RETINOBLASTOMA RELATED 1 switches mitosis to meiosis in rice
The transition from mitosis to meiosis is a critical event in the reproductive development of all sexually reproducing species. However, the mechanisms that regulate this process in plants remain largely unknown. Here, we find that the rice (Oryza sativa L.) protein RETINOBLASTOMA RELATED 1 (RBR1) i...
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description | The transition from mitosis to meiosis is a critical event in the reproductive development of all sexually reproducing species. However, the mechanisms that regulate this process in plants remain largely unknown. Here, we find that the rice (Oryza sativa L.) protein RETINOBLASTOMA RELATED 1 (RBR1) is essential to the transition from mitosis to meiosis. Loss of RBR1 function results in hyper-proliferative sporogenous-cell-like cells (SCLs) in the anther locules during early stages of reproductive development. These hyper-proliferative SCLs are unable to initiate meiosis, eventually stagnating and degrading at late developmental stages to form pollen-free anthers. These results suggest that RBR1 acts as a gatekeeper of entry into meiosis. Furthermore, cytokinin content is significantly increased in rbr1 mutants, whereas the expression of type-B response factors, particularly LEPTO1, is significantly reduced. Given the known close association of cytokinins with cell proliferation, these findings imply that hyper-proliferative germ cells in the anther locules may be attributed to elevated cytokinin concentrations and disruptions in the cytokinin pathway. Using a genetic strategy, the association between germ cell hyper-proliferation and disturbed cytokinin signaling in rbr1 has been confirmed. In summary, we reveal a unique role of RBR1 in the initiation of meiosis; our results clearly demonstrate that the RBR1 regulatory module is connected to the cytokinin signaling pathway and switches mitosis to meiosis in rice.
This study provides evidence demonstrating that rice RBR1 serves as a molecular switch between mitosis and meiosis. The absence of LEPTO1 in rbr1-1 lepto1 exacerbates the impaired meiosis entry of rbr1 mutants, suggesting that RBR1 governs the transition from mitosis to meiosis through interactions with the cytokinin signaling pathway. |
doi_str_mv | 10.1016/j.xplc.2024.100857 |
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This study provides evidence demonstrating that rice RBR1 serves as a molecular switch between mitosis and meiosis. The absence of LEPTO1 in rbr1-1 lepto1 exacerbates the impaired meiosis entry of rbr1 mutants, suggesting that RBR1 governs the transition from mitosis to meiosis through interactions with the cytokinin signaling pathway.</description><identifier>ISSN: 2590-3462</identifier><identifier>EISSN: 2590-3462</identifier><identifier>DOI: 10.1016/j.xplc.2024.100857</identifier><identifier>PMID: 38433446</identifier><language>eng</language><publisher>China: Elsevier Inc</publisher><subject>cytokinin ; Cytokinins - metabolism ; Gene Expression Regulation, Plant ; Meiosis - genetics ; meiosis initiation ; Mitosis ; Oryza - genetics ; Oryza - metabolism ; Plant Proteins - genetics ; Plant Proteins - metabolism ; RETINOBLASTOMA RELATED1 ; rice</subject><ispartof>Plant communications, 2024-06, Vol.5 (6), p.100857, Article 100857</ispartof><rights>2024 The Author(s)</rights><rights>Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c351t-d2b72934b297638d24e9aac25fd3ecbdde88de3a7831a5e7666aef2befa7088d3</cites><orcidid>0000-0001-8428-8010 ; 0000-0002-0844-1121</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,782,786,866,27931,27932</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38433446$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Miao, Yongjie</creatorcontrib><creatorcontrib>You, Hanli</creatorcontrib><creatorcontrib>Liu, Huixin</creatorcontrib><creatorcontrib>Zhao, Yangzi</creatorcontrib><creatorcontrib>Zhao, Jiangzhe</creatorcontrib><creatorcontrib>Li, Yafei</creatorcontrib><creatorcontrib>Shen, Yi</creatorcontrib><creatorcontrib>Tang, Ding</creatorcontrib><creatorcontrib>Liu, Baohui</creatorcontrib><creatorcontrib>Zhang, Kewei</creatorcontrib><creatorcontrib>Cheng, Zhukuan</creatorcontrib><title>RETINOBLASTOMA