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Independent Domestication of Two Old World Cotton Species Jonathan F Ecology, Evolution and Organismal Biology Ecology, Evolution and Organismal Biology Publications 2016 Independent Domestication of Two Old World Cotton Species Jonathan F. Wendel Iowa State University, [email protected] Simon Renny-Byfield Iowa State University Justin T. Page Brigham Young University Joshua A. Udall Brigham Young University William S. Sanders Mississippi State University SeFoe nelloxtw pa thige fors aaddndition addal aitutionhorsal works at: http://lib.dr.iastate.edu/eeob_ag_pubs Part of the Agronomy and Crop Sciences Commons, Behavior and Ethology Commons, Plant Breeding and Genetics Commons, and the Population Biology Commons The ompc lete bibliographic information for this item can be found at http://lib.dr.iastate.edu/ eeob_ag_pubs/232. 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]. Independent Domestication of Two Old World Cotton Species Abstract Domesticated cotton species provide raw material for the majority of the world's textile industry. Two independent domestication events have been identified in allopolyploid cotton, one in Upland cotton ( Gossypium hirsutum L.) and the other to Egyptian cotton ( Gossypium barbadense L.). However, two diploid cotton species, Gossypium arboreum L. and Gossypium herbaceum L., have been cultivated for several millennia, but their status as independent domesticates has long been in question. Using genome resequencing data, we estimated the global abundance of various repetitive DNAs. We demonstrate that, despite negligible divergence in genome size, the two domesticated diploid cotton species contain different, but compensatory, repeat content and have thus experienced cryptic alterations in repeat abundance despite equivalence in genome size. Evidence of independent origin is bolstered by estimates of divergence times based on molecular evolutionary analysis of f7,000 orthologous genes, for which synonymous substitution rates suggest that G. arboreum and G. herbaceum last shared a common ancestor approximately 0.4–2.5 Ma. These data are incompatible with a shared domestication history during the emergence of agriculture and lead to the conclusion that G. arboreum and G. herbaceum were each domesticated independently. Keywords Gossypium, repetitive DNA, molecular evolution, genome size, crop plants Disciplines Agronomy and Crop Sciences | Behavior and Ethology | Ecology and Evolutionary Biology | Plant Breeding and Genetics | Population Biology Comments This article is published as Renny-Byfield, Simon, Justin T. Page, Joshua A. Udall, William S. Sanders, Daniel G. Peterson, Mark A. Arick, Corrinne E. Grover, and Jonathan F. Wendel. "Independent domestication of two Old World cotton species." Genome biology and evolution 8, no. 6 (2016): 1940-1947. 10.1093/gbe/ evw129. Posted with permission. Creative Commons License This work is licensed under a Creative Commons Attribution-Noncommercial 4.0 License Authors Jonathan F. Wendel, Simon Renny-Byfield, Justin T. Page, Joshua A. Udall, William S. Sanders, Daniel G. Peterson, Mark A. Arick II, and Corrinne E. Grover This article is available at Iowa State University Digital Repository: http://lib.dr.iastate.edu/eeob_ag_pubs/232 GBE Independent Domestication of Two Old World Cotton Species Simon Renny-Byfield1,6,7,JustinT.Page2, Joshua A. Udall2, William S. Sanders3,4, Daniel G. Peterson3,5, Mark A. Arick II3,CorrinneE.Grover1, and Jonathan F. Wendel1,* 1Department of Ecology, Evolution and Organismal Biology, Iowa State University 2Plant and Wildlife Science Department, Brigham Young University 3Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University 4Department of Computer Science and Engineering, Mississippi State University 5Department of Plant and Soil Sciences, Mississippi State University 6DuPont Pioneer, Johnston, IA 7Present address: Department of Plant Sciences, University of California, Davis, CA *Corresponding author: E-mail: [email protected]. Accepted: May 26, 2016 Data deposition: The data used in this study have been previously published and data deposition to the NCBI SRA is detailed in the relevant references and in the supplementary file S1. Abstract Domesticated cotton species provide raw material for the majority of the world’s textile industry. Two independent domestication events have been identified in allopolyploid