A major gene for chilling tolerance variation in Indica rice codes for a kinase OsCTK1 that phosphorylates multiple substrates under cold
Summary Rice is susceptible to chilling stress. Identifying chilling tolerance genes and their mechanisms are key to improve rice performance. Here, we performed a genome‐wide association study to identify regulatory genes for chilling tolerance in rice. One major gene for chilling tolerance variati...
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Veröffentlicht in: | The New phytologist 2024-06, Vol.242 (5), p.2077-2092 |
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creator | Wu, Jiawen Liu, Huimin Zhang, Yan Zhang, Yingdong Li, Dongling Liu, Shiyan Lu, Shan Wei, Lihui Hua, Jian Zou, Baohong |
description | Summary
Rice is susceptible to chilling stress. Identifying chilling tolerance genes and their mechanisms are key to improve rice performance. Here, we performed a genome‐wide association study to identify regulatory genes for chilling tolerance in rice.
One major gene for chilling tolerance variation in Indica rice was identified as a casein kinase gene OsCTK1. Its function and natural variation are investigated at the physiological and molecular level by its mutants and transgenic plants. Potential substrates of OsCTK1 were identified by phosphoproteomic analysis, protein–protein interaction assay, in vitro kinase assay, and mutant characterization.
OsCTK1 positively regulates rice chilling tolerance. Three of its putative substrates, acidic ribosomal protein OsP3B, cyclic nucleotide‐gated ion channel OsCNGC9, and dual‐specific mitogen‐activated protein kinase phosphatase OsMKP1, are each involved in chilling tolerance. In addition, a natural OsCTK1 chilling‐tolerant (CT) variant exhibited a higher kinase activity and conferred greater chilling tolerance compared with a chilling‐sensitive (CS) variant. The CT variant is more prevalent in CT accessions and is distributed more frequently in higher latitude compared with the CS variant.
This study thus enables a better understanding of chilling tolerance mechanisms and provides gene variants for genetic improvement of chilling tolerance in rice. |
doi_str_mv | 10.1111/nph.19696 |
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Rice is susceptible to chilling stress. Identifying chilling tolerance genes and their mechanisms are key to improve rice performance. Here, we performed a genome‐wide association study to identify regulatory genes for chilling tolerance in rice.
One major gene for chilling tolerance variation in Indica rice was identified as a casein kinase gene OsCTK1. Its function and natural variation are investigated at the physiological and molecular level by its mutants and transgenic plants. Potential substrates of OsCTK1 were identified by phosphoproteomic analysis, protein–protein interaction assay, in vitro kinase assay, and mutant characterization.
OsCTK1 positively regulates rice chilling tolerance. Three of its putative substrates, acidic ribosomal protein OsP3B, cyclic nucleotide‐gated ion channel OsCNGC9, and dual‐specific mitogen‐activated protein kinase phosphatase OsMKP1, are each involved in chilling tolerance. In addition, a natural OsCTK1 chilling‐tolerant (CT) variant exhibited a higher kinase activity and conferred greater chilling tolerance compared with a chilling‐sensitive (CS) variant. The CT variant is more prevalent in CT accessions and is distributed more frequently in higher latitude compared with the CS variant.
This study thus enables a better understanding of chilling tolerance mechanisms and provides gene variants for genetic improvement of chilling tolerance in rice.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.19696</identifier><identifier>PMID: 38494697</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Adaptation, Physiological - genetics ; Casein ; Chilling ; chilling tolerance ; cold ; Cold Temperature ; Cooling ; Genes ; Genes, Plant ; genetic improvement ; Genetic Variation ; genetically modified organisms ; Genome-Wide Association Study ; Genomes ; GWAS ; haplotype ; Ion channels ; Kinases ; latitude ; major genes ; mitogen-activated protein kinase ; Mutants ; Mutation - genetics ; natural variation ; non-specific serine/threonine protein kinase ; Nucleotides ; Oryza - enzymology ; Oryza - genetics ; Oryza - physiology ; OsCTK1 ; Phosphatase ; Phosphorylation ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants, Genetically Modified ; protein-protein interactions ; Proteins ; proteomics ; ribosomal proteins ; Rice ; Substrate Specificity ; Substrates ; Transgenic plants ; Variation</subject><ispartof>The New phytologist, 2024-06, Vol.242 (5), p.2077-2092</ispartof><rights>2024 The Authors. © 2024 New Phytologist Foundation</rights><rights>2024 The Authors. New Phytologist © 2024 New Phytologist Foundation.</rights><rights>Copyright © 2024 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3466-98b37ec448898aa6ea688524c0c7237d7d11277d8d298f4506393f62af945303</cites><orcidid>0000-0002-3777-3344 ; 0000-0002-6496-5683</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%2Fnph.19696$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.19696$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38494697$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wu, Jiawen</creatorcontrib><creatorcontrib>Liu, Huimin</creatorcontrib><creatorcontrib>Zhang, Yan</creatorcontrib><creatorcontrib>Zhang, Yingdong</creatorcontrib><creatorcontrib>Li, Dongling</creatorcontrib><creatorcontrib>Liu, Shiyan</creatorcontrib><creatorcontrib>Lu, Shan</creatorcontrib><creatorcontrib>Wei, Lihui</creatorcontrib><creatorcontrib>Hua, Jian</creatorcontrib><creatorcontrib>Zou, Baohong</creatorcontrib><title>A major gene for chilling tolerance variation in Indica rice codes for a kinase OsCTK1 that phosphorylates multiple substrates under cold</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
Rice is susceptible to chilling stress. Identifying chilling tolerance genes and their mechanisms are key to improve rice performance. Here, we performed a genome‐wide association study to identify regulatory genes for chilling tolerance in rice.
