TDR INTERACTING PROTEIN 3, encoding a PHD‐finger transcription factor, regulates Ubisch bodies and pollen wall formation in rice
Summary Male reproductive development involves a complex series of biological events and precise transcriptional regulation is essential for this biological process in flowering plants. Several transcriptional factors have been reported to regulate tapetum and pollen development, however the transcr...
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| Veröffentlicht in: | The Plant journal : for cell and molecular biology 2019-09, Vol.99 (5), p.844-861 |
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| creator | Yang, Zhengfu Sun, Lianping Zhang, Peipei Zhang, Yingxin Yu, Ping Liu, Ling Abbas, Adil Xiang, Xiaojiao Wu, Weixun Zhan, Xiaodeng Cao, Liyong Cheng, Shihua |
| description | Summary
Male reproductive development involves a complex series of biological events and precise transcriptional regulation is essential for this biological process in flowering plants. Several transcriptional factors have been reported to regulate tapetum and pollen development, however the transcriptional mechanism underlying Ubisch bodies and pollen wall formation remains less understood. Here, we characterized and isolated a male sterility mutant of TDR INTERACTING PROTEIN 3 (TIP3) in rice. The tip3 mutant displayed smaller and pale yellow anthers without mature pollen grains, abnormal Ubisch body morphology, no pollen wall formation, as well as delayed tapetum degeneration. Map‐based cloning demonstrated that TIP3 encodes a conserved PHD‐finger protein and further study confirmed that TIP3 functioned as a transcription factor with transcriptional activation activity. TIP3 is preferentially expressed in the tapetum and microspores during anther development. Moreover, TIP3 can physically interact with TDR, which is a key component of the transcriptional cascade in regulating tapetum development and pollen wall formation. Furthermore, disruption of TIP3 changed the expression of several genes involved in tapetum development and degradation, biosynthesis and transport of lipid monomers of sporopollenin in tip3 mutant. Taken together, our results revealed an unprecedented role for TIP3 in regulating Ubisch bodies and pollen exine formation, and presents a potential tool to manipulate male fertility for hybrid rice breeding.
Significance Statement
TIP3, a PHD‐finger protein, functions as a transcriptional activator and physically interacts with TDR participating in tapetum programmed cell death, Ubisch body morphogenesis and pollen wall formation. Our results provide an insight into the molecular mechanism underlying tapetal programmed cell death (PCD) and pollen wall formation in rice. |
| doi_str_mv | 10.1111/tpj.14365 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6852570</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2215018147</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4765-d0aa55e80096a228710269b43186448cedacc14337419ad1fa27be4f459519b83</originalsourceid><addsrcrecordid>eNqFkt1qFDEYhoModq0eeAMS8ESh2-Zv_k4KZbu2K2W7LFPwLGQymW2WbLImM5aeiVfgNXolfu3WooKYk4-QJ2_yJB9Cryk5pDCO-u36kAqeZ0_QiEIZc8o_PUUjUuVkXAjK9tCLlNaE0ILn4jna45QwSmg2Qt_q0yWezevp8mRSz-ZneLG8rKezOeYH2HgdWutXWOHF-emPr987mJiI-6h80tFuexs87pTuQzzA0awGp3qT8FVjk77GDWyGmfIt3gbnjMc3yjnchbhR9zutx9Fq8xI965RL5tVD3UdXH6b15Hx8cXk2m5xcjLUowKklSmWZKQlYKcbKAhzyqhGclrkQpTat0hpegYNwpVraKVY0RnQiqzJaNSXfR8e73O3QbEyrjQcRJ7fRblS8lUFZ-eeKt9dyFb7IvMxYVhAIePcQEMPnwaRebkDUOKe8CUOSjLOiKhgc-H-U0YzQkooC0Ld_oeswRA8vAVRJWHXnCdT7HaVjSCma7vHelMi7JpDQBPK-CYB987voI_nr1wE42gE31pnbfyfJevFxF_kTlSq6fA</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2280291026</pqid></control><display><type>article</type><title>TDR INTERACTING PROTEIN 3, encoding a PHD‐finger transcription factor, regulates Ubisch bodies and pollen wall formation in rice</title><source>Wiley Free Content</source><source>IngentaConnect Free/Open Access Journals</source><source>Wiley Online Library Journals Frontfile Complete</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><creator>Yang, Zhengfu ; Sun, Lianping ; Zhang, Peipei ; Zhang, Yingxin ; Yu, Ping ; Liu, Ling ; Abbas, Adil ; Xiang, Xiaojiao ; Wu, Weixun ; Zhan, Xiaodeng ; Cao, Liyong ; Cheng, Shihua</creator><creatorcontrib>Yang, Zhengfu ; Sun, Lianping ; Zhang, Peipei ; Zhang, Yingxin ; Yu, Ping ; Liu, Ling ; Abbas, Adil ; Xiang, Xiaojiao ; Wu, Weixun ; Zhan, Xiaodeng ; Cao, Liyong ; Cheng, Shihua</creatorcontrib><description>Summary
