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Defects in meiotic chromosome segregation lead to unreduced male gametes in Arabidopsis SMC5/6 complex mutants
Structural maintenance of chromosome 5/6 (SMC5/6) complex is a crucial factor for preserving genome stability. Here, we show that mutants for several Arabidopsis (Arabidopsis thaliana) SMC5/6 complex subunits produce triploid offspring. This phenotype is caused by a meiotic defect leading to the pro...
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Published in: | The Plant cell 2021-09, Vol.33 (9), p.3104-3119 |
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container_title | The Plant cell |
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creator | Yang, Fen Fernández-Jiménez, Nadia Tučková, Martina Vrána, Jan Cápal, Petr Díaz, Mariana Pradillo, Mónica Pecinka, Ales |
description | Structural maintenance of chromosome 5/6 (SMC5/6) complex is a crucial factor for preserving genome stability. Here, we show that mutants for several Arabidopsis (Arabidopsis thaliana) SMC5/6 complex subunits produce triploid offspring. This phenotype is caused by a meiotic defect leading to the production of unreduced male gametes. The SMC5/6 complex mutants show an absence of chromosome segregation during the first and/or the second meiotic division, as well as a partially disorganized microtubule network. Importantly, although the SMC5/6 complex is partly required for the repair of SPO11-induced DNA double-strand breaks, the nonreduction described here is SPO11-independent. The measured high rate of ovule abortion suggests that, if produced, such defects are maternally lethal. Upon fertilization with an unreduced pollen, the unbalanced maternal and paternal genome dosage in the endosperm most likely causes seed abortion observed in several SMC5/6 complex mutants. In conclusion, we describe the function of the SMC5/6 complex in the maintenance of gametophytic ploidy in Arabidopsis. |
doi_str_mv | 10.1093/plcell/koab178 |
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Here, we show that mutants for several Arabidopsis (Arabidopsis thaliana) SMC5/6 complex subunits produce triploid offspring. This phenotype is caused by a meiotic defect leading to the production of unreduced male gametes. The SMC5/6 complex mutants show an absence of chromosome segregation during the first and/or the second meiotic division, as well as a partially disorganized microtubule network. Importantly, although the SMC5/6 complex is partly required for the repair of SPO11-induced DNA double-strand breaks, the nonreduction described here is SPO11-independent. The measured high rate of ovule abortion suggests that, if produced, such defects are maternally lethal. Upon fertilization with an unreduced pollen, the unbalanced maternal and paternal genome dosage in the endosperm most likely causes seed abortion observed in several SMC5/6 complex mutants. In conclusion, we describe the function of the SMC5/6 complex in the maintenance of gametophytic ploidy in Arabidopsis.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1093/plcell/koab178</identifier><identifier>PMID: 34240187</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Chromosome Segregation ; DNA Breaks, Double-Stranded ; Meiosis ; Pollen - genetics ; Pollen - growth & development</subject><ispartof>The Plant cell, 2021-09, Vol.33 (9), p.3104-3119</ispartof><rights>American Society of Plant Biologists 2021. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><rights>American Society of Plant Biologists 2021. All rights reserved. For permissions, please email: journals.permissions@oup.com 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c390t-c6b042201613e1281bd9dabacb37c561f659c7d8429537a3bc4934cfe8bbdf833</citedby><cites>FETCH-LOGICAL-c390t-c6b042201613e1281bd9dabacb37c561f659c7d8429537a3bc4934cfe8bbdf833</cites><orcidid>0000-0003-3887-3897 ; 0000-0002-0483-8041 ; 0000-0002-3048-4259 ; 0000-0001-6171-8516 ; 0000-0001-9277-1766 ; 0000-0002-4196-0134 ; 0000-0001-6625-6015 ; 0000-0002-8888-9101</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34240187$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Fen</creatorcontrib><creatorcontrib>Fernández-Jiménez, Nadia</creatorcontrib><creatorcontrib>Tučková, Martina</creatorcontrib><creatorcontrib>Vrána, Jan</creatorcontrib><creatorcontrib>Cápal, Petr</creatorcontrib><creatorcontrib>Díaz, Mariana</creatorcontrib><creatorcontrib>Pradillo, Mónica</creatorcontrib><creatorcontrib>Pecinka, Ales</creatorcontrib><title>Defects in meiotic chromosome segregation lead to unreduced male gametes in Arabidopsis SMC5/6 complex mutants</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>Structural maintenance of chromosome 5/6 (SMC5/6) complex is a crucial factor for preserving genome stability. Here, we show that mutants for several Arabidopsis (Arabidopsis thaliana) SMC5/6 complex subunits produce triploid offspring. This phenotype is caused by a meiotic defect leading to the production of unreduced male gametes. The SMC5/6 complex mutants show an absence of chromosome segregation during the first and/or the second meiotic division, as well as a partially disorganized microtubule network. Importantly, although the SMC5/6 complex is partly required for the repair of SPO11-induced DNA double-strand breaks, the nonreduction described here is SPO11-independent. The measured high rate of ovule abortion suggests that, if produced, such defects are maternally lethal. Upon fertilization with an unreduced pollen, the unbalanced maternal and paternal genome dosage in the endosperm most likely causes seed abortion observed in several SMC5/6 complex mutants. In conclusion, we describe the function of the SMC5/6 complex in the maintenance of gametophytic ploidy in Arabidopsis.