 4x ¼ 20

P. mairei

10; 10 + 2B

References Haga (1961), Kayano (1961), Miyamoto and Kurita (1990), Miyamoto et al. (1991) and Uchino and Wang (1997) Gagnidze et al. (1985) and Punina et al. (2005) Laane (1969), Kartashova et al. (1974), Belaeva and Siplivinsky (1976), Krogulevich (1976), Malla et al. (1979), Bjerketvedt and Laane (1982), Löve and Löve (1982), Krasnikov (1991) and Chepinoga et al. (2010) Haga (1937), Krogulevich (1978), Sokolovskaya and Probatova (1985), Hong and Zhu (1987), Hong and Sauer (1990), Miyamoto et al. (1991, 1992, 1999), Li and Qi (1993), Miyamoto (1993) and Li (1998) Gu and Na (1986) Haga (1934, 1937), Darlington and Cour (1940), Kurabayashi et al. (1958), Miyamoto et al. (1992), Miyamoto (1993), Li (1998) and Pellicer et al. (2010) Kurosawa (1966), Gu and Na (1986), Miyamoto et al. (1992) and Li (1998) Gu and Li (1988), Miyamoto et al. (1992) and Li (1998) Gu and Li (1988), Gu et al. (1992), Miyamoto et al. (1992), Li (1998) and Wang et al. (2004) Gu and Na (1986), Kotseruba and Myakoshina (1999) and Punina et al. (2001, 2005) Gu and Li (1988), Miyamoto et al. (1992), Li (1998) and Kotseruba (2001) Gotoh and Kikkawa (1937) and Hsu (1971) Gu and Na (1986) Gu and Li (1988), Gu (1988), Li (1998) and Miyamoto et al. 1992 Gu and Li (1988), Wang (1989), Miyamoto et al. (1992) and Li (1998) Miyamoto et al. (1992), Li (1998) and Wang et al. (2004) Gu et al. (1992) and Li (1998) Kurosawa (1966), Gu and Na (1986), Wang (1989), Miyamoto et al. (1992), Li and Qi (1993) and Li (1998) Kurosawa (1971) and Gu and Na (1986) Larsen (1963), Mehra and Sachdeva (1979), Malla et al. (1981), Hong and Zhu (1987), Chatterjee et al. (1989) and Miyamoto et al. (1992, 1999) Gu and Na (1986), Gu et al. (1992), Miyamoto et al. (1992) and Li (1998)

Fig. 3.9 Karyotype data mapped along the plastome-based phylogenetic tree to investigate chromosome evolution within Paris

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Table 3.5 Genome sizes of 24 Paris species Taxa P. tetraphylla P. incompleta P. quadrifolia P. verticillata P. bashanensis P. japonica P. thibetica P. vaniotii (1) P. vaniotii (2) P. vaniotii (3) P. forrestii (1) P. forrestii (2) P. forrestii (3) P. forrestii (4) P. dunniana P. vietnamensis P. chinensis P. caobangensis (1) P. caobangensis (2) P. fargesii P. cronquistii P. delavayi P. liiana (1) P. liiana (2) P. liiana (3) P. yunnanensis (1) P. yunnanensis (2) P. yunnanensis (3) P. yunnanensis (4) P. luquanensis P. lancifolia (1) P. lancifolia (2) P. yanchii P. marmorata P. polyphylla P. mairei a

1C value (pg)a 40.75 42.25 50.52 31.21 29.38 152.23 51.30 55.38 57.13 60.80 87.27 55.37 57.13 55.76 59.98 62.90 55.34 65.30 64.13 60.83 63.44 61.79 52.98 59.14 58.30 50.80 57.13 57.72 54.22 64.60 50.13 54.80 53.75 70.36 54.22 55.96

1C value (Mb)b 39848.61 41315.61 49408.56 30518.49 28735.56 148880.94 50171.61 54162.53 55872.93 59461.07 85352.92 54150.40 55872.93 54538.05 58662.94 61513.02 54125.05 63867.73 62714.51 59488.40 62047.34 60433.99 51817.22 57842.48 57013.19 49678.36 55872.93 56451.88 53023.27 63175.47 49031.35 53592.40 52570.94 68816.14 53022.27 54732.67

Data source Pellicer et al. (2014) Pellicer et al. (2014) Pellicer et al. (2014) Pellicer et al. (2014) This study Pellicer et al. (2010) This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study This study Pellicer et al. (2014) This study

Standards used for genome size assessment: P. polyphylla 1C value (pg) ¼ 54.22; 1C value (Mb) ¼ 53022.27 (Pellicer et al. 2014) 1pg ¼ ~987 Mb (Dolezel et al. 2003)

b

evolution of large genome size in Paris, I here present a general survey of genome size across Paris species using flow cytometry technology. My investigation represents the most comprehensive survey of genome size in Paris, with 1C values reported for 24 species (Table 3.5). Overall, 1C values in Paris varied by approximately 5.18-fold, ranging from 29.38 pg in P. bashanensis to 152.23 pg in P. japonica. Interestingly, in five species with slender rhizomes, namely, P. bashanensis (1C ¼ 29.38 pg), P. incompleta (1C ¼ 42.25 pg), P. quadrifolia (1C ¼ 50.52 pg), P. tetraphylla

(1C ¼ 40.75 pg), and P. verticillata (1C ¼ 31.21 pg), the mean genome size (1C ¼ 38.82 pg) is significantly ( p < 0.01) smaller than that of species with thick rhizomes (1C ¼ 58.93 pg). In addition, species for which more than one sample was examined, their genome size differed among individuals. For instance, 1C values varied from 64.12 to 65.30 pg in P. caobangensis, from 55.37 to 87.27 pg in P. forrestii, from 50.13 to 54.80 pg in P. lancifolia, from 55.38 to 60.80 pg in P. vaniotii, from 52.98 to 59.14 pg in P. liiana, and from 50.80 to 57.72 pg in P. yunnanensis. Given its high levels of diversity in genome size, Paris

3.5 Genomes

represents an ideal model for investigating the origin and evolution of genome gigantism.

3.5.2

Possible Mechanisms Underlying the Formation of Large Genomes

There are still great technical difficulties in sequencing large and giant genomes, the mechanisms underlying the formation of large genomes remain poorly understood (Dodsworth et al. 2015). Previous studies suggested that the main mechanisms contributing to genome expansion in plants are polyploidy and the proliferation of repetitive DNA sequences, especially transposable elements (Leitch and Leitch 2012). In diploids, the proliferation of transposable elements has largely contributed to the expansion of genome size (Hawkins et al. 2006, 2009; Piegu et al. 2006; Kejnovsky et al. 2012; Slotkin et al. 2012). Given that most species in Paris are diploid, the large or giant genomes in this genus can be explained by a burst of transposable elements that dramatically expanded Paris genomes (Pellicer et al. 2014). Interestingly, Paris (as well as the sister genus Trillium) has the lowest chromosome number (2n ¼ 10) in Melanthiaceae. Analysis of chromosome diversity and evolution in Melanthiaceae suggests that such low chromosome number probably resulted from recurrent chromosome losses (Pellicer et al. 2014). However, nearly all Paris species have large chromosome sizes, based on the total karyotype length of more than 90 μm (Gu and Li 1988; Pellicer et al. 2014). This suggests that chromosome losses in Paris were most likely accompanied by high rates of chromosomal expansion. Polyploidization (or whole genome duplication) was shown to be the main cause of expansion of chromosome size in plants (Adams and Wendel 2005; Grover and Wendel 2010; Leitch and Leitch 2012). Therefore, ancient polyploidization and chromosomal rearrangements may have played important roles in the formation of large genomes in Paris.

3.5.3

Plastid Genomes

The chloroplast, which possesses an independent genome (plastome), is a key organelle in plant cells for photosynthesis and carbon assimilation as well as biosynthetic pathways of starch, fatty acids, pigments, and amino acids (Palmer 1985; Neuhaus and Emes 2000; Daniell et al. 2016). Chloroplast is a self-replicating organelle, which is maternally inherited in most angiosperms (Palmer 1985). A typical angiosperm plastome encodes 113 unique genes arranged in a quadripartite structure, consisting of a large single copy (LSC, 80–90 kb) region and a small single copy (SSC, 16–27 kb) region separated by a pair of inverted repeat (IR, 20–30 kb) regions (Wicke et al. 2011). Because of the essential roles of

45

chloroplast in flowering plants, plastomes have been subjected to strong selective pressures, leading to conserved genome size, genome structure, gene content, and gene organization (Wicke et al. 2011; Daniell et al. 2016). Thus, information on gene content, structural arrangement, gene loss or pseudogenization, cytonuclear gene transfer, and sequence variations is valuable for elucidating evolutionary relationships in plants (Jansen et al. 2007; Moore et al. 2007, 2010; Comer et al. 2015; Barrett et al. 2016). Plastome sequencing can also offer genetic information related to synthesis of metabolic compounds, biopharmaceuticals, and tolerance to biotic and abiotic stresses (De-Cosa et al. 2001; Dufourmantel et al. 2004; Viitanen et al. 2004; Liu et al. 2007; Verma et al. 2010; Lee et al. 2011; Jin et al. 2012; Su et al. 2015). Therefore, the availability and use of complete plastome sequences in biotechnology is likely to increase the performance of crops in the field (Wurbs et al. 2007; Wu et al. 2010; Daniell et al. 2016; Vining et al. 2017). Given the great economic importance of Paris species in the pharmaceutical industry, comprehensive and evolutionary analyses of their plastomes will help reconstruct robust phylogeny to resolve taxonomic issues in this genus and also help develop molecular markers for the conservation and management of endangered species and germplasms.

3.5.3.1 General Features The size of Paris plastomes ranged from 155,957 to 158,643 bp, which identically exhibited a typical quadripartite structure, comprising the LSC (83,635–84,670 bp) and SSC (18,207–19,586 bp) regions separated by a pair of IRs (26,805–27,810 bp) (Fig. 3.10, Table 3.6). The overall GC content of Paris plastomes varied from 37.2% to 37.7%, however, it was unevenly distributed in LSC, SSC, and IRS. The highest GC content was found in the IR regions (41.6–42.4.6%), followed by LSC (35.6–36.0%). The lowest GC content was identified in the SSC region (31.2–31.8%). All Paris plastomes exhibited identical IR expansion/contraction pattern. The IR/LSC and IR/SSC boundaries in Paris species were located between ycf1 and rps2 (Fig. 3.11). Paris plastomes encoded 114 unique genes, including 80 proteincoding genes, 30 tRNA genes, and 4 rRNA genes (Table 3.7). Multiple sequence alignment using Mauve indicated the absence of structural rearrangements in Paris plastomes (Fig. 3.12). These results suggest that Paris plastomes are highly conserved in size, structure, gene content, and organization. The IR/LSC boundaries of monocot plastomes generally expand into the trnH–rps19 gene cluster, and the IR expansion always results in the duplication of the trnH gene. This differs from non-monocot angiosperms whose IR/LSC junctions are located at the intergenic spacer region between psbA and trnH (Plunkett and Downie 2000). Within

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Fig. 3.10 Plastome map of Paris species

Melanthiaceae, expansion of the IR region into the rpl19 gene was only observed in the basally branched tribe Melanthieae (Yang et al. 2019); by contrast, this type of IR/LSC boundary has been widely observed in some monocot orders such as Asparagales, Commelinales, Zingiberales, and Poales (Wang et al. 2008; Zhu et al. 2016; Lopes et al. 2018). Interestingly, a more progressive expansion of IR into rps3 was found in Chionographideae, Heloniadeae,

Xerophylleae, and Parideae, suggesting that a secondary slippage of IR regions from rps19 to rps3 may have exclusively occurred in Melanthiaceae derived lineages (Yang et al. 2019).

3.5.3.2 Pseudogenization of Plastid cemA Because of the presence of several internal stop codons in coding regions, the plastid cemA was identified as a

3.5 Genomes

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Table 3.6 Features of Paris plastomes

Species P. tetraphylla (MN125596) P. incompleta (MN125572) P. quadrifolia (MN125594) P. verticillata (MH796669) P. bashanensis (MN125580) P. japonica (MH796668) P. thibetica (MN125569) P. vaniotii (MN125567) P. forrestii (MN125565) P. dunniana (MN125592) P. vietnamensis (MN125575) P. xichouensis (MN125585) P. chinensis (MN125588) P. caobangensis (MN125593) P. qiliangiana (MN125576) P. fargesii (MN125595) P. cronquistii (MN125574) P. delavayi (MN125581) P. liiana (MN175249) P. yunnanensis (MN125583) P. luquanensis (MN125573) P. lancifolia (MN125590) P. yanchii (MN125582) P. marmorata (MN709610) P. polyphylla (MN686110) P. mairei (MN125598)

Total Length (bp) 156,567 157,610 157,350 157,946 157,320 155,957 157,389 156,846 157,198 158,256 158,101 158,225 158,060 158,256 158,354 158,643 158,586 158,575 158,252 158,406 157,901 157,833 157,918 157,703 157,817 157,753

GC (%) 37.5 37.7 37.7 37.6 37.7 37.6 37.4 37.4 37.4 37.2 37.3 37.3 37.3 37.2 37.2 37.2 37.2 37.2 37.3 37.3 37.3 37.3 37.3 37.4 37.4 37.4

LSC Length (bp) 83,748 83,691 83,691 83,710 83,671 83,635 84,137 83,930 84,139 84,642 84,566 84,670 84,528 84,564 84,409 84,483 84,432 84,519 84,370 84,340 84,079 84,255 84,073 84,135 84,137 84,134

GC (%) 35.9 36.0 36.0 35.9 36.0 35.9 35.8 35.7 35.7 35.5 35.6 35.6 35.6 35.6 35.6 35.6 35.6 35.6 35.7 35.7 35.8 35.7 35.7 35.7 35.7 35.7

SSC Length (bp) 18,691 19,535 19,553 19,586 19,537 18,712 18,290 18,410 18,207 18,588 18,425 18,445 18,510 18,544 18,539 18,540 18,562 18,478 18,622 18,588 18,600 18,500 18,547 18,434 18,538 18,459

pseudogene in all Paris plastomes (Ji et al. 2019). The cemA gene encodes an inner membrane protein involved in CO2 uptake and is a key plastid gene involved in photosynthesis (Wicke and Naumann 2018). The loss or pseudogenization of this gene has been commonly detected in diverse non-photosynthetic heterotrophic plants (Wicke et al. 2011, 2016; Wicke and Naumann 2018). To our knowledge, the functional loss of cemA from plastomes of photosynthetic autotrophic angiosperms has only been detected in Paris and its sister genus Trillium in Melanthiaceae (Do et al. 2014; Huang et al. 2016; Yang et al. 2019; Ji et al. 2019). Therefore, this mutation provides a molecular synapomorphy to recognize the tribe Parideae. Interestingly, the net photosynthesis rate of Paris species is consistently low under various light conditions, which is likely responsible for the slow plant growth rate in Paris (Su and Zhang 2003; Zhang et al. 2012). Additionally, the low rhizome biomass yield is a key limiting factor affecting the supply of Rhizoma Paridis (dried rhizomes of medicinal Paris) to the pharmaceutical

GC (%) 31.8 31.8 31.8 31.7 31.8 31.7 31.6 31.5 31.5 31.2 31.4 31.4 31.4 31.3 31.3 31.4 31.3 31.4 31.3 31.3 31.4 31.4 31.4 31.5 31.4 31.4

IRs Length (bp) 27,064 27,192 27,053 27,325 27,056 26,805 27,481 27,253 27,426 27,513 27,555 27,555 27,511 27,574 27,703 27,810 27,796 27,789 27,630 27,739 27,611 27,539 27,649 27,567 27,571 27,580

GC (%) 41.9 42.4 42.4 42.3 42.4 42.2 41.9 42.0 41.9 41.8 41.8 41.8 41.8 41.8 41.7 41.6 41.7 41.6 41.8 41.7 41.8 41.8 41.7 41.9 41.9 41.9

Coding sequence Length GC (bp) (%) 91,943 40.1 92,552 40.1 92,422 40.1 92,651 40.1 92,455 40.1 92,026 40.0 92,137 40.0 91,981 40.0 92,071 40.0 92,383 39.9 92,389 40.0 92,389 40.0 92,365 40.0 92,380 40.0 92,402 40.0 92,509 40.0 92,569 40.0 92,461 40.0 91,829 40.0 92,599 40.0 92,542 40.0 92,440 40.0 92,260 40.0 92,406 40.0 91,787 40.0 92,424 40.0

Non-coding sequence Length GC (bp) (%) 64,624 33.8 66,058 34.2 64,928 34.2 65,295 34.1 64,865 34.2 63,931 34.0 65,252 33.7 64,865 33.8 65,127 33.7 65,873 33.4 65,712 33.5 65,836 33.4 65,695 33.4 65,876 33.4 65,952 33.4 66,134 33.4 66,017 33.4 66,114 33.3 66,423 33.5 65,807 33.5 65,359 33.6 65,393 33.6 65,658 33.5 65,297 33.6 66,030 33.6 65,329 33.7

industry (Li et al. 2015). In view of the functional importance of cemA gene in photosynthesis, genetic modification and re-functionalization of this gene may improve the performance of medicinal Paris in the field.

3.5.3.3 Hotspots of Sequence Variation Although Paris plastomes are conserved in size, structure, gene content, and organization, they show high level of interspecific sequence variability. Sliding window analysis of entire plastomes discovered five hypervariable plastid DNA regions, namely, ycf1, ycf2, trnN_GUU-ndhF, rpl32trnL_UAG, and rpl2-rpl23-trnI_CAU-ycf2 (Fig. 3.13), each containing 1044, 247, 396, 83, and 115 variable nucleotides, respectively, of which 566, 124, 203, 28, and 77 were parsimony-informative, respectively, and represented 3–9% of each sequence. These plastid DNA regions can be used as efficient DNA markers for phylogenetic reconstruction, population genetic investigation, and species discrimination.

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Fig. 3.11 Comparison of IR/LSC and IR/SSC boundaries among Paris plastomes

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3.5 Genomes

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Table 3.7 Gene content of Paris plastomes Category of genes Self-replication

Genes for photosynthesis

Other genes

Genes of unknown function

Group of gene Ribosomal RNA genes Transfer RNA genes

Ribosomal protein (small subunit) Ribosomal protein (large subunit) RNA polymerase Translational initiation factor Subunits of photosystem I Subunits of photosystem II Subunits of cytochrome Subunits of ATP synthase Large subunit of Rubisco Subunits of NADH Dehydrogenase Maturase Envelope membrane protein Subunit of acetyl-CoA Synthesis gene ATP-dependent protease Component of TIC complex Conserved open reading frames

Name of gene rrn4.52, rrn52, rrn162, rrn232 trnC_GCA, trnD_GUC, trnE_UUC, trnF_GAA, trnG_GCC, trnG_UCC*, trnH_GUG2, trnK_UUU*, trnL_UAA*, trnL_UAG, trnM_CAU, trnP_UGG, trnQ_UUG, trnR_UCU, trnS_GCU, trnS_GGA, trnS_UGA, trnT_UGU, trnT_GGU, trnV_UAC*, trnY_GUA, trnW_CCA, trnfM_CAU, trnA_UGC*2, trnI_CAU2, trnI_GAU*2, trnL_CAA2, trnN_GUU2, trnR_ACG2, trnV_GAC2 rps2, rps3, rps4, rps72, rps8, rps11, rps12**2, rps14, rps15, rps16*, rps18, rps192 rpl2*2, rpl14, rpl16*, rpl20, rpl222, rpl232, rpl32, rpl33, rpl36 rpoA, rpoB, rpoC1*, rpoC2 infA psaA, psaB, psaC, psaI, psaJ, ycf3**, ycf4 psbA, psbB, psbC, psbD, psbE, psbF, psbH, psbI, psbJ, psbK, psbL, psbM, psbN, psbT, psbZ petA, petB*, petD*, petG, petL, petN atpA, atpB, atpE, atpF*, atpH, atpI rbcL ndhA*, ndhB*2, ndhC, ndhD, ndhE, ndhF, ndhG, ndhH, ndhI, ndhJ, ndhK matK cemA# accD ccsA clpP** ycf1 ycf22, ycf15#2

2 Two gene copies in IR regions, * With one intron, ** With two introns, # Pseudogene. The triplication of trnI_CAU was found in P. verticillata and P. incompleta, and the duplicate of trnI_CAU was found in P. quadrifolia and P. bashanensis between rpl23 and ycf2

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Fig. 3.12 Multiple Mauve alignment of Paris plastomes

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References

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Fig. 3.13 Sliding window analysis of nucleotide diversity (π) among Paris plastomes

References Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141. https://doi.org/10.1016/j. pbi.2005.01.001 Barrett CF, Baker WJ, Comer JR et al (2016) Plastid genomes reveal support for deep phylogenetic relationships and extensive rate variation among palms and other commelinid monocots. New Phytol 209:855–870. https://doi.org/10.1111/nph.13617 Belaeva VA, Siplivinsky VN (1976) Chromosome numbers and taxonomy of some species of Baikal Flora. Bot Zurn SSSR 61:873–880 Bennetzen JL, Ma JX, Devos K (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127–132. https://doi. org/10.1093/aob/mci008 Bjerketvedt D, Laane MM (1982) Accessory chromosomes in Norwegian populations of Paris quadrifolia L. Cytologia 47:391–398 Brunet J, Von-Oheimb G (1998) Migration of vascular plants to secondary woodlands in southern Sweden. J Ecol 86:429–438. https://doi. org/10.2307/2648468 Camacho JPM (2005) B chromosomes. In: Gregory TR (ed) The evolution of the genome. Elsevier, San Diego, pp 223–285 Camacho JPM, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution. Philos Trans R Soc B 355:163–178. https://doi.org/10. 1098/rstb.2000.0556 Chatterjee A, Ghosh S, Roy SC (1989) A cytological survey of eastern Himalayan plants III. Cell Chromosome Res 12:22–29 Chepinoga VV, Gnutikov AA, Rosbakh SA (2010) IAPT/IOPB chromosome data 9. Taxon 59:1298–1299. https://doi.org/10.12705/ 653.44 Comer JR, Zomlefer WB, Barrett CF et al (2015) Resolving relationships within the palm subfamily Arecoideae (Arecaceae) using plastid sequences derived from next-generation sequencing. Am J Bot 102:888–899. https://doi.org/10.3732/ajb.1500057 Cunninghamia AB, Brinckmann JA, Bi YF, Pei SJ, Schippmann U, Luo P (2018) Paris in the spring: a review of the trade, conservation and opportunities in the shift from wild harvest to cultivation of Paris polyphylla (Trilliaceae). J Ethnopharmacol 222:208–216. https://doi. org/10.1016/j.jep.2018.04.048

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4

Economic Importance

4.1

Medicinal Importance

4.1.1

Overall Information

Paris species are traditionally used as medicinal herbs in China, India, Nepal, and other neighboring countries as well (Cunningham et al. 2018). Paris species are well known in China, where nearly all species having a thick rhizome are used to treat various diseases; for example, the dried rhizomes of Paris chinensis and P. yunnanensis bear the pharmaceutical name “Rhizoma Paridis” (China Pharmacopoeia Commission 2015). The earliest literature on Paris species utilized as herbal medicine dates back to 2000 years ago, during the Chinese Dong-Han Dynasty (25–220 AD) (Li et al. 2015). Rhizoma Paridis (Fig. 4.1) was originally used to treat snake bites and swelling. In the last 50 years, its hemostasis, anti-inflammatory, analgesic, cough suppressant, antipyretic, anti-tumor, immuno-stimulating, anthelmintic, antimicrobial, and protective effects on ethanol- or indomethacin-induced gastric mucosal lesions, and other therapeutic properties became known and were described. In India, Paris species are locally known as “Satwa” and used mainly in both Unani and Ayurvedic medicine (Maity et al. 2004). In the Himalayan regions, rhizomes and aerial organs of Paris species are used to treat burns, injuries, diarrhea, fever, stomachache, gastritis, intestinal wounds, poisoning, skin diseases, snakebites, typhoid, ulcers, and wounds (Farooquee et al. 2004; Maity et al. 2004; Tiwari et al. 2010; Jamir and Lanusunep 2012; Lalsangluaii et al. 2013; Pfoze et al. 2013; Mir et al. 2014; Sharma and Samant 2014). Because of their diverse medicinal properties, Paris species are called the “jack of all trades” in India (Shah et al. 2012). In Nepal, the rhizomes of Paris species are not only used against snakebites, insect bites, pain, fever, intestinal parasites, and external wounds, but also in veterinary medicine for the treatment of diarrhea and dysentery in cattle (Baral and Kurmi 2006; Dutta 2007). In Vietnam, the aerial organs of Paris species are used to treat the flu and fever,

while the rhizome is effective as a hemostatic and analgesic agent, and for treating injuries, fractures, snakebites, and skin diseases (Duc and An 2014). Currently, there are ca. 90 commercial drugs and health products whose raw materials include Rhizoma Paridis (Table 4.1). Among them, the most famous are ‘Yunnan Baiyao’, a patented Chinese medicine, and the ‘Gongxuening Capsule’, a commercial drug develop from the total steroidal saponins of Rzhizoma Paridis. The yearly market value of these pharmaceutical products was estimated at more than 10 billion CNY (ca. 1.6 billion USD) (Huang et al. 2012).

4.1.2

Traditional Uses and Ethnopharmacological Properties

Ethnopharmacological knowledge of medicinal plant species is very useful for their conservation and for discovering novel biological resources (Cox and Balick 1994; Heinrich and Gibbons 2001; Muthu et al. 2006). Unfortunately, medicinal plants and the traditional knowledge of them are rapidly declining in modern society (Cox and Balick 1994; Rai et al. 2000). Despite the great importance of Paris species for the pharmaceutical industry, a systematic global documentation of their ethnopharmacological knowledge still remains unavailable. Based on an extensive literature review and an ethnobotanical survey, both the traditional uses and ethnopharmacological properties of different Paris species are summarized in Table 4.2. This knowledge will help in the exploration and protection of Paris species. A total of 20 species within the genus Paris possess medicinal values (medicinal Paris), in that they are or have been used as traditional medicines in both East Asia (China, India, Myanmar, Nepal, Vietnam) and Europe. For these species, their rhizomes are the part that is most commonly used for the treatment of various diseases. Compared with the use of aerial parts in medicinal preparations, the frequent use of rhizomes would have a destructive impact on the growth of

# Science Press 2021 Y. Ji, A Monograph of Paris (Melanthiaceae), https://doi.org/10.1007/978-981-15-7903-5_4

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4 Economic Importance

potential. Although the commercial breeding of Paris species as ornamentals has yet to begin, they do possess highly desirable gardening traits making them valuable for future development and utilization. Here, six representative species are described to illustrate this potential of Paris species for their ornamental benefits.

4.2.1

Fig. 4.1 Photographs of Rhizoma Paridis (a, b, c) and the processed pieces (d)

these plant populations in nature (Heinrich et al. 1998). Because collecting rhizomes inevitably leads to higher plant mortality, continual over-exploitation of wild populations over time will leave medicinal Paris more prone to extinction. Accordingly, to implement the dual aims of in situ protection and sustainable utilization of wild populations of medicinal Paris, it is imperative that other plant parts (e.g., leaves, stem) serve as alternative sources to the rhizomes. Interestingly, the main chemical components in the stems and leaves of P. yunnanensis are similar to those in its rhizomes; this suggests that the aboveground parts and the rhizomes of medicinal Paris may well harbor similar pharmacological properties; if so, the aerial organs (especially the leaves) may offer an alternative and more sustainable source of active ingredients compared to the rhizomes (Qin et al. 2018). Medicinal Paris are traditionally relied upon for treating approximately 30 diseases, including asthma, colds, cough, fever, flu, diarrhea, gynecological disease, headache, insect bites, mumps, mastitis, rheumatic pain syndrome, pain, pneumonia, pruritus, skin diseases, snakebites, swollen and sore throat, tonsillitis, traumatic hemorrhage, tumors, ulcers, wounds, etc. Of those, analgesic, hemostasis, anti-inflammation, and anti-tumor are the major ethnopharmacological properties ascribed to medicinal Paris. Traditional knowledge of medicinal Paris species can provide insights into the search for natural products with relevant bioactivities. Further, most of these taxa show high levels of similarity in their traditional uses and ethnopharmacological properties, suggesting resource substitutions among medicinal Paris species is likely feasible.

4.2

Horticultural Potential

With a whorl of 4–15 leaves and a solitary flower developing at the stem apex, the distinctive morphology of Paris species is so striking that no gardener can ignore their horticultural

P. cronquistii (Takht.) H. Li

This species is distributed in southwestern China and northern Vietnam. Similar to its congeneric relatives, P. cronquistii has leaf-like sepals, and linear or filiform petals. However, it is unique in having leaves that are abaxially purple or have purple markings (Fig. 4.2). In recent years, P. cronquistii was introduced and cultivated in home gardens by farmers in southwestern China (namely in Yunnan, Sichuan, Guizhou, and Guangxi). Seedling can be produced from seeds and through vegetative propagation. With its substantial shade-tolerance and unique morphology, P. cronquistii has great potential for use as an indoor potted flower plant.

4.2.2

P. delavayi Franch

P. delavayi can be easily distinguished from its congeneric species by its purple and usually reflexed sepals, and dark purple petals (Fig. 4.3). This species is an endemic plant found only in central and southwest China. In recent years, wild populations of P. delavayi have been introduced and cultivated by local farmers in their courtyards and vegetative gardens, for medicinal purposes. Unfortunately, the Paris saponins I, II, VI, and VII contents in the dried rhizomes of P. delavayi are much lower than the quality standard components of the Chinese Pharmacopoeia (China Pharmacopoeia Commission 2015). This restricts its prospects for cultivation as a medicinal plant. Nevertheless, its beautiful flower and distinguished morphology means that P. delavayi could become a promising ornamental plant.

4.2.3

P. lancifolia Hayata

Within the genus Paris, P. lancifolia is distinctive in possessing numerous narrow and slender sessile (or subsessile) leaves (Fig. 4.4). In central and southwestern China, wild populations of P. lancifolia were introduced and cultivated by local famers for medicinal purposes. Due to its beautiful overall appearance as a plant and its distinguished leaf morphology, P. lancifolia is also a promising candidate for flower breeding.

4.2 Horticultural Potential

57

Table 4.1 List of commercial drugs and healthy products use “Rhizoma Paridis” as raw material Drug names “Baibaodan” powder “Baibaodan” liniment “Baibaodan” capsule “Biyan Qingdu” granules “Biyunsha Yigan” granules “Boerning” capsule “Boluohuo Zhongyang” tincture “Caoxian Yigan” capsule “Changchun Hongyao” capsule “Changchun Hongyao” tablet “Chanwu Babugao” plaster “Chonglou Jiedu” tincture “Diedabang” tincture “Fufang Chonglou” tincture “Fufang Chuanbei Zhike” Oral solution “Fufang Shedan Chuanbei” Oral solution “Fufang Xueshangyizhihao” liniment “Fufang Xueshen” capsule “Fufang Yanlian” tablet “Fuzhiqing” ointment “Ganfule” capsule “Ganfule” tablet “Gongxuening” capsule “Gufengning” capsule “Hongwei Sheyao” tablet “Houshu Kouhan” tablet “Jianghuang Xiaocuo” liniment “Jiedu Tonglin” pill “Jingu Tengtong” tincture “Jiuwei Shuangjie” Oral solution “Kangbingdu” granules “Keyangmin” granules “Lanhua Kening” tablet “Loulian” capsule “Lujin Zhuanggu” tincture “Niaoqingshu” granules “Panlongqi” tablet “Panlongqi” tincture “Qinggan Baidu” pill “Qingre Zhike” granules “Qiying Neixiao” plaster “Qizhen” capsule “Quyu Yiwei” capsule “Quyu Yiwei” tablet “Reduqing” tablet “Rendong Ganmao” granules “Ruanjian” Oral solution “Rupiqing” tablet “Sanjie Zhitong” plaster

Therapeutical usages Arthralgia, external wounds, gynecological disease, stomachache Rheumatic pain syndrome, wounds Arthralgia, external wounds, gynecological disease, stomachache Chronic inflammation of nasopharynx, swollen and sore throat Hepatitis B Tumors Skin diseases, insect bites Diarrhea, hepatitis B, hypochondria External wounds External wounds Pain caused Herpes zoster, skin pruritus, insect bites, mumps External wounds, swelling and pain. External wounds, swelling and pain, mastitis, mumps Asthma, bronchitis, cough, cold Asthma, bronchitis, cough, cold Arthralgia, external wounds Prostatic hyperplasia Bronchitis, cold, cough, laryngitis, tonsillitis Hemorrhoids, hemorrhage, pruritus, skin disease, swelling and pain Liver cancer Liver cancer Gynecological disease Rheumatic pain syndrome Insect and snake bites Sore and swollen throat Rheumatic pain syndrome Urethritis Rheumatic pain syndrome Cold, cough, fever, headache, sore, and swollen throat Flu Dermatitis, eczema, pruritus, urticaria Bronchitis, cough Primary hepatocellular carcinoma II Rheumatic pain syndrome Gonorrhea, prostatitis Rheumatic pain syndrome, wounds Rheumatic pain syndrome, wounds Chronic hepatitis Bronchitis, cough, fever, sore and swollen throat External wounds, swelling and pain Breast tumor, gastric cancer, lung cancer Gastritis Gastritis Flu, laryngitis, mumps, tonsillitis Fever, flu, sore and swollen throat Liver cancer Hyperplasia of mammary gland Mastalgia (continued)

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4 Economic Importance

Table 4.1 (continued) Drug names “Sanqi Xueshangning” capsule “Sanqi Xueshangning” powder “Shangyi” aerosol “Sanmei Ruzuoqing” capsule “Shaolin Dieda Zhitong” plaster “Shenbei Zhike” granules “Shenbo Shuyin” solution “Shennong Zhentong” plaster “Tongshu” capsule “Tongxuekang” capsule “Waiyong Wudi” plaster “Weisheng” powder “Xian’er Tuire” granules “Xiao’er Qingre” Ling tablet “Xiao’er Tuire” mixture “Xiao’er Tuire” granules “Xiao’er Tuire” Oral solution “Xiaozheng Fuzheng” Oral solution “Xiaozhijie” ointment “Xiongdan Dieda” plaster “Xuanqi Tongbi” capsule “Xuedan Weichang” pill “Xueshangyizhihao Suxiozhitong” liniment “Yili Zhitong” pill “Yinbing Xiaocuo” tincture “Yinlian Qinggan” mixture “Yinlian Qinggan” granules “Yuanqi Gutong” tincture “Yunnan Baiyao” capsule “Yunnan Baiyao” tablet “Yunnan Hongyao” powder “Zhanjiang Sheyao” tablet “Zhongtong” liniment “Zhongtong” gel “Zhongtong” aerosol

4.2.4

Therapeutical usages Gynecological diseases, hemoptysis External wounds, gastrointestinal bleeding, swelling and pain External wounds, burn Mammary glands External wound, swelling and pain Bronchitis, cough Gynecological diseases External wounds, rheumatic arthralgia External wounds, rheumatic pain syndrome External wounds, gastrointestinal bleeding, inflammation External wounds, rheumatic pain syndrome Gastroenteritis, fever, scabies Cold, fever, mumps, sore and swollen throat Asthma, cold, fever, sore swollen throat Cold, conjunctival hyperemia, fever, headache, sore throat, upper respiratory infection Cold, conjunctival hyperemia, fever, headache, sore throat, upper respiratory infection Cold, conjunctival hyperemia, fever, headache, sore throat, upper respiratory infection Lung cancer Hemorrhoid, swelling and bleeding, skin diseases External wounds, swelling and pain Rheumatic pain syndrome Gastrorrhagia, peptic ulcer Arthralgia, external wounds Analgesic Acne Viral hepatitis Viral hepatitis Osteoarthritis, rheumatic pain syndrome Bronchiectasis, external wounds, hematemesis, hemoptysis, hematochezia, hemorrhoids, metrorrhagia, hemorrhage, skin infections, swelling and pain, ulcer bleeding Bronchiectasis, external wounds, hematemesis, hemoptysis, hematochezia, hemorrhoids, metrorrhagia, hemorrhage, skin infections, swelling and pain, ulcer bleeding Bronchiectasis, external wounds, hematemesis, hemoptysis, hematochezia, hemorrhoids, metrorrhagia, hemorrhage, skin infections, swelling and pain, ulcer bleeding Insect and snake bites Wounds, rheumatic pain syndrome Wounds, rheumatic pain syndrome Wounds, rheumatic pain syndrome

P. luquanensis H. Li

P. luquanensis is a Chinese endemic plant narrowly distributed in northern Yunnan and southwestern Sichuan. It is a unique species because of its dwarf plant size, and leaf color variegation and chimerism (Fig. 4.5), all of which are key decorative traits sought after in ornamental plants. Since P. luquanensis individuals are collected from wild and sold as garden plants by local farmers, its natural populations have severely deteriorated in recent years. For effective protection and management of germplasm resources of P. luquanensis,

both in situ and ex situ conservation strategies and action are urgently needed.

4.2.5

P. marmorata Stearn

Besides P. luquanensis, P. marmorata is another species in the Paris that possesses color variegation and chimerism in its leaves. With a relatively higher plant height and oblong or lanceolate leaves, P. marmorata (Fig. 4.6) is easily distinguished from P. luquanensis. Occurring in southwestern

4.2 Horticultural Potential

59

Table 4.2 Traditional uses and ethnopharmacological properties of Paris species Species P. quadrifolia

Part used Whole plant

Medicinal uses Headache, skin disease, wounds

P. verticillata

Rhizome, whole plant

Traumatic hemorrhage, rheumatic pain syndrome, snake bites, swollen and sore throat, ulcer, wounds (China) Asthma, cough (Korea) Diarrhea, fever, traumatic hemorrhage, injury, rheumatic pain syndrome, swollen and sore throat, tonsillitis (China) Asthma, cough, diarrhea, traumatic hemorrhage, rheumatic pain syndrome, snake bites, swollen and sore throat, tonsillitis, ulcer, wounds (China) Diarrhea, traumatic hemorrhage, rheumatic pain syndrome, snake bites, swollen and sore throat, ulcer, wounds Traumatic hemorrhage, snake biting, stomachache, ulcer, wounds (China)

P. thibetica

Rhizome Rhizhome, aerial organs Rhizome

P. vaniotii

Rhizome

P. forrestii

Rhizome

P. Bashanensis

Rhizome, aerial organs Rhizome P. dunniana

Rhizome

P. vietnamensis

Rhizome

P. Xichouensis

Rhizome Rhizome

P. chinensis

Rhizome

P. Qiliangiana P. fargesii

Rhizome Rhizome Rhizome

P. cronquistii

Rhizome

P. delavayi

Rhizome

P. yunnanensis

Rhizome

P. Luquanensis

Rhizome

P. lancifolia

Rhizome

Diarrhea, traumatic hemorrhage, fever, stomachache, gastritis, skin diseases, snake bites, typhoid, ulcers, wounds (India) Fever, traumatic hemorrhage, insect bites, intestinal parasites, snake bites, pain, external wounds (Nepal) Fever, cold, flue, traumatic hemorrhage, snake bites, wounds (China) Traumatic hemorrhage, rheumatic pain syndrome, snake bites, stomachache, swollen and sore throat, ulcer, wounds (China) Traumatic hemorrhage, snake bites, wounds (Vietnam) Traumatic hemorrhage, rheumatic pain syndrome, snake bites, stomachache, swollen and sore throat, ulcer, wounds (China) Asthma, cough, diarrhea, headache, traumatic hemorrhage, gynecological disease, mastitis, rheumatic pain syndrome, pneumonia, pruritus, snake bites, swollen and sore throat, tonsillitis, tumor, ulcer, wounds (China) Traumatic hemorrhage, snake bites, wounds (Vietnam) Traumatic hemorrhage, snake bites, ulcers, wounds Traumatic hemorrhage, rheumatic pain syndrome, snake bites, swollen and sore throat, ulcer, wounds (China) Traumatic hemorrhage, rheumatic pain syndrome, snake biting, swollen and sore throat, ulcer, wounds (China) Asthma, cough, diarrhea, traumatic hemorrhage, ulcer, wounds Cough, diarrhea, gynecological disease, mastitis, headache, traumatic hemorrhage, mumps, rheumatic pain syndrome, pneumonia, skin disease, snake bites, swollen and sore throat, tonsillitis, tumor, ulcer, wounds (China) Traumatic hemorrhage, mumps, rheumatic pain syndrome, stomachache, ulcer, wounds (China) Traumatic hemorrhage, gynecological disease, mastitis, rheumatic pain syndrome, snake biting, swollen and sore throat, ulcer, wounds (China)

Data resources Allen and Hatfield 2004; Jacquemyn et al. 2005, 2006; Guarino et al. 2008; Stefanowicz-Hajduk et al. 2011; Sõukand and Kalle 2011 Lu 1989; Zhu 1989; Li et al. 1995; State Administration of Traditional Chinese Medicine, Editorial Board of Chinese Materia Medica 1999 Kim et al. 2011 Fang et al. 2007

Dao et al. 2003; Zhu 2010

This study

Health Bureau of Nujiang Lisu Autonomous Prefecture, Yunnan Province. 1991; Dao et al. 2003; Zhu 2010 Farooquee et al. 2004; Maity et al. 2004; Tiwari et al. 2010; Jamir et al., 2012; Mir et al. 2014; Sharma and Samant 2014 Baral and Kurmi 2006; Dutta 2007 This study Long and Li 2004; Zhu 2007; Li 2008; Lee et al. 2008;

Duc and An 2014 This study

Huang 1980; Fang 1990; Guo et al. 1990; Li 1990; Yu 1997; Li 1998; Qi and Luo 2000; Yang et al. 2001; Pan et al. 2003; Zhang and Zhong 2005; Huang et al. 2006; Zhu 2007; Long and Yuan 2009; Dai 2009; Zhu et al. 2012 Duc and An 2014 This study Zhu 2009; Lin et al. 2012

This study

This study Lan 1975; Huang 1980; Su and Wei 1983; Li and He 1990; Zhu 1991, 2009; He and Huang 1999; Jia 2005; He and Ma 2006

This study Li and He 1990; Qiu and Du 2005; Yin and Zhang 2010, 2011; Yin et al. 2014 (continued)

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4 Economic Importance

Table 4.2 (continued) P. marmorata

Rhizome

P. polyphylla

Rhizome

Rhizome, aerial organs Rhizome P. mairei

Rhizome

Asthma, cough, traumatic hemorrhage, stomachache, ulcer, wounds (China) Asthma, cough, diarrhea, traumatic hemorrhage, mastitis, mumps, rheumatic pain syndrome, snake bites, swollen and sore throat, tonsillitis, ulcer, wounds (China) Diarrhea, fever, stomachache, gastritis, skin diseases, snake bites, traumatic hemorrhage, typhoid, ulcers, wounds (India) Fever, insect bites, intestinal parasites, snake bites, traumatic hemorrhage, pains, wounds (Nepal) Traumatic hemorrhage, stomachache, ulcer, wounds (China)

Zhu 2003 This study

Farooquee et al. 2004; Maity et al. 2004; Tiwari et al. 2010; Jamir and Lanusunep 2012; Lalsangluaii et al. 2013; Pfoze et al. 2013; Mir et al. 2014; Sharma and Samant 2014 Baral and Kurmi 2006; Dutta 2007 This study

Fig. 4.2 Unique morphology of Paris cronquistii showing its ornamental potentials

China and Himalayas, P. marmorata is commonly harvested as a medicinal herb by indigenous people. This has led to severe decrease in the sizes of its wild populations in recent years. Great attention should be paid to conserving the germplasm of this important horticultural species.

4.2.6

P. yunnanensis Franch

P. yunnanensis is one of the botanical origins of Rhizoma Paridis, a famous Chinese medicinal material (China Pharmacopoeia Commission 2015). Since the 2000s, this species has been massively cultivated in China to supply raw materials for the pharmaceutical industry. P. yunnanensis can produce multiple aerial stems from the same rhizome, and its flowers are unique in having distally widened petals (Fig. 4.7). Because of its beautiful plant appearance and distinguished morphology, P. yunnanensis is fast becoming

Fig. 4.3 Unique morphology of Paris delavayi showing its ornamental potentials

an eye-catching plant. From the perspective of comprehensive utilization of plant resources, this species can be cultivated for both medicinal and ornamental purposes.

4.3 Phytochemistry Fig. 4.4 Unique morphology of Paris lancifolia showing its ornamental potentials

Fig. 4.5 Unique morphology of Paris luquanensis showing its ornamental potentials

Fig. 4.6 Unique morphology of Paris marmorata showing its ornamental potentials

Fig. 4.7 Unique morphology of Paris yunnanensis showing its ornamental potentials

4.3

Phytochemistry

Kromer (1901) first conducted an investigation on the chemical compounds of Paris species and obtained sucrose from the dried and powdered fruits of P. quadrifolia.

61

Subsequently, Dutt et al. (1938) obtained two glycosides, paridin and paristyphnin, from the rhizomes of P. polyphylla collected from Nepal. However, the chemical structures of these compounds were not determined due to the technological and scientific limitations in the early 1900s. Huang and Zhou (1962) isolated diosgenin from the rhizomes of P. yunnanensis. Huang (1965) reported that diosgenin was found in six Paris species collected from Yunnan Province, China and only three of them contained pennogenin. Furthermore, he isolated dioscin from P. cronquistii. Singh et al. (1966) detected diosgenin monoglucoside from P. polyphylla. Subsequently, three diosgenin glycosides and one pregnane glycoside were isolated from the dried rhizomes of P. polyphylla and their structures were elucidated by NMR spectroscopy and mass spectrometry (Nohara et al. 1973). In 1975, pennogenin rhamnosyl-chacotrioside was obtained from the dried aerial organs of P. tetraphylla. Several years later, Miyamura et al. (1982) obtained two new furostanol glycosides and two new pennogenin glycosides from P. polyphylla. From 1981 to 1995, a series of steroidal glycosides were identified from the rhizomes of P. yunnanensis, P. axialis (syn. P. vaniotii), and P. luquanensis (Chen and Zhou 1981, 1984, 1987; Chen et al. 1983a, b). To realize the comprehensive utilization of resources, the chemical constituents of the seeds and aerial organs of P. yunnanensis were investigated and a series of flavonoid glycosides and steroidal saponins were identified (Chen et al. 1990a, b; Chen and Zhou 1992; Chen et al. 1995a, b). Recently, Qin et al. (2012, 2013, 2016, 2018) carried out a detailed study on the chemical constituents and bioactivity of the stems and leaves of P. yunnanensis and obtained 53 compounds including 20 new glycosides. The results showed that the main chemical components in the stems and leaves were similar to those in the rhizomes; however, the stems and leaves contained nuatigenin-type saponins, which were not found in rhizomes. In recent years, some researchers have used HPLC and UPLC-MSn in positive and negative-ion modes to rapidly identify the chemical compounds of Paris species. According to the characteristic fragmentation patterns of known steroidal saponins (i.e., Paris saponins I, II, H, and VII, gracillin, and dioscin) isolated from P. polyphylla, 23 constituents (including five new compounds) were structurally characterized on the basis of their retention time and ESI analyses (Man et al. 2009). Additionally, a metabolomicsbased UPLC/Q-TOF MS method was developed by Kang et al. (2017), who detected 146 metabolites from P. yunnanensis, including 42 potential novel compounds. For more than a hundred years, over 200 compounds have been isolated and identified from Paris species, including steroidal saponins, triterpenoid saponins, flavonoids, flavonoid glycosides, β-ecdysone, sitosterol, pyrrolizidine alkaloids, fatty acid esters, and polysaccharides. Of these

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4 Economic Importance

Fig. 4.8 Representative steroidal saponins from Paris species

Fig. 4.9 Representative saponins isolated from Paris species

compounds, steroidal saponins, which mainly belong to four skeleton types: spirostane (diosgenin, pennogenin, and nuatigenin), furostane, cholestane, and pregnane saponins (Fig. 4.8), are the predominant components in Paris species.

4.3.1

Steroidal Saponins

Spirostane-type saponins are the most common and representative steroidal glycosides in Paris species, which consist of a hexacyclic A-F ring system. All spirostane glycosides possess a double bond between C-5 and C-6 and a β-configuration oligosaccharide group mainly linked to the aglycone at C-3. The sugars primarily include D-glucose, L-rhamnose, L-arabinose, D-xylose, and D-apiose. Their aglycones are mainly classified as diosgenin and pennogenin; the latter is a 17α-hydroxylated derivate of diosgenin. Ten spirostane-type saponins, named paris saponins I, II, V, VI, VII, and H, dioscin, pennogenin 3-O-β-chacotrioside, gracillin, and 17-hydroxygracillin, are the main compounds

within Paris species. Among them, paris saponins I, II, and V, dioscin, and gracillin belong to diosgenin saponins while the rest are pennogenin saponins. According to the Chinese Pharmacopoeia (China Pharmacopoeia Commission 2015), paris saponins I, II, VI, and VII (Fig. 4.9) are officialized as the quality control components of medicinal Paris species; the minimum total content of the four saponins must be 0.6%. Polyhydroxylated saponin is a subtype of spirostane saponin which has the hydroxyls linked at C-1, C-3, C-5, C-6, C-7, C-17, C-21, C-23, and C-24. 24-Hydroxypennogenin glycosides were found in P. axialis (syn. P. vaniotii) by Chen and Zhou (1984, 1987). Three polyhydroxylated steroidal glycosides, parisyunnanosides G
I, isolated from P. yunnanensis were reported (Kang et al. 2012). Two highly oxygenated spirostanol saponins, paristenosides A and B, were obtained from the rhizomes of P. polyphylla var. stenophylla (syn. P. lancifolia) (Jin et al. 2016). Nuatigenin-type steroidal saponins isolated from the aboveground organs of Paris species are thought to be

4.3 Phytochemistry

derivatives of spirostanol saponins (Wang et al. 2007). Chen et al. (1995a) first isolated one nuatigenin-type saponin from the aerial organs of P. yunnanensis. Qin et al. (2016) reported 11 nuatigenin-type saponins from the stems and leaves of P. yunnanensis. Furostanol saponins, which have a β-glucosyl unit at the C-26 position of the aglycone moiety, are also an important type of steroidal saponins in Paris species; furostanol saponins are easily transformed into spirostanol saponins by β-glucosidase (Inoue and Ebizuka, 1996). Therefore, furostanol saponins are generally considered to be precursors of spirostane saponins. In 1980, Singh and Takur first isolated two new furostanol saponins from P. polyphylla. Furostanol saponins with 17-hydroxy and 22-OMe or a double bond between C-20 and C-22 (such as Pseudoproto-Pb) were isolated from P. polyphylla and P. yunnanensis (Singh et al. 1982a, 1982b; Xu et al. 2007; Zhao et al. 2009; Qin et al. 2012, 2016). From the biosynthetic perspective, the cholestane-type steroidal saponins are steroidal saponin-like glycosides (Bai et al. 2014). Seven cholestane saponins with the aglycone of kryptogenin, dehydrokryptogenin, E-ring aromatized sapogenin, and (20R, 25R)-cholestan-5-en-3β, 16β, 20, 26-tetraol-22-one were isolated from P. yunnanensis, P. chinensis, P. polyphylla var. pseudothibetica (syn. P. delavayi), and P. verticillata. Polyhydroxylated cholestane saponins may be an important precursor of aromatized cholestane, furostanol, and spirostane saponins (Huang et al. 2005; Zhao et al. 2007; Xiao et al. 2009; Sun et al. 2014; Qin et al. 2016). Pregnanes are C21 steroidal compounds found as either monomers or glycosides. Small amounts of pregnane saponins have been obtained from Paris species and might be degraded components of the major furostanol and spirostanol saponins. Pregna-5, 16-dien-3β-ol-20-one 3-O-β-chacotrioside was the first pregnane saponin isolated from Paris species (Nohara et al. 1973). To date, nine pregnane glycosides have been isolated from Paris (Nohara et al. 1973; Chen et al. 1990b; Huang et al. 2007; Kang et al. 2012; Qin et al. 2012, 2013; Liu et al. 2015).

4.3.2

Phytoecdysones

Phytoecdysones may be the key precursors in the biosynthetic pathway of steroidal saponins (Wang et al. 2017). Over the past several decades, five phytoecdysones have been found in different Paris species (Fig. 4.10). Nohara et al. (1981) detected ecdysterones from P. quadrifolia. Singh et al. (1982) then reported a novel phytoecdysone, paristerone, from the tubers of P. polyphylla. β-Ecdysone has been isolated and determined from P. polyphylla and P. fargesii (Huang et al. 2010; Zhan et al. 2011). Besides,

63

Fig. 4.10 Representative phytoecdysones isolated from Paris species

5-hydroxyecdysterone and 20-hydroxyecdysone have been found in P. quadrifolia (Jenett-Siems et al. 2012).

4.3.3

Phytosterols

Phytosterols, known as plant sterols, are cholesterol-like molecules found in plants. Eight phytosterols were isolated from Paris species, which are determined as daucosterol, stigmasterol, β-sitosterol, and their derivatives. Two new phytosterol glycosides, pariposides E and F, were isolated and identified by Wu et al. (2012) from the rhizomes of P. yunnanensis.

4.3.4

Flavonoids

Flavonoids and their glycosides are the second large category of secondary metabolites in different Paris species. At present, approximately 22 flavonoids and their glycosides have been isolated from this genus (Fig. 4.11). The skeletal structures are classified into flavonols, biflavones, and chalcones and the glycosylation sites are mostly at C-3 in flavonols. Chen et al. (1995a) first reported two kaempferol glycosides from the aerial organs of P. yunnanensis. Later, Wang et al. (2007) isolated two known flavonoid glycosides from the rhizome of P. yunnanensis and their structures were elucidated by spectroscopic methods.

4.3.5

Triterpenoid Saponins

Triterpenoids and their saponins are rare in the genus Paris. Wu et al. (2013) isolated six novel oleanane-type triterpenoid saponins (paritrisides A–F) and nine known triterpenoid saponins from the rhizomes of P. yunnanensis (Fig. 4.12). Subsequently, the same research group reported two known oleanane-type triterpenoid saponins from this species (Wu et al. 2017). It is notable that no other study has isolated triterpenoid saponins from P. yunnanensis; furthermore, no triterpenoid saponin has been identified in other congeneric species. Further investigation is needed to examine whether Paris species contain triterpenoid saponins.

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4 Economic Importance

Fig. 4.11 Representative flavonoids isolated from Paris species

Fig. 4.12 Representative chemical skeletal structures of triterpenoid saponins isolated from Paris species

4.3.6

Others

Previous research on the chemical composition of Paris species has primarily focused on steroidal saponins. However, Paris also contains a small number of phenylpropanoid glycosides, fatty acid esters, pyrrolizidine alkaloids, and polysaccharides. From the rhizomes of P. yunnanensis, two phenylpropanoid glycosides (parispolyside F and 2-feruloylO-α-D-glucopyranoyl-(10 ! 2)-3,6-O-feruloyl-β-Dfructofuranoside) and a ramification of the phenolic glycoside (parispolyside G) were obtained (Wang et al. 2007; Yan et al. 2008). Kim et al. (2010) isolated three new pyrrolizidine alkaloids (verticillatins A–C), as well as seven known pyrrolizidine alkaloids from the roots of P. verticillata.

4.4

Pharmaceutical Prospects

The main medicinally active ingredients of Paris are steroidal saponins. Modern pharmacological researches demonstrate that these saponins possess wide biological activities, such as anti-tumor, hemostatic, uterine contractile agonistic, antibacterial, antiviral, immune regulation, anti-oxidation, antimyocardial ischemia, etc.

4.4.1

Anti-Tumor

In recent years, substantial evidence has shown that the ethanol (EtOH), water (H2O), and methanol (MeOH) extracts of P. polyphylla possess marked growth-inhibitory effect on

tumors, including breast cancer, bladder cancer, prostate cancer, lung cancer, and ovarian cancer. Xie et al. (2017) found that saponins isolated from P. polyphylla exhibited anti-tumor activity against breast cancer cell lines (MCF-7 and MDA-MB-231) and found that paris saponin-induced autophagy promotes breast cancer cell apoptosis via the Akt/mTOR signaling pathway. Sun et al. (2007) showed that the ethanol extract had a more powerful inhibitory effect than the aqueous extract on human cell lines, including human liver carcinoma cell lines (HepG-2 and SMMC7721), human gastric cancer cell line (BGC-823), human colon adenocarcinoma cell lines (LoVo and SW-116), and esophagus adenocarcinoma cell line (CaEs-17). The ethanol extract of P. polyphylla also could inhibit the growth of prostate cancer and induce apoptosis of prostate cancer cells in vitro and in vivo (Zhang et al. 2018). Wen et al. (2012) showed that paris saponin H had a remarkable cytotoxic effect on A549 cells with an IC50 value of 1.53 μg/mL. Li et al. (2017) found that paris saponin I induced mitophagic and apoptotic cell death in human breast cancer cells by increasing mitochondrial PINK1 levels. Other research showed that paris saponin II inhibited colorectal carcinogenesis by regulating mitochondrial fission and the NF-κB pathway (Chen et al. 2019).

4.4.2

Hemostatic Activity

Exploring the biological activities of the total steroidal saponins extracted from the rhizomes of P. yunnanensis, Fu et al. (2008) showed that the pennogenin saponins are primarily responsible for hemostatic activity. Their synergistic actions on platelet aggregation were observed with pennogenin glycosides and with other known platelet agonists, suggesting that these glycosides are platelet agonists. Aggregation in response to the pennogenin glycosides involved the activation of αIIbβ3, which could be inhibited by cAMP; this was dependent upon extracellular calcium, secreted ADP, and thromboxane synthesis, and was mediated by phosphatidylinositol-3-kinase. These results

References

suggested that pennogenin saponins from Paris species represent a new type of platelet agonist. Further research revealed that paris saponin VII (also named saponin Tg, a main pennogenin saponin in Paris species) induced platelet activation depends on dense granule secretion of ADP, which in turn activates the P2Y1 and P2Y12 receptor signaling pathways (Cong et al. 2012). The total saponins extracted from the rhizomes and aboveground organs of P. yunnanensis were evaluated for their in vitro hemostatic properties using rabbit blood (Qin et al. 2018). The results revealed that total steroidal saponins extracted from either rhizomes or aboveground organs of P. yunnanensis displayed similar maximal platelet aggregation rates of 45% and 43% at a concentration of 1.5 mg/mL, respectively. This suggested that the aerial organs can be an alternative and more sustainable source of active ingredients related to hemostatic activity compared to the rhizomes (Qin et al. 2018).

4.4.3

Uterine Contractile Agonistic Activity

Guo et al. (2008) reported that the total steroidal saponins of P. yunnanensis dose-dependently induced phasic myometrial contractions in vitro. Through bioassay-guided separation, the study found that total spirostanol saponins exhibited contractile activity in myometrium and paris saponin H was identified as the active ingredient. Furthermore, the contractile response of rat myometrium to paris saponin H was significantly enhanced with advancing pregnancy. A further study indicated that some spirostanol glycosides may represent a new type of contractile agonist for the uterus and their synergism may be responsible for the therapeutic effect of P. polyphylla on abnormal uterine bleeding (Yu et al. 2010).

65

et al. (2006), antifungal activity of C-27 steroidal saponins was associated with their aglycone moieties and the number of monosaccharide units in their sugar chains. The saponins with four or five monosaccharide units exhibited significant activity against Cryptococcus neoformans and Aspergillus fumigatus, which is comparable to the positive control of amphotericin B. In addition, the antifungal potency of these compounds was not associated with cytotoxicity to mammalian cells. This suggests that the C-27 steroidal saponins may be potential antifungal targets for further preclinical studies (Yang et al. 2006).

4.4.5

Other Activities

In addition to the above bioactivities, Rhizoma Paridis also provides the benefits of immune regulation, anti-fibrosis, and anti-cirrhosis (Zhang et al. 2007; Man et al. 2014). Wang et al. (2010) reported that both the methanol extract and pure compounds (paris saponin I and dioscin) from the rhizomes of P. polyphylla showed a promising anthelmintic activity against Dactylogyrus intermedius. Four spirostanal saponins, dioscin, paris saponins I, II, and H, showed strongly protective effects on ethanol- or indomethacin-induced gastric mucosal lesions. Wang et al. (2017) found an inhibitory effect of the Rhizoma Paridis total saponins (RPS) and the main monomer compounds (paris saponins I, II, VI, and H) on gastric emptying and gastrointestinal motility in vitro and in vivo. The inhibition of gastric emptying and contractions of the antral circular strip by RPS predominantly involves muscarinic receptors.

