ZmTDM1 encodes a tetratricopeptide repeat domain protein and is required for meiotic exit in maize
SUMMARY Elaborate cell‐cycle control must be adopted to ensure the continuity of the meiotic second division and termination after that. Despite its importance, however, the genetic controls underlying the meiotic cell cycle have not been reported in maize. Here, we characterized a meiotic cell‐cycl...
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Veröffentlicht in: | The Plant journal : for cell and molecular biology 2024-03, Vol.117 (5), p.1517-1527 |
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description | SUMMARY
Elaborate cell‐cycle control must be adopted to ensure the continuity of the meiotic second division and termination after that. Despite its importance, however, the genetic controls underlying the meiotic cell cycle have not been reported in maize. Here, we characterized a meiotic cell‐cycle controller ZmTDM1, which is a homolog of Arabidopsis TDM1 and encodes a canonical tetratricopeptide repeat domain protein in maize. The Zmtdm1 homozygous plants exhibited complete male sterility and severe female abortion. In Zmtdm1 mutants, cell‐cycle progression was almost identical to that of wild type from leptotene to anaphase II. However, chromosomes in the tetrad failed meiotic termination at the end of the second division and underwent additional divisions in succession without DNA replication, reducing the ploidy to less than haploid in the product. In addition, two ZmTDM1‐like homologs (ZmTDML1 and ZmTDML2) were not functional in meiotic cell‐cycle control. Moreover, ZmTDM1 interacted with RING‐type E3 ubiquitin ligase, revealing that it acts as a subunit of the APC/C E3 ubiquitin ligase complex. Overall, our results identified a regulator of meiotic cell cycle in maize and demonstrated that ZmTDM1 is essential for meiotic exit after meiosis II.
Significance Statement
In this study, we identified that ZmTDM1 is a regulator of meiotic cell‐cycle control in maize. It encodes a protein harboring four tetratricopeptide repeats (TPR) and is required for determining meiosis exit after the second meiotic division. |
doi_str_mv | 10.1111/tpj.16579 |
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Elaborate cell‐cycle control must be adopted to ensure the continuity of the meiotic second division and termination after that. Despite its importance, however, the genetic controls underlying the meiotic cell cycle have not been reported in maize. Here, we characterized a meiotic cell‐cycle controller ZmTDM1, which is a homolog of Arabidopsis TDM1 and encodes a canonical tetratricopeptide repeat domain protein in maize. The Zmtdm1 homozygous plants exhibited complete male sterility and severe female abortion. In Zmtdm1 mutants, cell‐cycle progression was almost identical to that of wild type from leptotene to anaphase II. However, chromosomes in the tetrad failed meiotic termination at the end of the second division and underwent additional divisions in succession without DNA replication, reducing the ploidy to less than haploid in the product. In addition, two ZmTDM1‐like homologs (ZmTDML1 and ZmTDML2) were not functional in meiotic cell‐cycle control. Moreover, ZmTDM1 interacted with RING‐type E3 ubiquitin ligase, revealing that it acts as a subunit of the APC/C E3 ubiquitin ligase complex. Overall, our results identified a regulator of meiotic cell cycle in maize and demonstrated that ZmTDM1 is essential for meiotic exit after meiosis II.
