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Mutational Dynamics and Phylogenetic Utility of Plastid Introns and Spacers in Early Branching Eudicots Supervisor: Prof

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Mutational Dynamics and Phylogenetic Utility of Plastid Introns and Spacers in Early Branching Eudicots Supervisor: Prof Mutational dynamics and phylogenetic utility of plastid introns and spacers in early branching eudicots Dissertation zur Erlangung des akademischen Grades Doctor rerum naturalium (Dr. rer. nat.) vorgelegt der Mathematisch-Naturwissenschaftlichen Fakultät der Technischen Universität Dresden von Dipl.-Biol. Anna-Magdalena Barniske geboren am 19. März 1976 in Halle/Saale Eingereicht am 26.10.2009 Verteidigt am 16.12.2009 Die Dissertation wurde in der Zeit von 02/2005 bis 10/2009 im Institut für Botanik angefertigt 1. Gutachter: Prof. Dr. Christoph Neinhuis, Dresden 2. Gutachter: Prof. Dr. Dietmar Quandt, Bonn 2 to my grandmother 3 Table of contents ACKNOWLEDGEMENTS 5 INTRODUCTION 6 INTRODUCTION – THE EARLY-DIVERGING EUDICOTS 6 MATERIAL, METHODS & RELATED DISCUSSION 9 RESULTS & DISCUSSION 12 CONCLUSIONS 15 CHAPTER 1 16 CORROBORATING THE BRANCHING ORDER AMONG EUDICOTS: TESTING FOR PHYLOGENETIC SIGNAL AMONG CHLOROPLAST INTRONS AND SPACERS 16 1.1 ABSTRACT 17 1.2 INTRODUCTION 18 1.3 MATERIAL AND METHODS 21 1.4 RESULTS 36 1.5 DISCUSSION 45 1.5.1 Relationships among early-diverging eudicots 45 1.5.2 Testing hypotheses of a unique genome history with parsimony, Bayesian and likelihood approaches 49 1.5.3 Molecular evolution of genomic regions studied 51 1.5.4 Phylogentic structure 58 1.6 CONCLUSIONS 63 1.7 APPENDICES 65 CHAPTER 2 76 RESOLVING THE BACKBONE OF THE FIRST DIVERGING EUDICOT ORDER: THE RANUNCULALES 76 2.1 ABSTRACT 77 2.2 INTRODUCTION 77 2.3 MATERIAL AND METHODS 80 2.4 RESULTS 83 2.5 DISCUSSION 91 CHAPTER 3 101 PHYLOGENETIC RELATIONSHIPS AMONG ANEMONE, PULSATILLA, HEPATICA AND CLEMATIS (RANUNCULACEAE) 101 3.1 ABSTRACT 102 3.2 INTRODUCTION 102 3.3 MATERIAL AND METHODS 104 3.4 RESULTS & DISCUSSION 113 3.4.1 Sequence variability 113 3.4.2 Phylogeny of the tribe Anemoneae 115 3.4.3 Phytogeographical aspects within the subtribe Anemoninae 125 REFERENCES 127 CURRICULUM VITAE 147 PUBLICATION LIST 149 VERSICHERUNG 150 4 Acknowledgements This thesis wouldn’t have been possible without the support and interaction of several persons, first of all Prof. Dr. Dietmar Quandt and Prof. Dr. Christoph Neinhuis. Prof. Quandt gave me the opportunity to participate in his project on the evolution of early- diverging eudicots. He supported me in taking delight in a subject new to me. Prof. Neinhuis has offered me the opportunity to be a part of his research group and to conduct the work not only in a modern well-equipped laboratory but also in a warm atmosphere. Both encouraged, supported and helped me especially in difficult situations. Furthermore I like to thank Prof. Dr. Thomas Borsch, Prof. Dr. Kai Müller, Andreas Worberg, in particular Karsten Salomo and everyone from the eudicots-evolutionary- research group for all kind of help including support in the laboratory or with calculations when needed and proof reading as well as many helpful discussions. I whish to express my gratitude to the Botanical Garden Dresden in particular the custodian Dr. Barbara Ditsch, for providing fresh plant material in an incomplex way. Further supply of plant material from various colleagues as well as the Botanical Gardens Bonn, Ghent and Talca is gratefully acknowledged. Additionally I want to warmly thank the whole plant phylogenetics working group who made my work much more pleasant. I enjoyed being a member of this group and benefited a lot from working with the colleagues. My special thanks to Ursula Arndt and Sylvi Malcher for taking care of the official tasks, Volker Buchbender, Dr. Sanna Olsson and Lars Symmank for many fruitful and motivating discussions as well as Dr. Stefan Wanke for his support. Above all I thank my family and friends for supporting and encouraging me over the years. This thesis was embedded in the project „Mutational dynamics of non-coding genomic regions and their potential for reconstructing evolutionary relationships in eudicots“ (grants BO1815/2 and QU153/2) supported by the Deutsche Forschungsgemeinschaft. The funding of the project is kindly acknowledged. 