MYB3R-mediated active repression of cell cycle and growth under salt stress in Arabidopsis thaliana
Under environmental stress, plants are believed to actively repress their growth to save resource and alter its allocation to acquire tolerance against the stress. Although a lot of studies have uncovered precise mechanisms for responding to stress and acquiring tolerance, the mechanisms for regulat...
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Veröffentlicht in: | Journal of plant research 2021-03, Vol.134 (2), p.261-277 |
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creator | Okumura, Toru Nomoto, Yuji Kobayashi, Kosuke Suzuki, Takamasa Takatsuka, Hirotomo Ito, Masaki |
description | Under environmental stress, plants are believed to actively repress their growth to save resource and alter its allocation to acquire tolerance against the stress. Although a lot of studies have uncovered precise mechanisms for responding to stress and acquiring tolerance, the mechanisms for regulating growth repression under stress are not as well understood. It is especially unclear which particular genes related to cell cycle control are involved in active growth repression. Here, we showed that decreased growth in plants exposed to moderate salt stress is mediated by MYB3R transcription factors that have been known to positively and negatively regulate the transcription of G2/M-specific genes. Our genome-wide gene expression analysis revealed occurrences of general downregulation of G2/M-specific genes in Arabidopsis under salt stress. Importantly, this downregulation is significantly and universally mitigated by the loss of MYB3R repressors by mutations. Accordingly, the growth performance of Arabidopsis plants under salt stress is significantly recovered in mutants lacking MYB3R repressors. This growth recovery involves improved cell proliferation that is possibly due to prolonging and accelerating cell proliferation, which were partly suggested by enlarged root meristem and increased number of cells positive for CYCB1;1-GUS. Our ploidy analysis further suggested that cell cycle progression at the G2 phase was delayed under salt stress, and this delay was recovered by loss of MYB3R repressors. Under salt stress, the changes in expression of MYB3R activators and repressors at both the mRNA and protein levels were not significant. This observation suggests novel mechanisms underlying MYB3R-mediated growth repression under salt stress that are different from the mechanisms operating under other stress conditions such as DNA damage and high temperature. |
doi_str_mv | 10.1007/s10265-020-01250-8 |
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Although a lot of studies have uncovered precise mechanisms for responding to stress and acquiring tolerance, the mechanisms for regulating growth repression under stress are not as well understood. It is especially unclear which particular genes related to cell cycle control are involved in active growth repression. Here, we showed that decreased growth in plants exposed to moderate salt stress is mediated by MYB3R transcription factors that have been known to positively and negatively regulate the transcription of G2/M-specific genes. Our genome-wide gene expression analysis revealed occurrences of general downregulation of G2/M-specific genes in Arabidopsis under salt stress. Importantly, this downregulation is significantly and universally mitigated by the loss of MYB3R repressors by mutations. Accordingly, the growth performance of Arabidopsis plants under salt stress is significantly recovered in mutants lacking MYB3R repressors. This growth recovery involves improved cell proliferation that is possibly due to prolonging and accelerating cell proliferation, which were partly suggested by enlarged root meristem and increased number of cells positive for CYCB1;1-GUS. Our ploidy analysis further suggested that cell cycle progression at the G2 phase was delayed under salt stress, and this delay was recovered by loss of MYB3R repressors. Under salt stress, the changes in expression of MYB3R activators and repressors at both the mRNA and protein levels were not significant. This observation suggests novel mechanisms underlying MYB3R-mediated growth repression under salt stress that are different from the mechanisms operating under other stress conditions such as DNA damage and high temperature.</description><identifier>ISSN: 0918-9440</identifier><identifier>EISSN: 1618-0860</identifier><identifier>DOI: 10.1007/s10265-020-01250-8</identifier><identifier>PMID: 33580347</identifier><language>eng</language><publisher>Singapore: Springer Singapore</publisher><subject>Abiotic stress ; Active control ; Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Biomedical and Life Sciences ; Cell Cycle ; Cell growth ; Cell proliferation ; Deoxyribonucleic acid ; DNA ; DNA damage ; Environmental stress ; G2 phase ; Gene expression ; Gene Expression Regulation, Plant ; Genes ; Genomes ; High temperature ; Life Sciences ; Meristems ; Mutation ; Plant Biochemistry ; Plant Ecology ; Plant Physiology ; Plant Sciences ; Plants, Genetically Modified - metabolism ; Ploidy ; Regular Paper – Genetics/Developmental Biology ; Repressors ; Salinity tolerance ; Salt Stress ; Salts ; Stress, Physiological ; Transcription factors</subject><ispartof>Journal of plant research, 2021-03, Vol.134 (2), p.261-277</ispartof><rights>The Botanical Society of Japan 2021</rights><rights>The Botanical Society of Japan 2021.