Significance Statement
In this study, we identified that ZmTDM1 is a regulator of meiotic cell‐cycle control in maize. It encodes a protein harboring four tetratricopeptide repeats (TPR) and is required for determining meiosis exit after the second meiotic division.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.16579</identifier><identifier>PMID: 38047628</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Anaphase ; Anaphase-Promoting Complex-Cyclosome - genetics ; Anaphase-Promoting Complex-Cyclosome - metabolism ; APC/C ; Arabidopsis - genetics ; Cell cycle ; Cell Cycle Proteins - genetics ; Cell Cycle Proteins - metabolism ; chromosome ; Chromosomes ; Corn ; DNA biosynthesis ; Homology ; maize ; Male sterility ; Meiosis ; Meiosis - genetics ; Ploidy ; Proteins ; Tetratricopeptide Repeat ; Ubiquitin-protein ligase ; Ubiquitin-Protein Ligases - metabolism ; Zea mays - genetics ; Zea mays - metabolism ; ZmTDM1</subject><ispartof>The Plant journal : for cell and molecular biology, 2024-03, Vol.117 (5), p.1517-1527</ispartof><rights>2023 Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2024 Society for Experimental Biology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3139-2158112efd2872b8f2eda77a36528926ae70437be68d8e57d0e9b4eff04467893</cites><orcidid>0000-0002-1381-5087 ; 0000-0003-3640-8502</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.16579$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.16579$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38047628$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Ting</creatorcontrib><creatorcontrib>Zhao, Shuang‐Hui</creatorcontrib><creatorcontrib>He, Yan</creatorcontrib><title>ZmTDM1 encodes a tetratricopeptide repeat domain protein and is required for meiotic exit in maize</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
Elaborate cell‐cycle control must be adopted to ensure the continuity of the meiotic second division and termination after that. Despite its importance, however, the genetic controls underlying the meiotic cell cycle have not been reported in maize. Here, we characterized a meiotic cell‐cycle controller ZmTDM1, which is a homolog of Arabidopsis TDM1 and encodes a canonical tetratricopeptide repeat domain protein in maize. The Zmtdm1 homozygous plants exhibited complete male sterility and severe female abortion. In Zmtdm1 mutants, cell‐cycle progression was almost identical to that of wild type from leptotene to anaphase II. However, chromosomes in the tetrad failed meiotic termination at the end of the second division and underwent additional divisions in succession without DNA replication, reducing the ploidy to less than haploid in the product. In addition, two ZmTDM1‐like homologs (ZmTDML1 and ZmTDML2) were not functional in meiotic cell‐cycle control. Moreover, ZmTDM1 interacted with RING‐type E3 ubiquitin ligase, revealing that it acts as a subunit of the APC/C E3 ubiquitin ligase complex. Overall, our results identified a regulator of meiotic cell cycle in maize and demonstrated that ZmTDM1 is essential for meiotic exit after meiosis II.
Significance Statement
In this study, we identified that ZmTDM1 is a regulator of meiotic cell‐cycle control in maize. It encodes a protein harboring four tetratricopeptide repeats (TPR) and is required for determining meiosis exit after the second meiotic division.</description><subject>Anaphase</subject><subject>Anaphase-Promoting Complex-Cyclosome - genetics</subject><subject>Anaphase-Promoting Complex-Cyclosome - metabolism</subject><subject>APC/C</subject><subject>Arabidopsis - genetics</subject><subject>Cell cycle</subject><subject>Cell Cycle Proteins - genetics</subject><subject>Cell Cycle Proteins - metabolism</subject><subject>chromosome</subject><subject>Chromosomes</subject><subject>Corn</subject><subject>DNA biosynthesis</subject><subject>Homology</subject><subject>maize</subject><subject>Male sterility</subject><subject>Meiosis</subject><subject>Meiosis - genetics</subject><subject>Ploidy</subject><subject>Proteins</subject><subject>Tetratricopeptide Repeat</subject><subject>Ubiquitin-protein ligase</subject><subject>Ubiquitin-Protein Ligases - metabolism</subject><subject>Zea mays - genetics</subject><subject>Zea mays - metabolism</subject><subject>ZmTDM1</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kEtP3DAURq2qqAy0i_4BZKmbsgj4FdtZoqG8BGoXU6nqxnLiG8mjSRxsRzx-PS5DWSBxN3dxj48-fwh9peSIljnO0_qIylo1H9CCcllXnPI_H9GCNJJUSlC2i_ZSWhNCFZfiE9rlmgglmV6g9u-wOr2hGMYuOEjY4gw52hx9FyaYsneAI0xgM3ZhsH7EUwwZyrajwz6V4-3sIzjch4gH8CH7DsO9z7gw5cEjfEY7vd0k-PKy99Hvsx-r5UV1_fP8cnlyXXUlblMxWmtKGfSOacVa3TNwVilb_sN0w6QFRQRXLUjtNNTKEWhaAX1PhJBKN3wffd96S8LbGVI2g08dbDZ2hDAnUyxKaMkVKei3N-g6zHEs6QxrONW1Es_U4ZbqYkgpQm-m6AcbHwwl5l_xphRvnosv7MGLcW4HcK_k_6YLcLwF7vwGHt43mdWvq63yCXpYjBs</recordid><startdate>202403</startdate><enddate>202403</enddate><creator>Zhang, Ting</creator><creator>Zhao, Shuang‐Hui</creator><creator>He, Yan</creator><general>Blackwell