View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Digital Repository @ Iowa State University Ecology, Evolution and Organismal Biology Ecology, Evolution and Organismal Biology Publications 11-26-2018 A Malvaceae mystery: A mallow maelstrom of genome multiplications and maybe misleading methods? Justin L. Conover Iowa State University, [email protected] Nisa Karimi University of Wisconsin-Madison Noah Stenz University of Wisconsin-Madison Cécile Ané University of Wisconsin-Madison Corrinne E. Grover IFoowlalo Swta tthie Usn iaverndsit ay,dd coritrioninne@ial wasorktates.e adut: https://lib.dr.iastate.edu/eeob_ag_pubs Part of the Ecology and Evolutionary Biology Commons, Genetics and Genomics Commons, See next page for additional authors and the Plant Breeding and Genetics Commons The ompc lete bibliographic information for this item can be found at https://lib.dr.iastate.edu/ eeob_ag_pubs/322. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html. This Article is brought to you for free and open access by the Ecology, Evolution and Organismal Biology at Iowa State University Digital Repository. It has been accepted for inclusion in Ecology, Evolution and Organismal Biology Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. A Malvaceae mystery: A mallow maelstrom of genome multiplications and maybe misleading methods? Abstract Previous research suggests that Gossypium has undergone a 5- to 6-fold multiplication following its divergence from Theobroma. However, the number of events, or where they occurred in the Malvaceae phylogeny remains unknown. We analyzed transcriptomic and genomic data from representatives of eight of the nine Malvaceae subfamilies. Phylogenetic analysis of nuclear data placed Dombeya (Dombeyoideae) as sister to the rest of Malvadendrina clade, but the plastid DNA tree strongly supported Durio (Helicteroideae) in this position. Intraspecific Ks plots indicated that all sampled taxa, except Theobroma (Byttnerioideae), Corchorus (Grewioideae), and Dombeya (Dombeyoideae), have experienced whole genome multiplications (WGMs). Quartet analysis suggested WGMs were shared by Malvoideae-Bombacoideae and Sterculioideae- Tilioideae, but did not resolve whether these are shared with each other or Helicteroideae (Durio). Gene tree reconciliation and Bayesian concordance analysis suggested a complex history. Alternative hypotheses are suggested, each involving two independent autotetraploid and one allopolyploid event. They differ in that one entails an allopolyploid origin for the Durio lineage, whereas the other invokes an allopolyploid origin for Malvoideae-Bombacoideae. We highlight the need for more genomic information in the Malvaceae and improved methods to resolve complex evolutionary histories that may include allopolyploidy, incomplete lineage sorting, and variable rates of gene and genome evolution. Disciplines Ecology and Evolutionary Biology | Genetics and Genomics | Plant Breeding and Genetics Comments This is the peer reviewed version of the following article: Conover, Justin L., Nisa Karimi, Noah Stenz, Cécile Ané, Corrinne E. Grover, C. Skema, Jennifer A. Tate et al. "A Malvaceae mystery: A mallow maelstrom of genome multiplications and maybe misleading methods?." Journal of Integrative Plant Biology (2018), which has been published in final form at doi: 10.1111/jipb.12746. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions. Authors Justin L. Conover, Nisa Karimi, Noah Stenz, Cécile Ané, Corrinne E. Grover, C. Skema, Jennifer A. Tate, Kirsten Wolff, Samuel A. Logan, Jonathan F. Wendel, and David A. Baum This article is available at Iowa State University Digital Repository: https://lib.dr.iastate.edu/eeob_ag_pubs/322 Research Article A Malvaceae mystery: A mallow maelstrom of genome multiplications and maybe misleading methods? Running Title: WGMs in the Malvaceae Justin L. Conover1†, Nisa Karimi2†, Noah Stenz2,3, Cécile Ané2,4, Corrinne E. Grover1, C. Skema5, Jennifer A. Tate6, Kirsten Wolff7, Samuel A. Logan7, Jonathan F. Wendel1 and David A. Baum2,8* 1Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA, 50011, USA 2Department of Botany, University of Wisconsin Madison, WI, 53706, USA 3Current address: 7421 Allemande Way, Chattanooga, TN, 37421, USA 4 Department of Statistics, University of Wisconsin Madison, WI, 53706, USA 5Morris Arboretum of the University of Pennsylvania, 100 E. Northwestern Avenue, Philadelphia, PA, 19118, USA 6Institute of Fundamental Sciences, Massey University, Palmerston North 4442, New Zealand 