2012•NatureOpen access
Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres
Andrew H. Paterson, Jonathan F. Wendel, Heidrun Gundlach, Hui Guo, Jerry W. Jenkins, Dianchuan Jin, Danny J Llewellyn, Kurt C. Showmaker, Shengqiang Shu, Joshua A. Udall, Mi‐Jeong Yoo, Robert Byers, Wei Chen, Adi Doron‐Faigenboim, Mary V. Duke, Lei Gong, Jane Grimwood, Corrinne E. Grover, Kara Grupp, Guanjing Hu, Tae‐Ho Lee, Jingping Li, Lifeng Lin, Tao Liu, Barry S. Marler, Justin T. Page, Alison W. Roberts, Elisson Antonio da Costa Romanel, William S. Sanders, Emmanuel Szadkowski, Xu Tan, Haibao Tang, Chunming Xu, Jinpeng Wang, Zining Wang, Dong Xiang Zhang, Lan Zhang, Hamid Ashrafi, Frank Bedon, John Bowers, Curt L. Brubaker, Peng Wah Chee, Sayan Das, Alan R. Gingle, Candace H. Haigler, David B. Harker, Lúcia Vieira Hoffmann, Ran Hovav, Donald C. Jones, Cornelia Lemke, Shahid Mansoor, Mehboob‐ur‐ Rahman, Lisa K. Rainville, Aditi Rambani, Umesh K. Reddy, Junkang Rong, Yehoshua Saranga, Brian E. Scheffler, Jodi Scheffler, David M. Stelly, Barbara A. Triplett, Allen Van Deynze, Maité F. S. Vaslin, Vijay Namdeo Waghmare, Sally A. Walford, Robert Wright, Essam A. Zaki, Tianzhen Zhang, Elizabeth S. Dennis, Klaus Mayer, Daniel Gunnar Peterson, Daniel S. Rokhsar, Xiyin Wang, Jeremy Schmutz
Abstract
The Gossypium genus is used to investigate emergent consequences of polyploidy in cotton species; comparative genomic analyses reveal a complex evolutionary history including interactions among subgenomes that result in genetic novelty in elite cottons and provide insight into the evolution of spinnable fibres. A phylogenetic and genomic study of plants of the cotton genus Gossypium provides insights into the role of polyploidy in the angiosperm evolution, and specifically, in the emergence of spinnable fibres in domesticated cottons. The authors show that an abrupt five- to sixfold ploidy increase about 60 million years ago, and allopolyploidy reuniting divergent genomes approximately 1–2 million years ago, conferred a roughly 30-fold duplication of ancestral flowering plant genes in the 'elite' cottons G. hirsutum and G. barbadense compared to their presumed progenitor G. raimondii. Polyploidy often confers emergent properties, such as the higher fibre productivity and quality of tetraploid cottons than diploid cottons bred for the same environments1. Here we show that an abrupt five- to sixfold ploidy increase approximately 60 million years (Myr) ago, and allopolyploidy reuniting divergent Gossypium genomes approximately 1–2 Myr ago2, conferred about 30–36-fold duplication of ancestral angiosperm (flowering plant) genes in elite cottons (Gossypium hirsutum and Gossypium barbadense), genetic complexity equalled only by Brassica3 among sequenced angiosperms. Nascent fibre evolution, before allopolyploidy, is elucidated by comparison of spinnable-fibred Gossypium herbaceum A and non-spinnable Gossypium longicalyx F genomes to one another and the outgroup D genome of non-spinnable Gossypium raimondii. The sequence of a G. hirsutum AtDt (in which ‘t’ indicates tetraploid) cultivar reveals many non-reciprocal DNA exchanges between subgenomes that may have contributed to phenotypic innovation and/or other emergent properties such as ecological adaptation by polyploids. Most DNA-level novelty in G. hirsutum recombines alleles from the D-genome progenitor native to its New World habitat and the Old World A-genome progenitor in which spinnable fibre evolved. Coordinated expression changes in proximal groups of functionally distinct genes, including a nuclear mitochondrial DNA block, may account for clusters of cotton-fibre quantitative trait loci affecting diverse traits. Opportunities abound for dissecting emergent properties of other polyploids, particularly angiosperms, by comparison to diploid progenitors and outgroups.