Molecular dissection of maize seedling salt tolerance using a genome‐wide association analysis method
Summary Salt stress is a major devastating abiotic factor that affects the yield and quality of maize. However, knowledge of the molecular mechanisms of the responses to salt stress in maize is limited. To elucidate the genetic basis of salt tolerance traits, a genome‐wide association study was perf...
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Veröffentlicht in: | Plant biotechnology journal 2021-10, Vol.19 (10), p.1937-1951 |
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container_title | Plant biotechnology journal |
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creator | Luo, Meijie Zhang, Yunxia Li, Jingna Zhang, Panpan Chen, Kuan Song, Wei Wang, Xiaqing Yang, Jinxiao Lu, Xiaoduo Lu, Baishan Zhao, Yanxin Zhao, Jiuran |
description | Summary
Salt stress is a major devastating abiotic factor that affects the yield and quality of maize. However, knowledge of the molecular mechanisms of the responses to salt stress in maize is limited. To elucidate the genetic basis of salt tolerance traits, a genome‐wide association study was performed on 348 maize inbred lines under normal and salt stress conditions using 557 894 single nucleotide polymorphisms (SNPs). The phenotypic data for 27 traits revealed coefficients of variation of >25%. In total, 149 significant SNPs explaining 6.6%–11.2% of the phenotypic variation for each SNP were identified. Of the 104 identified quantitative trait loci (QTLs), 83 were related to salt tolerance and 21 to normal traits. Additionally, 13 QTLs were associated with two to five traits. Eleven and six QTLs controlling salt tolerance traits and normal root growth, respectively, co‐localized with QTL intervals reported previously. Based on functional annotations, 13 candidate genes were predicted. Expression levels analysis of 12 candidate genes revealed that they were all responsive to salt stress. The CRISPR/Cas9 technology targeting three sites was applied in maize, and its editing efficiency reached 70%. By comparing the biomass of three CRISPR/Cas9 mutants of ZmCLCg and one zmpmp3 EMS mutant with their wild‐type plants under salt stress, the salt tolerance function of candidate genes ZmCLCg and ZmPMP3 were confirmed. Chloride content analysis revealed that ZmCLCg regulated chloride transport under sodium chloride stress. These results help to explain genetic variations in salt tolerance and provide novel loci for generating salt‐tolerant maize lines. |
doi_str_mv | 10.1111/pbi.13607 |
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Salt stress is a major devastating abiotic factor that affects the yield and quality of maize. However, knowledge of the molecular mechanisms of the responses to salt stress in maize is limited. To elucidate the genetic basis of salt tolerance traits, a genome‐wide association study was performed on 348 maize inbred lines under normal and salt stress conditions using 557 894 single nucleotide polymorphisms (SNPs). The phenotypic data for 27 traits revealed coefficients of variation of >25%. In total, 149 significant SNPs explaining 6.6%–11.2% of the phenotypic variation for each SNP were identified. Of the 104 identified quantitative trait loci (QTLs), 83 were related to salt tolerance and 21 to normal traits. Additionally, 13 QTLs were associated with two to five traits. Eleven and six QTLs controlling salt tolerance traits and normal root growth, respectively, co‐localized with QTL intervals reported previously. Based on functional annotations, 13 candidate genes were predicted. Expression levels analysis of 12 candidate genes revealed that they were all responsive to salt stress. The CRISPR/Cas9 technology targeting three sites was applied in maize, and its editing efficiency reached 70%. By comparing the biomass of three CRISPR/Cas9 mutants of ZmCLCg and one zmpmp3 EMS mutant with their wild‐type plants under salt stress, the salt tolerance function of candidate genes ZmCLCg and ZmPMP3 were confirmed. Chloride content analysis revealed that ZmCLCg regulated chloride transport under sodium chloride stress. These results help to explain genetic variations in salt tolerance and provide novel loci for generating salt‐tolerant maize lines.