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c468t-a7dfa6a42863666ea75b111670a90321418497444222e812eacada26739c02f53</citedby><cites>FETCH-LOGICAL-c468t-a7dfa6a42863666ea75b111670a90321418497444222e812eacada26739c02f53</cites><orcidid>0000-0002-9635-9709</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s10265-020-01250-8$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s10265-020-01250-8$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33580347$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Okumura, Toru</creatorcontrib><creatorcontrib>Nomoto, Yuji</creatorcontrib><creatorcontrib>Kobayashi, Kosuke</creatorcontrib><creatorcontrib>Suzuki, Takamasa</creatorcontrib><creatorcontrib>Takatsuka, Hirotomo</creatorcontrib><creatorcontrib>Ito, Masaki</creatorcontrib><title>MYB3R-mediated active repression of cell cycle and growth under salt stress in Arabidopsis thaliana</title><title>Journal of plant research</title><addtitle>J Plant Res</addtitle><addtitle>J Plant Res</addtitle><description>Under environmental stress, plants are believed to actively repress their growth to save resource and alter its allocation to acquire tolerance against the stress. Although a lot of studies have uncovered precise mechanisms for responding to stress and acquiring tolerance, the mechanisms for regulating growth repression under stress are not as well understood. It is especially unclear which particular genes related to cell cycle control are involved in active growth repression. Here, we showed that decreased growth in plants exposed to moderate salt stress is mediated by MYB3R transcription factors that have been known to positively and negatively regulate the transcription of G2/M-specific genes. Our genome-wide gene expression analysis revealed occurrences of general downregulation of G2/M-specific genes in Arabidopsis under salt stress. Importantly, this downregulation is significantly and universally mitigated by the loss of MYB3R repressors by mutations. Accordingly, the growth performance of Arabidopsis plants under salt stress is significantly recovered in mutants lacking MYB3R repressors. This growth recovery involves improved cell proliferation that is possibly due to prolonging and accelerating cell proliferation, which were partly suggested by enlarged root meristem and increased number of cells positive for CYCB1;1-GUS. Our ploidy analysis further suggested that cell cycle progression at the G2 phase was delayed under salt stress, and this delay was recovered by loss of MYB3R repressors. Under salt stress, the changes in expression of MYB3R activators and repressors at both the mRNA and protein levels were not significant. This observation suggests novel mechanisms underlying MYB3R-mediated growth repression under salt stress that are different from the mechanisms operating under other stress conditions such as DNA damage and high temperature.</description><subject>Abiotic stress</subject><subject>Active control</subject><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Biomedical and Life Sciences</subject><subject>Cell Cycle</subject><subject>Cell growth</subject><subject>Cell proliferation</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA damage</subject><subject>Environmental stress</subject><subject>G2 phase</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Genomes</subject><subject>High temperature</subject><subject>Life Sciences</subject><subject>Meristems</subject><subject>Mutation</subject><subject>Plant Biochemistry</subject><subject>Plant Ecology</subject><subject>Plant Physiology</subject><subject>Plant Sciences</subject><subject>Plants, Genetically Modified - metabolism</subject><subject>Ploidy</subject><subject>Regular Paper – Genetics/Developmental Biology</subject><subject>Repressors</subject><subject>Salinity tolerance</subject><subject>Salt Stress</subject><subject>Salts</subject><subject>Stress, Physiological</subject><subject>Transcription factors</subject><issn>0918-9440</issn><issn>1618-0860</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>BENPR</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNp9kUlPHDEQhS2UKAwkf4BDZCkXLg3lpb0cCWKTQJGicMjJqnG7Z4x6uid2N4h_j4dhkXLgVCXVV69K7xFywOCIAejjzICrugIOFTBeQ2V2yIwpZiowCj6RGdjSWylhl-zlfAfAdG3NF7IrRG1ASD0j_ubvT_G7WoUm4hgain6M94GmsE4h5zj0dGipD11H_aPvAsW-oYs0PIxLOvVNSDRjN9I8bmgae3qScB6bYZ1jpuMSu4g9fiWfW-xy-PZS98nt-dmf08vq-tfF1enJdeWlMmOFumlRoeRGCaVUQF3PGWNKA1oQnElmpNVSSs55MIwH9NggV1pYD7ytxT453Oqu0_BvCnl0q5g3v2Mfhik7Lo0thkkNBf3xH3o3TKkv3xXK1trKcrhQfEv5NOScQuvWKa4wPToGbhOB20bgSgTuOQJnytL3F-lpXmx9W3n1vABiC-Qy6hchvd_-QPYJo5OPlg</recordid><startdate>20210301</startdate><enddate>20210301</enddate><creator>Okumura, Toru</creator><creator>Nomoto, Yuji</creator><creator>Kobayashi, Kosuke</creator><creator>Suzuki, Takamasa</creator><creator>Takatsuka, Hirotomo</creator><creator>Ito, Masaki</creator><general>Springer