MicroRNA156 amplifies transcription factor-associated cold stress tolerance in plant cells
MicroRNAs may increase cold stress tolerance by regulating stress-related signal transduction pathways and by modulating the expression of transcription factors. However, the molecular mechanism by which microRNAs enhance cold stress tolerance is not fully understood. Here, we report that overexpres...
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Veröffentlicht in: | Molecular genetics and genomics : MGG 2019-04, Vol.294 (2), p.379-393 |
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description | MicroRNAs may increase cold stress tolerance by regulating stress-related signal transduction pathways and by modulating the expression of transcription factors. However, the molecular mechanism by which microRNAs enhance cold stress tolerance is not fully understood. Here, we report that overexpression of rice microRNA156 (OsmiR156) results in increased cell viability and growth rate under cold stress in Arabidopsis, pine, and rice. OsmiR156 increases cold stress tolerance by targeting OsSPL3. OsSPL3 positively regulates the expression of OsWRKY71, a negative regulator of the transcription factors OsMYB2 and OsMYB3R-2. OsMYB2 counteracts cold stress by activating the expression of the stress-response genes OsLEA3, OsRab16A, and OsDREB2A. OsMYB3R-2 counteracts cold stress by activating the expression of OsKNOLLE2, OsCTP1, OsCycB1.1, OsCycB2.1, and OsCDC20.1. In OsmiR156 transgenic rice cell lines, the transcript levels of OsLEA3, OsRab16A, OsDREB2A, OsKNOLLE2, OsCTP1, OsCycB1.1, OsCycB2.1, and OsCDC20.1 were increased by OsWRKY71 knockdown and inversely regulated by OsWRKY71 overexpression, indicating that OsmiR156 enhances cold stress tolerance by regulating the expression of transcription factor genes in plant cells. These results will increase our understanding of microRNA-related cold stress tolerance in different plant species, including monocotyledonous, dicotyledonous, and gymnosperm plant species, and will be valuable in plant molecular biotechnology. |
doi_str_mv | 10.1007/s00438-018-1516-4 |
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However, the molecular mechanism by which microRNAs enhance cold stress tolerance is not fully understood. Here, we report that overexpression of rice microRNA156 (OsmiR156) results in increased cell viability and growth rate under cold stress in Arabidopsis, pine, and rice. OsmiR156 increases cold stress tolerance by targeting OsSPL3. OsSPL3 positively regulates the expression of OsWRKY71, a negative regulator of the transcription factors OsMYB2 and OsMYB3R-2. OsMYB2 counteracts cold stress by activating the expression of the stress-response genes OsLEA3, OsRab16A, and OsDREB2A. OsMYB3R-2 counteracts cold stress by activating the expression of OsKNOLLE2, OsCTP1, OsCycB1.1, OsCycB2.1, and OsCDC20.1. In OsmiR156 transgenic rice cell lines, the transcript levels of OsLEA3, OsRab16A, OsDREB2A, OsKNOLLE2, OsCTP1, OsCycB1.1, OsCycB2.1, and OsCDC20.1 were increased by OsWRKY71 knockdown and inversely regulated by OsWRKY71 overexpression, indicating that OsmiR156 enhances cold stress tolerance by regulating the expression of transcription factor genes in plant cells. These results will increase our understanding of microRNA-related cold stress tolerance in different plant species, including monocotyledonous, dicotyledonous, and gymnosperm plant species, and will be valuable in plant molecular biotechnology.</description><identifier>ISSN: 1617-4615</identifier><identifier>EISSN: 1617-4623</identifier><identifier>DOI: 10.1007/s00438-018-1516-4</identifier><identifier>PMID: 30478522</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Animal Genetics and Genomics ; Arabidopsis - genetics ; Biochemistry ; Biomedical and Life Sciences ; Biotechnology ; Cell lines ; Cellular stress response ; Cold ; Cold Temperature ; Cold tolerance ; Cold-Shock Response - genetics ; Flowers & plants ; Gene Expression Regulation, Plant - genetics ; Gene Knockdown Techniques ; Growth rate ; Human Genetics ; Life Sciences ; Microbial Genetics and Genomics ; MicroRNAs ; MicroRNAs - genetics ; miRNA ; Original Article ; Oryza ; Oryza - genetics ; Oryza - growth & development ; Plant cells ; Plant Cells - metabolism ; Plant Genetics and Genomics ; Plant Proteins - genetics ; Plants, Genetically Modified - genetics ; Plants, Genetically Modified - growth & development ; Signal transduction ; Transcription factors ; Transcription Factors - genetics ; Transduction</subject><ispartof>Molecular genetics and genomics : MGG, 2019-04, Vol.294 (2), p.379-393</ispartof><rights>Springer-Verlag GmbH Germany, part of Springer Nature 2018</rights><rights>Molecular Genetics and Genomics is a