Phylogeny and Biogeography of Paeonia (PAEONIACEAE)
Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of the Ohio State University
By Tao Sang, B.S., M.S.
The Ohio State University 1996
Dissertation Committee: Daniel J. Crawford, Keith R. Davis, Tod F. Stuessy
The completion of this project would not have been possible without the generous assistance of numerous people I wish to express my sincere appreciation to my major professor. Tod F. Stuessy, for his invaluable advice constant encouragement, and continuous support throughout all phases of my graduate study. Sincere appreciation is also expressed to Dr. Daniel J. Crawford for his generous help and invaluable guidance in all aspects of my research and study at OSU. I am deeply indebted to Dr. G. Ledyard Stebbins for his support and encouragement of the project as well as helpful discussions. I thank Professor De-yuan Hong for his continuous support, stimulating suggestions, and generous help in many aspects of this project. I thank Dr. Keith Davis for serving in my advisory, general exam, and dissertation committee, and for his valuable comments on my dissertation draft.
Numerous friends and colleagues provided help and assistance during my field trips to California, Bulgaria, China, Greece, and Spain. Special thanks go to Abdeslam E. Aallali, David J. Keil, Xue-yi Li, Joaquin M. Mesa, Kaiyu Pan, Yianlong Pei, D. Petkova, Tim S. Ross, Dagui Tang, Dimitris Tzandoudakis, and Dessi Usunov. I thank Bruce Bartholomew, G. L. Osti, Loren H. Rieseberg, and Nigel Rowland for providing plant materials; and the Royal Botanic Gardens, Kew, for allowing collection of leaf materials. Thanks also go to my colleagues and friends, Jorge Arriagada, Erica Armstrong, Marybeth Cosner, Melanie Devore, Betsy Esselman, Karia Gengler, Seung-Chul Kim, Hongqi Li, Ming Yang, Xuanii Yao, James Zech, and Liming Zhao for their help and useful discussions.
I am grateful to Mr. Roy Klehm (Klehm Nursery, South Barrington, Illinois) for his generous financial support of the field work. This research was also supported* by a National Science Foundation Doctoral Dissertation Improvement Grant DEB-9321616 to T.F.S. and T.S., a Sigma Xi Grant-in-Aid of Research, a Graduate Student Research Grant from American Society of Plant Taxonomists, two Janice Beatley Herbarium (OS) Awards, and a Graduate Student Alumni Research Award from the Ohio State University
The curators of the following herbaria are acknowledged for allowing study of specimens, either through loans or during visits: ATH, GH, GRA, K, KUN, NY, PE, SO, SOM, SZ. UC, UPA, US, and WUK.
Finally, I give my most special thanks to my wife, Wanxiao, for her love, support, understanding, and help during four years of my graduate study
January 19, 1966 Born - Sichuan, P. R. China
1986 B.S., Botany, Fudan University, Shanghai, P. R. China
1989 M.S., Botany, Fudan University, Shanghai, P. R. China
1990-91 Teaching Assistant, Department of Botany, Ohio University, Athens, Ohio
1991-94 Graduate Teaching/Research Associate, Department of Plant Biology, The Ohio State University, Columbus, Ohio
1994-95 Presidential Fellow, The Ohio State University, Columbus, Ohio
PUBLICATIONS see file Literature
Abstracts Presented To Meetings see file Literature
FIELDS OF STUDY Major field: Plant Biology, Studies in Plant Evolution and Systematics with Professor Tod F. Stuessy
TABLE OF CONTENTS
LIST OF TABLES
LIST OF FIGURES
chapter 1 Documentation of reticulate evolution in peonies (PAEONIA) using ITS sequences of nrDNA: Implications for biogeography and concerted ecolution
Materials and methods
chapter 2 Complex reticulate evolution in peonies revealed by nuclear and chloroplast DNA
Materials and Methods
Results and Discussion
chapter 3 Evolution of chloroplast DNA intergenic spacers and phylogenetic implications in peonies (PAEONIA. PAEONIACEAE)
Materials and Methods
chapter 4 Evolution, Classification and Biogeography of PAEONIA (PAEONIACEAE)
Materials and Methods
List of REFERENCES
LIST OF TABLES, LIST OF FIGURES see file Tables
Peonies (Paeonia. Paeoniaceae), with great ornamental and medicinal value, have been known as "king of flowers" in China and "queen of herbs" in Greece for more than one thousand years. Beyond ornament and medicine, peonies have offered many intriguing problems for plant systematists.
