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 Hu; Tae 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

doi:10.1038/nature11798

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

Publikation: Beitrag in Fachzeitschrift › Artikel › Begutachtung

1000 Zitate (Scopus)

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.

Originalsprache	Englisch
Seiten (von - bis)	423-427
Seitenumfang	5
Fachzeitschrift	Nature
Jahrgang	492
Ausgabenummer	7429
DOIs	https://doi.org/10.1038/nature11798
Publikationsstatus	Veröffentlicht - 20 Dez. 2012
Extern publiziert	Ja

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Paterson, A. H., Wendel, J. F., Gundlach, H., Guo, H., Jenkins, J., Jin, D., Llewellyn, D., Showmaker, K. C., Shu, S., Udall, J., Yoo, M. J., Byers, R., Chen, W., Doron-Faigenboim, A., Duke, M. V., Gong, L., Grimwood, J., Grover, C., Grupp, K., ... Schmutz, J. (2012). Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature, 492(7429), 423-427. https://doi.org/10.1038/nature11798

@article{0b76f8d119c945168f9f8d7f2ee2e80a,

title = "Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres",

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.",

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

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 Cient{\'i}fico e Tecnol{\'o}gico PDJ150690/2012-6 (E.R.), Funda{\c c}{\~a}o 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.",

year = "2012",

month = dec,

day = "20",

doi = "10.1038/nature11798",

language = "English",

volume = "492",

pages = "423--427",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Research",

number = "7429",

}

Paterson, AH, Wendel, JF, Gundlach, H, Guo, H, Jenkins, J, Jin, D, Llewellyn, D, Showmaker, KC, Shu, S, Udall, J, Yoo, MJ, Byers, R, Chen, W, Doron-Faigenboim, A, Duke, MV, Gong, L, Grimwood, J, Grover, C, Grupp, K, Hu, G, Lee, TH, Li, J, Lin, L, Liu, T, Marler, BS, Page, JT, Roberts, AW, Romanel, E, Sanders, WS, Szadkowski, E, Tan, X, Tang, H, Xu, C, Wang, J, Wang, Z, Zhang, D, Zhang, L, Ashrafi, H, Bedon, F, Bowers, JE, Brubaker, CL, Chee, PW, Das, S, Gingle, AR, Haigler, CH, Harker, D, Hoffmann, LV, Hovav, R, Jones, DC, Lemke, C, Mansoor, S, Rahman, MU, Rainville, LN, Rambani, A, Reddy, UK, Rong, JK, Saranga, Y, Scheffler, BE, Scheffler, JA, Stelly, DM, Triplett, BA, Van Deynze, A, Vaslin, MFS, Waghmare, VN, Walford, SA, Wright, RJ, Zaki, EA, Zhang, T, Dennis, ES, Mayer, KFX, Peterson, DG, Rokhsar, DS, Wang, X & Schmutz, J 2012, 'Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres', Nature, Jg. 492, Nr. 7429, S. 423-427. https://doi.org/10.1038/nature11798

TY - JOUR

T1 - Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres

AU - Paterson, Andrew H.

AU - Wendel, Jonathan F.

AU - Gundlach, Heidrun

AU - Guo, Hui

AU - Jenkins, Jerry

AU - Jin, Dianchuan

AU - Llewellyn, Danny

AU - Showmaker, Kurtis C.

AU - Shu, Shengqiang

AU - Udall, Joshua

AU - Yoo, Mi Jeong

AU - Byers, Robert

AU - Chen, Wei

AU - Doron-Faigenboim, Adi

AU - Duke, Mary V.

AU - Gong, Lei

AU - Grimwood, Jane

AU - Grover, Corrinne

AU - Grupp, Kara

AU - Hu, Guanjing

AU - Lee, Tae Ho

AU - Li, Jingping

AU - Lin, Lifeng

AU - Liu, Tao

AU - Marler, Barry S.

AU - Page, Justin T.

AU - Roberts, Alison W.

AU - Romanel, Elisson

AU - Sanders, William S.

AU - Szadkowski, Emmanuel

AU - Tan, Xu

AU - Tang, Haibao

AU - Xu, Chunming

AU - Wang, Jinpeng

AU - Wang, Zining

AU - Zhang, Dong

AU - Zhang, Lan

AU - Ashrafi, Hamid

AU - Bedon, Frank

AU - Bowers, John E.

AU - Brubaker, Curt L.

AU - Chee, Peng W.

AU - Das, Sayan

AU - Gingle, Alan R.

AU - Haigler, Candace H.

AU - Harker, David

AU - Hoffmann, Lucia V.

AU - Hovav, Ran

AU - Jones, Donald C.

AU - Lemke, Cornelia

AU - Mansoor, Shahid

AU - Rahman, Mehboob Ur

AU - Rainville, Lisa N.

AU - Rambani, Aditi

AU - Reddy, Umesh K.

AU - Rong, Jun Kang

AU - Saranga, Yehoshua

AU - Scheffler, Brian E.

AU - Scheffler, Jodi A.

AU - Stelly, David M.

AU - Triplett, Barbara A.

AU - Van Deynze, Allen

AU - Vaslin, Maite F.S.

AU - Waghmare, Vijay N.

AU - Walford, Sally A.

AU - Wright, Robert J.

AU - Zaki, Essam A.

AU - Zhang, Tianzhen

AU - Dennis, Elizabeth S.

AU - Mayer, Klaus F.X.

AU - Peterson, Daniel G.

AU - Rokhsar, Daniel S.

AU - Wang, Xiyin

AU - Schmutz, Jeremy

N1 - 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.

PY - 2012/12/20

Y1 - 2012/12/20

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84871428041&partnerID=8YFLogxK

U2 - 10.1038/nature11798

DO - 10.1038/nature11798

M3 - Article

C2 - 23257886

AN - SCOPUS:84871428041

SN - 0028-0836

VL - 492

SP - 423

EP - 427

JO - Nature

JF - Nature

IS - 7429

ER -

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

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