Male reproductive development involves a complex series of biological events and precise transcriptional regulation is essential for this biological process in flowering plants. Several transcriptional factors have been reported to regulate tapetum and pollen development, however the transcriptional mechanism underlying Ubisch bodies and pollen wall formation remains less understood. Here, we characterized and isolated a male sterility mutant of TDR INTERACTING PROTEIN 3 (TIP3) in rice. The tip3 mutant displayed smaller and pale yellow anthers without mature pollen grains, abnormal Ubisch body morphology, no pollen wall formation, as well as delayed tapetum degeneration. Map‐based cloning demonstrated that TIP3 encodes a conserved PHD‐finger protein and further study confirmed that TIP3 functioned as a transcription factor with transcriptional activation activity. TIP3 is preferentially expressed in the tapetum and microspores during anther development. Moreover, TIP3 can physically interact with TDR, which is a key component of the transcriptional cascade in regulating tapetum development and pollen wall formation. Furthermore, disruption of TIP3 changed the expression of several genes involved in tapetum development and degradation, biosynthesis and transport of lipid monomers of sporopollenin in tip3 mutant. Taken together, our results revealed an unprecedented role for TIP3 in regulating Ubisch bodies and pollen exine formation, and presents a potential tool to manipulate male fertility for hybrid rice breeding.
Significance Statement
TIP3, a PHD‐finger protein, functions as a transcriptional activator and physically interacts with TDR participating in tapetum programmed cell death, Ubisch body morphogenesis and pollen wall formation. Our results provide an insight into the molecular mechanism underlying tapetal programmed cell death (PCD) and pollen wall formation in rice.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.14365</identifier><identifier>PMID: 31021015</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Anthers ; Biological activity ; Biosynthesis ; Cloning ; Degeneration ; Disruption ; exine ; Fertility ; Flowering ; Flowering plants ; Gene expression ; Gene regulation ; genes ; Lipids ; male fertility ; Male sterility ; males ; Microspores ; molecular cloning ; Monomers ; Morphology ; mutants ; Original ; Oryza sativa ; PHD‐finger ; Plant breeding ; Plant reproductive structures ; Plants (botany) ; Pollen ; pollen exine ; Proteins ; rice ; sporopollenin ; TIP3 ; transcription (genetics) ; Transcription activation ; Transcription factors ; transcriptional activation ; Ubisch bodies</subject><ispartof>The Plant journal : for cell and molecular biology, 2019-09, Vol.99 (5), p.844-861</ispartof><rights>2019 The Authors. published by Society for Experimental Biology and John Wiley & Sons Ltd</rights><rights>2019 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2019 John Wiley & Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4765-d0aa55e80096a228710269b43186448cedacc14337419ad1fa27be4f459519b83</citedby><cites>FETCH-LOGICAL-c4765-d0aa55e80096a228710269b43186448cedacc14337419ad1fa27be4f459519b83</cites><orcidid>0000-0002-0996-600X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Ftpj.14365$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.14365$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31021015$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Zhengfu</creatorcontrib><creatorcontrib>Sun, Lianping</creatorcontrib><creatorcontrib>Zhang, Peipei</creatorcontrib><creatorcontrib>Zhang, Yingxin</creatorcontrib><creatorcontrib>Yu, Ping</creatorcontrib><creatorcontrib>Liu, Ling</creatorcontrib><creatorcontrib>Abbas, Adil</creatorcontrib><creatorcontrib>Xiang, Xiaojiao</creatorcontrib><creatorcontrib>Wu, Weixun</creatorcontrib><creatorcontrib>Zhan, Xiaodeng</creatorcontrib><creatorcontrib>Cao, Liyong</creatorcontrib><creatorcontrib>Cheng, Shihua</creatorcontrib><title>TDR INTERACTING PROTEIN 3, encoding a PHD‐finger transcription factor, regulates Ubisch bodies and pollen wall formation in rice</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary
Male reproductive development involves a complex series of biological events and precise transcriptional regulation is essential for this biological process in flowering plants. Several transcriptional factors have been reported to regulate tapetum and pollen development, however the transcriptional mechanism underlying Ubisch bodies and pollen wall formation remains less understood. Here, we characterized and isolated a male sterility mutant of TDR INTERACTING PROTEIN 3 (TIP3) in rice. The tip3 mutant displayed smaller and pale yellow anthers without mature pollen grains, abnormal Ubisch body morphology, no pollen wall formation, as well as delayed tapetum degeneration. Map‐based cloning demonstrated that TIP3 encodes a conserved PHD‐finger protein and further study confirmed that TIP3 functioned as a transcription factor with transcriptional activation activity. TIP3 is preferentially expressed in the tapetum and microspores during anther development. Moreover, TIP3 can physically interact with TDR, which is a key component of the transcriptional cascade in regulating tapetum development and pollen wall formation. Furthermore, disruption of TIP3 changed the expression of several genes involved in tapetum development and degradation, biosynthesis and transport of lipid monomers of sporopollenin in tip3 mutant. Taken together, our results revealed an unprecedented role for TIP3 in regulating Ubisch bodies and pollen exine formation, and presents a potential tool to manipulate male fertility for hybrid rice breeding.
