Dynamic Roles for Small RNAs and DNA Methylation during Ovule and Fiber Development in Allotetraploid Cotton
DNA methylation is essential for plant and animal development. In plants, methylation occurs at CG, CHG, and CHH (H = A, C or T) sites via distinct pathways. Cotton is an allotetraploid consisting of two progenitor genomes. Each cotton fiber is a rapidly-elongating cell derived from the ovule epider...
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| description | DNA methylation is essential for plant and animal development. In plants, methylation occurs at CG, CHG, and CHH (H = A, C or T) sites via distinct pathways. Cotton is an allotetraploid consisting of two progenitor genomes. Each cotton fiber is a rapidly-elongating cell derived from the ovule epidermis, but the molecular basis for this developmental transition is unknown. Here we analyzed methylome, transcriptome, and small RNAome and revealed distinct changes in CHH methylation during ovule and fiber development. In ovules, CHH hypermethylation in promoters correlated positively with siRNAs, inducing RNA-dependent DNA methylation (RdDM), and up-regulation of ovule-preferred genes. In fibers, the ovule-derived cells generated additional heterochromatic CHH hypermethylation independent of RdDM, which repressed transposable elements (TEs) and nearby genes including fiber-related genes. Furthermore, CHG and CHH methylation in genic regions contributed to homoeolog expression bias in ovules and fibers. Inhibiting DNA methylation using 5-aza-2'-deoxycytidine in cultured ovules has reduced fiber cell number and length, suggesting a potential role for DNA methylation in fiber development. Thus, RdDM-dependent methylation in promoters and RdDM-independent methylation in TEs and nearby genes could act as a double-lock feedback mechanism to mediate gene and TE expression, potentiating the transition from epidermal to fiber cells during ovule and seed development. |
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In plants, methylation occurs at CG, CHG, and CHH (H = A, C or T) sites via distinct pathways. Cotton is an allotetraploid consisting of two progenitor genomes. Each cotton fiber is a rapidly-elongating cell derived from the ovule epidermis, but the molecular basis for this developmental transition is unknown. Here we analyzed methylome, transcriptome, and small RNAome and revealed distinct changes in CHH methylation during ovule and fiber development. In ovules, CHH hypermethylation in promoters correlated positively with siRNAs, inducing RNA-dependent DNA methylation (RdDM), and up-regulation of ovule-preferred genes. In fibers, the ovule-derived cells generated additional heterochromatic CHH hypermethylation independent of RdDM, which repressed transposable elements (TEs) and nearby genes including fiber-related genes. Furthermore, CHG and CHH methylation in genic regions contributed to homoeolog expression bias in ovules and fibers. Inhibiting DNA methylation using 5-aza-2'-deoxycytidine in cultured ovules has reduced fiber cell number and length, suggesting a potential role for DNA methylation in fiber development. Thus, RdDM-dependent methylation in promoters and RdDM-independent methylation in TEs and nearby genes could act as a double-lock feedback mechanism to mediate gene and TE expression, potentiating the transition from epidermal to fiber cells during ovule and seed development.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1005724</identifier><identifier>PMID: 26710171</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Bias ; Cotton ; Deoxyribonucleic acid ; Development ; DNA ; DNA Methylation ; DNA sequencing ; Epigenesis, Genetic ; Epigenetics ; Gene expression ; Gene Expression Regulation, Developmental ; Gene Expression Regulation, Plant ; Genes, Plant ; Genomes ; Gossypium - genetics ; Gossypium - growth & development ; Methods ; Methylation ; MicroRNAs - genetics ; Nucleotide sequencing ; Observations ; Ovule - genetics ; Ovule - growth & development ; Plant Vascular Bundle - genetics ; Plant Vascular Bundle - growth & development ; Plants ; Promoter Regions, Genetic ; RNA sequencing ; Roles ; Tetraploidy ; Textile fibers</subject><ispartof>PLoS genetics, 2015-12, Vol.11 (12), p.e1005724-e1005724</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Song et al 2015 Song et al</rights><rights>2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Song Q, Guan X, Chen ZJ (2015) Dynamic Roles for Small RNAs and DNA Methylation during Ovule and Fiber Development in Allotetraploid Cotton. 