References 4.4.4

Antimicrobial

Pennogenin saponins have been reported to show antifungal activity (Deng et al. 2008). For example, Paris saponin V, Paris saponin VI, and pennogenin 3-O-β-chacotrioside exhibited significant antifungal effects against Candida albicans (Chen et al. 2016). Qin et al. (2018) reported that the total steroid saponins of the rhizomes and the total steroid saponins of the stems and leaves of P. yunnanensis showed antifungal activity against Aspergillus fumigatus, Candida albicans (5314 and Y0109), and Candida parapsilosis (2019). The main active ingredients were paris saponins I, II, V, VI, and VII, dioscin, and chonglouoside SL-5. Chonglouoside SL-6, a saponin with the sapogenin of 27-hydroxyruscogenin glycoside bearing 1,27-di-O-sugar units isolated from the stems and leaves of P. yunnanensis, showed good anti-bacterial activity against Propionibacterium acnes with an MIC value of 3.9 μg/mL (Qin et al. 2012). According to the research results by Yang

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5

Phylogeny, Classification, Biogeography, and Evolution

5.1

Ancient and Recent Hybridization

Phylogenetic reconstruction based on limited sequence variations and taxon sampling always result in significant phylogenetic errors, particularly in recently diverged and rapidly radiated lineages (Rieseberg and Soltis 1991; Rokas and Carroll 2005; Whitfield and Lockhart 2007; Philippe et al. 2011; Sun et al. 2015). Recently, the next-generation sequencing technology which is capable of generating orders of magnitude more sequence data than Sanger sequencing has been increasingly used for resolution of perplexing problems in plant phylogenetics (Jansen et al. 2007; Moore et al. 2007; Parks et al. 2009; Philippe et al. 2009; Moore et al. 2010; Zhou et al. 2012; Barrett et al. 2014; Ma et al. 2014; Stull et al. 2015; Attigala et al. 2016; Zhang et al. 2017; Carlsen et al. 2018; Mckain et al. 2018; Lin et al. 2019). To reconstruct robust phylogeny in Paris, nuclear ribosomal DNA (nrDNA) and complete plastome sequences were yielded and analyzed for all currently recognized Paris species (see Chap. 6). The phylogeny satisfactorily resolved the relationships among Paris species, further confirming that phylogenetic analyses based on a larger number of sequence variations can significantly improve the phylogenetic resolution at low taxonomic levels (Parks et al. 2009; UribeConvers et al. 2017; Vargas et al. 2017; Ma et al. 2018; Lin et al. 2019). Phylogenetic analyses of whole plastome DNA sequences (Fig. 5.1) recovered five well-supported clades within Melanthiaceae, which corresponded to the five tribes (Melanthieae, Chionographideae, Heloniadeae, Xerophylleae, and Parideae) as previously recognized by Zomlefer et al. (2001). The inter-tribal relationships are consistent with previously recovered in previous studies (Zomlefer et al. 2001, 2006; Kim et al. 2013, 2016, 2019; Huang et al. 2016; Ji et al. 2019; Yang et al. 2019), but received relatively higher support values. Within the tribe Parideae, the monophyly of Paris and Trillium as well as their sister relationship were robustly supported. In Paris,

five clades corresponding to the five sections circumscribed by Ji (2006) were recovered with strong branch support; along the backbone of the phylogenetic tree, the successive divergence of the Paris sect. Paris, P. sect. Kinugasa, P. sect. Thibeticae, P. sect. Axiparis, and P. sect. Euthyra was fully supported. Similar to previous studies (Ji et al. 2006, 2019), significant cytonuclear discordance was detected in Paris: the nuclear phylogeny failed to recovered Paris, together with two sections within the genus (P. sect. Axiparis and Euthyra) as monophyletic (Fig. 5.2). The cytonuclear incongruence detected in Paris may have been caused by ancient hybridization and recent introgression between extant species (Ji et al. 2019). By comparison, the plastid phylogeny of Paris is more congruent with morphological evidence, suggesting nuclear introgression without “chloroplast capture” (Rieseberg and Soltis 1991; Soltis and Kuzoff 1995; Soltis et al. 1996; Wendel and Doyle 1998; Wiens 1998; Philippe et al. 2005; Quicke et al. 2007; Renoult et al. 2009; Xiang et al. 2013; Bruun-Lund et al. 2017; Folk et al. 2017; Lin et al. 2019) is most likely responsible for the cytonuclear discordance in Paris phylogeny (Arnold et al. 1991; Rieseberg and Wendel 1993; Setoguchi and Watanabe 2000; Seehausen 2004; Folk et al. 2017). Therefore, the non-monophyly of Paris in nuclear tree may have resulted from a past outcross between P. sect. Paris and Trillium after P. sect. Paris diverged from the rest of the genus; this hybridization event most possibly triggered the occurrence of P. japonica (Ji et al. 2019), a putative allo-octaploid between Paris and Trillium (Haga 1937). The non-monophyly of P. sect. Axiparis and P. sect. Euthyra in nuclear phylogeny can also be attributed to past hybridization. The sister relationship between the clade consisting of P. luquanensis, P. mairei, P. marmorata, and P. polyphylla (P. sect. Euthyra) and the clade of P. forrestii (sect. Axiparis) suggest that P. forrestii likely originated from the hybridization between the ancestors of sect. Axiparis and the P. luquanensis, P. mairei, P. marmorata, and P. polyphylla clade. Likewise, the well-supported sister

# Science Press 2021 Y. Ji, A Monograph of Paris (Melanthiaceae), https://doi.org/10.1007/978-981-15-7903-5_5

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Fig. 5.1 Phylogenetic tree generated by the maximum likelihood (ML) and Bayesian inference analyses of complete plastome DNA sequences. The ML bootstrap percentages and BI posterior probabilities are showed above the branches

Fig. 5.2 Conflicting tree topologies between nuclear ribosomal DNA (left) and plastome (right) phylogenies. The ML bootstrap percentages and BI posterior probabilities are showed above the branches

5.1 Ancient and Recent Hybridization 71

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relationship between P. vaniotii and the P. caobangensis, P. chinensis, P. cronquistii, P. delavayi, P. dunniana, P. fargesii, P. qiliangiana, P. vietnamensis, and P. xichouensis clade implies that hybridization could have occurred between their ancestors. Similar to P. japonica, P. forrestii and P. vaniotii may have been derived from ancient hybridization (Ji et al. 2019). The universal discordance among species of P. sect. Euthyra in the shallow branches of nuclear and plastid trees suggests that recent (or extant) hybridization between sympatric species of this section is likely if their pollination mechanisms are compatible (Ji et al. 2006, 2019). Based on their distinct positions in the plastid and nuclear tree topologies, it is reasonable to propose that hybridization or introgression may occur between species in the following pairs: P. caobangensis and P. fargesii; P. lancifolia and P. yanchii; P. luquanensis and P. yunnanensis; P. fargesii and P. delavayi/P. croquistii; and P. yanchii and P. yunnanensis. Moreover, P. qiliangiana can be a hybrid between P. chinensis and P. delavayi/P. croquistii. The morphological intermediates found in the above species pairs justify this hypothesis.

5.2

Generic Circumscription

One of the objectives of the monographic study of Paris is to resolve the long-standing controversies in the taxonomic delimitation of the genus. Historically, it was recognized as one genus (Franchet 1888a, b; Hara 1969; Li 1998; Ji 2006) or separated into three genera (Takhtajan 1983; Farmer and Schilling). A plant lineage should not be recognized unless it is a well-supported monophyletic, and possesses significant morphological distinctiveness (Backlund and Bremer 1998). The plastome phylogenies strongly support Paris as a monophyletic group, and sister to Trillium. The sister relationship between Paris and Trillium can be supported by morphological and cytological evidence. These two genera share the morphological synapomorphies of a whorl of leaves, a solitary flower borne at the stem apex, and have the same base chromosome number (x ¼ 5), as well as the molecular synapomorphy of the pseudogenization of the plastid cemA gene (Ji et al. 2006, 2019; Yang et al. 2019). However, Paris is morphologically distinct in its >3-merous flowers and leaves

by compared with the 3-merous condition of Trillium. Moreover, in all species of Paris, pollen is oblate-spheroidal (versus spherical in Trillium) (see Chap. 2). On the basis of both phylogenetically monophyly and morphological distinctiveness, it is reasonable to recognize Paris as a single genus (Franchet 1888a, b; Hara 1969; Li 1998; Ji 2006) rather than dividing it into three genera (Takhtajan 1983; Farmer and Schilling 2002). Although nrDNA phylogenies failed to recover the genus Paris as monophyletic, this can be attributed to the ancient hybridization between the ancestor of P. sect. Paris and the Trillium, which led to the speciation of P. japonica. Given that plastome phylogenies revealed all Paris species have a common maternal ancestor, it is reasonable to define Paris as a single genus even though it possesses a putative intergeneric hybrid (P. japonica).

5.3

Infrageneric Classification

Both the nuclear and plastid phylogenies do not support the classification of Li (1998), but justify the infrageneric subdivision proposed by Ji et al. (2006). The updated classification by Ji et al. (2006) was robustly supported by both molecular and morphological evidence (Ji et al. 2006, 2019; Table 5.1). As a result, I collapsed P. sect. Dunnianae H. Li, P. sect. Fargesianae H. Li, and P. sect. Marmoratae H. Li as synonyms of P. sect. Euthyra Franchet. The nomenclatural consequence of this collapse includes the redefinition of the section Euthyra sensu Li (1998). Here, the infrageneric system (Fig. 5.3) is formally presented with a key to the sections. (1) Paris sect. Paris, Hara, J. Fac. Sci. Univ. Tokyo, Sect. 3, Bot. 10: 142. 1969. Type: Paris quadrifolia L.

Rhizome long and slender; stamens 2-whorled; ovary rounded, 4- to 10-loculed with axile placentation; fruit a rounded berry; seeds without sarcotesta or aril. (2) P. sect. Kinugasa (Tategawi et Suto) Hara, J. Fac. Sci. Univ. Tokyo, Sect. 3, Bot. 10: 142. 1969. Type: Paris japonica (Franch. et Sav.) Franch.

Table 5.1 Comparison of morphology among the five re-circumscribed sections in Paris Rhizome Stamens Ovary shape Placentation type Fruit Seeds

Sect. Euthyra Thick 2- to 4-whorled Angular Parietal Capsule With sarcotesta

Sect. Thibeticae Thick 2-whorled Angular Parietal Capsule With imperfect aril

Sect. Axiparis Thick 2- or 3-whorled Angular Axile Berry With imperfect aril

Sect. Paris Long and slender 2-whorled Rounded Axile Berry Without sarcotesta or aril

Sect. Kinugasa Thick 2-whorled Angular Axile Berry Without sarcotesta or aril

5.3 Infrageneric Classification

73

Fig. 5.3 Comparison of rhizome, flower, fruit, and seed morphologies among the five currently recognized Paris sections

Rhizome thick; stamens 2-whorled; ovary angular, 4- to 10-loculed with axile placentation; fruit an angular, juicy berry; seeds without sarcotesta or aril.

Rhizome thick; stamens 2-whorled; ovary angular, 1-loculed with partial placentation; fruit a dehiscent capsule; seeds black, imperfectly enveloped with red, juicy aril.

(3) P. sect. Thibeticae H. Li, Bull. Bot. Res Harbin 6: 132. 1986. Type: Paris thibetica Franch.

(4) P. sect. Axiparis H. Li, Acta Bot. Yunnan. 6: 365. 1984. Type: Paris vaniotii Lėvl.

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5 Phylogeny, Classification, Biogeography, and Evolution

Rhizome thick; stamens 2- to 3-whorled; ovary angular, 4to 10-loculed with axile placentation; fruit berry; seeds white or yellow, imperfectly enveloped with spongy aril. (5) P. sect. Euthyra (Salisb.) Franch. in Mem. Soc. Philim. Cent. (Paris) 24: 277. 1888. -P. sect. Dunniana H. Li, Acta Bot. Yunnan. 6: 357. 1984. -P. sect. Marmoratae H. Li, Acta Bot. Yunnan. 6: 357. 1984. -P. sect. Fargesianae H. Li, Acta Bot. Yunnan. 6: 359. 1984. Type: Paris polyphylla Smith. Rhizome thick; stamens 2- to 4-whorled; ovary angular, 1-loculed with partial placentation; fruit a dehiscent capsule; seeds covered with red or orange sarcotesta; pollen ornamentation foveolate. Key to sections of Paris L. 1a. Rhizome long and slender; ovary and fruit rounded...............................................1. Paris sect. Paris 1b. Rhizome thick; ovary and fruit angular 2a. Sepals showy; seeds without sarcotesta or aril............................................2. P. sect. Kinugasa 2b. Sepals leaf-like; seeds covered by sarcotesta or aril 3a. Ovary axile placentation; fruit an indehiscent berry..........................................4. P. sect. Axiparis 3b. Ovary parietal placentation; fruit a dehiscent capsule 4a. Seeds black, imperfectly enveloped with red, juicy aril............................3. P. sect. Thibeticae 4b. Seeds white, covered with red or orange sarcotesta.............................5. P. sect. Euthyra

5.4

Historical Biogeography

The biogeographic scenario of Paris has been addressed primarily based on plastome phylogeny (Ji et al. 2019). Molecular dating (Fig. 5.4) revealed the divergence between Paris and Trillium occurred at ~32.07 Mya (95% HPD: 36.22–27.92 Mya). Within the genus Paris, the successive divergence of P. sect. Paris, P. sect. Kinugasa, P. sect. Thibeticae, P. sect. Axiparis, and P. sect. Euthyra took place at ~28.59 Mya (95% HPD: 33.24–24.4 Mya), ~20.9 Mya (95% HPD: 29.44–10.24 Mya), 8.19 Mya (95% HPD: 11.37–5.66 Mya), and ~5.54 Mya (95% HPD: 7.26–3.52 Mya), respectively. Reconstruction of the ancestral area implies that the most recent common ancestor (MRCA) of Paris most likely occurred in northeastern Asia and northern China, and has experienced five dispersal and six vicariance events during its diversification and formation current geographic distribution (Fig. 5.5). It is interesting to note that the basic karyotype of species currently occurring in

northeastern Asia, northern China, and Europe is K (2n) ¼ 6m + 2t + 2st and K(2n) ¼ 6m + 2t + 2st, whereas species in subtropical and tropical areas have the “tropical” karyotype, K(2n) ¼ 6m + 4t (Li et al. 1988, 1998). Asymmetrical karyotypes have traditionally been considered derivatives of ancestral cytotypes that were more symmetrical (Stebbins 1971). Therefore, the “tropical” karyotype in Paris may represent the apomorphic state. The “temperate origin” scenario of Paris revealed by molecular phylogeny (Ji et al. 2019) can also be justified by cytological evidence. The basal divergence within Paris was dated to 28.59 Mya (the early Oligocene) (Fig. 5.4), accompanied by a dispersal and a vicariance event (Fig. 5.5). The global climate change event occurring during that time led to the expansion of forest vegetation at the high latitudes of Eurasia (Collinson 1992; Zachos et al. 2001). Therefore, divergence of P. sect. Paris from taxa with thick rhizomes was most possibly triggered by these events (Ji et al. 2019). Interestingly, the divergence of P. sect. Kinugasa (P. japonica) and P. tetraphylla, two species currently endemic to Japan, is associated with two independent vicariance events (Fig. 5.5). Their divergence ages were estimated around 20.9 Mya and 17.31 Mya (Fig. 5.4), in the early Miocene when the opening of Japan Sea isolated islands of Japan from East Asian Continent (Santosh 2011). The colonization of P. sect. Thibeticae, P. sect. Axiparis, and P. sect. Euthyra in subtropical East Asia, associated with three dispersal events (Fig. 5.5), may have been driven by the introduction and intensification of Asian monsoon in the Miocene (Ji et al. 2019). The onset of monsoonal climate in the Oligocene/Miocene boundary constructed a connection between forests from low to high latitudes of East Asia (Sun and Wang 2005), facilitating the migration of the MRCA of these taxa into subtropical areas. In addition, the enhancement of summer monsoon in the late Miocene established a more humid climate in East Asia (Wan et al. 2007; Jacques et al. 2011; Zhang et al. 2012), which had created favorable habitats in subtropical areas that facilitated the dispersal and divergence of P. sect. Thibeticae, P. sect. Axiparis, and P. sect. Euthyra (Ji et al. 2019). In conclusion, the robust phylogeny based on whole plastome sequences provides a valuable framework to elucidate the historical biogeography of Paris. The phylogenomic analyses of the plastome suggest that the divergence of the genera Paris and Trillium could be traced back to the early Oligocene, and the data are indicative of the “temperate origin” scenario of current Paris species. In addition, the historical events, such as the opening of the Japan Sea and the establishment of monsoonal climate in East Asia, played critical roles in the formation of the extant distribution pattern of this genus.

5.4 Historical Biogeography

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Fig. 5.4 Molecular dating inferred from plastome phylogeny. Numbers above/under the tree branches represent the mean ages (Mya) of divergence and the 95% confidence interval of each node

76 Fig. 5.5 Reconstruction of the ancestral area of Paris, with extant species being assigned to (a) southwestern China and the Himalayas, (b) eastern, central, and southern China and northern Indochina, (c) northeastern Asia and northern China, (d) Europe and the Caucasus

5 Phylogeny, Classification, Biogeography, and Evolution

5.6 Origin and Evolution of Genomic Gigantism

5.5

Species Diversification

Under the framework of phylogenetic analyses and molecular dating, the change in the diversification rate for Paris over time was inferred using semi-logarithmic lineage through time (LTT) plot (Paradis and Schliep 2019) and Bayesian Analysis of Macroevolutionary Mixtures (BAMM) (Rabosky et al. 2014). Both analyses suggested a drastically increased diversification rate in Paris since the Miocene/Pliocene transition (Fig. 5.6), which was likely responsible for the occurrence of approximately 80% the extant taxa in this genus. Ji et al. (2019) proposed that the sudden acceleration in species diversification rate inferred in Paris may have been driven by the further enhancement of monsoonal climate in the summer, which established two distinct monsoon regimes in subtropical East Asia since the late Miocene (Sun and Wang 2005; Li et al. 2008; Yao et al. 2011). From that time, southwestern China and the eastern Himalayas have basically been controlled by the Indian monsoon, while eastern China and northern Indochina have primarily been governed by the Pacific monsoon (An et al. 2001; Li et al. 2008; Yao et al. 2011, 2012). This climatic differentiation resulted in profound habitat heterogeneity between the two abovementioned regions (Li and Li 1997; Wang et al. 2012; Lu et al. 2018), and may have triggered significant vicariance and allopatric speciation in Paris (Ji et al. 2019). The LTT and BAMM analyses (Fig. 5.6) also revealed that the most extensive speciation in Paris took place in the Pliocene and the Pleistocene, temporally coinciding with the rapid uplift of Qinghai-Tibetan Plateau in the late Neocene (ca. 3.6 Ma; An et al. 2001; Harrison et al. 2001; Royden et al. 2008; Shi et al. 2006) and the Pleistocene glaciation/ interglaciation cycles in East Asia (Shi 1998). These historical events dramatically influenced biological processes in East Asia (Axelrod et al. 1998; Li and Fang 1999; Qiu et al. 2011), and are expected to have driven diversification of a wide spectrum of plant clades (Axelrod et al. 1998; Qian and Ricklefs 2000; Wu et al. 2005; Wen et al. 2014; Favre et al. 2015). They would also have triggered a radiative speciation in Paris (Ji et al. 2019).

5.6

Origin and Evolution of Genomic Gigantism

Paris is fairly distinctive because species within this genus possesses large genomes and have a high diversity of genome sizes (see Chap. 3); therefore, it provides an ideal model to investigate genome evolution. Although insights into the mechanisms that drive the formation of large genomes and genomic gigantism remain limited (Hidalgo et al. 2017), the robust plastome phylogeny reconstructed for Melanthiaceae

77

and Paris provided insight into the origin and evolution of large (or giant) genomes in Paris (Morgan 2001; Wendel et al. 2002; Bennetzen et al. 2005; Hidalgo et al. 2017). Within Melanthiaceae, most taxa have small or very small genomes, and large (or giant) genomes have been exclusively documented in the tribe Parideae (Pellicer et al. 2014). A previous study suggested that a genome size expansion took place posterior to the divergence of Xerophylleae and Parideae but anterior to the splitting of Paris and Trillium (Pellicer et al. 2014). Molecular dating indicated that the stem age and crown age of Parideae were approximately 52.66 Mya and 32.07 Mya (Fig. 5.4), suggesting that the intensive genome expansion would occur over ~20 million years. During this period, the ancestral genome of extant Paris and Trillium would have gradually expanded, indicating that the genome size may have slowly increased in Parideae over tens of millions of years rather than an explosive increase event (Yang et al. 2019). The plastome phylogeny recovered Paris sect. Paris (slender rhizome lineage) as the earliest diverging clade in the genus. The mean genome size (1C ¼ 38.82 pg) of species in this section is significantly ( p < 0.01) smaller than that of species with thick rhizomes (1C ¼ 58.93 pg). This suggests that the genome evolution in Paris can be characterized by a general trend towards genome size expansion. As previously discussed in this chapter, inter-sectional and interspecific hybridization could be very common during the evolution of species with a thick rhizome. Additionally, the data suggest that the largest eukaryotic genome holder, P. japonica, is likely an inter-generic hybrid between Paris and Trillium. Therefore, the genome size expansion P. japonica may have been related to these hybridization events. The the plastid phylogenomic analyses indicated that section Paris is successively sister to P. japonica (P. sect. Kinugasa), P. thibetica (P. sect. Thibeticae), P. sect. Axiparis, and P. sect. Euthyra (Fig. 5.1). This suggests that the formation of the giant genome (1C ¼ 152.23 pg) of P. japonica most likely occurred after the divergence of P. japonica. Aside from the large genome size of P. japonica, two species (Trillium  hagae and T. rhombifolium) with genome sizes 1C > 100 pg have been found in the genus Trillium (Leitch et al. 1998, 2010; Hidalgo et al. 2017). The monophyly of both Trillium and Paris suggests that the formation of the giant genomes in P. japonica and Trillium species may have been independent events (Yang et al. 2019). The genome size of P. japonica is approximately threefold larger than that of the mean genome size of the other species with a thick rhizome. Some studies have shown that the genome size variation in plants is under selective constrains and has not evolved purely by drift (Kang et al. 2014; Wright et al. 2014; Carta and Puruzzi 2016), but due to the environment and ecology (Knight et al. 2005). In general,

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Fig. 5.6 Historical diversification of Paris based on (a) the lineage through time (LTT) plots analysis, and (b) Bayesian Analysis of Macroevolutionary Mixtures (BAMM)

References

plants with larger genomes share some morphological traits, such as large plant size and stomatal size (Knight and Beaulieu 2008). Due to the susceptibility of plants with large stomata to drought, it is expected that only those species occurring in humid habitats can sustain larger genomes (Knight and Beaulieu 2008; Carta and Puruzzi 2016). Compared with the monsoonal climate in East Asian continent that is characterized by significant differences in seasonal precipitation (Wan et al. 2007; Jacques et al. 2011), the maritime climate of the islands of Japan (Fukutome et al. 2003) provide more humid habitats, facilitating the evolution of P. japonica towards genomic gigantism (Yang et al. 2019). Based on the observation of a negative correlation between genus-level diversity and the genus-average genome size in plants (Vinogradov 2003; Knight et al. 2005). Knight et al. (2005) and Suda et al. (2005) hypothesized that species with large-sized genomes may diversify more slowly (the large genome constraint hypothesis). Paris is fairly distinctive in angiosperms with its possession of large genomes. The minimum documented genome size in the genus is P. bashanensis (1C ¼ 29.38 pg, see Chap. 3), which is much larger than the mean genome size of all angiosperms (Pellicer et al. 2010, 2014). Moreover, Paris has the largest known eukaryotic genome, that of P. japonica, 1C ¼ 148.88 Gb (Pellicer et al. 2010; Dodsworth et al. 2015). Lineage diversification analyses suggest that Paris may have undergone a species radiation since the Miocene/ Pliocene boundary (Fig. 5.6), which is not consistent with the prediction that large genome size could limit speciation (Knight et al. 2005; Suda et al. 2005). Therefore, the generality of the large genome constraint hypothesis requires further evaluation (Ji et al. 2019). Acknowledgement This chapter was modified from the paper published by our group in BMC Plant Biology (Ji et al. 2019; 19:543). The related contents are re-used with the permission.

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6

Taxonomic Revision

Paris Linn. Linnaeus, Pl. Sp. Ed. 1: 367. 1753; Franch., Mem. Soc. Philom. Cent. (Paris) 24: 278. 1888; Hara, Journ. Fac. Sci. Univ. Tokyo, sect. 3, 10 (10): 175. 1969; Wang et Tang, Fl. Reipubl. Popularis Sin. 15 (2) 86. 1978. H. Li, Bull. Bot. Res. Harbin 6 (1): 138. 1986; H. Li, The Genus Paris (Trilliaceae) 63. 1998; S. Y. Liang et V. G. Soukup, Fl. China 24: 98. 2000. Type: Paris quadrifolia Linn. Daiswa Rafinesque, Fl. Tellur. 4: 18. 1838; A. Takhtajan, Brittonia 35: 255. 1983. Type: Daiswa polyphylla (Franch.) Raf. [¼Paris polyphylla Franch.] Euthyra Salisbury, Gen. Fl.: 16. 1866. Type: Euthyra polyphylla (Franch.) Salisb. [¼Paris polyphylla Franch.] Kinugasa Tatewaki et Suto, Trans. Sapp. Nat. His. Soc 14: 36. 1935. Type: Kinugasa japonica (Franch. et Sav.) Tatewaki et Suto [¼Paris japonica (Franch. et Sav.) Franch] Perennial herb. Rhizome slender (usually branched) or thick (seldom branching), white or yellow-brown outside, and white outside, bearing an apical bud and numerous adventitious roots. Stem erect, cylindrical, green or purple. Leaves net-veined, 4 (rarely 3) to 15 in an apical whorl, petiolate or sessile; leaf blade lanceolate to ovate, mid-vein and the first pair of lateral veins obvious, net veins inconspicuous. Flower solitary and terminal, basic merosity roughly equal to (or less than) leaf number. Peduncle green or purple; sepals green, leaf-like, lanceolate to ovate. Petals linear (occasionally absent), yellow-green (rarely white or dark red), longer or shorter than sepals. Stamens 2–4  petal number, filament thin and narrow, anthers basifixed, and dehiscing by a lateral slit. Ovary rounded or angular, uni(parietal placentation) or multi-locular (axile placentation), ovules numerous, arranged along carpel suture or central axis of ovary. Style short, erect or curved. Fruit an indehiscent berry or a loculicidal capsule. Seed several to many, with or without a thick outer covering (sarcotesta or aril). Basic chromosome number x ¼ 5.

As noted in Chap. 1, the circumscription and subdivision of the genus Paris have been debated for a long time (Rafinesque 1838; Salisbury 1866; Franchet 1888b; Tatewaki and Suto 1935; Hara 1969; Takhtajan 1983; Li 1998). The monophyly of Paris circumscribed here is fully supported by plastome-based phylogeny (Ji et al. 2019), as well as morphological, cytological, and palynological features. Additionally, the subdivision of the genus into five sections as well as the intersectional relationships is also justified by both molecular and morphological evidence. The genus consists of 26 species, occurring in East Asia and Europe (Fig. 3.1 in Chap. 3). 1a. Rhizome long and slender; style without an enlarged base, fruit rounded (1. P. sect. Paris) 2a. Leaves 4 (rarely 5 or 6); flower 4-merous, sepals reflexed 3a. Petals present, free portion of connective longer than 4 mm, stigma shorter than 5 mm 4a. Leaves obovate; sepals oblong-lanceolate, 5–10 mm wide...............................................3. P. quadrifolia 4b. Leaves oblong to elliptic; sepals narrowly lanceolate, 3–5 mm wide ......................5. P. bashanensis 3b. Petals absent, free portion of connective shorter than 2 mm, stigma longer than 8 mm......1. P. tetraphylla 2b. Leaves usually 6–10; flower 4- to 6-merous, sepals spreading horizontally 5a. Petals present, stigma short............4. P. verticillata 5b. Petals absent, stigma longer than stamen...........................................2. P. incompleta 1b. Rhizome thick; style with an enlarged base, fruit angular 6a. Sepals showy; seeds without sarcotesta or aril .................6. P. japonica (2. P. sect. Kinugasa) 6b. Sepals leaf-like; seeds covered by sarcotesta or aril 7a. Ovary multiple-locular with axile placentation; fruit an indehiscent berry (4. P. sect. Axiparis) 8a. Stamens 2  petal number ................9. P. forrestii

# Science Press 2021 Y. Ji, A Monograph of Paris (Melanthiaceae), https://doi.org/10.1007/978-981-15-7903-5_6

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6 Taxonomic Revision

8b. Stamens 3  (rarely 2  or 4 ) petal number................................................8. P. vaniotii 7b. Ovary single-locular with parietal placentation; fruit a dehiscent capsule 9a. Seeds black, imperfectly covered with red, and juicy aril.........................7. P. thibetica (3. P. sect. Thibeticae) 9b. Seeds white, wholly enveloped with red or orange sarcotesta (5. P. sect. Euthyra) 10a. Stamens 3–4  petal number 11a. Stamens 4 (rarely 3)  petal number; leaves oblong-obovate to obovate, apex acute, sepals oblong-lanceolate, shorter than petals...................................10. P. dunniana 11b. Stamens 3  petal number, leaves elliptic to ovate, apex acuminate, sepals lanceolate, longer than petals ............12. P. xichouensis 10b. Stamens 2  (rarely 3 ) petal number 12a. Leaves adaxially with white or pale-green markings along the veins 13a. Plant glabrous 14a. Grown plants higher than 30 cm; leaf blades cordate at base, apex acute, caudiform................17. P. cronquistii 14b. Grown plants shorter than 30 cm; leaf blade cuneate at base, apex acuminate 15a. Leaves obovate or obovate-oblong; petals much longer than sepals ................21. P. luquanensis 15b. Leaves oblong or lanceolateoblong; petals shorter or slightly longer than sepals...................24. P. marmorata 13b. Plant pubescent or papillose-pubescent ...........25. P. mairei 12b. Leaves adaxially without markings 16a. Stamens less than 8 mm, free portion of connective ellipsoid or subglobose....16. P. fargesii 16b. Stamens longer than 1 cm, free portion of connective not ellipsoid or subglobose 17a. Free portion of connective longer than 4 mm 18a. Sepals usually purple; petals much shorter than sepals, reflexed............18. P. delavayi 18b. Sepals green; petals longer or as long as sepals, erect or spreading horizontally...........23. P. yanchii 17b. Free portion of connective shorter than 3 mm 19a. Leaves with 2–3 pairs of lateral veins, basally developed

20a. Petals usually shorter than sepals .........13. P. chinensis 20b. Petals longer than or as long as sepals 21a. Stylar base cyan purple, stellate........................11. P. vietnamensis 21b. Stylar base white, purple or dark red 22a. Petals 2–5 mm wide 23a. Leaves 20–30  8–15 cm; petals 2–3 mm wide, slightly widened at the tip ..........19. P. liiana 23b. Leaves 8–15  3–7 cm; petals 3–3 mm wide ...............20. P. yunnanensis 22b. Petals 1–2 mm wide...................15. P. qiliangiana 19b. Leaves with a pair of lateral veins, basally developed 24a. Leaves 4–6, leathery, adaxially lustrous ........14. P. caobangensis 24b. Leaves 9–15, membranous or papyraceous 25a. Leaves linear to lanceolate (oblong-lanceolate), sessile or with very short petiole........................22. P. lancifolia 25b. Leaves oblong to long elliptic, petiole 1–3 cm long ..........................25. P. polyphylla

6.1

Section Paris

Paris sect. Paris, Hara, J. Fac. Sci. Univ. Tokyo, Sect. 3, Bot. 10: 142. 1969. Rhizome long and slender; stamens 2  petal number; ovary rounded, 4- to 10-loculed with axile placentation, style base not enlarged; fruit a rounded berry; seeds without sarcotesta or aril. 1. Paris tetraphylla A. Gray., Bot. Jap. 412. 1858; Franch., Mem. Soc. Philom. Cent. (Paris) 24: 284. 1888; Ohwi, Fl. Jap. new. Ed. Rev. 162. 1969; H. Li, Bull. Bot.

6.1 Section Paris

Res. Harbin 6 (1): 139. 1986; B. Mitchell, Plantsman 9 (2): 86. 1987; H. Li, The Genus Paris (Trilliaceae) 62. 1998. Type: Japan, 01. Jan. 1856, C. Wright s. n. (Holotype, GH). Perennial herb. Rhizome slender, usually branched. Stem erect, green, cylindrical, 25.0–45.0 cm tall. Leaves usually 4 (rarely 5 or 6) in an apical whorl, sessile; leaf blades green, obovate, broad obovate, or oblong-lanceolate, ca. 4.0–12.0 cm  2.0–5.0 cm, base cuneate, apex acuminate, glabrous, with a pair of lateral veins, basally developed, arching to the tip of the leaf. Flower 4-merous; pedicel green, 3.0–10.0 cm long; sepals green, ovate or lanceolate, reflexed, 1.0–3.0 cm  0.2–1.0 cm; petals absent, subulate when present. Stamens 2  sepal number, arranged in 2 whorls; filament greenish yellow, 2.0–8.0 mm; anthers pale yellow, 2.0–6.0 mm long, dehiscing by a lateral slit; free portion of connective inconspicuous. Ovary 4-loculed, globose, axial placentation; stigmas 4, 8.0–12.0 mm, usually erect. Fruit a globose berry, 4.0–15.0 mm in diameter, purplish black, indehiscent. Seeds a tetrahedral sphere, without aril or sarcotesta (Figs. 6.1 and 6.2). Phenology: flowering April–May, fruiting June– September. Habitats: deciduous broad-leaved and coniferous forests; ca. 200–1400 m. Distribution: endemic to Japan (Akita, Aomori, Fukui, Fukushima, Gifu, Gunma, Hiyama, Hyogo, Ibaraki, Ishikari, Ishikawa, Iwate, Kagawa, Kamikawa, Kanagawa, Kochi, Kyoto, Mie, Miyagi, Miyazaki, Nagano, Nagasaki, Nara, Niigata, Okayama, Oshima, Rumoi, Saitama, Shiga, Shimane, Shizuoka, Tochigi, Tokachi, Tokushima, Tokyo, Tottori, Yamagata, Yamanashi). Additional specimens examined: JAPAN, AKITA, Honjo: 04 May 2003, Yukiko Abe s. n. (TNS). Kazuno: 12 Aug. 1976, Hiroshi Takahashi s. n. (TNS). Miyakawa: 01 Jun. 1941, Misao Hemmi 258 (TNS). Oga: 07 Jun. 2007, Goro Kokubugata 9773 (TNS). Yamase: 10 Aug. 1936, G. Koie s. n. (TNS). Yuzawa: 28 May 1974, Toshiyuki Nakaike s. n. (TNS). AOMORI, Iwaki: 19 Jun. 1961, Hiroshi Ito s. n. (TNS); loc. eodem, 06 Aug. 1961, K. Kogure s. n. (TNS); loc. eodem, Aug. 1885, Hanzaburo Sakurai s. n. (TNS). FUKUI, Ono: 26 Aug. 1973, Hiroo Kanai 731274 (TNS). FUKUSHIMA, Koriyama: 840–920 m, 37 320 N, 140 120 E, 01 Jul. 1993, T. Kajita et al. 28317(HAST). Hinoemata: 28 Aug. 1934, Hideo Koidzumi 93821 (TNS); loc. eodem, 24 Jun. 1941, Daikichi Hoshi & H. Koidzumi 108684 (TNS). Nishigo: 29 Jul. 1958, S. Okuyama 19254 (TNS). Shimogo: 07 Jun. 1961, S. Okuyama 16900 (TNS). Takine: 01 Jun. 1978, Y. Kadota 5068 (TNS). Tateiwa: 30 Jul. 1942, Shunki Okuyama 6838 (TNS). GIFU, Hagiwara: 19 Jun. 1986, Hiroshi Takahashi 17672 (TNS). Itadori: 10 Aug. 1986, Hiroshi Takahashi 17433 (TNS). Kamioka: 29 Jun. 1989, Hiroshi Takahashi 17689 (TNS). Neo: 05 Jun. 1982, Hiroshi Takahashi 6011 (TNS). Shirakawa: 27 May 1985, H. Takahashi & H. Takano 1628 (TNS); loc. eodem,

85

07 Jun. 1976, G. Murata 30023 (TNS); loc. eodem, 07 Jun. 1976, K. Mimoro & S. Tsugaru s. n. (TNS); loc. eodem, 18 May 1983, H. Takahashi & H. Takano 7736 (TNS). Tokuyama: 13 Jun. 1982, Hiroshi Takahashi 6051 (TNS). GUNMA, Agatsuma: 07 Aug. 1969, K. Masuda 2762 (TNS). Fujimi: 21 Jun. 1953, T. Wakana s. n. (TNS). Katashina: 05 Jun. 1948, Tetsuya Kawasaki 2657 (TNS); loc. eodem, 21 Jul. 1934, Shunki Okuyama s. n. (TNS); loc. eodem, 02 Aug. 1954, Kiyoshi Sugano s. n. (TNS). Minakami: 24 Jul. 1934, Shunki Okuyama s. n. (TNS). Momono: 20 Jun. 1954, H. Utsumi s. n. (TNS). Murota: 06 Jun. 1935, Tatsuo Satow 5055 (TNS). Niiharu: 05 Aug. 1976, Hiroshi Takahashi 2721 (TNS); loc. eodem, 12 Jul. 1957, S. Okuyama, Y. Fueki & H. Utsumi 13207 (TNS). Tsukiyono: 06 Jun. 1956, Tsukiyono-machi s. n. (TNS). HIYAMA, Assabu: 22 May 1950, T. Nakai & N. Maruyama s. n. (TNS). HYOGO, Haga: 18 Aug. 1968, G. Murata & N. Fukuoka 254 (TNS). Kami: 09 May 2008, Goro Kokubugata, Atsushi Ebihara & Yukiko Saito 10643 (TNS). Kanzaki: 02 May 1992, Shinya Miyake 1505 (TNS). Onsen: 11 Aug. 1993, Shinji Fujii 3787 (TNS). Yumesaki: 03 May 1976, T. Kodama 14300 (TNS). IBARAKI, Makabe: 28 May 1997, F. Konta & Y. Momose 88 (TNS); loc. eodem, 19 May 1982, E. Miki 2042 (TNS). Sakuragawa: 12 Feb. 2004, Goro Kokubugata 1656 (TNS). Tsukuba: 30 May 1949, S. Okuyama s. n. (TNS); loc. eodem, 08 May 1971, S. Okuyama 23220 (TNS). ISHIKARI, Chitose: 10 Jul. 1997, Hiroshi Takahashi 17202 (TNS); loc. eodem, 30 May 1989, T. Sugawara & S. Kobayashi 251301 (HAST). Sapporo: 23 Jun. 1967, N. Kurosaki 4330 (TNS). ISHIKAWA, Oguchi: 15 Jun. 1952, N. Satomi s. n. (TNS). Shiramine: 09 Aug. 1903, Hanzaburo Sakurai s. n. (TNS); loc. eodem, 31 Jul. 1972, M. Sakakibara s. n. (TNS). IWATE, Kamaishi: 30 Jun. 1967, H. Koyama & S. Sasamura 2525 (TNS). Kawai: 22 May 1967, E. Ito & M. Togashi 122 (TNS). Matsuo: 31 Aug. 1962, H. Koyama 1489 (TNS). Matsuo: 08 Sep. 1968, M. Kikuchi (TNS). Ofunato: 23 Jun. 1967, H. Koyama & M. Hotta 2218 (TNS). Ohasama: 17 Jul. 1967, S. Okuyama 12318 (TNS); loc. eodem, 18 Jul. 1967, S. Okuyama 12317 (TNS). Sumita: 24 Jun. 1967, H. Koyama & M. Hotta 2305 (TNS). Takizawa: 01 Sep. 1900, Hanzaburo Sakurai s. n. (TNS). KAGAWA, Shionoe: 28 Apr. 1939, Yoshizo Ujike s. n. (TNS); loc. eodem, 15 Aug. 1949, H. Toyoshima s. n. (TNS). KAMIKAWA, Asahikawa: 09 Jun. 1918, Hideo Koidzumi 79703 (TNS). Furano: 12 Jun. 1978, K. Mimoro & S. Tsugaru 4848 (TNS). KANAGAWA, Hakone: 23 May 1933, Hajime Yamamoto 2039 (TNS); loc. eodem, 22 May 1933, Hajime Yamamoto 2121 (TNS); loc. eodem, 16 Aug. 1941, Hideo Koidzumi 110003 (TNS); loc. eodem, 01 Jun. 1952, Chizuru Ohkawa s. n. (TNS); loc. eodem, 10 Jun. 1933, Hideo Koidzumi 43247 (TNS); loc. eodem, 06 Dec. 1989, Y. Nakagome s. n. (O). KOCHI, Higashitsuno: 17 May 1993, S. Fujii & R. Ohfuji 808 (TNS). Hongawa: 30 Sep. 1950, Hongawa-

86

Fig. 6.1 Paris tetraphylla (drawn by M. Shen). Rhizome and stem (a), aerial shoot (b), and berry (c)

6 Taxonomic Revision

6.1 Section Paris

87

Fig. 6.2 Leaves (a), fruit (b), flower (c), and pistil (d) of Paris tetraphylla

mura 11396 (TNS). Umaji: 20 Aug. 1930, Tagawa Motozi s. n. (TNS). KYOTO, Kuta: 17 Jul. 1932, Hajime Yamamoto 202 (TNS). MIE, Komono: 20 Jul. 1971, Hiroshi Takahashi 960 (TNS). MIYAGI, Sendai: 38 180 N, 140 390 E, 250–400 m, 31 May 1946 Arika Kimura s. n. (HAST). Kurikoma: 08 Aug 1952, S. O. 11114 (TNS). Naruko: 04 Jul. 1997, Hiroshi Takahashi 17224 (TNS). Shiroishi:

28 May 1978, R. Suzuki s. n. (TNS). MIYAZAKI, Iino-son: 05 May 1894, Tokutaro Ito s. n. (TNS). Kobayashi: 29 Jul. 1917, Zentaro Tashiro s. n. (TNS). Takachiho: 13 May 1947, Makoto Togashi 4836 (TNS). NAGANO, Agematsu: 08 Aug. 1891, Tokutaro Ito s. n. (TNS). Akaho: 01 Aug. 1922, S. Yoshimura & H. Koidzumi 66378 (TNS). Azumi: 10 Jul. 1920, Hideo Koidzumi 309 (TNS). Hirao: 13 Jul.

88

1931, Hideo Koidzumi 29333 (TNS). Hokujo: 28 Jul. 1920, Y. Yazawa s. n. (TNS); loc. eodem, 09 Aug. 1928, Hajime Yamamoto 0.174 (TNS). Iijima: 03 Aug. 1924, Hideo Koidzumi 7184 (TNS). Iriyamabe: Jul. 1921, Hideo Koidzumi 2667 (TNS). Kisawa: 03 Aug. 1956, M. Muramatsu 2511 (TNS). Matsumoto: 08 Jul. 1980, F. Yokouchi (TNS). Minamishinano: 24 Aug. 1998, T. Shimizu, A. Nakagaki & N. Kato 42432 (TNS). Miyada: 28 Jul. 1893, Hanzaburo Sakurai (TNS); loc. eodem, 06 Aug. 1891, Tokutaro Ito s. n. (TNS). Nagano: 23 Jun. 2010, Goro Kokubugata s. n. (TNS). Nanakubo: 01 Oct. 1927, Hideo Koidzumi 54411 (TNS). Omachi: 06 Jun. 1974, K. Mimoro, S. Tsugaru & K. Nishiyama 1508 (TNS). Oshika: 08 Aug. 1955, M. Muramatsu 1458 (TNS). Sakae: 24 Jun. 1971, S. Ito 608 (TNS). Sanada: 15 Jun. 1969, Shunsuke Serizawa 10148 (TNS). Shinano: 23 Jul. 2010, Goro Kokubugata 13815 (TNS). Togakushi: 27 Jul. 1927, Hideo Koidzumi 72980 (TNS); loc. eodem, 30 Jul. 1960, S. Okuyama 22189 (TNS); loc. eodem, Aug. 1921, Tameko Shiota s. n. (TNS). Yaegochi: 14 Jun. 1930, Hideo Koidzumi 23319 (TNS). Yamada: 29 Aug. 1942, Shunki Okuyama 7283 (TNS). NAGASAKI, Omura: 11 May 1955, Saburo Toyama (TNS). NARA, Tenkawa: May 1888, Hanzaburo Sakurai s. n. (TNS). NIIGATA, Aikawa: 15 May 1954, Shunki Okuyama 10892 (TNS). Koide: 26 Aug. 1967, Fumihiro Konta 6425 (TNS). Mikuni: 13 Jul. 1951, Y. Satake & E. Ito s. n. (TNS); loc. eodem, 19 Jul. 1936, Shunki Okuyama s. n. (TNS). Yunotani: 26 Aug. 1967, S. Kitamura & G. Murata 2834 (TNS). OKAYAMA, Chuuo: 28 May 1960, K. Takayama s. n. (TNS). OSHIMA, Hakodate: 1853–1856, C. Wright s. n. (NY, HUH). RUMOI, Mashike: 06 Aug. 1942, Hideo Koidzumi 111145 (TNS). SAITAMA, Otaki: 25 Jun. 1967, Tarosaku Takano s. n. (TNS). Yokoze: 03 May 1949, Tetsuya Kawasaki 4742 (TNS). SHIGA, Komatsu: 31 May 1931, Akira Yamamoto 0.202 (TNS). Otsu: 12 May 1932, Hajime Yamamoto 883 (TNS). SHIMANE, Iinan: 09 May 2008, Goro Kokubugata 10620 (TNS). SHIZUOKA, Fujinomiya: 17 May 1964, Junichi Sugimoto s. n. (TNS); loc. eodem, 05 Sep. 1968, T. Haibara et al. 92 (TNS); loc. eodem, 18 May 1984, Takatoshi Sato 5161 (TNS); loc. eodem, 25 Apr. 1987, F. Konta, T. Miyazawa & J. Kitagawa 3 (TNS). Gotemba: 08 May 1976, A. Takahashi & F. Konta 10876 (TNS). Higashiizu: 06 Aug. 1970, M. Ichikawa, T. Fujimura & F. Konta 1363 (TNS); loc. eodem, 20 May 1959, Junichi Sugimoto s. n. (TNS). Honkawane: 19 Jul. 1970, K. Hasegawa 20 (TNS); loc. eodem, 28 May 1977, S. Kusaka 161 (TNS); loc. eodem, 13 Aug. 1980, F. Konta 292 (TNS). Misakubo: 05 May 1975, N. Fukui & M. Fukui KFF764 (TNS). Oyama: 22 May 1960, Hiroshi Ito s. n. (TNS). Shizuoka: 30 May 1971, F. Konta 9194 (TNS); loc. eodem, 20 May 1975, Y. Kamijo 176-b s. n. (TNS); loc. eodem, 06 Jun. 1984, Nobuko Morihiro 102 (TNS); loc. eodem, 18 Jun. 1985, Fumihiro Konta 15532 (TNS);

6 Taxonomic Revision

loc. eodem, 28 Jul. 1973, Y. Saiki, T. Noro & K. Morinaga 3290 (TNS). Susono: 26 Aug. 1970, S. Okuyama 23516 (TNS); loc. eodem, 14 Sep. 1975, Y. Kadota & N. Kadota 874 (TNS). Suyama: 26 May 1953, Yoshisuke Satake s. n. (TNS). TOCHIGI, Nasu: 18 Aug. 1952, Koichi Ogawa s. n. (TNS). Nikko: Aug. 1883, Hanzaburo Sakurai s. n. (TNS); loc. eodem, Y. Nakano s. n. (TNS). Nikko: 27 Sep. 1976, Ohba H. & Murata J. 615 (TNS). TOKACHI, Hiroo: 03 Aug. 1970, H. Koyama & N. Fukuoka 3419 (TNS). Nakagawa: 1918, S. Sugawara s. n. (TNS). TOKUSHIMA, Higashiiyayama-son: 17 May 1964, Chikaichi Abe 15390 (TNS). TOKYO, Hinohara: 12 Aug. 1964, Y. Ishii 148 (TNS). Nariki: 21 May 1933, K. Hisauchi s. n. (TNS); loc. eodem, 17 Jun. 1934, Shunki Okuyama s. n. (TNS). TOTTORI, Daisen: 26 Jul. 1966, G. Masamune s. n. (TNS). YAMAGATA, Asahi: 08 Jun. 1886, S. Tsugaru & T. Takahashi 6829 (TNS). YAMANASHI, Kamikuishiki: 15 May 1976, F. K. 10952 (TNS); loc. eodem, 17 Aug. 1967, F. Konta & H. Takahashi 311 (TNS); loc. eodem, 14 May 1967, Akira Takahashi FK 10952 (TNS); loc. eodem, 08 Aug. 1927, Hajime Yamamoto 202 (TNS). Nanbu: 25 May 1975, Yuichi Kadota 65 (TNS). Narusawa: 09 Jul. 1976, T. Shinkai, A. Takahashi & F. Konta FK11307 (TNS). Nishikatsura: 11 Oct. 1954, Okuyama S. 16377 (TNS); loc. eodem, May 1936, Kimiko Shirai (TNS). Seitetsu: 10 Jul. 1938, Shunki Okuyama 9519 (TNS). Uenohara: 09 Jun. 1940, K. Hisauti 2728 (TNS). 2. Paris incompleta M. Bieb., Fl. Taur. -Cauc. 1: 306. 1808; Franch., Mem. Soc. Philom. Cent. (Paris) 24: 283. 1888; Knorring in Komarov, Fl. URSS 4: 470. 1963; Hara, Journ. Fac. Sci. Univ. Tokyo. Sect. 3, 10 (10): 175. 1969; H. Li, Bull. Bot. Res. Harbin 6 (1): 139. 1986; B. Mitchell, Plantsman 9 (2): 87. 1987; H. Li, The Genus Paris (Trilliaceae). 63. 1998. Paris apetala Hoffm., Commentat. Soc. Phys. -Med. Univ. Litt. Caes. Mosq. 1 (1): 5. 1808. Paris octophylla Hoffm., Hort. Mosq. 27. 1808. Perennial herb. Rhizome slender, usually branched. Stem green, 13.0–33.0 cm tall. Leaves 6–12 in an apical whorl; leaf blades green, oblanceolate, obovate, or ovate-oblong, ca. 6.0–13.0  2.0–4.0 cm, acuminated or acute at apex, base cuneate; major veins 3, obvious; subsessile. Flower 4- to 6-merous; pedicel 3.0–12.0 cm; sepals green, lanceolate to ovate-lanceolate, 2.0–5.0 cm  1.0–2.0 cm, spreading horizontally; petals absent. Stamens 2  sepal number, arranged in 2 whorls, filament red, 3.0–6.0 mm long, anthers yellow, dehiscing by a lateral slit, 5.0–8.0 mm long, without free portion of connective. Ovary purplish red, with 4 locules, axile placentation; style inconspicuous, stigmas yellow, 12.0–25.0 mm in length. Berry globose, ca. 5.0–12.0 mm in diameter, gray-black. Seeds brown, without aril or sarcotesta (Fig. 6.3). Phenology: flowering April–May, fruiting June– September. Habitats: coniferous forests; ca. 600–2000 m.

6.1 Section Paris

Fig. 6.3 Paris incompleta (drawn by M. Shen): rhizome and stem (a), aerial shoot (b), and flower (c)

89

90

Distribution: Georgia (Chakvi, Adjara, South Ossetia, Abkhazia), Russia (Black Sea Shore; Caucasus, Krasnodar Krai & Adygea; Caucasus, Stavropol Krai, KarachayCherkessia & Kabardino-Balkaria; Caucasus, North Ossetia, Ingushetia & Chechnya; North Ossetia-Alania; Krasnodar Krai), and Turkey (Artvin, Cinciva, Trabzon). Notes: Bieberstein (1808) did not design the holotype of P. incompleta when this species was described. This issue may have been ignored by Franchet (1888a), Hara (1969), and Li (1998) in their taxonomic revisions on the genus Paris. To date, no specimen examined by Bieberstein has been found. Therefore, the lectotypfication of P. incompleta remains to be resolved in the future. Additional specimens examined: GEORGIA, Chakvi: 41 410 N, 41 490 E, 350 m, 23 Jun. 1999, M. Merello 2360 (E). Adjara: 41 400 N, 41 520 E, 115 m, 10 May 2010, Brown et al. 119 (L). South Ossetia: 29 Aug. 1959, Ш. Кутателадзе, И. Манденова & А. Шхиян (MW). Abkhazia: 20 Aug. 1888, А. П. Иванов s. n. (MW). RUSSIA, BLACK SEA SHORE: 25 Mar. 1996, С. Исаев, Н. Орлова & Д. Соколов s. n. (MW). CAUCASUS, KRASNODAR KRAI & ADYGEA: 43 390 N, 40 220 E, 1000 m, 04 Jul. 2011, М. Н. Кожин s. n. (MW); loc. eodem, 44 0 15N, 39 160 E, 09 Jun. 2009, М. Н. Кожин Kr-777 (MW); loc. eodem, 43 400 N, 40 110 E, 390 m, 04 Sep. 2008, А. Серегин, Л. Ашуркова & З. Винокурова C-969 (MW); loc. eodem, 43 590 N, 40 080 E, 11 Jun. 1937, В. Олюнин s. n. (MW); loc. eodem, 13 Jun. 1939, Г. Исакина s. n. (MW); loc. eodem, 20 Jul. 1905, V. Miller s. n. (MW); loc. eodem, 02 Aug. 1931, А. Кожевников s. n. (MW); loc. eodem, 1600 m, 20 Jul. 1941, П. Смирнов s. n. (MW); loc. eodem, 43 580 N, 40 100 E, 27 May 1957, Г. Гроссет s. n. (MW); loc. eodem, 43 400 N, 40 120 E, 14 May 1966, И. Л. Крылова & А. П. Исайкина s. n. (MW); loc. eodem, Г. Микешин s. n. (MW). CAUCASUS, STAVROPOL KRAI, KARACHAY-CHERKESSIA & KABARDINOBALKARIA: 02 Jul. 1966, Аввакумова s. n. (MW); loc. eodem, 18 Jun. 1972, Чубатова s. n. (MW); loc. eodem, 10 Jul. 1964, А. Гражданкин s. n. (MW); loc. eodem, 14 Jul. 1964, Л. П. Алешин s. n. (MW); loc. eodem, 21 May 1965, Крылова, Михайлова 120 (MW); loc. eodem, 17 Jun. 1962, Магулаев s. n. (MW); loc. eodem, 43 270 N, 41 440 E, 28 Jul. 1938, М. Назаров 15684 (MW); loc. eodem, 44 030 N, 42 020 E, 15 May 2006, А. С.Зернов, Д. К. Текеев 4747 (MW); loc. eodem, 43 250 N, 41 390 E, 25 Jun. 1962, В. Павлов s. n. (MW); loc. eodem, 27 Mar. 1963, Гомозова & Флоренская s. n. (MW); loc. eodem, 43 260 N, 41 410 E, Jun. 1964, Баева s. n. (MW); loc. eodem, 13 Jul. 1964, Лисицына & Никольский s. n. (MW); loc. eodem, 13 Jul. 1964, Баранов s. n. (MW); loc. eodem, 13 Jul. 1964, Сухобокова & Шкуратова s. n. (MW); loc. eodem, Jun. 1966, В. Садовников s. n. (MW); loc. eodem, 43 150 N, 41 410 E, 10 Jul. 1973, Г. Корнейчук s. n. (MW); loc. eodem, 12 Jul. 1974, Грачев s. n. (MW). CAUCASUS, NORTH

6 Taxonomic Revision

OSSETIA, INGUSHETIA & CHECHNYA: 42 470 N, 44 000 E, 25 Aug. 1975, А. Амирханов s. n. (MW); loc. eodem, 22 Apr. 1988, И. А. Николаев s. n. (MW); loc. eodem, 42 450 N, 44 000 E, А. Амирханов s. n. (MW); loc. eodem, 11 Apr. 1899, Marcowicz s. n. (MW). NORTH OSSETIA-ALANIA, Vladikavkaz: 42 500 N, 44 380 E, 05 Jun. 1988, Vladikavkaz s. n. (MW). Alagirsky: 42 460 N, 44 000 E, A. Amirhanov s. n. (MW); loc. eodem, 42 400 N, 44 010 E, 1700 m, 10 Jun. 1976, A. Amirhanov s. n. (MW). KRASNODAR KRAI, Tuapsinsky: 42 060 N, 39 080 E, 01 May 1987, Н. Шведчикова s. n. (MW). Gelendzhik: 44 220 N, 38 310 E, 14 Jun. 1981, Е. Е. Гогина s. n. (MW). Sochi: 43 560 N, 39 190 E, 19 Apr. 2009, О. А. Калашникова s. n. (MW); loc. eodem, 43 390 N, 40 230 E, 1000 m, 04 Jul. 2011, M. N. Kozhin Kr-1137 (MW); loc. eodem, 43 490 N, 39 430 E, 200–300 m, 07 May 1997, С. В. Полевова & А. Б. Шипунов s. n. (MW). TURKEY, Artvin: 1829 m, 29 Jun. 1962, J. Apold et al. 122 (E); loc. eodem, 2000 m, 01 Jul. 1960, Stainton 5926 (E); loc. eodem, 1750, 28 May 1976, A. Duzenli 656 (E); loc. eodem, 1800 m, 11 Aug. 1957, Davis D. 32232 (E); loc. eodem, 2000 m, 01 Jul. 1960, Stainton 5926 (E); loc. eodem, 1500 m, 14 Jul. 1986, Archibald & C. James 7756 (E); loc. eodem, 29 Jun 1962, J. Apold 122 (E); loc. eodem, 28 May 1976, A. Duzenli 656 (E). Cinciva: 457 m, 23 Apr. 1959, K. M. Guichard TUR/28/59 (E). Trabzon: 1219.2 m, 17 May 1960, P. Furse & P. Synge 179 s. n. (E); loc. eodem, 1450 m, 03 Jun. 1968, Baytop Asuman & Baytop Turhan 15310 (E); loc. eodem, 1900 m, 05 Jun. 1961, E. Hennipman, et al. 1861 (NHN). 3. Paris quadrifolia Linn., Pl. Sp. Ed. 1: 367. 1753; Franch., Mem. Soc. Philom. Cent. (Paris) 24: 278. 1888; Knorring, Fl. URSS 4: 469. fig. 29: 1, a. 1963; Hara, Journ. Fac. Sci. Univ. Tokyo, sect. 3, 10 (10): 175. 1969; H. Li, Bull. Bot. Res. Harbin 6 (1): 138. 1986; H. Li, The Genus Paris (Trilliaceae) 63. 1998. Type: Netherlands, George Clifford s. n. (Holotype, BM). Paris pentafolia Renault, Fl. Orna. 26. 1804. Paris trifolia P. Renault, Fl. Orna. 26. 1804. Perennial herb. Rhizome horizontal, slender, usually branched, 2.5–4.0 mm in diameter, 10.0–30.0 cm long. Stem erect, 10.0–25.0 cm tall. Leaves usually 4 (rarely 5–6) in an apical whorl, subsessile; leaf blades obovate, apex acute, base cuneate, green, ca. 5.0–10.0 cm  2.5–7.5 cm. Flower 4-merous; pedicel green, 2.0–8.0 cm; sepals green, reflexed, lanceolate, 9.0–20.0 mm  5.0–12.0 mm; petals, linear, greenish-yellow, shorter than sepals. Stamens 8  petal number, arranged in 2 whorls; filaments green, 6.0–8.0 mm long; anthers yellow, 6.0–9.0 mm long; free portion of connective green, 5.0–8.0 mm long. Ovary green to purple, globose, 4-loculed, axile placentation; style short, 4-lobed, stigma ca. 5.0 mm long. Berry globose, black, ca. 4.0–15.0 mm in diameter. Seeds subglobose, brown, without aril or sarcotesta (Figs. 6.4 and 6.5).