Publishing Ltd</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>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><orcidid>https://orcid.org/0000-0002-1381-5087</orcidid><orcidid>https://orcid.org/0000-0003-3640-8502</orcidid></search><sort><creationdate>202403</creationdate><title>ZmTDM1 encodes a tetratricopeptide repeat domain protein and is required for meiotic exit in maize</title><author>Zhang, Ting ; Zhao, Shuang‐Hui ; He, Yan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3139-2158112efd2872b8f2eda77a36528926ae70437be68d8e57d0e9b4eff04467893</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Anaphase</topic><topic>Anaphase-Promoting Complex-Cyclosome - genetics</topic><topic>Anaphase-Promoting Complex-Cyclosome - metabolism</topic><topic>APC/C</topic><topic>Arabidopsis - genetics</topic><topic>Cell cycle</topic><topic>Cell Cycle Proteins - genetics</topic><topic>Cell Cycle Proteins - metabolism</topic><topic>chromosome</topic><topic>Chromosomes</topic><topic>Corn</topic><topic>DNA biosynthesis</topic><topic>Homology</topic><topic>maize</topic><topic>Male sterility</topic><topic>Meiosis</topic><topic>Meiosis - genetics</topic><topic>Ploidy</topic><topic>Proteins</topic><topic>Tetratricopeptide Repeat</topic><topic>Ubiquitin-protein ligase</topic><topic>Ubiquitin-Protein Ligases - metabolism</topic><topic>Zea mays - genetics</topic><topic>Zea mays - metabolism</topic><topic>ZmTDM1</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Ting</creatorcontrib><creatorcontrib>Zhao, Shuang‐Hui</creatorcontrib><creatorcontrib>He, Yan</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</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><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Ting</au><au>Zhao, Shuang‐Hui</au><au>He, Yan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>ZmTDM1 encodes a tetratricopeptide repeat domain protein and is required for meiotic exit in maize</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2024-03</date><risdate>2024</risdate><volume>117</volume><issue>5</issue><spage>1517</spage><epage>1527</epage><pages>1517-1527</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>SUMMARY
Elaborate cell‐cycle control must be adopted to ensure the continuity of the meiotic second division and termination after that. Despite its importance, however, the genetic controls underlying the meiotic cell cycle have not been reported in maize. Here, we characterized a meiotic cell‐cycle controller ZmTDM1, which is a homolog of Arabidopsis TDM1 and encodes a canonical tetratricopeptide repeat domain protein in maize. The Zmtdm1 homozygous plants exhibited complete male sterility and severe female abortion. In Zmtdm1 mutants, cell‐cycle progression was almost identical to that of wild type from leptotene to anaphase II. However, chromosomes in the tetrad failed meiotic termination at the end of the second division and underwent additional divisions in succession without DNA replication, reducing the ploidy to less than haploid in the product. In addition, two ZmTDM1‐like homologs (ZmTDML1 and ZmTDML2) were not functional in meiotic cell‐cycle control. Moreover, ZmTDM1 interacted with RING‐type E3 ubiquitin ligase, revealing that it acts as a subunit of the APC/C E3 ubiquitin ligase complex. Overall, our results identified a regulator of meiotic cell cycle in maize and demonstrated that ZmTDM1 is essential for meiotic exit after meiosis II.
Significance Statement
In this study, we identified that ZmTDM1 is a regulator of meiotic cell‐cycle control in maize. It encodes a protein harboring four tetratricopeptide repeats (TPR) and is required for determining meiosis exit after the second meiotic division.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>38047628</pmid><doi>10.1111/tpj.16579</doi><tpages>1527</tpages><orcidid>https://orcid.org/0000-0002-1381-5087</orcidid><orcidid>https://orcid.org/0000-0003-3640-8502</orcidid></addata></record> |
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subjects | Anaphase Anaphase-Promoting Complex-Cyclosome - genetics Anaphase-Promoting Complex-Cyclosome - metabolism APC/C Arabidopsis - genetics Cell cycle Cell Cycle Proteins - genetics Cell Cycle Proteins - metabolism chromosome Chromosomes Corn DNA biosynthesis Homology maize Male sterility Meiosis Meiosis - genetics Ploidy Proteins Tetratricopeptide Repeat Ubiquitin-protein ligase Ubiquitin-Protein Ligases - metabolism Zea mays - genetics Zea mays - metabolism ZmTDM1 |
title | ZmTDM1 encodes a tetratricopeptide repeat domain protein and is required for meiotic exit in maize |
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