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...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Journal of integrative plant biology 2020-10, Vol.62 (10), p.1594-1606
Hauptverfasser: Wang, Bin, Fang, Ruiqiu, Chen, Faming, Han, Jingluan, Liu, Yao‐Guang, Chen, Letian, Zhu, Qinlong
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 1606
container_issue 10
container_start_page 1594
container_title Journal of integrative plant biology
container_volume 62
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
format Article
fullrecord <record><control><sourceid>wanfang_jour_proqu</sourceid><recordid>TN_cdi_wanfang_journals_zwxb202010010</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><wanfj_id>zwxb202010010</wanfj_id><sourcerecordid>zwxb202010010</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3874-65290890552639ff4ccf326bb699e03f4d0a99abd4e9c42bf757389d4fea2cd03</originalsourceid><addsrcrecordid>eNp9kd1qFDEYhoMotq6eeAESEEGEqfmbnxyug7aVQgUVD0Mm82WbZSbZJjNtt0eCN-A1eiWm7toDDwwJCeHJ8-XjReg5JUc0j7drt-mOKJNMPECHtBaiqCWRD_O5qlkhSc0O0JOU1oTwhlTsMTrgjAopKnqIfiyxD1cw4LZtT359_zltN4BvnTfYOr-CiDcxTOA8_rz8RrE2k7vSEyR8no6XjIQbjqeAI6zmIV_jles6iDAM-cFFGCGkSSeXsPZ9XtNF9vWQq4XNCH7CmYrOwFP0yOohwbP9vkBfP7z_0p4UZ-fHp-3yrDC8qUVRlUySRpKyZBWX1gpjLGdV11VSAuFW9ERLqbtegDSCdbYua97IXljQzPSEL9Crnfdae6v9Sq3DHH2uqG6vbzpGGKEkz8y93nG598sZ0qRGl0zuSnsIc1KM12VJSiJkRl_-g947mRCVbEqSP7tAb3aUiSGlCFZtoht13CpK1F2E6i5C9SfCDL_YK-duhP4e_ZtZBui-DTfA9j8q9fH007ud9DdZdqZL</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2446985026</pqid></control><display><type>article</type><title>A novel CCCH‐type zinc finger protein SAW1 activates OsGA20ox3 to regulate gibberellin homeostasis and anther development in rice</title><source>Wiley Online Library All Journals</source><source>Alma/SFX Local Collection</source><creator>Wang, Bin ; Fang, Ruiqiu ; Chen, Faming ; Han, Jingluan ; Liu, Yao‐Guang ; Chen, Letian ; Zhu, Qinlong</creator><creatorcontrib>Wang, Bin ; Fang, Ruiqiu ; Chen, Faming ; Han, Jingluan ; Liu, Yao‐Guang ; Chen, Letian ; Zhu, Qinlong</creatorcontrib><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><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>
fulltext fulltext
identifier ISSN: 1672-9072
ispartof Journal of integrative plant biology, 2020-10, Vol.62 (10), p.1594-1606
issn 1672-9072
1744-7909
language eng
recordid cdi_wanfang_journals_zwxb202010010
source Wiley Online Library All Journals; Alma/SFX Local Collection
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
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-12T23%3A03%3A53IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-wanfang_jour_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20novel%20CCCH%E2%80%90type%20zinc%20finger%20protein%20SAW1%20activates%20OsGA20ox3%20to%20regulate%20gibberellin%20homeostasis%20and%20anther%20development%20in%20rice&rft.jtitle=Journal%20of%20integrative%20plant%20biology&rft.au=Wang,%20Bin&rft.date=2020-10&rft.volume=62&rft.issue=10&rft.spage=1594&rft.epage=1606&rft.pages=1594-1606&rft.issn=1672-9072&rft.eissn=1744-7909&rft_id=info:doi/10.1111/jipb.12924&rft_dat=%3Cwanfang_jour_proqu%3Ezwxb202010010%3C/wanfang_jour_proqu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2446985026&rft_id=info:pmid/32149461&rft_wanfj_id=zwxb202010010&rfr_iscdi=true