cotton, one in Upland cotton (Gossypium hirsutum L.) and the other to Egyptian cotton (Gossypium barbadense L.). However, two diploid cotton species, Gossypium arboreum L. and Gossypium herbaceum L., have been cultivated for several millennia, but their status as independent domesticates has long been in question. Using genome resequencing data, we estimated the global abundance of various repetitive DNAs. We demonstrate that, despite negligible divergence in genome size, the two domesticated diploid cotton species contain different, but compensatory, repeat content and have thus experienced cryptic alterations in repeat abundance despite equivalence in genome size. Evidence of independent origin is bolstered by estimates of divergence times based on molecular evolutionary analysis of f7,000 orthologous genes, for which synonymous substitution rates suggest that G. arboreum and G. herbaceum last shared a common ancestor approximately 0.4–2.5 Ma. These data are incompatible with a shared domestication history during the emergence of agriculture and lead to the conclusion that G. arboreum and G. herbaceum were each domesticated independently. Key words: Gossypium, repetitive DNA, molecular evolution, genome size, crop plants. Introduction possible introgression between crops and wild relatives, culti- Understanding the origins of crop plants and their relation- vation far outside the native range, and rarity or extinction of ships to wild relatives have long been central concerns of plant wild ancestors. Accordingly, the wild ancestors and germ- biologists. This historical interest, stimulated by the impor- plasm relationships of some of our major crop species have tance of this understanding to crop plant improvement, remained obscure. traces to before the landmark volumes by de Candolle A case in point concerns the two Old World cultivated (1883) and Darwin (1868) and remains an area of active re- cotton species, Gossypium arboreum and Gossypium herba- search today (Abbo et al. 2012; Hancock 2012; Meyer and ceum (fig. 1). Both species have an ancient history of cultiva- Purugganan 2013; Olsen and Wendel 2013). A major chal- tion, extending back perhaps 5,000 years or more lenge in the study of crop plants has been determining the (Chowdhury and Buth 1971). This antiquity of original domes- wild ancestors of domesticated species. This difficulty reflects tication followed by human-mediated dispersal over vast geo- multiple processes, including the often dramatic morphologi- graphic ranges, extending from Africa through the Levant and cal transformation between progenitor and derivative, Indian subcontinent into the Far East, has generated extensive ß The Author(s) 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 1940 Genome Biol. Evol. 8(7):1940–1947. doi:10.1093/gbe/evw129 Advance Access publication June 11, 2016 Downloaded from https://academic.oup.com/gbe/article-abstract/8/6/1940/2574112 by Iowa State University user on 05 December 2017 Independent Domestication of Two Old World Species GBE and their relationships to each other are unclear. Two oppos- ing views have been forwarded, one that stresses the overall similarity of the two species and a second that emphasizes their differences. Hutchinson, a proponent of the first view, proposed G. herbaceum subsp. africanum as a model of the ancestor of both species (Hutchinson and Ghose 1937; Hutchinson 1954; Fryxell 1978).AccordingtoHutchinson’s hypothesis, G. arboreum arose from G. herbaceum early in the history of diploid cotton cultivation, suggesting one culti- vated cotton species arose from another. An alternative hy- pothesis is that G. arboreum and G. herbaceum diverged prior to domestication. Fryxell (1978) and Wendel et al. (1989) among others argue that genetic differences between the two species are too great to have arisen during the relatively FIG.1.—Morphological differences between fiber from wild and do- brief period in which domesticated cottons have existed. Thus, mesticated A-genome diploid cotton species. Shown are single seeds with single celled trichomes (fiber) from two cotton species, Gossypium herba- according to this view, cultivated Old World cottons originated ceum and Gossypium arboreum. Gossypium arboreum exists only as a from at least two independent domestication events from two cultigen. different wild progenitor species. The purpose of this study was
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