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The Pennsylvania State University The Pennsylvania State University The Graduate School Intercollege Graduate Degree Program in Plant Biology PHYLOGENOMIC ANALYSIS OF ANCIENT GENOME DUPLICATIONS IN THE HISTORY OF PLANTS A Dissertation in Plant Biology by Yuannian Jiao © 2011 Yuannian Jiao Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2011 The dissertation of Yuannian Jiao was reviewed and approved* by the following: Claude dePamphilis Professor of Biology Dissertation Advisor Chair of Committee Hong Ma Professor of Biology John Carlson Professor of Molecular Genetics Webb Miller Professor of Comparative Genomics and Bioinformatics Naomi Altman Professor of Statistics Teh-hui Kao Chair of Plant Biology Graduate Program *Signatures are on file in the Graduate School iii ABSTRACT Whole-genome duplication (WGD), or polyploidy, followed by gene loss and diploidization, has generally been viewed as a primary source of material for the origin of evolutionary novelties. Most flowering plants have been shown to be ancient polyploids that have undergone one or more rounds of WGDs early in their evolution, and many lineages have since undergone additional, independent and more recent genome duplications. It was suggested that the paleopolyploidy events were crucial to the radiation and success of angiosperms, but evidence for proposed ancient genome duplications remains equivocal. Plant genomes are highly dynamic and usually go through intense structural rearrangements and gene loss following duplication. Old(er) WGDs can not be detected using within-genome colinearity method. Although the occurrence of WGD event(s) is well accepted, the actual number, phylogenetic timing, and age of the event(s) remain equivocal. Here we mainly employed phylogenomic approach to address following questions: 1) To more precisely time and evaluate the fates of genes following genome duplications in eudicots, we built a phylogenomic pipeline to reconstruct the evolutionary relationships of 4433 gene families from the complete gene sets of Arabidopsis, Populus, Vitis, and Oryza. For each family, we determined the gene duplications relative to the evolutionary tree of the organisms, and also matched gene pairs of specific WGD events for later synonymous substitution (Ks) analysis. Concentrations of duplication events at shared branch points in the gene family phylogenies confirmed some of the results of earlier studies, and also indicated new interesting signals for polyploidy events. 2) To track more ancient WGDs pre-dating the divergence of monocots and eudicots, we used comprehensive phylogenomic analyses of nine sequenced plant genomes and more than 12.6 million new expressed-sequence-tag (EST) sequences from phylogenetically pivotal lineages. Two additional, previously unnoticed ancient WGDs have been elucidated in the common ancestor of extant seed plants dated at ~ 319 million iv years ago (mya) and extant angiosperms dated at ~ 192 mya, respectively. Significantly, these ancestral WGDs resulted in the diversification of regulatory genes important to seed and flower development, suggesting that they were involved in major innovations that ultimately contributed to the rise and eventual dominance of seed plants and angiosperms. 3) To precisely time the γ event, which was proposed before the separation of all rosids, we mapped the duplication events onto phylogenetic trees that include the paralogs created by the γ event and orthologous genes from other species. The overwhelming majority of well-resolved Vitis duplications were placed before the separation of rosids and asterids and after the split of monocots and eudicots, providing evidence for the WGD (γ) early in eudicot evolution. A large proportion of the Vitis duplications were placed after the divergence of basal eudicots, supporting the γ triplication was likely restricted to core-eudicots. Global gene family phylogenies are a valuable complement to genome-scale structural analysis, incorporating extensive genome-wide evidence even without a sequenced genome, and facilitate a better understanding of WGD events in plants. v TABLE OF CONTENTS Chapter 1 Introduction ............................................................................................................. 1 Brief history of gene duplication research ....................................................................... 1 Mechanisms of gene duplication...................................................................................... 2 The evolutionary significance of whole genome duplications......................................... 3 Fate of the duplicated genes............................................................................................. 5 How whole genome duplication is studied ...................................................................... 8 Identification of block duplications.......................................................................... 8 Age distributions of duplicated genes ...................................................................... 9 Duplication histories from phylogenomic analysis of gene families ....................... 11 Current research on dating duplication events in flowering plants.................................. 12 Contents of this dissertation............................................................................................. 15 References........................................................................................................................ 16 Chapter 2 Tracking the history of genome duplications in flowering plants: evidence from global gene family phylogenies ....................................................................................... 23 Background ...................................................................................................................... 24 Results and Discussion..................................................................................................... 30 Initial screen with four genomes .............................................................................. 30 Rosid-wide or Eudicot-wide large-scale duplication events? .................................. 34 Duplications in asterids ............................................................................................ 37 One or two rounds of duplication in the Arabidopsis lineage after the split of rosid I and rosid II ............................................................................................ 40 Conclusions...................................................................................................................... 45 Materials and methods ..................................................................................................... 46 Gene Family Search ................................................................................................. 46 Alignment................................................................................................................. 47 Phylogenetic Analysis.............................................................................................. 48 Scoring Gene Duplications....................................................................................... 48 Rate of Synonymous Substitution (Ks) Calculation................................................. 49 Finite Mixture Models of Genome Duplications ..................................................... 49 List of abbreviations......................................................................................................... 50 References........................................................................................................................ 50 Chapter 3 Ancestral polyploidy in seed plants and angiosperms............................................. 55 Background ...................................................................................................................... 55 Results and Discussion..................................................................................................... 60 Phylogenomic evidence for ancient gene duplications ............................................ 60 Ancient duplications are concentrated in time ......................................................... 67 Synteny analysis of ancient gene duplications......................................................... 70 Implications for plant evolution ............................................................................... 73 Methods............................................................................................................................ 77 vi Phylogenetic analysis ............................................................................................... 77 Scoring gene duplications ........................................................................................ 78 Finite mixture models of genome duplications........................................................ 78 Molecular dating analyses and 95% confidence intervals ....................................... 79 Rate of synonymous substitution (Ks) calculation ................................................... 80 GO enrichment for orthogroups with ancient duplication ....................................... 80 References........................................................................................................................ 81 Chapter 4 Phylogenomic dating of the gamma polyploidy event in flowering plants............. 85 Background .....................................................................................................................
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