The genus Paeonia. comprising approximately 35 diploid (2n = 10) and tetraploid species of shrubs and perennial herbs, occurs widely in five disjunct areas of the northern hemisphere, eastern Asia, central Asia, the western Himalayas, the Mediterranean region, and pacific North America. Paeonia has long been a taxonomically difficult group, presumably because it has undergone extensive reticulate evolution, i.e., speciation via hybridization.
Reticulate evolution, particularly when combined with polyploidization, is an important evolutionary mechanism in plants. Reconstructing reticulate evolution, however, has been a remarkably challenging task. Although the application of molecular markers has greatly facilitated the detection of hybridization and the recognition of allopolyploids in many plant groups, difficulties remain, largely due to lack of understanding the complex dynamic of molecular evolution. In this study, reticulate evolution was documented in Paeonia
section Paeonia based on nucleotide additivity detected by directly sequencing PCR products of internal transcribed spacers (ITS) of nuclear ribosomal DNA. The study, thus, provides an example of successfully using ITS sequences to reconstruct reticulate evolution in plants, and further demonstrates that sequence data can be highly informative and accurate for detecting hybridization. The maintenance of parental sequences in the species of hybrid origin is likely due to the slowing of concerted evolution caused by the long generation time of peonies. The partial and uneven homogenization of parental sequences displayed in nine species of hybrid origin may have resulted from gradients of gene conversion.
To understand further these complex reticulate evolutionary patterns and their molecular consequences in section Paeonia. the rapidly evolving chloroplast gene, matK, was sequenced. A comparison of phylogenetic reconstructions based on nuclear (ITS) and chloroplast (matK) DNA sequences revealed an even more complex pattern of reticulate evolution in this section. Besides hybrid species detected by ITS sequence additivity, additional hybrids are identified by comparing their different positions on ITS and matK phylogenies which result from inheritance of maternal chloroplast DNA and fixation for paternal ITS sequences. The study, therefore, demonstrates that reticulate evolution has played a primary role in speciation in peonies and can be reconstructed by careful interpretation of independent gene phylogenies.
Phylogenetic information is also examined from two intergenic spacers of chloroplast DNA (cpDNA), psbA-trnH and trnL-trnF. Since noncoding intergenic spacers of cpDNA are presumably under less functional constraint and thus may evolve more rapidly, they are considered to be potentially useful sources of phylogenetic information at low taxonomic level. It was found, in peonies, that the intergenic spacer psbA-trnH evolves more rapidly and less homoplasiously than the matK coding region, and may serve as a new phylogenetic marker at the intrageneric level. However, the phylogenetic value of the frequently used intergenic spacer trnL-trnF is questionable because it evolves more slow and more homoplasious than the matK coding region in peonies. Nonetheless, the study suggests that a short cpDNA intergenic spacer alone may not provide enough synapomorphic characters to group closely related species whose relationships may be assessed by rapidly evolving sequences of multiple coding and noncoding regions of cpDNA.
Based on molecular evolutionary studies, classification, evolution of morphology and cytology, and biogeography of Paeonia are discussed. Phylogenetic reconstructions support previous recognition of three sections, Oneapia, Moutan, and Paeonia. within the genus, and two subsections within section Moutan. In section Paeonia, however, two taxonomic subsections are not in agreement with phylogenetic relationships. Taxonomic difficulties within this section are attributed to complex reticulate evolution. In comparison with DNA sequence divergence, section Oneapia evolved very slowly in morphology, whereas morphology of subsection Vaginatae of section Moutan diverged more rapidly. Among species of hybrid origin in section Paeonia, the proportion of diploids is surprisingly high, suggesting that hybrid speciation at the diploidy level is quite frequent in peonies.
Biogeographically, the Eurasian and western North American disjunction between section Oneapia and the rest of the genus may have resulted from interruption of continuous distribution of peonies in eastern Asia and western North America through the Bering land bridge during middle Miocene. Pleistocene glaciation may have served as a primary factor triggerring extensive reticulate evolution within section Paeonia and that also drastically shifted distributional ranges of both parental and hybrid species.