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
Hauptverfasser: Wu, Jiawen, Liu, Huimin, Zhang, Yan, Zhang, Yingdong, Li, Dongling, Liu, Shiyan, Lu, Shan, Wei, Lihui, Hua, Jian, Zou, Baohong
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container_end_page 2092
container_issue 5
container_start_page 2077
container_title The New phytologist
container_volume 242
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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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 ; 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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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