RELATED 1 switches mitosis to meiosis in rice</title><title>Plant communications</title><addtitle>Plant Commun</addtitle><description>The transition from mitosis to meiosis is a critical event in the reproductive development of all sexually reproducing species. However, the mechanisms that regulate this process in plants remain largely unknown. Here, we find that the rice (Oryza sativa L.) protein RETINOBLASTOMA RELATED 1 (RBR1) is essential to the transition from mitosis to meiosis. Loss of RBR1 function results in hyper-proliferative sporogenous-cell-like cells (SCLs) in the anther locules during early stages of reproductive development. These hyper-proliferative SCLs are unable to initiate meiosis, eventually stagnating and degrading at late developmental stages to form pollen-free anthers. These results suggest that RBR1 acts as a gatekeeper of entry into meiosis. Furthermore, cytokinin content is significantly increased in rbr1 mutants, whereas the expression of type-B response factors, particularly LEPTO1, is significantly reduced. Given the known close association of cytokinins with cell proliferation, these findings imply that hyper-proliferative germ cells in the anther locules may be attributed to elevated cytokinin concentrations and disruptions in the cytokinin pathway. Using a genetic strategy, the association between germ cell hyper-proliferation and disturbed cytokinin signaling in rbr1 has been confirmed. In summary, we reveal a unique role of RBR1 in the initiation of meiosis; our results clearly demonstrate that the RBR1 regulatory module is connected to the cytokinin signaling pathway and switches mitosis to meiosis in rice.
This study provides evidence demonstrating that rice RBR1 serves as a molecular switch between mitosis and meiosis. The absence of LEPTO1 in rbr1-1 lepto1 exacerbates the impaired meiosis entry of rbr1 mutants, suggesting that RBR1 governs the transition from mitosis to meiosis through interactions with the cytokinin signaling pathway.</description><subject>cytokinin</subject><subject>Cytokinins - metabolism</subject><subject>Gene Expression Regulation, Plant</subject><subject>Meiosis - genetics</subject><subject>meiosis initiation</subject><subject>Mitosis</subject><subject>Oryza - genetics</subject><subject>Oryza - metabolism</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>RETINOBLASTOMA RELATED1</subject><subject>rice</subject><issn>2590-3462</issn><issn>2590-3462</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kEtPwzAQhC0EolXpH-CAcuTS4lecROollACVApVKOFuOvRGukqbEKY9_T0oK4sRpR7szI-2H0DnBU4KJuFpPP7alnlJMebfAoR8coSH1IzxhXNDjP3qAxs6tMcbUJ0Qw_xQNWMgZ41wM0WyVZIvH5XUaP2XLh9hbJWmcJTce8dy7bfULOK-ybe2s89raq8B-S7vxGqvhDJ0UqnQwPswRer5Nsvn9JF3eLeZxOtHMJ-3E0DygEeM5jQLBQkM5REpp6heGgc6NgTA0wFQQMqJ8CIQQCgqaQ6EC3J3YCF32vdumft2Ba2VlnYayVBuod0525QFjPuais9LeqpvauQYKuW1spZpPSbDcg5NruQcn9-BkD64LXRz6d3kF5jfyg6kzzHoDdF--WWik0xY2GoxtQLfS1Pa__i9Vq3w-</recordid><startdate>20240610</startdate><enddate>20240610</enddate><creator>Miao, Yongjie</creator><creator>You, Hanli</creator><creator>Liu, Huixin</creator><creator>Zhao, Yangzi</creator><creator>Zhao, Jiangzhe</creator><creator>Li, Yafei</creator><creator>Shen, Yi</creator><creator>Tang, Ding</creator><creator>Liu, Baohui</creator><creator>Zhang, Kewei</creator><creator>Cheng, Zhukuan</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><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><orcidid>https://orcid.org/0000-0001-8428-8010</orcidid><orcidid>https://orcid.org/0000-0002-0844-1121</orcidid></search><sort><creationdate>20240610</creationdate><title>RETINOBLASTOMA RELATED 1 switches mitosis to meiosis in rice</title><author>Miao, Yongjie ; You, Hanli ; Liu, Huixin ; Zhao, Yangzi ; Zhao, Jiangzhe ; Li, Yafei ; Shen, Yi ; Tang, Ding ; Liu, Baohui ; Zhang, Kewei ; Cheng, Zhukuan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c351t-d2b72934b297638d24e9aac25fd3ecbdde88de3a7831a5e7666aef2befa7088d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>cytokinin</topic><topic>Cytokinins - metabolism</topic><topic>Gene Expression Regulation, Plant</topic><topic>Meiosis - genetics</topic><topic>meiosis initiation</topic><topic>Mitosis</topic><topic>Oryza - genetics</topic><topic>Oryza - metabolism</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>RETINOBLASTOMA RELATED1</topic><topic>rice</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Miao, Yongjie</creatorcontrib><creatorcontrib>You, Hanli</creatorcontrib><creatorcontrib>Liu, Huixin</creatorcontrib><creatorcontrib>Zhao, Yangzi</creatorcontrib><creatorcontrib>Zhao, Jiangzhe</creatorcontrib><creatorcontrib>Li, Yafei</creatorcontrib><creatorcontrib>Shen, Yi</creatorcontrib><creatorcontrib>Tang, Ding</creatorcontrib><creatorcontrib>Liu, Baohui</creatorcontrib><creatorcontrib>Zhang, Kewei</creatorcontrib><creatorcontrib>Cheng, Zhukuan</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><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><jtitle>Plant communications</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Miao, Yongjie</au><au>You, Hanli</au><au>Liu, Huixin</au><au>Zhao, Yangzi</au><au>Zhao, Jiangzhe</au><au>Li, Yafei</au><au>Shen, Yi</au><au>Tang, Ding</au><au>Liu, Baohui</au><au>Zhang, Kewei</au><au>Cheng, Zhukuan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>RETINOBLASTOMA RELATED 1 switches mitosis to meiosis in rice</atitle><jtitle>Plant communications</jtitle><addtitle>Plant Commun</addtitle><date>2024-06-10</date><risdate>2024</risdate><volume>5</volume><issue>6</issue><spage>100857</spage><pages>100857-</pages><artnum>100857</artnum><issn>2590-3462</issn><eissn>2590-3462</eissn><abstract>The transition from mitosis to meiosis is a critical event in the reproductive development of all sexually reproducing species. However, the mechanisms that regulate this process in plants remain largely unknown. Here, we find that the rice (Oryza sativa L.) protein RETINOBLASTOMA RELATED 1 (RBR1) is essential to the transition from mitosis to meiosis. Loss of RBR1 function results in hyper-proliferative sporogenous-cell-like cells (SCLs) in the anther locules during early stages of reproductive development. These hyper-proliferative SCLs are unable to initiate meiosis, eventually stagnating and degrading at late developmental stages to form pollen-free anthers. These results suggest that RBR1 acts as a gatekeeper of entry into meiosis. Furthermore, cytokinin content is significantly increased in rbr1 mutants, whereas the expression of type-B response factors, particularly LEPTO1, is significantly reduced. Given the known close association of cytokinins with cell proliferation, these findings imply that hyper-proliferative germ cells in the anther locules may be attributed to elevated cytokinin concentrations and disruptions in the cytokinin pathway. Using a genetic strategy, the association between germ cell hyper-proliferation and disturbed cytokinin signaling in rbr1 has been confirmed. In summary, we reveal a unique role of RBR1 in the initiation of meiosis; our results clearly demonstrate that the RBR1 regulatory module is connected to the cytokinin signaling pathway and switches mitosis to meiosis in rice.
This study provides evidence demonstrating that rice RBR1 serves as a molecular switch between mitosis and meiosis. The absence of LEPTO1 in rbr1-1 lepto1 exacerbates the impaired meiosis entry of rbr1 mutants, suggesting that RBR1 governs the transition from mitosis to meiosis through interactions with the cytokinin signaling pathway.</abstract><cop>China</cop><pub>Elsevier Inc</pub><pmid>38433446</pmid><doi>10.1016/j.xplc.2024.100857</doi><orcidid>https://orcid.org/0000-0001-8428-8010</orcidid><orcidid>https://orcid.org/0000-0002-0844-1121</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | cytokinin Cytokinins - metabolism Gene Expression Regulation, Plant Meiosis - genetics meiosis initiation Mitosis Oryza - genetics Oryza - metabolism Plant Proteins - genetics Plant Proteins - metabolism RETINOBLASTOMA RELATED1 rice |
title | RETINOBLASTOMA RELATED 1 switches mitosis to meiosis in rice |
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