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In plants, methylation occurs at CG, CHG, and CHH (H = A, C or T) sites via distinct pathways. Cotton is an allotetraploid consisting of two progenitor genomes. Each cotton fiber is a rapidly-elongating cell derived from the ovule epidermis, but the molecular basis for this developmental transition is unknown. Here we analyzed methylome, transcriptome, and small RNAome and revealed distinct changes in CHH methylation during ovule and fiber development. In ovules, CHH hypermethylation in promoters correlated positively with siRNAs, inducing RNA-dependent DNA methylation (RdDM), and up-regulation of ovule-preferred genes. In fibers, the ovule-derived cells generated additional heterochromatic CHH hypermethylation independent of RdDM, which repressed transposable elements (TEs) and nearby genes including fiber-related genes. Furthermore, CHG and CHH methylation in genic regions contributed to homoeolog expression bias in ovules and fibers. Inhibiting DNA methylation using 5-aza-2'-deoxycytidine in cultured ovules has reduced fiber cell number and length, suggesting a potential role for DNA methylation in fiber development. Thus, RdDM-dependent methylation in promoters and RdDM-independent methylation in TEs and nearby genes could act as a double-lock feedback mechanism to mediate gene and TE expression, potentiating the transition from epidermal to fiber cells during ovule and seed development.</description><subject>Bias</subject><subject>Cotton</subject><subject>Deoxyribonucleic acid</subject><subject>Development</subject><subject>DNA</subject><subject>DNA Methylation</subject><subject>DNA sequencing</subject><subject>Epigenesis, Genetic</subject><subject>Epigenetics</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes, Plant</subject><subject>Genomes</subject><subject>Gossypium - genetics</subject><subject>Gossypium - growth & development</subject><subject>Methods</subject><subject>Methylation</subject><subject>MicroRNAs - genetics</subject><subject>Nucleotide sequencing</subject><subject>Observations</subject><subject>Ovule - genetics</subject><subject>Ovule - growth & development</subject><subject>Plant Vascular Bundle - genetics</subject><subject>Plant Vascular Bundle - growth & development</subject><subject>Plants</subject><subject>Promoter Regions, Genetic</subject><subject>RNA sequencing</subject><subject>Roles</subject><subject>Tetraploidy</subject><subject>Textile fibers</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVk99rUzEUxy-iuDn9D0QDguhDa37em_silM1pYW6wqa8hzT23zUiTLskd9r83Xbuxgg9KHhKSz_mewzn5VtVrgseENeTTdRii1268moMfE4xFQ_mT6pAIwUYNx_zpo_NB9SKla4yZkG3zvDqgdUMwachh5U7WXi-tQZfBQUJ9iOhqqZ1Dl-eThLTv0Mn5BH2HvFg7nW3wqBui9XN0cTs4uANO7QwiOoFbcGG1BJ-R9WjiXMiQo165YDt0HHIO_mX1rNcuwavdflT9PP3y4_jb6Ozi6_R4cjYydSvzqG4444zUwNq6azWdQdsZKnjHe0kpzGjNAJjQWPSUzTiVhgOtJUhDGe51y46qt1vdkjypXaOSIk3NWYOJZIWYboku6Gu1inap41oFbdXdRYhzpWO2xoHqQcuuZgJkW3OOaaulJtgYQrU0YHTR-rzLNsyW0JnSgajdnuj-i7cLNQ-3itctFZgUgQ87gRhuBkhZLW0y4Jz2EIZN3YIKWfNS_VH1bovOdSnN-j4URbPB1YQLIhhupCzU-C9UWR2UUQcPvS33ewEf9wIKk-F3nushJTW9uvwP9vzf2Ytf--z7R-wCtMuLFNyw-XRpH-Rb0MSQUoT-odUEq4017ieuNtZQO2uUsDePx_QQdO8F9geR4Qgi</recordid><startdate>20151201</startdate><enddate>20151201</enddate><creator>Song, Qingxin</creator><creator>Guan, Xueying</creator><creator>Chen, Z Jeffrey</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20151201</creationdate><title>Dynamic Roles for Small RNAs and DNA Methylation during Ovule and Fiber Development in Allotetraploid Cotton</title><author>Song, Qingxin ; Guan, Xueying ; Chen, Z