A novel CCCH‐type zinc finger protein SAW1 activates OsGA20ox3 to regulate gibberellin homeostasis and anther development in rice
Male sterility is a prerequisite for hybrid seed production. The phytohormone gibberellin (GA) is involved in regulating male reproductive development, but the mechanism underlying GA homeostasis in anther development remains less understood. Here, we report the isolation and characterization of a n...
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Veröffentlicht in: | Journal of integrative plant biology 2020-10, Vol.62 (10), p.1594-1606 |
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creator | Wang, Bin Fang, Ruiqiu Chen, Faming Han, Jingluan Liu, Yao‐Guang Chen, Letian Zhu, Qinlong |
description | Male sterility is a prerequisite for hybrid seed production. The phytohormone gibberellin (GA) is involved in regulating male reproductive development, but the mechanism underlying GA homeostasis in anther development remains less understood. Here, we report the isolation and characterization of a new positive regulator of GA homeostasis, swollen anther wall 1 (SAW1), for anther development in rice (Oryza sativa L.). Rice plants carrying the recessive mutant allele saw1 produces abnormal anthers with swollen anther wall and aborted pollen. Clustered regularly interspaced short palindromic repeats (CRISPR)/CRIPSR‐associated protein 9‐mediated knockout of SAW1 in rice generated similar male sterile plants. SAW1 encodes a novel nucleus‐localizing CCCH‐tandem zinc finger protein, and this protein could directly bind to the promoter region of the GA synthesis gene OsGA20ox3 to induce its anther‐specific expression. In the saw1 anther, the significantly decreased OsGA20ox3 expression resulted in lower bioactive GA content, which in turn caused the lower expression of the GA‐inducible anther‐regulator gene OsGAMYB. Thus, our results disclose the mechanism of the SAW1‐GA20ox3‐GAMYB pathway in controlling rice anther development, and provide a new target gene for the rapid generation of male sterile lines by genome editing for hybrid breeding.
A novel nucleus‐localized CCCH‐tandem zinc‐finger transcription factor SAW1 enhances the expression of anther‐specific OsGA20ox3 for GA homeostasis and anther development in rice. Loss‐of‐function of SAW1 significantly decreases OsGA20ox3 expression leading to low bioactive GA content and low expression of GA‐inducible gene OsGAMYB during anther development. |
doi_str_mv | 10.1111/jipb.12924 |
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A novel nucleus‐localized CCCH‐tandem zinc‐finger transcription factor SAW1 enhances the expression of anther‐specific OsGA20ox3 for GA homeostasis and anther development in rice. Loss‐of‐function of SAW1 significantly decreases OsGA20ox3 expression leading to low bioactive GA content and low expression of GA‐inducible gene OsGAMYB during anther development.</description><identifier>ISSN: 1672-9072</identifier><identifier>EISSN: 1744-7909</identifier><identifier>DOI: 10.1111/jipb.12924</identifier><identifier>PMID: 32149461</identifier><language>eng</language><publisher>China (Republic : 1949- ): Wiley Subscription Services, Inc</publisher><subject>anther development ; Anthers ; CCCH proteins ; CRISPR ; CRISPR/Cas9 ; Genome editing ; Genomes ; gibberellin ; Gibberellins ; Homeostasis ; Male sterility ; Oryza sativa ; Plant hormones ; Pollen ; Proteins ; Rice ; Zinc ; Zinc finger proteins</subject><ispartof>Journal of integrative plant biology, 2020-10, Vol.62 (10), p.1594-1606</ispartof><rights>2020 Institute of Botany, Chinese Academy of Sciences</rights><rights>2020 Institute of Botany, Chinese Academy of Sciences.</rights><rights>Copyright © Wanfang Data Co. Ltd. All Rights Reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3874-65290890552639ff4ccf326bb699e03f4d0a99abd4e9c42bf757389d4fea2cd03</citedby><cites>FETCH-LOGICAL-c3874-65290890552639ff4ccf326bb699e03f4d0a99abd4e9c42bf757389d4fea2cd03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.wanfangdata.com.cn/images/PeriodicalImages/zwxb/zwxb.jpg</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fjipb.12924$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fjipb.12924$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1416,27923,27924,45573,45574</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32149461$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Bin</creatorcontrib><creatorcontrib>Fang, Ruiqiu</creatorcontrib><creatorcontrib>Chen, Faming</creatorcontrib><creatorcontrib>Han, Jingluan</creatorcontrib><creatorcontrib>Liu, Yao‐Guang</creatorcontrib><creatorcontrib>Chen, Letian</creatorcontrib><creatorcontrib>Zhu, Qinlong</creatorcontrib><title>A novel CCCH‐type zinc finger protein SAW1 activates OsGA20ox3 to regulate gibberellin homeostasis and anther development in rice</title><title>Journal of integrative plant biology</title><addtitle>J Integr Plant Biol</addtitle><description>Male sterility is a prerequisite for hybrid seed production. The phytohormone gibberellin (GA) is involved in regulating male reproductive development, but the mechanism underlying GA homeostasis in anther development remains less understood. Here, we report the isolation and characterization of a new positive regulator of GA homeostasis, swollen anther wall 1 (SAW1), for anther development in rice (Oryza sativa L.). Rice plants carrying the recessive mutant allele saw1 produces abnormal anthers with swollen anther wall and aborted pollen. Clustered regularly interspaced short palindromic repeats (CRISPR)/CRIPSR‐associated protein 9‐mediated knockout of SAW1 in rice generated similar male sterile plants. SAW1 encodes a novel nucleus‐localizing CCCH‐tandem zinc finger protein, and this protein could directly bind to the promoter region of the GA synthesis gene OsGA20ox3 to induce its anther‐specific expression. In the saw1 anther, the significantly decreased OsGA20ox3 expression resulted in lower bioactive GA content, which in turn caused the lower expression of the GA‐inducible anther‐regulator gene OsGAMYB. Thus, our results disclose the mechanism of the SAW1‐GA20ox3‐GAMYB pathway in controlling rice anther development, and provide a new target gene for the rapid generation of male sterile lines by genome editing for hybrid breeding.