6.1 Section Paris

Fig. 6.4 Paris quadrifolia (drawn by M. Shen): rhizome and stem (a), aerial shoot (b), stamen (c), style and stigma (d), and seeds (e)

91

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6 Taxonomic Revision

Fig. 6.5 Aerial shoots (a, b) and flower (c) of Paris quadrifolia

Phenology: flowering from April–June, fruiting July– September. Habitats: deciduous broad-leaved and coniferous forests; ca. 50–1600 m. Distribution: Siberia to Ural, Caucasus, and Europe. Austria (Allgau Alps, Piburg), Belarus, France (Auvergne, Cantal, Haut-Rhin, Maine-Et-Loire, Orne, Val-d'Oise), Georgia (South Ossetia), Germany (Barnim, Bavaria, Brandenburg, Ostalbkreis, Palatinate), Italy (Molveno), Latvia, Luxembourg, Moldova, Netherlands (Gelderland, Limburg, North Brabant, Overijssel), Norway (Akershus,

Aust-Agder, Buskerud, Finnmark, Hedmark, Hordaland, Nordland, Oppland, Østfold, Sogn Og Fjordane, Telemark, Troms, Trøndelag, Vest-Agder, Vestfold), Poland (Przebieczany, Schlesien), Russia (Altai & Sayan Mountains, Altai Republic, Arkhangelsk, Bashkortostan, Belgorod, Buryatia, Chelyabinsk, Irkutsk, Ivanovo, Kaluga, Karelia, Kemerovo, Khakassia, Khanty-Mansi Autonomous Okrug, Komi, Kostroma, Krasnoyarsk, Kursk, Mordovia, Moscow, Murmansk, Nizhny Novgorod, Novosibirsk, Oryol, Ryazan, Smolensk, Stavropol, Sverdlovsk, Tambov, Tula, Tuva, Tver, Vladimir, Vologda, Yaroslavl), Slovakia

6.1 Section Paris

(Banska Bystrica), Spain (Cuenca, Huesca, Asturias, Lérida, Lugo, Zamora), Sweden (Dalarna, Gotheborg, Hälsingland, Norrbotten, Östergötland, Skåne, Södermanland, Stockholm, Uppsala), Switzerland (Glarus, Valais, Vaud), Ukraine (North Ukrainian Region, South Ukrainian Region, West Ukrainian Region), United Kingdom (England, Scotland). Additional specimens examined: AUSTRIA, Allgau Alps: 1200–1300 m, 19 Jun. 1987, Germany-Chinese Exped. 35288 (KUN). Piburg: 03 Aug. 1970, A. V. Dreemen s. n. (NHN). BELARUS: 24 May 2003, О. В. Созинов s. n. (MW); loc. eodem, 26 May 1918, М. Нейштадт s. n. (MW); loc. eodem, 11 Jun. 1935, Двораковский s. n. (MW). FRANCE, AUVERGNE: 06 Jun. 1947, Stud. Biol. Rheno-Trai. 34 (NHN). CANTAL, St. Jacques Des Blats: 13 Jun. 1953, Th. H. Ten Berge 92 (NHN). Vallières: 17 Apr. 1922, P. Jovet s. n. (P). HAUT-RHIN, Mittlach: 24 Mar. 1954, Stud Biol Rheno-Trai in Itinere 82 (NHN). MAINEET-LOIRE, Brain-Sur-Allonnes: Apr. 1846, L. d'Espinay s. n. (P). ORNE, Beaufai: 15 May 1890, R. Ménager s. n. (P). VAL-D'OISE, Domont: 25 May 1922, P. Jovet s. n. (P). Montlignon: 22 May 1921, P. Jovet s. n. (P). GEORGIA, SOUTH OSSETIA: 42 320 N, 44 090 E, 1600 m, 25 Jun. 1955, Гатцук Л. Шафранова Л. Шорина Н. s. n. (MW). GERMANY, BARNIM, Eberswalde: 08 Jun. 1884, C. Scheppig s. n. (NHN). BAVARIA: 320 m, 09 Jun. 1987, Germany-Chinese Exped. 35.187 (KUN). BRANDENBURG, Märkisch-Oderland: 47 m, 15 May 2008, T. Dürbye & H. Ketelhut DÜR 4187 (B). OSTALBKREIS, Bartholoma: 01 Jul. 1980, D. O. Wijnands 746 (NHN). PALATINATE, Palatinate Forest: 09 Jun. 1987, Germany-Chinese Exped. s. n. (KUN). ITALY, Molveno: 1000 m, 04 Aug. 1959, Boom B. K. 37528 (HNH). LATVIA: Н. Шведчикова s. n. (MW); loc. eodem, 57 0 27 N, 27 010 E, 08 Jul. 1987, Н. Шведчикова s. n. (MW); loc. eodem, 57 310 N, 24 480 E, 28 Jul. 1981, Н. Шведчикова s. n. (MW); loc. eodem, 56 580 N, 21 200 E, 03 Aug. 1988, Н. Шведчикова s. n. (MW). LUXEMBOURG: 16. Jul. 1963, Timmermans A., s. n. (NHN). MOLDOVA: 25 May 1956, Т. С. Гейдеман s. n. (MW); loc. eodem, 07 May 1954, М. Ф. Харакоз s. n. (MW); loc. eodem, 07 May 1952, М. C. Пожарисская s. n. (MW); loc. eodem, 19 Jun. 1951, Шабанова s. n. (MW). NETHERLANDS, GELDERLAND, Nijmegen: 18 May 1982, E. J. WEEDA s. n. (NHN). LIMBURG, Bemelen: 20 May 1939, Excursie Leidse Biologen s. n. (NHN). Epen: Schimmel H 20 (NHN). Etenaken:16 Jun. 1932, Kruyt W. s. n. (NHN). Oud-Valkenburg: 12 May.

93

1951, Reijnders 107 (NHN). NORTH BRABANT, Ulvenhout: Evers s. n. (NHN). OVERIJSSEL, Twente: 10 Apr. 1959, W. H. A. Hekking s. n. (NHN). NORWAY, AKERSHUS, Asker: 59 500 N, 27 100 E, 14 Jun. 1886, Joh. Dyring s. n. (BG). Drøbak: 59 420 N, 10 390 E, 01 Jan. 1899, Jens Holmboe s. n. (BG). Fornebo: 59 540 N, 10 370 E, Ths. H. Poulsson s. n. (O). Sandvika: 19 May 1882, E. Jørgensen s. n. (BG). AUST-AGDER, Tvedestrand: 58 380 N, 08 510 E, 01 Jan. 1864, S. Lund s. n. (O); loc. eodem, 58 370 N, 08 560 E, 31 May 1899, B. Lynge s. n. (BG); loc. eodem, 58 370 N, 08 560 E, 01 Jan. 1877, Eleonore Holmboe s. n. (BG). BUSKERUD, Modum: 60 010 N, 09 590 E, 12 Jun. 1886, Isak Collijn s. n. (BG). FINNMARK, Alta: 70 200 N, 23 150 E, J. M. Norman s. n. (O); loc. eodem, 69 500 N, 23 130 E, 01 Jan. 1852, J. M. Norman s. n. (O); loc. eodem, 69 550 N, 23 310 E, J. M. Norman s. n. (O); loc. eodem, 70 020 N, 23 160 E, J. M. Norman s. n. (O); loc. eodem, 69 590 N, 22 200 E, Henry Kristensen s. n. (O); loc. eodem, 14 Jul. 1864, J. M. Norman s. n. (BG). Børselven: 70 200 N, 25 360 E, 26 Aug. 1863, J. M. Norman s. n. (O). Karasjok: 69 280 N, 24 440 E, 01 Jan. 1864, J. M. Norman s. n. (O); loc. eodem, 68 560 N, 25 360 E, 03 Sep. 1874, J. M. Norman s. n. (O). Kautokeino: 69 090 N, 23 460 E, 01 Jan. 1864, J. M. Norman s. n. (O). Loppa: 70 220 N, 21 260 E, 30 Jun. 1870, J. M. Norman s. n. (O). Nesseby: 70 110 N, 28 370 E, 12 Aug, 1852, Chr. Sommerfelt s. n. (O); loc. eodem, 01 Jul. 1857, Th. M. Fries s. n. (O). Sør-Varanger: 69 410 N, 30 070 E, J. M. Norma s. n. (O). HEDMARK, Hamar: 61 000 N, 11 070 E, 01 Jun. 1878, Jon Rud s. n. (O). Stange: 60 380 N, 11 210 E, 01 Jan. 1872, N. Bryhn s. n. (BG). HORDALAND, Askøy: 60 310 N, 05 050 E, 01 Jan. 1898, O. Grolle-Olsen s. n. (BG). Bergen: 60 190 N, 05 200 E, S. K. Slettemark s. n. (BG); loc. eodem, 60 200 N, 05 220 E, 01 May 1872, Dr. Crawfurd s. n. (BG); loc. eodem, 60 210 N, 05 200 E, Finne s. n. (BG); loc. eodem, 01 Jun. 1888, 60 210 N, 05 200 E, G. F. Heiberg s. n. (BG); loc. eodem, 60 230 N, 05 210 E, Ukjent s. n. (BG); loc. eodem, 60 200 N, 05 210 E, S. K. Slettemark s. n. (BG); loc. eodem, 60 160 E, 05 200 E, 01 Jan. 1879, B. Kaalaas s. n. (BG); loc. eodem, 60 200 N, 05 220 E, 21 Jul. 1865, H. Greve s. n. (BG). Etne: 59 400 N, 05 570 E, 12 Jun. 1863, Chr. Sommerfelt s. n. (O). Granvin: 60 330 N, 06 400 E, 08 Jul. 1889, S. K. Selland s. n. (BG). Odda: 60 060 N, 06 460 E, 29 Jul. 1888, O. Grolle-Olsen s. n. (BG). Os: 60 130 N, 05 270 E, 01 Jan. 1868, Jan Greve s. n. (BG). NORDLAND, Alstahug: 66 010 N, 12 370 E, 1193 m, Ove Dahl s. n. (O). Evenes: 68 280 N, 16 420 E, 15 Aug. 1865, J. M. Norman s. n. (O). Flakstad: 68 070 N, 13 080 E, 11 Jul. 1897, Jonas R. Landmark s. n. (BG). Rødø: 66 410 N, 13 050 E, Anon. s. n. (TRH); loc. eodem, 66 400 N,

94

13 050 E, 12 Jun. 1876, J. M. Norman s. n. (O). Vågan: 68 150 N, 14 500 E, 05 Aug. 1869, J. M. Norman s. n. (O). OPPLAND, Dovre: 62 000 N, 09 150 E, 01 Jan. 1836, Bl. s. n. (O). Jevnaker: 60 170 N, 10 230 E, H. Th. Meinich s. n. (BG). Lillehammer: 61 080 N, 10 230 E, 01 Jun. 1869, Gustav Olstad s. n. (O). Mærradalen: 59 560 N, 10 390 E, 28 May 1854, L. Sylow s. n. (O). Maridalen: 59 580 N, 10 430 E, 01 May 1878, B. Kaalaas s. n. (BG). Ringebu: 61 340 N, 10 180 E, S. C. Sommerfelt s. n. (O). Sør-Aurdal: 60 400 N, 09 390 E, 25 Jul. 1870, Chr. Sommerfelt s. n. (O). Skjåk: 61 550 N, 07 400 E, 09 Aug. 1976, Arnfinn Skogen s. n. (BG). Oslo: 59 580 N, 10 430 E, 01 Jan. 1877, E. Poulsson s. n. (O); loc. eodem, 59 580 N, 10 430 E, 01 Jun. 1870, N. Moe s. n. (BG); loc. eodem, 59 580 N, 10 430 E, 12 Jun. 1845, Printz s. n. (O); loc. eodem, 59 580 N, 10 430 E, M. N. Blytt s. n. (BG). ØSTFOLD, Rømskog: 59 420 N, 11 560 E, Monica Kristiansen Ola Martin Wergeland Krog s. n. (O). Trøgstad: 59 380 N, 11 190 E, 23 Jun. 1875, H. Sommerfelt s. n. (O). SOGN OG FJORDANE, Maristuen: 61 020 N, 07 380 E, 01 Jul. 1888, Jan Greve (BG). TELEMARK, Kviteseid: 59 250 N, 08 350 E, Gunhild Mevasstøl s. n. (O); loc. eodem, 59 250 N, 08 300 E, 02 Jun. 1914, Astrid Karlsen s. n. (BG). Porsgrunn: 59 060 N, 09 450 E, 01 Jan. 1873, Joh. Dyring s. n. (BG); loc. eodem, 59 060 N, 09 450 E, 13 Jun. 1932, K. Fægri s. n. (BG). TROMS, Bardu: 68 460 N, 18 350 E, 26 Aug. 1875, J. M. Norman s. n. (O). Dyrøy: 69 050 N, 17 340 E, 05 Aug. 1870, J. M. Norman s. n. (O). Karlsøy: 70 130 N, 19 200 E, Bryhn s. n. (O). Kvæfjord: 68 460 N, 16 070 E, J. M. Norman s. n. (O). Målselv: 68 580 N, 19 130 E, 21 Jun. 1863, J. M. Norman s. n. (BG). TRØNDELAG, Gauldal: 62 530 N, 10 300 E, 01 Jul. 1922, A. W. Trethewy s. n. (BG). Lian: 59 510 N, 10 470 E, M. N. Blytt s. n. (O). Melhus: 63 110 N, 10 170 E, 01 Jan. 1874, Hagb. Strøm s. n. (O). Nærøy: 01 Jan. 1852, J. M. Norman s. n. (O). Oppdal: 62 320 N, 09 310 E, M. N. Blytt s. n. (O). Orkdal: 62 180 N, 09 430 E, Nissen s. n. (O). Røros: 62 34N, 11 410 E, 01 Aug. 1919, s. n. (BG); loc. eodem, 62 340 N, 11 410 E, 16 Jul. 1921, Joh. Dyring s. n. (BG). Trondhjem: 63 240 N, 10 210 E, 26 Jun. 1898, Jens Holmboe s. n. (BG). Tydal: 62 580 N, 11 450 E, 20 Jul. 1921, Rolf Nordhagen s. n. (BG). VEST-AGDER, Farsund: 58 070 N, 06 410 E, 16 Jul. 1922, Anna Grostøl s. n. (BG). Kristiansand: 58 080 N, 08 000 E, 01 Jan. 1871, R. E. Fridtz s. n. (O); loc. eodem, 58 580 N, 08 030 E, 10 Jun. 1934, A. Danielsen s. n. (BG). Vennesla: 58 250 N, 07 440 E, 28 Jul. 1951, A. Danielsen s. n. (BG). VESTFOLD, Mølen: 59 290 N, 10 300 E, Asbjørn Hagen s. n. (O). Re: 59 250 N, 10 190 E, 17 Jun. 1906, Joh. Dyring s. n. (BG). POLAND, Przebieczany: 49 580 N, 20 060 E, 300 m, 30 Jun. 2006, J. Żelazny s. n. (O). Schlesien: 01 Jun. 1870, M. Firle s. n. (RB).

6 Taxonomic Revision

RUSSIA, ALTAI & SAYAN MOUNTAINS: 01 Aug. 1934, A. Goncharova s. n. (MW); loc. eodem, 21 Jul. 1979, Д. Шауло 81 (MW); loc. eodem, 20 Jun. 1961, Astaf'eva s. n. (MW); loc. eodem, 700 m, 28 Jun. 1970, I. Krasnoborov s. n. (MW); loc. eodem, 1060 m, 20 Jul. 1978, D. Shaulo 1388 (MW); loc. eodem, 09 Jun. 1984, I. Pshenichnaya s. n. (MW); loc. eodem, 18 Aug. 1948, S. A. Nikitin s. n. (MW); loc. eodem, 24 May 1973, G. Dyuryagina s. n. (MW); loc. eodem, 22 Jul. 1946, A. Shreter 879 (MW); loc. eodem, 15 Jun. 1960, Kryukova s. n. (MW); loc. eodem, 03 Jun. 1965, Kul'vinova s. n. (MW). ALTAI REPUBLIC, Choysky: 51 490 N, 85 190 E, 06 Jun. 1984, I. Pshenichnaya s. n. (MW). ARKHANGELSK OBLAST, Onezhsky: 63 480 N, 38 210 E, 23 Jun. 1973, Melanholin s. n. (MW). Solovecky: 65 030 N, 35 330 E, 18 Aug. 1986, Konopleva s. n. (MW); loc. eodem, 65 060 N, 35 370 E, 15 Jul. 1985, M. Stolyarskaya s. n. (MW). Ustyansky: 60 530 N, 43 130 E, 22 Jul. 1996, A. P. Bezdelova s. n. (MW); loc. eodem, 60 540 N, 43 130 E, 04 Jul. 1996, V. V. Neronov s. n. (MW). BASHKORTOSTAN, Duvansky: 55 350 N, 58 190 E, 11 Jun. 1957, P. P. Zhudova s. n. (MW). BELGOROD OBLAST, Gubkinsky: 51 110 N, 37 380 E, 29 May 1921, М. А. Vadkovskaya s. n. (MW). Novooskolsky: 50 460 N, 37 520 E, 17 May 1852, Gornitskiy s. n. (MW). BURYATIA, Kabansky: 51 320 N, 105 320 E, 11 Aug. 2009, N. Gamova s. n. (MW). Mukhorshibirsky: 50 510 N, 107 190 E, 31 May 2012, L. Abramova s. n. (MW). CHELYABINSK OBLAST, Katav-Ivanovsky: 54 390 N, 58 410 E, 890 m, 11 Jul. 1973, V. B. Kuvaev, T. Kagarlitskaya & A. Lazarev 42-23 (MW); loc. eodem, 54 340 N, 58 490 E, 710 m, 19 Jul. 1973, V. B. Kuvaev, T. Kagarlitskaya & A. Lazarev 80 (MW). Verkhneuralsky: 54 800 N, 59 350 E, 31 Jul. 1930, N. Sokolova s. n. (MW). IRKUTSK OBLAST, Nizhneudinsky: 54 540 N, 99 010 E, 02 Jun. 1902, B. P. Bogorodsky s. n. (MW). Ust-Ilimsky: 57 520 N, 102 490 E, 08 Aug. 2007, A. Seregin, I. Seregina & A. Hohlov S-263 (MW). IVANOVO OBLAST, Uzhursky: 56 300 N, 41 460 E, 31 May 1936, S. Stulov s. n. (MW). KALUGA OBLAST, Borovsky: 55 120 N, 36 190 E, 30 Jun. 1975, N. Vorob'ev & V. Mochalov s. n. (MW); loc. eodem, 55 160 N, 36 260 E, 04 Jul. 1976, T. Gracheva & E. Kalinina s. n. (MW). Khvastovichsky: 54 250 N, 35 170 E, 06, Jul. 2001, A. Scherbakov s. n. (MW). KARELIA, Loukhsky: 66 200 N, 33 500 E, 02 Aug. 2001, A. B. Shipunov s. n. (MW). KEMEROVO OBLAST, Tisulsky: 55 500 N, 88 250 E, 09 Jul. 1984, V. Tril s. n. (MW). KHAKASSIA, Beysky: 52 580 N, 91 160 E, 22 Jun. 1965, Kul'vinova s. n. (MW). KHANTY-MANSI AUTONOMOUS OKRUG, Nefteyugansky: 60 070 N, 71 320 E, 08 Aug. 1991, N. Shvedchikova s. n. (MW); loc. eodem, 60 150 N, 72 080 E, 15 Aug. 1991, N. Shvedchikova s. n. (MW); loc.

6.1 Section Paris

eodem, 60 02 0 N, 71 170 E, 19 Aug. 1996, N. Shvedchikova s. n. (MW). Sovetsky: 61 520 N, 64 230 E, 17 Jun. 1941, K. Gornovskiy s. n. (MW). KOMI, Pechora: 65 210 N, 58 680 E, 04 Aug. 1926, Naumova 352 (MW). TroitskoPechorsky: 62 380 N, 57 250 E, 09 Jul. 1925, V. S. Govoruhin s. n. (MW); loc. eodem, 62 320 N, 58 570 E, 05 Aug. 1925, V. S. Govoruhin s. n. (MW). Vuktyl: 64 040 N, 59 250 E, 300 m, 19 Aug. 1948, V. B. Kuvaev 918 (MW). KOSTROMA OBLAST, Kostromskoy: 57 370 N, 40 470 E, 22 May 1878, I. Meissner s. n. (MW); loc. eodem, 57 490 N, 40 520 E, 28 Aug. 2007, N. V. Ivanova 101 (MW). Ponazyrevsky: 58 170 N, 46 140 E, 25 Jun. 1940, N. Lebedinova s. n. (MW), Susaninsky, 58 120 N, 41 470 E, 06 Jun. 1913, A. E. Zhadovskiy 169 (MW). KRASNOYARSK KRAI, Baikitsky: 60 530 N, 97 230 E, 29 Jun. 1938, Vershinin s. n. (MW). Beryozovsky: 55 570 N, 92 440 E, 01 Jun. 1914, Kuznetsov s. n. (MW). Kezhemsky: 58 190 N, 100 030 E, 05 Jun. 1978, D. N. Shaulo s. n. (MW). Kozulsky: 56 110 N, 91 350 E, 06 Jun. 1966, Kul'vinova s. n. (MW). Motyginsky: 58 050 N, 93 520 E, 03 Aug. 1960, A. P. Tyrtikov s. n. (MW). SeveroYeniseysky: 60 290 N, 92 520 E, 02 Jul. 1960, A. P. Tyrtikov s. n. (MW). Turukhansky: 62 270 N, 89 010 E, 22 Jun. 1977, V. B. Kuvaev s. n. (MW); loc. eodem, 62 180 N, 89 010 E, 29 Jun. 1972, L. Sobolevloc s. n. (MW); loc. eodem, 62 180 N, 89 020 E, 29 Jun. 1972, A. Ermolaev s. n. (MW); loc. eodem, 62 200 N, 88 580 E, 22 Jun. 1994, D. A. Shahin s. n. (MW); loc. eodem, 62 180 N, 88 580 E, 18 Jun. 1994, V. B. Kuvaev, D. A. Shahin & S. Mulikov s. n. (MW); loc. eodem, 62 180 N, 89 020 E, 13 Jul. 1978, V. B. Kuvaev & N. Burskaya s. n. (MW); loc. eodem, 60 590 N, 89 340 E, 21 Jun. 1979, V. B. Kuvaev, A. Savich & Savin s. n. (MW); loc. eodem, 62 270 N, 89 010 E, 22 Jun. 1977, В. Б. Куваев s. n. (MW); loc. eodem, 60 560 N, 89 340 E, 29 Jun. 1988, V. B. Kuvaev & M. Ivanova s. n. (MW). KURSK OBLAST, Kursky: 51 340 N, 36 130 E, 23 Jun. 1931, Alehin V. V. s. n. (MW). MORDOVIA, Bolshebereznikovsky: 54 030 N, 45 530 E, 07 Jun. 1965, K. G. Malyutin s. n. (MW). MOSCOW OBLAST, Dmitrovsky: 56 310 N, 37 440 E, 29 May 1947, V. Vehov s. n. (MW); loc. eodem, 56 200 E, 37 280 E, 13 Jun. 1926, N. Kats s. n. (MW). Domodedovsky: 55 290 N, 37 420 E, 05 Jun. 1915, P. Smirnov s. n. (MW). Kashirsky: 54 510 N, 38 100 E, 23 Aug. 1925, P. A. Smirnov s. n. (MW). Kolomensky: 55 110 N, 38 500 E, 13 May 1966, V. Tihomirov s. n. (MW). Leninsky: 55 320 N, 37 370 E, 29 Jul. 1915, P. Smirnov s. n. (MW); loc. eodem, 55 310 N, 37 370 E, 14 May 1914, P. Smirnov s. n. (MW). Lukhovitsky: 55 020 N, 38 550 E, 12 Aug. 1933, A. P. Shimanyuk s. n. (MW). Moscow Region: 15 Jun. 1887, I. N. Gorozhankin s. n. (MW); loc. eodem, 22 May 1888, M. I. Golenkin s. n. (MW); loc. eodem, 25 May 1891, P. V. Syuzev s. n. (MW); loc. eodem, 01 Aug. 1935, M. Lagutina s. n. (MW); loc. eodem, 03 Jun. 1954,

95

Shitova s. n. (MW); loc. eodem, 04 Jun. 1954, V. Ya. Andreev s. n. (MW); loc. eodem, 01 Jun. 1914, A. Razumov s. n. (MW); loc. eodem, 25 May 1907, N. Kuznetsov s. n. (MW); loc. eodem, 16 Jun. 1953, P. Zhudova s. n. (MW); loc. eodem, 04 Jun. 1959, A. V. Habarov s. n. (MW); loc. eodem, 09 Jun. 1969, E. Alexeev s. n. (MW); loc. eodem, 27 May 1969, I. Gubanov s. n. (MW); loc. eodem, 12 Jun. 1970, L. Suhonosenko s. n. (MW); loc. eodem, 12 Jun. 1970, L. Suhonosenko s. n. (MW); loc. eodem, 22 Jun. 1961, Tsedova s. n. (MW); loc. eodem, 01 Jun. 1961, Bogoslovskaya s. n. (MW); loc. eodem, 30 May 1946, T. Trofimov s. n. (MW); loc. eodem, 05 Jul. 1954, L. Paramonova s. n. (MW); loc. eodem, 11 Jun. 1972, I. A. Gubanov s. n. (MW); loc. eodem, 30 Jun. 1952, Roginskaya s. n. (MW); loc. eodem, 30 Jun. 1960, Mart’yanova s. n. (MW); loc. eodem, 06 Jun. 1961, A. V. Barsukova s. n. (MW); loc. eodem, 02 Jun. 1961, N. Kudryashova s. n. (MW); loc. eodem, 07 Jun. 1957, S. M. Razumovskiy s. n. (MW); loc. eodem, 14 Jun. 1952, Dombrovskaya s. n. (MW); loc. eodem, 15 May 1957, G. Zagorodnyaya s. n. (MW); loc. eodem, 07 Jun. 1956, T. Kamshilova s. n. (MW); loc. eodem, 17 May 1961, N. Shamardina s. n. (MW); loc. eodem, 08 Jun. 2003, M. Gonko s. n. (MW); loc. eodem, 01 Jul. 1948, Grebennikova s. n. (MW); loc. eodem, 22 Jul. 1961, Popkova s. n. (MW); loc. eodem, 03 Jun. 1954, Zhukova s. n. (MW); loc. eodem, 03 Jun. 1954, Deryabicheva s. n. (MW); loc. eodem, 14 Jun. 1969, L. Suhonosenko s. n. (MW); loc. eodem, 10 Aug. 1946, N. S. Smirnov s. n. (MW); loc. eodem, 07 Aug. 1947, N. Smirnov s. n. (MW); loc. eodem, 01 Sep. 1947, T. Trofimov s. n. (MW); loc. eodem, 11 Sep. 1946, T. Trofimov s. n. (MW); loc. eodem, 24 Aug. 1946, T. Trofimov s. n. (MW); loc. eodem, 17 Jul. 1928, V. Alehin s. n. (MW); loc. eodem, 07 Jun. 1946, P. Smirnov s. n. (MW); loc. eodem, 26 May 1947, T. Trofimov s. n. (MW); loc. eodem, 01 Jun. 1947, T. Trofimov s. n. (MW); loc. eodem, 04 Aug. 1947, T. Trofimov s. n. (MW); loc. eodem, 26 Sep. 1947, T. Trofimov s. n. (MW); loc. eodem, 21 Jun. 1948, Bogoyavlenskiy s. n. (MW); loc. eodem, 03 Aug. 1952, Garkavi s. n. (MW); loc. eodem, 10 Jun. 1968, Makaenkova s. n. (MW); loc. eodem, 02 Jun. 1971, N. A. Kirillina s. n. (MW); loc. eodem, 03 Jun. 1986, T. V. Korostyleva s. n. (MW); loc. eodem, 20 Jun. 1965, L. Urbantsova s. n. (MW). Moskva: 55 440 N, 37 240 E, 02 Jul. 1922, M. I. Nazarov s. n. (MW); loc. eodem, 55 350 N, 37 320 E, 06 Jun. 1924, V. Voroshilov s. n. (MW); loc. eodem, 55 510 N, 37 460 E, 07 Jun. 1945, P. Smirnov s. n. (MW); loc. eodem, 55 350 N, 37 330 E, 10 Jun. 1981, V. Kuvaev s. n. (MW); loc. eodem, 55 350 N, 37 340 E, 28 Jul. 1981, V. Kuvaev s. n. (MW); loc. eodem, 55 440 N, 37 240 E, 13 May 1912, A. N. Petunnikov s. n. (MW); loc. eodem, 05 Jun. 1860, A. N. Petunnikov s. n. (MW); loc. eodem, 27 Jun. 1885, A. N. Petunnikov s. n. (MW). Mozhaysky: 55 390 E, 35 410 E, 12 Jun. 1942, S. Levitskiy s. n. (MW).

96

Noginsky: 55 510 N, 38 410 E, 09 Jun. 1969, N. Vodolazskaya s. n. (MW). Odinsovsky: 55 430 N, 37 160 E, 20 Jun. 1939, Kozhevnikov s. n. (MW); loc. eodem, 55 410 N, 37 070 E, 26 May 1914, D. P. Syreyschikov s. n. (MW); loc. eodem, 55 420 N, 36 430 E, 22 Jul. 1940, Garkavi s. n. (MW). Odintsovsky: 55 420 N, 36 430 E, 22 Jul. 1940, Eh. Garkavi s. n. (MW). Pushkinsky: 56 010 N, 37 500 E, 12 Aug. 1907, D. P. Syreyschikov s. n. (MW). Ramensky: 55 330 N, 38 010 E, 02 Jul. 1924, M. I. Nazarov 9292 (MW); loc. eodem, 55 330 N, 38 260 E, 04 Jun. 1990, V. Tihomirov 7273 (MW). Ruzsky: 55 450 N, 36 300 E, 07 Jun. 1947, N. Smirnov s. n. (MW). Serpukhovsky: 54 510 N, 37 380 E, 02 Jun. 1971, I. A. Gubanov s. n. (MW); loc. eodem, 54 510 N, 37 330 E, 17 Jun. 1946, P. Smirnov s. n. (MW). Solnechnogorsky: 56 120 N, 37 010 E, 03 Jun. 1922, D. P. Syreyschikov s. n. (MW); loc. eodem, 56 110 N, 36 580 E, 13 Jun. 1923, D. P. Syreyschikov s. n. (MW); loc. eodem, 56 080 N, 37 100 E, 15 May 1948, T. Trofimov s. n. (MW). Stupinsky: 54 520 N, 38 110 E, 23 Aug. 1925, P. A. Smirnov s. n. (MW). Volokolamsky: 56 010 N, 36 130 E, 28 Jun. 1938, Garkavi s. n. (MW). Yegoryevsky: 55 160 N, 39 030 E, 23 May 1969, V. Novikov s. n. (MW). Zvenigorod: 29 May 1949, V. N. Sukachev 120 (MW). MURMANSK OBLAST, Tersky: 66 450 N, 33 460 E, 21 Jun. 2013, V. Borodulina s. n. (MW); loc. eodem, 66 150 N, 39 190 E, 22 Aug. 2006, Abramova L. A. s. n. (MW). Lovozersky: 66 230 N, 40 180 E, 15 Jul. 2015, Kopeina E. I. (MW). NIZHNY NOVGOROD OBLAST, Borsky: 56 210 N, 44 520 E, 28 May 1998, N. M. Reshetnikova s. n. (MW). Volodarsky: 56 120 N, 42 570 E, 15 Jul. 1926, А. Уранов s. n. (MW). NOVOSIBIRSK OBLAST, Narovchatsky: 53 520 N, 43 440 E, 24 May 1888, К. А. Космовский 590 (MW); loc. eodem, 24 May 1888, K. A. Kosmovskiy s. n. (MW). Toguchinsky: 54 350 N, 84 510 E, 20 Jun. 1975, N. Laschinskiy s. n. (MW). ORYOL OBLAST, Glazunovsky: 52 250 N, 36 100 E, 15 Jun. 1887, K. A. Kosmovskiy s. n. (MW). RYAZAN OBLAST, Kasimovsky: 55 030 N, 41 140 E, 15 Jul. 1972, V. K. Glazunova & Tihomirov 10302 (MW). Shatsky: 54 010 N, 41 440 E, 02 Jul. 1957, Vorontsova & Karpova s. n. (MW). Spassky, 54 470 N, 40 350 E, 09 Jun. 1968, V. Tihomirov, G. Davydova & V. Laschenkova 2511 (MW); loc. eodem, 54 390 N, 40 460 E, 23 Jun. 1928, V. Tihomirov & Hantimer s. n. (MW). SMOLENSK OBLAST, Demidovsky: 55 330 N, 31 450 E, 14 May 2000, N. M. Reshetnikova s. n. (MW). Yartsevsky: 55 060 N, 32 410 E, 12 Jun. 1957, Mul'tanovskaya s. n. (MW). STAVROPOL KRAI, Karachay-Cherkessia & Kabardino-Balkaria: 43 250 N, 41 390 E, 17 May 2006, A. S. Zernov 4769 (MW); loc. eodem, 43 500 N, 42 250 E, 12 May 2008, A. S. Zernov & I. P. Polyudchenkov 6680 (MW); loc. eodem, 06 Aug. 2005, L. B Kurasheva s. n. (MW); loc. eodem, 08 Jun. 1962,

6 Taxonomic Revision

Magulaev s. n. (MW); loc. eodem, 19 May 1908, Z. Atmanskih s. n. (MW); loc. eodem, 18 Jun. 1972, Chubatova s. n. (MW). SVERDLOVSK OBLAST, Novolyalinsky: 59 270 N, 59 170 E, 380 m, 22 Aug. 1975, V. Kuvaev 399-4 (MW). Severouralsk: 60 200 N, 59 130 E, 600 m, 25 Jun. 2002, A. Seregin U-122 (MW). TAMBOV OBLAST, Tambov: 52 430 N, 41 270 E, 07 May 1920, P. Smirnov s. n. (MW). Tambovsky: 52 480 N, 41 330 E, 25 Jun. 1920, A. A. Dmitriev s. n. (MW); loc. eodem, 52 300 N, 41 270 E, 09 Jun. 1920, M. A. Vadkovskaya s. n. (MW). Tomsky: 56 250 N, 84 520 E, 21 Jun. 1958, V. Kuvaev s. n. (MW). Verkhneketsky: 58 230 N, 84 060 E, 13 Jun 1982, G. A. Eliseeva s. n. (MW). Znamensky: 52 280 N, 41 150 E, 26 May 1917, P. Smirnow s. n. (MW). TULA OBLAST, Sheksninsky: 53 590 N, 37 080 E, 12 Jun. 1975, I. A. Gubanov s. n. (MW). Yasnogorsky: 54 220 N, 37 390 E, 24 May 1972, Alyushin 305 (MW). TUVA OBLAST, Kaa-Khemsky: 51 270 N, 95 360 E, 25 Jul. 1975, I. M. Krasnoborov 1129 (MW). Kyzylsky: 51 530 N, 94 350 E, 26 Jul. 1975, Korotkova E. 1288 (MW). TVER OBLAST, Tver: 56 510 N, 35 540 E, 21 May 1917, М. Назаров 2234 (MW); loc. eodem, 56 510 N, 35 550 E, 21 May 1917, M. Nazarov s. n. (MW); loc. eodem, 56 520 N, 35 550 E, A. A. Pletnev s. n. (MW). VLADIMIR OBLAST, Gorokhovetsky: 56 100 N, 42 230 E, 23 May 1971, V. Tihomirov & N. Oktyabreva 5789-1 (MW); loc. eodem, 56 120 N, 42 380 E, 14 May 1970, I. Gubanov, V. Novikov & T. Makeeva s. n. (MW). GusKhrustalny: 55 290 N, 40 180 E, 19 Jun. 1995, V. N. Tihomirov, S. V. Polevova & V. V. Ptushenko s. n. (MW); loc. eodem, 55 440 N, 40 390 E, 15 Jun. 1972, V. Tihomirov & N. Neischenko 10303 (MW); loc. eodem, 55 350 N, 41 160 E, 20 Jul. 1976, V. S. Novikov & N. V. Lavrova s. n. (MW). Kovrovsky: 56 250 N, 41 290 E, 09 Jul. 2006, A. Seregin 2616 (MW). Melenkovsky: 55 190 N, 41 280 E, 04 Aug. 1976, L. F. Volosnova s. n. (MW); loc. eodem, 55 220 N, 41 460 E, 23 May 1914, M. I. Nazarov 5008 (MW); loc. eodem, 55 230 N, 41 470 E, 23 May 1912, M. Nazarov 604 (MW); loc. eodem, 55 200 N, 41 370 E, 15 May 1914, M. I. Nazarov 4931 (MW). Petushinsky: 55 490 N, 39 220 E, 02 Jun. 1969, I. Gubanov, V. Novikov & V. Tihomirov s. n. (MW). Ramensky: 55 330 N, 38 010 E, 02 Jul. 1924, М. И. Назаров 9292 (MW). Ruzsky: 55 450 N, 36 300 E, 07 Jun. 1947, Н. Смирнов s. n. (MW). Serpukhovsky: 54 510 N, 37 330 E, 07 Jun. 1946, П. Смирнов s. n. (MW). Sobinsky: 56 040 N, 40 060 E, 16 Aug. 2001, A. Seregin 954 s. n. (MW). Sudogodsky: 55 440 N, 41 080 E, 30 Jun. 1972, V. Tihomirov & F. Rahmatulina 10298 (MW); loc. eodem, 55 510 N, 40 420 E, 6 Jun. 1972, V. Tihomirov & F. Rahmatulina 10299 (MW); loc. eodem, 55 530 N, 40 450 E, 5 Jun. 1972, V. Tihomirov, E. Klyuykov & A. Chichev 10301 (MW). Suzdalsky: 56 340 N, 40 320 E, 02 Jun. 2006, A. Seregin

6.1 Section Paris

2485 (MW). Vyaznikovsky: 56 060 N, 41 490 E, 16 Jun. 1971, V. Tihomirov, E. Alexeev & T. Zhirnova 5771 (MW). VOLOGDA OBLAST, Kirillovsky: 59 550 N, 38 330 E, 14 Aug. 1994, Shvedchikova N. s. n. (MW); loc. eodem, 59 520 N, 38 160 E, 15 Aug. 1994, Shvedchikova N. s. n. (MW). YAROSLAVL OBLAST, Baikal & Transbaikal Region: 30 Jun. 1911, M. Korotkiy s. n. (MW); loc. eodem, 09 Jun. 1953, I. Maslova s. n. (MW) ; loc. eodem, 14 Jul. 1967, Афонина s. n. (MW); loc. eodem, 28 May 1912, K. Meyer s. n. (MW); loc. eodem, 27 Jul. 2002, V. S. Sun Den-Ho s. n. (MW); loc. eodem, 08 Jul. 1976, Shibanova s. n. (MW); loc. eodem, 08 Jun. 1915, Yu. Tsinzerling s. n. (MW). Nekouzsky: 58 030 N, 38 140 E, 14 Jun. 2014, Eh. V. Garin s. n. (MW). Pereslavsky: 56 410 N, 38 550 E, 09 May 2010, S. Polevova s. n. (MW); loc. eodem, 56 430 N, 38 460 E, 02 Jun. 1930, E. Sidorova s. n. (MW); loc. eodem, 59 070 N, 46 010 E, 14 May 1990, Zhmylev s. n. (MW). SLOVAKIA, BANSKA BYSTRICA: 48 450 N, 19 0 53 E, 1111 m, 08 Aug. 2009, T. Dürbye & A. Kirchhoff 4631 (B). SPAIN, CUENCA: G. López s. n. (MA). HUESCA, Bielsa: Del Campo s. n. (MA). ASTURIAS: 01 Jan. 1807, Bernabé Salcedo s. n. (MA). LÉRIDA: Neé & Villiers s. n. (MA). LUGO, Pedrafita do Cebreiro: 22 Jul. 2010, M. Serrano R. Carbajal s. n. (SANT). ZAMORA, Requejo: 42 010 N, 06 480 W, 1323 m, David Losada s. n. (MA). SWEDEN, DALARNA, Orsa: 01 Jun. 2000, Astrid Björkman s. n. (BG). GOTHEBORG, Rya Skog: 28 May 1917, Anders Holmertz s. n. (O). HÄLSINGLAND: 01 Aug. 1913, H. F. Lundberg s. n. (O). NORRBOTTEN, Jokkmokk: 18 Jul. 1965, Stud. biol. Rheno-Trai. 1793 (NHN). ÖSTERGÖTLAND, Krokek: 30 May 1907, Ebbe Linde s. n. (BG). SKÅNE: 14 May 1894, Carl Edv. Foisack s. n. (O). SÖDERMANLAND, Oxelösund: 01 Jun. 1906, Erik Asplund s. n. (BG); loc. eodem, 03 Jul. 1902, Erik Asplund s. n. (BG). STOCKHOLM, Djurö: 15 Jun. 1945, Carl Lundin s. n. (O). Singö: 23 Jul. 1921, Fredr. Sundstedt s. n. (O). UPPSALA, Bondkyrka: 2 Jun. 1925, Erik Asplund s. n. (O). VÄSTERGÖTLAND: 01 Jun. 1899, C. G. H. Thedenius s. n. (O). SWITZERLAND, GLARUS, Klontalersee: 850 m, 08 Aug. 1973, Veldwerk groer LEP23016 (NHN). VALAIS: 19 Jul. 1993, Herb Hekker F s. n. (NHN). VAUD, Gryon: 1050 m, 19 May 1948, R. T. Simon Thomas 1113 (NHN). UKRAINE, NORTH UKRAINIAN REGION: 09 Jul. 1915, K. Zalesskiy s. n. (MW); loc. eodem, 16 Jun. 1889, P. Sanicki s. n. (MW). SOUTH UKRAINIAN REGION: 49 150 N, 28 260 E, 06 Jul. 1927, I. A. Borzova s. n. (MW); loc. eodem, 24 Jul. 1927, I. Borzova s. n. (MW); loc. eodem, 49 020 N, 28 180 E, 07 Jun. 1927, I. A. Borzova s. n. (MW); loc. eodem, 49 190 N, 28 290 E, 17 Jul. 1927, Z. M. Snyatinovskaya s. n. (MW); loc. eodem, 27 May 1928,

97

G. Przhibishevskiy s. n. (MW). WEST UKRAINIAN REGION: 25 Jun. 1970, Makeeva T. A. s. n. (MW). UNITED KINGDOM, ENGLAND, Essex: 30 Dec. 1899, British Museum s. n. (MNHNL). Lincolnshire: 53 350 N, 00 160 W, 01 May 1870, Frederick Arnold Lees s. n. (BM); loc. eodem, 52 550 N, 00 200 W, 19 Jul. 1893, Frank Simpson Alston s. n. (BM); loc. eodem, 55 130 N, 00 390 W, 28 May 1955, Cole Colln. s. n. (BM); loc. eodem, 27 May 1856, Bogg Colln s. n. (BM). Somerset: 11 Jun. 1955, G. H. BRYAN s. n. (TAM); loc. eodem, 30 Jun. 1985, G. H. Bryan s. n. (TAM). SCOTLAND, Perthshire: Don George 163 (E). 4. Paris verticillata M. Bieb., Fl. Taur. -Caucas. 3: 287. 1819; Hand.-Mazz., Symb. Sin. 7 (5): 1214. 1936; Hara, Bot. Mag. Tokyo 52: 513. 1938; Hara, Journ. Fac. Sci. Univ. Tokyo, sect. 3, Bot. 10 (10): 165. 1969; Inst. Bot. Bor. -Occid. Fl. Tsining. 1: 353. 1976; Icon. Corm. Sin. 5: 515. 1976; Wang et Tang, Fl. Reip. Pop. Sin. 15: 88. 1978; H. Li, Bull. Bot. Res. Harbin 6 (l): 137. 1986; B. Mitchell, Plantsman 9 (2): 85. 1987; H. Li, The Genus Paris (Trilliaceae) 61. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 93. 2000. Paris obovata Ledeb., Icon. Pl. 1: t. 16. 1828.  Paris quadrifolia L. var. obovata (Ledeb.) Regel et Tiling, Mem. Soc. Philom. Cent. (Paris) 24: 282. 1888.  Paris verticillata M. Bieb. var. obovata (Ledeb.) Hara, Journ. Fac. Sci. Univ. Tokyo, sect. 3, Bot. 10: 165. 1969. Type: Russia, Irkutsk, s. n. (HAL). Paris hexaphylla Cham., Linnaea 6: 586. 1831.  Paris quadrifolia L. var. hexaphylla (Cham.) Fedtsch, Trudy Imp. S. -Peterburgsk. Bot. Sada 31: 121. 1912. Paris dahurica Fisch. ex Turcz., Bull. Soc. Nat. Mosc. 27 (2): 105. 1854.  Paris quadrifolia L. var. dahurica (Fisch.) Franch., Nouv. Arch. Mus. Paris. Ser. 2, 10: 96. 1888. Paris manshurica Kom., Key Pl. Far. East. Reg. URSS 1: 385. 1931.  Paris hexaphylla Cham. var. manshurica (Kom.) Vorosch., Byull. Glavn. Bot. Sada 84: 31. 1972. Perennial herb. Rhizome slender, usually branched, with fibrous roots on nodes, 15.0–40.0 cm long, 2.5–4.0 mm in diameter. Stem erect, cylindrical, green or purple, 14.0–30.0 cm. Leaves 6–9 in a terminal whorl, subsessile; leaf blades narrowly oblong, obovate or obovata-lanceolate, green, papyraceous, acuminated at apex, base cuneate, ca. 5.0–13.0 cm  1.5–4.0 cm; lateral veins 1 pair, basally developed, net veins inconspicuous. Flower solitary, 4- to 6-merous; developing from the top of stem; pedicel green, erect, 5.5–15.0 cm long; sepals green, ovate-lanceolate, 2.5–5.0 cm  0.7–2.0 cm; petals linear or filiform, green, 1.5–4.0 cm long, shorter than sepals. Stamens 2  petal number, arranged in 2 whorls; filaments yellowish green or dark red, 4.0–8.0 mm long; anthers yellow, 5.5–12.0 mm, dehiscing by a lateral slit; free portion of connective yellowish-green, 4.0–8.0 mm. Ovary subglobose, purple,

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4 (or 5)-loculed with axial placentation; style purple, short; stigmas 4–6, slender, erect, 4.0–12.0 mm, outward curved at fruiting. Berry purplish black, globose, indehiscent, ca. 7.0–10.0 mm in diameter in diameter. Seeds ovoid, brown, 2–3 mm in diameter, without aril or sarcotesta (Figs. 6.6 and 6.7). Phenology: flowering May–June; fruiting from July to September. Habitats: deciduous broad-leaved and coniferous forests; 600–3600 m. Distribution: China. Beijing (Fangshan, Fengtai, Mentougou, Yanqing), Chongqing (Kaizhou, Nanchuan), Gansu (Huating, Kangxian, Minxian, Xiahe, Wenxian, Wudu, Zhouqu), Hebei (Chengde, Chicheng, Laishui, Mount Xiaowutai, Neiqiu, Pingquan, Weichang, Wu’an, Xinglong, Yuxian, Zhuolu, Zhengding), Heilongjiang (Dailing, Hulin, Huma, Jiayin, Jinshantun, Mishan, Ning’an, Raohe, Shangzhi, Yichun), Henan (Huixian, Lingbao, Ruyang, Songxian), Jilin (Antu, Changbai, Fusong, Helong, Huadian, Jiaohe, Linjiang, Panshi, Yanbian), Liaoning (Anshan, Benxi, Fengcheng, Fushun, Huanren, Kaiyuan, Kuandian, Lingyuan, Qingyuan, Xifeng), Nei Mongol (Arxan, Ergun, Genhe, Oroqen, Ulanhot, Yakeshi, Zhuozi), Ningxia (Jingyuan), Shaanxi (Fengxian, Foping, Huayin, Liuba, Longxian, Meixian, Ningshan, Qinling, Shanyang, Shiquan, Taibai, Xi’an, Yangxian, Zhashui, Zhen’an), Shanxi (Anze, Huozhou, Jiaocheng, Jiexiu, Lishi, Lingshi, Ningwu, Qinshui, Qinyuan, Wutai, Yangcheng, Yanhu, Yicheng, Yongji, Yuanqu). Japan (Fukushima, Hokkaido, Nagana, Shizuoka, Suruga, Yamanashi). Kazakhstan (Western Altai Mountains). Korean Peninsula (Sobaeksan). Mongolia. Russia (Amur, Khabarovsk, Krasnoyarsk, Sakhalin, Sakha, Primorsky, Zabaykalsky, Irkutsk). Notes: Bieberstein (1819) did not designate the holotype of P. verticillata. This issue may have been ignored by Franchet (1888a), Hara (1969), and Li (1998) in their taxonomic revisions of the genus. Unfortunately, no specimen examined by Bieberstein has been found to date. The lectotypfication of this species remains to be resolved in the future. Additional specimens examined. CHINA, BEIJING, Fangshan: 13 Aug. 1975, Wang JW s. n. (PEY). Fengtai: 18 Aug. 1951, Yang CG 570 (PE). Mentougou: 25 Aug. 1989, Zheng L 062997 (BNU); loc. eodem, 21 Aug. 1989, Peng YL 062999 (BNU); loc. eodem, Aug. 1989, Huang QQ 062998 (BNU); loc. eodem, 13 Aug. 1991, Kang N 062966 (BNU); loc. eodem, 17 Aug. 1989, Yang GJ 062996 (BNU); loc. eodem, 17 Aug. 1991, Beijing Normal University 062963 (BNU); loc. eodem, 24 Aug. 1990, Zhang CH 062964 (BNU); loc. eodem, 11 Jul. 1984, Yin SM 062983 (BNU); loc. eodem, 05 Jul. 1984, Wang XH 062980 (BNU); loc. eodem, Wang YN 062990 (BNU); loc. eodem, 01 Jul. 1982, Beijing Normal University 062977 (BNU); loc. eodem,

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10 Jul. 2017, Liao WJ, Tian X & Zhou JL NS-059 (JJF); loc. eodem, 11 Jul. 2017, Yuan MM, Wu YJ & Zhang L 170711047 (JJF). Yanqing: 26 Jun. 1984, Group 3 3145 (BJTC); loc. eodem, Jun. 1984, Group 4 4100 (BJTC); loc. eodem, Jun. 1984, Group 5 5137 (BJTC); loc. eodem, 29 Jun. 1984, Group 1 1113 (BJTC); loc. eodem, 29 Apr. 1984, Group 8 8087 (BJTC). CHONGQING, Kaizhou: 17 Apr. 2004, Liu ZY 2041081 (IMC). Nanchuan: 23 May 2014, Liu ZY 20141553 (IMC); loc. eodem, 16 Jun. 1996, Liu ZY 962476 (IMC); loc. eodem, 08 May 1982, Liu ZY & Tan SX 3186 (IMC). GANSU, Huating: 17 May 2014, He Y & Hao JC GSL2014050637 (BNU). Kangxian: 08 May 1963, He YQ & Tang CL 394 (WUK). Minxian: 23 May 1957, Huanghe River Expedition 3203 (NAS, PE); loc. eodem, 05 Jun. 1951, Wang ZB 14066 (WUK); loc. eodem, 23 May 1957, Taohe Expedition 3203 (PE). Xiahe: 03 Jul. 1937, Fu KT 975 (WUK, PE); loc. eodem, 01 Jul. 1937, Wang TP 6950 (WUK, PE). Wenxian: 16 Jul. 1959, Zhang ZY 7002 (WUK); loc. eodem, 03 May 1964, Wang ZB 19190 (WUK). Wudu: 12 May 1959, Zhang ZY 1918 (WUK, LBG); loc. eodem, 07 Jun. 1954, Zhang ZY 3928 (WUK). Zhouqu: 18 Sep. 1958, He YQ 626 (WUK); loc. eodem, 21 May 1959, Jiang S et al. 00409 (PE). HEBEI, Chengde: 1959, Nankai University 0035 (PE); loc. eodem, 11 Jun. 1994, Hu JP 3 (BJTC); loc. eodem, 12 Jul. 2006, Liu SW 0411009 (BJTC); loc. eodem, 12 Jul. 2006, Li FY 0406020 (BJTC); loc. eodem, 25 Jun. 2001, Hao X 058 (BJTC); loc. eodem, 26 Jun. 1997, Lin L 9605041 (BJTC). Chicheng: Jul. 1976, Wang JW s. n. (PEY); loc. eodem, 19 Jul. 2007, Li N 200702049 (PEM); loc. eodem, 19 Jul. 2007, Sun JW, Wen EY & Hu XX 200701167 (PEM). Laishui: 03 Jun. 1934, Liu KM 2299 (PE); loc. eodem, 31 May 1934, Liu KM 2252 (PE); loc. eodem, 08 Jul. 1934, Liu KM 2725 (PE). Mount Xiaowutai: 08 May 1935, Liu Y 11317 (PEY); loc. eodem, 18 Jul. 1931, Wang TP 697 (WUK); loc. eodem, 29 May 1930, Kung HW 162 (WUK). Neiqiu: 30 Jul. 1950, Liu Y & Liu XY 13230 (PE); loc. eodem, Aug. 1950, Liu XY 1241 (PE); loc. eodem, 30 Jul. 1950, Liu Y 13230 (NAS); loc. eodem, Aug. 1950, Liu XY 1241 (NAS); loc. eodem, 05 Jun. 1951, Liu XY 322 (NAS, PE). Pingquan: 17 Jun. 2014, Wang ZT, Qu S & Xu LS 140464 (PE); loc. eodem, 18 Jun. 2014, Wang ZT, Qu S & Xu LS 140482 (PE); loc. eodem, 22 May 2014, Group 4 130823140522014LY (HBNU). Weichang: 18 Jun. 2005, Liu LQ et al. 0019 (PE). Wu’an: 04 Jul. 1958, Guan KJ 5836 (PE); loc. eodem, 16 May 2014, Group 15 130481140516017LY (HBNU). Xinglong: 27 Jul. 1956, Herbaria 2203 (PE); loc. eodem, 29 Jun. 1986, Group 6 040 (BJTC); loc. eodem, 06 Jul. 1985, Group 5 s. n. (BJTC); loc. eodem, 29 Jul. 1986, Group 3 030 (BJTC); loc. eodem, 17 Jun. 1981, Group C 0065 (BJTC); loc. eodem, 16 Jun. 1981, Group 4 0032 (BJTC); loc. eodem, 04 Sep. 1981. Bao PY 671

6.1 Section Paris

Fig. 6.6 Paris verticillata (drawn by M. Shen): rhizome and stem (a), aerial shoot (b), and berry (c)

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100

Fig. 6.7 Rhizome (a), flower (b), mature berry (c), and seeds (d) of Paris verticillata

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6.1 Section Paris

(BJTC); loc. eodem 16 Jun. 1981, Group 2 33 (BJTC); loc. eodem, 21 Jun.2000, Sun Z 2 (BJTC); loc. eodem, 08 Jul. 1985, Group 2 053 (BJTC); loc. eodem, 16 Jun. 1981, Group A 0042 (BJTC); loc. eodem, Group 4 021 (BJTC); loc. eodem, 17 Jun. 2000, Group 1 5 (BJTC); loc. eodem, 11 Jun. 1993, Group 2 92¼001 (BJTC); loc. eodem, 11 Jun. 1993, Group 4 924002 (BJTC); loc. eodem, 11 Jun. 1993, Group 1 921011 (BJTC); loc. eodem, 11 Jun. 1993, Group 3 923001 (BJTC); loc. eodem, 21 Jun. 1998, Yue C 9703014 (BJTC); loc. eodem, 19 Jun. 1998, Xu X 97046 (BJTC). Yuxian: 18 Jul. 1931, Wang TP 697 (PE); loc. eodem, 29 May 1930, Kung HW 162 (PE); loc. eodem, 04 Jul. 1936, Wu & Yang 2672 (PE); loc. eodem, 17 Jun. 1959, Li TQ 841 (PE); loc. eodem, Aug. 1929, Li JF 10809 (PE); loc. eodem, 08 Jul. 1934, Wang CW 61577 (PE). Zhuolu: 19 May 1955, Yang CG 1523 (NAS, PE); loc. eodem, 09 Jun. 1953, Yang CG 1290 (PE); loc. eodem, 23 May 1952, Yang CG 831 (PE). Zhengding: 18 Aug. 1951, Yang CG 57 (PE). HEILONGJIANG, Dailing: 29 Jul. 2014, Wang Y 075 (JMSU). Hulin: 17 Jul. 1980, Li SX 3222 (IFP). Huma: 04 Aug. 1950, Han LF 670 (IFP); loc. eodem, 27 Jul. 1986, Li SX 7290 (IFP); loc. eodem, 07 Jul. 1986, Fang ZF 3947 (IFP); loc. eodem, 16 Jul. 1950, Zhu YC 156 (IFP). Jiayin: 01 Jun. 1983, Ding TY 830338 (IFP). Jinshantun: 05 Aug. 2014, Wang Y 709 (JMSU); loc. eodem, 20 Jul. 2014, Wang CB 201408139 (JMSU). Mishan: 12 Jun. 1982, Jiamusi University 82053 (JMSU). Ning’an: 22 Jun. 2013, Zhang S 53 (JMSU); loc. eodem, 23 Jun. 2013, Gao TT 1094 (JMSU); loc. eodem, 25. Jun. 2013, Gu CY 61 (JMSU); loc. eodem, 22 Jun. 2013, Qi YQ 5088 (JMSU); loc. eodem, 20 Jul. 2014, Wang CB 201408139 (JMSU); loc. eodem, 22 Jul. 1975, Fu PY 3374 (IFP); loc. eodem, 13 Jul. 2016, Gao HS 3230 (JMSU); loc. eodem, 13 Jul. 2016, Liu W 4357 (JMSU); loc. eodem, 13 Jul. 2016, Liu Y 71 (JMSU); 13 Jul. 2016, Guan YZ 84 (JMSU); loc. eodem, 12 Jul. 2016, Liu XH 91 (JMSU); loc. eodem, 19 Jul. 2016, Zhang SJ 160701046 (JMSU); loc. eodem, 13 Jul. 2016, Man ZX 92 (JMSU); loc. eodem, 30 Jun. 2007, Teng ZH 27 (JMSU); loc. eodem, 02 Jun. 1954, Wang GZ 1771 (IFP). Raohe: 19 Jul. 1980, Li JY 3218 (IFP). Shangzhi: 28 May 1949, Mitsuzo Noda s. n. (IFP); loc. eodem, Yu JQ 30 (JMSU); loc. eodem, 04. Jul. 2008, Gao Y 027 (JMSU); loc. eodem, 02 Jul. 2008, Li YY 99 (JMSU); loc. eodem, 29 Jun. 2008, Wang Y 20 (JMSU); loc. eodem, 01 Jul. 2008, Zhang Y 008 (JMSU); loc. eodem, 08. Jul. 2006, Han X 083 (JMSU); loc. eodem, 30 Jun. 2007, Chang YY 50 (JMSU); loc. eodem, 29 Jun. 2007, Hong S 11 (JMSU); loc. eodem, 01 Jul. 2007, Tan B 69 (JMSU); loc. eodem, 17 Jun. 2007, Yang LL 19 (JMSU). Yichun: 08 Jul. 2008, Wang CB 08151 (JMSU); loc. eodem, 01 Jul. 2008, Cai XQ 0701016 (JMSU); loc. eodem, 30 May 2017, Yang N 053018 (JMSU); loc. eodem, 31 May 2014, Xu ZQ 0198 (JMSU); loc. eodem, 09 Jun. 1985, Ding TY 1893

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(IFP); loc. eodem, 09 Jul. 1983, Ding TY 830595 (IFP); loc. eodem, 08 Jul. 1956, Liu SE 7054 (IFP); loc. eodem, 03 Aug. 1956, Liu SE 7892 (IFP); loc. eodem, 24 Aug. 1962, Liu CQ 400 (IFP); loc. eodem, 25 Jul. 1951, Liu SE 3387 (IFP); loc. eodem, 04 Aug. 1959, Wang W 783 (IFP); loc. eodem, 02 Aug. 1987, Ding TY 1981 (IFP); loc. eodem, 03 Aug. 1956, Liu SE et al. 7892 (PE); loc. eodem, 08. Jul. 1956, Liu SE et al. 054 (PE); loc. eodem, 08 Jul. 1956, Liu SE et al. 3313 (PE). HENAN, Huixian: Jul. 1980, He RB 014 (HENU); loc. eodem, Jul. 1980, He RB 0011 (HENU); loc. eodem, Jul. 1980, He RB 0012 (HENU); loc. eodem, May 1974, Xu CX 064 (HENU); loc. eodem, May 1974, Xu CX 014 (HENU); loc. eodem, Jun. 1959, Xu CX 015 (HENU); loc. eodem, Jun. 1959, Xu CX 0151 (HENU); loc. eodem, Jun. 1959, Xu CX 0147 (HENU); loc. eodem, Jun. 1959, He RB 20600 (HENU); loc. eodem, Jun. 1959, He RB 0148 (HENU); loc. eodem, Jun. 1959, He RB 616 (HENU); loc. eodem, Jun. 1959, He RB 0241 (HENU). Lingbao: 16 Aug. 2016, Zhu CS et al. 160816115 (AU); loc. eodem, 16 Aug. 2016, Hou XL, Xin WW & Zhang RP 549 (AU). Ruyang: 01 May 2006, Zhu CS 51023 (IBSC). Songxian: 30 Aug. 1983, Plant Resources Expedition L0341 (PE). JILIN, Antu: 03 Sep. 1959, Fu PY 1305 (WUK, IFP); loc. eodem, 05 Aug. 1982, Li SX 5163 (IFP); loc. eodem, 05 Jun. 1960, Wang CS 4576 (IFP); loc. eodem, 03 Sep. 1959, Li JY 607 (IFP); loc. eodem, 14 Jul. 1963, Wang W 1912 (IFP); loc. eodem, 10 Jun. 1960, Wang CS 4740 (IFP); loc. eodem, 11 Aug. 1979, Zhao SD 2507 (IFP); loc. eodem, 01 Jun. 1986, Liu QJ 107 (IFP); loc. eodem, 27 May 1984, Fang ZF 3204 (IFP); loc. eodem, 08 Sep. 1959, Fu PY et al. 1805 (PE); loc. eodem, 03 Aug. 2011, Li P LP1108015 (CSH). Changbai: 24 Aug. 1963, Li SX 839 (IFP); loc. eodem, 18 Aug. 1986, Yuan HD 34027 (PE). Fusong: 14 Jul. 1950, Mitsuzo Noda 79 (IFP); loc. eodem, 03 Aug. 1987, Fu PY 4710 (IFP); loc. eodem, 15 Aug. 1986, Hong DY et al. 33864 (PE); loc. eodem, 14 Aug. 1986, Hong DY et al. 33785 (PE); loc. eodem, 04 Aug. 1986, Hong DY et al. 33348 (PE); loc. eodem, 06 Jun. 1962, Li CH 98 (IGA); loc. eodem, 06 Jun. 1962, Wang FX 98 (IGA); loc. eodem, 01 Jun. 1962, Yi FK 98 (IGA); loc. eodem, 03 May 2016, Zhong X ZX03904 (CSH). Helong: 08 Sep. 1959, No. 2 Yanbian Expedition 656 (PE). Huadian: 06 Aug. 1950, Ma YQ 7 (PEY); loc. eodem, 20 May 1951, Ma YJ 345 (PEY); loc. eodem, 19 May 1925, Sato J 9186 (IFP); loc. eodem, 03 Aug. 1957, Qian JJ 653 (PE); loc. eodem, 01 Jun. 1962, Temperate Forests Expedition 016 (PE); loc. eodem, 08 Jun. 1931, Kung HW 1469 (PE); loc. eodem, 16 Jul. 1950, Zhu YC, Baranov & Zhao DC 156 (PE); loc. eodem, 09 Jun. 1931, Kung HW 1511 (PE); loc. eodem, 20 Jun. 1955, Dongling Expedition 265 (PE). Jiaohe: 30 May 1954, Liu SE et al. 5702 (WUK). Linjiang: 13 Jun. 1950, Wu ZY et al. 813 (PE); loc. eodem, 22 Jun. 1950, Liu SE et al. 957 (PE). Panshi: 10 May 2017, An HC 016 (JJF). Yanbian: 20 Jun. 2016, Zheng XM & Lin

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HY HZU13679 (ZJU). LIAONING, Anshan: 21 May 1975, Fu PY 3090 (IFP); loc. eodem, 27 May 1956, Zhu YC 400 (IFP); loc. eodem, 29 May 1950, Liu SE 588 (IFP); loc. eodem, 16 May 1961, Yang RJ et al. B12 (SYAUF). Benxi: 28 Jun. 1963, Li SX 640 (IFP); loc. eodem, 13 Aug. 1965, Lin CQ 964 (IFP); loc. eodem, 19 May 1950, Mitsuzo Noda 569 (IFP); loc. eodem, 19 May 1950, Han CQ 280 (IFP). Fengcheng: 14 May 1983, Li SX 5625 (IFP); loc. eodem, 18 May 1960, Deng YC 175 (IFP); loc. eodem, 06 Aug. 2009, Li ZY 231 (IFP). Fushun: Ye J B29 (SYAUF). Huanren: 23 Aug. 1964, Cui SC 211 (IFP); loc. eodem, 11 Jul. 1985, Li SX 6724 (IFP). Kaiyuan: 06 Jun. 1961, Deng YC 114 (IFP). Kuandian: 28 May 1984, Li SX 6443 (IFP); loc. eodem, 30 Aug. 1978, Li SY 7822 (IFP). Lingyuan: 04 Jul. 1959, Li SX 316 (IFP). Qingyuan: 25 Jul. 2003, Cao W & Zhu GX 217 (PE). Xifeng: 18. May 1974, Fu PY 2950 (IFP); loc. eodem, 19 Jun. 1983, Li SX 5815 (IFP); loc. eodem, 18 Jun. 1982, Xu WD 18 (IFP); loc. eodem, 16 May 1984, Li SX 6174 (IFP). NEI MONGOL, Arxan: 30 Jun. 2013, Zhang CL 0244 (YAK); loc. eodem, 19 Jun. 1963, Fu PY 2061 (IFP); loc. eodem, 21 Aug. 1987, Cui XJ 74 (IFP). Ergun: 10 Jun. 2014, Zhang XJ 0098 (YAK); loc. eodem, 07 Aug. 2014, Wang YY 086 (YAK). Genhe: 01 Jul. 1985, Zhang CL 0882 (YAK); loc. eodem, 10 Jun. 2014, Zhang CL 0056 (YAK); loc. eodem, 16 Aug. 1951, Wang Z 2027 (IFP); loc. eodem, 17 Oct. 1951, Wang Z 1482 (IFP). Oroqen: 05 Jun. 2015, Zhang CL 0503 (YAK). Ulanhot: 24 Jun. 2009, Fu DZ et al. 09062444 (PE). Yakeshi: 07 Jun. 2015, Zhang CL 0098 (YAK); loc. eodem, 27 Jul. 1954, Wang GZ 2841 (IFP). Zhuozi: 25 Aug. 2015, Hong M 150921150825086 (IMMU). NINGXIA, Jingyuan: 30 May 1972, Ningxia Chinese Medicinal Herbs Survey 3-0027 (WUK). SHAANXI, Fengxian: 21 Sep. 1951, Liu JM 10696 (WUK). Foping: 11 Jun. 1952, Fu KJ 4474 (WUK, IBSC). Huayin: 17 Aug. 1966, Wang ZB 19763 (WUK); loc. eodem, 08 Aug. 1932, Hao KS 4015 (WUK, PE). Liuba: 03 Apr. 1970, Shaanxi Chinese Medicinal Herbs Survey 798 (WUK). Longxian:10 Aug. 2013, Liu QR & He Y GSL201308087 (BNU); loc. eodem, 27 May 1983, Yang JX 4391 (WUK). Meixian: 15 Jul. 1938, Liou TN & Tsoong PC 2192 (WUK); loc. eodem, 21 May 1971, Wang ZB 19854 (WUK); loc. eodem, 29 Jun. 1999, Zhu et al. 1353 (PE); loc. eodem, 22 Jun. 2000, Zhu et al. 2431 (PE). Ningshan: 01 Jun. 1969, Xing JQ 18066 (WUK); loc. eodem, 28 May 1959, Xing JQ 3746 (WUK); loc. eodem, 25 Aug. 2009, Jiang ZM, Du C & Liu PL 1299 (WUK); loc. eodem, 17 Jul. 2008, Jiang ZM, Du C & Liu PL 98 (WUK); loc. eodem, 24 May 1959, Xing JQ 2234 (IBSC); loc. eodem, 10 May 1988, Cui TC 1097 (PE). Qinling: 02 Jul. 2015, Qin J 201503084 (XJTU). Shanyang: 27 Jun. 1957, Herbarium 190 (WUK). Shiquan: 28 May 1959, Xing JF 3746 (NAS). Taibai: 11 Aug. 1977, Guo YH & Hu ZX 530 (WUK, IBSC); loc. eodem, 04 Jun. 1965, Tang CL 1483 (WUK, IBSC); loc. eodem, 18 Jul.

