Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres

Andrew H. Paterson*, Jonathan F. Wendel, Heidrun Gundlach, Hui Guo, Jerry Jenkins, Dianchuan Jin, Danny Llewellyn, Kurtis C. Showmaker, Shengqiang Shu, Joshua Udall, Mi Jeong Yoo, Robert Byers, Wei Chen, Adi Doron-Faigenboim, Mary V. Duke, Lei Gong, Jane Grimwood, Corrinne Grover, Kara Grupp, Guanjing HuTae Ho Lee, Jingping Li, Lifeng Lin, Tao Liu, Barry S. Marler, Justin T. Page, Alison W. Roberts, Elisson Romanel, William S. Sanders, Emmanuel Szadkowski, Xu Tan, Haibao Tang, Chunming Xu, Jinpeng Wang, Zining Wang, Dong Zhang, Lan Zhang, Hamid Ashrafi, Frank Bedon, John E. Bowers, Curt L. Brubaker, Peng W. Chee, Sayan Das, Alan R. Gingle, Candace H. Haigler, David Harker, Lucia V. Hoffmann, Ran Hovav, Donald C. Jones, Cornelia Lemke, Shahid Mansoor, Mehboob Ur Rahman, Lisa N. Rainville, Aditi Rambani, Umesh K. Reddy, Jun Kang Rong, Yehoshua Saranga, Brian E. Scheffler, Jodi A. Scheffler, David M. Stelly, Barbara A. Triplett, Allen Van Deynze, Maite F.S. Vaslin, Vijay N. Waghmare, Sally A. Walford, Robert J. Wright, Essam A. Zaki, Tianzhen Zhang, Elizabeth S. Dennis, Klaus F.X. Mayer, Daniel G. Peterson, Daniel S. Rokhsar, Xiyin Wang, Jeremy Schmutz

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

961 Scopus citations

Abstract

Polyploidy often confers emergent properties, such as the higher fibre productivity and quality of tetraploid cottons than diploid cottons bred for the same environments. Here we show that an abrupt five-to sixfold ploidy increase approximately 60million years (Myr) ago, and allopolyploidy reuniting divergent Gossypium genomes approximately 1-2 Myr ago, 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 Brassica 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 A t D t (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.

Original languageAmerican English
Pages (from-to)423-427
Number of pages5
JournalNature
Volume492
Issue number7429
DOIs
StatePublished - 20 Dec 2012

Bibliographical note

Funding Information:
Acknowledgements The work, conducted by the US Department of Energy Joint Genome Institute, is supported by the Office of Science of the US Department of Energy under Contract no. DE-AC02-05CH11231. The authors appreciate financial support from the US National Science Foundation (DBI 98-72630 to A.H.P., J.F.W., A.R.G.; DBI 02-11700 to J.F.W., A.H.P., J.U., A.R.G.; DBI 02-08311, IIP-0917856; IIP-1127755 to A.H.P.; IOS 1025947 to C.H.H.), USDA (ARS-58-6402-7-241, 58-6402-1-644 and 58-6402-1-645 to D.G.P.; ARS 6402-21310-003-00 to B.E.S.; NRI 00-52100-9685 and 02-35301-12045 to A.H.P.), Bayer CropScience and The Consortium for Plant Biotechnology Research (A.H.P.), Cotton, Inc. (P.W.C., D.C.J., A.H.P., D.M.S., A.V.-D., J.F.W.), Georgia State Support Committee (P.W.C., A.H.P.), Texas State Support Committee (R.J.W.), Pakistan–US Science and Technology Cooperation Program (P.W.C., S.M., A.H.P., M.u.R.), US–Egypt Science and Technology Cooperation Program (A.H.P., E.A.Z.), Fulbright Scholar Program (S.M., E.A.Z.), Conselho Nacional de Desenvolvimento Científico e Tecnológico PDJ150690/2012-6 (E.R.), Fundação de Amparo a Pesquisa Pensa Rio E-26/110.324/2010 (M.F.S.V.), Texas AgriLife (D.M.S.), and Brigham Young University (BYU) Mentored Environment Grants (J.U.). RNA-seq reads were mapped by students on Marylou at the Fulton Supercomputer Center at BYU. We thank L. S. Dure III, G. O. Myers, J. McD Stewart, T. A. Wilkins and J. Zhu for co-endorsing the sequencing of G. raimondii by the US Department of Energy.

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