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Evolution by Ancient Gene and Genome Duplication in Hexapods and Land Plants

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Evolution by Ancient Gene and Genome Duplication in Hexapods and Land Plants Evolution by Ancient Gene and Genome Duplication in Hexapods and Land Plants Item Type text; Electronic Dissertation Authors Li, Zheng Publisher The University of Arizona. Rights Copyright © is held by the author. Digital access to this material is made possible by the University Libraries, University of Arizona. Further transmission, reproduction, presentation (such as public display or performance) of protected items is prohibited except with permission of the author. Download date 11/10/2021 02:05:02 Link to Item http://hdl.handle.net/10150/645813 EVOLUTION BY ANCIENT GENE AND GENOME DUPLICATION IN HEXAPODS AND LAND PLANTS by Zheng Li __________________________ Copyright © Zheng Li 2020 A Dissertation Submitted to the Faculty of the DEPARTMENT OF ECOLOGY AND EVOLUTIONARY BIOLOGY In Partial Fulfillment of the Requirements For the Degree of DOCTOR OF PHILOSOPHY In the Graduate College THE UNIVERSITY OF ARIZONA 2020 2 THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE As members of the Dissertation Committee, we certify that we have read the dissertation prepared by: Zheng Li, titled: “Evolution by Ancient Gene and Genome Duplication in Hexapods and Land Plants" and recommend that it be accepted as fulfilling the dissertation requirement for the Degree of Doctor of Philosophy. Sep 10, 2020 _________________________________________________________________ Date: ____________ Michael S. Barker Sep 10, 2020 _________________________________________________________________ Date: ____________ Michael J. Sanderson Sep 10, 2020 _________________________________________________________________ Date: ____________ John J. Wiens Sep 10, 2020 _________________________________________________________________ Date: ____________ Wendy Moore Final approval and acceptance of this dissertation is contingent upon the candidate’s submission of the final copies of the dissertation to the Graduate College. I hereby certify that I have read this dissertation prepared under my direction and recommend that it be accepted as fulfilling the dissertation requirement. Sep 10, 2020 _________________________________________________________________ Date: ____________ Michael S. Barker Dissertation Committee Chair Department of Ecology & Evolutionary Biology 3 DEDICATION This dissertation is dedicated to my beloved mother, Guohuan He. 4 TABLE OF CONTENTS ABSTRACT.........................................................................................................................5 INTRODUCTION...............................................................................................................6 PRESENT STUDY............................................................................................................13 REFERENCES..................................................................................................................18 APPENDIX A: EARLY GENOME DUPLICATIONS IN CONIFERS AND OTHER SEED PLANTS………………………………………………………….........30 APPENDIX B: MULTIPLE LARGE-SCALE GENE AND GENOME DUPLICATIONS DURING THE EVOLUTION OF HEXAPODS...........................77 APPENDIX C: ANCIENT POLYPLOIDY AND LOW RATE OF CHROMOSOME LOSS EXPLAIN FERNS WITH HIGH CHROMOSOME NUMBERS.................156 APPENDIX D: PATTERNS AND PROCESSES OF DIPLOIDIZATION IN LAND PLANTS…………………………………………………...….......................................216 5 ABSTRACT Gene and genome duplications have been found across the eukaryotic tree of life. Yet, many aspects of evolution by gene and genome duplications remain unclear, especially ancient duplications. In my dissertation, I focus on the incidence of ancient gene and genome duplication in different lineages of land plants and hexapods, their impact on genome evolution, and the pattern and processes of diploidization following polyploidy. In Appendix A, I use transcriptomes of gymnosperms and outgroups, and a novel phylogenetic algorithm to provide the first comprehensive study of ancient WGD in gymnosperms. In Appendix B, I use over 150 insect genomes and transcriptomes to infer ancient WGDs and other large-scale gene duplications during the evolution of hexapods. In Appendix C, I investigate ancient WGD in ferns from over 140 fern transcriptomes and test the long standing hypothesis on high chromosome number in ferns. In Appendix D, I summarize current studies on the patterns and processes of diploidization in the land plants and provide directions for testing hypotheses and understanding diploidization in the future. As a whole, this work improves our understanding of the mode and tempo of eukaryotic genome evolution and diversity. 