Significance Statement
TIP3, a PHD‐finger protein, functions as a transcriptional activator and physically interacts with TDR participating in tapetum programmed cell death, Ubisch body morphogenesis and pollen wall formation. Our results provide an insight into the molecular mechanism underlying tapetal programmed cell death (PCD) and pollen wall formation in rice.</description><subject>Anthers</subject><subject>Biological activity</subject><subject>Biosynthesis</subject><subject>Cloning</subject><subject>Degeneration</subject><subject>Disruption</subject><subject>exine</subject><subject>Fertility</subject><subject>Flowering</subject><subject>Flowering plants</subject><subject>Gene expression</subject><subject>Gene regulation</subject><subject>genes</subject><subject>Lipids</subject><subject>male fertility</subject><subject>Male sterility</subject><subject>males</subject><subject>Microspores</subject><subject>molecular cloning</subject><subject>Monomers</subject><subject>Morphology</subject><subject>mutants</subject><subject>Original</subject><subject>Oryza sativa</subject><subject>PHD‐finger</subject><subject>Plant breeding</subject><subject>Plant reproductive structures</subject><subject>Plants (botany)</subject><subject>Pollen</subject><subject>pollen exine</subject><subject>Proteins</subject><subject>rice</subject><subject>sporopollenin</subject><subject>TIP3</subject><subject>transcription (genetics)</subject><subject>Transcription activation</subject><subject>Transcription factors</subject><subject>transcriptional activation</subject><subject>Ubisch bodies</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNqFkt1qFDEYhoModq0eeAMS8ESh2-Zv_k4KZbu2K2W7LFPwLGQymW2WbLImM5aeiVfgNXolfu3WooKYk4-QJ2_yJB9Cryk5pDCO-u36kAqeZ0_QiEIZc8o_PUUjUuVkXAjK9tCLlNaE0ILn4jna45QwSmg2Qt_q0yWezevp8mRSz-ZneLG8rKezOeYH2HgdWutXWOHF-emPr987mJiI-6h80tFuexs87pTuQzzA0awGp3qT8FVjk77GDWyGmfIt3gbnjMc3yjnchbhR9zutx9Fq8xI965RL5tVD3UdXH6b15Hx8cXk2m5xcjLUowKklSmWZKQlYKcbKAhzyqhGclrkQpTat0hpegYNwpVraKVY0RnQiqzJaNSXfR8e73O3QbEyrjQcRJ7fRblS8lUFZ-eeKt9dyFb7IvMxYVhAIePcQEMPnwaRebkDUOKe8CUOSjLOiKhgc-H-U0YzQkooC0Ld_oeswRA8vAVRJWHXnCdT7HaVjSCma7vHelMi7JpDQBPK-CYB987voI_nr1wE42gE31pnbfyfJevFxF_kTlSq6fA</recordid><startdate>201909</startdate><enddate>201909</enddate><creator>Yang, Zhengfu</creator><creator>Sun, Lianping</creator><creator>Zhang, Peipei</creator><creator>Zhang, Yingxin</creator><creator>Yu, Ping</creator><creator>Liu, Ling</creator><creator>Abbas, Adil</creator><creator>Xiang, Xiaojiao</creator><creator>Wu, Weixun</creator><creator>Zhan, Xiaodeng</creator><creator>Cao, Liyong</creator><creator>Cheng, Shihua</creator><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0996-600X</orcidid></search><sort><creationdate>201909</creationdate><title>TDR INTERACTING PROTEIN 3, encoding a PHD‐finger transcription factor, regulates Ubisch bodies and pollen wall formation in rice</title><author>Yang, Zhengfu ; Sun, Lianping ; Zhang, Peipei ; Zhang, Yingxin ; Yu, Ping ; Liu, Ling ; Abbas, Adil ; Xiang, Xiaojiao ; Wu, Weixun ; Zhan, Xiaodeng ; Cao, Liyong ; Cheng, Shihua</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4765-d0aa55e80096a228710269b43186448cedacc14337419ad1fa27be4f459519b83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Anthers</topic><topic>Biological activity</topic><topic>Biosynthesis</topic><topic>Cloning</topic><topic>Degeneration</topic><topic>Disruption</topic><topic>exine</topic><topic>Fertility</topic><topic>Flowering</topic><topic>Flowering plants</topic><topic>Gene expression</topic><topic>Gene regulation</topic><topic>genes</topic><topic>Lipids</topic><topic>male fertility</topic><topic>Male sterility</topic><topic>males</topic><topic>Microspores</topic><topic>molecular cloning</topic><topic>Monomers</topic><topic>Morphology</topic><topic>mutants</topic><topic>Original</topic><topic>Oryza sativa</topic><topic>PHD‐finger</topic><topic>Plant breeding</topic><topic>Plant reproductive structures</topic><topic>Plants (botany)</topic><topic>Pollen</topic><topic>pollen exine</topic><topic>Proteins</topic><topic>rice</topic><topic>sporopollenin</topic><topic>TIP3</topic><topic>transcription (genetics)</topic><topic>Transcription