6 Taxonomic Revision

1963, Liang YM 112 (WUK); loc. eodem, 09 Jul. 1957, Fu KJ 9414 (WUK); loc. eodem, 02 Aug. 1956, Qingling Expedition 460 (WUK); loc. eodem, 27 Apr. 1939, Fu KT 2521 (PE); loc. eodem, 14 Jul. 1938, Liu T & Tsoong PC 2110 (PE); loc. eodem, 03 Aug. 1933, Wang TP 1751 (PE). Xi’an: Liu FY 8513159 (XJTU). Yangxian: 06 Aug. 1959, Yang JX 780 (WUK). Zhashui: 13 Jul. 2012, Li SF et al. 17175 (XBGH); loc. eodem, 24 May 2013, Li SF et al. 17769 (XBGH). Zhen’an: 05 Jun. 1973, Hou XX & Guo YH 826 (WUK, IBSC). SHANXI, Anze: 09 Jul. 2016, Zhang N 1389 (SXTCM). Huozhou: 09 Jun. 1957, Huanghe River Expedition 788 (PE); loc. eodem, 09 Jun. 1957, Huanghe River Expedition 788 (NAS, WUK). Jiaocheng: 08 Jul. 2008, Chai L 5-039 (SXU); loc. eodem, 07 Jul. 2008, Wu YL 1-055 (SXU). Jiexiu: 14 Jun. 1959, Liu XY 5240 (WUK); loc. eodem, 21 Jun. 1957, Liu JM 1311 (PE). Lishi: 05 Jul. 1955, Huanghe River Expedition 2433 (WUK, PE); loc. eodem, 03 Jun. 1955, Huanghe River Expedition 1458 (PE). Lingshi: Class 2 of 82nd Botany 850498 (SXU). Ningwu: 14 Aug. 1929, Hsia WY 1578 (PE). Qinshui: 04 Aug. 1985, Ding LM & Wang HL 858483 (SXU). Qinyuan: 25 Jul. 1984, Shanxi Expedition 2712 (WUK); loc. eodem, 09 Aug. 1985, Li BL 830393 (SXU). Wutai: 15 Jul. 1959, Chen YL 1625 (PE). Yangcheng: 19 May 1959, Bao SY & Yan SJ 130 (PE). Yanhu: 25 May 1957 Huanghe River Expedition 424 (NAS). Yicheng: 08 May 1957, Huanghe River Expedition 0034 (PE). Yongji: 21 May 1962, Liu TW 0166 (PE); loc. eodem, 25 May 1957, Fenhe Expedition 424 (PE). Yuanqu: 13 Jul. 1984, Shanxi Expedition 2261 (WUK); loc. eodem, 13 Jul. 1984, Shanxi Expedition 2356 (WUK). JAPAN, FUKUSHIMA, Minamisōma: 37 450 N, 140 0 43 E, 490 m, 22 May 1993, Nji Toyoda & Koji Yonekura 93288 (HAST); loc. eodem, 37 450 N, 140 430 E, 490 m, 08 May 1998, Koji Yonekura 98550 (HAST). HOKKAIDO: 31 May 1957, Murata G. & Shimizu T. 1746 (TNS). NAGANA, Minamiazumi: 800–1400 m, 09 Jun. 1979, Murata J. & Chen TT 7573 (NHN); loc. eodem, 950–1200 m, 24 May 1977, Murata G., Koyama H. & Nimura H. 30377 (NHN). SHIZUOKA: 06 Aug. 1976, Fumihiro Chikada 108 (KUN). SURUGA: 24 Jul. 1914, Makino T. 139471 (NHN). YAMANASHI, Mount Kita: 23 Jul. 1982, Izumi Hiromasa s. n. (KUN). MONGOLIA: 46 400 N, 119 500 E, 09 Jul. 1987, Ганболд Э. s. n. (MW); loc. eodem, 49 24 N, 107 260 E, 15 Jul. 1981, Gubanov I. A. s. n. (MW); loc. eodem, 48 520 N, 111 450 E, 02 Aug. 1987, Gubanov I. A. s. n. (MW); loc. eodem, 27, Jul. 1977, Банникова И. А. s. n. (MW). KAZAKHSTAN, Western (Kazakhstan) Altai Mountains: 08 Aug. 1932, А. Г. Воронов s. n. (MW). SOUTH KOREA, SOBAEKSAN: 19 May 1995, Lee C., Kim Y. C. & Kim H. G. s. n. (HAST); loc. eodem, 20 May 1995, Bae Mi-hyun s. n. (HAST).

6.1 Section Paris

RUSSIA, AMUR OBLAST, Zeksky: 54 30 N, 127 21 E, 363 m, 15 Aug. 2014, Dudov S. V. & Kotel0 nikova K. V. 2014_S_055 (MW); loc. eodem, 54 50 N, 126 540 E, 06 Jul. 1977, Ignatov M. & Petelin D. s. n. (MW); loc. eodem, 53 520 N, 127 230 E, 01 Aug. 1977, Gubanov I. A., Grishakov Y. S. & Tuzov O. A. s. n. (MW); loc. eodem, 54 50 N, 127 50 E, 25 Jun. 1958, Nepli G. N. s. n. (MW); loc. eodem, 55 390 N, 130 430 E, 840 m, 01 Aug. 1985, Petelin D. A. s. n. (MW); loc. eodem, 52 10 N, 129 250 E, 30. Jun. 1955, Tyrtikov A. s. n. (MW); loc. eodem, 54 050 N, 127 050 E, 25 Jun. 1958, Непли ГН s. n. (MW); loc. eodem, 53 470 N, 127 090 E, 03 Jun. 1978, Игнатов М. С. s. n. (MW). KHABAROVSK KRAI, Ayano-Maysky: 57 50 N, 137 200 E, 27 Jun. 1979, Kharkevich S. s. n. (MW); loc. eodem, 57 360 N, 137 170 E, 10 Jun. 1979, Kharkevich S. s. n. (MW). Sovetsko-Gavansky: 43 00 N, 134 70 E, 25 May 1945, Zhudova P. 1125 (MW). Verkhnebureinsky: 51 550 N, 134 470 E, 780 m, 01 Aug. 1988, Petelin D. A. & Kemnits O. Y. 88-271 (MW); loc. eodem, 51 520 N, 134 250 E, 10 Jul. 1988, Berzina MV s. n. (MW); loc. eodem, 51 580 N, 134 520 E, 11 Aug. 1990, Borisov B. I. s. n. (MW); loc. eodem, 51 340 N, 134 340 E, 780 m, 11 Aug. 1989, Petelin D. A. 89-143 (MW); loc. eodem, 51 420 N, 134 270 E, 14 Aug. 1989, Borisov B. I. s. n. (MW); loc. eodem, 51 400 N, 134 370 E, 17 Aug. 1989, Zabelkin N. A. s. n. (MW); loc. eodem, 52 120 N, 134 250 E, 23 Aug. 1987, Anikina M. I. s. n. (MW); loc. eodem, 52 080 N, 134 180 E, 07 Aug. 1987, Аникина МИ s. n. (MW). Nanaysky: 49 250 N, 136 190 E, 250 m, 19 Jul. 1988, Krasnoborov I\M 3 (MW). Baikal: 12 Aug. 1933, Tarasov s. n. (MW). KRASNOYARSK KRAI, Kezhemsky: 60 530 N, 97 230 E, 29 Jun. 1938, Вершинин s. n. (MW); loc. eodem, 58 190 N, 100 030 E, 05 Jun. 1978, Д. Н. Шауло s. n. (MW). SAKHALIN OBLAST, Yuzhno-Sakhalinsk: 46 570 N, 142 460 E, 22 Jun. 2013, Korznikov K. A. s. n. (MW). Yuzhno-Kurilsky: 43 550 N, 145 320 E, 20 Jul. 1985, Shvedchikova N. s. n. (MW). Nogliksky: 52 250 N, 142 490 E, 01 Oct. 2011, Крутенко Т. В. s. n. (MW). Lensky: 60 160 N, 114 130 E, 01 Aug. 1953, Kuvaev V. & Nikolaev V. 87/2 (MW). SAKHA, Olyokminsky: 59 440 N, 118 170 E, 10 Aug. 1952, V. Kuvaev 75 (MW). PRIMORSKY KRAI, Ussuriisky: 43 370 N, 132 210 E, 01 Jul. 1971, Kosharovskaya I. B. s. n. (MW); loc. eodem, 43 370 N, 132 130 E, 02 Jun. 1980, Potapova N. s. n. (MW). Olginsky: 44 30 N, 135 80 E, 26 Jun. 1973, Pospelova E. s. n. (MW). Vladivostok: 42 570 N, 131 430 E, 350 m, 03 Jul. 1941, Vehov V. N. & Dvorakovskiy M. S. s. n. (MW). Artyom: 43 160 N, 132 160 E, 26 May 1982, Barkalov V. Y. s. n. (MW). Khasansky: 43 60 N, 131 330 E, 20 May 1963, Nechaeva T. I. s. n. (MW). Lazovsky: 43 160 N, 134 20 E, 23 Aug. 1944, Zhudova P. & Pokrovskaya 1127 (MW); loc. eodem, 43 000 N, 134 070 E, 25 May 1945, Жудова П s. n. (MW); loc. eodem, 43 010 N, 134 050 E, 16 Jul. 1944, Жудова П, s. n. (MW); loc. eodem, 43 160 N, 134 020 E, 0

103

23 Apr. 1944, Жудова П s. n. (MW). Chuguyevsky: 43 410 N, 134 080 E, 13 Jul. 1946, Жудова П s. n. (MW). ZABAYKALSKY KRAI, Priargunsky: 50 390 N, 118 350 E, 26 Jun. 1931, Nazarov M. I. s. n. (MW). IRKUTSK: Besser W. s. n. (K). 5. Paris bashanensis Wang et Tang, Fl. Reip. Pop. Sin. 15: 88. 1978; H. Li, The Genus Paris (Trilliaceae) 60. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 93. 2000. Type: China. Sichuan, Baoxing, Song ZP 38238 (Holotype, SZ). Paris quadrifolia L. var. setchuanensis Franch., Journ. Bot. 12: 191. 1898.  Paris verticillata var. setchuanensis (Franch.) Hand.-Mazz., Symb. Sin. 7: 1214. 1936.  Paris setchuenensis (Franch.) Barkalov, Sosud. Rost. Sovet. Dal’nego Vostaka 3: 171. 1988. Type: China, Chongqing, Chengkou, R. P. Farges 414 (Holotype, P; Isotype, PE). Perennial herb. Rhizome slender, usually branched, 2.0–4.0 mm in diameter, 20.0–30.0 cm long. Stem erect, cylindrical, green, glabrous, 10.0–30.0 cm tall. Leaves 4 (rarely 5) in an apical whorl, subsessile; leaf blades green, oblong-lanceolate to oblong, ca. 5.0–8.5 cm  1.5–3.5 cm, base cuneate, apex acuminate, glabrous; one pair of lateral veins basally developed, net veins inconspicuous. Flower solitary and terminal, 4 (rarely 5)-merous; pedicel green, 3.0–7.0 cm; sepals green, usually reflexed, narrowly lanceolate, ca. 1.0–3.0 cm  2.0–5.0 mm; petals filiform to linear, yellowish-green, slightly longer than (or as long as) sepals. Stamens 2  petal number, arranged in 2 whorls; filaments light green, 3.0–5.0 mm long; anthers yellow, 7.0–12.0 mm long, dehiscing by a lateral slit; free portion of connective subulate, yellowish-green, 4.0–14.0 mm long. Ovary purplish black, globose, 4 (or 5)-loculed with axile placentation. Style purple, ca. 2.0 mm; stigmas 4 (or 5)-lobed, erect, purple, 4.0–7.0 mm long. Berry subglobose, ca. 8.0–12.0 mm in diameter, purplish black, indehiscent (Figs. 6.8 and 6.9). Phenology: flowering May–June, fruiting July– September. Habitats: deciduous broad-leaved forests, bamboo thickets; ca. 1400–2750 m. Distribution: endemic to China: Chongqing (Chengkou, Nanchuan, Wuxi), Hubei (Shennongjia, Xingshan), Sichuan (Baoxing, Maoxian, Ngawa, Pingwu, Wenchuan). Additional specimens examined. CHINA, CHONGQING, Chengkou: Farges s. n. (P). Nanchuan: 14 May 1972, Liu SQ 77424 (IMC). Wuxi: May 2016, He S WX1605003 (HWA). HUBEI, Shennongjia: 16 Jul. 1985, Liu GJ 50147 (JMSU, PEM). Xingshan: 24 May 1957, Liu Y 194 (KUN, IBSC); loc. 01 Jan. 1957, Liu Y 191 (KUN). SICHUAN, Baoxing: 1936, Qu GL 3318 (PE). Maoxian: 10 Jun. 1959, South-to-North Water Diversion 00707 (KUN). Ngawa: 06 Jun. 2016, Zhong X ZX03917 (CSH). Pingwu: 16 Jun. 2014, Zhang SR et al. 2012 (PE). Wenchuan: 09 Aug. 2007, He XJ, Zhao QS & Wang Q 153256 (SZ).

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Fig. 6.8 Paris bashanensis (drawn by M. Shen): rhizome (a), stem (b), aerial shoot (c), and berry (d)

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6.2 Section Kinugasa

105

Fig. 6.9 Aerial shoot (a), rhizome and stem (b), and flower (c) of Paris bashanensis

6.2

Section Kinugasa

Paris sect. Kinugasa (Tategawi et Suto) Hara in J. Fac. Sci. Univ. Tokyo, Sect. 3, Bot. 10: 142. 1969. Rhizome thick; stamens 2-whorled; ovary angular, 4- to 10-loculed with axile placentation, style with an enlarged base; fruit an angular and juicy berry; seeds without sarcotesta or aril. 6. Paris japonica (Franch. et Sav.) Franch., Mem. Soc. Philom. Cent. (Paris) 24: 290, t. 24 A. 1888; Matsumura, Ind. Pl. Jap. 2 (1): 209. 1905; Ohwi, Fl. Jap. 320. 1953; Hara, Journ. Fac. Sci. Univ. Tokyo. Sect. 3, 10 (10): 167. 1969; H. Li, Bull. Bot. Res. Harbin 6 (1): 136. 1986; H. Li, The Genus Paris (Trilliaceae) 64. 1998.  Trillidium japonicum

Franch. et Sav., Enum. Pl. Jap. 2: 56. 1877.  Trillium japonicum (Franch. et Sav.) Matsumura, Shokubutsu Meii ed. 2: 298. 1895.  Kinugasa japonica (Franch. et Sav.) Tatewaki et Suto, Trans. Sapporo Nat. Hist. Soc. 14: 36. 1935. Type: Japan, Ishikawa, Hak-san Mountain, Rein 2945 (Holotype, P). Kinugasa japonica Franch. et Sav. var. tomentosa Miyabe et Tategawi, Trans. Sapporo Nat. Hist. Soc. 14: 36. 1935. Perennial herb. Rhizome thickened, 5.0–8.0 cm long, brown outside and white inside, 2.5–4.0 cm in diameter. Stem 30.0–40.0 cm tall, erect, green glabrous (occasionally papillose-pubescent). Leaves 6–12 in an apical whorl, subsessile; leaf blades oblong-obovate, apex acute, base tapering, ca. 10–30.0 cm  3.0–10.0 cm. Flower solitary, 6 to 10-merous; pedicel green, erect, 1.5–7.0 cm; sepals white

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and showy, oblong to obovate, ca. 2.0–5.0 cm  6.0–13.0 mm; petals linear, 1.0–2.0 cm, much shorter than sepals. Stamens 2  petal number, arranged in 2 whorls; filaments white, 5.0–8.0 mm long; anthers yellow, 6.0–10.0 mm long, dehiscing by a lateral slit. Ovary 7- to 10-loculed with axile placentation, ovoid or globose, green at base, white apically, with 6–10 slight ridges; style white, short, with an enlarged base; stigmas white, 3.0–7.0 mm; ovules numerous, globose. Berry indehiscent, ca. 8.0–25.0 mm in diameter, green at base, white apically (Figs. 6.10 and 6.11). Phenology: flowering June–July, fruiting August– October. Habitats: deciduous broad-leaved and coniferous forests; 1000–2100 m. Distribution: endemic to Japan: Honshu (Fukushima, Gunma, Ishikawa, Nagano, Niigata, Shinano, Toyama, Yamagata). Additional Specimens examined. JAPAN, FUKUSHIMA, Hinoemata: 8 Jul. 1935, Daikichi Hoshi s. n. (TNS); 23 Jul. 1934, Shunki Okuyama s. n. (TNS). Ichinoki: Aug. 1904, G. Nakahara s. n. (TNS). GUNMA, Minakami: 2 Aug. 1958, M. Tobe s. n. (TNS). ISHIKAWA, Hakusan: 16 Aug. 1951, Azuma M. s. n. (NHN). NAGANO, Azumi: 29 Jun. 1941, Y. Satake & S. Okuyama s. n. (TNS). Hokujo: 25 Aug. 1902, Y. Yabe s. n. (TNS); loc. eodem, 27 Jul. 1917, K. Matsushima s. n. (TNS); loc. eodem, 16 Aug. 1951, J. Ohwi s. n. (TNS); loc. eodem, Aug. 1931, U. Faurie s. n. (TNS). Omachi: 31 Jul. 1959, S. Okuyama & H. Utsumi 15587 (TNS). Taira: 11 Jul. 1925, Hideo Koidzumi 8734 (TNS); loc. eodem, 11 Jul. 1925, Hideo Koidzumi 51068 (TNS). NIIGATA, Mikuni: 22 Jul. 1930, Hideo Koidzumi 24257 (TNS). Myokokogen: 16 Jul. 1962, Fumihiro Konta 440 (TNS). Kotaki: 20 Aug. 1922, Hideo Koidzumi 4380 (TNS). Suginosawa: 19 Jul. 1897, Kano Watanabe s. n. (TNS). Yamato: 2 Sep. 1905, M. Nakamura s. n. (TNS); loc. eodem, 17 Aug. 1934, Hideo Koidzumi 92795 (TNS). Yunotani: 3 Aug. 1939, S. Okuyama s. n. (TNS). SHINANO, Shirouma: 16 Aug. 1951, Ohwi J. 319 (NHN). TOYAMA, Tateyama: 17 Jul. 1955, S. Okuyama 10552 (TNS); loc. eodem, 19 Jul. 1955, S. Okuyama 10563 (TNS). Uchiyama: 27 Aug. 1928, Hideo Koidzumi 17868 (TNS); loc. eodem, 27 Aug. 1928, Hideo Koidzumi 58774 (TNS). YAMAGATA, Tachikawa: 16 Jul. 1954, Hitoshi Okutsu s. n. (TNS).

6.3

Section Thibeticae

Paris sect. Thibeticae H. Li in Bull. Bot. Res Harbin 6: 132. 1986. Rhizome thick; stamens 2-whorled; ovary angular, 1-loculed with partial placentation; fruit a dehiscent capsule; seeds black, imperfectly enveloped with red and juicy aril.

7. Paris thibetica Franch., Nouv. Arch. Mus. Hist. Nat. II, 10: 184. 1888; Franch., Mem. Soc. Philom. Cent. (Paris) 24: 285. 1888; Hand.-Mazz., Symb. Sin. 1: 1215. 1936; Icon Cormorph. Sin. 5. 516. fig. 7862. 1976; H. Li, Bull. Bot. Res. Harbin 6 (1). 132. 1986; H. Li, The Genus Paris (Trilliaceae) 50. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 93. 2000.  Daiswa thibetica (Franch.) Takht., Brittonia 35 (3): 265. 1983; B. Mitchell, Plantsman 10 (3): 181. 1988.  Paris polyphylla Smith var. thibetica (Franch.) Hara, Journ. Fac. Sci. Univ. Tokyo, sect. 3, Bot. 10: 159, 176. 1969; Wang et Tang, Fl. Reip. Pop. Sin. 15:95. 1978. Type: China, Sichuan, Baoxing, Apr–May 1869, David A. s. n. (Holotype, P; Isotype, K, LE). Paris thibetica Franch. var. apetala Hand.-Mazz., Anz. Akad. Wiss. Wien, Math. -Naturwiss. Kl. 62: 149. 1925, Symb. Sin.7: 1215. 1936; H. Li, Bull. Bot. Res. Harbin 6 (1): 133. 1986; Wang et Tang, Fl. Reip. Pop. Sin. 15: 95. 1978; H. Li, The Genus Paris (Trilliaceae) 52. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 93. 2000. Type: China: Yunnan, Zwischen Salwin und Irrawadi, 3500 m, 5 July 1916, Handel-Mazzetti 9383 (Holotype, E) Paris polyphylla Smith var. appendiculata Hara, Fl. East. Himal. 410. 1966. Type: Bakkim-Jongri, 2500–4000 m, May 1960, Hara 366 (Holotype, TI). Paris wenxianensis Z. X. Peng & R. N. Zhao, Acta Bot. Boreal. -Occid. Sin. 6 (2): 133. 1986. Type: China, Gansu, Wenxian, 1900 m, 06 May 1980, Zhao RN 550291 (LZU). Perennial herb. Rhizome thick, yellowish brown outside and white inside, ca. 7.0–15 cm  0.5–1.5 cm. Stem erect, green or purple, glabrous (occasionally papillose-pubescent), 20.0–50.0 cm tall. Leaves green, 7–12 in a terminal whorl, sessile or with a short petiole (2.0–3.0 mm); leaf blades oblanceolate to oblong, green abaxially, apex acuminate, base cuneate, ca. 5.0–15.0 cm  1.0–2.0 cm. Flower solitary, basic merosity 4–7; pedicel green or purple, 4.5–15.0 cm long, slightly elongated at fruiting; sepals green, narrowly lanceolate to lanceolate, ca. 3.0–6.0 cm  1.0–1.5 cm; petals (occasionally absent) filiform, yellowish-green, 3.0–7.0 cm long; stamens 2  sepal number, arranged in two whorls, 2.0–5.0 cm long; filaments green, 5.0–12.0 mm long; anthers golden yellow, 6.0–20.0 mm long, free portion of connective 8.0–35.0 mm, greenish yellow. Ovary conical with 7–12 ridges, green at base, purple or dark red apically, unilocular with parietal placentation; ovules numerous, white. Style purple or dark red, short, with an enlarged base, stigmas 2.0–10.0 mm long. Capsule dehiscent, subglobose, green, 1.5–4.0 cm in diameter. Seeds numerous, ovate, 2.0–3.0 mm  2.0–2.5 mm, bright black, smooth, hard, imperfect enveloped by red and juicy aril (Figs. 6.12 and 6.13). Phenology: flowering March–April, fruiting May– September.

6.3 Section Thibeticae

Fig. 6.10 Whole plant (a) and berry (b) of Paris japonica (drawn by M. Shen)

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108

Fig. 6.11 Flower (a), stamens and pistil (b), and mature berry of Paris japonica (c)

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6.3 Section Thibeticae

Fig. 6.12 Whole plant (a), dehisced capsule (b), and seeds of Paris thibetica (c) (drawn by M. Shen)

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Fig. 6.13 Paris thibetica (photographed by Y. Ji). Petals present (a) or absent (b), flower (c), pistil (d), transverse section of ovary showing parietal placentation (e), mature capsule (f), and seeds (g and h)

6.4 Section Axiparis

Habitats: Deciduous broad-leaved and coniferous forests, bamboo thickets and alpine Rhododendron scrubs; 1600–3600 m. Distribution: China: Qinghai (Xunhua), Sichuan (Baoxing, Ebian, Emeishan, Jinyang, Luding, Mabian, Meigu, Pingwu, Shifang, Shimian, Tianquan, Xingjin), Yunnan (Binchuan, Fugong, Gongshan, Lanping, Lushui, Tengchong, Yangbi). Nepal (Kathmandu, Sankhuwasabha, Taplejung, Ilam). Notes: Because of the absence of petals, Handel-Mazzetti (1925) recognized a conspecific variety (P. thibetica var. apetala, Fig. 6.13b) under P. thibetica. From observations of cultivated plant materials, I found that the absence/presence of petals for a single plant individual changes in different years. Recognition of a variety based on this instability may be unreasonable. Therefore, I here reduced P. thibetica var. apetala as the synonym of P. thibetica. Additional specimens examined. CHINA, QINGHAI, Xunhua: 16 May 1959, Yan SZ 790 (WUK); loc. eodem, 22 Jun. 1964, Wei ZF 275 (WUK); loc. eodem, 24 Jun. 1964, Wei ZF 295 (WUK). SICHUAN, Baoxing: 1869, David s. n. (PE). Ebian: ZHAO ZX 73 (PE). Emeishan: 2450 m, 09 May 1964, Wang JW, Li CL & Guan KJ 398 (PEY). Jinyang: 3000 m, 16 May 1959, Sichuan Economic Botany Expedition, Liangshan 3033 (PE, CDBI). Kangding: 2200 m, 24 Jun. 1982, Lang KY 141 (KUN). Luding: 3200 m, 01 Sep. 1980, Vegetation Survey 23506 (CDBI). Mabian: 3200 m, 26 May 1931, Wang FZ 22944 (PE). Meigu: 28 390 20.700 N, 103 50 19.300 E, 2330 m, 24 May 2007, Gao LM & Wu D GLM-07732 (KUN). Pingwu: 32 310 2500 N, 104 420 4300 E, 1800–2050 m, 20 Apr. 2013, Zhang SR et al. 0229 (PE); loc. eodem, 22 Apr. 2013, Zhang L et al. 341 (PE); loc. eodem, 2000 m, 01 May 1961, Tang XN et al. 00116 (CDBI). Shifang: 1200 m, 25 Jul. 2007, He XJ, Zhan QS & Wang Q 138367 (SZ). Shimian: 07 Jun. 2018, JI YH 2018062 (KUN). Tianquan: 1936, QU GL 2427 (PE). Xingjing: 2700 m, 26 Jun. 1934, Harry Smith 10145 (PE). YUNNAN, Binchuan: 1942, Wang HC 1736 (KUN). Fugong: 26 320 3800 N, 98 550 35.600 E, 2230 m, 31 May 2015, Li H et al. 150-1 (KUN); loc. eodem, 27 100 4500 N, 98 430 4400 E, 2999 m, 02 May 2004, Gaoligong Biodiversity Survey 20193 (HAST). Gongshan: 27 370 3400 N, 98 350 3400 E, 2905 m, 01 Jul. 2000, Li H 11872 (KUN); loc. eodem, 27 420 54.100 N, 98 300 7.800 E, 2770 m, 02 May 2002, Li H 14830 (KUN); loc. eodem, 27 530 50.900 N, 98 400 23.300 E, 1572 m, 06 Jun. 2015, Li H et al. 165-1 (KUN); loc. eodem, 27 480 4700 N, 98 300 1800 E, 3000 m, 29 Sep. 2002, Li H et al. 16715 (KUN); loc. eodem, 27 470 53.200 N, 98 300 11.800 E, 3030 m, 21 Aug. 2006, Li H et al. 33895 (KUN); loc. eodem, 2300 m, 15 Aug. 1991, Dulongjiang Expedition 5970 (KUN). Lanping: 26 570 38.400 N, 99 140 12.500 E, 2095 m, 20 Apr. 2016, Wang YH et al. 003 (KUN); loc. eodem, 26 570 38.200 N, 99 140

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12.500 E, 2130 m, 27 May 2015, Li H et al. 121-1 (KUN). Lushui: 25 560 39.300 N, 98 440 54.800 E, 1740 m, 21 Apr. 2016, Wang YH 006 (KUN); loc. eodem, 3000 m, 13 Jul. 1960, NW Yunnan Expedition 10406 (KUN); loc. eodem, 25 540 44.900 N, 99 010 21.200 E, 2450 m, 29 May 2015, Li H et al. 130-1 (KUN); loc. eodem, 25 560 39.300 N, 98 440 54.800 E, 1710 m, 30 May 2015, Li H et al. 138-1 (KUN); loc. eodem, 25 280 4100 N, 98 410 2100 E, 3080 m, 11 May 2005, Li H et al. 22699 (KUN); loc. eodem, 25 580 1900 N, 98 400 5400 E, 3232 m, 11 May 2005, Li H et al. 23949 (KUN); loc. eodem, 25 580 2400 N, 98 410 1500 E, 3125 m, 19 May 2005, Li H et al. 24516 (KUN); loc. eodem, 26 00 53.100 N, 98 380 4400 E, 2230 m, 05 May 2007, Gao LM GLM-07564 (KUN); loc. eodem, 25 580 25.200 N, 99 410 49.800 E, 3102 m, 21 May 2008, Jin XH & Zhang T 296 (PE). Tengchong: 2700 m, 11 May 1964, Wu SG 6778 (KUN); loc. eodem, 3640 m, 25 May 1964, Wu SG 6907 (KUN); loc. eodem, 2600 m, 04 Jun. 1964, Wu SG 7013 (KUN). Weixi: 2800 m, 26 May 1940, Feng GM 4145 (PE). Yangbi: 3000 m, 04 May 1981, Sino-British Expedition to Cangshan 126 (KUN); loc. eodem, 3000 m, 04 May 1981, Sino-British Expedition to Cangshan 143 (KUN); loc. eodem, 2900 m, 07 May 1981, Sino-British Expedition to Cangshan 320 (KUN); loc. eodem, 25 460 N, 100 010 E, 3450 m, 28 Jun. 1984, Sino-US Expedition to Yunnan 563 (KUN); loc. eodem, 2800 m, 28 Aug. 1963, NE Yunnan Jinshajiang Expedition 4101 (PE). NEPAL, Kathmandu: 27 430 0.1200 N, 85 190 0.1200 E, 17 Mar. 1803, Francis Buchanan-Hamilton s. n. (NHMUK). Sankhuwasabha: 3150 m, 21 Aug. 1998, Japan-Nepal Botanical Expedition to East Nepal 9810111 (E). Taplejung: 27 290 5500 N, 87 550 700 E, 2900–3300 m, 12 Jun. 1992, S. Noshiro, S. Akiyama & N. Acharya 9240736 (NHN, E). Ilam: 27 50 000 N, 88 10 700 E, 3059 m, 15 Jun. 2007, Adhikari B. et al. LKSRB 97 (E).

6.4

Section Axiparis

Paris sect. Axiparis H. Li, Act. Bot. Yunnan. 6: 365. 1984. Rhizome thick; stamens 2- to 3-whorled; ovary angular, 4to 10-loculed with axile placentation, style with an enlarged base; fruit ridged berry; seeds white or yellow, imperfectly enveloped with spongy aril. 8. Paris vaniotii Lévl., Mem. Pontif. Accad. Romana Nuovi Lincei 24: 355. 1906; H. Li, Act. Bot. Yunnan. 6 (4): 359. 1984; H. Li, Bull. Bot. Res. Harbin 6 (1): 135. 1986; H. Li, The Genus Paris (Trilliaceae) 55. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 93. 2000. Type: China, Guizhou, Guiding, 25 May 1902, Cavalerie & Pierre Julien 1309 (Holotype, E). Paris axialis H. Li, Act. Bot. Yunnan 6 (3): 273, fig. 1. 1984; 1. c. 6 (4): 359. 1984; H. Li, Bull. Bot. Res. Harbin

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6 (1): 134. 1986; H. Li, The Genus Paris (Trilliaceae) 53. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 93. 2000. Type: China, Yunnan, Yiliang: 1900 m, 17 Jun. 1982, Li H, Chen Y, & Yu HY 1322 (Holotype; Isotype, KUN); loc. eodem, 14 Sep. 1972, NE Yunnan Expedition 630 (Paratype, KUN). Paris guizhouensis S. Z. He, Guizhou Sci. 3 (3): 16. 1990. Type: China, Guizhou, Zhenning, 1400 m, 10 Mar. 1987, He SZ 293 (HGCM). Paris axialis H. Li var. rubra H. H. Zhou, K. Y. Wu, & R. Tao, Act. Bot. Yunnan. 13 (4): 424. 1991; H. Li, The Genus Paris (Trilliaceae) 55. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 93. 2000. Type: China, Guizhou, Shuicheng, 2000 m, 01 Oct. 1990, Zhou HH 9031 (Holotype, KUN). Paris undulata H. Li et V. G. Soukup, Acta Bot. Yunnan, Suppl. 5: 16 1992; H. Li, The Genus Paris (Trilliaceae) 41. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 91. 2000. Type: China, Sichuan, Mountain Emei, 18. May 1988, Li H 88168 (Holotype, KUN). Paris lihengiana G.W. Hu & Q. F. Wang, Phytotaxa 392 (1): 045–053. 2019. Type: China, Yunnan, Weixin, 27 530 N, 104 460 E, 1440 m, 24 Apr. 2011, Hu, Wang & Zhao HGW-00655 (Holotype; Isotype, HIB). Paris variabilis Z. Y. Yang, C. J. Yang & Y. H. Ji., Phytotaxa 401 (3): 190–198. 2019. Type: China, Yunnan, Shuifu, 28.359 N, 104.404 E, 1580 m, 19 May 2017, Ji & Yang 039 (Holotype; Isotypes: KUN). Perennial herb. Rhizome cylindrical, occasionally branched, oblique or horizontal, 5.0–15.0 cm long, 1.0–3.0 cm in diameter. Stem erect, cylindrical, purplish red or green, glabrous (occasionally pubescence), 30.0–70.0 cm tall. Leaves green, 5–7 in an apical whorl; leaf blades narrowly lanceolate, oblong-oblanceolate, oblong, oblongovate, and obovate, base shallowly cordate, rounded or cuneate, apex acute or acuminate, ca. 6.0–19.0  1.6–12.0 cm; petiole 0.5–6.0 cm long; lateral veins 1–2 pairs, basally developed. Flower solitary and terminal, basic merosity 4–7; pedicel green or purple, 5.0–37.0 cm; sepals ovatelanceolate, or lanceolate to narrowly lanceolate, green, papery or membranous, ca. 2.8–8.6  0.8–2.5 cm; petals filiform to linear, greenish yellow, much longer than sepals, usually curled. Stamens 3 (rarely 4 and 2)  petal number, filaments greenish yellow, 3.0–8.0 mm, anthers golden yellow, dehiscing by a lateral slit, 5.0–9.0 mm long, free portion of connective 0.5–1.0 mm long, acute. Ovary conical, green or bluish violet, with 4–7 ridges, 4–7-loculed, axile placentation, ovules numerous, anatropous; style with an enlarged base, purplish red, cyan purple, or orange yellow; stigmas 4–7, 2.0–5.0 mm long. Berry subglobose, ca. 10.0–25.0 mm in diameter, dark red at maturity, indehiscent. Seeds numerous, yellow-brown, ovoid, partly enveloped by white, spongy aril (Figs. 6.14, 6.15 and 6.16).

6 Taxonomic Revision

Phenology: flowering in April, fruiting July–October. Habitats: evergreen (deciduous) broad-leaved and coniferous forests, bamboo thickets; ca. 700–3000 m. Distribution: endemic to China: Chongqing (Jiangjin, Nanchuan), Guizhou (Daozhen, Nayong, Shuicheng, Xingyi, Zheng’an), Hubei (Shengnongjia), Hunan (Nanyue, Sangzhi, Xinning), Sichuan (Baoxing, Dujiangyan, Ebian, Emeishan, Hongya, Junlian, Leibo, Luding, Muchuan, Tianquan, Wenchuan, Xide), Yunnan (Daguan, Shuifu, Sujiang, Yanjin). Notes: Since 1980, a total of 6 taxa (namely, P. axialis, P. axialis var. rubra, P. guizhouensis, P. lihengiana, P. undulatis, and P. variabilis) whose morphologies are similar to P. vaniotii have been described (Li 1984; He 1990; Zhou et al. 1991; Li 1992; Xu et al. 2019; Yang et al. 2019). These taxa share stamens 3  petal number and similar fruit and seed morphology with P. vaniotii but differ from them in the leaf shape. As a result of critical examination of a large number of specimens of these taxa, I found that their leaf shape successively varies from narrowly lanceolate in P. lihengiana (Fig. 6.17a), to lanceolate in P. vaniotii (Fig. 6.17b), oblong-oblanceolate in P. vaniotii (Fig. 6.17c, d) and P. undulatis (Fig. 6.17e, f), oblong in guizhouensis (Fig. 6.17h) and variabilis (Fig. 6.17g), oblong-ovate in P. axialis (Fig. 6.17i), and obovate in P. axialis (Fig. 6.17j, k). Species delineation based on such a trait would result in taxonomic over-splitting of species. Accordingly, these taxa here are reduced to synonyms of P. vaniotii. Additional specimens examined, CHINA, CHONGQING, Jiangjin: 106 260 52.2900 N, 28 330 01.6700 E, 1581.51 m, 08 Jul. 2017, Liu ZY et al. S-2676 (IMC). Nanchuan: 670 m, 26 Jul. 2004, Liu X 20141689 (IMC); loc. eodem, 670 m, 19 Jun. 1983, Liu ZY 4206 (IMC); loc. eodem, 1950 m, 10 Jun. 1983, Liu ZY 4171 (IMC); loc. eodem, 850 m, 11 Jun. 1986, Liu ZY 9188 (IMC); loc. eodem, 1600 m, 11 Apr. 1979, Liu ZY 790923 (IMC); loc. eodem, 1600 m, 11 Apr. 1979, Liu ZY 790922 (IMC); loc. eodem, 1600 m, 11 Apr. 1979, Liu ZY 790923 (IMC); loc. eodem, 1600 m, 11 Apr. 1979, Liu ZY 790924 (IMC); loc. eodem, 850 m, 22 May. 1986, Liu ZY 8525 (IMC); loc. eodem, 1100 m, 28 May. 1986, Liu ZY 8654 (IMC); loc. eodem, 1000 m, 15 Jun. 1986, Liu ZY 11415 (IMC); loc. eodem, 1000 m, 11 Jun. 1986, Liu ZY 8957 (IMC); loc. eodem, 1000 m, 11 Jun. 1986, Liu ZY 8959 (IMC). GUIZHOU, Daozhen: 1500 m, 17 Apr. 2003, Liu ZY 2030664 (IMC); loc. eodem, 650 m, 03 Jun. 2003, Liu ZY 2032189 (IMC). Nayong: 2000 m, 25 Jul. 1959, Bijie Expedition 410 (PE). Shuicheng: 03 Jul. 1990, Zhou HH 9013 (KUN). Xingyi: 20 Nov. 2016, Deng CY 522301161120269LY (GZTM). Zheng’an: 28 210 2300 N, 107 190 3500 E, 1403.3 m, 19 Apr. 2016, Guang FQ 520324160419004LY (GZTM). HUBEI, Shengnongjia: 05 May 2006, Zhang XL s. n. (WH). HUNAN, Nanyue: 1000 m, 06 Apr. 2003, Li MH &

6.4 Section Axiparis

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Fig. 6.14 Paris vaniotii (drawn by M. Shen): whole plant (a), mature berry (b), transverse section of ovary (c), and seeds (d)

Kuang QY 735 (PE). Sangzhi: 1450 m, 09 Sep. 1990, Cao TR 090593 (CSFI). Xinning: 640 m, 13 Apr. 2017, Li H, Gao XY, & Liu CN 051 (KUN). SICHUAN, Baoxing: 1936, Chu KL 3925 (WUK); loc. eodem, 1500 m, 03 Sep. 1963, Guan KJ 2798 (PE); loc. eodem, 1936, Qu GL 3925 (PE); loc. eodem, 10 Jun. 1954, Song ZP 38162 (WUK). Dujiangyan: 1900 m, 01 Jun. 1987, Chen WL C-0069

(HX); loc. eodem, 1800 m, 26 May 1999, Feng ZB & Wu GJ 990086 (HX); loc. eodem, 1600 m, 26 Apr. 1987, Fu DZ 87-0217 (HX); loc. eodem, 07 May 1939, Fang WP 13446 (PE; IBSC). Ebian: 13 Oct. 1939, Liou TN & Wang C 1419 (PE). Emeishan: Yao CW s. n. (PE); loc. eodem, 10 Aug. 1928, Fang WP 2749 (PE); loc. eodem, 11 May 1952, Jiang XL & Zhang XS 30500 (PE); loc. eodem, 02 Aug. 1952, Jiang

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6 Taxonomic Revision

Fig. 6.15 Flowers of Paris vaniotii showing stamens 3  petal number

XL & Zhang XS 31894 (PE); loc. eodem, 2500 m, 06 Oct. 1963, Tian JQ & Liu JJ 0018 (PE); loc. eodem, 1800 m, 05 Jun. 1957, Yang GH 55140 (PE); loc. eodem, 02 Jun. 1960, Medicinal Plants Survey 12583 (CDBI); loc. eodem, 22 Jun. 1955, Sino-Soviet Expedition 2207 (PE); loc. eodem, 29 May 1939, Zhou HC 9997 (PE); loc. eodem, 29 Aug. 1956, Zhu ZY et al. 830 (PE); loc. eodem, May 2004, Nian CL 040508 (SZ). Hongya: 18 Jul. 1930, Tu TH 321 (PE).

Junlian: 1600 m, 26 Apr. 1959, Yibin Wild Plants Survey 0163 (PE; CDBI). Leibo: 1200 m, 09 Jun. 1959, Liangshan Wild Plant Survey 0551 (KUN; PE; CDBI); loc. eodem, 1860 m, 02 Apr. 1964, Yin KF & Chen QH 0096 (CDBI). Luding: 1880 m, 04 May 2008, He XJ & Zhao QS 160241 (SZ). Muchuan: 05 May 1959, Sichuan Economic Botany Expedition, Leshan 2001 (CDBI). Tianquan: 2300 m, 03 Jun. 1953, Tsiang XL 34297 (PE); loc. eodem, 2450 m,

6.4 Section Axiparis

115

Fig. 6.16 Pistil (a), transverse (b) and longitudinal (c) section of ovary, mature berry (d), transverse section of berry (e), and seeds (f) of Paris vaniotii

27 Aug. 1963, Guan KJ 2018 (PE); loc. eodem, 23 Jun. 1951, Hu WG & He Z 10079 (WUK); loc. eodem, 2050 m, 25 Apr. 1953, Jiang XJ 33972 (IBSC); loc. eodem, 1936, Chu KL 2534 (PE); loc. eodem, 1700 m, 02 Apr. 1980, Yang YB 21764 (CDBI). Wenchuan: 1600 m, 02 May 2008, He XJ & Zhao QS 157210 (SZ). Xide: 1900 m, 22 Apr. 2009, He XJ & Zhao QS 199488 (SZ). YUNNAN, Daguan: 1870 m, 17 May 2016, Li H et al. 018 (KUN); loc. eodem, 1870 m, 17 May 2016, Li H et al. 019 (KUN); loc. eodem, 1870 m, 17 May 2016, Li H et al. 021 (KUN). Shuifu: 400 m, 07 Apr. 2002, Liu ZY 2020151 (IMC); loc. eodem, 28 210 32.400 N, 104 240 14.400 E, 1580 m, 19 May 2017, Ji YH & Yang CJ

040 (KUN). Sujiang: 1900 m, 19 May 1973, Sun BX 0332 (KUN). Yanjin: 27 500 27.600 N, 104 520 15.600 E, 1650 m, 19 May 2017, Ji YH & Yang CJ 049 (KUN). 9. Paris forrestii (Takht.) H. Li, Act. Bot. Yunnan. 6 (4): 359. 1984; H. Li, Bull. Bot. Res. Harbin 6 (1): 135. 1986; H. Li, The Genus Paris (Trilliaceae) 56. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 93. 2000.  Daiswa forrestii Takht., Brittonia 35 (3): 268, 1983; B. Mitchell, Plantsman 10 (3): 174. 1988. Type: China, Yunnan, Tengchong, 25 300 N, 98 250 E, May 1931, G. Forrest 29602 (Holotype, E; Isotype, BM).