6 INTRODUCTION Polyploidy is perhaps most well recognized as an important component of plant evolution and speciation (Stebbins, 1950 Grant, 1981). In flowering plants and ferns about 15% and 31% speciation events, respectively, are due to recent polyploidization (Wood et al., 2009). Most land plants are now known to be ancient polyploids that have rediploidized (One Thousand Plant Transcriptomes Initiative, 2019). Comparative genomic studies have shown plant genomes are highly dynamic and plants experienced cycles of polyploidy followed by diploidization (Wolfe, 2001 Jiao et al., 2011 Arrigo and Barker, 2012 Li et al., 2015 Wendel, 2015a Van de Peer et al., 2017 One Thousand Plant Transcriptomes Initiative, 2019). Different from plants, polyploidy is considered to be rarer in animals (Muller, 1925 Orr, 1990 Mable, 2004). Recent advancements in genome sequencing and analyses have found ancient polyploidy across the tree of life (Aury et al., 2006 Storchová et al., 2006 Van de Peer et al., 2017 Li, Tiley, et al., 2018 One Thousand Plant Transcriptomes Initiative, 2019). Polyploidy is also an important component of genome evolution. Genome duplication can double the genome size and chromosome numbers during polyploid formation (Otto, 2007). The process of diploidization following polyploidy can significantly change genome content (Arrigo and Barker, 2012 Murat et al., 2017) and gene networks (Thomas et al., 2006 Freeling , 2009 Defoort et al., 2019) may have provided novel genetic variation that was important for the evolution of plant diversity (Tank et al., 2015 Landis et al., 2018). 7 Ancient genome duplications in gymnosperms Polyploidy is a common mode of speciation and evolution in angiosperms (Stebbins, 1950 Grant, 1981). The signatures of ancient WGD are found in most of the vascular plants (One Thousand Plant Transcriptomes Initiative, 2019). Recent analyses also provide evidence that an ancient WGD shared by seed plants, and all flowering plants experienced another round of paleopolyploidy (Jiao et al., 2011). In contrast, there is little evidence indicating whole genome duplication played a significant role in the gymnosperms (Wood et al., 2009), except in a few genera (such as Ephedra) in which polyploidy is prevalent (Ahuja, 2005 Ickert-Bond et al., 2020). One of the major consequences of polyploidy is the increase in genome size by doubling the whole genome (Otto, 2007). Many gymnosperms, especially conifers, have huge genomes (Murray, 1998 Ahuja et al., 2005). The first gymnosperm genome sequenced, the Norway spruce, was published in Nature in 2014. In this study, researchers found evidence of the seed plant genome duplication but no ancient WGD specific to gymnosperm (Nystedt et al., 2013). They proposed the large genome size in conifers is due to transposable element proliferation without ancient WGD (Nystedt et al., 2013). However, this result contradicted some previous studies on G-banding in chromosomes and genome size of conifers which suggested ancient WGD might have occurred during the evolution of conifers (Drewry, 1982 Ahuja, 2005). Before my dissertation research, little was known about ancient genome duplication in gymnosperms. It was also unclear whether the seed plant WGD is restricted to seed plants or shared with monilophytes. In Appendix A, I used 24 transcriptomes of gymnosperms and three outgroups, and a novel phylogenetic algorithm 8 to provide the first comprehensive study of ancient WGD in gymnosperms. My study also improved the phylogenetic placement of the ancestral seed plant WGD. Ancient gene and genome duplications in hexapods Different from plants, polyploidy has long been considered rarer in animals (Muller, 1925 Orr, 1990). Although less common, polyploidy has been found in some animal lineages (Otto and Whitton, 2000 Mable, 2004). Multiple recent WGDs have been recorded in fish (Mable et al., 2011). All teleost fish have polyploid ancestry and all the Salmonidea share another ancient WGD (Van de Peer et al., 2003 Van de Peer, 2004 Meyer and Van de Peer, 2005 Berthelot et al., 2014). More broadly, Ohno hypothesized that two rounds of ancient WGDs (the 2R hypothesis) occurred in the ancestry of all the vertebrates (Ohno, 1970). According to this hypothesis, most vertebrates, including humans, are descendants of an ancient polyploid (Makalowski, 2001). Although whether two rounds of WGDs occurred has been debated (Furlong and Holland, 2002 Hughes and Robert, 2003 Kasahara, 2007), several recent genomic studies provide strong evidence for the 2R hypothesis (Dehal et al., 2005) (Putnam et al., 2008 Smith et al., 2013). Recent genomic analyses also revealed multiple paleopolyploidies in the ancestry of various invertebrate lineages. In chelicerates, evidence of ancient WGD has been found in horseshoe crabs (Nossa et al., 2014 Kenny et al., 2017 Nong et al., 2020 Shingate et al., 2020) and spiders (Clarke et al., 2015 Schwager et al., 2017). Genome and chromosome number
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