One major gene for chilling tolerance variation in Indica rice was identified as a casein kinase gene OsCTK1. Its function and natural variation are investigated at the physiological and molecular level by its mutants and transgenic plants. Potential substrates of OsCTK1 were identified by phosphoproteomic analysis, protein–protein interaction assay, in vitro kinase assay, and mutant characterization.
OsCTK1 positively regulates rice chilling tolerance. Three of its putative substrates, acidic ribosomal protein OsP3B, cyclic nucleotide‐gated ion channel OsCNGC9, and dual‐specific mitogen‐activated protein kinase phosphatase OsMKP1, are each involved in chilling tolerance. In addition, a natural OsCTK1 chilling‐tolerant (CT) variant exhibited a higher kinase activity and conferred greater chilling tolerance compared with a chilling‐sensitive (CS) variant. The CT variant is more prevalent in CT accessions and is distributed more frequently in higher latitude compared with the CS variant.
This study thus enables a better understanding of chilling tolerance mechanisms and provides gene variants for genetic improvement of chilling tolerance in rice.</description><subject>Adaptation, Physiological - genetics</subject><subject>Casein</subject><subject>Chilling</subject><subject>chilling tolerance</subject><subject>cold</subject><subject>Cold Temperature</subject><subject>Cooling</subject><subject>Genes</subject><subject>Genes, Plant</subject><subject>genetic improvement</subject><subject>Genetic Variation</subject><subject>genetically modified organisms</subject><subject>Genome-Wide Association Study</subject><subject>Genomes</subject><subject>GWAS</subject><subject>haplotype</subject><subject>Ion channels</subject><subject>Kinases</subject><subject>latitude</subject><subject>major genes</subject><subject>mitogen-activated protein kinase</subject><subject>Mutants</subject><subject>Mutation - genetics</subject><subject>natural variation</subject><subject>non-specific serine/threonine protein kinase</subject><subject>Nucleotides</subject><subject>Oryza - enzymology</subject><subject>Oryza - genetics</subject><subject>Oryza - physiology</subject><subject>OsCTK1</subject><subject>Phosphatase</subject><subject>Phosphorylation</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants, Genetically Modified</subject><subject>protein-protein interactions</subject><subject>Proteins</subject><subject>proteomics</subject><subject>ribosomal proteins</subject><subject>Rice</subject><subject>Substrate Specificity</subject><subject>Substrates</subject><subject>Transgenic plants</subject><subject>Variation</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU1rFDEYx4Modq0e_AIS8FIP0-b95VgWbYul9bAHb0M2k-lmzSRjMmPZj-C3brpbPQjSwEPCk9_zC-EPwHuMTnFdZ3HcnGIttHgBFpgJ3ShM5UuwQIioRjDx_Qi8KWWLENJckNfgiCqmKycX4Pc5HMw2ZXjnooN9PdiND8HHOzil4LKJ1sFfJnsz-RShj_Aqdt4amH29sKlzZT9l4A8fTXHwtixXXzGcNmaC4yaVWnkXzFS5YQ6TH4ODZV6XKe97c-xcfTOF7i141ZtQ3Lun_RisvnxeLS-b69uLq-X5dWMpE6LRak2ls4wppZUxwhmhFCfMIisJlZ3sMCZSdqojWvWMI0E17QUxvWacInoMTg7aMaefsytTO_hiXQgmujSXlmJOuUQa8WdRooVEXGNBKvrxH3Sb5hzrP1qKOCGEIfko_HSgbE6lZNe3Y_aDybsWo_YxybYm2e6TrOyHJ-O8Hlz3l_wTXQXODsC9D273f1N78-3yoHwA5manSw</recordid><startdate>202406</startdate><enddate>202406</enddate><creator>Wu, Jiawen</creator><creator>Liu, Huimin</creator><creator>Zhang, Yan</creator><creator>Zhang, Yingdong</creator><creator>Li, Dongling</creator><creator>Liu, Shiyan</creator><creator>Lu, Shan</creator><creator>Wei, Lihui</creator><creator>Hua, Jian</creator><creator>Zou, Baohong</creator><general>Wiley Subscription Services, Inc</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>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-3777-3344</orcidid><orcidid>https://orcid.org/0000-0002-6496-5683</orcidid></search><sort><creationdate>202406</creationdate><title>A major gene for chilling tolerance variation in Indica rice codes for a kinase OsCTK1 that phosphorylates multiple substrates under cold</title><author>Wu, Jiawen ; Liu, Huimin ; Zhang, Yan ; Zhang, Yingdong ; Li, Dongling ; Liu, Shiyan ; Lu, Shan ; Wei, Lihui ; Hua, Jian ; Zou, Baohong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3466-98b37ec448898aa6ea688524c0c7237d7d11277d8d298f4506393f62af945303</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adaptation, Physiological - genetics</topic><topic>Casein</topic><topic>Chilling</topic><topic>chilling tolerance</topic><topic>cold</topic><topic>Cold Temperature</topic><topic>Cooling</topic><topic>Genes</topic><topic>Genes, Plant</topic><topic>genetic improvement</topic><topic>Genetic Variation</topic><topic>genetically modified organisms</topic><topic>Genome-Wide Association