Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement

Polyploidy is an evolutionary innovation for many animals and all flowering plants, but its impact on selection and domestication remains elusive. Here we analyze genome evolution and diversification for all five allopolyploid cotton species, including economically important Upland and Pima cottons....

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Veröffentlicht in:Nature genetics 2020-05, Vol.52 (5), p.525-533
Hauptverfasser: Chen, Z. Jeffrey, Sreedasyam, Avinash, Ando, Atsumi, Song, Qingxin, De Santiago, Luis M., Hulse-Kemp, Amanda M., Ding, Mingquan, Ye, Wenxue, Kirkbride, Ryan C., Jenkins, Jerry, Plott, Christopher, Lovell, John, Lin, Yu-Ming, Vaughn, Robert, Liu, Bo, Simpson, Sheron, Scheffler, Brian E., Wen, Li, Saski, Christopher A., Grover, Corrinne E., Hu, Guanjing, Conover, Justin L., Carlson, Joseph W., Shu, Shengqiang, Boston, Lori B., Williams, Melissa, Peterson, Daniel G., McGee, Keith, Jones, Don C., Wendel, Jonathan F., Stelly, David M., Grimwood, Jane, Schmutz, Jeremy
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container_issue 5
container_start_page 525
container_title Nature genetics
container_volume 52
creator Chen, Z. Jeffrey
Sreedasyam, Avinash
Ando, Atsumi
Song, Qingxin
De Santiago, Luis M.
Hulse-Kemp, Amanda M.
Ding, Mingquan
Ye, Wenxue
Kirkbride, Ryan C.
Jenkins, Jerry
Plott, Christopher
Lovell, John
Lin, Yu-Ming
Vaughn, Robert
Liu, Bo
Simpson, Sheron
Scheffler, Brian E.
Wen, Li
Saski, Christopher A.
Grover, Corrinne E.
Hu, Guanjing
Conover, Justin L.
Carlson, Joseph W.
Shu, Shengqiang
Boston, Lori B.
Williams, Melissa
Peterson, Daniel G.
McGee, Keith
Jones, Don C.
Wendel, Jonathan F.
Stelly, David M.
Grimwood, Jane
Schmutz, Jeremy
description Polyploidy is an evolutionary innovation for many animals and all flowering plants, but its impact on selection and domestication remains elusive. Here we analyze genome evolution and diversification for all five allopolyploid cotton species, including economically important Upland and Pima cottons. Although these polyploid genomes are conserved in gene content and synteny, they have diversified by subgenomic transposon exchanges that equilibrate genome size, evolutionary rate heterogeneities and positive selection between homoeologs within and among lineages. These differential evolutionary trajectories are accompanied by gene-family diversification and homoeolog expression divergence among polyploid lineages. Selection and domestication drive parallel gene expression similarities in fibers of two cultivated cottons, involving coexpression networks and N 6 -methyladenosine RNA modifications. Furthermore, polyploidy induces recombination suppression, which correlates with altered epigenetic landscapes and can be overcome by wild introgression. These genomic insights will empower efforts to manipulate genetic recombination and modify epigenetic landscapes and target genes for crop improvement. Sequencing and genomic diversification of five allopolyploid cotton species provide insights into polyploid genome evolution and epigenetic landscapes for cotton improvement.
doi_str_mv 10.1038/s41588-020-0614-5
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Jeffrey ; Sreedasyam, Avinash ; Ando, Atsumi ; Song, Qingxin ; De Santiago, Luis M. ; Hulse-Kemp, Amanda M. ; Ding, Mingquan ; Ye, Wenxue ; Kirkbride, Ryan C. ; Jenkins, Jerry ; Plott, Christopher ; Lovell, John ; Lin, Yu-Ming ; Vaughn, Robert ; Liu, Bo ; Simpson, Sheron ; Scheffler, Brian E. ; Wen, Li ; Saski, Christopher A. ; Grover, Corrinne E. ; Hu, Guanjing ; Conover, Justin L. ; Carlson, Joseph W. ; Shu, Shengqiang ; Boston, Lori B. ; Williams, Melissa ; Peterson, Daniel G. ; McGee, Keith ; Jones, Don C. ; Wendel, Jonathan F. ; Stelly, David M. ; Grimwood, Jane ; Schmutz, Jeremy</creator><creatorcontrib>Chen, Z. 