</description><identifier>ISSN: 1467-7644</identifier><identifier>EISSN: 1467-7652</identifier><identifier>DOI: 10.1111/pbi.13607</identifier><identifier>PMID: 33934485</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Abiotic factors ; Abiotic stress ; Annotations ; Association analysis ; association mapping ; Chloride transport ; Coefficient of variation ; Content analysis ; Corn ; CRISPR ; Crops ; Gene expression ; Gene mapping ; Genes ; Genetic diversity ; genetic loci ; Genome-wide association studies ; Genomes ; Homeostasis ; Inbreeding ; maize ; Metabolism ; Metabolites ; Molecular modelling ; Mutants ; Nucleotides ; Phenotypic variations ; Plant growth ; Quantitative trait loci ; Rice ; Salinity ; Salinity tolerance ; Salt ; Salt tolerance ; Seedlings ; Single-nucleotide polymorphism ; Sodium chloride ; Stress</subject><ispartof>Plant biotechnology journal, 2021-10, Vol.19 (10), p.1937-1951</ispartof><rights>2021 The Authors. Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.</rights><rights>2021 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.</rights><rights>2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4437-dde9bdd5c4a4a594ab2bb64b4e7f7d7190154a6c883f8067bed46b999ea622023</citedby><cites>FETCH-LOGICAL-c4437-dde9bdd5c4a4a594ab2bb64b4e7f7d7190154a6c883f8067bed46b999ea622023</cites><orcidid>0000-0003-0694-016X ; 0000-0003-2044-6846 ; 0000-0001-5737-2583</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%2Fpbi.13607$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fpbi.13607$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,864,885,1416,11560,27922,27923,45572,45573,46050,46474</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33934485$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Luo, Meijie</creatorcontrib><creatorcontrib>Zhang, Yunxia</creatorcontrib><creatorcontrib>Li, Jingna</creatorcontrib><creatorcontrib>Zhang, Panpan</creatorcontrib><creatorcontrib>Chen, Kuan</creatorcontrib><creatorcontrib>Song, Wei</creatorcontrib><creatorcontrib>Wang, Xiaqing</creatorcontrib><creatorcontrib>Yang, Jinxiao</creatorcontrib><creatorcontrib>Lu, Xiaoduo</creatorcontrib><creatorcontrib>Lu, Baishan</creatorcontrib><creatorcontrib>Zhao, Yanxin</creatorcontrib><creatorcontrib>Zhao, Jiuran</creatorcontrib><title>Molecular dissection of maize seedling salt tolerance using a genome‐wide association analysis method</title><title>Plant biotechnology journal</title><addtitle>Plant Biotechnol J</addtitle><description>Summary
Salt stress is a major devastating abiotic factor that affects the yield and quality of maize. However, knowledge of the molecular mechanisms of the responses to salt stress in maize is limited. To elucidate the genetic basis of salt tolerance traits, a genome‐wide association study was performed on 348 maize inbred lines under normal and salt stress conditions using 557 894 single nucleotide polymorphisms (SNPs). The phenotypic data for 27 traits revealed coefficients of variation of >25%. In total, 149 significant SNPs explaining 6.6%–11.2% of the phenotypic variation for each SNP were identified. Of the 104 identified quantitative trait loci (QTLs), 83 were related to salt tolerance and 21 to normal traits. Additionally, 13 QTLs were associated with two to five traits. Eleven and six QTLs controlling salt tolerance traits and normal root growth, respectively, co‐localized with QTL intervals reported previously. Based on functional annotations, 13 candidate genes were predicted. Expression levels analysis of 12 candidate genes revealed that they were all responsive to salt stress. The CRISPR/Cas9 technology targeting three sites was applied in maize, and its editing efficiency reached 70%. By comparing the biomass of three CRISPR/Cas9 mutants of ZmCLCg and one zmpmp3 EMS mutant with their wild‐type plants under salt stress, the salt tolerance function of candidate genes ZmCLCg and ZmPMP3 were confirmed. Chloride content analysis revealed that ZmCLCg regulated chloride transport under sodium chloride stress. These results help to explain genetic variations in salt tolerance and provide novel loci for generating salt‐tolerant maize lines.