Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis
Leaf primordia are generated at the periphery of the shoot apex, developing into flat symmetric organs with adaxial-abaxial polarity, in which the indeterminate state is repressed. Despite the crucial role of the ASYMMETRIC LEAVES1 (AS1)-AS2 nuclear-protein complex in leaf adaxial-abaxial polarity s...
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| Veröffentlicht in: | Development (Cambridge) 2013-05, Vol.140 (9), p.1958-1969 |
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| container_end_page | 1969 |
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| container_issue | 9 |
| container_start_page | 1958 |
| container_title | Development (Cambridge) |
| container_volume | 140 |
| creator | Iwasaki, Mayumi Takahashi, Hiro Iwakawa, Hidekazu Nakagawa, Ayami Ishikawa, Takaaki Tanaka, Hirokazu Matsumura, Yoko Pekker, Irena Eshed, Yuval Vial-Pradel, Simon Ito, Toshiro Watanabe, Yuichiro Ueno, Yoshihisa Fukazawa, Hiroshi Kojima, Shoko Machida, Yasunori Machida, Chiyoko |
| description | Leaf primordia are generated at the periphery of the shoot apex, developing into flat symmetric organs with adaxial-abaxial polarity, in which the indeterminate state is repressed. Despite the crucial role of the ASYMMETRIC LEAVES1 (AS1)-AS2 nuclear-protein complex in leaf adaxial-abaxial polarity specification, information on mechanisms controlling their downstream genes has remained elusive. We systematically analyzed transcripts by microarray and chromatin immunoprecipitation assays and performed genetic rescue of as1 and as2 phenotypic abnormalities, which identified a new target gene, ETTIN (ETT)/AUXIN RESPONSE FACTOR3 (ARF3), which encodes an abaxial factor acting downstream of the AS1-AS2 complex. While the AS1-AS2 complex represses ETT by direct binding of AS1 to the ETT promoter, it also indirectly activates miR390- and RDR6-dependent post-transcriptional gene silencing to negatively regulate both ETT and ARF4 activities. Furthermore, AS1-AS2 maintains the status of DNA methylation in the ETT coding region. In agreement, filamentous leaves formed in as1 and as2 plants treated with a DNA methylation inhibitor were rescued by loss of ETT and ARF4 activities. We suggest that negative transcriptional, post-transcriptional and epigenetic regulation of the ARFs by AS1-AS2 is important for stabilizing early leaf partitioning into abaxial and adaxial domains. |
| doi_str_mv | 10.1242/dev.085365 |
| format | Article |
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Despite the crucial role of the ASYMMETRIC LEAVES1 (AS1)-AS2 nuclear-protein complex in leaf adaxial-abaxial polarity specification, information on mechanisms controlling their downstream genes has remained elusive. We systematically analyzed transcripts by microarray and chromatin immunoprecipitation assays and performed genetic rescue of as1 and as2 phenotypic abnormalities, which identified a new target gene, ETTIN (ETT)/AUXIN RESPONSE FACTOR3 (ARF3), which encodes an abaxial factor acting downstream of the AS1-AS2 complex. While the AS1-AS2 complex represses ETT by direct binding of AS1 to the ETT promoter, it also indirectly activates miR390- and RDR6-dependent post-transcriptional gene silencing to negatively regulate both ETT and ARF4 activities. Furthermore, AS1-AS2 maintains the status of DNA methylation in the ETT coding region. In agreement, filamentous leaves formed in as1 and as2 plants treated with a DNA methylation inhibitor were rescued by loss of ETT and ARF4 activities. We suggest that negative transcriptional, post-transcriptional and epigenetic regulation of the ARFs by AS1-AS2 is important for stabilizing early leaf partitioning into abaxial and adaxial domains.