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Here we analyze genome evolution and diversification for all five allopolyploid cotton species, including economically important Upland and Pima cottons. Although these polyploid genomes are conserved in gene content and synteny, they have diversified by subgenomic transposon exchanges that equilibrate genome size, evolutionary rate heterogeneities and positive selection between homoeologs within and among lineages. These differential evolutionary trajectories are accompanied by gene-family diversification and homoeolog expression divergence among polyploid lineages. Selection and domestication drive parallel gene expression similarities in fibers of two cultivated cottons, involving coexpression networks and N 6 -methyladenosine RNA modifications. Furthermore, polyploidy induces recombination suppression, which correlates with altered epigenetic landscapes and can be overcome by wild introgression. These genomic insights will empower efforts to manipulate genetic recombination and modify epigenetic landscapes and target genes for crop improvement. Sequencing and genomic diversification of five allopolyploid cotton species provide insights into polyploid genome evolution and epigenetic landscapes for cotton improvement.</description><subject>631/114/2184</subject><subject>631/208/177</subject><subject>631/208/212/2302</subject><subject>631/208/2491/1559</subject><subject>631/449/711</subject><subject>Agriculture</subject><subject>Analysis</subject><subject>Animal Genetics and Genomics</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Biological evolution</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Cancer Research</subject><subject>Cotton</subject><subject>Cotton Fiber</subject><subject>Crop improvement</subject><subject>Datasets</subject><subject>Divergence</subject><subject>Domestication</subject><subject>Economic importance</subject><subject>Epigenetic inheritance</subject><subject>Epigenetics</subject><subject>Epigenomics</subject><subject>Epigenomics - methods</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Flowering</subject><subject>Flowering plants</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant - genetics</subject><subject>Gene Function</subject><subject>Genes</subject><subject>Genetic engineering</subject><subject>Genome assembly algorithms</subject><subject>Genome, Plant - genetics</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Genomics - methods</subject><subject>Gossypium - genetics</subject><subject>Human Genetics</subject><subject>Innovations</subject><subject>N6-methyladenosine</subject><subject>Phylogeny</subject><subject>Plant breeding</subject><subject>Plant hybridization</subject><subject>Plants (botany)</subject><subject>Polyploidy</subject><subject>Positive selection</subject><subject>Recombination</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Sequence annotation</subject><subject>Synteny</subject><subject>Textile industry</subject><subject>Transposons</subject><issn>1061-4036</issn><issn>1546-1718</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNqNkl1rFDEUhgdRbK3-AG8k6E29mJrvmbkRSqlroVDw6zZkMye7KTPJmGQW99-bZWvrioLk4oRznvOecPJW1UuCzwhm7bvEiWjbGlNcY0l4LR5Vx0RwWZOGtI_LvWRrjpk8qp6ldIsx4Ry3T6sjRhlhlDfH1WoBPozOoN5tICZnndHZBZ9QsMiWHFqElLaTm0ekhyFMYdhOQ3A9ShMYBwlp36O8BheRGydtMgoemZBzCSURwwZG8Pl59cTqIcGLu3hSff1w-eXiY319s7i6OL-ujWQ015zrnllCuBBacy6FZaTRLZVLIUTHrQFtGrAM-FJaIjXTRFDaGSYpplL27KR6v9ed5uUIvSmjox7UFN2o41YF7dRhxbu1WoWNaihmmNAi8HovEFJ2KhmXwaxN8B5MVkSSToi2QKd3U2L4PkPKanTJwDBoD2FOirKOYdY03U7vzR_obZijLztQlGPSth1u2AO10gMo520ojzM7UXUuKcOcckEKdfYXqpweyhcGD9aV_EHD24OGwmT4kVd6Tkldff70_-zNt0OW7FkTizsi2PsFE6x21lR7a6piTbWzphKl59XvP3Pf8cuLBaB7IJWSX0F82NS_VX8C1MzsUg</recordid><startdate>20200501</startdate><enddate>20200501</enddate><creator>Chen, Z. 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Jeffrey ; Sreedasyam, Avinash ; Ando, Atsumi ; Song, Qingxin ; De Santiago, Luis M. ; Hulse-Kemp, Amanda M. ; Ding, Mingquan ; Ye, Wenxue ; Kirkbride, Ryan C. ; Jenkins, Jerry ; Plott, Christopher ; Lovell, John ; Lin, Yu-Ming ; Vaughn, Robert ; Liu, Bo ; Simpson, Sheron ; Scheffler, Brian E. ; Wen, Li ; Saski, Christopher A. ; Grover, Corrinne E. ; Hu, Guanjing ; Conover, Justin L. ; Carlson, Joseph W. ; Shu, Shengqiang ; Boston, Lori B. ; Williams, Melissa ; Peterson, Daniel G. ; McGee, Keith ; Jones, Don C. ; Wendel, Jonathan F. ; Stelly, David M. ; Grimwood, Jane ; Schmutz, Jeremy</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c632t-44ad3f11455aa4465f317a826b55594fceac7ef3e4b6f16a3a15229c3620266d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>631/114/2184</topic><topic>631/208/177</topic><topic>631/208/212/2302</topic><topic>631/208/2491/1559</topic><topic>631/449/711</topic><topic>Agriculture</topic><topic>Analysis</topic><topic>Animal