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Fig. 6.17 Variation in leaf shape of Paris vaniotii

6 Taxonomic Revision

6.4 Section Axiparis

Paris longistigmata H. Li, Act. Bot. Yunnan. 6 (3): 275, 1984. Type: China, Yunnan, Baoshan, J. S. Yang 63-1590 (Holotype, KUN). Paris rugosa H. Li & Kurita, Acta Bot. Yunnan. Suppl. 5: 13. 1992; H. Li, The Genus Paris (Trilliaceae) 58. 1998. Type: China, Yunnan, Gongshan, 1620 m, 16 May 1991, Dulongjiang Expedition 5388 (Holotype, KUN). Paris dulongensis H. Li & Kurita, Acta Bot. Yunnan. Suppl. 5: 14. 1992; H. Li, The Genus Paris (Trilliaceae) 59. 1998. Type: China, Yunnan, Gongshan, 1550 m, Dulongjiang Botany Expedition 6765 (Holotype, KUN); loc. eodem, Dulongjiang Botany Expedition 5329 (Paratype, KUN). Paris tengchongensis Y. H. Ji, C. J. Yang & Y. L. Huang, Phytotaxa 306 (3): 234–236. 2017. Type: China. Yunnan, Tengchong, 3120 m, 25 340 0200 N, 98 160 2300 E, 14 Apr. 2015, Ji YH 1341 (Holotype, KUN; Isotype KUN, PE). Perennial herb. Rhizome cylindrical, thickened with multiple nodes. Stem erect, cylindrical, green, purple, or purplish black, 15.0–60.0 cm tall. Leaves 4–7 in a terminal whorl at the apex of the stem; leaf blades oblanceolate, oblong, oblong obovate, or obovate, base subrounded to subcordate, apex acute or acuminate, wrinkled or not, lateral veins 1–2 pairs, basally developed, occasionally depressed adaxially and prominent abaxially, petiole 2.5–7.0 cm long. Flower solitary, basic merosity 4–7; pedicel green or purple, 4.5–40.0 cm long, erect in flowering, and bending in fruiting; sepals green (occasionally with purple markings), ovate, oblong or ovate-lanceolate, ca. 1.5–5.0 cm  0.6–2.0 cm; petals yellowish-green (occasionally dark red), filiform, ca. 0.1 mm  4.5–12.5 cm. stamens 2  petal number, arranged in 2 whorls; filaments greenish-yellow, 3.0–7.0 mm; anthers light yellow, 5.0–15.0 mm, dehiscing by a lateral slit; free portion of connective inconspicuous. Ovary green or red with 4–7 longitudinal ridges, axile placentation. Style 1.5–5.5 mm, red, orange, or purplish green, with an enlarged base; stigmas 4–7, 4.0–13.0 mm long, usually revolute. Berry ridged, green or dark red at maturity, indehiscent, 1.0–4.0 in diameter. Seeds numerous, white or yellow, ovoid, slightly enveloped by spongy aril (Figs. 6.18, 6.19 and 6.20). Phenology: flowering March–May, fruiting June– October. Habitats: evergreen (deciduous) broad-leaved and coniferous forests, bamboo thickets, and Rhododendron scrubs; ca. 600–3200 m. Distribution: Burma (Taunggyi). China: Sichuan (Panzhihua, Yanyuan), Tibet (Bome, Dinggye, Gyirong, Medog, Nyalam, Nyingchi, Zayü), Yunnan (Deqin, Fugong, Gongshan, Lanping, Lushui, Lijiang, Ninge, Shangri-la, Tengchong, Yunlong). India (Sirohi). Nepal (Jumla). Notes: Since the discovery of P. forrestii, three species (P. dulongensis, P. rugosa, and P. tengchongensis) morphologically similar to P. forrestii have been described (Li 1992; Ji et al. 2017). I carefully examined specimens and living

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plants of these species. Except for their leaf shape, these species exhibit high levels of similarity in flower, fruit, and seed morphology with P. forrestii. It is noteworthy that the oblanceolate or oblong leaves in P. dulongensis (Fig. 6.21c, d, e) and obovate leaves in P. rugosa (Fig. 6.21k, m, n), as well as oblong or elliptic leaves in P. tengchongensis (Fig. 6.21f), can be found in P. forrestii (Fig. 6.21a, b, g, h, i, j, l). Additionally, the types of these species were collected from the Gaoligong Mountains, western Yunnan, China, and the localities are closer to each other. Therefore, I here treat P. dulongensis, P. rugosa, and P. tengchongensis as synonyms of P. forrestii. Additional specimens examined. BURMA, Taunggyi: 1524 m, May 1938, Dickason F. G. s. n. (NHN). CHINA, SICHUAN, Panzhihua: 25 Jun. 1983, QinghaiTibet Expedition 11427 (PE). Yanyuan: 20 Jul. 1983, Qinghai-Tibet Expedition 12081 (PE). TIBET, Bome: 14 May 1986, T. Naito, Lang KY & Y. Tateishi 990 (PE); loc. eodem, 25 Apr. 1986, Wang JT & Yoshiaki takeda 0193 (PE). Dinggye: 06 Jun. 1975, Qinghai-Tibet Expedition 5579 (HNWP); loc. eodem, 07 Jun. 1975, Qinghai-Tibet Expedition 5620 (HNWP). Gyirong: 2380 m, 07 Jun. 1972, Tibet Chinese Medicinal Herbs Survey 456 (PE); loc. eodem, 14 Jul. 1975, Qinghai-Tibet Expedition 6806 (PE). Medog: 14 Jun. 1983, Li BS & Cheng SZ 05043 (PE); loc. eodem, 1800 m, 06 Aug. 2010, S Tibet Expedition 2186 (PE); loc. eodem, 2000 m, 31 Aug. 1990 Yao G et al. 4045 (NAS); loc. eodem, 2100 m, 23 Apr. 1993, Sun H, Zhou ZK & Yu HY 5312 (KUN); loc. eodem, 1000 m, 29 Apr. 1993, Sun H, Zhou ZK & Yu HY 5950 (KUN); loc. eodem, 26 Dec. 1992, Sun H, Zhou ZK & Yu HY 2631 (KUN); loc. eodem, 1400 m, 15 Apr. 1993, Sun H, Zhou ZK & Yu HY 5212 (KUN); loc. eodem, 2000 m, 21 Apr. 1993, Sun H, Zhou ZK & Yu HY 5616 (KUN); loc. eodem, 2500 m, 26 Oct. 1992, Sun H, Zhou ZK & Yu HY 0562 (KUN); loc. eodem, 2100 m, 27 Oct. 1992, Sun H, Zhou ZK & Yu HY 0800 (KUN); loc. eodem, 2300 m, 03 Aug. 1974, Qinghai-Tibet Expedition 74-4023 (KUN); loc. eodem, 600 m, 29 Nov. 1992, Sun H, Zhou ZK & Yu HY 1767 (KUN); loc. eodem, 08 Apr. 1983, Li BS & Cheng SZ 03981 (PE); loc. eodem, 20 Apr. 1983, Li BS & Cheng SZ 04144 (PE); loc. eodem, 30 Dec. 1982, Li BS & Cheng SZ 02353 (PE); loc. eodem, 19 Sep. 2012, FLPH Tibet Expedition 12-1874 (PE); loc. eodem, 19 Jan. 1983, Li BS & Cheng SZ 03484 (PE); loc. eodem, 24 Jun. 1983, Li BS & Cheng SZ 05181 (PE); loc. eodem, 24 Sep. 2003, Yin JT et al. s. n. (HITBC). Nyalam: 23 Aug. 1972, Tibet Chinese Medicinal Herbs Survey 1423 (HNWP); loc. eodem, 24 Aug. Tibet Chinese Medicinal Herbs Survey 1972 (PE); loc. eodem, 2200 m, 30 Jun. 1975, Qinghai-Tibet Expedition 6663 (PE); loc. eodem, 2300 m, 24 Aug. 1972, Tibet Chinese Medicinal Herbs Survey 1446 (PE). Nyingchi: 2900 m, 15 Jun. 1972, Tibet Chinese Medicinal Herbs Survey 3391 (PE). Zayü: 2400 m, 25 Jun. 1980, Ni ZC et al. 0179 (PE); loc. eodem,

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Fig. 6.18 Paris forrestii (drawn by M. Shen). Aerial shoot (a), mature berry (b), and seeds (c)

6 Taxonomic Revision

6.4 Section Axiparis

119

Fig. 6.19 Paris forrestii. Mature berry (a), seeds (b), pistil (c), and longitudinal (d) and transverse (e) section of ovary showing axile placentation

28 Jun. 1979, Huang RF 0245 (HNWP); loc. eodem, 2650 m, 18 Jun. 1973, Qinghai-Tibet Expedition 195 (PE); loc. eodem, 2210 m, 04 Jul. 1973, Qinghai-Tibet Expedition 570 (PE); loc. eodem, 2220 m, 04 Jul. 1973, Qinghai-Tibet Expedition 73-570 (PE). YUNNAN, Deqin: 2700–3300 m, 18 Jul. 1940, Feng GM 5610 (KUN). Fugong: 26 320 38.000 N, 98 550 35.600 E, 31 May 2015, Li H et al. 148-1 (KUN); loc. eodem, 27 090 56.800 N, 98 460 51.100 E, 01 May 2004, Li H et al. 19997 (KUN); loc. eodem, 26 320 38.000 N, 98 550 35.600 E, 2230 m, 31 May 2015, Li H et al. 148-2 (KUN); loc. eodem, 26 320 38.000 N, 98 550 35.600 E, 2230 m, 31 May 2015, Li H et al. 148-3 (KUN); loc. eodem, 27 100 45.400 N, 98 430 44.400 E, 2999 m, 04 May 2004, Li H et al. 20192 (KUN); loc. eodem, 01 Aug. 1979, Lin Q 791958 (KUN). Gongshan: 05 Aug. 2013, Jin XH et al. ST2092 (PE); loc. eodem, 27 Jul. 2013, Jin XH et al. ST1164 (PE); loc. eodem, 27 Jul. 2013, Jin XH et al. ST1135 (PE); loc. eodem, 26 Jul. 2013, Jin XH et al. ST1082 (PE); loc. eodem, 1480 m, 23 Sep. 2014, Li H, Yang J & Wang YH Nj-023 (KUN); loc. eodem, 27 520 35.200 N , 98 200 7.000 E, 02 Jun. 2015, Li H et al. 156-2 (KUN); loc. eodem, 27 530 50.900 N, 98 400 23.300 E, 1572 m, 06 Jun. 2015, Li H et al. 166-3 (KUN); loc. eodem, 27 500 15.000 N, 98 410 16.600 E, 1510 m, 01 Jun. 2015, Li H et al. 152-2 (KUN); loc. eodem, 27 370 4300 N, 98 350 3600 E, 3010 m, 12 Aug. 2006, Li H et al. 33193 (KUN); loc. eodem, 27 520 38.300 N, 98 200 7.500 E, 1550 m, 23 Jul. 2002, Li H, Li R & Diao ZL 15167 (KUN); loc. eodem, 27 420 47.200 N, 98 170 45.900 E, 2751 m, 18 Aug. 2006, Li H et al. 32440 (KUN); loc. eodem, 1990 m, 17 May 2001, Li H et al. 13860 (KUN); loc. eodem, 27 370 5100 N, 98 350 3400 E, 2960 m, 01 Jul. 2000, Li H et al. 12121 (KUN); loc. eodem, 27 370 5100 N,

98 350 3400 E, 3000 m, 01 Jul. 2000, (KUN); loc. eodem, Li H et al. 12130 (KUN); loc. eodem, 1330 m, 25 May 1991, Dulongjiang River Expedition 7068 (KUN); loc. eodem, 2500 m, 21 Apr. 1991, Dulongjiang River Expedition 6284 (KUN); loc. eodem, 2500 m, 17 Apr. 1991, Dulongjiang River Expedition 6093 (KUN); loc. eodem, 2300 m, 16 May 1991, Dulongjiang River Expedition 6797 (KUN); loc. eodem, 11 Feb. 1991, Dulongjiang River Expedition 4003 (KUN); loc. eodem, 2000 m, 28 Mar. 1991, Dulongjiang River Expedition 5267 (KUN); loc. eodem, 2500–2600 m, 03 Jun. 1990, Yang ZH 90-1317 (KUN); loc. eodem, 24 Sep. 2014, Li H, Yang J & Wang YH NJ0018 (KUN); loc. eodem, 24 Sep. 2014, Li H, Yang J & Wang YH NJ001-13 (KUN); loc. eodem, 27 500 15.000 N, 98 410 16.600 E, 1510 m, 01 Jun. 2015, Li H et al. 152-1 (KUN); loc. eodem, 27 530 50.900 N, 98 400 23.300 E, 1572 m, 06 Jun. 2015, Li H et al. 164-2 (KUN); loc. eodem, 27 500 15.000 N, 98 410 16.600 E, 1510 m, 01 Jun. 2015, Li H et al. 152-3 (KUN); loc. eodem, 26 570 38.200 N, 99 140 12.500 E, 2130 m, 27 May 2015, Li H et al. 119-3 (KUN); loc. eodem, 27 480 000 N, 98 300 400 E, 2830 m, 01 Sep. 2006, Li H et al. 31722 (KUN); loc. eodem, 27 430 39.800 N, 98 370 18.500 E, 17 Jul. 2002, Li H, Li R & Diao ZL 15032 (KUN); loc. eodem, 27 Apr. 1991, Dulongjiang River Expedition 6627 (KUN); loc. eodem, 2800–3200 m, 08 Sep. 1940, Feng GM 7639 (KUN); loc. eodem, 03 Aug. 1979, Deng XF 791370 (KUN); loc. eodem, 1580 m, 28 Apr. 1991, Dulongjiang River Expedition 6645 (KUN); loc. eodem, 1540 m, 25 May 1991, Dulongjiang River Expedition 7069 (KUN); loc. eodem, 1560 m, 28 Apr. 1991, Dulongjiang River Expedition 6647 (KUN); loc. eodem, 1500 m, 19 May 1991, Dulongjiang River Expedition 6857 (KUN);

120

Fig. 6.20 Flowers and berry of Paris forrestii showing stamens 2  petal number and variation in style length

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6.4 Section Axiparis

Fig. 6.21 Variation in leaf shape in Paris forrestii

121

122

loc. eodem, 1330 m, 16 May 1991, Dulongjiang River Expedition 6787 (KUN); loc. eodem, 27 530 50.900 N, 98 400 23.300 E, 1572 m, 06 Jun. 2015, Li H et al. 162-4 (KUN); loc. eodem, 27 470 1.000 N, 98 190 58.900 E, 1400 m, 22 Sep. 2004, Li H, Diao ZL & Li R 581 (KUN); loc. eodem, 28 010 13.800 N, 98 190 15.300 E, 1651 m, 05 Jun. 2015, Li H et al. 167-3 (KUN); loc. eodem, 27 530 50.900 N, 98 400 23.300 E, 06 Jun. 2015, Li H et al. 163-5 (KUN); loc. eodem, 2250 m, 30 Oct. 2004, Li H et al. 21597, 1400 m, 19 May 1991, Dulongjiang River Expedition 6865 (KUN); loc. eodem, 1350 m, 16 May 1991, Dulongjiang River Expedition 6765 (KUN); loc. eodem, 1550 m, 28 Apr. 1991, Dulongjiang River Expedition 6668 (KUN); loc. eodem, 1540 m, 28 Apr. 1991, Dulongjiang River Expedition 6639 (KUN); loc. eodem, 1400 m, 19 May 1991, Dulongjiang River Expedition 6864 (KUN); loc. eodem, 1651 m, 05 Jun. 2015, Li H et al. 167-2 (KUN); loc. eodem, 1540 m, 29 Mar 1991, Dulongjiang River Expedition 5329 (KUN). Lanping: 26 570 38.400 N, 99 140 12.500 E, 2095 m, 20 Apr. 2016, Wang YH et al. 001 (KUN); loc. eodem, 26 570 38.200 N, 99 140 12.500 E, 27 May 2015, Li H et al. 120-3 (KUN); loc. eodem, 26 570 38.200 N, 99 140 12.500 E, 2130 m, 27 May 2015, Li H et al. 120-4 (KUN); loc. eodem, 26 570 38.200 N, 99 140 12.500 E, 2130 m, 27 May 2015, Li H et al. 119-1 (KUN); loc. eodem, 26 570 38.400 N, 99 140 12.500 E, 2095 m, 20 Apr. 2016, Wang YH et al. 004 (KUN); loc. eodem, 26 570 38.200 N, 99 140 12.500 E, 2130 m, 27 May 2015, Li H et al. 122-1 (KUN). Lushui: 25 560 39.300 N, 98 440 54.800 E, 1740 m, 21 Apr. 2016, Wang YH et al. 005 (KUN); loc. eodem, 25 560 39.300 N, 98 440 54.800 E, 1710 m, 30 May 2015, Li H et al. 139-2 (KUN); loc. eodem, 25 540 44.900 N, 99 010 21.200 E, 29 May 2015, Li H et al. 133-2 (KUN); loc. eodem, 25 590 3000 N, 98 390 5700 E, 2510 m, 16 May 2005, Li H et al. 24248 (KUN); loc. eodem, 25 280 4100 N, 98 410 2100 E, 3080 m, 11 May 2005, Li H et al. 22707 (KUN); loc. eodem, 25 580 2100 N, 98 410 1.400 E, 3180 m, 14 May 2005, Li H et al. 22871 (KUN); loc. eodem, 25 580 2400 N, 98 410 1500 E, 3125 m, 19 May 2005, Li H et al. 24519 (KUN); loc. eodem, 25 590 200 N, 98 390 5800 E, 2950 m, 15 Oct. 1998, Li H, Bruce Bartholomew & Diao ZL 10436 (KUN); loc. eodem, 25 Sep. 2014, Li H, Yang J & Wang YH NJ-001-A2 (KUN); loc. eodem, 25 560 39.300 N, 98 440 54.800 E, 1710 m, 30 May 2015, Li H et al. 142-1 (KUN); loc. eodem, 2900 m, 04 Oct. 1997, Gaoligong Expedition 9932 (KUN); loc. eodem, 26 30 000 N, 98 390 3400 E, 2360 m, 15 May 2005, Li H et al. 22983 (KUN); loc. eodem, 26 30 4300 N, 98 370 8.700 E, 2057 m, Li H et al. 24085 (KUN); loc. eodem, 26 70 1400 N, 98 340 2500 E, 1600 m, 12 May 2005, Li H et al. 23990 (KUN). Lijiang: 22 May 1939, Qin RC 20521 (KUN). Ninger: 2800 m, 10 May 1955, Sino-Soviet Expedition 6280 (PE). Shangri-la: 02 Oct. 2002, Fang ZD et al. K-1328 (SABG). Tengchong: 25 460 5800 N, 98 360 58.800 E, 2220 m, 14 May 2006, Li H et al. 29425 (KUN);

6 Taxonomic Revision

loc. eodem, 25 430 57.100 N, 98 410 4100 E, 1960 m, 14 May 2006, Li H et al. 30036 (KUN); loc. eodem, 25 460 5800 N, 98 360 58.800 E, 2220 m, Li H et al. 29391 (KUN); loc. eodem, 24 510 1800 N, 98 450 4300 E, 2146 m, 27 May 2005, Li H et al. 25033 (KUN); loc. eodem, 1850 m, 19 May 1964, Wu SG 6734 (KUN); loc. eodem, 25 470 39.800 N, 98 370 18.500 E, 2650 m, 14 May 2006, Li H et al. 29277 (KUN); loc. eodem, 24 550 3800 N, 98 450 900 E, 2400 m, 04 Sep. 2003, Li H et al. 18755 (KUN); loc. eodem, 24 550 2600 N, 98 450 9.100 E, 2405 m, 30 May 2005, Li H et al. 25133 (KUN); loc. eodem, 1900 m, 01 Jan. 1992, Wu SG 6941 (KUN). Weixi: Nov. 1935, Wang QW 70462 (PE); loc. eodem, 2600–2700 m, 19 Jul. 1940, Feng GM 4935 (KUN, PE); loc. eodem, 20 May 1940, Feng GM 4045 (KUN); loc. eodem, 2500 m, 30 Apr. 1940, Feng GM 3567 (KUN); loc. eodem, 2500–2700 m, 26 May 1940, Feng GM 4171 (KUN). Yunlong: 2200 m, 02 Sep. 2016, Li H, Lei LG & Liu YC 036 (KUN). INDIA, Sirohi: 07 Apr. 1948, F. Kingdon-Ward 17221 (NY). NEPAL, Jumla: 23 Jul. 2019, Zhou GH s.n. (KUN).

6.5

Section Euthyra

Paris sect. Euthyra (Salisb.) Franch., Mem. Soc. Philim. Cent. (Paris) 24: 277. 1888. -P. sect. Dunniana H. Li in Act. Bot. Yunnan. 6: 357. 1984. -P. sect. Marmoratae H. Li in Act. Bot. Yunnan. 6: 357. 1984. -P. sect. Fargesianae H. Li in Act. Bot. Yunnan. 6: 359. 1984. Rhizome thick; stamens 2- to 4-whorled; ovary angular, 1-loculed with partial placentation; fruit a dehiscent capsule; seeds covered with red or orange sarcotesta. 10. Paris dunniana Lévl. In Fedde., Repert. Spec. Nov. Regni. Veg. 9: 78. 1910; H. Li, Act. Bot. Yunnan. 6 (4): 357. 1984; H. Li, The Genus Paris (Trilliaceae) 23. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 89. 2000.  Daiswa dunniana (Lévl.) Takht., Brittonia 35: 257 1983; B. Mitchell, Plantsman 10 (3):173. 1988. Type: China, Guizhou, Luodian, Mar. 1909, J. Cavalerie 3652 (Holotype, E; Isotype, E, PE). Paris hainanensis Merr., Philipp. J. Sci. 23: 238. 1923; Lingnan. Sci. Journ. 5: 43. 192; fl. Hainan. 4: 120, fig. 1027, 1977;  Daiswa hainanensis (Merr.) Takht., Brittonia 35: 258. 1983; B. Mitchell, Plantsman 10 (3): 175. 1988. Type: China, Hainan, Apr. 1920, McClure 9347 (Lectotype, PNH; Isotype, GH); loc. eodem, 21 Apr. 1922, McClure 9213 (Syntype, PNH). Perennial herb, 1.0–3.0 m tall. Rhizome thick, 8.0–19.0 cm long. Stem green or dark red, glabrous. Leaves 5–8, green, membranous, obovate-oblong, apex abruptly narrow. Flower solitary, basic merosity 5–8; pedicel erect, green or purple, ca. 60.0–15.0 cm long; sepals green, membranous, oblong-lanceolate, ca. 5.0–12.0 cm  1.5–3. 5 cm; petals

6.5 Section Euthyra

greenish-yellow, filiform. Stamens 3–4  petal number, 18.0–40.0 mm long; filaments green, 5.0–15.0 mm long; anthers 12.0–25.0 mm, free portion of connective acute, 1.0–4.0 mm long. Ovary ovoid with ridges, pale green or purple, 8.0 mm long, 5.0 mm thick, unilocular with parietal placentation. Ovules numerous, arranged along placentas. Style 1.0–3.0 mm, purplish-red, with an enlarged base; stigma 5–8, ca. 5.0 mm, curled after flowering. Capsule pale green at maturity, subspherical, ca. 2.5–4.0 cm in diameter, dehiscent. Seeds numerous, ca. 4.0 mm in diameter, irregular spherical, covered with orange sarcotesta (Figs. 6.22, 6.23 and 6.24). Phenology: flowering from March to April, capsule dehiscing from October to November. Habitats: evergreen broad-leaved forests; ca. 400–1100 m. Distribution: endemic to China: Guangxi (Fangchenggang), Guizhou (Luodian), Hainan (Baoting). Additional specimens examined. CHINA, GUANGXI, Fangchenggang: 22 Mar. 2010, Shiwan Mountain Collection Team 2088 (IBK). Shangsi: 29 Mar. 1991, Huang CC 21466 (GXMI). HAINAN, Baoting: 21 Dec. 1954, Diaoluoshan Expedition 3248 (PE); loc. eodem, 07 Jun. 1935, Hou KZ 72769 (IBK); loc. eodem, 26 Apr. 1935, Hou KZ 72153 (IBK). 11. Paris vietnamensis (Takha.) H. Li, Act. Bot. Yunnan 6 (4): 357. 1984; H. Li, Bull. Bot. Res. Harbin 6 (1): 113. 1986; H. Li, The Genus Paris (Trilliaceae) 27. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 89. 2000.  Daiswa hainanensis (Merr.) Takht. subsp. vietnamensis Takht., Brittonia. 35 (3): 259. 1983; B. Mitchell, Plantsman 10 (3): 176. 1988. TYPE: Vietnam, Tam Dao, 14 Jun. 1981, G. Yakovlev et al. 860a (Holotype, LE; Isotype, HNV). Perennial herb. Rhizome thick, brown outside and white inside, ca. 20.0–40.0 cm  5.0–10.0 cm. Stem green, cylindrical, 30.0–150.0 cm tall. Leaves 4–7; leaf blades membranous, green, oblong, obovate-oblong, and obovate, apex acuminate, base rounded to broad cuneate, ca. 10.0–30.0 cm  5.0–50.0 cm; lateral veins 2 pairs, basally developed; petiole purple, 3.5–10.0 cm long. Flower solitary, basic merosity 4–7; sepals, green, lanceolate or oblong-lanceolate, ca. 3.0–10.0 cm  1.0–4.0 cm; petals yellowish-green, filiform or linear, ca. 3.5–10.0 cm  0.5–3.5 mm, longer than or as long as sepals. Stamens 2 or 3  petal number; filaments purple, 4.0–10.0 mm long; anthers brown, 8.0–13.0 mm long, dehiscing by a lateral slit; free portion of connective usually purple, 1.0–4.0 mm long. Ovary pale purple, green occasionally, unilocular with parietal placentation, 4–7 ridged; style cyan purple, inconspicuous, base thickened; stigmas 4–7, 5.0–10.0 mm long, outside curved. Capsule pale green, ca. 2.5–4.0 cm in diameter, purplish-red apically, dehiscing along longitudinal ridges. Seeds numerous

123

subglobose, 3.0–6.0 mm in diameter, enveloped by orange succulent testa (Figs. 6.25, 6.26 and 6.27). Phenology: flowering January–March, fruiting April– December. Habitats: evergreen broad-leaved forests; ca. 600–2000 m. Distribution: China: Guangxi (Hezhou, Luocheng), Yunnan (Cangyuan, Jianshui, Jingdong, Jinghong, Jinping, Lüchun, Maguan, Malipo, Mangshi, Menghai, Mengla, Pingbian, Qiubei, Shuangbai, Shuangjiang, Xichou). Laos (Oudomxai). Vietnam (Mai Châu). Additional specimens examined. CHINA, GUANGXI, Hezhou: 21 Oct. 2009, Jiang SH & Hang YS JRH852 (IBK). Luocheng: 07 Jun. 1957, Chen XQ 1164 (KUN). YUNNAN, Cangyuan: 830 m, 24 May 1974, Li YH 011607 (KUN). Jianshui: 09 Apr. 1933, Cai XT 53106 (PE). Jingdong: 1800 m, 28 Apr. 1959, Xu SG 5049 (KUN); loc. eodem, 2200 m, 01 Jan. 1940, Li MG 3534 (KUN). Jinghong: 01 Sep. 1936, Wang QW 78693 (KUN). Jinping: 25 Apr. 1956, Sino-Soviet Expedition to Yunnan 544 (PE); loc. eodem, 12 May 1956, Sino-Soviet Expedition to Yunnan 1384 (PE). Lüchun: 1900 m, 19 Sep. 1973, Tao DD 187 (KUN). Maguan: 1450 m, 14 Jun. 1959, Wu QA 8405 (KUN). Malipo: 11 Feb. 1940, Wang QW 86740 (PE). Mangshi: 2100 m, 06 Sep. 1958, Xiong RL 580230 (KUN). Menghai: May 1984, Tao GD 44099 (HITBC). Mengla: 680 m, 16 Oct. 1959, Yunnan Tropical Expedition 59-13375 (KUN). Pingbian: 19 Apr. 1933, Cai XT 55234 (PE); loc. eodem, 13 Jul. 1934, Cai XT 60845 (PE). Qiubei: 1360 m, 09 Oct. 1980, Li H 310 (KUN). Shuangbai: 1450 m, 01 Oct. 1958, Huang SQ 0143 (KUN). Shuangjiang: 1550 m, 10 Sep. 1957, Xin JS 817 (KUN). Xichou: 06 May 1959, Wu QA 7901 (KUN). LAOS, OUDOMXAI: 09 Dec. 1996, Wang H & Li BG 3116 (HITBC). VIETNAM, Mai Châu: 22  440 4000 N, 104 520 3200 E, 1300–1440 m, 09 Apr. 2001, L. Averyanov & P. K. Loc HAL834 (NY). 12. Paris xichouensis (H. Li) Y. H. Ji, H. Li & Z. K. Zhou, Acta Phytotaxon. Sin. 44 (5): 612–613. 2006.  Paris cronquistii Takht. var. xichouensis H. Li, Bull. Bot. Res. Harbin 6 (1):113. 1986; H. Li, The Genus Paris (Trilliaceae) 26. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 89. 2000. Type: China, Yunnan, Xichou, Wang SZ 483 (Holotype, KUN). Perennial herb. Rhizome thickened, 2.0–8.5 cm long, 2.0–5.0 cm in diameter. Stem erect, 20.0–100.0 cm tall, green, often reddish purple. Leaves 4–7, green; leaf blades oblong or ovate, base cordate, sparsely rounded, apex abruptly narrow, caudiform, ca. 20.0–30.0 cm  10.0–20.0 cm, 2–3 pairs of lateral veins, basally developed; petiole 3.0–8.5 cm long, purple. Flower solitary, basic merosity

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Fig. 6.22 Paris dunniana (drawn by M. Shen). Rhizome (a), aerial shoot (b), flower (c), young fruit (d), and dehisced capsule (e)

6.5 Section Euthyra

125

Fig. 6.23 Habitat and plant height of Paris dunniana

4–7; pedicels 15.0–80.0 cm long, green or purple; sepals green, lanceolate, or ovate-lanceolate, ca. 3.0–12.0 cm  1.0–2.5 cm; petals yellowish green, filiform, shorter than sepals. Stamens 3  petal number, 19.0–30.0 mm long; filaments pale green, 3.0–10.0 mm long; anthers golden yellow, 10.0–15.0 mm long, dehiscing by a lateral slit; free portion of connective green, 1.0–6.0 mm long. Ovary green, with 4–7 ridges, unilocular with parietal placentation; ovules numerous, arranged in 2 rows along the placenta; style 2.0–3.0 mm long, purplish-red, slightly

concave; style cyan-purple, yellowish red, thickened; stigmas 4–6, yellowish red or purple, usually revolute. Capsule green to red, ca. 1.5–3.0 cm in diameter, dehiscent. Seeds numerous, subglobose, covered by an orange succulent testa (Figs. 6.28 and 6.29). Phenology: flowering February–April, fruiting May– November. Habitats: evergreen broad-leaved forests; 1200–1500 m. Distribution: China: Yunnan (Malipo, Xichou). Vietnam (Ha Giang).

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6 Taxonomic Revision

Fig. 6.24 Aerial shoot (a), flower (b), pistil (c), transverse section of ovary (d), and leaf morphology (e, f) of Paris dunniana

6.5 Section Euthyra

Fig. 6.25 Paris vietnamensis (drawn by M. Shen). Rhizome (a), stem and leaves (b), flower (c), and capsule (d)

127

128

Fig. 6.26 Flower (a), pistil (b, c), longitudinal section of ovary (d), and dehisced capsule (e) of Paris vietnamensis

6 Taxonomic Revision

6.5 Section Euthyra

Fig. 6.27 Leaf shape variation in Paris vietnamensis

129

130

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Fig. 6.28 Paris xichouensis (drawn by M. Shen). Rhizome (a), stem and leaves (b), flower (c), young fruit (d), dehisced capsule (e)

6.5 Section Euthyra

131

Fig. 6.29 Aerial shoot (a), flower (b), leaves (c, d), pistil (e), young fruit (f), transverse section of ovary (g), and matured fruit (h) of Paris xichouensis

132

Notes: P. xichouensis was first described as a variety under P. cronquistii by Li (1986). Based on molecular evidences, Ji et al. (2006b) raised its taxonomic status as a species. This treatment was justified by recent phylogenetic analyses of complete plastomes and nuclear ribosomal DNA sequences (Ji et al. 2019). Additional specimens examined. CHINA, YUNNAN, Malipo: Yang SX & Gong X 98846 (KUN). Xichou: Ji YH 0249 (KUN); loc. eodem, 1060 m, 26 May 1964, Wang SZ 483A (KUN); loc. eodem, 1060 m, 26 May 1964, Wang SZ 483B (KUN). VIETNAM, Ha Giang: Nguyen Quynh Nga & Pham Thanh Huyen 10512 (NIMM). 13. Paris chinensis Franch., Nouv. Arch. Mus. Hist. Nat. II, 10: 97. 1888; Hand.-Mazz., Symb. Sin. 7: 1215. 1936; T. C. Huang et K. C. Yang, Taiwania 33: 122. 1988; B. Mitchell, Plantsman 10 (3): 170, 171. 1988.  Paris polyphylla Smith var. chinensis (Franch.) Hara, Journ. Fac. Sci. Univ. Tokyo sect. 3, 10 (10): 176. 1969; H. Li, Bull. Bot. Res. Harbin 6 (l): 122. 1986; Wang et Tang, Fl. Reip. Pop. Sin. 15: 92, pl. 32: 1–3. 1978; H. Li, The Genus Paris (Trilliaceae) 37. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 90. 2000.  Daiswa chinensis (Franch.) Takht., Brittonia 35: 259. 1983. Type: China, Sichuan, Baoxing, 1870, A. David s. n. (Holotype, P). Paris polyphylla Smith var. platipetala Franch., Journ. Bot. (Morot) 12: 191. 1898; P0 ei et Chou, lcon. Chin. Medic. Pl. 7: fig. 303. 1964. Type: China, Chongqing, Chengkou, 2000 m, Farges 573 (Holotype, P). Paris formosana Hayata, Journ. Coll. Sci. Imp. Univ. Tokyo 30 (1): 367. 1911. Type: China, Taiwan, 1908, T. Kawakami & U. Mori 3573 (Holotype, GH). Paris kwantungensis Miao, Acta Sci. Nat. Univ. Sunyatseni 3: 74. 1982.  Paris polyphylla Smith var. kwantungensis (R. H. Miao) S. C. Chen & S. Y. Liang, Acta Phytotax. Sin. 33: 490. 1995. Type: China, Guangdong, Xinyi, 21 Mar. 1932, C. Wang 32199 (Holotype, SYS). Paris brachysepala Pamp., Nuovo Giorn. Bot. Ital. n. s., 22: 266. 1915.  Daiswa chinensis Franch. subsp. brachysepala (Pamp.) Takht., Brittonia 35: 262. 1983. Type: China, Hubei, Jun. 1912, C. Silvestri 3384 (Holotype, FI). Perennial herb. Rhizome thickened, ca. 8.0–25.0 cm  1.5–10.0 cm. Stem erect, cylindrical, green or reddish purple, 25.0–84.0 cm tall, glabrous, yellowish green occasionally, purple at upper portion. Leaves 5–12 in a whorl; leaf blades green, oblong, ovate, lanceolate or oblanceolate, base cuneate (rarely rounded), ca. 8.0–20.0 cm  2.0–8.0 cm; petiole green or purple, 0.1–3.5 cm long. Flower solitary, basic merosity 4–8; sepals green, lanceolate, ca. 2.5–8.0  0.8–3 cm; petals yellowish green, linear (up to 3.0 mm wide), much shorter (occasionally slightly longer) than sepals, usually reflexed. Stamens in 2  petal number, arranged in whorls, 9.0–18.0 mm long;

6 Taxonomic Revision

filaments pale green, 3.0–7.0 mm long; anthers yellow, 5.0–10.0 mm long, dehiscing by a lateral slit; free portion of connective inconspicuous, or 0.5–2.0 mm, acute. Ovary unilocular with parietal placentation, green, smooth or tuberculate, with 4–8 ridges. Style purple or dark red, 0–2.0 mm, with an enlarged base; stigmas purple or dark red, 4.0–10.0 mm long, erect at flowering, revolute at fruiting. Capsule subglobose, green, 2.0–5.0 cm in diameter, dehiscing irregularly. Seeds numerous, ovoid, enveloped by red and juicy sarcotesta (Figs. 6.30, 6.31 and 6.32). Phenology: flowering from March–May, fruiting June– October. Habitats: evergreen (deciduous) broad-leaved and coniferous forests, bamboo thickets, and scrubs; ca. 150–2800 m. Distribution: China: Anhui (Chizhou, Huangshan, Huoshan, Ningguo), Chongqing (Beibei, Chengkou, Fengdu, Jiangjin, Nanchuan, Pengshui, Qianjiang, Wulong, Wuxi, Youyang, Yunyang, Zhongxian), Fujian (Anxi, Jiangle, Jianyang, Liancheng, Nanjing, Pinghe, Pucheng, Shanghang, Shaowu, Taining, Tong’an, Wuyi Mountain, Yanping, Yongchun, Yongtai), Guangdong (Conghua, Dapu, Deqing, Fengkai, Guangning, Heping, Huaiji, Huicheng, Jiaoling, Lechang, Lianping, Lianyang, Longmen, Meixian, Raoping, Qujiang, Renhua, Ruyuan, Shixing, Xinyi, Yangchun, Yangshan, Yingde, Zengcheng), Guangxi (Binyang, Fengshan, Gongcheng, Hengxian, Huanjiang, Jinxiu, Lingui, Lingyu, Longlan, Longlin, Longsheng, Longzhou, Mashan, Pingnan, Quanzhou, Rongshui, Shangsi, Tiane, Tianlin, Wuming, Xilin, Xing’an), Guizhou (Anlong, Anshun, Chishui, Dafang, Daozhen, Duyun, Hezhang, Huishui, Jiangkou, Jinping, Kaili, Leishan, Liuzhi, Puding, Shiqian, Suiyang, Xingyi, Xishui, Xiuwen, Zhengan), Henan (Luanchuan, Lushan, Neixiang, Ruyang, Shangcheng, Songxian, Xiuwu, Xixia), Hubei (Badong, Fangxian, Hefeng, Shennongjia, Tongshan, Xingshan, Xuanen, Yingshan), Hunan (Anyang, Baojing, Chaling, Daoxian, Dong’an, Fenghuang, Hengshan, Hongjiang, Jishou, Lianyuan, Linwu, Longshan, Pingjiang, Sangzhi, Shimen, Suining, Xinning, Yanling, Yizhang, Yongshun, Yuanling, Zhijiang), Jiangsu (Jiangpu, Jurong), Jiangxi (Anfu, Anyuan, Chaisang, Chongyi, Dingnan, Fuliang, Fenyi, Guangchang, Guixi, Huichang, Jing’an, Jingangshan, Jiujiang, Julian Mountain, Lichuan, Longnan, Lushan, Ningdu, Ruijin, Shangyou, Shicheng, Suichuan, Wuning, Wuyuan, Xiushui, Yanshan, Yifeng, Yihuang, Yongxin), Shaanxi (Chang’an, Baoji, Danfeng, Fengxian, Foping, Huayin, Huxian, Meixian, Nanzheng, Ningshan, Pingli, Shiquan, South Mount Wutai, Taibai, Zhen’an, Zhashui), Shanxi (Anze, Huozhou, Jishan, Lingbao, Lishan, Ta-pieh Mountains, Yangcheng, Yicheng, Yuanqu), Sichuan (Baoxing, Beichuan, Cangxi, Dujiangyan, Emeishan, Hanyuan, Heishui, Jiulong, Kangding, Lixian, Luding, Mabian, Maoxian, Muli, Ningnan, Ningnan, Tianquan, Wanyuan,

6.5 Section Euthyra

Fig. 6.30 Paris chinensis (drawn by M. Shen). Rhizome and stem (a), leaves and flower (b), and dehisced capsule (c)

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134

Fig. 6.31 Leaf shape variation in Paris chinensis

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6.5 Section Euthyra

Fig. 6.32 Paris chinensis. Flower (a), young fruit (b), dehisced capsule (c), pistil (d), longitudinal (e), and transverse (f) section of ovary

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136

Weiyuan, Wenchuan, Yanbian, Yibin), Taiwan (Chiayi, Hsinchu, Hualien, Miaoli, Nantou, New Taipei, Taichung, Taidong, Taipei, Yilan, Yunlin), Yunnan (Chengjiang, Daguan, Huize, Jingdong, Jinghong, Jinping, Longling, Lüchun, Luoping, Luxi, Malipo, Mengla, Pingbian, Shizong, Weixin, Wenshan, Xichou, Xinping, Yongde, Yongshan, Yuanyang, Zhaoyang), Zhejiang (Anji, Hangzhou, Lin’an, Longquan, Kaihua, Suichang, Tiantai, Wuyi, Wencheng, Xianju, Yunhe, Zhoushan). Thailand (Lampoon, Mae Fa Luang). Vietnam (Ha Giang). Notes: Hara (1969) reduced P. chinensis as a conspecific variety under P. polyphylla, and the treatment was followed by Wang and Tang (1978), Li (1984a, 1998), and Liang and Soukup (2000). Nevertheless, our molecular phylogenetic studies revealed that P. chinensis is genetically distinct from P. polyphylla (Ji et al. 2019, 2020), which provide support for recognizing it as a distinct species. Additional specimens examined. CHINA, ANHUI, Chizhou: 18 May 2016, Shao JW, Zhang W & Meng WQ ANUB01079 (HZU). Huangshan: 06 Sep. 1935, Liou TN & Tsoong PC 3124 (PE); loc. eodem, 12 May 2016, Li HQ et al. ecnu0866 (HZU); loc. eodem, 12 Apr. 2017, Li P et al. HZU30471 (HZU); loc. eodem, 29 Mar. 1983, Wang XW 888A (IBSC); loc. eodem, 04 Jun. 1964, Yan ZN 2540 (HHBG). Huoshan: 25 Apr. 1983, Deng MB & Yao G 81547 (NAS); loc. eodem, 18 Jun. 2005, Liu M et al. A50065 (PE). Jinzhai: 14 May 1984, Yao G 8944 (KUN). Ningguo: 1000 m, 21 May 2006, Liu M A70062 (KUN). Yuexi: 05 May 2014, Zhao XL s. n. (PE). CHONGQING, Beibei: 29 Mar. 1964, Guan KJ, Wang JW & Li ZL 0067 (PE); loc. eodem, 05 Jul. 2016, He S JYSC0414 (HWA); loc. eodem, Apr. 1989, Yang YL 1969 (HWA); loc. eodem, Mar. 1981, Huang ZM 360 (HWA). Chengkou: 24 Jun. 1958, Dai TL 100996 (PE); loc. eodem, 16 Aug. 1958, Dai TL 101923 (PE). Fengdu: 02 Sep. 1997, Liu ZY 972035 (IMC). Jiangjin: 08 Mar. 2016, Liu ZY et al. S-0436 (IMC); loc. eodem, 10 Mar. 2016, Liu ZY et al. S-0228 (IMC); loc. eodem, 22 Apr. 2017, Liu ZY et al. S-1453 (IMC); loc. eodem, 10 Apr. 2017, Liu ZY et al. S-1257 (IMC); loc. eodem, 26 Jul. 2004, Liu X 20141688 (IMC); loc. eodem, 02 Jul. 2012, Jiangjin Expedition 500116-250 (IMC). Nanchuan: 1700–1800 m, 11 Apr. 2014, Wu L et al. 4514 (BNU); loc. eodem, 1600 m, 08 Jun. 1986, Liu ZY 8882 (IMC); loc. eodem, 1000 m, 11 Jun. 1986, Liu ZY 8921 (IMC); loc. eodem, 1000 m, 11 Jun. 1986, Liu ZY 8926 (IMC); loc. eodem, 1000 m, 11 Jun. 1986, Liu ZY 8955 (IMC); loc. eodem, 900 m, 11 Jun. 1986, Liu ZY 8990 (IMC); loc. eodem, 850 m, 11 Jun. 1986, Liu ZY 9188 (IMC); loc. eodem, 850 m, 11 Jun. 1986, Liu ZY 9198 (IMC); loc. eodem, 15 Apr. 1984, Liu ZY 4892 (IMC); loc. eodem, 08 Apr. 1980, Specimen Group 801821 (IMC); loc. eodem, 08 Apr. 1980, Specimen Group 801820 (IMC); loc.

6 Taxonomic Revision

eodem, 08 Apr. 1980, Specimen Group 801830 (IMC); loc. eodem, 17 Apr. 1957, Li GF 60556 (IBSC); loc. eodem, 11 Apr. 1957, Li GF 60429 (IBSC); loc. eodem, 09 Apr. 2008, Liu ZY 2080218 (IMC); loc. eodem, 16 May 1976, Liu ZY 760233 (IMC); loc. eodem, 03 May 1957, Xiong JH & Zhou ZL 90674 (IBSC); loc. eodem, 06 May 1964, Chen XQ & Liang YK 2168 (PE); loc. eodem, 06 May 1964, Chen XQ & Liang YK 02169 (PE); loc. eodem, Chu KL 1173 (PE). Pengshui: 16 May 2007, Feng ZB, Zhu DH & Li XJ 20070415 (HX); loc. eodem, 20 Jun. 2012, Pengshui Expedition 500243-002-069-01 (IMC). Qianjiang: 10 May 1979, Liu ZY 297 (IMC); loc. eodem, 18 Aug. 1988, Zhao ZC 88-1790 (IMC). Wulong: 07 Nov. 2007, Liu ZY 181606 (IMC); loc. eodem, 25 Apr. 1998, Liu ZY 981097 (IMC). Wuxi: 12 Jul. 2004, Chen YS et al. 1508 (WUK); loc. eodem, Aug. 2016, He S WX1605003 (HWA). Youyang: 22 Aug. 1984, Liu ZY 6759 (IMC). Yunyang: 28 May 2013, Yunyang Expedition 500235-130528-480-LY (IMC). Zhongxian: 12 May 2013, Zhongxian Expedition 500233-130512-235LY (IMC). FUJIAN, Anxi: 17 Apr. 1958, Fang YY & Lin JH 1002 (FJIDC). Jiangle: 400–660 m, 21 May 1991, Longxi Mountain Expedition s. n. (HAST). Jianyang: 22 Mar. 2018, Hou XL & Zhang RP 91550 (AU). Liancheng: 13 Oct. 1932, Wang DS 990 (PE); loc. eodem, 11 Oct. 1932, Lin R 3883 (PE). Nanjing: 06 May 1959, Huang SM 190139 (IBSC); loc. eodem, 05 May 1959, Wu ZF 150023 (IBSC); loc. eodem, 31 Jul. 1963, Xiamen University 392 (PE). Pinghe: 15 Apr. 1954, Wang 3710 (AU); loc. eodem, 15 Apr. 1954, Wang 3712 (AU). Pucheng: 14 Apr. 1958, Hou YM & Zheng RH (FJIDC). Shanghang: 20 Oct. 1982, Zhang YT 82115 (FJSI); loc. eodem, 05 Aug. 1987, Li HB 1441 (FJSI). Shaowu: 04 Nov. 1935, Zhou HC 5354 (IBSC). Taining: 03 Jun. 1979, Li MS 193 (IBSC, FJSI). Tong’an: 11 Apr. 1958, Fang YY & Lin JH s. n. (FJIDC). Wuyi Mountain: 20 Jul. 1980, Wuyi Mountain Expedition 80-0154 (IBSC); loc. eodem, 15 Aug. 1958, Qiu PX 1978 (PE). Yanping: 02 May 2016, Hou XL 2016050270 (AU). Yongchun: 28 Apr. 1958, Fang YY & Lin JH s. n. (FJIDC). Yongtai: 30 Aug. 1960, s. n. (FJIDC). GUANGDONG, Conghua: 16 Nov. 1958, Deng L 8555 (IBSC); loc. eodem, 03 Mar. 1935, Tsang WT 24973 (IBSC); loc. eodem, 07 Apr. 1958, Huang Z 44817 (IBSC). Dapu: 09 May 1984, Dapu Expedition 462 (IBSC). Deqing: 27 Jul. 1958, Liu YG 1159 (IBSC). Fengkai: 15 Jun. 1958, Huang C 164327 (IBSC); loc. eodem, 01 Dec. 1980, Ding GQ & Yu L 6855 (IBSC). Guangning: 21 Aug. 1983, Shi GL 14450 (IBSC). Heping: 03 Aug. 1987, Zhang GC et al. 329 (IBSC). Huaiji: 31 Sep. 1933, Tsang WT 22915 (IBSC); loc. eodem, 20 Nov. 1933, Tsang WT 23232 (IBSC). Huicheng: 16 Apr. 1931, Gao XP 51326 (IBK). Jiaoling: 06 May 1957, Deng L 4546 (IBK). Lechang: 10 Apr. 1959, Cheng YQ 170005 (IBSC); loc. eodem, 07 Dec. 1931, Gao XP 51977 (IBSC); loc. eodem, 22 Apr. 1943, Chen SQ 3147 (IBSC); loc. eodem, 15 May

6.5 Section Euthyra

1972, Luo XR 549 (IBSC); loc. eodem, 25 Nov. 1930, Chen NQ 42271 (IBSC); loc. eodem, 22 Apr. 1942, Chen SQ 3147 (IBK). Lianping: 04 May 1957, Liu YG 159 (IBSC, PE). Lianyang: 12 Jun. 1959, Wu SZ 70198 (IBSC); loc. eodem, 13 Oct. 1958, Tan PX 59817 (IBSC); loc. eodem, 22 May 1958, Tan PX 57995 (IBSC). Longmen: 22 Jul. 1981, Zhang GC 257 (IBSC); loc. eodem, 23 Oct. 1996, Chen BH 48 (IBSC). Meixian: 04 Aug. 1932, Tsang WT 21439 (IBSC); loc. eodem, 08 Jun. 1959, Li SY 180185 (IBSC). Qujiang: 27 Mar. 1930, Gap XP 50208 (PE). Raoping: 16 Apr. 1931, Chen NQ 42672 (IBSC). Renhua: 21 Sep. 1958, Deng L 7726 (IBSC); loc. eodem, 11 May 1936, Tsang WT 26353 (IBSC). Ruyuan: 08 Apr. 1971, Yue71 22 (IBSC); loc. eodem, 26 Nov. 1956, Huang Z 42643 (IBSC); loc. eodem, Jun. 1933, Gao XP 9108 (PE); loc. eodem, Huang Z 44063 (IBSC). Shixing: 09 Jul. 1958, Deng L 6682 (IBSC); loc. eodem, 27 Jun. 1982, Shixing Collection Team 69 (IBSC). Xinyi: 15 Jan. 2003, Tan CM et al. Xinyi505 (IBSC); loc. eodem, 24 Apr. 1932, Huang Z 32198 (IBSC, IBK). Yangchun: 19 May 1991, Liu N et al. 1797 (IBSC). Yangshan: 21 Nov. 1958, Tan PX 60284 (IBSC); loc. eodem, 20 Oct. 1970, Chinese Medicinal Herbs Survey s. n. (IBSC). Yingde: 06 May 1930, Gao XP 50474 (PE). Zengcheng: 21 Apr. 1932, Tsang WT 20634 (PE); loc. eodem, 11 Apr. 1932, Tsang WT 20192 (PE); loc. eodem, 21 Apr. 1932, Tsang WT 20295 (PE). GUANGXI, Binyang: 13 May 1957, Chen ZZ 50551 (IBK). Fengshan: 06 Oct. 1958, Chang CC 11246 (IBSC). Gongcheng: 13 Jun. 1994, DQ 940244 (GXMI). Hengxian: 06 May 1957, Chen ZZ 50471 (PE). Huanjiang: 21 Apr. 2012, Jiang RH, Yang JC & Mo SS 11491 (IBK); loc. eodem, 21 Apr. 2012, Huang YS, Liao YB & Han MQ Y1363 (IBK). Jinxiu: 12 Sep. 1981, Dayao Mountain Expedition 10506 (IBK, IBSC); loc. eodem, 25 Aug. 1993, DZ 930124 (GXMI); loc. eodem, 07 Mar. 2013, Guo M et al. 451324130307007LY (GXMG). Lingui: 22 Mar. 1953, Chen SQ 94520 (IBSC, BJM); loc. eodem, 1153 m, 17 Apr. 2014, Gui LJ 450322140417016LY (GXMG). Lingyun: 20 Apr. 1957, Huang Z 43153 (IBSC). Longlan: 23 Jun. 1957, Huang Z 43595 (IBSC). Longlin: 25 May 1957, Liang CF & Wu DL 32357 (IBSC); loc. eodem, 25 May 1957, Liang CF & Wu DL 32383 (IBSC). Longsheng: 10 Oct. 1956, Yu SL & Qin HF 700683 (IBSC); loc. eodem, 04 Jul. 1957, Qin HF & Li ZT 700683 (IBSC); loc. eodem, 26 Jun. 1958, Chen ZZ 51067 (PE); loc. eodem, 19 Apr. 2014, Longsheng Expedition 450328140419042LY (GXMI). Longzhou: 07 Jun. 1957, Chen SQ 11643 (IBSC). Mashan: 06 Sep. 1958, Zhong SQ 301537 (KUN). Napo: 07 May 2013, Wu L 3553 (BNU); loc. eodem, 26 Apr. 1989, S China Expedition 148 (IBSC); loc. eodem, 27 Oct. 1935, Gao XP 55973 (IBSC). Pingnan: 21 May 1936, Huang Z 39238 (IBSC); loc. eodem, 17 Jul. 1934, Wang ZR 5276 (IBSC). Quanzhou: 18 Jun. 1959, Huang DA 60402 (IBSC); loc. eodem, 26 Jun.

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1937, Zhong JX 83350 (IBSC); loc. eodem, 13 May 1936, Zhong JX 81608 (IBSC). Rongshui: 1200 m, 20 Jun. 1958, Chen SQ 14585 (PE); loc. eodem, 2000 m, 15 Jun. 1959, Lv QH 2489 (PE); loc. eodem, 07 Nov. 2001, Damiao Mountain Expedition D1126 (IBK); loc. eodem, Sep. 2001, Damiao Mountain Expedition D0109 (IBK); loc. eodem, 14 Jun. 1992, Liang DR & Li L 08276 (GXMG). Shangsi: 28 Apr. 1944, Chen SQ 5013 (IBSC). Tiane: 19 Aug. 2014, Tiane Expedition 451222140819020LY (GXMG). Tianlin: 26 Apr. 2013, Tianlin Expedition 451029130426021 (GXMI); loc. eodem, 14 Mar. 2013, Tianlin Expedition 451029130314096 (GXMI); loc. eodem, 30 Nov. 1986, Longtan Expedition 01390 (IBK). Wuming: 05 Aug. 2010, Wu L et al. D0323 (IBK); loc. eodem, 27 Mar. 2011, Wu L et al. D1793 (IBK); loc. eodem, 29 Jun. 1990, Huang CC et al. 03840 (GXMI). Xilin: 25 Jun. 1936, Su HH 67829 (IBSC). Xing’an: May 1953, Guangxi Expedition 480 (IBSC); loc. eodem, 27 May 1953, Guangxi Expedition 805 (IBSC); loc. eodem, 25 Jul. 1958, Chen ZZ 51304 (IBSC); loc. eodem, 16 May 1982, Li GZ 11504 (IBK); loc. eodem, 29 May 1980, Li GZ & Lu B 10407 (IBK). GUIZHOU, Anlong: 22 Jun. 1960, Guizhou Expedition 5682 (IBSC); loc. eodem, 13 Jun. 1960, Zhang ZS & Zhang YT 5233 (PE). Anshun: 30 Mar. 1935, Feng SW 0133 (PE). Chishui: 06 Apr. 1990, Lan KM 90-0172 (GZAC). Dafang: 25 Apr. 2016, Wang YX 522422160425007LY (GZTM). Daozhen: 21 Apr. 2003, Liu ZY 2031036 (IMC); loc. eodem, 13 Jan. 2003, Liu ZY 2030065 (IMC); loc. eodem, 06 Apr. 2016, Survey 520325160406404 LY (GZTM); loc. eodem, 18 Aug. 1984, Wang, Chang & Chen D 0283 (GFS). Duyun: 1130 m, 28 May 2011, Zheng ZQ 1140183 (QNUN); loc. eodem, 28 May 2011, Wang B DPS20115351 (QNUN). Hezhang: 03 Jul. 2015, Rao YD 522428150703055 LY (GZTM). Huishui: 07 Jul. 1986, Wang P 02831 (ZY); loc. eodem, 21 May 1975, Huang WL & Tu YL 079 (GNUG). Jiangkou: 2200 m, 28 Jul. 1983, Hunan-Guizhou Expedition 002767 (KUN). Jinping: 04 Oct. 2014, Long ZC 522628141104263LY (GZTM); loc. eodem, Jun. 1965, Class 217 65.0163 (GFS). Kaili: 20 May 1959, Cao ZY 1840 (PE). Leishan: 28 Apr. 1959, S Guizhou Expedition 00852 (PE); loc. eodem, 30 Apr. 1959, S Guizhou Expedition 00946 (PE); loc. eodem, 22 Aug. 2015, Mao S 522634150822002LY (GZTM). Libo: 31 Aug. 2006, Liu LH G200040 (JIU). Liuzhi: 27 May 2014, Xiong HJ 520203140527001LY (GZTM). Puding: 20 Oct. 2014, Gu M 520422141120003LY (GZTM). Shiqian: 28 Jul. 1988, Wuling Mountain Expedition 2215 (PE). Suiyang: 06 Jun. 1982, Shi K 02831 (ZY). Xingyi: 20 Jul. 1960, Zhang ZS & Zhang YT 6408 (PE). Xishui: 25 Mar. 2016, Zhao FG 520330160325017 LY (GZTM); loc. eodem, 08 Mar. 2013, Rao ZT XS026 (ZY). Xiuwen: 01 Oct. 2015, Guo ZK 520123151001244LY (GZTM). Zhengan: Zheng JH 520324151016006LY (GZTM). HENAN, Luanchuan:

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13 Jun. 2015, Yang WG 168 (HEAC). Lushan: 26 Apr. 2015, Yang WG 174 (HEAC). Neixiang: 33 230 6000 N, 111 520 6000 E, 1400–1600 m, 27 May 1994, D. E. Boufford et al. 26281 (HAST). Ruyang: 1959, Xinxiang University 22823 (PE). Shangcheng: 31 Aug. 1984, Plant Resources Expedition D1309 (PE); loc. eodem, Jul. 1978, Wang P 0342 (HENU); loc. eodem, Aug. 1958, Wang P 21631 (HENU); loc. eodem,Jul. 1978, Wang P 0243 (HENU). Songxian: 14 Sep. 1960, Guan KJ & Dai TL 2608 (PE). Xiuwu: Jun. 1997, Xing ZF 97061 (HENU); loc. eodem, Jun. 1997, Xing ZF 97032 (HENU); loc. eodem, Jul. 1998, Xin ZH 108 (HENU); loc. eodem, Jul. 1997, Xin ZH 011 (HENU); loc. eodem, May 1998, Fan XM 0009 (HENU). Xixia: 30 Jul. 1960, Guan KJ & Dai TL 1602 (PE). HUBEI, Badong: 22 Jul. 1957, Fu GX & Zhang ZS 00975 (IBSC, PE); loc. eodem, 06 Oct. 1952, Chen QL 1919 (PE). Fangxian: 23 Sep. 1958, Zhu GF 268 (IBSC); loc. eodem, 24 May 1987, Chen LQ IV040181 (CCAU). Hefeng: 13 May 1959, Peng FS 957 (WUK); loc. eodem, 14 Aug. 1988, Wang YM 6298 (PE). Shennongjia: 29 May 1987, Chen LQ IV040833 (CCAU); loc. eodem, 01 Jun. 1996, Ecology 25 (CTGU); loc. eodem, 1850 m, 22 Aug. 1976, Shennongjia Botany Expedition 30475 (PE). Tongshan: 28 Jun. 2000, Wang J 102 (CCAU). Xingshan: 24 May 1957, Liu Y 191 (PE). Xuanen: 10 Jul. 1958, Li HJ 3454 (PE). Yingshan: 27 May 1957, Liu YY 500 (NAS). HUNAN, Anyang: 2650 m, 18 Jun. 1973, Qinghai-Tibet Expedition 73-195 (KUN). Baojing: 10 Aug. 2012, Su XJ & Liu HB 433125D00030810119 (JIU); loc. eodem, 942 m, 14 Aug. 2012, Su XJ & Liu HB 433125D00020814050 (JIU). Chaling: 828 m, 15 Jul. 2014, Zhang DG & Chen GX LXP-06-1904 (JIU). Daoxian: 26 Jun. 1959, Tan PX 61834 (IBSC). Dong’an: 22 May 1965, Lin Y & Yang XX 16335 (IBSC); loc. eodem, 06 Apr. 1986, Huang QS 0533 (HUFD). Fenghuang: 800 m, 15 Sep. 1988, Wuling Mountain Expedition 1121 (PE). Hengshan: 27 May 1944, Zhang HD 3327 (IBSC); loc. eodem, 07 Apr. 1951, Hwang H & Chia 130510 (IBSC). Hongjiang: 06 May 1954, Li ZT 2038 (IBSC, PE); loc. eodem, Apr. 1953, Li ZT 727 (IBSC); loc. eodem, 670 m, 11 Apr. 2017, Li H, Gao XY & Liu CN 047 (KUN). Jishou: 01 May 1990, Gu Z 0218 (JIU). Lianyuan: 26 Apr. 1986, Nie JY et al. 002 (HUFD). Linwu: 27 Apr. 2016, Wu L, Luo JL & Wen ZJ 5161 (CSFI); loc. eodem, 1550 m, 05 Aug. 1964, Huang MX 111841 (IBSC, FJSI); loc. eodem, 04 Oct. 1960, Huang MX 111346 (IBSC). Longshan: 813 m, 10 Apr. 2013, Tian DK, Xiao Y & Chen Y LS-1262 (CSH). Pingjiang: 17 Nov. 2011, Xu YF et al. 1502 (CSFI); loc. eodem, 11 Jun. 2014, Zhou JJ & Zhou D 140611013 (CSFI). Sangzhi: 1600 m, 07 Jul. 1988, Beijing Expedition 002585 (PE); loc. eodem, 12 Jul. 2003, Tan CM et al. Sangzhi143 (JJF); loc. eodem, 15 Jun. 2016, Wu L & Zhou JJ 5449 (CSF); loc. eodem, 18 May 1988, Lin Q 318 (IBSC); loc. eodem, 07 Jul. 1988, Beijing Expedition 002673 (PE); loc. eodem, 04 Jul. 1988, Beijing Expedition

6 Taxonomic Revision

2267 (PE); loc. eodem, 1450 m, 28 Aug. 1988, Beijing Expedition 4237 (PE). Shimen: 700 m, 07 Jul. 1987, Hupingshan Expedition 1074 (PE). Suining: 07 May 2014, Zhou JJ & Song ZP 1405076 (CSFI); loc. eodem, 15 Apr. 2014, Zhou JJ & Song ZP 1404047 (CSFI); loc. eodem, 22 May 2013, Zhou JJ & Zhou D 13393 (CSFI). Xinning: Apr. 1985, Luo YB 2089 (PE); loc. eodem, 510 m, 12 Apr. 2017, Li H, Gao XY & Liu CN 048 (KUN); loc. eodem, 510 m, 12 Apr. 2017, Li H, Gao XY & Liu CN 049 (KUN). Yanling: 09 Apr. 2014, Liao WB, Zhao WY & Yang WS LXP13-5337 (SYS); loc. eodem, 11 Apr. 2014, Liao WB, Zhao WY & Yang WS LXP13-5505 (SYS); loc. eodem, 16 Apr. 2014, WB, Zhao WY & Yang WS LXP13-5566 (SYS). Yizhang: 28 Oct. 1944, Liang BH & Xu XH 85108 (IBSC); loc. eodem, 23 Jul. 1957, Liu LH 1372 (IBSC); loc. eodem, 25 Sep. 1942, Liang BH 83680 (IBSC); loc. eodem, 12 Jun. 1963 Department of Biology, Hunan University 6263 (NAS); loc. eodem, 11 May 1942, Chen SQ 977 (PE, IBSC); loc. eodem, 19 Oct. 1942, Chen SQ 2691 (PE). Yongshun: 1026 m, 31 May 2014, Lei KD 4331271405310445 (JIU); loc. eodem, 06 Aug. 1958, Liu LH 9437 (PE); loc. eodem, 23 Jul. 1953, Hunan Expedition 0182 (PE); loc. eodem, 700 m, 11 Jun. 1988, Beijing Expedition 1560 (PE); loc. eodem, 04 Jun. 1988, Beijing Expedition 01050 (PE); loc. eodem, 350 m, 31 May 1988, Beijing Expedition 0667 (PE); loc. eodem, 350 m, 29 May 1988, Beijing Expedition 295 (PE); loc. eodem, 520 m, 27 May 1988, Beijing Expedition 0245 (PE); loc. eodem, 900 m, 10 Jun. 1988, Beijing Expedition 01371 (PE); loc. eodem, 700 m, 11 Jun. 1988, Beijing Expedition 1559 (PE); loc. eodem, 10 Sep. 2004, Zhang H 040910098 (JIU); loc. eodem, 11 Jul. 2005, Xiao ZG 05071102 (JIU); loc. eodem, 13 Jul. 2006, Hu SF 0607132109 (JIU); loc. eodem, 18 Apr. 2008, Yang B 080418057 (JIU); loc. eodem, 16 Jul. 2007, Long DG 070716091 (JIU); loc. eodem, 12 Jul. 2008, Zhang DG 080712222 (JIU); loc. eodem, 271 m, 08 Mar. 2014, Zhang DG zdg4331270011 (JIU). Yuanling: 26 Jun. 1988, Wuling Mountain Expedition 625 (IBSC); loc. eodem, 600 m, 08 Jun. 1988, Wuling Mountain Expedition 55 (PE). Zhijiang: 16 Oct. 1988, Wuling Mountain Expedition 2250 (IBSC, PE); loc. eodem, 450 m, 28 May 1986, Chen ZB 288 (HUFD). JIANGSU, Jiangpu: 03 Jan. 1956, Deng MB, Yuan CT & Zhang GY 3788 (PE). Jurong: 06 Jun. 1920, Su LF 142 (PE). JIANGXI, Anfu: 14 Sep. 1954, Jiangxi Expedition 1252 (PE). Anyuan: 18 May 1958, Hu QM & Li QH 2018 (LBG). Chaisang: 24 Apr. 2018, Li XZ & Cai RY 1804248 (JJF); loc. eodem, 11 Apr. 2017, Yi GH 1704138 (JJF); loc. eodem, 12 Apr. 2016, Yi GH & Li XZ 1604211 (JJF); loc. eodem, 10 Jun. 2010, Tan CM, Yi GH & Zhang LP 10519 (JJF, CCAU); loc. eodem, 30 Mar. 2007, Huang DM 07045 (JJF, HIMC); loc. eodem, 23 Mar. 2007, Li XZ & Gan DZ 07026 (JJF); loc. eodem,17 Apr. 1990, Tan CM & Gui JH 90001 (JJF); loc. eodem, 07 Nov. 2009, Dong AM 1721