Jeffrey</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c698t-67434316e396d9a2be9dc254d4f822eb263ee35a05f23b428c4e268e8c230fa93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Bias</topic><topic>Cotton</topic><topic>Deoxyribonucleic acid</topic><topic>Development</topic><topic>DNA</topic><topic>DNA Methylation</topic><topic>DNA sequencing</topic><topic>Epigenesis, Genetic</topic><topic>Epigenetics</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genes, Plant</topic><topic>Genomes</topic><topic>Gossypium - genetics</topic><topic>Gossypium - growth & development</topic><topic>Methods</topic><topic>Methylation</topic><topic>MicroRNAs - genetics</topic><topic>Nucleotide sequencing</topic><topic>Observations</topic><topic>Ovule - genetics</topic><topic>Ovule - growth & development</topic><topic>Plant Vascular Bundle - genetics</topic><topic>Plant Vascular Bundle - growth & development</topic><topic>Plants</topic><topic>Promoter Regions, Genetic</topic><topic>RNA sequencing</topic><topic>Roles</topic><topic>Tetraploidy</topic><topic>Textile fibers</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Song, Qingxin</creatorcontrib><creatorcontrib>Guan, Xueying</creatorcontrib><creatorcontrib>Chen, Z Jeffrey</creatorcontrib><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: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Song, Qingxin</au><au>Guan, Xueying</au><au>Chen, Z Jeffrey</au><au>Stroud, Hume</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dynamic Roles for Small RNAs and DNA Methylation during Ovule and Fiber Development in Allotetraploid Cotton</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2015-12-01</date><risdate>2015</risdate><volume>11</volume><issue>12</issue><spage>e1005724</spage><epage>e1005724</epage><pages>e1005724-e1005724</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>DNA methylation is essential for plant and animal development. In plants, methylation occurs at CG, CHG, and CHH (H = A, C or T) sites via distinct pathways. Cotton is an allotetraploid consisting of two progenitor genomes. Each cotton fiber is a rapidly-elongating cell derived from the ovule epidermis, but the molecular basis for this developmental transition is unknown. Here we analyzed methylome, transcriptome, and small RNAome and revealed distinct changes in CHH methylation during ovule and fiber development. In ovules, CHH hypermethylation in promoters correlated positively with siRNAs, inducing RNA-dependent DNA methylation (RdDM), and up-regulation of ovule-preferred genes. In fibers, the ovule-derived cells generated additional heterochromatic CHH hypermethylation independent of RdDM, which repressed transposable elements (TEs) and nearby genes including fiber-related genes. Furthermore, CHG and CHH methylation in genic regions contributed to homoeolog expression bias in ovules and fibers. Inhibiting DNA methylation using 5-aza-2'-deoxycytidine in cultured ovules has reduced fiber cell number and length, suggesting a potential role for DNA methylation in fiber development. Thus, RdDM-dependent methylation in promoters and RdDM-independent methylation in TEs and nearby genes could act as a double-lock feedback mechanism to mediate gene and TE expression, potentiating the transition from epidermal to fiber cells during ovule and seed development.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26710171</pmid><doi>10.1371/journal.pgen.1005724</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Bias Cotton Deoxyribonucleic acid Development DNA DNA Methylation DNA sequencing Epigenesis, Genetic Epigenetics Gene expression Gene Expression Regulation, Developmental Gene Expression Regulation, Plant Genes, Plant Genomes Gossypium - genetics Gossypium - growth & development Methods Methylation MicroRNAs - genetics Nucleotide sequencing Observations Ovule - genetics Ovule - growth & development Plant Vascular Bundle - genetics Plant Vascular Bundle - growth & development Plants Promoter Regions, Genetic RNA sequencing Roles Tetraploidy Textile fibers |
| title | Dynamic Roles for Small RNAs and DNA Methylation during Ovule and Fiber Development in Allotetraploid Cotton |
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