7School of Natural and Environmental Sciences, Newcastle University, NE1 7RU, UK 8Wisconsin Institute for Discovery, 330 N Orchard St, Madison, WI 53715, USA †These authors contributed equally to this work. *Correspondence: [email protected] Special Issue: Polyploidy and Evolution Edited by:Yuxian Zhu, Wuhan University, China This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: [10.1111/jipb.12746] This article is protected by copyright. All rights reserved. Received: August 23, 2018; Accepted: November 18, 2018 1 Abstract Previous research suggests that Gossypium has undergone a 5- to 6-fold multiplication following its divergence from Theobroma. However, the number of events, or where they occurred in the Malvaceae phylogeny remains unknown. We analyzed transcriptomic and genomic data from representatives of eight of the nine Malvaceae subfamilies. Phylogenetic analysis of nuclear data placed Dombeya (Dombeyoideae) as sister to the rest of Malvadendrina clade, but the plastid DNA tree strongly supported Durio (Helicteroideae) in this position. Intraspecific Ks plots indicated that all sampled taxa, except Theobroma (Byttnerioideae), Corchorus (Grewioideae), and Dombeya (Dombeyoideae), have experienced whole genome multiplications (WGMs). Quartet analysis suggested WGMs were shared by Malvoideae-Bombacoideae and Sterculioideae-Tilioideae, but did not resolve whether these are shared with each other or Helicteroideae (Durio). Gene tree reconciliation and Bayesian concordance analysis suggested a complex history. Alternative hypotheses are suggested, each involving two independent autotetraploid and one allopolyploid event. They differ in that one entails an allopolyploid origin for the Durio lineage, whereas the other invokes an allopolyploid origin for Malvoideae-Bombacoideae. We highlight the need for more genomic information in the Malvaceae and improved methods to resolve complex evolutionary histories that may include allopolyploidy, incomplete lineage sorting, and variable rates of gene and genome evolution. INTRODUCTION An exciting revelation from the genomics revolution is the large number of ancient whole genome multiplication (WGM) events that punctuate angiosperm evolution, with many plant lineages experiencing multiple WGMs over their histories (Adams and Wendel 2005; Cui et al. 2006; Van de Peer et al. 2009; Wood et al. 2009; Jiao et al. 2011; Bowers et al. 2013; Soltis et al. 2015; Van de Peer et al. 2017). Polyploidy is frequently considered a source of evolutionary innovation (Stebbins 1947; Grant 1971) leading to increased species diversification and phenotypic innovation (Soltis and Soltis 2016). Thus, WGMs just prior to the radiation of such families as the Asteraceae, Brassicaceae, Fabaceae, Poaceae, and Solanaceae have been assigned a causal role in those clade’s species-richness (Paterson et al. 2004; Soltis et al. 2009; Cannon et al. 2015). 2 Despite the profound importance of WGMs in plant evolution, the identification and characterization of past events is often challenging. In particular, mechanisms such as rapid fractionation and rediploidization tend to remove evidence of the WGMs that precipitated them (Wendel 2015; Cheng et al. 2018). Maize, for example, was classically considered a pure diploid, but genomic research has since reclassified maize as a stabilized paleo-allotetraploid that rapidly jettisoned much of its duplicated genome (Gaut and Doebley 1997; Schnable et al. 2011; Zhao et al. 2017). Multiple methods have been developed to infer ancient WGMs, each leveraging different, though sometimes overlapping, lines of evidence. Early inferences were based on replicated intragenomic synteny, such as seen in maize (Wendel et al.1986; Helentjaris et al.1988; Gaut and Doebley 1997) and Arabidopsis (Vision et al. 2000). Soon after, synonymous substitution “peaks” in EST distance data among paralogs within a genome were used to infer WGMs (Schlueter et al. 2004). Since then, methods including gene tree/species tree reconciliation (Ness et al. 2011), collinearity of full genome sequences (Tang et al. 2010), and statistical methods based on gene counts (Rabier et al. 2013) have been combined to uncover many WGM events, some of them very old. Genomic evidence for WGM in the Malvaceae was first described in the publication of the Gossypium raimondii genome, where collinearity data supported an ancient 5- to 6-fold WGM sometime after its divergence from chocolate (Theobroma cacao), estimated at approximately 90 million years ago (Paterson