copyright of Springer, (2018). All Rights Reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c438t-5f35cafe513660b19625223fe793cb99baa5d9714b61c62aac702b53355ca6273</citedby><cites>FETCH-LOGICAL-c438t-5f35cafe513660b19625223fe793cb99baa5d9714b61c62aac702b53355ca6273</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00438-018-1516-4$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00438-018-1516-4$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>315,781,785,27928,27929,41492,42561,51323</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30478522$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhou, Mingqin</creatorcontrib><creatorcontrib>Tang, Wei</creatorcontrib><title>MicroRNA156 amplifies transcription factor-associated cold stress tolerance in plant cells</title><title>Molecular genetics and genomics : MGG</title><addtitle>Mol Genet Genomics</addtitle><addtitle>Mol Genet Genomics</addtitle><description>MicroRNAs may increase cold stress tolerance by regulating stress-related signal transduction pathways and by modulating the expression of transcription factors. However, the molecular mechanism by which microRNAs enhance cold stress tolerance is not fully understood. Here, we report that overexpression of rice microRNA156 (OsmiR156) results in increased cell viability and growth rate under cold stress in Arabidopsis, pine, and rice. OsmiR156 increases cold stress tolerance by targeting OsSPL3. OsSPL3 positively regulates the expression of OsWRKY71, a negative regulator of the transcription factors OsMYB2 and OsMYB3R-2. OsMYB2 counteracts cold stress by activating the expression of the stress-response genes OsLEA3, OsRab16A, and OsDREB2A. OsMYB3R-2 counteracts cold stress by activating the expression of OsKNOLLE2, OsCTP1, OsCycB1.1, OsCycB2.1, and OsCDC20.1. In OsmiR156 transgenic rice cell lines, the transcript levels of OsLEA3, OsRab16A, OsDREB2A, OsKNOLLE2, OsCTP1, OsCycB1.1, OsCycB2.1, and OsCDC20.1 were increased by OsWRKY71 knockdown and inversely regulated by OsWRKY71 overexpression, indicating that OsmiR156 enhances cold stress tolerance by regulating the expression of transcription factor genes in plant cells. These results will increase our understanding of microRNA-related cold stress tolerance in different plant species, including monocotyledonous, dicotyledonous, and gymnosperm plant species, and will be valuable in plant molecular biotechnology.</description><subject>Animal Genetics and Genomics</subject><subject>Arabidopsis - genetics</subject><subject>Biochemistry</subject><subject>Biomedical and Life Sciences</subject><subject>Biotechnology</subject><subject>Cell lines</subject><subject>Cellular stress response</subject><subject>Cold</subject><subject>Cold Temperature</subject><subject>Cold tolerance</subject><subject>Cold-Shock Response - genetics</subject><subject>Flowers & plants</subject><subject>Gene Expression Regulation, Plant - genetics</subject><subject>Gene Knockdown Techniques</subject><subject>Growth rate</subject><subject>Human Genetics</subject><subject>Life Sciences</subject><subject>Microbial Genetics and Genomics</subject><subject>MicroRNAs</subject><subject>MicroRNAs - genetics</subject><subject>miRNA</subject><subject>Original Article</subject><subject>Oryza</subject><subject>Oryza - genetics</subject><subject>Oryza - growth & development</subject><subject>Plant cells</subject><subject>Plant Cells - metabolism</subject><subject>Plant Genetics and Genomics</subject><subject>Plant Proteins - genetics</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Plants, Genetically Modified - growth & development</subject><subject>Signal transduction</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transduction</subject><issn>1617-4615</issn><issn>1617-4623</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp1kM1KAzEURoMotlYfwI0MuHEzmptMks6yiH9QFUQ3bkImzUjKdDLmThe-vRlbFQRXCeR8N989hBwDPQdK1QVSWvBpTmGagwCZFztkDBJUXkjGd3_uIEbkAHFJKSjJ1D4ZcVqoqWBsTF7vvY3h6WEGQmZm1TW-9g6zPpoWbfRd70Ob1cb2IeYGMVhverfIbGgWGfbRYWJD4xJuXebbrGtM22fWNQ0ekr3aNOiOtueEvFxfPV_e5vPHm7vL2Ty3qXyfi5oLa2ongEtJKyglS8147VTJbVWWlTFiUSooKglWMmOsoqwSnIsUS-vwCTnbzO1ieF877PXK49DAtC6sUTPgU1mU6gs9_YMuwzq2qd1AKclLIYtEwYZKZhCjq3UX_crEDw1UD-L1RrxO4vUgXg-Zk-3kdbVyi5_Et-kEsA2A6al9c_H36_-nfgKy5ozy</recordid><startdate>20190401</startdate><enddate>20190401</enddate><creator>Zhou, Mingqin</creator><creator>Tang, Wei</creator><general>Springer Berlin Heidelberg</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>7SS</scope><scope>7TK</scope><scope>7TM</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>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20190401</creationdate><title>MicroRNA156 amplifies transcription factor-associated cold stress tolerance in plant cells</title><author>Zhou, Mingqin ; Tang, Wei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c438t-5f35cafe513660b19625223fe793cb99baa5d9714b61c62aac702b53355ca6273</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animal Genetics and Genomics</topic><topic>Arabidopsis - genetics</topic><topic>Biochemistry</topic><topic>Biomedical and Life Sciences</topic><topic>Biotechnology</topic><topic>Cell lines</topic><topic>Cellular stress response</topic><topic>Cold</topic><topic>Cold Temperature</topic><topic>Cold tolerance</topic><topic>Cold-Shock Response - genetics</topic><topic>Flowers & plants</topic><topic>Gene Expression Regulation, Plant - genetics</topic><topic>Gene Knockdown Techniques</topic><topic>Growth rate</topic><topic>Human Genetics</topic><topic>Life Sciences</topic><topic>Microbial Genetics and Genomics</topic><topic>MicroRNAs</topic><topic>MicroRNAs - genetics</topic><topic>miRNA</topic><topic>Original Article</topic><topic>Oryza</topic><topic>Oryza - genetics</topic><topic>Oryza - growth & development</topic><topic>Plant cells</topic><topic>Plant Cells - metabolism</topic><topic>Plant Genetics and Genomics</topic><topic>Plant Proteins - genetics</topic><topic>Plants, Genetically Modified - genetics</topic><topic>Plants, Genetically Modified - growth & development</topic><topic>Signal transduction</topic><topic>Transcription factors</topic><topic>Transcription Factors - genetics</topic><topic>Transduction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhou, Mingqin</creatorcontrib><creatorcontrib>Tang, Wei</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular genetics and genomics : MGG</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhou, Mingqin</au><au>Tang, Wei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>MicroRNA156 amplifies transcription factor-associated cold stress tolerance in plant cells</atitle><jtitle>Molecular genetics and genomics : MGG</jtitle><stitle>Mol Genet Genomics</stitle><addtitle>Mol Genet Genomics</addtitle><date>2019-04-01</date><risdate>2019</risdate><volume>294</volume><issue>2</issue><spage>379</spage><epage>393</epage><pages>379-393</pages><issn>1617-4615</issn><eissn>1617-4623</eissn><abstract>MicroRNAs may increase cold stress tolerance by regulating stress-related signal transduction pathways and by modulating the expression of transcription factors. However, the molecular mechanism by which microRNAs enhance cold stress tolerance is not fully understood. Here, we report that overexpression of rice microRNA156 (OsmiR156) results in increased cell viability and growth rate under cold stress in Arabidopsis, pine, and rice. OsmiR156 increases cold stress tolerance by targeting OsSPL3. OsSPL3 positively regulates the expression of OsWRKY71, a negative regulator of the transcription factors OsMYB2 and OsMYB3R-2. OsMYB2 counteracts cold stress by activating the expression of the stress-response genes OsLEA3, OsRab16A, and OsDREB2A. OsMYB3R-2 counteracts cold stress by activating the expression of OsKNOLLE2, OsCTP1, OsCycB1.1, OsCycB2.1, and OsCDC20.1. In OsmiR156 transgenic rice cell lines, the transcript levels of OsLEA3, OsRab16A, OsDREB2A, OsKNOLLE2, OsCTP1, OsCycB1.1, OsCycB2.1, and OsCDC20.1 were increased by OsWRKY71 knockdown and inversely regulated by OsWRKY71 overexpression, indicating that OsmiR156 enhances cold stress tolerance by regulating the expression of transcription factor genes in plant cells. These results will increase our understanding of microRNA-related cold stress tolerance in different plant species, including monocotyledonous, dicotyledonous, and gymnosperm plant species, and will be valuable in plant molecular biotechnology.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>30478522</pmid><doi>10.1007/s00438-018-1516-4</doi><tpages>15</tpages></addata></record> |
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subjects | Animal Genetics and Genomics Arabidopsis - genetics Biochemistry Biomedical and Life Sciences Biotechnology Cell lines Cellular stress response Cold Cold Temperature Cold tolerance Cold-Shock Response - genetics Flowers & plants Gene Expression Regulation, Plant - genetics Gene Knockdown Techniques Growth rate Human Genetics Life Sciences Microbial Genetics and Genomics MicroRNAs MicroRNAs - genetics miRNA Original Article Oryza Oryza - genetics Oryza - growth & development Plant cells Plant Cells - metabolism Plant Genetics and Genomics Plant Proteins - genetics Plants, Genetically Modified - genetics Plants, Genetically Modified - growth & development Signal transduction Transcription factors Transcription Factors - genetics Transduction |
title | MicroRNA156 amplifies transcription factor-associated cold stress tolerance in plant cells |
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