Genetics and Genomics</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Biological evolution</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Cancer Research</topic><topic>Cotton</topic><topic>Cotton Fiber</topic><topic>Crop improvement</topic><topic>Datasets</topic><topic>Divergence</topic><topic>Domestication</topic><topic>Economic importance</topic><topic>Epigenetic inheritance</topic><topic>Epigenetics</topic><topic>Epigenomics</topic><topic>Epigenomics - methods</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>Flowering</topic><topic>Flowering plants</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant - genetics</topic><topic>Gene Function</topic><topic>Genes</topic><topic>Genetic engineering</topic><topic>Genome assembly algorithms</topic><topic>Genome, Plant - genetics</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Genomics - methods</topic><topic>Gossypium - genetics</topic><topic>Human Genetics</topic><topic>Innovations</topic><topic>N6-methyladenosine</topic><topic>Phylogeny</topic><topic>Plant breeding</topic><topic>Plant hybridization</topic><topic>Plants (botany)</topic><topic>Polyploidy</topic><topic>Positive selection</topic><topic>Recombination</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Sequence annotation</topic><topic>Synteny</topic><topic>Textile industry</topic><topic>Transposons</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Z. Jeffrey</creatorcontrib><creatorcontrib>Sreedasyam, Avinash</creatorcontrib><creatorcontrib>Ando, Atsumi</creatorcontrib><creatorcontrib>Song, Qingxin</creatorcontrib><creatorcontrib>De Santiago, Luis M.</creatorcontrib><creatorcontrib>Hulse-Kemp, Amanda M.</creatorcontrib><creatorcontrib>Ding, Mingquan</creatorcontrib><creatorcontrib>Ye, Wenxue</creatorcontrib><creatorcontrib>Kirkbride, Ryan C.</creatorcontrib><creatorcontrib>Jenkins, Jerry</creatorcontrib><creatorcontrib>Plott, Christopher</creatorcontrib><creatorcontrib>Lovell, John</creatorcontrib><creatorcontrib>Lin, Yu-Ming</creatorcontrib><creatorcontrib>Vaughn, Robert</creatorcontrib><creatorcontrib>Liu, Bo</creatorcontrib><creatorcontrib>Simpson, Sheron</creatorcontrib><creatorcontrib>Scheffler, Brian E.</creatorcontrib><creatorcontrib>Wen, Li</creatorcontrib><creatorcontrib>Saski, Christopher A.</creatorcontrib><creatorcontrib>Grover, Corrinne E.</creatorcontrib><creatorcontrib>Hu, Guanjing</creatorcontrib><creatorcontrib>Conover, Justin L.</creatorcontrib><creatorcontrib>Carlson, Joseph W.</creatorcontrib><creatorcontrib>Shu, Shengqiang</creatorcontrib><creatorcontrib>Boston, Lori B.</creatorcontrib><creatorcontrib>Williams, Melissa</creatorcontrib><creatorcontrib>Peterson, Daniel G.</creatorcontrib><creatorcontrib>McGee, Keith</creatorcontrib><creatorcontrib>Jones, Don C.</creatorcontrib><creatorcontrib>Wendel, Jonathan F.</creatorcontrib><creatorcontrib>Stelly, David M.</creatorcontrib><creatorcontrib>Grimwood, Jane</creatorcontrib><creatorcontrib>Schmutz, Jeremy</creatorcontrib><creatorcontrib>USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium &amp; 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Jeffrey</au><au>Sreedasyam, Avinash</au><au>Ando, Atsumi</au><au>Song, Qingxin</au><au>De Santiago, Luis M.</au><au>Hulse-Kemp, Amanda M.</au><au>Ding, Mingquan</au><au>Ye, Wenxue</au><au>Kirkbride, Ryan C.</au><au>Jenkins, Jerry</au><au>Plott, Christopher</au><au>Lovell, John</au><au>Lin, Yu-Ming</au><au>Vaughn, Robert</au><au>Liu, Bo</au><au>Simpson, Sheron</au><au>Scheffler, Brian E.</au><au>Wen, Li</au><au>Saski, Christopher A.</au><au>Grover, Corrinne E.</au><au>Hu, Guanjing</au><au>Conover, Justin L.</au><au>Carlson, Joseph W.</au><au>Shu, Shengqiang</au><au>Boston, Lori B.</au><au>Williams, Melissa</au><au>Peterson, Daniel G.</au><au>McGee, Keith</au><au>Jones, Don C.</au><au>Wendel, Jonathan F.</au><au>Stelly, David M.