</description><identifier>ISSN: 0950-1991</identifier><identifier>EISSN: 1477-9129</identifier><identifier>DOI: 10.1242/dev.085365</identifier><identifier>PMID: 23571218</identifier><language>eng</language><publisher>England</publisher><subject>Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis - physiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Blotting, Northern ; Cell Proliferation ; Chromatin Immunoprecipitation ; DNA (Cytosine-5-)-Methyltransferases - genetics ; DNA (Cytosine-5-)-Methyltransferases - metabolism ; DNA Methylation ; DNA, Plant - genetics ; DNA, Plant - metabolism ; DNA-Binding Proteins - genetics ; DNA-Binding Proteins - metabolism ; Gene Expression Regulation, Plant ; Gene Silencing ; Genes, Plant ; Nuclear Proteins - genetics ; Nuclear Proteins - metabolism ; Oligonucleotide Array Sequence Analysis ; Phenotype ; Plant Leaves - genetics ; Plant Leaves - metabolism ; Plant Leaves - physiology ; Promoter Regions, Genetic ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Transcription, Genetic</subject><ispartof>Development (Cambridge), 2013-05, Vol.140 (9), p.1958-1969</ispartof><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c422t-5c9de944520e0c6cb66034b2d54ccfb01c5190c2011e16bf7833e8db3312c1b43</citedby><cites>FETCH-LOGICAL-c422t-5c9de944520e0c6cb66034b2d54ccfb01c5190c2011e16bf7833e8db3312c1b43</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,777,781,3665,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23571218$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Iwasaki, Mayumi</creatorcontrib><creatorcontrib>Takahashi, Hiro</creatorcontrib><creatorcontrib>Iwakawa, Hidekazu</creatorcontrib><creatorcontrib>Nakagawa, Ayami</creatorcontrib><creatorcontrib>Ishikawa, Takaaki</creatorcontrib><creatorcontrib>Tanaka, Hirokazu</creatorcontrib><creatorcontrib>Matsumura, Yoko</creatorcontrib><creatorcontrib>Pekker, Irena</creatorcontrib><creatorcontrib>Eshed, Yuval</creatorcontrib><creatorcontrib>Vial-Pradel, Simon</creatorcontrib><creatorcontrib>Ito, Toshiro</creatorcontrib><creatorcontrib>Watanabe, Yuichiro</creatorcontrib><creatorcontrib>Ueno, Yoshihisa</creatorcontrib><creatorcontrib>Fukazawa, Hiroshi</creatorcontrib><creatorcontrib>Kojima, Shoko</creatorcontrib><creatorcontrib>Machida, Yasunori</creatorcontrib><creatorcontrib>Machida, Chiyoko</creatorcontrib><title>Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis</title><title>Development (Cambridge)</title><addtitle>Development</addtitle><description>Leaf primordia are generated at the periphery of the shoot apex, developing into flat symmetric organs with adaxial-abaxial polarity, in which the indeterminate state is repressed. Despite the crucial role of the ASYMMETRIC LEAVES1 (AS1)-AS2 nuclear-protein complex in leaf adaxial-abaxial polarity specification, information on mechanisms controlling their downstream genes has remained elusive. We systematically analyzed transcripts by microarray and chromatin immunoprecipitation assays and performed genetic rescue of as1 and as2 phenotypic abnormalities, which identified a new target gene, ETTIN (ETT)/AUXIN RESPONSE FACTOR3 (ARF3), which encodes an abaxial factor acting downstream of the AS1-AS2 complex. While the AS1-AS2 complex represses ETT by direct binding of AS1 to the ETT promoter, it also indirectly activates miR390- and RDR6-dependent post-transcriptional gene silencing to negatively regulate both ETT and ARF4 activities. Furthermore, AS1-AS2 maintains the status of DNA methylation in the ETT coding region. In agreement, filamentous leaves formed in as1 and as2 plants treated with a DNA methylation inhibitor were rescued by loss of ETT and ARF4 activities. We suggest that negative transcriptional, post-transcriptional and epigenetic regulation of the ARFs by AS1-AS2 is important for stabilizing early leaf partitioning into abaxial and adaxial domains.