</description><subject>Abiotic factors</subject><subject>Abiotic stress</subject><subject>Annotations</subject><subject>Association analysis</subject><subject>association mapping</subject><subject>Chloride transport</subject><subject>Coefficient of variation</subject><subject>Content analysis</subject><subject>Corn</subject><subject>CRISPR</subject><subject>Crops</subject><subject>Gene expression</subject><subject>Gene mapping</subject><subject>Genes</subject><subject>Genetic diversity</subject><subject>genetic loci</subject><subject>Genome-wide association studies</subject><subject>Genomes</subject><subject>Homeostasis</subject><subject>Inbreeding</subject><subject>maize</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Molecular modelling</subject><subject>Mutants</subject><subject>Nucleotides</subject><subject>Phenotypic variations</subject><subject>Plant growth</subject><subject>Quantitative trait loci</subject><subject>Rice</subject><subject>Salinity</subject><subject>Salinity tolerance</subject><subject>Salt</subject><subject>Salt tolerance</subject><subject>Seedlings</subject><subject>Single-nucleotide polymorphism</subject><subject>Sodium chloride</subject><subject>Stress</subject><issn>1467-7644</issn><issn>1467-7652</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp1kc9u1DAQhyNERUvhwAsgS1zaw7ax43-5INGq0EpFcICzNbYnW1dOvNgJ1XLiEXhGnoRst6wACV9sjT99M6NfVb2g9Qmdz-nKhhPayFo9qg4ol2qhpGCPd2_O96unpdzWNaNSyCfVftO0DedaHFTL9ymimyJk4kMp6MaQBpI60kP4hqQg-hiGJSkQRzLObIbBIZnKpghkiUPq8ef3H3fBI4FSkgtwr4AB4rqEQnocb5J_Vu11EAs-f7gPq89vLz6dXy6uP7y7On9zvXCcN2rhPbbWe-E4cBAtB8usldxyVJ3yirY1FRyk07rpdC2VRc-lbdsWQTJWs-awer31ribbo3c4jBmiWeXQQ16bBMH8_TOEG7NMX43mWjJBZ8HRgyCnLxOW0fShOIwRBkxTMUwwylvO6KbXq3_Q2zTlee8NpTTVotVqpo63lMuplIzdbhham018Zo7P3Mc3sy__nH5H_s5rBk63wF2IuP6_yXw8u9oqfwF8T6eV</recordid><startdate>202110</startdate><enddate>202110</enddate><creator>Luo, Meijie</creator><creator>Zhang, Yunxia</creator><creator>Li, Jingna</creator><creator>Zhang, Panpan</creator><creator>Chen, Kuan</creator><creator>Song, Wei</creator><creator>Wang, Xiaqing</creator><creator>Yang, Jinxiao</creator><creator>Lu, Xiaoduo</creator><creator>Lu, Baishan</creator><creator>Zhao, Yanxin</creator><creator>Zhao, Jiuran</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>L6V</scope><scope>LK8</scope><scope>M7P</scope><scope>M7S</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-0694-016X</orcidid><orcidid>https://orcid.org/0000-0003-2044-6846</orcidid><orcidid>https://orcid.org/0000-0001-5737-2583</orcidid></search><sort><creationdate>202110</creationdate><title>Molecular dissection of maize seedling salt tolerance using a genome‐wide association analysis method</title><author>Luo, Meijie ; Zhang, Yunxia ; Li, Jingna ; Zhang, Panpan ; Chen, Kuan ; Song, Wei ; Wang, Xiaqing ; Yang, Jinxiao ; Lu, Xiaoduo ; Lu, Baishan ; Zhao, Yanxin ; Zhao, Jiuran</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4437-dde9bdd5c4a4a594ab2bb64b4e7f7d7190154a6c883f8067bed46b999ea622023</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Abiotic factors</topic><topic>Abiotic stress</topic><topic>Annotations</topic><topic>Association analysis</topic><topic>association mapping</topic><topic>Chloride transport</topic><topic>Coefficient of variation</topic><topic>Content analysis</topic><topic>Corn</topic><topic>CRISPR</topic><topic>Crops</topic><topic>Gene expression</topic><topic>Gene mapping</topic><topic>Genes</topic><topic>Genetic diversity</topic><topic>genetic loci</topic><topic>Genome-wide association studies</topic><topic>Genomes</topic><topic>Homeostasis</topic><topic>Inbreeding</topic><topic>maize</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Molecular modelling</topic><topic>Mutants</topic><topic>Nucleotides</topic><topic>Phenotypic variations</topic><topic>Plant growth</topic><topic>Quantitative trait loci</topic><topic>Rice</topic><topic>Salinity</topic><topic>Salinity tolerance</topic><topic>Salt</topic><topic>Salt tolerance</topic><topic>Seedlings</topic><topic>Single-nucleotide polymorphism</topic><topic>Sodium