</au><au>Grimwood, Jane</au><au>Schmutz, Jeremy</au><aucorp>USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement</atitle><jtitle>Nature genetics</jtitle><stitle>Nat Genet</stitle><addtitle>Nat Genet</addtitle><date>2020-05-01</date><risdate>2020</risdate><volume>52</volume><issue>5</issue><spage>525</spage><epage>533</epage><pages>525-533</pages><issn>1061-4036</issn><eissn>1546-1718</eissn><abstract>Polyploidy is an evolutionary innovation for many animals and all flowering plants, but its impact on selection and domestication remains elusive. Here we analyze genome evolution and diversification for all five allopolyploid cotton species, including economically important Upland and Pima cottons. Although these polyploid genomes are conserved in gene content and synteny, they have diversified by subgenomic transposon exchanges that equilibrate genome size, evolutionary rate heterogeneities and positive selection between homoeologs within and among lineages. These differential evolutionary trajectories are accompanied by gene-family diversification and homoeolog expression divergence among polyploid lineages. Selection and domestication drive parallel gene expression similarities in fibers of two cultivated cottons, involving coexpression networks and N 6 -methyladenosine RNA modifications. Furthermore, polyploidy induces recombination suppression, which correlates with altered epigenetic landscapes and can be overcome by wild introgression. These genomic insights will empower efforts to manipulate genetic recombination and modify epigenetic landscapes and target genes for crop improvement. Sequencing and genomic diversification of five allopolyploid cotton species provide insights into polyploid genome evolution and epigenetic landscapes for cotton improvement.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>32313247</pmid><doi>10.1038/s41588-020-0614-5</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0001-8552-7394</orcidid><orcidid>https://orcid.org/0000-0002-3468-4119</orcidid><orcidid>https://orcid.org/0000-0002-4336-8994</orcidid><orcidid>https://orcid.org/0000-0002-3796-4829</orcidid><orcidid>https://orcid.org/0000-0002-7943-3997</orcidid><orcidid>https://orcid.org/0000-0002-3558-6000</orcidid><orcidid>https://orcid.org/0000-0001-9523-259X</orcidid><orcidid>https://orcid.org/0000-0003-1968-8952</orcidid><orcidid>https://orcid.org/0000-0002-8356-8325</orcidid><orcidid>https://orcid.org/0000-0003-2258-5081</orcidid><orcidid>https://orcid.org/0000-0001-5006-8036</orcidid><orcidid>https://orcid.org/0000-0003-3878-5459</orcidid><orcidid>https://orcid.org/0000-0001-7336-7012</orcidid><orcidid>https://orcid.org/0000000338785459</orcidid><orcidid>https://orcid.org/0000000185527394</orcidid><orcidid>https://orcid.org/0000000319688952</orcidid><orcidid>https://orcid.org/000000019523259X</orcidid><orcidid>https://orcid.org/0000000234684119</orcidid><orcidid>https://orcid.org/0000000243368994</orcidid><orcidid>https://orcid.org/0000000150068036</orcidid><orcidid>https://orcid.org/0000000279433997</orcidid><orcidid>https://orcid.org/0000000237964829</orcidid><orcidid>https://orcid.org/0000000173367012</orcidid><orcidid>https://orcid.org/0000000322585081</orcidid><orcidid>https://orcid.org/0000000235586000</orcidid><orcidid>https://orcid.org/0000000283568325</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1061-4036
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issn 1061-4036
1546-1718
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7203012
source MEDLINE; Nature; SpringerNature Journals
subjects 631/114/2184
631/208/177
631/208/212/2302
631/208/2491/1559
631/449/711
Agriculture
Analysis
Animal Genetics and Genomics
BASIC BIOLOGICAL SCIENCES
Biological evolution
Biomedical and Life Sciences
Biomedicine
Cancer Research
Cotton
Cotton Fiber
Crop improvement
Datasets
Divergence
Domestication
Economic importance
Epigenetic inheritance
Epigenetics
Epigenomics
Epigenomics - methods
Evolution
Evolution, Molecular
Flowering
Flowering plants
Gene expression
Gene Expression Regulation, Plant - genetics
Gene Function
Genes
Genetic engineering
Genome assembly algorithms
Genome, Plant - genetics
Genomes
Genomics
Genomics - methods
Gossypium - genetics
Human Genetics
Innovations
N6-methyladenosine
Phylogeny
Plant breeding
Plant hybridization
Plants (botany)
Polyploidy
Positive selection
Recombination
Ribonucleic acid
RNA
Sequence annotation
Synteny
Textile industry
Transposons
title Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement
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