</description><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Blotting, Northern</subject><subject>Cell Proliferation</subject><subject>Chromatin Immunoprecipitation</subject><subject>DNA (Cytosine-5-)-Methyltransferases - genetics</subject><subject>DNA (Cytosine-5-)-Methyltransferases - metabolism</subject><subject>DNA Methylation</subject><subject>DNA, Plant - genetics</subject><subject>DNA, Plant - metabolism</subject><subject>DNA-Binding Proteins - genetics</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Silencing</subject><subject>Genes, Plant</subject><subject>Nuclear Proteins - genetics</subject><subject>Nuclear Proteins - metabolism</subject><subject>Oligonucleotide Array Sequence Analysis</subject><subject>Phenotype</subject><subject>Plant Leaves - genetics</subject><subject>Plant Leaves - metabolism</subject><subject>Plant Leaves - physiology</subject><subject>Promoter Regions, Genetic</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Transcription, Genetic</subject><issn>0950-1991</issn><issn>1477-9129</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUtv1DAUhS0EosPAhh-AvCyoKb5-JJNl1AdUqopEh3VkOzczRs4DOxk6_WP9eyTM0C2Lq3Ol-51zF4eQ98DOgUv-ucLdOVspkaoXZAEyy5IceP6SLFiuWAJ5DifkTYw_GWMizbLX5IQLlQGH1YI8XY7a04Cb0evBdS3tanq1Xt_c0dPi-7X4SDfYIsWHPmCM893saXEPSXHPz-jvrbNb2mjXDtNEOmyRXt4VtMFhuz_medyhP6MuUtfuOr_DalpoHLRx3j0-__Soa6or_eC0T7T5q7TXYXAz4drN7CrC5Kq6Prr4lryqtY_47qhL8uP6an3xNbn99uXmorhNrOR8SJTNK8ylVJwhs6k1acqENLxS0traMLAKcmY5A0BITZ2thMBVZYQAbsFIsSSnh9w-dL9GjEPZuGjRe91iN8YSlIJUpHLy_RcVPAUJM7sknw6oDV2MAeuyD67RYV8CK-dOy6nT8tDpBH845o6mweoZ_Vei-APoyZzs</recordid><startdate>201305</startdate><enddate>201305</enddate><creator>Iwasaki, Mayumi</creator><creator>Takahashi, Hiro</creator><creator>Iwakawa, Hidekazu</creator><creator>Nakagawa, Ayami</creator><creator>Ishikawa, Takaaki</creator><creator>Tanaka, Hirokazu</creator><creator>Matsumura, Yoko</creator><creator>Pekker, Irena</creator><creator>Eshed, Yuval</creator><creator>Vial-Pradel, Simon</creator><creator>Ito, Toshiro</creator><creator>Watanabe, Yuichiro</creator><creator>Ueno, Yoshihisa</creator><creator>Fukazawa, Hiroshi</creator><creator>Kojima, Shoko</creator><creator>Machida, Yasunori</creator><creator>Machida, Chiyoko</creator><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>7X8</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope></search><sort><creationdate>201305</creationdate><title>Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis</title><author>Iwasaki, Mayumi ; Takahashi, Hiro ; Iwakawa, Hidekazu ; Nakagawa, Ayami ; Ishikawa, Takaaki ; Tanaka, Hirokazu ; Matsumura, Yoko ; Pekker, Irena ; Eshed, Yuval ; Vial-Pradel, Simon ; Ito, Toshiro ; Watanabe, Yuichiro ; Ueno, Yoshihisa ; Fukazawa, Hiroshi ; Kojima, Shoko ; Machida, Yasunori ; Machida, Chiyoko</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c422t-5c9de944520e0c6cb66034b2d54ccfb01c5190c2011e16bf7833e8db3312c1b43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Blotting, Northern</topic><topic>Cell Proliferation</topic><topic>Chromatin Immunoprecipitation</topic><topic>DNA (Cytosine-5-)-Methyltransferases - genetics</topic><topic>DNA (Cytosine-5-)-Methyltransferases - metabolism</topic><topic>DNA Methylation</topic><topic>DNA, Plant - genetics</topic><topic>DNA, Plant - metabolism</topic><topic>DNA-Binding Proteins - genetics</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene Silencing</topic><topic>Genes, Plant</topic><topic>Nuclear Proteins - genetics</topic><topic>Nuclear Proteins - metabolism</topic><topic>Oligonucleotide Array Sequence Analysis</topic><topic>Phenotype</topic><topic>Plant Leaves - genetics</topic><topic>Plant Leaves - metabolism</topic><topic>Plant Leaves - physiology</topic><topic>Promoter Regions, Genetic</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><topic>Transcription, Genetic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Iwasaki, Mayumi</creatorcontrib><creatorcontrib>Takahashi, Hiro</creatorcontrib><creatorcontrib>Iwakawa, Hidekazu</creatorcontrib><creatorcontrib>Nakagawa, Ayami</creatorcontrib><creatorcontrib>Ishikawa, Takaaki</creatorcontrib><creatorcontrib>Tanaka, Hirokazu</creatorcontrib><creatorcontrib>Matsumura, Yoko</creatorcontrib><creatorcontrib>Pekker, Irena</creatorcontrib><creatorcontrib>Eshed, Yuval</creatorcontrib><creatorcontrib>Vial-Pradel, Simon</creatorcontrib><creatorcontrib>Ito, Toshiro</creatorcontrib><creatorcontrib>Watanabe, Yuichiro</creatorcontrib><creatorcontrib>Ueno, Yoshihisa</creatorcontrib><creatorcontrib>Fukazawa, Hiroshi</creatorcontrib><creatorcontrib>Kojima, Shoko</creatorcontrib><creatorcontrib>Machida, Yasunori</creatorcontrib><creatorcontrib>Machida, Chiyoko</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>Development (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Iwasaki, Mayumi</au><au>Takahashi, Hiro</au><au>Iwakawa, Hidekazu</au><au>Nakagawa, Ayami</au><au>Ishikawa, Takaaki</au><au>Tanaka, Hirokazu</au><au>Matsumura, Yoko</au><au>Pekker, Irena</au><au>Eshed, Yuval</au><au>Vial-Pradel, Simon</au><au>Ito, Toshiro</au><au>Watanabe, Yuichiro</au><au>Ueno, Yoshihisa</au><au>Fukazawa, Hiroshi</au><au>Kojima, Shoko</au><au>Machida, Yasunori</au><au>Machida, Chiyoko</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis</atitle><jtitle>Development (Cambridge)</jtitle><addtitle>Development</addtitle><date>2013-05</date><risdate>2013</risdate><volume>140</volume><issue>9</issue><spage>1958</spage><epage>1969</epage><pages>1958-1969</pages><issn>0950-1991</issn><eissn>1477-9129</eissn><abstract>Leaf primordia are generated at the periphery of the shoot apex, developing into flat symmetric organs with adaxial-abaxial polarity, in which the indeterminate state is repressed. Despite the crucial role of the ASYMMETRIC LEAVES1 (AS1)-AS2 nuclear-protein complex in leaf adaxial-abaxial polarity specification, information on mechanisms controlling their downstream genes has remained elusive. We systematically analyzed transcripts by microarray and chromatin immunoprecipitation assays and performed genetic rescue of as1 and as2 phenotypic abnormalities, which identified a new target gene, ETTIN (ETT)/AUXIN RESPONSE FACTOR3 (ARF3), which encodes an abaxial factor acting downstream of the AS1-AS2 complex. While the AS1-AS2 complex represses ETT by direct binding of AS1 to the ETT promoter, it also indirectly activates miR390- and RDR6-dependent post-transcriptional gene silencing to negatively regulate both ETT and ARF4 activities. Furthermore, AS1-AS2 maintains the status of DNA methylation in the ETT coding region. In agreement, filamentous leaves formed in as1 and as2 plants treated with a DNA methylation inhibitor were rescued by loss of ETT and ARF4 activities. We suggest that negative transcriptional, post-transcriptional and epigenetic regulation of the ARFs by AS1-AS2 is important for stabilizing early leaf partitioning into abaxial and adaxial domains.</abstract><cop>England</cop><pmid>23571218</pmid><doi>10.1242/dev.085365</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0950-1991 |
| ispartof | Development (Cambridge), 2013-05, Vol.140 (9), p.1958-1969 |
| issn | 0950-1991 1477-9129 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_1551636483 |
| source | MEDLINE; EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection; Company of Biologists |
| subjects | Arabidopsis Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis - physiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Blotting, Northern Cell Proliferation Chromatin Immunoprecipitation DNA (Cytosine-5-)-Methyltransferases - genetics DNA (Cytosine-5-)-Methyltransferases - metabolism DNA Methylation DNA, Plant - genetics DNA, Plant - metabolism DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Gene Expression Regulation, Plant Gene Silencing Genes, Plant Nuclear Proteins - genetics Nuclear Proteins - metabolism Oligonucleotide Array Sequence Analysis Phenotype Plant Leaves - genetics Plant Leaves - metabolism Plant Leaves - physiology Promoter Regions, Genetic RNA, Messenger - genetics RNA, Messenger - metabolism Transcription Factors - genetics Transcription Factors - metabolism Transcription, Genetic |
| title | Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis |
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