Singapore</general><general>Springer Nature B.V</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>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7ST</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PCBAR</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-9635-9709</orcidid></search><sort><creationdate>20210301</creationdate><title>MYB3R-mediated active repression of cell cycle and growth under salt stress in Arabidopsis thaliana</title><author>Okumura, Toru ; Nomoto, Yuji ; Kobayashi, Kosuke ; Suzuki, Takamasa ; Takatsuka, Hirotomo ; Ito, Masaki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c468t-a7dfa6a42863666ea75b111670a90321418497444222e812eacada26739c02f53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Abiotic stress</topic><topic>Active control</topic><topic>Arabidopsis</topic><topic>Arabidopsis - 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Academic</collection><jtitle>Journal of plant research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Okumura, Toru</au><au>Nomoto, Yuji</au><au>Kobayashi, Kosuke</au><au>Suzuki, Takamasa</au><au>Takatsuka, Hirotomo</au><au>Ito, Masaki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>MYB3R-mediated active repression of cell cycle and growth under salt stress in Arabidopsis thaliana</atitle><jtitle>Journal of plant research</jtitle><stitle>J Plant Res</stitle><addtitle>J Plant Res</addtitle><date>2021-03-01</date><risdate>2021</risdate><volume>134</volume><issue>2</issue><spage>261</spage><epage>277</epage><pages>261-277</pages><issn>0918-9440</issn><eissn>1618-0860</eissn><abstract>Under environmental stress, plants are believed to actively repress their growth to save resource and alter its allocation to acquire tolerance against the stress. Although a lot of studies have uncovered precise mechanisms for responding to stress and acquiring tolerance, the mechanisms for regulating growth repression under stress are not as well understood. It is especially unclear which particular genes related to cell cycle control are involved in active growth repression. Here, we showed that decreased growth in plants exposed to moderate salt stress is mediated by MYB3R transcription factors that have been known to positively and negatively regulate the transcription of G2/M-specific genes. Our genome-wide gene expression analysis revealed occurrences of general downregulation of G2/M-specific genes in Arabidopsis under salt stress. Importantly, this downregulation is significantly and universally mitigated by the loss of MYB3R repressors by mutations. Accordingly, the growth performance of Arabidopsis plants under salt stress is significantly recovered in mutants lacking MYB3R repressors. This growth recovery involves improved cell proliferation that is possibly due to prolonging and accelerating cell proliferation, which were partly suggested by enlarged root meristem and increased number of cells positive for CYCB1;1-GUS. Our ploidy analysis further suggested that cell cycle progression at the G2 phase was delayed under salt stress, and this delay was recovered by loss of MYB3R repressors. Under salt stress, the changes in expression of MYB3R activators and repressors at both the mRNA and protein levels were not significant. This observation suggests novel mechanisms underlying MYB3R-mediated growth repression under salt stress that are different from the mechanisms operating under other stress conditions such as DNA damage and high temperature.</abstract><cop>Singapore</cop><pub>Springer Singapore</pub><pmid>33580347</pmid><doi>10.1007/s10265-020-01250-8</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-9635-9709</orcidid></addata></record> |
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subjects | Abiotic stress Active control Arabidopsis Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Biomedical and Life Sciences Cell Cycle Cell growth Cell proliferation Deoxyribonucleic acid DNA DNA damage Environmental stress G2 phase Gene expression Gene Expression Regulation, Plant Genes Genomes High temperature Life Sciences Meristems Mutation Plant Biochemistry Plant Ecology Plant Physiology Plant Sciences Plants, Genetically Modified - metabolism Ploidy Regular Paper – Genetics/Developmental Biology Repressors Salinity tolerance Salt Stress Salts Stress, Physiological Transcription factors |
title | MYB3R-mediated active repression of cell cycle and growth under salt stress in Arabidopsis thaliana |
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