A novel nucleus‐localized CCCH‐tandem zinc‐finger transcription factor SAW1 enhances the expression of anther‐specific OsGA20ox3 for GA homeostasis and anther development in rice. Loss‐of‐function of SAW1 significantly decreases OsGA20ox3 expression leading to low bioactive GA content and low expression of GA‐inducible gene OsGAMYB during anther development.</description><subject>anther development</subject><subject>Anthers</subject><subject>CCCH proteins</subject><subject>CRISPR</subject><subject>CRISPR/Cas9</subject><subject>Genome editing</subject><subject>Genomes</subject><subject>gibberellin</subject><subject>Gibberellins</subject><subject>Homeostasis</subject><subject>Male sterility</subject><subject>Oryza sativa</subject><subject>Plant hormones</subject><subject>Pollen</subject><subject>Proteins</subject><subject>Rice</subject><subject>Zinc</subject><subject>Zinc finger proteins</subject><issn>1672-9072</issn><issn>1744-7909</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNp9kd1qFDEYhoMotq6eeAESEEGEqfmbnxyug7aVQgUVD0Mm82WbZSbZJjNtt0eCN-A1eiWm7toDDwwJCeHJ8-XjReg5JUc0j7drt-mOKJNMPECHtBaiqCWRD_O5qlkhSc0O0JOU1oTwhlTsMTrgjAopKnqIfiyxD1cw4LZtT359_zltN4BvnTfYOr-CiDcxTOA8_rz8RrE2k7vSEyR8no6XjIQbjqeAI6zmIV_jles6iDAM-cFFGCGkSSeXsPZ9XtNF9vWQq4XNCH7CmYrOwFP0yOohwbP9vkBfP7z_0p4UZ-fHp-3yrDC8qUVRlUySRpKyZBWX1gpjLGdV11VSAuFW9ERLqbtegDSCdbYua97IXljQzPSEL9Crnfdae6v9Sq3DHH2uqG6vbzpGGKEkz8y93nG598sZ0qRGl0zuSnsIc1KM12VJSiJkRl_-g947mRCVbEqSP7tAb3aUiSGlCFZtoht13CpK1F2E6i5C9SfCDL_YK-duhP4e_ZtZBui-DTfA9j8q9fH007ud9DdZdqZL</recordid><startdate>202010</startdate><enddate>202010</enddate><creator>Wang, Bin</creator><creator>Fang, Ruiqiu</creator><creator>Chen, Faming</creator><creator>Han, Jingluan</creator><creator>Liu, Yao‐Guang</creator><creator>Chen, Letian</creator><creator>Zhu, Qinlong</creator><general>Wiley Subscription Services, Inc</general><general>Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou 510642, China</general><general>College of Life Sciences, South China Agricultural University, Guangzhou 510642, China%State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou 510642, China</general><general>Dongyang Institute of Maize Research, Zhejiang Academy of Agricultural Sciences, Dongyang 322100, China%State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou 510642, China</general><general>College of Life Sciences, South China Agricultural University, Guangzhou 510642, China</general><general>State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou 510642, China</general><general>Guangdong Provincial Key Laboratory of Protein Function and Regulation in Agricultural Organisms, South China Agricultural University, Guangzhou 510642, China</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7T7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>2B.</scope><scope>4A8</scope><scope>92I</scope><scope>93N</scope><scope>PSX</scope><scope>TCJ</scope></search><sort><creationdate>202010</creationdate><title>A novel CCCH‐type zinc finger protein SAW1 activates OsGA20ox3 to regulate gibberellin homeostasis and anther development in rice</title><author>Wang, Bin ; Fang, Ruiqiu ; Chen, Faming ; Han, Jingluan ; Liu, Yao‐Guang ; Chen, Letian ; Zhu, Qinlong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3874-65290890552639ff4ccf326bb699e03f4d0a99abd4e9c42bf757389d4fea2cd03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>anther development</topic><topic>Anthers</topic><topic>CCCH proteins</topic><topic>CRISPR</topic><topic>CRISPR/Cas9</topic><topic>Genome editing</topic><topic>Genomes</topic><topic>gibberellin</topic><topic>Gibberellins</topic><topic>Homeostasis</topic><topic>Male sterility</topic><topic>Oryza sativa</topic><topic>Plant hormones</topic><topic>Pollen</topic><topic>Proteins</topic><topic>Rice</topic><topic>Zinc</topic><topic>Zinc