6.5 Section Euthyra

(SZG). Chongyi: 07 Jun. 1965, Nie MX et al. 8706 (LBG). Dayu: 21 Aug. 1964, Yang ZB & Yao G 1305 (PE); loc. eodem, 1962, Yue JS 1413 (PE, LBG); loc. eodem, 09 Jul. 1962, Yue JS 1563 (LBG). Dingnan: 19 May 1958, Hu QM 2080 (PE, LBG). Fenyi: 26 Mar. 1959, Lai SS 0029 (PE). Fuliang: 03 May 1959, Li QH & Chen C 705 (PE, LBG); loc. eodem, 16 May 1959, Li QH & Chen C 00860 (LBG). Guangchang: Oct. 1976, Shan HR & Zhang SC 762113 (LBG). Guixi: 16 Oct. 1979, Shen & Huang 140 (LBG). Huichang: 10 Jul. 1958, Hu QM 3398 (PE, LBG). Jing’an: 20 Oct. 1938, Xiong YG 01408 (LBG). Jingangshan: 24 May 2016, Zhao WY et al. LXP-13-18293 (SYS). Jiujiang: 16 May 1977, Wu ZY L144 (KUN). Julian Mountain: 05 Apr. 1993, Xie QH 93130 (IBSC); loc. eodem, 26 Oct. 1992, Tang PR & Liang YL 92008 (IBSC). Lianxi: 05 Oct. 2015, Dong AM 2228 (JJF); loc. eodem, 20 Jul. 2013, Dong AM 2077 (JJF); loc. eodem, 07 Apr. 2013, Tan CM, Yi GH & Cai RY 13068 (JJF); loc. eodem, 02 Nov. 2012, Dong AM 2050 (JJF); loc. eodem, 05 Aug. 2011, Dong AM 1938 (JJF); loc. eodem, 08 May 2011, Dong AM 1873 (JJF); loc. eodem, 28 Jun. 2009, Dong AM 1578 (JJF); loc. eodem, 19 Oct. 2008, Tan CM, Yi GH & Dong AM 081699 (JJF); loc. eodem, 21 Sep. 2006, Dong AM 1178 (JJF). Lichuan: 28 May 1958, Nie MX & Lai SS 2638 (PE, LBG); loc. eodem, 22 Apr. 2015, Tong HP 0008 (JJF); loc. eodem, 05 Oct. 2012, Tan CM et al. 12789 (JJF). Longnan: 09 Oct. 1959, Wang HC 99 (LBG); loc. eodem, 26 Apr. 1996, Tan CM & Zhu DH 9604178 (JJF, SZG); loc. eodem, 20 Apr. 1998, Tan CM, Mo D & Chen ZS 98052 (JJF). Lushan: 07 Apr. 2013, Tan CM, Yi GH & Cai RY 13068 (BH); loc. eodem, 14 Nov. 2017, Dong AM 2498 (JJF); loc. eodem, 10 May 2017, Cai RY et al. 1705370 (JJF); loc. eodem, 26 Oct. 2016, Dong AM 2416 (JJF); loc. eodem, 13 Apr. 2002, Tan CM, Yi LM & Li YZ 02065 (JJF); loc. eodem, 30 Apr. 1953, Wang MJ 1509 (NAS). Ningdu: Hu QM 5510 (PE). Ruijin: 08 Aug. 1958, Hu QM 4080 (IBSC, PE, LBG); loc. eodem, 15 Jul. 1958, Hu QM 3558 (PE, LBG). Shangyou: 02 Jun. 2015, Zhao WY et al. LXP-13-12442 (SYS); loc. eodem, 03 May 1965, Nie MX et al. 08008 (IBSC, LBG); loc. eodem, 800 m, 20 Jul. 1971, Jiangxi Expedition 0384 (PE). Shicheng: 21 Aug. 1958, Hu QM 4500 (LBG). Suichuan: 07 Apr. 1959, Lai SS 0088 (LBG); loc. eodem, 15 May 2016, Zhao WY et al. (SYS). Wuning: 20 Sep. 1938, Xiong YG 1222 (LBG); loc. eodem, 23 Aug. 2016, Zhang JH 2380 (JJF); loc. eodem, 18 Apr. 1996, Tan CM, Zhu DH & Cao ZH 9604093A (JJF); loc. eodem, 28 Oct. 1996, Tan CM, Zhang JH & Xiong JS 9610152 (JJF); loc. eodem, 19 Jul. 2000, Zhang JH 001031 (JJF); loc. eodem, 06 May 1997, Tan CM 97540 (SZG). Wuyuan: 05 Apr. 1959, Li QH & Chen C 136 (PE, LBG); loc. eodem, 1959, Li QH & Chen C 00352 (PE, LBG). Xiushui: 26 May 2007, Miao YQ 07573 (JJF); loc. eodem, Miao YQ & Yu YM 20150806 (JJF); loc. eodem, 13 May 2013, Miao YQ 1423 (JJF); loc. eodem, 04 Nov. 2011, Miao

139

YQ 1146 (JJF); loc. eodem, 15 Apr. 2006, Miao YQ 135 (JJF); loc. eodem, 26 May 2007, Miao YQ 07573 (SZG). Xunwu: 29 Apr. 1958, Hu QM 1580 (LBG); loc. eodem, 13 Aug. 1962, Yue JS et al. 1796 (PE, IBSC). Yanshan: 13 Apr. 2017, Tan CM et al. Tan17062 (JJF). Yifeng: 19 May 1959, Xiong J 3701 (LBG). Yihuang: 01 Jul. 1932, Jiang Y 197 (IBSC); loc. eodem, 14 Jul. 1959, Li QH & Chen C 1690 (PE, LBG). Yongxin: 11 Jul. 1959, Lai SS 1292 (PE, LBG); loc. eodem, 21 Jun. 2016, Zhao WY LXP-13-19187 (SYS). SHAANXI, Chang’an: 07 Jul. 1986, Li FR s. n. (XJTU). Baoji: 26 May 1977, Hu ZX & Guo YH 213 (IBSC). Danfeng: 23 Sep. 1958, He SB 411 (IBSC). Fengxian: 13 Jun. 1977, Fu KJ 17406 (WUK). Foping: 11 Jun. 1952, Fu KJ 4474 (PE). Huayin: 27 May 1938, W. Y. Hsia 4426 (PE). Huxian: 13 Jul. 1951, Guo BZ 346 (PE); loc. eodem, 19 Jun. 2003, Han J et al. 066 (XJTU). Meixian: 15 Jun. 1999, Zhu et al. 1301 (PE). Nanzheng: 17 Apr. 1973, Hou XX 288 (IBSC, WUK, FJSI); loc. eodem, 11 Apr. 1973, Hou XX 139 (WUK). Ningshan: 28 May 1959, Xing JQ 2608 (IBSC); loc. eodem, 04 Jun. 1959, Xing JQ 5683 (IBSC); loc. eodem, 27 Apr. 1988, Cui TC 1018 (PE). Pingli: 2050 m, 24 Jun. 2005, Chen YS et al. 3095 (WUK); loc. eodem, 05 Jul. 2004, Chen YS et al. 795 (WUK); loc. eodem, 24 May 1959, Li PY 2539 (WUK). Shiquan: 26 May 1959, Xing JQ 3595 (WUK). South Mount Wutai: 15 May 1939, Liou TN, Tsoong PC & Tien CS 196 (PE). Taibai: 29 Aug. 1937, T. N. Liou & P. C. Tsoong 333 (PE); loc. eodem, 01 Sep. 1937, T. N. Liou & P. C. Tsoong 520 (PE); loc. eodem, 11 Jul. 1955, Taibai Expedition 55223 (PE); loc. eodem, 1568 m, 30 Jul. 2009, Li SF et al. 12255 (XBGH); loc. eodem, 28 Jul. 2009, Li SF et al. 12137 (XBGH). Xunyi: 02 Apr. 1959, Zhong ZC 00303 (CDBI). Zhashui: 24 May 2013, Li SF et al. 17769 (XBGH). Zhen’an: 1250 m, 04 Jun. 1973, Hou XX & Guo YH 775 (FJSI); loc. eodem, 05 Jun. 1973, Hou XX & Guo YH 826 (FJSI). SHANXI, Anze: Jul. 2004, No. 2 Chinese Medicine Department 00000121 (SXTCM). Huozhou: 19 Jul. 1954, Shanxi Expedition 552 (PE). Jishan: 15 May 1959, Ma F 137 (WUK). Lingbao: 05 Aug. 2014, Li JM et al. 14080568 (HEAC). Lishan: Jun. 2002, Zhang ML 0203004 (SXTCM). Ta-pieh Mountains: Jul. 1978, Wang P 246 (HENU); loc. eodem, Aug. 1959, Wang P 0349 (HENU); loc. eodem, Jul. 1978, Henan University 0348 (HENU); loc. eodem, Jul. 1978, Wang P 0347 (HENU); loc. eodem, Wang P 0345 (HENU); loc. eodem, Wang P 0344 (HENU). Yangcheng: 28 Jul. 1959, Bao SY & Yan SJ 2146 (PE). Yicheng: 11 Oct. 1982, Fu KJ 18463 (XJTU). Yuanqu: 16 May 1960, Liu XY 20049 (PE); loc. eodem, 16 May 1960, Liu XY 20045 (PE). SICHUAN, Baoxing: Apr. 1954, Song ZP 38154 (IBSC); loc. eodem, 19 May 1958, Zhang XS & Ren YX 4838 (PE); loc. eodem, 03 Sep. 1963, Guan KJ & Wang WC 2798 (PE); loc. eodem, 03 Sep. 1963, Guan KJ & Wang WC 2800 (PE). Beichuan: 29 May 2007,

140

Zhu DH 3842 (HX). Cangxi: 01 May 1959, Qin ZS 02710 (CDBI). Dujiangyan: 1930, Wang FT 20367 (PE); loc. eodem, 08 May 1987, Zhao ZL 87-0540 (HX); loc. eodem, 29 Jul. 1987, Fu DZ et al. 87-1367 (HX); loc. eodem, 17 Mar. 1987, Gao JL & Zhao ZL 87-0062 (HX); loc. eodem, 19 May 1987, Fu DZ & Zhao ZL87-0759 (HX); loc. eodem, 26 Apr. 1987, Fu DZ 87-0250 (HX); loc. eodem, 21 Apr. 1987, Fu DZ et al. 87-0180 (HX); loc. eodem, 04 Apr. 2002, Zhu DH 55 (HX); loc. eodem, 16 May 2007, Zhu ZB, Zhu DH & Li XJ 20070415 (HX); loc. eodem, 07 May 1939, Fang WP13446 (PE). Emeishan: 24 Aug. 1956, Zhu ZY et al. 830 (PE); loc. eodem, 05 Aug. 1927, Zhou TY & Xu GJ 20 (PE); loc. eodem, 13 Jun. 1939, Zhang XZ & Zhang G 179 (PE); loc. eodem, 07 Apr. 1997, Li CH 97-385 (PE); loc. eodem, 13 Jun. 1931, Ching & Shun 194 (CQNM); loc. eodem, 11 May 1952, Xiong JH, Zhang XB & Jiang XL 30483 (IBSC). Hanyuan: 13 Aug. 1938, Wang TP 8677 (PE). Heishui: 02 Jul. 1959, Jiang S et al. 01524 (PE). Jiulong: 2360 m, 09 Aug. 1979, Wang QQ 21460 (CDBI). Kangding: 19 Jun. 1953, Jiang XJ 36033 (IBSC). Lixian: 08 Oct. 1956, Li X 2450 (IBSC); loc. eodem, 28 Oct. 1956, Li X 46542 (IBSC). Luding: 2800 m, Oct. 1982, Xu GH 41155 (CDBI). Mabian: 1930, Wang FT 22877 (PE); loc. eodem, 1930, Wang FT 22897 (PE). Maoxian: 10 Jun. 1959, Jiang S et al. 00708 (PE); loc. eodem, 16 Jun. 1959, Maowen Expedition 2729 (PE); loc. eodem, 09 Aug. 2001, Gao XF & Peng YL 1599 (CDBI). Muli: Oct. 1982, Sichuan Vegetation Survey 578 (CDBI); loc. eodem, 23 Oct. 1982, Pu FF & Yao G 442 (NAS). Ningnan: 21 Aug. 1984, Liang YF et al. 84-34 (PE). Ningnan: 15 Aug. 1984, Liang YF et al. 84-32 (PE). Tianquan: 09 May 1936, Qu GL 2534 (IBSC); loc. eodem, 27 Aug. 1963, Guan KJ et al. 2016 (PE); loc. eodem, 05 May 1960, Sichuan Institute of Forestry Tian00111 (CDBI); loc. eodem, 24 May 1986, Wang JT & Yoshiaki takeda 0721 (CDBI). Wanyuan: 09 Jun. 1959, Sichuan Economic Botany Expedition 2438 (CDBI). Weiyuan: 01 May 1960, Neijiang College Sichuan Economic Botany Expedition, Neijiang 7052 (CDBI). Wenchuan: 02 May 2008, He XJ & Zhao QS 157209 (SZ). Yanbian: 12 Sep. 2002, Gao XF et al. 3373 (PE). Yibin: 04 Jun. 1982, Sun CR 110 (IBSC). TAIWAN, Chiayi: 23 310 5200 N, 120 380 1300 E, 26 Mar. 1932, T. Sata s. n. (TAI); loc. eodem, 23 300 1600 N, 120 410 1800 E, 30 Mar. 1989, Huang ZQ 13985 (TAI); loc. eodem, 14 May 2001, Chen ZZ et al. 658 (PE); loc. eodem, 23 290 3800 N, 120 420 5800 E, 1840 m, 13 Feb. 1995, Wang GY et al. 761 (HAST). Hsinchu: 24 330 1300 N, 121 130 1100 E, 1600 m, 21 Feb. 2002, Huang YY, Chen HY & Wu YH 972 (HAST); loc. eodem, 24 410 1400 N, 121 180 3000 E, 1500–1650 m, 25 Mar. 2010, Peng JY et al. 22432 (HAST). Hualien: 24 10 3100 N, 121 200 5400 E, 20 Apr. 1936, Noriaki Fukuyama s. n. (TAI); loc. eodem, 24 130 5400 N, 121 380 3600 E, 01 May 1961, T. Shimizu 12538 (TAI); loc. eodem, 23 550 1500 N, 121 270 5400 E, 1500–1600 m,16 Apr. 2003,

6 Taxonomic Revision

Lin PR et al. 175 (HAST); loc. eodem, 24 10 000 N, 121 190 6000 E, 2000–2100 m, 22 May 1993, Liao QZ et al. 1429 (HAST); loc. eodem, 24 110 600 N, 121 350 5800 E, 1000 m, 24 Apr. 2001, Chen ZZ et al. 630 (HAST); loc. eodem, 23 550 600 N, 121 270 2100 E, 1550–1750 m, 17 Apr. 2003, Lin PR et al. 189 (HAST); loc. eodem, 24 170 2100 N, 121 380 400 E, 1830 m, 08 May 2000, Qiu ST, Mou SJ & Yang GZ 6298 (HAST); loc. eodem, 23 570 4100 N, 121 290 300 E, 21 Feb. 1984, Huang ZQ 10238 (TAI). Miaoli: 24 280 700 N, 120 590 4500 E, Huang SF s. n. (TAI); loc. eodem, 24 310 2800 N, 120 570 1900 E, 28 Jan. 1982, Gao MC 9580 (TAI). Nantou: 23 470 1600 N, 120 460 5500 E, 18 Feb. 1959, Huang, Kou & Kao 952 (TAI); loc. eodem, 23 350 3800 N, 120 520 4600 E, 29 Mar. 1961, Huang ZQ 2178 (TAI); loc. eodem, 24 60 5100 N, 121 180 4000 E, 15 Oct. 1992, Huang SF & Hsieh TH 4923 (TAI); loc. eodem, 05 May 1998, Wang CM & Tsai YH 03155 (PE); loc. eodem, 23 410 6000 N, 120 470 6000 E, 700 m, 10 May 1993, Liao QZ 1263 (HAST); loc. eodem, 26 Apr. 1986, Yang YZ 2982 (HAST); loc. eodem, 23 400 1400 N, 120 460 4500 E, 1150 m, 03 Apr. 1997, Peng JY et al. 1679-1 (HAST); loc. eodem, 1200 m, 17 Feb. 1994, Peng JY et al. 15909 (HAST). New Taipei: 24 430 4800 N, 121 260 300 E, 1600–1800 m, 05 Apr. 1995, Wang GY et al. 859 (HAST); loc. eodem, 24 520 5300 N, 121 330 600 E, 530 m, 07 Oct. 1997, Gao RQ 74 (HAST); loc. eodem, 25 90 3100 N, 121 360 1200 E, 500 m, 18 Mar. 2001, Huang YY & Qi YZ 270 (HAST); loc. eodem, 900 m, 06 Apr. 2004, Liang HZ, Wu JQ & Gu XM 3730 (HAST). Taichung: 1400–2000 m, 09 Oct. 1997, Yang ZY et al. 9509 (HAST); loc. eodem, 24 160 3300 N, 120 580 300 E, 09 Oct. 1957, Liu TS et al. 128 (TAI); loc. eodem, 24 150 2000 N, 121 140 5100 E, 12 Apr. 1985, Tang WS 1232 (TAI); loc. eodem, 24 150 2000 N, 121 140 5100 E, 12 Apr. 1985, Huang ZQ 10380 (TAI). Taidong: 05 Aug. 1931, Y Y1646 (TAI); loc. eodem, 22 300 3000 N, 120 410 3400 E, 09 Jul. 1918, E. Matuda 151 (TAI). Taipei: 25 100 2600 N, 121 350 3000 E, 10 Aug. 2000, Huan HY 1493 (TAI); loc. eodem, 12 Apr. 1983, Hsieh CF & Tang WS 12 (TAI); loc. eodem, 700 m, 02 Oct. 1991, Wang ZJ 603 (HAST); loc. eodem, 25 100 4200 N, 121 300 5400 E, 700–750 m, 24 Feb. 1994, Chen ZX 430 (HAST); loc. eodem, 25 100 000 N, 121 300 000 E, 600–900 m, 03 Apr. 1998, Wang QM 3007 (HAST); loc. eodem, 25 90 2300 N, 121 320 1600 E, 29 Apr. 1930, S. Suzuki 4340 (TAI); loc. eodem, 24 450 4700 N, 121 250 400 E, 27 Aug. 1935, S. Suzuki 18969 (TAI); loc. eodem, 25 100 900 N, 121 310 5400 E, 29 Mar. 1936, Simada Hidetaro 1365 (TAI); loc. eodem, 24 470 1500 N, 121 280 3000 E, 07 Apr. 1939, Suzuki Tokio 17866 (TAI); loc. eodem, 24 490 000 N, 121 300 000 E, 08 Oct. 1937, Suzuki Tokio 16980 (TAI); loc. eodem, 16 Jun. 1941, S. Miuda & J. Fukuyama 72 (TAI); loc. eodem, 25 100 2200 N, 121 310 3300 E, 08 Jun. 1942, Toru Yoshida s. n. (TAI); loc. eodem, 25 100 2200 N, 121 310 3300 E, 23 Apr. 1944, R. Sho 29 (TAI); loc. eodem, 24 560 200 N, 121 370 900 E, 28 Oct. 1932,

6.5 Section Euthyra

S. Sasaki s. n. (TAI); loc. eodem, 07 Apr. 1983, Yang GZ 1331 (TAI); loc. eodem, 25 100 5700 N, 121 300 4500 E, 04. Ap. 1988, Huang ZQ 13451 (TAI); loc. eodem, 25 100 2200 N, 121 310 3300 E, 10 Apr. 1981, Chen YF 2237 (TAI); loc. eodem, 25 80 000 N, 121 350 000 E, 17 Apr. 1999, NTU, Pharmacy 869 (TAI); loc. eodem, 25 100 2200 N, 121 310 3300 E, 25 Mar. 1985, J. Murata & Yang TY 7865 (TAI); loc. eodem, 24 490 1000 N, 121 280 4400 E, 27 Apr. 1934, Suzuki Tokio 11187 (TAI). Yilan: 24 360 5700 N, 121 280 5200 E, 1160 m, 19 Mar. 2009, Peng JY, Huang JY & Weng ML 22032 (HAST); loc. eodem, 1100 m, 30 Mar. 1991, Peng JY 13808 (HAST); loc. eodem, 24 350 2600 N, 121 260 200 E, 1500 m, 06 Apr. 2000, Lin JH & Chen JZ 106 (HAST); loc. eodem, 24 280 4500 N, 121 270 5600 E, 2340 m, 07 Jul. 1999, Liang HZ et al. 1222 (HAST); loc. eodem, 24 370 900 N, 121 280 2100 E, 1270 m, 16 Feb. 1998, Peng JY et al. 17087 (HAST); loc. eodem, 24 290 3600 N, 121 320 800 E, 1925 m, 05 May 2011, Peng JY et al. 22974 (HAST); loc. eodem, 24 220 5600 N, 121 230 300 E, 14 Jul.1937, Simada Hidetaro 1331 (TAI); loc. eodem, 24 290 5500 N, 121 310 3200 E, 07 Aug. 1928, S. Suzuki s. n. (TAI); loc. eodem, 24 290 5500 N, 121 280 300 E, 25 Mar. 1930, S. Suzuki 3754 (TAI); loc. eodem, 24 220 5400 N, 121 230 400 E, 27 May 1974, Huang ZQ 7698 (TAI); loc. eodem, 24 290 5500 N, 121 280 300 E, 25 Mar. 1930, S. Suzuki 3754 (TAI). Yunlin: 23 360 000 N, 120 410 1600 E, 29 Apr. 1990, Huang ZQ 14574 (TAI). YUNNAN, Chengjiang: 06 Aug. 1939, Zhang HD 690 (IBSC). Daguan: 1870 m, 17 May 2016, Li H et al. 022 (KUN); loc. eodem, 09 Jul. 2015, Cao AJ Zhaotong1 (KUN). Huize: 04 Aug. 2017, Liu ED et al. 7320 (KUN). Jingdong: 18 Jun. 1981, Deng XF 00063 (KUN). Jinghong: 29 Jul. 1977, Tao GD 15650 (HITBC). Jinping: 540 m, 25 May 1961, Xuan SJ 0164 (KUN). Longling: 24 490 3300 N, 98 460 1800 E, 2120 m, 26 May 2005, Li H et al. 23792 (KUN). Lüchun: 21 Oct. 1995, Wu SG 603 (KUN). Luoping: 1900 m, 28 May 1989, Hongshui River Expedition 1922 (KUN). Luxi: 05 Nov. 2015, Zhao WY et al. LXP-1309616 (SYS). Malipo: 13 Jan. 1940, Wang CW 83183 (PE); loc. eodem, 22 Mar. 2002, Shui YM et al. 20160 (PE); loc. eodem, 22 560 4500 N, 104 360 5400 E, 1590 m, 12 May 2017, Liu ED et al. 5867 (KUN). Mengla: 720 m, 20 Apr. 1989, Zhu H & Wang H 2395 (KUN). Pingbian: 30 Apr. 1962, Feng GM 22264 (IBSC); loc. eodem, 23 Oct. 2012, Pingbian Traditional Chinese Medicinal Herbs Resources Survey 5325231310 (IMDY). Shizong: 1750 m, 16 Nov. 1985, Sun H 0195 (KUN). Weixin: 10 Nov. 2016, Luo ZQ 201605-1 (KUN). Wenshan: 12 Aug. 1947, Feng KM 11171 (PE). Xichou: 02 Jun. 1964, s. n. (HITBC). Xinping: 2300 m, 13 May 1990, Yuxi Expedition 3075 (KUN). Yongde: 2810 m, 15 Jul. 2002, Liu ED 5142 (KUN). Yongshan: 05 Jul. 1932, Cai HT 51208 (IBK). Yuanyang: 1300 m, 07 Jun. 1974, Lüchun Expedition 1620 (KUN); loc. eodem, 1100 m, 09 Jun. 1974, Luchun Expedition 1844

141

(KUN). Zhaoyang: 1860 m, 16 May 2016, Li H et al. 014 (KUN). ZHEJIANG, Anji: 30 May 1957, He XY 24076 (HHBG). Hangzhou: 22 Apr. 1980, Hangzhou Herbarium 1376 (HHBG). Lin’an: 22 Jun. 1957, Deng MB et al. 4747 (PE); loc. eodem, 07 May 1957, He XY 22609 (HHBG). Longquan: 25 Jun. 1972, Zhejiang Medicinal Flora Compilation Group 1801 (ZM); loc. eodem, 08 Jul. 1972, Zhejiang Medicinal Flora Compilation Group 2384 (ZM); loc. eodem, 25 Jun. 1972, Zhejiang Medicinal Flora Compilation Group 863 (ZM); loc. eodem, 06 Apr. 1959, Zhang SR 4591 (HHBG). Kaihua: 31 May 1959, Zhejiang Plant Resources Survey 26253 (PE); loc. eodem, 31 May 1959, Zhejiang Plant Resources Survey 24253 (HHBG). Suichang: 24 Apr. 1959, Zhejiang Plant Resources Survey 25678 (PE); loc. eodem, 25 May 1986, Zhang FG & Li ZY 5294 (ZM); loc. eodem, 28 Oct. 1964, Mao ZG 10397 (HHBG); loc. eodem, Zhejiang Plant Resources Survey 26464 (HHBG). Tiantai: 06 May 1924, Ching RC 1420 (PE). Wuyi: Apr. 1933, Chen S 1037 (PE). Wencheng: 15 Sep. 1972, Zhejiang Medicinal Flora Compilation Group 3486 (ZM). Xianju: 30 Nov. 1982, Hangzhou Herbarium 2795 (HHBG). Yunhe: 10 May 1930, Tsoong KK 407 (PE). Zhoushan: 20 Jun. 2007, Tian Q, Yang QH & Zhou XY CSYZXZ07-0317 (CSH). THAILAND, Lampoon: 18 340 4500 N, 99 00 2300 E, 05 Jun. 1993, Maxwell JF 93-578 (NHN). Mae Fa Luang: 27 Jan. 2009, Maxwell JF 09-28 (NHN). VIETNAM, Ha Giang: 22 390 2900 N, 105 190 3500 E, 900 m, 04 Mar. 2005, L. V. Averyanov et al. s. n. (P). 14. Paris caobangensis Y. H. Ji, H. Li & Z. K. Zhou, Act. Phytotax. Sin. 44 (6): 700. 2006. Type: Vietnam, Cao Bang, Yan Lac, 105 500 2900 E, 22 440 1600 N, 1100 m, 19 Apr. 2003, Ji YH 0127 (Holotype, KUN). Paris nitida G. W. Hu, Z. Wang & Q. F. Wang, Phytotaxa 314 (1): 145. 2017. Type: China, Hubei, Tongshan, 29 230 N, 114 350 E, 1070 m, 07 Apr. 2016, G. W. Hu & Z. Xu HGW-01060 (Holotype, HIB; Isotypes, HIB, HNNU). Perennial herb. Rhizome cylindrical, oblique or horizontal, 2.0–3.0 cm in diameter, 5.0–7.0 cm long, bearing a bud at the top, fleshy roots about 10.0 cm long. Stem erect, cylindrical, reddish purple at lower portion and whitish green at upper portion, 30.0–35.0 cm  3.0–5.0 mm. Leaves 4–6 in a whorl at the top of stem. Blades ovate, ovate-lanceolate, or oblong-lanceolate, green, coriaceous, acuminated at apex, base subrounded, ca. 9.5  4.5 cm; middle vein obvious, lateral veins 1 pair, basally developed, net veins inconspicuous; petiole green, 2.5–3.0 cm. Flower solitary, developing from the top of stem, basic merosity 4–6; pedicel yellowishgreen, 10.0–25.0 cm  2.5 mm; sepals 4–6, lanceolate to ovate-lanceolate, green, ca. 2.5–4.5  1.5–2.5 cm; petals narrowly linear at lower portion, gradually widened to 2.0–3.0 mm at the upper portion, greenish-yellow, 3.0–5.0 cm, longer (occasionally shorter) than sepals, reflexed occasionally. Stamens twice as many as the sepals,

142

filaments yellowish-green, 1.6–1.9 cm; anthers yellow, 6.0–9.0 mm; free portion of connective acute at apex, nearly absent. Ovary conic, green, with 4–6 longitudinal wings; ovules ovoid, transparent, numerous, arranged along placentas. Carpels 4–6, unilocular with parietal placentation; style purple, ca. 4.0 mm, with an enlarged base, stigmas 4–5lobed, purple. Fruit a capsule, subglobose, greenish yellow at maturity, ca. 2.0–2.5 cm in diameter, dehiscing along longitudinal ridges. Seeds numerous, covered by red and juicy sarcotesta (Figs. 6.33 and 6.34). Phenology: flowering March–May, fruiting June– November. Habitats: evergreen (or deciduous) broad-leaved forests, shady places; ca. 300–2900 m. Distribution: China: Guangxi (Guanyang), Guizhou (Daozhen), Hubei (Tongshan), Hunan (Changde). Vietnam (Cao Bang). Thailand (Chiang Mai). Notes: P. nitida is considered to be closely related to P. caobangensis, but differs from it in the coriaceous leaves and adaxially lustrous quality (Wang et al. 2017). Examinations of specimens and living plants indicate that these features are also possessed by P. caobangensis, suggesting that they are conspecific. Accordingly, I here reduced P. nitida as a synonym of P. caobangensis. Additional specimens examined. CHINA, GUANGXI, Guanyang: 16 Oct. 2018, Ji YH 2018208 (KUN). GUIZHOU, Daozhen: 17 Apr. 2003, Liu ZY 2030728 (IMC). HUNAN, Changde: 11 May 2018, Ji YH 2018026 (KUN). VIETNAM, CAO BANG: 20 May 2004, Ji YH 0159 (PE); loc. eodem, 22 440 N, 105 500 E, 13 Apr. 1999, P. H. Hoang & L. Averyanov CBL 1306 (P); loc. eodem, 22 470 N, 105 490 E, 15 Apr. 1999, P. H. Hoang & L. Averyanov CBL 1405 (P); loc. eodem, 22 470 N, 105 490 E, 18 Apr. 1999, P. H. Hoang & L. Averyanov CBL 1511 (P); loc. eodem, 23 070 N, 105 080 E, 01 May 1999, P. H. Hoang & L. Averyanov CBL 1901 (P). THAILAND, CHIANG MAI: 24 May 1998, J. F. Maxwell 98-557 (NHN). 15. Paris qiliangiana H. Li, J. Yang & Y. H. Wang, Phytotaxa 329 (2): 193. 2017. Type: China, Hubei, Zhuxi, 31 550 N, 109 400 E, 1004 m, 6 May 2017, Li & Yang 053-03 (Holotype, KUN; Isotype, KUN). Perennial herb. Rhizome thick, cylindrical, oblique or horizontal, yellowish-brown outside, white and starchy inside, 3.0–20.0 cm long, 0.8–4.0 cm in diameter, stems erect, green or purplish red, 15.0–50.0 cm. Leaves 4–8 in a terminal whorl; leaf blades green, oblong, ovate, obovate or oblanceolate, ca. 5.0–13.0  2.0–6.0 cm, apex acuminate, base subrounded, subcordate, or cuneate; lateral veins 1 pair, nearly basal; petioles green or dark purple, 1.0–4.0 cm. Flower solitary, basic merosity 4–7; pedicel green or reddish purple, 6.0–30.0 cm long; sepals green, ovate or lanceolate,

6 Taxonomic Revision

ca. 4.0–8.0  1.0–3.0 cm; petals linear, greenish yellow, longer than petals. Stamens 2  petal number, arranged in 2 whorls, 1.5–3.5 cm long, filaments yellow-green, 3.0–8.0 mm; anthers yellow or brown, 1.0–2.5 cm long, free portion of connective nearly absent. Ovary ovoid, green, unilocular with parietal placentation, 4–7-ridged; ovules ovate, white; style white or purplish red, 2.0–10.0 mm, with an enlarged base; stigmas 4–7, light yellow to purple, revolute at flowering. Capsule yellowish green at maturity, spheroidal, with 4–7 longitudinal ridges, ca. 2.0–3.0 cm in diameter, irregularly dehiscing between ridges. Seeds subglobose, ca. 0.3 cm in diameter, white, covered by red and juicy sarcotesta (Figs. 6.35, 6.36, 6.37 and 6.38). Phenology: flowering March–May, fruiting June– October. Habitats: deciduous broad-leaved and coniferous forests; ca. 720–1140 m. Distribution: endemic to China: Chongqing (Chengkou), Hubei (Shennongjia, Xingshan), Shaanxi (Langao, Meixian, Ningqiang, Ningshan, Pingli), Sichuan (Dujiangyan, Pingwu). Additional specimens examined. CHINA, CHONGQING, Chengkou: 18 Mar. 1908, s. n. (NHN). HUBEI, Shennongjia: 15 Jun. 1996, Shi SG S-W-0091 (PE); loc, eodem, 22 Aug. 1976, Shennongjia Botany Expedition 11548 (PE); loc, eodem, 21 Aug. 1976, Shennongjia Botany Expedition 11729 (PE). Xingshan: 24 May 1957, Liu Y 180 (PE). SHAANXI, Langao: 12 Oct. 2004, Chen YS et al. 1798 (WUK). Meixian: 17 Jul. 1971, Qinling Expedition 277 (WUK); loc, eodem, 17 Jul. 1971, Qinling Baiyao Expedition 278 (WUK). Ningqiang: 14 Sept. 1972, Qinling Baiyao Expedition 331 (WUK). Ningshan: 21 Jul. 2008, Jiang ZM, Du C & Liu PL 216 (WUK). Pingli: 03 Jul. 1959, 79 (WUK). SICHUAN, Dujiangyan: 01 Jun. 1963, Li YQ 072 (CDBI). Pingwu: 16 Jun. 2014, Zhang SR, Chen SR & Lang XA 2038 (PE). 16. Paris fargesii Franch., Journ. Bot. (Morot) 12: 190. 1898; Franch., lcon. Cormoph. Sin. 5: 516. fig. 7862. 1976; Wang et Tang, Fl. Reip. Pop. Sin. 15. 691. 1978; H. Li, Act. Bot. Yunnan 6 (4): 359. 1984; H. Li, Bull. Bot. Res. Harbin 6 (1): 131. 1986; H. Li, The Genus Paris (Trilliaceae) 48. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 92. 2000.  Paris polyphylla Smith subsp. fargesii (Franch.) Hara., Journ. Fac. Sci. Univ. Tokyo, Sect. 3, 10 (10): 177. 1969.  Daiswa fargesii (Franch.) Takht., Brittonia 35 (3): 264. 1983; B. Mitchell, Plantsman 10 (3): 174. 1988; T. C. Huang et K. C. Yang, Taiwania 33: 122. 1988.  Paris polyphylla Smith var. fargesii (Franch.) S. Dasgupta, Fasc. Fl. India 23: 109. 2006. Type: China, Chongqing, Chengkou, R. P. Farges 573 (Holotype, P). Paris petiolata Baker ex C. H. Wright var. membranacea C. H. Wright, Journ. Linn. Soc. 36: 145. 1903. Type: China, Hubei, Mar. 1889, A. Henry 5385 (Holotype, K).

6.5 Section Euthyra

143

Fig. 6.33 Paris caobangensis (drawn by M. Shen). Rhizome and stem (a), and aerial shoot (b)

Paris hookeri Lévl., Repert. Spec. Nov. Regni Veg. 7: 231. 1909. Type: China, Guizhou, Guiding, Nov. 1907, J. Cavalerie s. n. (Holotype, E). Daiswa fargesii Franch. var. brevipetalata T. C. Huang & K. C. Yang, Taiwania 33: 123. 1988.  Paris fargesii Franch. var. brevipetalata (T. C. Huang & K. C. Yang) T. C. Huang & K. C. Yang, Taiwania 34: 52. 1989. Type: China, Taiwan, Yilan, Huang TC & Yang KC 10803 (Holotype, TAI).

Paris fargesii Franch. var. latipetala H. Li & V. G. Soukup, Acta Bot. Yunnan. Suppl. 5: 17. 1992. Type: China, Guizhou, Guiding, 11 May 1987, Li H 87-167 (Holotype, KUN); loc. eodem, Li H 88-198 (Paratype, CINCI). Perennial herb. Rhizome thick, 8.0–20 cm long, 1.0–4.0 cm in diameter. Stem erect, cylindrical, green or purplish. Leaves 4–6; leaf blades green, ovate, or ovateoblong, apex acuminate, base cordate or rounded, ca. 7.5–18.0 cm  4.0–11.5 cm, lateral veins 2–3 pairs, basally

144 Fig. 6.34 Aerial shoot (a), leaf shape variation (b), flower (c), sepal shape variation (d), stamens (e), pistil (f), transverse section of ovary (g), young fruit (h), and dehisced capsule (i) of Paris caobangensis

6 Taxonomic Revision

6.5 Section Euthyra

Fig. 6.35 Paris qiliangiana (drawn by M. Shen): whole plant (a) and dehisced capsule (b)

145

146

Fig. 6.36 Aerials shoots of Paris qiliangiana (a, b, c), and the obverse (d) and reverse (e) side of leaf blade

6 Taxonomic Revision

6.5 Section Euthyra

147

Fig. 6.37 Flower (a), sepals (b), stamens (c), pistil (d), young fruit (e), and dehisced capsule (f) of Paris qiliangiana

developed; petiole green or purple, 1.5–9.5 cm long. Flower solitary, basic merosity 4–6; pedicel green or purplish, 15.0–50.0 cm; sepals green, ovate, ovate-lanceolate or lanceolate, ca. 3.0–5.5 cm  0.8–2.5 cm, apex acuminate to caudiform; petals linear, yellowish green or purplish black, 1.5–8.0 cm long. Stamens in 2 whorls, short, erect, 6.0–7.0 mm long; filaments 1.0–3.0 mm long; anthers

2.0–4.0 mm; free portion of connective purple-black, transversely ellipsoid, subglobose, or shortly conical. Ovary angular, square, or pentagonal, unilocular with parietal placentation; ovules numerous, on 2 longitudinal rows along every placenta. Style short, purplish black, with an enlarged base; stigmas 3.0–5.0 mm long, revolute gradually at flowering. Capsule subglobose, purplish black or green,

148

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Fig. 6.38 Longitudinal (a) and transverse (b) section of ovary showing parietal placentation in Paris qiliangiana

ca. 1.5–3.5 cm in diameter, dehiscing along longitudinal ridges. Seeds numerous, ca. 3.0 mm in diameter, covered by red and juicy sarcotesta (Figs. 6.39 and 6.40). Phenology: flowering March–April, fruiting May– October. Habitats: evergreen and deciduous broad-leaved forests; ca. 500–2100 m. Distribution: China: Chongqing (Chengkou, Jiangjin, Nanchuan), Guangdong (Ruyuan), Guangxi (Baise, Longsheng, Longzhou, Shangsi), Guizhou (Anlong, Ceheng, Daozhen, Guiding, Leishan, Shiqian, Suiyang, Xiuwen, Yinjiang), Hubei (Badong, Shennongjia, Wufeng, Xingshan), Hunan (Chenzhou, Cili, Jishou, Sangzhi, Suining, Xupu, Yongshun, Yuanling), Sichuan (Emeishan, Gulin, Hongya, Shifang, Wenchuan, Xuyong), Taiwan (Hualien, Yilan), Yunnan (Daguan, Guangnan). Vietnam (Cao Bang). Notes: Two conspecific varieties, namely, P. fargesii var. brevipetalata and P. fargesii var. latipetala, were described under this species based on the length and width of petals (Huang and Yang 1988; Li 1992). Specimens of this species were carefully examined, and it was observed that the petal successively varied from 1.5 to 8.0 cm in length, and from 1.0 mm to 5.0 mm in width. Infraspecific subdivision based on this character may be unreasonable. Therefore, the two taxa are here reduced as synonyms of P. fargesii. Additional specimens examined. CHINA, CHONGQING, Chengkou: M. Labbe Farges s. n. (PE). Jiangjin: 16 May 2017, Li ZY & Zhang J S-1776 (IMC); loc. eodem, 29 Jul. 2006, Liu X 2067646 (IMC); loc. eodem, 21 Aug. 1997, Liu ZY 971647 (IMC). Nanchuan: 28 Apr. 1996. Liu ZY 18611 (IMC); loc. eodem, 28 Apr. 1996. Liu ZY 18616 (IMC); loc. eodem, 28 Apr. 1996. Liu ZY 18617 (IMC); loc. eodem, 28 Apr. 1996. Liu ZY 18619 (IMC); loc. eodem, 28 Apr. 1996. Liu ZY 18601 (IMC); loc.

eodem, 11 Apr. 1996, Liu ZY 15585 (IMC); loc. eodem, 14 Apr. 1982, Tan SY, Zhang JL & Li ZL 3102 (IMC); loc. eodem, 15 May 1970, Liu ZY 70625 (IMC); loc. eodem, 06 Apr. 1981, Liu ZY 812400 (IMC); loc. eodem, 06 Apr. 1981, Tan SX 812404 (IMC); loc. eodem, 15 May 1970, Liu ZY 70035 (IMC); loc. eodem, 16 Apr. 2007, Liu ZY 2007009 (IMC); loc. eodem, 01 Aug. 2007, Liu ZY 70390 (IMC); loc. eodem, 19 Jun. 1983, Liu ZY 4206 (IMC); loc. eodem, 20 Jun. 1996, Liu ZY 18648 (IMC). GUANGDONG, Ruyuan: 02 Apr. 1934, Gao XP 54007 (IBSC). GUANGXI, Baise: 13 Oct. 1989, Detachment in S China 2517 (IBSC). Longsheng: 29 Jul. 1957, Qin HF & Li ZT 72871 (IBSC); loc. eodem, 07 Jul. 1958, Chen ZZ 51195 (IBSC). Longzhou: 19 Nov. 1956, Li YK 91 (IBSC). Shangsi: 13 Apr. 1944, Chen SQ 4889 (IBSC). GUIZHOU, Anlong: 22 Jun. 1960, Guizhou Expedition 5682 (WUK). Ceheng: 24 Jul. 1985, Lan KM 85217 (GZAC). Daozhen: 27 Jul. 2003, Liu ZY 2033378 (IMC); loc. eodem, 19 Apr. 2003, Liu ZY 2030968 (IMC); loc. eodem, 18 Apr. 2003, Liu ZY 2030765(IMC); loc. eodem, 18 Apr. 2003, Liu ZY 2030785 (IMC). Guiding: Nov. 1907, Cavalerie J. s. n. (E). Leishan: 30 Apr. 1959, S Guizhou Expedition 947 (NAS). Shiqian: 02 Aug. 1988, Wuling Mountain Expedition 2865 (KUN). Suiyang: 19 Apr. 1990, Lan KM 90-0646 (GZAC). Xiuwen: 29 May 1999, No. 1 Jing982 003 (GFS). Yinjiang: 19 Apr. 1964, Zhang ZS 401592 (IBSC). HUBEI, Badong: Henry A. 5385 (K). Shennongjia: 08 May 1985, Shi SG & Gong SM 0088 (JMSU); loc. eodem, 10 Jul. 2008, Liu Z et al. 035 (WH). Wufeng: 20 Jul. 1992, Jiang JB & Jiang DS 0205 (CTGU). Xingshan: 24 May 1957, Liu Y 192 (PE); loc. eodem, 24 May 1957, Liu Y 193 (PE); loc. eodem, 24 May 1957, Liu Y 194 (PE). HUNAN, Chenzhou: 21 Sept. 2014, Xu YF & Zhou H 14092101 (CSFI). Cili: 19 Sept. 2016, Li RS & Li H 046 (KUN); loc. eodem, 19 Sept. 2016, Li RS & Li H 042 (KUN). Jishou: 25 Jun. 1987, Gu ZC 870625045

6.5 Section Euthyra

Fig. 6.39 Paris fargesii (drawn by M. Shen). Rhizome (a), aerial shoot (b), and dehisced capsule (c)

149

150

6 Taxonomic Revision

Fig. 6.40 Aerial shoot (a), flower (b, c), young fruit (d), dehisced capsule (e), pistil (f), longitudinal (g) and transverse (h) section of ovary, and leaf shape variation in Paris fargesii (i) (photographed by Y. Ji)

6.5 Section Euthyra

(JIU); loc. eodem, 20 Jul. 1987, Gu ZC 0481 (JIU). Sangzhi: 10 Sept. 1990, Cao TR 90589 (IBSC). Suining: 13 Apr. 2014, Zhou JJ & Song ZP 1404031 (CSFI). Xupu: 04 Oct. 2004, Q. Fan 4619 (SYS). Yongshun: 02 May 2008, Yang B 08050207 (JIU). Yuanling: 24 Jun. 1988, Zhang GC 580 (IBSC). SICHUAN, Emeishan: 28 Apr. 1940, Zhou HC 11582 (NAS); loc. eodem, 26 Aug. 1938, Zhou TY & Xu GJ s. n. (NAS). Gulin: 17 Apr. 2014, Wu L 4551 (BNU). Hongya: 01 Aug. 1938, Yao ZW 2622 (NAS). Shifang: 21 Jul. 2008, He XJ, Zhao QS & Wang Q 138181 (SZ). Wenchuan: 02 Jun. 2009, He XJ & Zhao QS 211388 (SZ). Xuyong: 15 Apr. 2012, Gao XF et al. HGX10069 (CDBI). TAIWAN, Hualien: 07 Apr. 2000, Yang GZ 6017 (HAST); loc. eodem, 02 Jun. 1993, Liao QZ 1505 (HAST). Yilan: 2000 m, 01 Jul. 1999, Liang HZ et al. 1234 (HAST); loc. eodem, 1720 m, 10 May 2002, Huang JY 795 (HAST). YUNNAN, Daguan: 1870 m, 17 May 2016, Li H et al. 020 (KUN); loc. eodem, 09 Jul. 2015, Cao AJ Zhaotong2 (KUN). Guangnan: 06 Mar. 1940, Wang CW 87531 (PE). 17. Paris cronquistii (Takht.) H. Li, Act. Bot. Yunnan 6 (4): 357. 1984; H. Li, Bull. Bot. Res. Harbin 6 (1):112. 1986; H. Li, The Genus Paris (Trilliaceae) 25. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 89. 2000.  Daiswa cronquistii Takht., Brittonia 35: 262. 1983; B. Mitchell, Plantsman 10 (3): 172. 1988. Type: China, Guangxi, Lingyun, 13 Apr. 1933, A. N. Steward & H. C. Cheo 187 (Holotype, NY; Isotype, PE, GH). Paris polyandra S. F. Wang, Bull. Bot. Res. Harbin 5 (1): 169. 1985. Type: China, Sichuan, Mt. Emei, 08 Apr. 1956, Xiao JX 48491 (SZ). Paris cronquistii (Takht.) H. Li var. brevipetalata H. X. Yin et H. Zhang, Acta Bot. Boreal. -Occident. Sin. 33 (1): 190. 2013. Type: China, Sichuan, Chongzhou, 1100 m, 27 Apr. 2011, Yin XH et al. 0427001 (Holotype, WCU). Perennial herb. Rhizome thick, 5.0–78.5 cm long, 2.0–3.0 cm in diameter. Stem erect, 20.0–100.0 cm tall, green, often reddish purple. Leaves 4–7, adaxially green with white markings along main veins, abaxially purple or green with purple markings; leaf blades ovate, base cordate, sparsely rounded, apex abruptly narrow, caudiform, 11.0–17.0 cm  5.5–11.0 cm, 2 pairs of curved lateral veins basally developed; petiole 2.5–7.6 cm long, purple. Flower solitary, basic merosity 4–7; pedicel 12.0–60.0 cm long, green or purple; sepals green, lanceolate, ovate-lanceolate, ca. 4.5–11.0 cm  1.3–2.0 cm; petals yellowish green, filiform, 2.0–8.0 cm long, shorter (rarely longer) than sepals. Stamens 3 or 2  petal number, 15.0–30.0 mm long; filaments pale green, 3.0–10.0 mm long; anthers golden yellow, 10.0–15.0 mm long; free portion of connective green or yellow, 1.0–6.0 mm long. Ovary green or lilac with 4–7 ridges, unilocular with parietal placentation; ovules

151

numerous, arranged in 2 rows on the placenta; style purplish green, yellowish red, 2.0–3.0 mm long, with an enlarged base; stigmas 5–6, yellowish red or purple, revolute. Capsule green to greenish-red at maturity, ca. 1.5–3.0 cm in diameter, dehiscing irregularly. Seeds numerous, subglobose, covered by red and juicy sarcotesta (Figs. 6.41, 6.42 and 6.43). Phenology: flowering April–June, fruiting July–October. Habitats: evergreen (or deciduous) broad-leaved and coniferous forests; ca. 200–1950 m. Distribution: China: Chongqing (Jiangjin, Nanchuan, Youyang), Guangxi (Lingyun, Napo, Tianlin), Guizhou (Daozhen), Sichuan (Xuyong), Yunnan (Funing, Fuyuan, Jinping, Malipo, Mengzi, Pingbian, Shuangbai, Xichou). Vietnam. Notes: P. cronquistii var. brevipetalata is believed to be distinct the proto-variety in its petals, which are shorter than its sepals. I carefully examined the holotype of P. cronquistii and found that its petal length (ca. 4 cm) is also shorter than its sepal length (ca. 5.5 cm). In addition, the petal length of P. cronquistii varies from 2 to 12 cm, so it thus cannot be used as a character for taxa delimitation. Accordingly, I here treat P. cronquistii var. brevipetalata as a synonym of P. cronquistii. Additional specimens examined. CHINA, CHONGQING, Jiangjin: 10 May 2016, Liu ZY & Zhang J S-0759 (IMC). Nanchuan: 07 Apr. 1981, Liu ZY 1236 (IMC); loc. eodem, 05 Apr. 1996, Liu ZY 15560 (P); loc. eodem, 1200 m, 29 Apr. 1996, Liu ZY 18613 (IMC); loc. eodem, 1200 m, 29 Apr. 1996, Liu ZY 18615 (IMC); loc. eodem, 700 m, 28 Apr. 198, Liu ZY & Zhang JL 4051 (IMC); loc. eodem, 850 m, 07 Apr. 1981, Liu ZY & Tan SX 812361 (IMC). Youyang: 1200 m, 26 Aug. 1984, Liu ZY 7022 (IMC). GUANGXI, Lingyun: 13 Apr. 1933, A. N. Steward & H. C. Cheo 187 (PE). Napo: 18 Jul. 2013, Nong DX et al. 451026130718028LY (GXMG). Tianlin: 1650 m, 25 Apr. 1989, Huanghe River Expedition 497 (KUN); loc. eodem, 18 Apr. 2013, Tianlin Expedition 451029130418002 (GXMG). GUIZHOU, Daozhen: 03 Apr. 2003, Liu ZY 2030445 (IMC); loc. eodem, 18 May 2003, Liu ZY 2031822 (IMC); loc. eodem, 03 Apr. 2003, Liu ZY 2030386 (IMC); loc. eodem, 03 Apr. 2003, Liu ZY 2030388 (IMC). SICHUAN, Xuyong: 15 May 2014, Zhang L, Zhou XM & Ju WB HGX14792 (CDBI). YUNNAN, Funing: 22 Aug. 1940, Wang CW 88724 (PE). Fuyuan: 1800 m, 20 Jun. 1989, Honghe River Expedition 2333 (KUN). Jinping: 15 Mar. 1958, Huang Q 170 (PE). Malipo: 16 Oct. 1998, Wang YZ, Peng H & Deng DS 4052 (PE). Mengzi: 1800 m, 01 Jan. 1939, Wang QW 83280 (KUN). Pingbian: 23 Jun. 1956, Sino-Soviet Expedition to Yunnan 3778 (PE). Shuangbai: 1450 m, 01 Oct. 1958, Huang SQ 0143 (KUN). Xichou: 18 Feb. 1994, Wu SG 516 (KUN); loc. eodem, 1450 m,

152

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Fig. 6.41 Paris cronquistii (drawn by M. Shen). Rhizome and stem (a), aerial shoot (b), the reverse side of leaf blade (c), and dehisced capsule (d)

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153

Fig. 6.42 Paris cronquistii: petals longer (a) or shorter (b) than sepals, leaf blade adaxially mottled with white along the leaf veins (c), abaxially with purple markings (d), stamens 2  (e) or 3  (f) petal number

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Fig. 6.43 Pistil of Paris cronquistii (a), with the longitudinal (b) and transverse section showing the parietal placentation (c)

17 Apr. 1987, Sun H & Qian ZG 01303 (KUN); loc. eodem, 1950 m, 04 Apr. 1959, Wu QA 7255 (KUN); loc. eodem, 1550 m, 11 May 1964, Wang SZ 260 (KUN). VIETNAM: 15 Feb. 1965, Sino-Vietnam Expedition 2272 (PE). 18. Paris delavayi Franch., Journ. Bot. (Morot) 12: 190. 1898; P0 ei et Chou, Icon. Chin. Medic. fig. 307. 1964; Hara, Journ. Fac. Sci. Univ. Tokyo, Sect. 3, 10 (10): 159. 1969; H. Li, Bull. Bot. Res. Harbin 6 (1): 114. 1986; H. Li, The Genus Paris (Trilliaceae) 28. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 89. 2000.  Daiswa delavayi (Franch.) Takht., Brittonia 35 (3): 269. 1983; B. Mitchell, Plantsman 10 (3):172. 1988. Type: China, Yunnan, Yanjin: 01 May 1894, J. M. Delavay s. n. (Holotype, P; Isotype, P). Paris henryi Diels, Bot. Jahrb. Syst. 29 (2): 252. 1901. Type: China, Hubei, 01 Jan. 1885, Henry A 5380 (Lectotype, B; Isotype, B, E). Paris bockiana Diels, Bot. Jahrb. Syst. 29 (2): 253. 1901.  Daiswa bockiana (Diels) Takht., Brittonia 35 (3): 267. 1983. Type: China, Chongqing, Nanchuan, 1891, Rosthorn A. V. & Bock C. 642 (B). Paris polyphylla Smith var. pseudothibetica H. Li, Bull. Bot. Res. Harbin 6 (1): 126. 1986. Type: China, Yunnan, Yiliang: 1900 m, 16 Jun. 1982, Li H, Chen Y & Yu HY 1275 (Holotype, KUN); loc. eodem, 1900 m, 17 Jun. 1982, Li H, Chen Y & Yu HY 1323 (Paratype, KUN). Paris polyphylla Smith var. pseudothibetica Li H. f. macrosepala H. Li, Bull. Bot. Res. Harbin 6 (1): 127. 1986.