chloride</topic><topic>Stress</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Luo, Meijie</creatorcontrib><creatorcontrib>Zhang, Yunxia</creatorcontrib><creatorcontrib>Li, Jingna</creatorcontrib><creatorcontrib>Zhang, Panpan</creatorcontrib><creatorcontrib>Chen, Kuan</creatorcontrib><creatorcontrib>Song, Wei</creatorcontrib><creatorcontrib>Wang, Xiaqing</creatorcontrib><creatorcontrib>Yang, Jinxiao</creatorcontrib><creatorcontrib>Lu, Xiaoduo</creatorcontrib><creatorcontrib>Lu, Baishan</creatorcontrib><creatorcontrib>Zhao, Yanxin</creatorcontrib><creatorcontrib>Zhao, Jiuran</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</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>Engineering Collection</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant biotechnology journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Luo, Meijie</au><au>Zhang, Yunxia</au><au>Li, Jingna</au><au>Zhang, Panpan</au><au>Chen, Kuan</au><au>Song, Wei</au><au>Wang, Xiaqing</au><au>Yang, Jinxiao</au><au>Lu, Xiaoduo</au><au>Lu, Baishan</au><au>Zhao, Yanxin</au><au>Zhao, Jiuran</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Molecular dissection of maize seedling salt tolerance using a genome‐wide association analysis method</atitle><jtitle>Plant biotechnology journal</jtitle><addtitle>Plant Biotechnol J</addtitle><date>2021-10</date><risdate>2021</risdate><volume>19</volume><issue>10</issue><spage>1937</spage><epage>1951</epage><pages>1937-1951</pages><issn>1467-7644</issn><eissn>1467-7652</eissn><abstract>Summary
Salt stress is a major devastating abiotic factor that affects the yield and quality of maize. However, knowledge of the molecular mechanisms of the responses to salt stress in maize is limited. To elucidate the genetic basis of salt tolerance traits, a genome‐wide association study was performed on 348 maize inbred lines under normal and salt stress conditions using 557 894 single nucleotide polymorphisms (SNPs). The phenotypic data for 27 traits revealed coefficients of variation of >25%. In total, 149 significant SNPs explaining 6.6%–11.2% of the phenotypic variation for each SNP were identified. Of the 104 identified quantitative trait loci (QTLs), 83 were related to salt tolerance and 21 to normal traits. Additionally, 13 QTLs were associated with two to five traits. Eleven and six QTLs controlling salt tolerance traits and normal root growth, respectively, co‐localized with QTL intervals reported previously. Based on functional annotations, 13 candidate genes were predicted. Expression levels analysis of 12 candidate genes revealed that they were all responsive to salt stress. The CRISPR/Cas9 technology targeting three sites was applied in maize, and its editing efficiency reached 70%. By comparing the biomass of three CRISPR/Cas9 mutants of ZmCLCg and one zmpmp3 EMS mutant with their wild‐type plants under salt stress, the salt tolerance function of candidate genes ZmCLCg and ZmPMP3 were confirmed. Chloride content analysis revealed that ZmCLCg regulated chloride transport under sodium chloride stress. These results help to explain genetic variations in salt tolerance and provide novel loci for generating salt‐tolerant maize lines.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>33934485</pmid><doi>10.1111/pbi.13607</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0003-0694-016X</orcidid><orcidid>https://orcid.org/0000-0003-2044-6846</orcidid><orcidid>https://orcid.org/0000-0001-5737-2583</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Abiotic factors Abiotic stress Annotations Association analysis association mapping Chloride transport Coefficient of variation Content analysis Corn CRISPR Crops Gene expression Gene mapping Genes Genetic diversity genetic loci Genome-wide association studies Genomes Homeostasis Inbreeding maize Metabolism Metabolites Molecular modelling Mutants Nucleotides Phenotypic variations Plant growth Quantitative trait loci Rice Salinity Salinity tolerance Salt Salt tolerance Seedlings Single-nucleotide polymorphism Sodium chloride Stress |
title | Molecular dissection of maize seedling salt tolerance using a genome‐wide association analysis method |
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