activation</topic><topic>Transcription factors</topic><topic>transcriptional activation</topic><topic>Ubisch bodies</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Zhengfu</creatorcontrib><creatorcontrib>Sun, Lianping</creatorcontrib><creatorcontrib>Zhang, Peipei</creatorcontrib><creatorcontrib>Zhang, Yingxin</creatorcontrib><creatorcontrib>Yu, Ping</creatorcontrib><creatorcontrib>Liu, Ling</creatorcontrib><creatorcontrib>Abbas, Adil</creatorcontrib><creatorcontrib>Xiang, Xiaojiao</creatorcontrib><creatorcontrib>Wu, Weixun</creatorcontrib><creatorcontrib>Zhan, Xiaodeng</creatorcontrib><creatorcontrib>Cao, Liyong</creatorcontrib><creatorcontrib>Cheng, Shihua</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Zhengfu</au><au>Sun, Lianping</au><au>Zhang, Peipei</au><au>Zhang, Yingxin</au><au>Yu, Ping</au><au>Liu, Ling</au><au>Abbas, Adil</au><au>Xiang, Xiaojiao</au><au>Wu, Weixun</au><au>Zhan, Xiaodeng</au><au>Cao, Liyong</au><au>Cheng, Shihua</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>TDR INTERACTING PROTEIN 3, encoding a PHD‐finger transcription factor, regulates Ubisch bodies and pollen wall formation in rice</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2019-09</date><risdate>2019</risdate><volume>99</volume><issue>5</issue><spage>844</spage><epage>861</epage><pages>844-861</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>Summary
Male reproductive development involves a complex series of biological events and precise transcriptional regulation is essential for this biological process in flowering plants. Several transcriptional factors have been reported to regulate tapetum and pollen development, however the transcriptional mechanism underlying Ubisch bodies and pollen wall formation remains less understood. Here, we characterized and isolated a male sterility mutant of TDR INTERACTING PROTEIN 3 (TIP3) in rice. The tip3 mutant displayed smaller and pale yellow anthers without mature pollen grains, abnormal Ubisch body morphology, no pollen wall formation, as well as delayed tapetum degeneration. Map‐based cloning demonstrated that TIP3 encodes a conserved PHD‐finger protein and further study confirmed that TIP3 functioned as a transcription factor with transcriptional activation activity. TIP3 is preferentially expressed in the tapetum and microspores during anther development. Moreover, TIP3 can physically interact with TDR, which is a key component of the transcriptional cascade in regulating tapetum development and pollen wall formation. Furthermore, disruption of TIP3 changed the expression of several genes involved in tapetum development and degradation, biosynthesis and transport of lipid monomers of sporopollenin in tip3 mutant. Taken together, our results revealed an unprecedented role for TIP3 in regulating Ubisch bodies and pollen exine formation, and presents a potential tool to manipulate male fertility for hybrid rice breeding.
Significance Statement
TIP3, a PHD‐finger protein, functions as a transcriptional activator and physically interacts with TDR participating in tapetum programmed cell death, Ubisch body morphogenesis and pollen wall formation. Our results provide an insight into the molecular mechanism underlying tapetal programmed cell death (PCD) and pollen wall formation in rice.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>31021015</pmid><doi>10.1111/tpj.14365</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-0996-600X</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Anthers Biological activity Biosynthesis Cloning Degeneration Disruption exine Fertility Flowering Flowering plants Gene expression Gene regulation genes Lipids male fertility Male sterility males Microspores molecular cloning Monomers Morphology mutants Original Oryza sativa PHD‐finger Plant breeding Plant reproductive structures Plants (botany) Pollen pollen exine Proteins rice sporopollenin TIP3 transcription (genetics) Transcription activation Transcription factors transcriptional activation Ubisch bodies |
| title | TDR INTERACTING PROTEIN 3, encoding a PHD‐finger transcription factor, regulates Ubisch bodies and pollen wall formation in rice |
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