Type: China, Yunnan, Yiliang, 1800 m, 17 Jun. 1982, Li H 1275 (KUN). Paris polyphylla Smith var. minor S. F. Wang, Bull. Bot. Res. Harbin 8 (3): 139. 1988; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 91. 2000. Type: China, Sichuan, Mt. Emei, 12 May 1986, Wang SF 6512 (SZ). Paris petiolata Baker ex C. H. Wright, Journ. Linn. Soc. Bot. 36: 145. 1903.  Paris fargesii Franch. var. petiolata (Baker ex C. H. Wright) F. T. Wang & Tang, Fl. Reipubl. Popul. Sin. 15: 91. 1978.  Paris delavayi Franch. var. petiolata (Baker ex C.H. Wright) H. Li, The Genus Paris (Trilliaceae) 28. 1998. Type: China, Sichuan, Prat 572 (Holotype, K). Paris delavayi Franch. var. ovalifolia H. Li, Bull. Bot. Res. Harbin 6 (1): 115. 1986. Type: Chian, Yunnan, Yiliang, Li H 1324 L (KUN). Perennial herb. Rhizome thick, 5–12 cm long, 1.5–4 cm in diameter. Stem erect, green or purple, 30.0–60.0 cm tall. Leaves 5–8, green, usually membranous, narrowly lanceolate, lanceolate, oblong-lanceolate, oblong, or ovate, apex acuminate, base cuneate to round, ca. 5.5–11.0 cm  1.0–4.5cm, petiole 0–2.5 cm in length. Flower solitary, basic merosity 4–7; pedicel green or purple, 1.0–15.0 cm long; sepals green or purple, 1.5–4.0 cm  0.3–1.0 cm, usually reflexed; petals dark purple (rarely yellowish-green), 0.5–1.0 mm wide. Stamens 2  petal number; filaments purple, 2.0–5.0 mm long; anthers yellow, 5–13 mm; free portion of connective purple, 2.0––15.0 mm long. Ovary

6.5 Section Euthyra

conical, green, unilocular with parietal placentation; style purple, with an enlarged base; stigma purple or dark red, 2.0–5.0 mm. Capsule conical, green, ca. 2.0–3.5 cm in diameter, dehiscing irregularly at maturity. Seed ellipsoid, covered by red and juicy sarcotesta (Figs. 6.44 and 6.45). Phenology: flowering April–May, fruiting June–October. Habitats: deciduous broad-leaved and coniferous forests; ca. 700–2900 m. Distribution: endemic to China: Chongqing (Chengkou, Nanchuan, Wushan), Guangxi (Jinxiu, Longsheng), Guizhou (Anlong, Ceheng, Danzhai, Daozhen, Dunyun, Leishan, Wangmo), Hubei (Shennongjia, Xingshan), Hunan (Longshan, Yizhang, Zhangjiajie), Jiangxi (Lushan), Sichuan (Dujiangyan, Emeishan, Hongya, Junlian, Leibo, Luding, Meigu, Nanjiang, Tianquan), Yunnan (Daguan, Dongchuan, Shuifu, Wenshan, Yanjin, Yiliang, Zhaoyang). Notes: (1) P. bockiana was reduced to P. polyphylla subsp. fargesii by Hara (1969), while Li (1986) reduced it to P. polyphylla var. stenophylla. I carefully examined the holotype, and found that its free portion of connective is purple and approximately 3.0 mm in length. This feature is consistent with that of P. delavayi but differs from both P. fargesii and P. lancifolia. Therefore, it should be reduced to P. delavayi. (2) Li (1998) proposed that P. delavayi var. petiolata is distinct from the typical variety in its ovate leaves (vs. narrowly lanceolate, lanceolate, and oblong-lanceolate leaves). However, P. delavayi has diverse leaf morphology, including narrowly lanceolate, lanceolate, oblong-lanceolate, oblong, oblong-ovate, and ovate leaves (Fig. 6.46). Characters (oblong and oblong-ovate leaves) intermediate between P. delavayi var. petiolata and the typical variety suggest that the difference in leaf shape is not robust enough to recognize them as distinct taxa. As a result, P. delavayi var. petiolata is here reduced to P. delavayi as a synonym. Additional specimens examined. CHINA, CHONGQING, Chengkou: Farges PG 573 (P); loc. eodem, 25 Jun. 1958, Dai TL 105424 (PE). Nanchuan: 06 Nov. 1935, Zhang XB 153 (NAS); loc. eodem, Qu GL 1217 (PE); loc. eodem, Qu GL 1226 (PE); loc. eodem, 30 May 1935, Qu ZX 1002 (PE); loc. eodem, 09 Jun. 1935, Qu ZX 1217 (PE); loc. eodem, 09 Jun. 1935, Qu ZX 1226 (PE); loc. eodem, 11 Jun. 1935, Qu ZX 1286 (PE); loc. eodem, 2050 m, 12 Jun. 1935, Qu ZX 1304 (PE); loc. eodem, 2050 m, 19 May 1964, Chen XQ & Lang KY 02363 (PE); loc. eodem, 1850 m, 19 May 1964, Chen XQ & Lang KY 02398 (PE); loc. eodem, 22 May 1964, Chen XQ & Lang KY 02422 (PE); loc. eodem, 22 May 1964, Chen XQ & Lang KY 02436 (PE); loc. eodem, 22 May 1964, Chen XQ & Lang KY 02438 (PE); loc. eodem, 23 May 1964, Chen XQ & Lang KY 02462 (PE); loc. eodem, 23 May 1964, Chen XQ & Lang KY 02467 (PE); loc. eodem, 2140 m, 23 May 1964, Chen XQ & Lang KY 02461 (PE); loc. eodem, 25 May 1932, Du DH 3144 (PE); loc. eodem, 840 m, 17 Apr. 1959, Li GF 60556

155

(PE); loc. eodem, 1700 m, 11 May 1957, Li GF 61061 (PE); loc. eodem, 21 May 1957, Li GF 61455 (PE); loc. eodem, 10 Jun. 1957, Li GF 61856 (PE); loc. eodem, 12 Jun. 1957, Li GF 62100 (PE, NAS); loc. eodem, 10 Jun. 1957, Li GF 618056 (KUN); loc. eodem, 1700 m, 10 May 1957, Li GF 60987 (KUN); loc. eodem, 18 May 1928, Fang WP 967 (IBSC); loc. eodem, 25 Mar. 1982, Tan SX & Zhang JL 3020 (IMC); loc. eodem, 25 Mar. 1982, Tan SX & Zhang JL 3026 (IMC); loc. eodem, 10 Jun. 1983, Liu ZY 4171 (IMC); loc. eodem, 10 Jun. 1983, Liu ZY 4174 (IMC); loc. eodem, 07 Jun. 1970, Liu SQ 700350 (IMC); loc. eodem, 07 Jun. 1970, Tan SX 700352 (IMC); loc. eodem, 11 Apr. 1996, Liu ZY 17961 (IMC); loc. eodem, 1800 m, 28 Apr. 1981, Liu ZY 815370 (IMC); loc. eodem, 1800 m, 28 Apr. 1981, Liu ZY 815371 (IMC); loc. eodem, 1800 m, 28 Apr. 1981, Liu ZY 815372 (IMC); loc. eodem, 1950 m, 09 May 1986, Liu ZY 8181 (IMC); loc. eodem, 1950 m, 09 May 1986, Liu ZY 8786 (IMC); loc. eodem, 1850 m, 08 May 1982, Liu ZY 3199 (IMC); loc. eodem, 1950–2000 m, 07 May 1978 Liu ZY 784034 (IMC); loc. eodem, 1700 m, 10 May 1976, Liu ZY 760716 (IMC); loc. eodem, 1700 m, 10 May 1976, Liu ZY 760718 (IMC); loc. eodem, 1650 m, 20 May 1976, Liu ZY 770290 (IMC); loc. eodem, 1650 m, 30 Apr. 1976, Liu ZY 760526 (IMC); loc. eodem, 1650 m, 30 Apr. 1976, Liu ZY 760529 (IMC); loc. eodem, 1650 m, 30 Apr. 1976, Liu ZY 760537 (IMC); loc. eodem, 1800 m, 29 Apr. 1980, Liu ZY 802644 (IMC); loc. eodem, 1800 m, 29 Apr. 1980, Liu ZY 802601 (IMC); loc. eodem, 1800 m, 29 Apr. 1980, Liu ZY 802600 (IMC); loc. eodem, 1800 m, 29 Apr. 1980, Liu ZY 802602 (IMC); loc. eodem, 27 Apr. 1980, Liu ZY & Liu LN 802411 (IMC); loc. eodem, Chu KL 1002 (PE); loc. eodem, 29 20 400 N, 107 110 4100 E, 2184 m, 10 May 2012, Nanchuan Expedition 5001190204-01 (IMC). Wushan: 03 May 1958, Yang GH 57936 (PE). GUANGXI, Jinxiu: 15 May 1995, D 950059 (GXMI). Longsheng: 25 440 N, 110 20 E, 08 Apr. 1962, Yuan SF & Liu LF 5144 (IBK); loc. eodem, 03 Jul. 1958, Chen ZZ 51145 (IBK); loc. eodem, 29 Jul. 1957, Qin HF & Li ZT 70871 (IBK). Luocheng: 10 Mar. 2013, Luocheng Expedition 451225130310031LY (IBK). GUIZHOU, Anlong: 1300 m, 17 May 1960, Zhang ZS & Zhang YT 2475 (PE). Ceheng: 1100–1300 m, 20 Aug. 1992, Yunnan-Guizhou-Guangxi Expedition D51046 (KUN). Danzhai: 31 May 2010, Chen TR et al. H-Danzhai-Z-0038 (BJFC). Daozhen: 1500 m, 17 Aug. 2003, Liu ZY 2030611 (IMC); loc. eodem, 1500 m, 17 Aug. 2003, Liu ZY 2030633 (IMC); loc. eodem, 1800 m, 22 Aug. 2003, Liu ZY 2031722 (IMC); loc. eodem, 1800 m, 22 Aug. 2003, Liu ZY 2031723 (IMC). Dunyun: 29 May 2009, Liu LD 0923042 (QNUN). Leishan: 1800 m, 29 Aug. 1959, Yunnan-Guizhou expedition 921 (PE); loc. eodem, 2100 m, 10 Jun. 1964, Hu CH 292 (PE). Wangmo: 1400 m, 13 Apr. 1960, Zhang ZS & Zhang YT 0760 (PE). HUBEI, Shennongjia: 215 m, 20 Jun. 1976, Shennongjia Expedition 10374 (PE); loc. eodem, 750 m,

156

Fig. 6.44 Paris delavayi (drawn by M. Shen): aerial shoot (a) and dehisced capsule (b)

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6.5 Section Euthyra

Fig. 6.45 Flower (a), pistil (b), longitudinal (c) and transverse (d) section of ovary, dehisced capsule (e), and seeds (f) of Paris delavayi

157

158

Fig. 6.46 Leaf shape variation in Paris delavayi

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6.5 Section Euthyra

09 May 2016, Zhao XL 2016050 (KUN); loc. eodem, 800 m, 09 May 2016, Zhao XL 2016054 (KUN); loc. eodem, 850 m, 09 May 2016, Zhao XL 2016058 (KUN). Xingshan: 27 May 1957, Liu Y 500 (PE). HUNAN, Longshan: 1200 m, 30 May 1958, Liu LH 1761 (PE). Yizhang: 25 240 N, 112 570 E, 02 Nov. 1944, Liang BH 85170 (IBK). Zhangjiajie: 700 m, 26 Mar. 2015, Luo H & Zhou JL 15032601 (CSFI). JIANGXI, Lushan: 13 Apr. 1951, Zou Y 00108 (LBG). SICHUAN, Dujiangyan: 1930, Wang FT 20732 (PE); loc. eodem, 1930, Wang FT 20895 (PE). Emeishan: 01 May 1940, Sun SL 1837 (PE); loc. eodem, 11 May 1952, Jiang XL et al. 30483 (PE); loc. eodem, 22 Jun. 1955, Sino-Soviet Expedition 2069 (PE). Hongya: 19 Jun. 1939, Yao ZW 3696 (PE). Junlian: 02 Apr. 1959, Yibin Wild Plants Survey 0170 (CDBI). Leibo: 1800 m, 30 May 1959, Guan ZT 8193 (PE); loc. eodem, 1800 m, 09 Jun. 1959, Guan ZT 8398 (PE). Luding: 29 540 N, 102 130 E, 2 May 1980, Wang QQ 22032 (CDBI); loc. eodem, 2200 m, 2 May 1980, Wang QQ 22032A (CDBI). Meigu: 21 Aug. 1959, Sichuan Economic Botany Expedition 1854 (KUN). Nanjiang: 02 Jun. 1960, Sichuan Economic Botany Expedition 19 (CDBI). Tianquan: 30 040 N, 102 450 E, 03 Jun. 1953, Jiang XL 34297 (IBK). YUNNAN, Daguan: 1870 m, 17 May 2016, Li H et al. 024 (KUN). Dongchuan: 2860 m, 10 Aug. 1964, NE Yunnan Expedition 539 (KUN). Shuifu: 26 Apr. 2002, Liu ZY 2022179 (IMC). Wenshan: 2990 m, 29 Sep. 1992, Shui YM 000421 (KUN); loc. eodem, HE XQ s. n. (KUN). Yanjin: 02 Apr. 1964, Yang JS 2939 (KUN). Yiliang: 1900 m, 17 Jun. 1982, Li H, Chen Y & Fei Y 1324 (HITBC); loc. eodem, 1850 m, 15 May 1981, NE Yunnan Expedition 0604 (KUN); loc. eodem, 1900 m, 17 Jun. 1982, Li H, Chen Y & Yu HY 1324 (KUN); loc. eodem, 1900 m, 17 Jun. 1982, Li H, Chen Y & Yu HY 1325 (KUN); loc. eodem, 1850 m, 13 Sep. 1972, NE Yunnan Expedition 603 (KUN); loc. eodem, 20 Mar. 1964, Yang JS & Liu DC 64-2798 (KUN). Zhaoyang: 1860 m, 16 May 2016, Li H et al. 010 (KUN); loc. eodem, 1860 m, 16 May 2016, Li H et al. 015 (KUN); loc. eodem, 2110 m, 16 May 2016, Li H et al. 016 (KUN). 19. Paris liiana Y. H. Ji, Front Plant Sci 11:411. 2020. Type: China. Yunnan: Yuanyang, Xiaoxinjie, 24 430 53.7600 N, 104 210 06.0100 E, 1599 m, 7 Aug. 2016, Ji YH 2016457 (Holotype, KUN); Qiubei, 24 030 55.4500 N, 104 100 57.5700 E, 1530 m, 12 Jul. 2016, Huang YL 006 (Paratype, KUN). Perennial herbs with cylindrical, oblique or horizontal rhizomes, yellowish brown outside, and white inside, 3.0–7.0 cm in diameter, 5.0–20.0 cm long, bearing a bud at the top, roots up to 30.0 cm long. Stem erect, cylindrical, purplish red or green, 50.0–150.0 cm tall. Leaves 5–12 in an apical whorl, green; petiole light green, 8.0–3.0 cm long; leaf blades elliptic or oblong-obovate, apex acute, 20–30 cm  8–15 cm oblong, 6.0–19.0  3.5–9.5 cm; two pairs of lateral veins, basally developed. Flower solitary and

159

terminal, basic merosity 5–10. Peduncle green or light purple, 25.0–50.0 cm; sepals 5–10, oblong or obovate-oblong, green, ca. 5–12  2.5–5 cm 3.5–8.6  1.6–2.2 cm; petals 5–10, filiform-linear, green at low portion, greenish yellow at upper portion, distally slightly widened to 2–3 mm, shorter or slightly longer than sepals. Stamens 2  petal number, filament greenish yellow, 3.0–6.0 mm, anthers golden yellow, dehiscing by a lateral slit, 1.5–4.0 cm long. Ovary pale green at base, purplish red apically, with 5–10 slight ridges, carpels 5–10, unilocular with parietal placenta; style 4.0–5.0 mm, with an enlarged base, purplish red, stigmas 5–10-lobed, dark brown. Capsule dehiscent, subglobose, green, dark red or brown at the top. Seeds numerous, with a red and juicy sarcotesta (Figs. 6.47 and 6.48). Phenology: flowering April–May, fruiting June– December. Habitats: evergreen broad-leaved forests dominated Castanopsis, Lithocarpus, Quercus, and Schima species; ca. 1200–2200 m. Distribution: endemic to China: Guangxi (Longlin, Nanning), Guizhou (Anlong, Xingyi), Yunnan (Eshan, Guangnan, Jingdong, Jinghong, Menghai, Mengla, Lancang, Longling, Lüchun, Luoping, Pingbian, Simao, Xichou, Xinping, Yanshan, Yuanjiang). Additional specimens examined: CHINA, GUANGXI, Longlin: 01 Jun. 1957, Liang CF & Wu DL 32471 (IBSC). Nanning: 07 Jul. 1973, Huang XC 5833 (GXMG). GUIZHOU, Anlong: 27 440 34.700 N, 98 360 17.100 E, 1800 m, 09 Jun. 1960, Guizhou Expedition 3167 (KUN); loc. eodem, 09 Jun. 1960, Zhang ZS & Zhang YT 4155 (PE). Xingyi: 20 Jul. 1960, Zhang ZS & Zhang YT 6408 (PE). YUNNAN, Eshan: 1350 m, 11 Jul. 1989, Yuxi Expedition 89-516 (KUN); loc. eodem, 1300 m, 29 Apr. 1988, Eshan Expedition 88-101 (KUN). Guangnan: 05 Jan. 2016, Guangnan Expedition 5326270519 (IMDY); loc. eodem, 20 Jan. 2016, Guangnan Expedition 5326270534 (IMDY). Jingdong: 21 Oct. 1956, Qiu BY 52963 (KUN); loc. eodem, 28 Apr. 1959, Xu SG 5049 (KUN); loc. eodem, 06 Dec. 1939, Li MG 2263 (KUN). Jinghong: Sept. 1936, Wang CW 78693 (PE); loc. eodem, May 1984, Tao GD 44099 (HITBC). Menghai: May 1936, Wang CW 74278 (PE); loc. eodem, 14 Jun. 2012, Menghai Census 5328220509 (IMDY); loc. eodem, 24 Apr. 2012, Menghai Census 5328220065 (IMDY); loc. eodem, 03 Oct. 1959, Cai XT 59-10459 (KUN); loc. eodem, 1650 m, 17 Jun. 1960, Yunnan Tropic Expedition 60-11693 (KUN). Mengla: 10 Nov. 1959, Pei SJ 59-11386 (KUN). Lancang: 20 Aug. 2015, Yang YP yi-173-1 (KUN). Longling: 17 May 2015, Longling Census 530523150517045LY (IMDY). Lüchun: 16 Oct. 1973, Tao DD 856 (KUN). Luoping: 27 May 1989, Hongshui River Expedition 1722 (KUN); loc. eodem, 2480 m, 28 May 1989, Hongshui River Expedition 1922 (KUN). Fengqing: 18 Jun. 1938, Yu TT 16348 (PE). Pingbian: 05 Oct. 1939, Wang CW

160 Fig. 6.47 Holotype (a), aerial shoots (b), leaf shape and size (c), flower (d), sepals (e), young fruit (f), and dehisced capsule (g) of Paris liiana

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161

Fig. 6.48 Development of aerial shoot in Paris liiana

82319 (PE). Simao: 29 May 2012, Simao Census 5308020534 (IMDY); loc. eodem, 14 Jun. 2012, Simao Census 5308020705 (IMDY); loc. eodem, 17 May 2012, Simao Census 5308020404 (IMDY). Xichou: 2200 m, 24 Sept. 1947, Feng GM 11993 (KUN). Xinping: 03 Jun. 2012, Xinping Census 5304270419 (IMDY). Yanshan: 1250–1320 m, 09 Oct. 1939, Wang QW 84252 (KUN). Yuanjiang: 08 Jun. 2012, Yuanjiang Census 5304280573 (IMDY). 20. Paris yunnanensis Franch., Mem. Philom. Cent. (Paris) 24: 290. 1888; C. H. Wright, Journ. Linn. Bot. 36: 145. 1903.  Paris polyphylla Smith var. yunnanensis (Franch.) Hand.-Mazz., Symb. Sin. 7: 1216. 1936; Hara, Journ. Fac. Sci. Univ. Tokyo. Sect. 3, 10 (10): 154. 1069; Wang et Tang, Fl. Reip. Pop. Sin. 15: 95. 1978; H. Li, Bull. Bot. Res. Harbin 6 (1): 119. 1986; H. Li, The Genus Paris (Trilliaceae) 35. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 90. 2000.  Daiswa yunnanensis (Franch. ) Takht., Brittonia 35 (3): 257. 1983; B. Mitchell, Plantsman 10 (3): 185. 1988. Type: China, Yunnan, Eryuan, 2000 m, J. M. Delavay 2227 (Holotype, P). Paris christii Lévl., Bull. Acad. Inter. Geogr. Bot. 12: 255. 1903. Type: China, Guizhou, Bodinier s. n. (Holotype, E). Paris mercieri Lévl., Bull. Acad. Int. Géogr. Bot. 12: 255. 1903. Type: China, Guizhou, Guiyang, 17 Jul. 1898, Bodinier 1635 (Holotype, E). Paris franchetiana Lévl., Bull. Acad. Int. Géogr. Bot. 12: 255. 1903. Type: China, Guizhou, Bodinier 712 (Holotype, E). Paris cavaleriei Lévl. et Vaniot, Nouv. Contrib. Liliac. Chine 24: 354. 1906. Type: China, Guizhou, Longli, 13 Jun. 1902, Cavalerie 1310 (Holotype, E). Paris gigas Lévl. et Vaniot, Nouv. Contrib. Liliac. Chine 24: 354. 1906. Type: China, Guizhou, Guiding, 23 Nov. 1902, Cavalerie 729 (Holotype, E). Paris pinfaensis Lévl., Repert. Spec. Nov. Regni Veg. 6: 265. 1909. Type: China, Guizhou, Guiding, Jun. 1907, Cavalerie 2023 (Holotype, E; Isotype, GH, K).

Paris aprica Lévl., Repert. Spec. Nov. Regni Veg. 6: 265. 1909. Type: China, Guizhou, Guiding, 25 Jun. 1907, Cavalerie 3023 (Holotype, Isotype, E). Paris atrata Lévl., Repert. Spec. Nov. Regni Veg. 12: 536. 1913. Type: China, Yunnan, Ninglang, Maire s. n. (Holotype, E). Paris polyphylla Smith var. nana H. Li, Bull. Bot. Res. Harbin 6 (1): 123. 1986. Type: China, Sichuan, Yibin, 07 Jul. 1977, Yibin Drug Inspection Institute Yi428 (KUN). Paris daliensis H. Li et V. G. Soukup, Act. Bot. Yunnanica, Supp. v: 15–16, fig. 3. 1992; H. Li, The Genus Paris (Trilliaceae) 32. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 89–90. 2000. Type: China, Yunnan, Dali, 2600 m, 06 Nov. 1986, H. Li & V. G. Soukup 1098 (Holotype, KUN; Isotype, CINC). Paris birmanica (Takht.) H. Li et H. Noltie., Edinb. J. Bot. 54 (3): 351–352. 1997; H. Li, The Genus Paris (Trilliaceae). 28. 1998.  Daiswa birmanica Takht., Brittonia 35 (3): 259, fig. 2. 1983; B. Mitchell, Plantsman 10 (3): 169. 1988; Type: Myanmar, Maymyo, 22 Jun. 1913, Lace John Henry 6233 (Holotype, E; Isotype, E). Paris polyphylla Smith var. emeiensis X. H. Yin, H. Zhang & D. Xue, Acta Phytotaxon. Sin. 45 (6): 822–827. 2007. Type: China, Sichuan, Mt. Emei, 1900 m, 27 Apr. 2006, Yin XH et al. 06121 (Holotype, SZ; Isotype, CDBI). Perennial herb. Rhizome thick, ca. 7–15.0 cm  1.5–6.0 cm. Stem, erect, 25.0–100.0 cm tall, glabrous, purple at lower portion and yellowish green at upper portion. Leaves 5–11; leaf blades green, ovate, obovate, oblong, or obovate-oblong, apex acute to acuminate, base cuneate to rounded, 5.0–15.0 cm  3.0–7.0 cm; petiole purple or green, 0.5–7.0 cm long. Flower solitary, basic merosity 4–7; pedicel green or purple, 0–45.0 cm long; sepals green, lanceolate, 2.5–7.0 cm long, yellowish green; petals yellow (rarely purple), 3.0–5.0 mm wide, longer than or as long as sepals. Stamens 2  petal number, arranged in 2 whorls, 10.0–25.0 mm long; filaments yellowish green, 3.0–10.0 mm long; anthers

162

yellow, 5.0–15.0 mm long, dehiscing by a lateral slit; free portion of connective inconspicuous. Ovary unilocular with parietal placentation, green, smooth or tuberculate, with 4–7 ridges; style purple, 0–2.0 mm, with an enlarged base; stigmas purple, 4.0–10.0 mm long, erect at flowering, revolute at fruiting. Capsule subglobose, green, irregularly dehiscing, 1.5–7.5 cm in diameter. Seeds numerous, ovoid, covered by red and juicy sarcotesta (Figs. 6.49, 6.50 and 6.51). Phenology: flowering April–June, fruiting June–October. Habitats: evergreen (or deciduous) broad-leaved and coniferous forests, bamboo thickets, and scrubs; ca. 1000–3200 m. Distribution: Burma (Mandalay, Shan States). China: Chongqing (Jiangjin, Nanchuan), Guangxi (Leye, Longsheng), Guizhou (Chishui, Daozhen, Guiding, Hezhang, Nayong, Qingzhen, Suiyang, Weining, Yinjiang, Zhengan), Sichuan (Butuo, Dechang, Ebian, Huidong, Huili, Jinyang, Jiulong, Kangding, Leibo, Luding, Mabian, Meigu, Muli, Shimian, Tianquan, Xichang, Xuzhou, Yanyuan, Zhaojue), Tibet (Mainling), Yunnan (Anning, Binchuan, Dali, Dayao, Deqin, Eryuan, Fugong, Fumin, Fuyuan, Gongshan, Heqing, Jiangchuan, Lanping, Lijiang, Longling, Longyang, Luquan, Lushui, Malipo, Midu, Qiubei, Shangrila, Shuifu, Songming, Tengchong, Weixi, Wenshan, Yangbi, Yingjiang, Yongping, Yongshan, Yongsheng, Yunlong, Zhaoyang). Notes: (1) Handel-Mazzetti (1936) reduced P. yunnanensis as a conspecific variety under P. polyphylla, and the treatment was followed by Hara (1969), Wang and Tang (1978), Li (1984a, 1998), and Liang and Soukup (2000). Nevertheless, phylogenetic analyses revealed that P. yunnanensis is phylogenetically distinct from P. polyphylla (Ji et al. 2006a, 2019, 2020), which provides support for recognizing it as a distinct species. (2) Except for a shortened pedicel and the thickened free portion of the connective, the leaf and flower morphologies of P. polyphylla var. emeiensis (Fig. 6.52d) and P. daliensis (Fig. 6.53) are almost identical to that of P. yunnanensis. These differences are not robust enough to recognize them as distinct taxa. Accordingly, here P. polyphylla var. emeiensis and P. daliensis are reduced to P. yunnanensis. Additional specimens examined. BURMA, MANDALAY, Maymyo: 1067 m, 10 Jun. 1925, Forest Botanist’s Collection 1637 (K). SHAN STATES, Keng Tung: 1676 m, May 1909, MacGregor 704 (E); Maymyo, 1036 m, 6 July 1912, Lace 5872 (E, K). Taunggyi: 20 470 N, 97 090 E, 1041 m, 21 Dec. 2016, Ji YH 2017010 (KUN). CHINA, CHONGQING, Jiangjin: 08 Mar. 2016, Liu ZY & Lin MX S-0436-b (IMC). Nanchuan: 27 Apr. 1984, Liu ZY 5066 (IMC); loc. eodem, 18 Apr. 1980, Specimen Group 0183 (IMC); loc. eodem, 1950 m, 10 Jun. 1983, Liu ZY 4171 (IMC); loc. eodem, 11 Apr. 1979, Liu ZY 790924 (IMC).

6 Taxonomic Revision

GUANGXI, Leye: 09 May 1989, Honghe River Expedition 1057 (KUN). Longsheng: 26 Jun. 1958, Chen ZZ 51067 (PE). GUIZHOU, Chishui: 25 May 2016, Hou XQ 520381160525513LY (GZTM). Daozhen: 17 Apr. 2003, Liu ZY 2030728 (IMC). Guiding: 05 Jun. 1907, Cavalerie & Pierre Julien 2023b (E); loc. eodem, 25 Jun. 1907, Cavalerie & Pierre Julien 3023 (E); loc. eodem, 23 Nov. 1902, Cavalerie & Pierre Julien 3729 (E). Hezhang: 03 Jul. 2015, Rao YD 522428150703055LY (GZTM). Nayong: 25 Jul. 1959, Bijie Expedition 388 (PE). Qingzhen: 15 Oct. 1956, Sichuan-Guizhou Expedition 1895 (PE); loc. eodem, 06 Jul. 1983, Le GD 830359 (GNUG). Suiyang: 19 May 2009, Shang M 093334 (ZY); loc. eodem, 12 May 2009, Zhang J KKS094217 (ZY). Weining: 09 Jul. 1959, Bijie Expedition 219 (PE); loc. eodem, 22 Jun. 2014, Weining Expedition 522427140620323LY (GZTM); loc. eodem, 25 Jun. 1983, Tu YL 289 (GNUG). Yinjiang: 15 May 2014, An MT YJ-2014-0071 (GZAC). Zhengan: 19 Apr. 2016, Zheng JH 520324160419005LY (GZTM). SICHUAN, Butuo: 02 Aug. 1959, Sichuan Economic Botany Expedition 5778 (CDBI). Dechang: 08 Jun. 1978, Zhao QS & Liu JS 5222 (CDBI); loc. eodem, 20 May 1959, Wu SG 908 (KUN). Ebian: 29 Sep. 1958, Yao CW 3037 (PE). Huidong: 2100 m, 02 Jun. 1959, Wu SG 1416 (CDBI, KUN); loc. eodem, 27 May 1978, Huidong Expedition 0007 (CQNM). Huili: 20 Jul. 1984, Liang YF et al. 84-18 (PE); loc. eodem, 03 Jun. 1978, Zhao QS & Liu JS 5727 (CDBI). Jinyang: 18 Sep. 1984, Liang YF et al. 84-41 (PE). Jiulong: 01 Jun. 1974, Wang QQ 4576 (CDBI); loc. eodem, 09 Aug. 1979, Wang QQ 21460 (IBSC). Kangding: 02 May 1974, Feng JH 06023 (CDBI); loc. eodem, 03May 1974, Sichuan Vegetation Survey 05293 (CDBI). Leibo: 1600 m, 09 Jun. 1959, Guan ZT 8378 (PE). Luding: 04 May 1981, Wang QQ 25147 (CDBI); loc. eodem, 02 May 1980, Liu ZG & Wang QQ 21953 (CDBI); loc. eodem, 1800 m, 08 Sep. 1981, Vegetation Survey 26064 (CDBI). Mabian: 1930, Wang FT 22897 (PE). Meigu: 02 Jul. 1976, Sichuan Vegetation Survey 13057 (CDBI). Muli: 17 Oct. 1984, Liang YF et al. 84-82 (PE). Shimian: 1955, Xie ZJ 40554 (PE). Tianquan: 02 Apr. 1980, Yang YB 21764 (CDBI). Xichang: 02 May 1978, Zhao QS & Hu G 4890 (CDBI); loc. eodem, 02 May 1978, Zhao QS & Hu G 4889 (CDBI). Xuzhou: 04 Jun. 1982, Sun CR 110 (IBSC). Yanyuan: 2200 m, 20 Jul. 1983, Qinghai-Tibet Expedition 12081 (KUN). Zhaojue: 02 Jun. 1976, Sichuan Vegetation Survey 12757 (CDBI). TIBET, Mainling: 2300 m, 14 Jul. 1985, Tibet Pharmaceutical Inspection Institute 0108 (KUN). YUNNAN, Anning: 14 Jul. 1965, Wu ZY 134 (KUN). Binchuan: 18 May 1996, Tao DD 9610 (KUN). Dali: 28 Aug. 1940, Chiu SF & Sping LH 50 (IBSC); loc. eodem, 08 Oct. 1946, Liu SE 21394 (PE); loc. eodem, Aug. 1941, Wang HC 1281 (PE, KUN); loc. eodem, 26 320 3800 N, 98 550 3500 E, 2230 m, 13 Sep. 2009, Yin ZJ, Wang ZH & Chen L 2196 (KUN); loc. eodem, 2600 m, 13 Jul. 2009, Yin

6.5 Section Euthyra

Fig. 6.49 Paris yunnanensis (drawn by M. Shen): rhizome (a), aerial shoot (b), and dehisced capsule (c)

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Fig. 6.50 Aerial shoots (a), flower (b), pistil (c), longitudinal (d) and transverse (e) section of ovary, and dehisced capsule (f) of Paris yunnanensis

6.5 Section Euthyra

Fig. 6.51 Variation in leaf shape of Paris yunnanensis

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Fig. 6.52 Pedicel length variation in Paris yunnanensis. Pedicel longer than 25 cm (a), 10–20 cm (b), shorter than 10 cm (c), and nearly absent (d)

ZJ, Dong HJ & Xiang CL 1092 (KUN); loc. eodem, 26 30 5300 N, 98 370 5600 E, 1950 m, 12 Sept. 1983, Sino-US Yunnan Expedition 0122 (KUN); loc. eodem, 24 520 2300 N, 98 430 3100 E, 1850 m, 15 Oct. 1991, N. Tanaka 21 (KUN); loc. eodem, 17 Oct. 1987, Li YH 00319 (KUN); loc. eodem, 2400 m, 09 May 1988, Guo HJ 246 (KUN); loc. eodem, 2000 m, 09 May 1988, Guo HJ 1486 (KUN); loc. eodem, 1250 m, 18 May 1984, Sino-German Expedition 403 (KUN); loc. eodem, 16 May 1984, Sino-German Expedition 179 (KUN); loc. eodem, 1300 m, 01 Jul. 1984, Sino-US Expedition to Yunnan 771 (KUN); loc. eodem, 21 Oct. 1929, Qin RC 25133 (KUN); loc. eodem, 2300 m, 07 Aug. 1963, Zhongdian Expedition 63-3957 (KUN). Dayao: 26 May 1989, Chen Y & Bai B 088 (KUN); loc. eodem, 04 Jun. 1989, Chen Y & Bai B 303 (KUN). Deqin: 25 380 N, 100 100 E, 2200–2350 m, 05 Jul. 1981, QinghaiTibet Expedition 1925 (KUN); loc. eodem, 3200 m, 05 Oct. 1959, Feng GM 23916 (KUN). Eryuan: 02 Sep. 1975, Qiu BY 60978 (CDBI); loc. eodem, 28 Jul. 1940, Qin RC 23287 (PE, KUN); loc. eodem, 01 Jun. 1886, Delavay J. M. s. n. (P). Fugong: 24 Sep. 2014, Li H, Yang J & Wang YH NJ009-B-3 (KUN); loc. eodem, 2100 m, 31 May 2015, Li H et al. 149-2 (KUN); loc. eodem, 2300 m, 31 May 2015, Li H et al. 149-3 (KUN). Fumin: 2500 m, 24 May 1964, Qiu BY 59204 (KUN). Fuyuan: 1900 m, 27 Jun. 1987, Spice Plants Expedition 870232 (KUN); loc. eodem, 24 520 2300 N, 98 430 3100 E, 1850 m, 20 Jun. 1989, Honghe River Expedition 2331 (KUN). Gongshan: 24 Sep. 2014, Li H, Yang J & Wang YH NJ009-2 (KUN); loc. eodem, 21 Apr. 2002, Li H, Ji YH & Li R 14574 (KUN); loc. eodem, 01 Jun. 2015, Li H et al. 154-1

(KUN); loc. eodem, 26 320 3800 N, 98 550 3600 E, 2230 m, 02 Jun. 2015, Li H et al. 158-3 (KUN); loc. eodem, 27 500 1500 N, 98 410 1700 E, 1510 m, 04 May 2002, Li H, Ji YH & Li R 14923 (KUN); loc. eodem, 27 590 5400 N, 98 370 1000 E, 2540 m, 24 Apr. 2002, Li H, Ji YH & Li R 14681 (E). Heqing: 18 Apr. 1939, Feng GM 714 (PE); loc. eodem, 1900 m, 22 Aug. 1929, Qin RC 23887 (KUN); loc. eodem, 1780 m, 20 Sep. 1962, Lü CZ 62011 (KUN). Jiangchuan: 700 m, 01 Nov. 1989, Yuxi Expedition 1364 (KUN). Lanping: 29 Jun. 1981, Hengduan Mountains Expedition 896 (PE). Lijiang: 2300 m, 27 Aug. 1988, Guo HJ 1966 (KUN); loc. eodem, 2750 m, 27 May 1988, Pei SJ 1585 (KUN); loc. eodem, 05 Jun. 1981, Qinghai-Tibet Expedition 367 (KUN); loc. eodem, 2380 m, 09 Aug. 1962, Zhongdian Expedition 644 (KUN); loc. eodem, 01 Jan. 1980, Li ST 80-239 (KUN); loc. eodem, 2400 m, 09 Jun. 1981, Qinghai-Tibet Expedition 780 (KUN, PE); loc. eodem, 02 Jul. 1956, Yunnan University 51 (IBSC); loc. eodem, 25 May 1939, Qin RC 20413 (PE). Longyang: 25 180 4600 N, 98 450 5700 E, 1900 m, 08 Nov. 1998, Li H, Bruce Bartholomew & Diao ZL 11657 (HAST). Luquan: 11 Jun. 1965, Woody Oil Expedition 65-0021 (LBG, KUN); loc. eodem, 11 Jun. 1952, Mao PY 01200 (IBSC); loc. eodem, 04 Dec. 1952, Mao PY 01915 (PE, KUN); loc. eodem, 2400 m, 07 Jun. 1982, Li H 1083 (KUN). Lushui: 2200 m, 25 Sep. 2014, Li H, Yang J & Wang YH NJ-009-A (KUN); loc. eodem, 2380 m, 16 May 2005, Li H et al. 23258 (KUN); loc. eodem, 24 Setp. 2014, Li H, Yang J & Wang YH NJ-009-B-1 (KUN); loc. eodem, 28 May 1981, Hengduan Mountains Expedition 201 (PE). Malipo: 1100 m, 13 May

6.5 Section Euthyra

167

Fig. 6.53 Aerial shoots (a), flower (b), stamens (c), pistil (d), longitudinal section of ovary (e), young fruit (f), and dehisced capsule (g) of Paris daliensis (syn. P. yunnanensis)

1964, Wang SZ 303 (KUN). Midu: Hou CL s. n. (IMDY). Qiubei: 2300 m, 03 May 1972, Yunnan Baiyao Factory s. n. (KUN). Shangri-la: 28 Sep. 2002, Fang ZD et al. K-1730 (SABG). Shuifu: 07 Apr. 2002, Liu ZY 2020551 (IMC); loc.

eodem, 12 Apr. 2003, Liu ZY 2021155 (IMC). Songming: 2400 m, 22 Aug. 1957, Qiu BY 54825 (KUN); loc. eodem, 10 Oct. 1950, Mao PY 144 (KUN). Tengchong: 11 May 2015, Tengchong Expedition 530522150511137LY (IMDY);

168

loc. eodem, 27 May 2005, Li H et al. 25015 (KUN); loc. eodem, 27 May 2005, Li H et al. 25014 (KUN). Weixi: Jul. 1935, Wang CW 64348 (PE); loc. eodem, 2600 m, 07 Jun. 1974, Yang JS 7056 (KUN); loc. eodem, 01 Jul. 1972, Yunnan Baiyao Factory s. n. (KUN); loc. eodem, 1500–2000 m, 01 Jul. 1935, Wang QW 67960 (KUN); loc. eodem, 1500–2000 m, 14 Nov. 1963, Lü CZ 63241 (KUN); loc. eodem, 3200 m, 03 Nov. 1940, Feng GM 8922 (KUN); loc. eodem, 2860 m, Feng GM 3942 (KUN); loc. eodem, 2600 m, 05 Nov. 1963, Lü CZ 63246 (KUN). Wenshan: 24 Apr. 1962, Feng GM 22163 (IBSC). Yangbi: loc. eodem, 2500 m, 23 Aug. 1984, K. Iwatsuki 915 (KUN); loc. eodem, 2100 m, 09 Aug. 1963, Zhongdian Expedition 63-4220 (KUN); loc. eodem, 1950 m, 04 Aug. 1963, Zhongdian Expedition 63-4050 (KUN). Yingjiang: 26 Nov. 1981, Tao GD 12628 (HITBC). Yongping: 02 May 1981, QinghaiTibet Expedition 93 (CDBI); loc. eodem, 1900 m, 01 Jun. 1972, Yunnan Baiyao Factory s. n. (KUN). Yongshan: 05 Jul. 1932, Cai HT 51208 (PE). Yongsheng: 12 Aug. 2012, Yongsheng Expedition 5307220315 (IMDY). Yunlong: 3450 m, 15 Oct. 1984, Yue ZS 84-016 (KUN). Zhaoyang: 1860 m, 16 May 2016, Li H et al. 012 (KUN). 21. Paris luquanensis H. Li, Act. Bot. Yunnan 4 (4): 353. 1982; H. Li, Act. Bot. Yunnan 6 (5): 358. 1984; H. Li, Bull. Bot. Res. Harbin 6 (1): 129, 1986; H. Li, The Genus Paris (Trilliaceae) 46. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 92. 2000. Type: China, Yunnan, Luquan, Zhu WM 671 (Holotype, HGUY); loc. eodem, Li H. 1082, 1326 (Paratype, KUN). Perennial herb. Rhizome thick, brown outside, ca. 1.5–5.0 cm  0.5–2.0 cm. Stem purple, erect, 5.0–20.0 cm tall, glabrous. Leaves 4–7; leaf blades obovate or elliptic, ca. 3.2–9.5 cm  2.0–6 cm, apex abruptly narrow, acute or short acuminate, base cuneate or wide cuneate, rarely rounded, green or deep green adaxially, dark purple abaxially, tinged with pale green along veins; petiole sessile, or 2.0–10.0 mm. Flower solitary, basic merosity 4–7; pedicel purple, 2.0–10.0 cm; sepals lanceolate, ovate-lanceolate or elliptic, with greenish white veins, ca. 1.5–4.0 cm  4.0–10.0mm, acuminated at apex, base slightly narrow; petals filiform, yellow, 2.0–5.0 cm in length, longer than sepals. Stamens  petal number, arranged in 2 whorls, 5.0–10.0 mm long; anthers linear, yellow, 2.0–6.0 mm long; free portion of connective inconspicuous. Ovary purple or green, ovoid, with 4–7 ridges, unilocular with parietal placentation, ovules numerous, ovate, white; style purple, 2.0–3.0 mm long; stigmas purple, short, erect, shorter than 1 mm, revolute at fruiting. Capsule green, ca. 1.0–2.5 cm in diameter. Seeds subglobose, ca. 4.0–6.0 mm in diameter, wholly enveloped by red and juicy sarcotesta (Figs. 6.54 and 6.55). Phenology: flowering from April–June, fruiting July– October.

6 Taxonomic Revision

Habitats: evergreen (or deciduous) broad-leaved and coniferous forests; ca. 2300–2800 m. Distribution: endemic to China: Sichuan (Huidong), Yunnan (Luquan). Additional specimens examined. CHINA, SICHUAN, Huidong: 30 Sept. 1961, 11963 (PE). YUNNAN, Luquan: 07 Jun. 1982, Li H, Chen Y & Fei Y 1182 (HITBC); loc. eodem, 16 Jun. 1982, Li H, Chen Y & Yu HY 1326 (KUN); loc. eodem, 16 Jun. 1982, Li H, Chen Y & Yu HY 1326A (KUN); loc. eodem, 16 Jun. 1982, Li H, Chen Y & Yu HY 1326B (KUN); loc. eodem, 16 Jun. 1982, Li H, Chen Y & Yu HY 1326C (KUN); loc. eodem, 16 Jun. 1982, Li H, Chen Y & Yu HY 1326D (KUN); loc. eodem, 16 Jun. 1982, Li H, Chen Y & Yu HY 1326E (KUN); loc. eodem, 16 Jun. 1982, Li H, Chen Y & Yu HY 1326F (KUN); loc. eodem, 16 Jun. 1982, Li H, Chen Y & Yu HY 1326G (KUN); loc. eodem, 16 Jun. 1982, Li H, Chen Y & Yu HY 1326I (KUN); loc. eodem, 16 Jun. 1982, Li H, Chen Y & Yu HY 1326K (KUN). 22. Paris lancifolia Hayata, Bot. Mag. (Tokyo) 20: 52. 1906; Hayata, Fl. Mont. Formos. t. 39. 1908; Y. Kimura in Nakai, Icon. Pl. As. Or. 236. 1940; S. S. Ying, Fl. Taiwan 5: 68. 1978.  Daiswa lancifolia (Hayata) Takht., Brittonia 35 (3): 266. 1983; Huang TC et Yang KC, Taiwania 33: 123. 1988. Type: China, Taiwan, Oct. 1905, S. Nagasawa 693 (not seen). Paris polyphylla Smith var. stenophylla Franch., Nouv. Arch. Mus. Hist. Nat. ser. 2, 10: 97. 1888; Hand.-Mazz., Symb. Sin. 7: 1216; 1936; Hara, Journ. Fac. Sci. Unit. Tokyo, Sect. 3, 10 (10): 176. 1969; Wang et Tang, Fl. Reip. Pop. Sin. 15: 94. 1978; H. Li, Bull. Bot. Res. Harbin 6 (1): 124. 1986; H. Li, The Genus Paris (Trilliaceae) 39. 1998. Type: China, Sichuan, Baoxing, Jun. 1869, A. David s. n. (Holotype, P). Paris polyphylla Smith var. brachystemon Franch., Journ. Bot. (Morot) 12: 191. 1898; Hara, Fl. East Himal 410. 1966; Hara, Journ. Fac. Soc. Univ. Tokyo, sect. 3, 10 (10): 1969. Type: China, Chongqing, Chengkou, Farges s. n. (Holotype, P). Paris hamifer Lévl. in Fedde, Repert. Spec. Nov. Regni Veg. 12: 288. 1913. Type: China, Yunnan, Ninglang, 3000 m, May 1912, Maire s. n. (Holotype, E). Paris arisanensis Hayata, Icon. Pl. Formosan. 9: 141. 1920; Y. Kimura in Nakai, Icon. Pl. As. Or. 3 (3): 235, t. 86. 1940. Type: China, Taiwan, Apr. 1916, B. Hayata s. n. (not seen). Paris taitungensis S. S. Ying, Quart. Journ. Chin. For. 8 (4): 139. 1975. Type: China, Taiwan, Taidong, Sangyang 1037 (NTUF). Paris polyphylla Smith var. latifolia Wang & Tang, Fl. Reip. Pop. Sin. 15: 94, 250. 1978.  Paris polyphylla Smith var. stenophylla Franch. f. latifolia (Wang & Tang) H. Li, Bull. Bot. Res. Harbin 6 (1): 125. 1986. Type: China, Shaanxi, Huayin, Xia WY 4426 (PE).

6.5 Section Euthyra Fig. 6.54 Paris luquanensis (drawn by M. Shen): whole plant (a) and dehisced capsule (b)

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Fig. 6.55 Whole plant (a), obverse (b) and reverse (c) side of leaves, flower (d), young fruit (e), and dehisced capsule (f) of Paris luquanensis

6.5 Section Euthyra

Paris polyphylla Smith var. panxiensis J. L. Liu, Acta Bot. Boreal. -Occident. Sin. 29 (8): 1697–1700. 2009. Type: China, Sichuan, Puge, 2600–2700 m, 01 Jul. 2005, Liu JL & Yang JM 4 935 (Holotype, XIAS). Perennial herb. Rhizome thickened, 9.0–18.0 cm  1.0–3.0 cm. Stem green or purple, erect, 25.0–75.0 cm tall, glabrous. Leaves 10–15 (occasionally 20), sessile or subsessile; leaf blade green, linear, narrowly lanceolate, lanceolate, oblanceolate, or oblong-lanceolate, membranous to papyraceous, apex acute or acuminate, base cuneate, 7.0–17.0 cm  0.4–2.0 cm. Flower solitary, basic number 4–7; pedicel green or purple, 5.0–25.0 cm long; sepals green, lanceolate, 2.0–7.0 cm long, yellowish green; petals filiform, usually longer than sepals. Stamens 2  petal number, 6.0–24.0 mm long; filaments green, 3.0–10.0 mm long; anthers yellow, 5.0–15.0 mm long; free portion of connective inconspicuous. Ovary unilocular with parietal placentation, purple, smooth or tuberculate, with 4–7 ridges; style purple, 0–2.0 mm, with an enlarged base; stigmas purple, 4.0–10.0 mm long, erect at flowering, revolute at fruiting. Capsule subglobose, green, irregularly dehiscent, 2.0–4.5 cm in diameter. Seeds numerous, wholly enveloped by red and juicy sarcotesta (Figs. 6.56 and 6.57). Phenology: flowering April–June, fruiting July–October. Habitats: evergreen (or deciduous) broad-leaved and coniferous forests, bamboo thickets, scrubs; ca. 1100–2300 m. Distribution: endemic to China: Anhui (Huoshan, Jinzhai), Chongqing (Chengkou, Nanchuan, Wulong, Wushan, Wuxi, Youyang), Fujian (Wuyishan), Gansu (Kangxian, Wudu), Guangxi (Longlin), Guizhou (Daozhen, Yinjiang), Henan (Lushi), Hubei (Hefeng, Jianshi, Shennongjia), Hunan (Pingjiang, Shimen, Suining), Jiangsu (Jurong), Jiangxi (Anfu, Shangrao, Xiushui), Shaanxi (Ansai, Baoji, Fengxian, Langao, Liuba, Nanzheng, Pingli, Taibai, Zhenping), Shanxi (Yicheng), Sichuan (Baoxing, Chongzhou, Dujiangyan, Ebian, Emeishan, Huili, Jinchuan, Kangding, Leibo, Leshan, Lixian, Luding, Mabian, Maoxian, Meigu, Mianning, Mianyang, Pingwu, Qingchuan, Shifang, Shimian, Tianquan, Wenchuan, Xiaojin, Yaan, Yuexi), Taiwan (Chiayi, Hsinchu, Hualien, Kaohsiung, Miaoli, Nantou, Pingtung, Taichung, Taidong, Taipei, Taoyuan, Yilan), Yunnan (Daguan, Songming, Zhaoyang), Zhejiang (Anji, Chun’an, Kaihua, Lin’an, Longquan, Suichang, Yongjia, Taishun). Notes: The taxonomic status of this species has been long in dispute. Molecular phylogenetic analyses showed that P. lancifolia is phylogenetically distinct from P. polyphylla (Ji et al. 2019, 2020), which provides support for recognizing it as a distinct species. Nevertheless, P. lancifolia as circumscribed here exhibits a high level of variation in leaf morphology, possessing linear, narrowly lanceolate, lanceolate, oblanceolate, and oblong-lanceolate leaves (Fig. 6.58).

171

This suggests that further investigation is needed to assess its taxonomic delimitation, and to construct infraspecific subdivisions. Additional specimens examined, CHINA, ANHUI, Huoshan: 25 Apr. 1983, Yao G & Deng MB 81547 (NAS). Jinzhai: 14 May 1984, Yao G 8944 (KUN). CHONGQING, Chengkou: 14 Sep. 2005, Chen YS, Wu ZH & Li B 3331 (WUK); loc. eodem, P. G. Farges s. n. (MNHN); loc. eodem, P. G. Farges 573 (P); loc. eodem, P. G. Farges 618 (P); loc. eodem, 02 May 1958, Dai TL 100578 (CDBI). Nanchuan: 12 Jun. 1935, Chu KL 1304 (CQNM); loc. eodem, 30 May. 1935, Chu KL 1002 (CQNM); loc. eodem, 16 May. 1980, Tan SX 802980 (IMC); loc. eodem, 29 May. 1981, Tan SX 815931 (IMC); loc. eodem, 07 Apr. 2013, Nanchuan Expedition 5001190601 (IMC); loc. eodem, 21 Aug. 1976, Liu ZY 762150 (IMC); loc. eodem, 21 Aug. 1976, Liu ZY 762151 (IMC); loc. eodem, 16 May. 1980, Liu ZY 802986 (IMC); loc. eodem, 16 May. 1980, Liu ZY 802985 (IMC); loc. eodem, 16 May. 1980, Liu ZY 802984 (IMC); loc. eodem, 14 May. 1986, Liu ZY 8325 (IMC); loc. eodem, 12 May. 1986, Liu ZY 8025 (IMC); loc. eodem, 29 Jul. 2006, Liu ZY 2067653 (IMC); loc. eodem, 27 May. 2005, Tan CM, Yi GH & Tan QP 05191 (JJF); loc. eodem, 29 Jul. 2006, Liu X 2067653 (IMC). Wulong: 25 Apr. 1998, Liu ZY 981098 (IMC). Wushan: 04 Jun. 1996, Chen ZD et al. 960953 (PE); loc. eodem,24 Apr. 1958, Yang GH 57824 (IBSC). Wuxi: 27 Jun. 1959, Li PY 2978 (WUK); loc. eodem, 11 Jul. 2004, Chen YS, Wu ZH & Li B s. n. (WUK); loc. eodem, 05 Jun. 2014, Zhang HY wx0128 (HWA); loc. eodem, 02 Jul. 1958, Yang GH 58945 (CDBI); loc. eodem, 02 Jun. 1962, Ni BZ ni00340 (CDBI); loc. eodem, 23 Jul. 1958, Yang GH 58945 (CDBI). Youyang: 22 Aug. 1984, Liu ZY 67580 (IMC). FUJIAN, Wuyishan: 04 Sep. 1980, Wuyi Expedition 1753 (FJSI); loc. eodem, 28 Aug. 1979, Wuyi Expedition 01035 (FJSI); loc. eodem, 27 Jun. 1984, Wang XQ 84102 (NAS); loc. eodem, 20 Jul. 1980, Wuyi Expedition 80-0154 (WUK); loc. eodem, 12 Aug. 1964, Jian CP, Ying JS & Ma C 400659 (PE). GANSU, Kangxian: 11 Aug. 1963, Zhang ZY 16555 (WUK). Wudu: 06 Sep. 1959, Zhang ZY 3502 (LBG); loc. eodem, 30 May. 1959, Zhang ZY 3068 (WUK); loc. eodem, 19 May. 1959, Xing JQ 2145 (WUK). GUANGXI, Longlin: 09 Apr. 1991, Wen HQ 00374 (IBK). GUIZHOU, Daozhen: 18 Apr. 2003, Liu ZY 2030771 (IMC); loc. eodem, 18 Apr. 2003, Liu ZY 2030774 (IMC); loc. eodem, 30 Apr. 2003, Liu ZY 2031086 (IMC); loc. eodem, 30 Apr. 2003, Liu ZY 2031095 (IMC); loc. eodem, 17 May. 2003, Liu ZY 2031336 (IMC); loc. eodem, 17 May. 2003, Liu ZY 2031373 (IMC); loc. eodem, 17 May. 2003, Liu ZY 2031376 (IMC); loc. eodem, 02 Aug. 2003, Liu ZY 2034433 (IMC). Yinjiang: 11 May. 1959, N Guizhou Expedition 744 (PE). HENAN, Lushi: 22 Aug. 1973, Fu KJ 17123 (WUK). HUBEI, Hefeng: 30 Apr. 1959, Peng FS 219 (WUK). Jianshi: 1951, Dai LY & Qian ZH 19 (PE).

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Fig. 6.56 Paris lancifolia (drawn by M. Shen): rhizome and stem (a), aerial shoot (b), and dehisced capsule (c)

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6.5 Section Euthyra

Fig. 6.57 Flower (a, b), pistil (c), transverse section of ovary (d), and dehisced capsule (e, f) of Paris lancifolia

173

174

Fig. 6.58 Variation in leaf shape in Paris lancifolia

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6.5 Section Euthyra

Shennongjia: 01 Sep. 1985, Liu ZY 40173 (PEM); loc. eodem, 17 Jun 2016, Xu XD & Li JR 2162180 (CCNU); loc. eodem, 10 Jun. 1985, Gong SM 0207 (JMSMC). Zhuxi: 05 May 2006, Gan QL 2111 (PE). HUNAN, Pingjiang: 14 Apr. 2013, Zhou JJ & Zhou D (CSFI). Shimen: 26 Jun. 1987, Hupingshan Expedition 0829 (PE). Suining: 14 Apr. 2013, Zhou JJ & Zhou D (CSFI). JIANGSU, Jurong: 09 Apr. 1933, Teng 367 (PE). JIANGXI, Anfu: 02 Oct. 1954, 1654 Jiangxi Expedition 1654 (PE). Shangrao: 17 May. 2007, Tan CM & Liu YZ 07233 (JJF). Xiushui: 13 Aug. 1959, Xiong J 05994 (LBG). SHAANXI, Ansai: 22 Jul. 1959, Li PY 7704 (WUK). Baoji: 14 Aug. 2014, Liu QR et al. s. n. (BNU). Fengxian: 14 Jun. 1977, Fu KJ 17500 (WUK); loc. eodem, 13 Jun. 1977, Fu KJ 17406 (WUK). Langao: 11 Oct. 2004, Chen YS, Wu ZH & Li B s. n. (WUK); loc. eodem, 18 Jul. 1970, Shaanxi Chinese Medicinal Herbs Survey 1670 (WUK); loc. eodem, 29 Jun. 2004, Chen YS, Wu ZH & Li B 525 (WUK); loc. eodem, 11 Jun. 2005, Chen YS, Wu ZH & Li B 2394 (WUK); loc. eodem, 10 Jun. 2005, Chen YS, Wu ZH & Li B et al. 2348 (WUK). Liuba: 03 Sep. 1977, Hu ZX & Guo YH 703 (WUK). Nanzheng: 19 Oct. 2005, Chen YS, Wu ZH & Li B 3990 (WUK). Pingli: 31 May. 1959, Li PY 2650 (WUK); loc. eodem, 07 Jul. 2004, Chen YS, Wu ZH & Li B 1056 (WUK). Taibai: 06 Jun. 1975, Hu ZX & Guo YH 565 (WUK). Zhenping: 23 May. 1966, Shaanxi Vegetation Survey 80 (WUK). SHANXI, Yicheng: 07 Jun. 1960, Liu XY 20371 (PE). SICHUAN, Baoxing: 11 Jun. 1933, Yu TT 1971 (CQNM); loc. eodem, 01 May. 1958, Sichuan Agricultural College 4838 (CDBI); loc. eodem, 18 Jul. 1936, Chu KL 3188 (IBSC); loc. eodem, 10 Sep. 1963, Guan KJ & Wang WC 3062 (PE); loc. eodem, 1936, Chu KL s. n. (PE); loc. eodem, 10 Sep. 1963, Guan KJ & Wang WC 3057 (PE); loc. eodem, 10 Sep. 1963, Guan KJ & Wang WC 3056 (PE); loc. eodem, 1954, Song ZP 38162A (PE); loc. eodem, 09 Oct. 1958, Zhang XS & Ren YX 07543 (PE). Chongzhou: 28 Jul. 2007, Feng Zb, Zhu DH & Li XJ 4373 (HX). Dujiangyan: 27 Aug. 2005, Zhu DH 3666 (HX); loc. eodem, 15 May. 1941, Wang FT 5115 (PE). Ebian: 16 May. 1932, Yu TT 761 (CQNM). Emeishan: loc. eodem, 15 May. 1982, Hekker F. s. n. (NHN); loc. eodem, 1952, Xiong JH, Zhang XB & Jiang XL 32666 (IBSC); loc. eodem, 02 Aug. 1952, Xiong JH, Zhang XB & Jiang XL 31892 (PE); loc. eodem, 23 Oct. 1938, Liu TN 12972 (PE); loc. eodem, 12 Sep. 1939, Sun XZ & Zhang G 1371 (PE); loc. eodem, 18 May. 1982, Quené-Boterenbrood & AJ s. n. (NHN); loc. eodem, 06 Jun. 1980, Wang LW & Zhang ZY 867 (PE); loc. eodem, 06 Oct. 1963, Tian JQ & Liu JJ 0016 (PE); loc. eodem, 1930, Tang T 000049 (PE); loc. eodem, 24 Jun. 1955, Sino-Soviet Expedition 2208 (PE); loc. eodem, 26 Jun. 1955, China-Soviet Expedition 2088 (PE); loc. eodem, 1935, Du DH 74 (CQNM). Huili: 23 Jul. 1984, Liang YF et al. 84-21 (PE). Jinchuan: 26 Apr. 1958, Li X 77243 (PE). Kangding:

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19 Jun. 1953, Jiang XL 36033 (PE). Leibo: 02 Apr. 1964, Yin KP & Chen QH 0069 (CDBI); loc. eodem, 15 May. 1983, Zhao QS & Shi JB 117115 (PE); loc. eodem, 08 Jun. 1983, Fang MY 117898 (PE); loc. eodem, 12 Jun. 1983, Zhao QS & Shi JB 117284 (PE). Leshan: 30 Apr. 2016, Hou YT, Guo CY & Hou CL 201605148 (QFNU); loc. eodem, 08 Sep. 1959, Guan ZT 6489 (PE). Lixian: 08 Oct. 1956, Li X 2450 (CDBI); loc. eodem, 28 Sep. 1956, Li X 46542 (CDBI). Luding: 01 Jun. 1983, Vegetation Survey 31088 (CDBI); loc. eodem, 02 May. 1980, Wang QQ 22032C (CDBI); loc. eodem, 02 Apr. 1984, Vegetation Survey 41735 (CDBI). Mabian: 27 May. 1931, Wang FZ 23000 (PE). Maoxian: 16 Jun. 1959, Maowen Expedition 2729 (CDBI). Meigu: 02 Jul. 1976, Sichuan Vegetation Survey 13505 (CDBI); loc. eodem, 02 Aug. 1959, Wild Plants Survey 5184 (CDBI). Mianning: 02 Jun. 1985, Li YJ 816 (CDBI). Mianyang: 13 Jul. 2005, D. E. Boufford et al. s. n. (GBIF). Pingwu: 21 Apr. 2014, Fu DZ, Chen SR & Shao YZ 1497 (PE). Qingchuan: 1930, Wang FT 22476 (PE). Shifang: 25 Jul. 2007, He XJ & Zhao QS 138367 (SZ). Shimian: 1955, Xie CJ 41031 (IBSC); loc. eodem, 1955, Xie CJ 39624 (IBSC). Tianquan: 19 Sep. 1953, Hu WG 37806 (IBSC); loc. eodem, 26 Apr. 1936, Qu GL 2427 (IBSC); loc. eodem, 28 Jun. 1951, Cui YW 4107 (PE); loc. eodem, 1936, Chu KL 2463 (PE); loc. eodem, 20 Oct. 1953, Jiang XL 37595 (PE); loc. eodem, 25 Apr. 1953, Jiang XL 33972 (PE); loc. eodem, 23 May 1986, Takeda Yoshiaki & Wang JT 0667 (PE). Wenchuan: 06 Jul. 1975, Sichuan Vegetation Survey 8201 (CDBI); loc. eodem, 19 Aug. 1982, Lang KY 1206 (PE). Xiaojin: 01 Aug. 1975, Sichuan Vegetation Survey 9794 (CDBI); loc. eodem, 06 Jun. 1959, Sichuan Economic Botany Expedition 203 (CDBI); loc. eodem, 18 Aug. 1975, Biological Institute 9794 (CDBI). Yaan: 12 Aug. 1961, Ying JS 10111 (PE). Yuexi: 03 Jul. 1959, Wild PlantS Survey 3594 (CDBI). TAIWAN, Chiayi: 12 Aug. 1989, Hu WH & Leu WP 258 (HAST); loc. eodem, 09 Jul. 1990, Jenn-Che Wang 6310 (HAST); loc. eodem, 02 Jul. 1989, Wang ZZ 5486 (HAST); loc. eodem, 18 Apr. 1996, Chen FC et al. 6508 (HAST); loc. eodem, 27 Mar. 2002, Chiu YT et al. 14580 (HAST); loc. eodem, 22 Mar. 1985, Huang SF 2616 (TAI); loc. eodem, 14 May. 2001, Naoki Naoki et al. 8 (HAST). Hsinchu: 17 Jul. 1935, Simada-Hidetaro 603 (TAI); loc. eodem, 05 May. 1995, Hsiao SC et al. 783 (HAST); loc. eodem, 15 Jul. 1935, Simada-Hidetaro 501 (TAI); loc. eodem, 20 Jun. 1973, Huang TC 6620 (TAI). Hualien: 02 Jun. 1993, Lü WB 1750 (HAST); loc. eodem, 23 Sep. 1984, Peng JY 7314 (HAST); loc. eodem, 11 Sep. 2001, Qi YZ & Huang YY 686 (HAST); loc. eodem, 19 Apr. 2003, Zhang HM, Chen FJ & Li ZW s. n. (HAST); loc. eodem, 21 Feb. 1994, Hsien-Tsung Hung & Lu YC 1365 (HAST); loc. eodem, 04 Jun. 2012, Zhang JW, Zhu XX & Deng T 5804 (HAST); loc. eodem, 19 Jul. 1994, Liu TY & Hsiao-Ying Shen 15 (HAST); loc. eodem, 13 Jun. 1997,

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Chun-Ching Chen, Ichiro Fukuda & Tsui-Ya Liu 1281 (HAST); loc. eodem, 14 Oct. 1992, Huang SF & T. H. Hsieh 4892 (TAI); loc. eodem, 10 Jul. 1937, Suzuki-Tokio, Fukuyama-Noriaki & Simada-Hidetaro 17679 (TAI); loc. eodem, 10 Aug 1956, Liu, Chen & Kao 158 (TAI); loc. eodem, 08 Aug 1956, Liu, Chen & Kao 9 (TAI); loc. eodem, T. Shimizu 12482 (TAI); loc. eodem, 27 Jul. 1936, Fukuyama & Suzuki-Tokio 16141 (TAI); loc. eodem, 07 Oct. 1983, W. S. Tang 88 (TAI); loc. eodem, 24 May. 1993, Huang SF & Yang KC & Hu MJ 5136 (TAI); loc. eodem, 25 Jul. 1986, Huang TC, Huang SF & Yang KC 12941 (TAI); loc. eodem, 14 May. 1965, Chao JM & Gao MT 6211 (TAI). Kaohsiung: 11 May. 1994, Wei-Hsin Hu et al. 477 (HAST). Miaoli: 05 May. 1999, Wu SH 1227 (HAST). Nantou: 04 Sep. 1998, Yang ZY 11193 (HAST); loc. eodem, 04 Jul. 1985, Peng JY 8167 (HAST); loc. eodem, 14 Oct. 1992, Liao CC et al. 25 (HAST); loc. eodem, 03 May. 1968, Cai HY & Wang CM 3155 (HAST); loc. eodem, 12 Jul. 1993, Yang KC, Huang SF & T. H. Hsieh s. n. (TAI); loc. eodem, 08 Jul. 1993, Huang SF, Yang KC & T. H. Hsieh 5316 (TAI); loc. eodem, 16 May. 1968, Gao MT 7242 (TAI); loc. eodem, 06 Sep. 1983. H. Ohashi & T. Nemoto 17176 (TAI); loc. eodem, 08 Aug. 1940, Nakamura Taisho 4551 (TAI); loc. eodem, 16 Oct. 1981, Huang TC 8517 (TAI); loc. eodem, 05 May. 1984, Tang WS 457 (TAI); loc. eodem, 17 Nov. 1984, Tang WS 874 (TAI); loc. eodem, 13 Aug. 1964, Gao MT 5874 (TAI). Pingtung: 30 Mar. 1987, Peng JY 10621 (HAST). Taichung: 03 Jul. 1999, Huang CY 465 (HAST); loc. eodem, 11 Sep. 1991, Leu WP, Liu SM & Hsu DS829 (HAST); loc. eodem, 06 Sep. 1983, Huang TC & Huang SF 9837 (TAI); loc. eodem, 05 Jul. 1986, Wang JC & Huang SF 3677 (TAI). Taidong: 10 Oct. 1937, Yoshimatsu Yamamoto & K. Mori 547 (TAI); loc. eodem, 23 Nov. 1987, Chen ZH 723 (HAST); loc. eodem, 24 Jul, 1988, Chen YK, Shen CH & Yang CK 1677 (HAST). Taipei: 05 Sep. 1934, Suzuki-Tokio 11722 (TAI); loc. eodem, 09 Sep. 1934, Suzuki-Tokio 11748 (TAI). Taoyuan: 09 Jun. 2000, Luo YT, Lu CC & Liu SC 467 (HAST); loc. eodem, 10 Apr. 2002, Wu SC 2617 (HAST); loc. eodem, 14 Apr. 1986, LIang NL et al. 2919 (HAST); loc. eodem, 10 Apr. 2002, Huang YY et al. 2843 (HAST); loc. eodem, 31 May. 1995, C. F. Hsieh et al. 6269 (HAST); loc. eodem, 10 Apr. 2002, Wu sSC et al. 2617 (TAI). Yilan: 04 Jun. 1995, Hsien-Tsung Hung et al. 1014 (HAST); loc. eodem, 08 Jun. 1985, Peng CY 877 (HAST); loc. eodem, 08 Jun. 2000, Chen JZ, et al. 395 (HAST); loc. eodem, 13 Aug. 2003, Cui ZX & Liang HZ s. n. (HAST); loc. eodem, 14 Jul. 1937, Simada-Hidetaro 1332 (TAI); loc. eodem, 03 Apr. 1986, Huang TC et al. 10804 (TAI); loc. eodem, 28 Aug. 1962, Chuang, Chao & Kao 4819 (TAI); loc. eodem, 14 Jul. 1937, Simada-Hidetaro 1332 (TAI); loc. eodem, 29 Jun. 1938, Ko s. n. (TAI); loc. eodem, 07 Aug. 1928, S. Suzuki s. n. (TAI); loc. eodem, 26 Mar. 1930, S. Suzuki s. n. (TAI); loc. eodem, 23 Aug. 1970, Chang-

6 Taxonomic Revision

Sheng Kuoh 1833 (TAI); loc. eodem, 09 May. 1972, Hsu SS 14071 (TAI); loc. eodem, 26 Aug. 1962, Chuang CC, Chao JM & Gao MT 4764 (TAI); loc. eodem, 25 Aug. 1962, Chuang CC, Chao JM & Gao MT 4764 (TAI); loc. eodem, 20 Aug. 1969, Chien-Chang Hsu 5849 (TAI); loc. eodem, 13 Oct. 1977, Jeng YC 1950 (TAI); loc. eodem, 14 Jul. 1937, Simada-Hidetaro 1332 (TAI); loc. eodem, 06 Nov. 1972, Gao MT 8594 (TAI); loc. eodem, 10 May. 2002, Liang HZ, Huang YY & Huang CY 794 (HAST). YUNNAN, Daguan: 17 May 2016, Li H, Wang QL, Zeng YJ et al. 023 (KUN). Songming: 14 Nov. 1957, Qiu BY 55397 (IBSC). Zhaoyang: 16 May 2016, Li H, Wang QL, Zeng YJ et al. 011 (KUN). ZHEJIANG, Anji: 03 May. 1987, Xu 0305 (ZMNH). Chun’an: 23 Oct. 1981, Hong L 1444 (HHBG). Kaihua: 1963, Wang JX 2135 (PE). Lin’an: 11 Jul. 1957, He XY 24558 (HHBG); loc. eodem, 20 May. 1957, Deng MB 4010 (PE); loc. eodem, 29 May. 2015, Internship Groupv TM008 (ZJU). Longquan: 08 Jul. 1987, Zhang et al. 5469 (ZM). Suichang: 20 Apr. 1991, Zhang & Xu 987 (ZM). Yongjia: 20 May. 1957, Deng, Huang & Yuan 4010 (HHBG). Taishun: 08 Jun. 1959, Zhang SY 5632 (PE). 23. Paris yanchii H. Li, L. G. Lei, & Y. M. Yang, J. West China For. Sci. 46 (1): 1–5. 2017. Type: China, Yunnan, Yunlong, 2500 m, 23 Apr. 2016, Wang YH et al. 009 (Holotype, KUN). Paris caojianensis B. Z. Duan & Y. Y. Liu, Phytotaxa 326 (4): 297–300. 2017. Type: China, Yunnan, Yunlong, 25 400 1800 N, 99 80 1900 E, 2160 m, 11 Aug. 2016, Duan BZ & Liu YY 055 (Holotype, DLU). Perennial herb, erect, glabrous. Rhizome thick, dark brown outside, white and starchy inside, ca. 2.5–8.5  0.2–4.5 cm. Stem erect, green or purple, 12.5–40.0 cm tall. Leaves 5–9, in a terminal whorl; petioles dark purple, 2.0–8.0  1.0–2 mm; leaf blades ovate to oblong, 4.0–9.5  1.5–3.5 cm, base attenuate to petiole, or cuneate to round, apex acuminate. Flower solitary and terminal; pedicel green or purple, ca. 3.5–5.0 cm  2.0–3.0 mm, elongates to 7.0–10.0 cm  3.0–4.0 mm in fruiting time; sepals 4–6, green adaxially, pale green abaxially, ovate to lanceolate, ca. 1.80–5.5 cm  0.5–1.9 cm, base round, apex long acuminate; petals linear, purple, but become green in fruiting time; stamens 2  petal number, 1.5–2.2 cm; filaments yellowish-green, 2.0–3.0 mm; anthers 5.0–10.0 mm, yellow; free portions of connectives linear, purple, 4.0–15.0 mm. Ovary ovoid, green, with 4–7 purple longitudinal ridges, ca. 2.5–4.0 mm  2.0–4.0 mm, unilocular with parietal placentation, anatropous ovules many, obovate, white; style purple, with an enlarged base; stigmas 4–7, purple, erect, 3.0–5.0 mm. Capsule globose with 5–6 longitudinal ridges, yellowish green, 2.0–4.0 cm in diameter, irregularly dehiscing. Seeds subglobose, ca. 3.0 mm in diameter, wholly enveloped by red and juicy sarcotesta (Figs. 6.59, 6.60 and 6.61).

