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The Pennsylvania State University The Graduate School Department of Biology INVESTIGATING EVOLUTION OF PLANT DEVELOPMENT IN BASAL ANGIOSPERMS A Dissertation in Biology by Barbara Joanne Bliss 2008 Barbara Joanne Bliss Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2008 The dissertation of Barbara Bliss was reviewed and approved* by the following: Hong Ma Professor of Biology Dissertation Co-Advisor Co-chair of Committee Claude dePamphilis Professor of Biology Dissertation Co-Advisor Co-chair of Committee Paula McSteen Assistant Professor Siela Maximova Research Associate Doug Cavener Professor of Biology Head of the Department of Biology *Signatures are on file in the Graduate School iii ABSTRACT Understanding the evolution of modern plants requires integrating findings from several disciplines, including plant physiology and development, molecular genetics, and genomics. Observations from model and non-model plants are brought together in a phylogenetic framework to derive hypotheses about how plant development evolved to generate the abundant diversity we see today. Testing those hypotheses requires a plant model system with the appropriate phylogenetic perspective: that of a basal lineage. The greatest diversity of plants today is among the angiosperms (flowering plants), a lineage which arose only about 160 million years ago. The most successful of these are the monocot and core eudicot flowering plant lineages, from which current plant model experimental systems are derived. For questions about the evolution of angiosperm development, a plant model from among the basal lineages is required. In addition to phylogenetic perspective, model systems possess features and degrees of availability, representation, and utility not found in other members of the taxa to which they belong. For all organisms, culturing requirements are central determinants of utility, but for studying the evolution of plant development, amenability to studies employing methods of genomics, genetics, molecular and developmental biology are also required. This dissertation describes the search for and selection of a proposed basal angiosperm experimental model, Aristolochia fimbriata, along with the development of initial technologies required for testing hypotheses about the evolution of plant iv development. Culturing, hand pollination, genetic transformation, and in vitro micropropagation and regeneration methods are described herein. Genes involved in flower form and architecture have been particularly important in the evolution of angiosperm diversity. The TCP gene family, so named for its founding members (TEOSINTE BRANCHED1, CYCLOIDEA, PROLIFERATING CELL FACTOR) has been shown to play important roles in evolution of form in both monocots and eudicots. Prior functional and phylogenetic analyses of this gene family revealed clades of TCP genes with two different kinds of gene function. Since then, additional sequence data from basal lineages and new studies providing insight into TCP gene function have become available. Together, these warrant an updated phylogeny and review of this important gene family. Preliminary phylogenetic analyses of the TCP gene family is described as a foundation for conducting future expression and functional analyses. A. fimbriata has floral and vegetative features that will facilitate evaluating the role of TCP genes in evolution of angiosperm form, and advance the use of this species as a basal angiosperm model system. v TABLE OF CONTENTS LIST OF FIGURES ..................................................................................................... ix LIST OF TABLES ....................................................................................................... xii LIST OF ABBREVIATIONS ...................................................................................... xiv ACKNOWLEDGEMENTS ......................................................................................... xvii Chapter 1 Introduction ................................................................................................ 1 Innovations in land plants ..................................................................................... 2 Bryophytes and tracheophytes: Controlling water and gravity ..................... 2 Spermatophytes: Efficient reproduction ........................................................ 6 Angiosperms: “Flowering” plants ................................................................. 8 Angiosperm phylogeny ......................................................................................... 11 Phylogenetic analysis .................................................................................... 11 Selection of sequence data ............................................................................. 12 Basal angiosperms ................................................................................................ 14 Tracheary elements ........................................................................................ 16 Double fertilization ........................................................................................ 17 Flower ............................................................................................................ 18 Floral developmental genetics .............................................................................. 23 Floral organ identity model ........................................................................... 23 Genes involved in floral organ identity ......................................................... 25 Broader applications ...................................................................................... 29 Basal angiosperm model ....................................................................................... 30 Transformation systems ................................................................................. 31 Regeneration systems .................................................................................... 33 Overview of dissertation ....................................................................................... 34 Chapter 2 Aristolochia fimbriata: A proposed experimental model for basal angiosperms .......................................................................................................... 37 Abstract ................................................................................................................. 41 Introduction ........................................................................................................... 42 Results................................................................................................................... 47 Evaluation of potential models in basal angiosperm orders and families ..... 47 Aristolochiaceae candidates considered ........................................................ 50 Physical and life cycle features of Aristolochia fimbriata ............................ 52 A phylogenetic perspective of genome sizes ................................................. 55 Methods for genetics ..................................................................................... 57 Discussion ............................................................................................................. 60 vi Aristolochia fimbriata has many characteristics of a valuable experimental model ................................................................................ 60 Aristolochia fimbriata is well positioned for studies of the evolution of development ........................................................................................... 61 Aristolochia contains highly developed biochemical pathways offering insight into evolution of biochemical synthesis and coevolution with insects ..................................................................................................... 64 Aristolochia can provide insight into development of woodiness ................. 66 Aristolochia can reveal features of the ancestor common to monocots and eudicots ............................................................................................ 67 Growing genomic resources in Aristolochiaceae support further development of model system ................................................................ 68 Conclusion ............................................................................................................ 71 Materials & Methods ............................................................................................ 72 Cultivation ..................................................................................................... 72 Genome sizing ............................................................................................... 73 Phylogenetic analysis .................................................................................... 73 Pollination experiments ................................................................................. 74 Genetic transformation .................................................................................. 75 Genomic PCR analysis .................................................................................. 76 Genetic transformation .................................................................................. 77 Supplemental Material ................................................................................... 77 Acknowledgements ......................................................................................
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