Study</topic><topic>Genomes</topic><topic>GWAS</topic><topic>haplotype</topic><topic>Ion channels</topic><topic>Kinases</topic><topic>latitude</topic><topic>major genes</topic><topic>mitogen-activated protein kinase</topic><topic>Mutants</topic><topic>Mutation - genetics</topic><topic>natural variation</topic><topic>non-specific serine/threonine protein kinase</topic><topic>Nucleotides</topic><topic>Oryza - enzymology</topic><topic>Oryza - genetics</topic><topic>Oryza - physiology</topic><topic>OsCTK1</topic><topic>Phosphatase</topic><topic>Phosphorylation</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants, Genetically Modified</topic><topic>protein-protein interactions</topic><topic>Proteins</topic><topic>proteomics</topic><topic>ribosomal proteins</topic><topic>Rice</topic><topic>Substrate Specificity</topic><topic>Substrates</topic><topic>Transgenic plants</topic><topic>Variation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wu, Jiawen</creatorcontrib><creatorcontrib>Liu, Huimin</creatorcontrib><creatorcontrib>Zhang, Yan</creatorcontrib><creatorcontrib>Zhang, Yingdong</creatorcontrib><creatorcontrib>Li, Dongling</creatorcontrib><creatorcontrib>Liu, Shiyan</creatorcontrib><creatorcontrib>Lu, Shan</creatorcontrib><creatorcontrib>Wei, Lihui</creatorcontrib><creatorcontrib>Hua, Jian</creatorcontrib><creatorcontrib>Zou, Baohong</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>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wu, Jiawen</au><au>Liu, Huimin</au><au>Zhang, Yan</au><au>Zhang, Yingdong</au><au>Li, Dongling</au><au>Liu, Shiyan</au><au>Lu, Shan</au><au>Wei, Lihui</au><au>Hua, Jian</au><au>Zou, Baohong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A major gene for chilling tolerance variation in Indica rice codes for a kinase OsCTK1 that phosphorylates multiple substrates under cold</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2024-06</date><risdate>2024</risdate><volume>242</volume><issue>5</issue><spage>2077</spage><epage>2092</epage><pages>2077-2092</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Summary
Rice is susceptible to chilling stress. Identifying chilling tolerance genes and their mechanisms are key to improve rice performance. Here, we performed a genome‐wide association study to identify regulatory genes for chilling tolerance in rice.
One major gene for chilling tolerance variation in Indica rice was identified as a casein kinase gene OsCTK1. Its function and natural variation are investigated at the physiological and molecular level by its mutants and transgenic plants. Potential substrates of OsCTK1 were identified by phosphoproteomic analysis, protein–protein interaction assay, in vitro kinase assay, and mutant characterization.
OsCTK1 positively regulates rice chilling tolerance. Three of its putative substrates, acidic ribosomal protein OsP3B, cyclic nucleotide‐gated ion channel OsCNGC9, and dual‐specific mitogen‐activated protein kinase phosphatase OsMKP1, are each involved in chilling tolerance. In addition, a natural OsCTK1 chilling‐tolerant (CT) variant exhibited a higher kinase activity and conferred greater chilling tolerance compared with a chilling‐sensitive (CS) variant. The CT variant is more prevalent in CT accessions and is distributed more frequently in higher latitude compared with the CS variant.
This study thus enables a better understanding of chilling tolerance mechanisms and provides gene variants for genetic improvement of chilling tolerance in rice.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>38494697</pmid><doi>10.1111/nph.19696</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-3777-3344</orcidid><orcidid>https://orcid.org/0000-0002-6496-5683</orcidid></addata></record> |
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subjects | Adaptation, Physiological - genetics Casein Chilling chilling tolerance cold Cold Temperature Cooling Genes Genes, Plant genetic improvement Genetic Variation genetically modified organisms Genome-Wide Association Study Genomes GWAS haplotype Ion channels Kinases latitude major genes mitogen-activated protein kinase Mutants Mutation - genetics natural variation non-specific serine/threonine protein kinase Nucleotides Oryza - enzymology Oryza - genetics Oryza - physiology OsCTK1 Phosphatase Phosphorylation Plant Proteins - genetics Plant Proteins - metabolism Plants, Genetically Modified protein-protein interactions Proteins proteomics ribosomal proteins Rice Substrate Specificity Substrates Transgenic plants Variation |
title | A major gene for chilling tolerance variation in Indica rice codes for a kinase OsCTK1 that phosphorylates multiple substrates under cold |
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