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Chromosome Segregation</subject><subject>DNA Breaks, Double-Stranded</subject><subject>Meiosis</subject><subject>Pollen - genetics</subject><subject>Pollen - growth & development</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNpVkUlvFDEQhS0URBa4ckQ-5tIzXnu5RIomkCAFcQAkbpaX6omh3e7Y7gj-fXqYYQSnKqlefa9UD6G3lKwo6fh6GiwMw_pn1IY27Qt0RiVnFeva7ydLTwSpRC3pKTrP-QchhDa0e4VOuWCC0LY5Q-MN9GBLxn7EAXws3mL7kGKIOQbAGbYJtrr4OOIBtMMl4nlM4GYLDgc9AN7qAAX-AK6TNt7FKfuMv3zayHWNbQzTAL9wmIseS36NXvZ6yPDmUC_Qtw_vv27uqvvPtx831_eV5R0pla0NEYwRWlMOlLXUuM5po63hjZU17WvZ2ca1gnWSN5obKzoubA-tMa5vOb9AV3vuNJsAzsJYkh7UlHzQ6beK2qv_J6N_UNv4pFpRL3ZkAVweACk-zpCLCj7vXq1HiHNWTErC6oYwuUhXe6lNMecE_dGGErULSe1DUoeQloV3_x53lP9NhT8DbJqSsQ</recordid><startdate>20210924</startdate><enddate>20210924</enddate><creator>Yang, Fen</creator><creator>Fernández-Jiménez, Nadia</creator><creator>Tučková, Martina</creator><creator>Vrána, Jan</creator><creator>Cápal, Petr</creator><creator>Díaz, Mariana</creator><creator>Pradillo, Mónica</creator><creator>Pecinka, Ales</creator><general>Oxford University Press</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-3887-3897</orcidid><orcidid>https://orcid.org/0000-0002-0483-8041</orcidid><orcidid>https://orcid.org/0000-0002-3048-4259</orcidid><orcidid>https://orcid.org/0000-0001-6171-8516</orcidid><orcidid>https://orcid.org/0000-0001-9277-1766</orcidid><orcidid>https://orcid.org/0000-0002-4196-0134</orcidid><orcidid>https://orcid.org/0000-0001-6625-6015</orcidid><orcidid>https://orcid.org/0000-0002-8888-9101</orcidid></search><sort><creationdate>20210924</creationdate><title>Defects in meiotic chromosome segregation lead to unreduced male gametes in Arabidopsis SMC5/6 complex mutants</title><author>Yang, Fen ; Fernández-Jiménez, Nadia ; Tučková, Martina ; Vrána, Jan ; Cápal, Petr ; Díaz, Mariana ; Pradillo, Mónica ; Pecinka, Ales</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c390t-c6b042201613e1281bd9dabacb37c561f659c7d8429537a3bc4934cfe8bbdf833</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Chromosome Segregation</topic><topic>DNA Breaks, Double-Stranded</topic><topic>Meiosis</topic><topic>Pollen - genetics</topic><topic>Pollen - growth & development</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Fen</creatorcontrib><creatorcontrib>Fernández-Jiménez, Nadia</creatorcontrib><creatorcontrib>Tučková, Martina</creatorcontrib><creatorcontrib>Vrána, Jan</creatorcontrib><creatorcontrib>Cápal, Petr</creatorcontrib><creatorcontrib>Díaz, Mariana</creatorcontrib><creatorcontrib>Pradillo, Mónica</creatorcontrib><creatorcontrib>Pecinka, Ales</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>PubMed Central (Full Participant titles)</collection><jtitle>The Plant cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Fen</au><au>Fernández-Jiménez, Nadia</au><au>Tučková, Martina</au><au>Vrána, Jan</au><au>Cápal, Petr</au><au>Díaz, Mariana</au><au>Pradillo, Mónica</au><au>Pecinka, Ales</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Defects in meiotic chromosome segregation lead to unreduced male gametes in Arabidopsis SMC5/6 complex mutants</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2021-09-24</date><risdate>2021</risdate><volume>33</volume><issue>9</issue><spage>3104</spage><epage>3119</epage><pages>3104-3119</pages><issn>1040-4651</issn><eissn>1532-298X</eissn><abstract>Structural maintenance of chromosome 5/6 (SMC5/6) complex is a crucial factor for preserving genome stability. Here, we show that mutants for several Arabidopsis (Arabidopsis thaliana) SMC5/6 complex subunits produce triploid offspring. This phenotype is caused by a meiotic defect leading to the production of unreduced male gametes. The SMC5/6 complex mutants show an absence of chromosome segregation during the first and/or the second meiotic division, as well as a partially disorganized microtubule network. Importantly, although the SMC5/6 complex is partly required for the repair of SPO11-induced DNA double-strand breaks, the nonreduction described here is SPO11-independent. The measured high rate of ovule abortion suggests that, if produced, such defects are maternally lethal. Upon fertilization with an unreduced pollen, the unbalanced maternal and paternal genome dosage in the endosperm most likely causes seed abortion observed in several SMC5/6 complex mutants. In conclusion, we describe the function of the SMC5/6 complex in the maintenance of gametophytic ploidy in Arabidopsis.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>34240187</pmid><doi>10.1093/plcell/koab178</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0003-3887-3897</orcidid><orcidid>https://orcid.org/0000-0002-0483-8041</orcidid><orcidid>https://orcid.org/0000-0002-3048-4259</orcidid><orcidid>https://orcid.org/0000-0001-6171-8516</orcidid><orcidid>https://orcid.org/0000-0001-9277-1766</orcidid><orcidid>https://orcid.org/0000-0002-4196-0134</orcidid><orcidid>https://orcid.org/0000-0001-6625-6015</orcidid><orcidid>https://orcid.org/0000-0002-8888-9101</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Chromosome Segregation DNA Breaks, Double-Stranded Meiosis Pollen - genetics Pollen - growth & development |
title | Defects in meiotic chromosome segregation lead to unreduced male gametes in Arabidopsis SMC5/6 complex mutants |
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