6.5 Section Euthyra

Fig. 6.59 Paris yanchii (drawn by M. Shen)

177

178 Fig. 6.60 Aerial shoot (a, b, c), flowers (d, e, f) showing length variation in free portion of connective, dehisced capsule (g), and seeds (h) of Paris yanchii

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6.5 Section Euthyra

179

Fig. 6.61 Pistil (a) of Paris yanchii, with longitudinal (b) and transverse (c) section of ovary showing the parietal placentation

Phenology: flowering April–June, fruiting July–October. Habitats: deciduous broad-leaved and coniferous forests; ca. 2300–2800 m. Distribution: endemic to China: Yunnan (Yunlong). Additional specimens examined. CHINA, YUNNAN, Yunlong: 2500 m, 19 Aug. 2016, Li H & Liu YC 029 (KUN); loc. eodem, 2500 m, 01 Sep. 2016, Li H, Lei LG, & Liu YC 030 (KUN); loc. eodem, 2500 m, 01 Sep. 2016, Li H, Lei LG, & Liu YC 031 (KUN); loc. eodem, 2500 m, 01 Sep. 2016, Li H, Lei LG, & Liu YC 032 (KUN). 24. Paris marmorata Stearn, Bull. Brit. Mus. Bot. 2: 79. 1956; Hara, Fl. East. Himal. 410. 1966; H. Li, Act. Bot. Yunnan. 6 (4): 357. 1984; H. Li, Bull. Bot. Res. Harbin 6 (1): 130. 1986; H. Li, The Genus Paris (Trilliaceae) 44. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 92. 2000.  Paris polyphylla Smith subsp. marmorata (Stearn) Hara, Journ. Fac. Sci. Univ. Tokyo, Sect. 3, 10 (10): 151, 174, 176. 1969. Type: Bhutan, Drugyel Dzong, 27 300 N, 89 190 E, 2850 m, May 1949, Ludlow, Sheriff & Hicks 16213 (Holotype, BM). Perennial herb. Rhizome thick, ca. 2.5–8.5 cm  0.5–2.0cm. Stem green or purple, erect, 5.0–35.0 cm tall. Leaves 4–8, sessile to subsessile; leaf blade oblong or lanceolate, adaxially green with white markings along veins, abaxially purple-red, glabrous, apex acuminate, base cuneate, wide cuneate or subrounded, leaf margin irregular or undulate– dentation, ca. 4.4–8.5 cm  1.1–2.2 cm. Flower solitary, basic merosity 4–7; pedicel green or purple, 3.0–10.0 cm long; sepals green, lanceolate or narrowly ovate-lanceolate, ca. 2.0–3.2 cm  5.0–10.0 mm; petals linear or filiform, greenish yellow, 1.5–3.5 cm, shorter or slight longer than sepals. Stamens 2  petal number, arranged in 2 whorls, 4.0–8.0 mm long; filaments green or purple, 2.0–5.0 mm

long; anthers yellow (occasionally purple), 2.0–5.0 mm long; free portion of connective inconspicuous. Ovary green, subglobose with 4–7 ridges, unilocular with parietal placentation; style conical, purple, 1.0–3.0 mm; stigmas 4–7, purple, short, 1.0–2.0 mm long. Capsule globose, with 4–7 ridges, 1–3 cm in diameter, irregularly dehiscing at maturity. Seeds subglobose, 3.0–4.0 mm in diameter, enveloped by red and juicy sarcotesta (Figs. 6.62, 6.63 and 6.64). Phenology: flowering April–May, fruiting June–October. Habitats: deciduous broad-leaved and coniferous forests, bamboo thickets, and scrubs; ca. 1500–3100 m. Distribution: China: Sichuan (Miyi, Yanbian, Yanyuan), Tibet (Dinggye, Lhozhag), Yunnan (Dali, Dayao, Gongshan, Lanping, Lijiang, Lushui, Yulong). Nepal (Province No. 1, Mechi). Additional specimens examined. CHINA, SICHUAN, Miyi: 3000 m, 08 Jul. 1983, Qinghai-Tibet Expedition 11870 (KUN). Yanbian: 2800 m, 27 Apr. 2003, Gao XF, Peng YL & Zhao HL 4498 (CDBI); loc. eodem, 2800 m, 28 Apr. 2003, Gao XF, Peng YL & Zhao HL 4539 (CDBI); loc. eodem, 2700 m, 26 Jun. 1983, Qinghai-Tibet Expedition 11574 (KUN). Yanyuan: 2700 m, 26 Jun. 1983, QinghaiTibet Expedition 11574 (KUN). TIBET, Dinggye: 07 Jun. 1975, Qinghai-Tibet Expedition 5618 (PE). Lhozhag: 17 Aug. 2013, Chen YS et al. 13-1442 (PE). YUNNAN, Dali: 2910 m, 04 May 1988, Guo HJ 1406 (KUN). Dayao: 3050 m, 07 Jun. 1989, Chen Y & Bai B 379 (KUN). Gongshan: 13 Apr. 2015, Jin XH 15223 (PE); loc. eodem, 27 520 3500 N, 98 200 700 E, 1490 m, 02 Jun. 2015, Li H et al. 159-2 (KUN). Lanping: 26 570 3800 N, 99 140 1200 E, 2130 m, 27 May 2015, Li H et al. 124-2 (KUN). Lijiang: 3300 m, 22 Apr. 1985, Hengduanshan Natural Botanical Garden 85-035 (KUN). Lushui: 25 540 4500 N, 99 010

180

Fig. 6.62 Paris marmorata (drawn by M. Shen). Rhizome and stem (a) and aerial shoot (b)

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6.5 Section Euthyra

Fig. 6.63 Aerial shoot (a), flower (b), leaf shape variation (c), and leaf morphology of Paris marmorata (photographed by Y. Ji)

181

182

6 Taxonomic Revision

Fig. 6.64 Paris marmorata (photographed by Y. Ji): pistil (a) and transverse section of ovary showing parietal placentation (b)

2100 E, 2450 m, 29 May 2015, Li H et al. 129-1 (KUN). Yulong: 13 May 2012, Yulong Expedition 5307210027 (IMDY). NEPAL, PROVINCE NO. 1, Khumbu Pasanglhamu: 27 410 3300 N, 86 430 4200 E, 2830 m, First Darwin Nepal Fieldwork Training Expedition 9 (E). MECHI: 02 Oct. 2007, Shrestha et al. 345 (E); loc. eodem, 27 40 1600 N, 88 270 0000 E, 2845 m,16 Jun. 2007, Adhikari et al. 123 (E). 25. Paris polyphylla Smith, Cycl. 26: 2. 1813; Wallich, Icon. Pl. As. Rar. 2: 24, 126. 1831; Kunth, Enu. Pl. 5: 18. 1850; Hook. f., Ill. Himal. 24. 1855; Franch., Mem. Soc. Philom, Cent. (Paris) 24: 287. 1888; Hook. f., Fl. Brit. Ind. 6: 362; 1892; Hand.-Mazz., Symb. Sin. 7: 1215. 1936; Hara, Fl. East. Himal. 410. 1966; Hara, Journ. Fac. Sci. Univ. Tokyo, sect. 3, 10 (10): 175. 1969; Hara, Icon Cormoph. Sin. 5: 515. 1976; Wang et Tang, Fl. Reip. Pop. Sin. 15: 92, pl. 31, 1–3. 1978; T. S. Liu et S. S. Ying, Fl. Taiwan, 5: 68, pl. 1283. 1978; H. Li, Bull. Bot. Res. Harbin 6 (1): 116. 1986; H. Li, The Genus Paris (Trilliaceae) 33. 1998; Y. Liang et V. G. Soukup, Fl. Chin. 24: 90. 2000.  Daiswa polyphylla (Smith) Raf., Fl. Tellur. 4: 48. 1838; Takht., Brittonia 35 (3): 254. 1983; B. Mitchell, Plantsman 10 (3): 177. 1988.  Euthyra polyphylla (Smith) Salisb. Gen. Fl.: 16. 1866. Type: Nepal, Naraianhetty, Mar. 1803, F. Buchanan s. n. (Holotype, LINN; Isotype, BM, GH). Paris debeauxii Lévl., Mem. Pont. Acad. Rom. Nuov. Lincei 24: 21. 1906. Type: China, Guizhou, Guiding, 24 Sep. 1902, J. Cavalerie 533 (Holotype, E). Paris marchandii Levl. in Fedde., Repert. Spec. Nov. Regni Veg. 12: 533. 1913. Paris biondii Pamp, Nuovo Giorn. Bot. Ital. n. s. 17: 241. 1919. Type: China, Hubei, 1907, C. silvestri 211 (Holotype, FI). Paris polyphylla Smith var. alba H. Li & R. J. Mitchell, Bull. Bot. Res. Harbin 6 (1): 123. 1986. type: China, Yunnan,

Dali, 2000 m, 14 May 1984, Sino-Germany Expedition 403 (KUN). Perennial herb. Rhizome thick, ca. 5–11.0 cm  1.0–3.0 cm. Stem green or purple, erect, 25.0–80.0 cm tall, glabrous. Leaves 5–11; leaf blades green, oblong, obovate-oblong, or oblanceolate, membranous to papyraceous, apex acute or acuminated, base rounded or narrowly cuneate, 7.0–17.0 cm  1.0–2.5 cm; petiole 0.2–2.0 cm. Flower solitary, basic merosity 4–7; pedicel usually purple, 5.0–25.0 cm; sepals green, lanceolate, 2.5–6.0 cm long; petals linear or filiform, low portion yellowish-green, upper portion yellow, longer than sepals. Stamens 2  petal number, 9.0–25.0 mm long; filaments green, 3.0–7.0 mm long; anthers yellow, 5.0–10.0 mm long; free portion of connective inconspicuous. Ovary unilocular with parietal placentation, purple, smooth or tuberculate, with 4–7 longitudinal ridges; style purple or yellowish-white, 0–2.0 mm, with an enlarged base; stigmas purple (occasionally yellowish-white), 4.0–10.0 mm long, erect at flowering, revolute at fruiting. Capsule subglobose, greenish-yellow, irregularly dehiscing, 1.0–4.0 cm in diameter. Seeds numerous, ovoid, 2.0–5.0 mm in diameter, enveloped by red and juicy sarcotesta (Figs. 6.65, 6.66 and 6.67). Phenology: flowering April–June, fruiting July–October. Habitats: deciduous broad-leaved and coniferous forests, bamboo thickets, and scrubs; ca. 1100–2800 m. Distribution: China: Gansu (Dangchang, Huating, Huixian, Kangxian, Lanzhou, Pingliang, Tianshui, Wenxian, Wudu, Zhangxian, Zhouqu), Guizhou (Daozhen, Yinjiang), Qinghai (Xunhua), Shaanxi (Chang’an, Fengxian, Huangling, Huayin, Huxian, Huyi, Langao, Liuba, Longxian, Maiji, Meixian, Mianxian, Nanzheng, Ningshan, Pingli, Qingshui, Shiquan, Taibai, Weinan, Xunyang, Yaozhou, Zhashui, Zhen’an, Zhenba, Zhenping), Sichuan (Baoxing, Chongzhou, Dujiangyan, Emeishan, Jiuzhaigou, Kangding,

6.5 Section Euthyra

Fig. 6.65 Paris polyphylla (drawn by M. Shen). Rhizome and stem (a), aerial shoot (b), and dehisced capsule (c)

183

184 Fig. 6.66 Paris polyphylla (photographed by Y. Ji). Aerial shoot (a), flower (b), pistil (c), longitudinal (d) and transverse (e) section of ovary showing parietal placentation

6 Taxonomic Revision

6.5 Section Euthyra

185

Fig. 6.67 Young fruit (a), dehisced capsule (b), and seeds (c) of Paris polyphylla (photographed by Y. Ji)

Lixian, Luding, Maoxian, Pingwu, Shimian, Tianquan, Wenchuan, Xichang), Tibet (Nyingchi, Bome, Cona, Mainling, Nyalam, Yadong, Zayü), Yunnan (Dali, Fengqing, Fugong, Gongshan, Lanping, Lianghe, Lijiang, Lushui, Shangri-la, Shuifu, Songming, Tengchong, Weixi, Yangbi, Yongde). Nepal (Baglung, Banepa, Humla, Kalikot, Kaski, Manang, Myagdi, Panchthar, Parbat, Sankhuwasabha, Sindhupalchok, Solukhumbu, Syangja). India (Assam, Manipur, Meghalaya, Mizoram, West Bengal). Additional specimens examined. CHINA, GANSU, Dangchang: 29 Jul. 1951, Wang ZB 14613 (PE). Huating: 16 May 2014, He Y & Hao JC GSL2014050591 (BNU). Huixian: 10 Jul. 1997, D. L. 97063 (PE). Kangxian: 1450 m, 06 May 1963, He YQ 329 (KUN). Lanzhou: 11 May 1964, Lanzhou Expedition 64713 (LZU). Pingliang: 01 Aug. 1953, Zhong SQ & Yang PL 157 (PE). Tianshui: 26 Jul. 1951, Zhang ZW 135 (PE). Wenxian: 02 May 2007, Baishui River Collection Team 3842 (PE); loc. eodem, 14 Jul. 2006, Baishui River Collection Team 2038 (PE); loc. eodem, 04 Jul. 2006, Baishui River Collection Team 1029 (PE); loc. eodem, 14 May 2007, Baishui River Collection Team 4924 (PE); loc. eodem, 21 Apr. 2007, Baishui River Collection Team 3352 (PE). Wudu: 2300 m, 10 Jun. 1959, Zhang ZY 4149 (LBG). Zhangxian: 13 Jun. 1956, Huanghe River Expedition 4823 (PE). Zhouqu: 18 Jul. 1998, Baishui River Collection Team 341 (PE). GUIZHOU, Daozhen: 17 May 2003, Liu ZY 2031307 (IMC); loc. eodem, 17 May 2003, Liu ZY 2031376 (IMC); loc. eodem, 17 May 2003, Liu ZY 2031336 (IMC); loc. eodem, 16 Apr. 2003, Liu ZY 2035571 (IMC). Yinjiang: 11 May 1959, N Guizhou Expedition744 (PE). QINGHAI, Xunhua: 13 Aug. 1973, Zhang HZ 235 (HNWP); loc. eodem, 23 Sep. 1971, Guo BZ & Yang YC 9640 (HNWP); loc. eodem, 13 Jul. 1991, Zhou LH 3597 (HNWP). SHAANXI, Chang’an: 23 May 2011, Li SF et al. 15383 (XBGH). Fengxian: 13 Jun. 1977, Fu KJ

17406 (WUK). Huangling: 31 Jul. 1970, Shaanxi Chinese Medicinal Herbs Survey 891 (WUK). Huayin: 07 Jun. 1971, Qinling Baiyao Expedition 270 (WUK). Huxian: 20 Aug. 1951, Guo BZ 551 (PE). Huyi: 20 Jun. 2002, Song X et al. 0001043 (XJTU). Langao: 16 Jun. 1972, Qinling Baiyao Expedition 306 (WUK); loc. eodem, 19 Jul. 2008, Bashan Collection Team 1829 (PE). Liuba: 28 May 2010, Li SF et al. 13547 (XBGH); loc. eodem, 29 May 2010, Li SF et al. 13667 (XBGH). Longxian: 23 Aug. 1971, Qinling Baiyao Expedition 289 (WUK); loc. eodem, 18 Jul. 1970, Chinese Medicinal Herb Expedition, Longxian 1030 (WUK). Maiji: 26 Jul. 1951, Liu JM 10221 (PE); loc. eodem, 13 Aug. 1980, Loess Team 4918 (WUK); loc. eodem, 18 Jun. 1964, Fu KJ 15156 (WUK). Meixian: 19 Jul. 2013, Qingling Expedition Tb023 (BNU). Mianxian: 28 Jul. 2008, QL439 (BNU). Nanzheng: 17 Apr. 1973, Hou XX 288 (IBSC, WUK, FJSI). Ningshan: 24 Jul. 1933, Kung HW 3186 (PE); loc. eodem, 19 Jul. 2007, Jing KX QL019 (BNU). Pingli: 21 Oct. 1991, Ying JS et al. 842 (XJTU); loc. eodem, 23 Jun. 2005, Chen YS et al. 3059 (WUK); loc. eodem, 23 Jun. 2005, Chen YS et al. 2963 (WUK); loc. eodem, 05 Jul. 2004, Chen YS et al. 795 (WUK). Qingshui: 24 Jun. 1986, Yang JX 6885 (WUK). Shiquan: 28 May 1959, Xing JQ 2665 (WUK). Taibai: 14 Jun. 2011, Xue RQ et al. 02 (XJTU). Weinan: 07 Jul. 1952, Wang ZB 15656 (PE). Xunyang: 10 Jul. 1959, Xunyang Expedition 0802 (HNWP). Yaozhou: 11 Jun. 1983, Zhang ZY 19328 (XJTU); loc. eodem, 16 Jun. 1983, Zhang ZY 19453 (WUK). Zhashui: 23 May 2011, Li SF et al. 15329 (XBGH). Zhen’an: 09 Jun. 2008, Li SF et al. 10459 (XBGH). Zhenba: 06 Jun. 1970, Chinese Medicinal Herb Expedition 20 (WUK). Zhenping: 08 Jul. 2004, Chen YS et al. 1200 (WUK). SICHUAN, Baoxing: 10 Setp. 1963, Guan KJ & Wang WC 3062 (PE). Chongzhou: 04 Nov. 2015, Ju WB & Chen DK AZH00690 (CDBI). Dujiangyan: 27 Aug. 2005,

186

Zhu DH 3670 (HX). Emeishan: 09 Jun. 1933, Peng ZB 6099 (KUN). Jiuzhaigou: 28 Jul. 1984, Chen WL et al. 8642 (PE); loc. eodem, 25 Sep. 2008, Gao XF & Gu L 10354 (CDBI). Kangding: 1934, Liu ZS 1109 (PE); loc. eodem, 24 Setp. 1951, Hu WG & He Z 11300 (PE); loc. eodem, 22 Jul. 1963, Guan KJ & Wang WC 141 (PE). Lixian: loc. eodem, 08 Oct. 1956, Li X 46736 (PE). Luding: 02 Jul. 1982, Vegetation Survey 41897 (CDBI). Maoxian: 04 Aug. 2001, Gao XF & Peng YL 1332 (CDBI); loc. eodem, 18 Apr. 2002, Gao XF & Peng YL 2244 (CDBI). Pingwu:19 Jun. 2014, Zhang SR, Chen SR & Lang XA 2107 (PE). Shimian: 1955, Xie ZJ 41031 (PE). Tianquan: 24 May 1986, Wang JT & Yoshiaki takeda 0721 (PE); loc. eodem, 23 May 1986, Wang JT & Yoshiaki takeda 0667 (PE). Wenchuan: 23 Apr. 2008, He XJ & Zhao QS 128121 (SZ). Xichang: 25 Jun. 1932, Yu TT 1125 (PE). TIBET, Bayi: 05 Jun. 1966, Zhang JW & Wang JT 0233 (PE). Bome: 28 Jun. 1965, Ying JS & Hong DY 650363 (PE); loc. eodem, Ying JS & Hong DY 650539 (PE). Cona: 10 Sep. 2015, Zhou Z et al. ZJW-3919 (KUN). Mainling: 3500 m, 27 Jul. 1972, Tibet Chinese Medicinal Herbs Survey 4209 (PE, HNWP). Nyalam: 23 Aug. 1972, Tibet Chinese Medicinal Herbs Survey 1423 (PE). Yadong: 04 Jun. 1975, Qinghai-Tibet Complement 750199 (PE); loc. eodem, 23 Jul. 2011, Gao XF et al. 14302 (PE). Zayü: 09 May 1952, Zhong QB 6382 (PE); loc. eodem, 22 Aug. 2009, Jin XH et al. SET-ET 606 (PE); loc. eodem, 23 Aug. 2009, Jin XH et al. SET-ET 642 (PE). YUNNAN, Dali: loc. eodem, 30 May 1955, Wu ZY et al. 1431 (PE). Fengqing: 10 Jun. 1938, Yu TT 16209 (PE). Fugong: 3200 m, 09 Sep. 1934, Cai XT 58428 (PE). Gongshan: 07 Sep. 1940, Feng GM 8220 (PE). Lanping: 29 Jun. 1981, Hengduan Mountains Expedition 0896 (PE). Lianghe: 21 Oct. 1974, Tao GD 12926 (HITBC). Lijiang: 03 Aug. 1981, Hengduan Mountains Expedition 02449 (PE). Lushui: 06 Jun. 1981, Zhao KY 201 (IGA). Shangri-la: 30 Apr. 1937, Yu TT 1180 (PE); loc. eodem, 17 Aug. 1981, Hengduan Mountains Expedition 3189 (PE); loc. eodem, 01 Jun. 1981, Qinghai-Tibet Expedition 987 (CDBI). Shuifu: 08 Apr. 2002, Liu ZY 2020675 (KUN). Songming: 14 Nov. 1957, Qiu BY 55397 (PE). Tengchong: 2720 m, 18 May 1965, Wu SG 6632 (KUN). Weixi: Jun. 1935, Wang QW 63754 (NAS). Yangbi: 25 May 1963, NW Yunnan Jinshajiang Expedition 4063 (PE). Yongde: 2810 m, 15 Jul. 2002, Liu ED 5142 (KUN). NEPAL, Baglung: 28 250 N, 83 30 E, 2438 m, 30 Apr. 1954, J. D. A. Stainton, W. R. Sykes & L. H. J. Williams 342 (BM). Banepa: May 05, Wallich N. 3711 (K); loc. eodem, Wallich N. 3710 (K). Humla: 29 500 2800 N, 2743 m, 24 May 1952, O. V. Polunin, W. R. Sykes & L. H. J. Williams 4154 (BM). Kalikot: 29 210 2200 N, 81 450 3600 E, 2896 m, 19 Apr. 1952, O. V. Polunin, W. R. Sykes & L. H. J. Williams 788 (BM). Kaski: 28 220 4800 N, 83 460 1200 E, 04 Apr. 1975, C. David Sayers 2379 (BM); loc. eodem, 28 190 5800 N, 84 30 1100 E, 2438 m, 18 Apr. 1954,

6 Taxonomic Revision

J. D. A. Stainton, W. R. Sykes & L. H. J. Williams 4872 (BM); loc. eodem, 28 150 600 N, 83 580 900 E, 3353 m, 14 Sep. 1954, J. D. A. Stainton, W. R. Sykes & L. H. J. Williams 8605 (BM). Manang: 28 340 4800 N, 84 100 1200 E, 2438 m, 27 May 1950, Donald George Lowndes 900 (BM). Myagdi: 28 310 1200 N, 83 160 4600 E, 2743 m, 28 Apr. 1954, J. D. A. Stainton, W. R. Sykes & L. H. J. Williams 2591 (BM). Panchthar: 2300 m, 09 Apr. 1967, Dan Henry Nicolson 3198 (BM). Parbat: 28 220 3600 N, 83 460 2200 E, 2590 m, 11 Jul. 1983, H. Ohba et al. 8330293 (BM). Sankhuwasabha: 27 390 300 N, 87 110 3000 E, 3353 m, 06 Oct. 1975, Leonard W. Beer 25564 (BM). Sindhupalchok: 2438 m, 27 Apr. 1931, K. N. Shasma 248 (E). Solukhumbu: 27 310 200 N, 86 350 1000 E, 2590.5 m, 13 Apr. 1905, Lall Dhwoj 92 (BM); loc. eodem, 27 440 3500 N, 86 420 5000 E, 2600 m, 08 May 1952, Albert Zimme 449 (BM). Syangja: 28 180 N, 83 460 E, 2286 m, 21 May 1954, J. D. A. Stainton, W. R. Sykes & L. H. J. William 5356 (BM). INDIA, ASSAM: Simons s. n. (NHN). MANIPUR: Watt G. 6771 (NHN). MEGHALAYA: 08 Jan. 1959, Deka GK 18326 (NHN). MIZORAM: 21 Apr. 1953, Koelz WN (NHN). WEST BENGAL, Singalila: 05 May 1959, Chatterjee AC & Mittal Soest JL s. n. (NHN). 26. Paris mairei Lévl. in Fedde, Repert. Spec. Nov. Regni Veg. 11: 302. 1912; H. Li, Act. Bot. Yunnan 6 (4): 357. 1984; H. Li, Bull. Bot. Res. Harbin 6 (1): 127. 1986; H. Li, The Genus Paris (Trilliaceae) 42. 1998; S. Y. Liang et V. G. Soukup, Fl. Chin. 24: 91. 2000. Type: China, Yunnan, Dongchuan, 2700 m, Jun. 1910, Maire 7457 (Holotype, E). Paris violacea Lévl. in Fedde, Repert. Spec. Nov. Regni Veg. 11: 302. 1912.  Daiswa violacea (Lév.) Takht., Brittonia 35: 266. 1983. Type: China, Yunnan, 3200 m, Jun. 1910, Maire 7458 (Holotype, E). Paris polyphylla Smith var. pubescens Hand.-Mazz., Anz. Akad. Wiss. Wien, Math. -Naturwiss. Kl. 62: 145. 1925; Symb. Sin. 7: 1215. 1936; Hara., Journ. Fac. Sci. Univ. Tokyo, Sect. 3, 10 (10): 176. 1969.  Paris pubescens (Hand.-Mazz.) Wang et Tang, Fl. Reip. Pop. Sin. 15: 96. 1978.  Daiswa pubescens (Hand.-Mazz.) Takht., Brittonia 35: 268. 1983; B. Mitchell, Plantsman 10 (3): 179. 1988. Type: China, Sichuan, 22 Feb. 1914, Handel-Mazzetti 2489 (Isotype, E). Paris stigmatosa S.-D. Zhang, Novon 18: 551. 2008. Type: China, Yunnan, Qiaojia, 2600–2900 m, 07 Jul. 2004, Wang H et al. 03-1372 (Holotype, KUN; Isotype, MO, PE, YUKU). Perennial herb. Rhizome thick, 5.0–17.5 cm long, 1.0–3.5 cm in diameter, brown outside, white and starchy inside. Stem 11.0–65.0 cm, purple or green, rough or pubescent (occasionally glabrous). Leaves 5–12; leaf blades oblanceolate, obovate to obovate-lanceolate, ca. 4.0–14.0 cm  1.5–4.5 cm, green, usually pubescent; the second pair lateral veins arching from the middle of midvein;

6.5 Section Euthyra

petiole usually pubescent, purple, 0.5–4.5 cm in length. Flower solitary, basic merosity 4–8; pedicel purple (rarely green), 4.5–18.5 cm long, pubescent (occasionally glabrous); sepals green, lanceolate, ovate-lanceolate, ca. 2.5–8.0 cm  0.7–2.0 cm, pubescent (occasionally glabrous); petals filiform or linear, yellowish green, 2.5–10.5 cm long, longer than sepals. Stamens 2  petal number, 0.8–2.0 cm; filaments purple or yellow, shorter than anthers, 2.0–6.0 mm long; anthers yellow, 3.0–15.0 mm long. Ovary green or purple with ridges, pubescent (occasionally glabrous), unilocular with parietal placentation. style purple, 1.0–4.0 mm long, with an enlarged base; stigmas purple, erect at flowering, revolute at fruiting. Capsule subglobose with ridges, pubescent (occasionally glabrous), irregularly dehiscing at maturity. Seeds numerous, subglobose, enveloped by red and juicy sarcotesta (Figs. 6.68, 6.69, 6.70 and 6.71). Phenology: flowering April–May, fruiting June–October. Habitats: deciduous broad-leaved and coniferous forests, bamboo thickets, and scrubs; ca. 1800–3500 m. Distribution: endemic to China: Guizhou (Nayong, Weining, Xishui), Sichuan (Daocheng, Dayi, Huidong, Jiulong, Jiuzhaigou, Kangding, Luding, Muli, Xichang, Yanbian, Yanyuan), Tibet (Dinggye, Nyingchi), Yunnan (Binchuan, Dali, Dayao, Deqin, Eryuan, Fengqing, Fugong, Fuyuan, Gongshan, Heqing, Jingdong, Lanping Lijiang, Longyang, Lushui, Qiaojia, Shangri-la, Songming, Tengchong, Weining, Weixi, Wuding, Yangbi, Yiliang, Yunlong, Zhaoyang). Additional specimens examined. CHINA, GUIZHOU, Nayong: 03 Aug. 1959, Bijie Expedition 701 (PE). Weining: 27 Sep. 1998, Wang HC 0090 (KUN). Xishui: 20 May 2014, Gu C XS14053154 (ZY). SICHUAN, Daocheng: 3200 m, 01 Sep. 1981, Qinghai-Tibet Expedition 6033 (KUN, HITBC); loc. eodem, 3800 m, 28 Jun. 1973, Sichuan Vegetation Survey Dao2278 (KUN, CDBI); loc. eodem, 02 Jun. 1971, Liu ZG 0096 (CDBI); loc. eodem, 01 Sep. 1971, Liu ZG 707 (CDBI). Dayi: 06 Jun. 2007, Feng ZB et al. 20070643 (HX). Huidong: 22 Jun. 1959, Wu SG 1154 (KUN). Jiulong: 20 Jun. 1960, Guan ZT 31-0719 (PE); loc. eodem, 1960, Guan ZT C-135 (PE); loc. eodem, 02 Jun. 1960, Ying JS 3748 (PE); loc. eodem, 30 Apr. 1959, Wang BX & Li BW 07514 (PE); loc. eodem, 09 Junl 1960, Guan ZT 350347 (PE). Jiuzhaigou: 15 Jun. 1986, Wu ZY et al. 684 (KUN). Kangding: 3060 m, 23 Jan. 1961, Sino-Soviet Expedition 2948 (KUN). Luding: 02 Apr. 1982, Vegetation Survey 41724 (CDBI). Muli: 17 Oct. 1984, Liang YF et al. 84-83 (PE); loc. eodem, Oct. 1982, Sichuan Vegetation Survey 442 (CDBI); loc. eodem, 3400 m, 22 Aug. 1983, Qinghai-Tibet Expedition 14165 (KUN); loc. eodem, 3000 m, 22 May 1937, Yu DJ 5577 (KUN); loc. eodem, 05 Sep. 1937, Yu TT 14168 (PE); loc. eodem, 02 Oct. 1937, Yu TT 14411 (PE); loc. eodem, 22 May 1937, Yu TT 5577 (PE); loc. eodem, 27 May 1927, Yu TT 5784 (PE); loc. eodem, Yu TT 5447

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(PE); loc. eodem, 02 Jul. 1978, Zhao QS 6251 (CDBI); loc. eodem, 23 Aug. 1983, Qinghai-Tibet Expedition 13288 (KUN); loc. eodem, 02 Aug. 1978, Zhao WS & Yang YB 8291 (CDBI). Xichang: 09 Jun. 1985, Li YJ 790 (CDBI). Yanbian: 23 Apr. 2003, Gao XF, Peng YL & Zhao HL 4393 (CDBI). Yanyuan: 1963, Zhang QL 63025-1 (PE); loc. eodem, 05 May 1960, Jiang S et al. 5586 (PE). TIBET, Dinggye: 07 Jun. 1975, Qinghai-Tibet Expedition 5620 (PE); loc. eodem, 06 Jun. 1975, Qinghai-Tibet Expedition 5579 (PE). Nyingchi: 03 Aug. 1975, Qinghai-Tibet Suppliment 751158 (PE). YUNNAN, Binchuan: 2250 m, 03 Jul. 1987, Bao SY 128 (KUN); loc. eodem, 3000 m, 30 Oct. 1987, Li YH 457 (KUN); loc. eodem, 21 Oct. 1946, Liu SE 21978 (PE); loc. eodem, 21 Dec. 1946, Liu SE 22088 (PE); loc. eodem, 16 May 1964, Zhou X 1006 (KUN). Dali: 2900–3100 m, 29 Aug. 1984, K. Iwatsuki 1532 (KUN); loc. eodem, 08 Sep. 1982, Sino-Japan Expedition 1021 (KUN); loc. eodem, 3000 m, 20 Oct. 1987, Li YH 00342 (KUN); loc. eodem, 3000 m, 13 May 1973, Lü ZW 73-207 (KUN); loc. eodem, 3200 m, 09 May 1981, Yu SW 135 (KUN); loc. eodem, 2850 m, 17 May 1981, Sino-British Expedition to Cangshan 0662 (KUN); loc. eodem, 3350 m, 13 May 1981, Sino-British Expedition to Cangshan 0510 (KUN); loc. eodem, May 1935, Wang QW 63210 (PE); loc. eodem, May 1935, Wang QW 63810 (PE). Dayao: 2950 m, 07 Jun. 1989, Chen Y & Bai B 377 (KUN); loc. eodem, 2800 m, 30 May 1989, Chen Y & Bai B 183 (KUN). Deqin: 3550 m, 01 Jul. 1981, Qinghai-Tibet Expedition 2333 (KUN); loc. eodem, 06 Jul. 1981, Qinghai-Tibet Expedition 1869 (KUN). Eryuan: 23 Sep. 1975, Qiu BY 60978 (KUN). Fengqing: 10 Jun. 1938, Yu TT 16209 (PE). Fugong: 27 90 50.400 N, 98 460 55.300 E, 2500 m, 10 Aug. 2005, Li H et al. 26873 (KUN); loc. eodem, 27 100 37.500 N, 98 440 34.200 E, 2900 m, 15 Aug. 2005, Li H et al. 28293 (KUN); loc. eodem, 27 100 37.900 N, 98 450 17.600 E, 2800 m, 15 Aug. 2005, Li H et al. 28354 (KUN); loc. eodem, 24 Sep. 2014, Li H, Yang J & Wang YH NJ010-A-1 (KUN); loc. eodem, 27 080 8.700 N, 98 500 3000 E, 1610 m, 27 Apr. 2004, Li H et al. 19876 (KUN); loc. eodem, 27 100 45.400 N, 98 430 44.400 E, 2999 m, 04 May 2004, Li H et al. 20191 (KUN); loc. eodem, 1650 m, 30 Sep. 1997, Gaoligong Expedition 9751 (KUN); loc. eodem, 2800–2900 m, 28 May 1982, Qinghai-Tibet Expedition 6989 (KUN); loc. eodem, 28 May 1982, Qinghai-Tibet Expedition 6984 (KUN). Fuyuan: 2500 m, 17 Jun. 1989, Honghe River Expedition 2217 (KUN). Gongshan: 27 Sep. 2007, Dian ZL & Chen Z DZL-022 (KUN); loc. eodem, 24 Sep. 2014, Li H, Yang J & Wang YH NJ-010-8 (KUN); loc. eodem, 21 Sep. 1997, Gaoligong Expedition 9612 (KUN); loc. eodem, 27 470 6.600 N, 98 280 42.000 E, 2500 m, 26 Jul. 2002, Li H, Li R & Diao ZL 15353 (KUN); loc. eodem, 27 470 39.400 N, 98 350 12.900 E, 2020 m, 20 Apr. 2002, Li H, Ji YH & Li R 14555 (KUN); loc. eodem, 27 470 5500 N, 98 350 19.600 E, 1790 m, 18 Aug.

188

Fig. 6.68 Aerial shoot (a), leaf morphology (b), and dehisced capsule (c) of Paris mairei (drawn by M. Shen)

6 Taxonomic Revision

6.5 Section Euthyra

189

Fig. 6.69 Aerial shoot of Paris mairei (a): petiole, pedicel, and margin of leaf blade papillose-pubescent (b); stem papillose-pubescent (c); leaf blade adaxially tinged with pale-green along the veins (d), abaxially pubescent (e, f)

190

Fig. 6.70 Flower and young fruit of Paris mairei (photographed by Y. Ji). Stamens 2  petal number (a); sepals oblong-lanceolate (b); adaxially smooth (c); abaxially pubescent (d); pistil pubescent (e);

6 Taxonomic Revision

longitudinal (f) and transverse section (g) of ovary showing parietal placentation; fruit densely pubescent (h)

6.5 Section Euthyra

Fig. 6.71 Dehisced capsule of Paris mairei

2006, Li H et al. 33620 (KUN); loc. eodem, 27 470 22.400 N, 98 310 45.600 E, 3010 m, 21 Aug. 2006, Li H et al. 33770 (KUN); loc. eodem, 28 40 000 N, 98 350 2000 E, 1500 m, 11 Nov. 2004, Li H et al. 22436 (KUN); loc. eodem, 27 480 4700 N, 98 300 1800 E, 3000 m, 29 Sep. 2002, Li H et al. 16715 (KUN); loc. eodem, 1990 m, 17 May 2001, Li H et al. 13859 (KUN); loc. eodem, 27 590 2.300 N, 98 390 41.600 E, 1560 m, 16 Apr. 2002, Li H, Ji YH & Li R 14409 (KUN); loc. eodem, 27 480 800 N, 98 300 30.500 E, 3120 m, 04 Oct. 2002, Li H et al. 16980 (KUN); loc. eodem, 28 30 16.400 N, 98 350 48.900 E, 1560 m, 11 Nov. 2004, Li H et al. 22448 (KUN); loc. eodem, 27 480 4700 N, 98 300 1800 E, 3000 m, 29 Sep. 2002, Li H et al. 16714 (KUN); loc. eodem, 28 00 17.100 N, 98 300 48.100 E, 2830 m, 01 Sep. 2006, Li H et al. 31721 (KUN). Heqing: 3000 m, 21 Sep. 1988, Li YH 2033 (KUN); loc. eodem, 2800 m, 30 Sep. 1958, Wang WC Dali317 (KUN); loc. eodem, 22 Aug. 1940, Qin RC 23887 (PE). Jingdong: 2650 m, 28 Jun. 1993, Peng H & Bai B 755 (KUN); loc. eodem, 17 Jul. 2003, Yang GP 21 (HITBC). Lanping: 26 570 38.400 N, 99 140 12.500 E, 2095 m, 20 Apr. 2016, Wang YH et al. 002 (KUN). Lijiang: 03 May 1985, Zhou X et al. 85-140 (KUN); loc. eodem, 28 May 1962, Zhang AL 100302 (KUN); loc. eodem, 24 May 1962, Zhang AL 100281 (KUN); loc. eodem, Yun A 5 (KUN); loc. eodem, Jul. 1935, Wang QW 70971 (PE); loc. eodem, 3250 m, 24 May 1985, Lin Q 771113 (KUN); loc. eodem, 3000–3150 m, 02 Oct. 1987, K. Iwatsuki 995 (KUN); loc. eodem, 3075 m, 26 May 1988, Pei SJ 1542 (KUN); loc. eodem, 3100 m, 11 Oct. 1987, Pei SJ 089 (KUN); loc. eodem, 3200 m, 23 May 1985, Sino-British Expedition 85-32 (KUN); loc. eodem, 2700–2800 m, 05 Jun. 1981, Qinghai-Tibet Expedition 367 (KUN); loc. eodem, 3000 m, 25 May 1985, Lin Q, Yu HY & Sun H 771148 (KUN); loc. eodem, 3250 m, 26 May 1985, Sino-British Expedition 85-230 (KUN); loc. eodem, 3120 m, 07 Sep. 1963, Bao CZ 63-20430 (KUN); loc. eodem, 2700 m, 09 Oct. 1960, Yu SW & Lü CZ 25031 (KUN); loc. eodem, 3000 m, 02 Sep. 1958, Wang WC Dali88 (KUN); loc. eodem, 3200 m, 14 Sep. 1955, Feng GM 21527 (KUN, PE); loc. eodem, 30 May 1997,

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Hong DY et al. H97096 (KUN); loc. eodem, 05 Jun. 1981, Qinghai-Tibet Expedition 367 (KUN, HITBC). Longyang: 2200 m, 08 May 1997, Diao ZL & Cui JY 9444 (KUN). Lushui: 29 May 2015, Li H et al. 131-3 (KUN); loc. eodem, 26 50 5200 N, 98 350 1600 E, 13 May 2005, Li H et al. 22851 (KUN); loc. eodem, 26 30 000 N, 98 390 3400 E, 2360 m, 15 May 2005, Li H et al. 22974 (KUN); loc. eodem, 26 10 4800 N, 98 380 4100 E, 2100 m, 19 May 2005, Li H et al. 23446 (KUN); loc. eodem, 25 580 3600 N, 98 430 5.300 E, 2720 m, 19 May 2005, Li H et al. 24474 (KUN); loc. eodem, 25 590 1600 N, 98 420 2300 E, 2737 m, 18 May 2005, Li H et al. 24433 (KUN); loc. eodem, 2800 m, 05 Oct. 1997, Gaoligong Expedition 10040 (KUN); loc. eodem, 26 20 5500 N, 98 360 5100 E, 2160 m, 13 May 2005, Li H et al. 22848 (KUN); loc. eodem, 26 430 900 N, 98 360 2700 E, 1859 m, 14 May 2005, Li H et al. 24125 (KUN). Qiaojia: 2900 m, 28 May 2005, Zhang SD & Lin NN 03-1803 (KUN). Shangri-la: 24 May 2000, Zhou ZK et al. 24 (KUN); loc. eodem, 17 Jul. 2014, Guo YJ et al. 14CS8297 (KUN); loc. eodem, 06 Aug. 1976, Wu ZY 4158 (KUN); loc. eodem, 23 Jun. 1963, Zhongdian Expedition 63-2644 (KUN); loc. eodem, 29 Aug. 1962, Zhongdian Expedition 1649 (PE, KUN); loc. eodem, 14 Sep. 1939, Feng KM 2379 (PE); loc. eodem, 22 May 1939, Feng KM 949 (PE); loc. eodem, 26 Sep. 1937, Yu TT 13445 (PE); loc. eodem, 3300–3400 m,16 Aug. 1962, Zhongdian Expedition 937 (KUN, PE). Songming: 12 Oct. 1953, Feng GM 50388 (IBSC). Tengchong: 25 470 39.800 N, 98 370 18.500 E, 2650 m,14 May 2006, Li H et al. 29296 (KUN); loc. eodem, 25 460 39.700 N, 98 420 30.100 E, 2390 m, 14 May 2006, Li H et al. 30233 (KUN); loc. eodem, 25 160 8.800 N, 98 420 2600 E, 2500 m, 14 May 2006, Li H et al. 29041 (KUN); loc. eodem, 25 270 20.600 N, 98 440 21.600 E, 2520 m, 14 May 2006, Li H et al. 29433 (KUN). Weining: 2250 m, 27 Sep. 1998, Wang HC 0090 (KUN). Weixi: 2500–2700 m, 26 May 1940, Feng GM 1471 (KUN); loc. eodem, Aug. 1935, Wang QW 68215 (PE). Wuding: 13 May 1982, Li H, Xu X & Yu HY 820 (HITBC). Yangbi: 25 430 N , 100 020 E, 2600–2800 m, 16 Jun. 1984, Sino-US Expedition to Yunnan 135 (KUN); loc. eodem, 2700 m, 25 Feb. 1963, Northwest Yunnan Team 4063 (KUN); loc. eodem, 3000 m, 05 May 1981, Sino-British Expedition to Cangshan 0222 (KUN); loc. eodem, 2900 m, 05 May 1981, Sino-British Expedition to Cangshan 0217 (KUN); loc. eodem, 2450 m, 02 May 1981, Sino-British Expedition to Cangshan 0050 (KUN); loc. eodem, 25 May 1963, N Yunnan Jinshajiang Expedition 4063 (PE); loc. eodem, 19 May 1982, Tong SQ 32819(KUN). Yiliang: 16 Jun. 1982, Li H, Chen Y & Fei Y 1314 (HITBC); loc. eodem, 1900 m, 17 Jun. 1982, Li H 1320 (KUN); loc. eodem, 1850 m, 16 Jun. 1982, Li H 1314 (KUN). Yunlong: 2500 m, 01 Sep. 2016, Li H, Lei LG & Liu YC 035

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(KUN). Zhaoyang: 1860 m, 16 May 2016, Li H et al. 013 (KUN). Acknowledgement The description, phenology, habitats, distribution, and specimens of Paris liiana in this chapter were modified from the paper published by our group in Frontiers in Plant Science (Ji et al. 2020; 11:411. doi: 10.3389/fpls.2020.00411). The related contents are re-used with the permission.

References Bieberstein M (1808) Flora Taurico-Caucasica, vol 1. Typis Academicis, Charkouiae Bieberstein M (1819) Flora Taurico-Caucasica, vol 3. Typis Academicis, Charkouiae Franchet A (1888a) Monographie du genere Paris. Gauthiers-Villars, Paris Franchet A (1888b) Monographie du genre Paris. Mémoires Publiés par la Société Philomathique 24:267–291 Handel-Mazzetti H (1925) Anzeiger der Akademie der Wissenschaften in Wien. Mathematische-naturwissenschaftliche Klasse. Vienna 62:145–149 Handel-Mazzetti H (1936) Symbolae Sinicae. J. Springer, Wien Hara H (1969) Variations in Paris polyphylla Smith with reference to other Asiatic species. J Fac Sci Univ Tokyo Sect 3(10):141–180 He SZ (1990) A new medicinal species of Paris from Guizhou province, China. Guizhou Sci 3:16 Huang TC, Yang KC (1988) Notes on the Flora of Taiwan (1) - The Daiswa (Trilliaceae) of Taiwan. Taiwania 33:122 Ji YH, Fritsch PW, Li H, Xiao TJ, Zhou ZK (2006a) Phylogeny and classification of Paris (Melanthiaceae) inferred from DNA sequence data. Ann Bot 98:245–256. https://doi.org/10.1046/j.1365-2885. 2002.00426.x Ji YH, Zhou ZK, Li H (2006b) Paris xichouensis, a new combination of Trilliaceae from China. Acta Phytotaxon Sin 44:612–613 Ji YH, Yang CJ, Huang YL (2017) A new species of Paris sect. Axiparis (Melanthiaceae) from Yunnan, China. Phytotaxa 306:234–236

6 Taxonomic Revision Ji YH, Yang LF, Chase MW et al (2019) Plastome phylogenomics, biogeography, and clade diversification of Paris (Melanthiaceae). BMC Plant Biol 19:543. https://doi.org/10.1186/s12870-019-2147-6 Ji YH, Liu CK, Yang J, Jin L, Yang ZY, Yang JB (2020) UltraBarcoding discovers a cryptic species in Paris yunnanensis (Melanthiaceae), a medicinally important plant. Front Plant Sci 11:411. https://doi.org/10.3389/fpls.2020.00411 Li H (1984a) Two new species of the genus Paris. Acta Bot Yunnan 6:273–276 Li H (1984b) The phylogeny of the genus Paris L. Acta Bot Yunnan 6:351–362 Li H (1986) A study on the taxonomy of the genus Paris L. Bull Bot Res 6:109–146 Li H (1992) New taxa of the genus Paris L. Act Bot Yunnan 5:13–18 Li H (1998) The Genus Paris (Trilliaceae). Science Press, Beijing Liang SY, Soukup VG (2000) Paris L. In: Wu ZY, Raven PH (eds) Flora of China, vol 24. Science Press/Botanical Garden Press, St Louis/Beijing, pp 88–95 Rafinesque CS (1838) Flora Tellurana, vol 4. Probasco, Philadelphia Salisbury RA (1866) Genera Plantarum. John Van Voorst, London Takhtajan A (1983) A revision of Daiswa (Trilliaceae). Brittonia 35:255–270. https://doi.org/10.2307/2806025 Tatewaki M, Suto K (1935) In: Sapporo HG (ed) Transactions of the Sapporo Natural History Society, vol 14. Hokkaido Imperial University, Sapporo, p 36 Wang FZ, Tang J (1978) Flora Reipubicae Popularis Sinicae, vol 15. Science Press, Beijing, pp 86–96 Wang Z, Cai XZ, Zhong ZX et al (2017) Paris nitida (Melanthiaceae), A new species from Hubei and Hunan, China. Phytotaxa 314:145–149 Xu Z, Wei N, Tan Y et al (2019) Paris lihengiana (Melanthiaceae: Parideae), a new species from Yunnan, China. Phytotaxa 392:045–053 Yang ZY, Yang CJ, Ji YH (2019) Paris variabilis (Melanthiaceae), A new species from southwestern China. Phytotaxa 401:190–198 Zhou HH, Wu KY, Tao R (1991) A variety of Paris axialis. Act Bot Yunnan 13:424

7

Conservation Considerations

7.1

Conservation Status

Globally, many plant species are threatened with extinction due to habitat degradation, climatic change, biological invasions, and expanding human activities. The genus Paris, now consisting of 25 species according to its latest taxonomic revision (see Chap. 6), has great medicinal and ornamental importance. Prior to the 2000s, Paris species were not cultivated in plantations, and the pharmaceutical industry primarily relied on Rhizoma Paridis collected from wild populations. Due to the huge consumption of raw materials by the pharmaceutical industry (~3,000,000 kg/ year), natural populations of Paris species have recently undergone dramatic declines due to overharvesting (He et al. 2006; Yang et al. 2011; Huang et al. 2012; Li et al. 2015; Cunningham et al. 2018). In just 30 years, the market price of Rhizoma Paridis in China has risen 100-fold, fetching 650 CNY (~100 USD)/kg in 2019. This lucrative demand has seriously limited the sustainable development of the pharmaceutical industry and derailed the conservation and management of Paris species (Li et al. 2015). It is undoubtedly crucial for plant conservation biologists to identify the principal factors threatening species most vulnerable and to assess the extinction risk of specific plant taxa (Hoffmann et al. 2008). Yet, despite the monumental importance of Paris to the pharmaceutical industry, the current conservation status of this plant genus remains poorly understood. Based on herbarium records, field investigations, and IUCN criteria (IUCN 2012), a comprehensive assessment of the extinction risk faced by Paris species worldwide is presented here. It is the first preliminary step towards strengthening the recognition and protection of threatened species in this genus.

7.1.1

Species Rarity

Based on available herbarium voucher specimens, a total of 2837 occurrence records were found, which encompass the 26 Paris species currently recognized taxonomically (see Chap. 6), for an average of 113 specimen records per species. Of those, Paris chinensis was the best-sampled species with 578 records, followed by P. quadrifolia having 375 records. A total of 10 species had at least 100 specimens, another 5 species had between 51 and 68 specimens, 7 species were represented by 11 to 50 specimens, and just 4 species had less than 10 specimens (Table 7.1). Because of their medicinal importance and morphological distinctiveness, Paris species are not easily overlooked and are indeed sought out in the wild by plant collectors. The specimen occurrence of Paris species may reflect natural features of their population sizes, in that those species with less herbarium specimens are most likely rare, or harder to access, or simply have relatively smaller populations. Eleven species within the Paris were identified as having less than 50 specimen records. According to the geographical distribution of these putatively rare species, five species (Paris bashanensis, P. dunniana, P. luquanensis, P. qiliangiana, and P. yanchii) are endemic to China, while another five taxa (P. caobangensis, P. cronquistii, P. liiana, P. vietnamensis, and P. xichouensis) mainly occur in subtropical and tropical areas of China and Northern Indochina, and the last species (P. marmorata) grows in southwest China and the Himalayas. Among them, P. dunniana, P. luquanensis, P. xichouensis, and P. yanchii possess a particularly narrow species range, while the other species feature scattered and discontinuous distribution patterns. This suggests that these rare Paris species probably have

# Science Press 2021 Y. Ji, A Monograph of Paris (Melanthiaceae), https://doi.org/10.1007/978-981-15-7903-5_7

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Conservation Considerations

Table 7.1 Herbarium collections of Paris species Species 1 P. tetraphylla 2 P. incompleta 3 P. quadrifolia 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26

P. verticillata P. bashanensis P. japonica P. thibetica P. vaniotii P. forrestii P. dunniana P. vietnamensis P. xichouensis P. chinensis P. caobangensis P. qiliangiana P. fargesii P. cronquistii P. delavayi P. liiana P. yunnanensis P. luquanensis P. lancifolia P. yanchii P. marmorata P. polyphylla P. mairei

Distribution Japan Georgia, Russia, Turkey Austria, Belarus, France, Georgia, Germany, Italy, Latvia, Luxembourg, Moldova, Netherlands, Norway, Poland, Russia, Slovakia, Sweden, Switzerland, Spain, Ukraine, United Kingdom China, Japan, Kazakhstan, Korean Peninsula, Mongolia, Russia China Japan China, Nepal China Burma, China, India, Nepal China China, Laos, Vietnam China, Vietnam China, Thailand, Vietnam China, Thailand, Vietnam China China China, Vietnam China, Vietnam Burma, China Burma, China China China China China, Nepal China, India, Nepal China

low dispersal ability or are specialized to restricted habitats; hence, they are more vulnerable to environmental changes and anthropogenic activities (Henle et al. 2004). The phylogenetic positions of these rare Paris species were mapped onto the tree generated by analyzing complete plastome DNA sequences (Fig. 7.1). Among the five sections as currently circumscribed, the rare taxa were restricted to P. sect. Paris (1 species) and P. sect. Euthyra (10 species); comparatively, the proportion of rare species is unusually high in P. sect. Euthyra. It is also noteworthy that nearly all of them occupied terminal branches on the tree’s topology, suggesting they are among the more recently diverged species. This finding supports the idea that recently evolved plant taxa may incur relatively higher extinction risks (McKinney 1997; McKinney and Lockwood 1999).

7.1.2

Extinction Risk

The IUCN Red List of categories and criteria are an easily and widely adopted system for identifying species at high risk of global extinction (IUCN 2012). Among the 26 Paris species assessed here (Table 7.2), P. luquanensis,

No. of specimen records 167 57 375 346 11 26 51 65 134 5 23 5 578 8 13 68 29 109 34 155 12 240 4 18 127 147

P. xichouensis, and P. yanchii could be reliably classified as critically endangered (CR), because of their strictly restricted (extent of occurrence