5 Introduction Introduction – The early-diverging eudicots During the last twenty years major progress has been made towards a better understanding of phylogenetic relationships among angiosperms. An early broad-scale molecular- phylogenetic analysis on the basis of rbcL sequence data (Chase & al., 2003; compare Figure 1) clearly revealed three major groups, with eudicots as well as monocots being monophyletic, arisen from a paraphyletic group of “basal” dicotyledonous angiosperms. A number of molecular investigations have consistently recovered the eudicotyledonous clade and increased confidence in its existence (e.g. Savolainen & al., 2000a; Qui & al., 2000; Soltis & al., 2000; Hilu & al., 2003; Kim & al., 2004).With about 200,000 species the eudicot clade contains the vast majority of angiosperm species diversity (Drinnan & al., 1994). As they are characterised by the possession of tricolpate and tricolpate-derived pollen the eudicots have also been called the tricolpate clade (Donoghue & Doyle, 1989). Based on the use of sequence data several lineages, such as Ranunculales, Proteales, Sabiaceae, Buxaceae plus Didymelaceae, and Trochodendraceae plus Tetracentraceae were identified as belonging to the early-diverging eudicots (= “basal eudicots”), while larger groups like asterids, Caryophyllales, rosids, Santalales, and Saxifragales were revealed as being members of a highly supported core clade, the so called “core eudicots” (Chase & al., 1993; Savolainen & al., 2000b; Soltis & al., 2000; 2003; Hilu & al., 2003; Worberg & al., 2007). Furthermore Gunnerales were shown to be the first-branching lineage within core eudicots, having a sistergroup relationship with the remainder of the clade (e.g. Soltis & al., 2003; Worberg & al., 2007). However, the exact branching order among the several lineages of the eudicots remained difficult to resolve. This thesis is to a great extent concentrated on resolving relationships among the different clades of the early-branching eudicots as well as on clarifying phylogenetic conditions inside distinct lineages, based on phylogenetic reconstructions using sequence data of fast-evolving and non-coding molecular regions. 6 Figure 1: Phylogeny of seed plants based on rbcL sequence data taken from Chase & al. (1993). The three major groups of angiosperms are shaded in colour: “basal” dicotyledonous angiosperms (green), monocots (blue), eudicots (brown). Chapter 1 deals with the placement of Sabiales and Proteales within the “basal” eudicot grade by analyzing a set of nine regions including spacers, group I and group II introns plus the coding matK from the large single copy region of the chloroplast genome. Up to now, five different coding regions have been used for reconstructing relationships within the early-diverging eudicots. Analysis of the plastid rbcL and atpB alone and in combination resulted in the recognition of all lineages (e.g. Chase & al., 1993; Savolainen & al., 2000a), albeit statistical support for their respective placements was not evident. However, close relations of the herbaceous Nelumbonaceae and the woody Platanaceae and Proteaceae emerged. The addition of the nuclear 18S (Hoot & al., 1999; Soltis & al., 2000) and the 26S, completing a four-gene analyses by Kim et al. (2004), resulted in improved support for most terminal clades, recovering the first-branching position of Ranunculales, while the respective placements of clades still needed to be verified. A similar hypothesis was yielded through the application of the rapidly evolving plastid matK gene (Hilu & al., 2003), additionally hinting on a sistergroup relationship of 7 Buxaceae and core eudicots. Worberg & al. (2007) combined the complete matK with four non-coding markers from the plastome in their analyses and were thus able to present a highly supported grade of Ranunculales, Sabiales (=Sabiaceae), Proteales (consisting of Nelumbonaceae, Platanaceae and Proteaceae), Trochodendrales (including Trochodendraceae and Tetracentraceae) and Buxales (Buxaceae plus Didymelaceae). As the only exception the position of Sabiales was only moderately supported or differed in model-based approaches, respectively. Thus the placement of Sabiales still remained to be cleared up with confidence. This difficult to resolve relationships inside the early- diverging eudicots were furthermore considered to be well adapted for testing and comparing the utility and performance of different non-coding and fast-evolving genomic partitions like spacers and introns in deep-level reconstructions. The aim of chapter 2 was to present a thorough reconstruction of phylogenetic relationships within the first-branching clade of the eudicots with an emphasis on the evolution of growth forms inside the group. Currently, the Ranunculales consist of seven families (Ranunculaceae, Berberidaceae, Menispermaceae, Lardizabalaceae, Circaeasteraceae, Eupteleaceae, and Papaveraceae; according to APG II, 2003) comprising predominantly herbaceous groups as well as woody lineages developing trees and lianescent or shrubby forms. A surprising result that emerged due to the increased use of molecular data for systematics is the inclusion of the woody Eupteleaceae, a monogeneric family that was previously placed next to Cercidiphyllaceae (Cronquist, 1981; 1988) or Hamamelididae (Takhtajan, 1997). Although phylogenetic hypotheses agreed in the exclusion of Eupteleaceae and the predominantly herbaceous Papaveraceae s.l. from a core clade, topologies differed in postulating Eupteleaceae being the first- branching
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