finger proteins</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Bin</creatorcontrib><creatorcontrib>Fang, Ruiqiu</creatorcontrib><creatorcontrib>Chen, Faming</creatorcontrib><creatorcontrib>Han, Jingluan</creatorcontrib><creatorcontrib>Liu, Yao‐Guang</creatorcontrib><creatorcontrib>Chen, Letian</creatorcontrib><creatorcontrib>Zhu, Qinlong</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Wanfang Data Journals - Hong Kong</collection><collection>WANFANG Data Centre</collection><collection>Wanfang Data Journals</collection><collection>万方数据期刊 - 香港版</collection><collection>China Online Journals (COJ)</collection><collection>China Online Journals (COJ)</collection><jtitle>Journal of integrative plant biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Bin</au><au>Fang, Ruiqiu</au><au>Chen, Faming</au><au>Han, Jingluan</au><au>Liu, Yao‐Guang</au><au>Chen, Letian</au><au>Zhu, Qinlong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A novel CCCH‐type zinc finger protein SAW1 activates OsGA20ox3 to regulate gibberellin homeostasis and anther development in rice</atitle><jtitle>Journal of integrative plant biology</jtitle><addtitle>J Integr Plant Biol</addtitle><date>2020-10</date><risdate>2020</risdate><volume>62</volume><issue>10</issue><spage>1594</spage><epage>1606</epage><pages>1594-1606</pages><issn>1672-9072</issn><eissn>1744-7909</eissn><abstract>Male sterility is a prerequisite for hybrid seed production. The phytohormone gibberellin (GA) is involved in regulating male reproductive development, but the mechanism underlying GA homeostasis in anther development remains less understood. Here, we report the isolation and characterization of a new positive regulator of GA homeostasis, swollen anther wall 1 (SAW1), for anther development in rice (Oryza sativa L.). Rice plants carrying the recessive mutant allele saw1 produces abnormal anthers with swollen anther wall and aborted pollen. Clustered regularly interspaced short palindromic repeats (CRISPR)/CRIPSR‐associated protein 9‐mediated knockout of SAW1 in rice generated similar male sterile plants. SAW1 encodes a novel nucleus‐localizing CCCH‐tandem zinc finger protein, and this protein could directly bind to the promoter region of the GA synthesis gene OsGA20ox3 to induce its anther‐specific expression. In the saw1 anther, the significantly decreased OsGA20ox3 expression resulted in lower bioactive GA content, which in turn caused the lower expression of the GA‐inducible anther‐regulator gene OsGAMYB. Thus, our results disclose the mechanism of the SAW1‐GA20ox3‐GAMYB pathway in controlling rice anther development, and provide a new target gene for the rapid generation of male sterile lines by genome editing for hybrid breeding.
A novel nucleus‐localized CCCH‐tandem zinc‐finger transcription factor SAW1 enhances the expression of anther‐specific OsGA20ox3 for GA homeostasis and anther development in rice. Loss‐of‐function of SAW1 significantly decreases OsGA20ox3 expression leading to low bioactive GA content and low expression of GA‐inducible gene OsGAMYB during anther development.</abstract><cop>China (Republic : 1949- )</cop><pub>Wiley Subscription Services, Inc</pub><pmid>32149461</pmid><doi>10.1111/jipb.12924</doi><tpages>12</tpages></addata></record> |
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subjects | anther development Anthers CCCH proteins CRISPR CRISPR/Cas9 Genome editing Genomes gibberellin Gibberellins Homeostasis Male sterility Oryza sativa Plant hormones Pollen Proteins Rice Zinc Zinc finger proteins |
title | A novel CCCH‐type zinc finger protein SAW1 activates OsGA20ox3 to regulate gibberellin homeostasis and anther development in rice |
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