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An aspartic protease 47 causes quantitative recessive resistance to rice black‐streaked dwarf virus disease and southern rice black‐streaked dwarf virus disease
Summary Rice black‐streaked dwarf virus disease (RBSDVD) and southern rice black‐streaked dwarf virus disease (SRBSDVD) are the most destructive viral diseases in rice. Progress is limited in breeding due to lack of resistance resource and inadequate knowledge on the underlying functional gene. Usin...
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Published in: | The New phytologist 2022-03, Vol.233 (6), p.2520-2533 |
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creator | Wang, Zhaoyun Zhou, Lian Lan, Ying Li, Xuejuan Wang, Jian Dong, Jingfang Guo, Wei Jing, Dedao Liu, Qing Zhang, Shaohong Liu, Zhiyang Shi, Wenjuan Yang, Wu Yang, Tifeng Sun, Feng Du, Linlin Fu, Hua Ma, Yamei Shao, Yudong Chen, Luo Li, Jitong Li, Shuo Fan, Yongjian Wang, Yunyue Leung, Hei Liu, Bin Zhou, Yijun Zhao, Junliang Zhou, Tong |
description | Summary
Rice black‐streaked dwarf virus disease (RBSDVD) and southern rice black‐streaked dwarf virus disease (SRBSDVD) are the most destructive viral diseases in rice. Progress is limited in breeding due to lack of resistance resource and inadequate knowledge on the underlying functional gene.
Using genome‐wide association study (GWAS), linkage disequilibrium (LD) decay analyses, RNA‐sequencing, and genome editing, we identified a highly RBSDVD‐resistant variety and its first functional gene.
A highly RBSDVD‐resistant variety W44 was identified through extensive evaluation of a diverse international rice panel. Seventeen quantitative trait loci (QTLs) were identified among which qRBSDV6‐1 had the largest phenotypic effect. It was finely mapped to a 0.8–1.2 Mb region on chromosome 6, with 62 annotated genes. Analysis of the candidate genes underlying qRBSDV6‐1 showed high expression of aspartic proteinase 47 (OsAP47) in a susceptible variety, W122, and a low resistance variety, W44. OsAP47 overexpressing lines exhibited significantly reduced resistance, while the knockout mutants exhibited significantly reduced SRBSDVD and RBSDVD severity. Furthermore, the resistant allele Hap1 of OsAP47 is almost exclusive to Indica, but rare in Japonica.
Results suggest that OsAP47 knockout by editing is effective for improving RBSDVD and SRBSDVD resistance. This study provides genetic information for breeding resistant cultivars. |
doi_str_mv | 10.1111/nph.17961 |
format | article |
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Rice black‐streaked dwarf virus disease (RBSDVD) and southern rice black‐streaked dwarf virus disease (SRBSDVD) are the most destructive viral diseases in rice. Progress is limited in breeding due to lack of resistance resource and inadequate knowledge on the underlying functional gene.
Using genome‐wide association study (GWAS), linkage disequilibrium (LD) decay analyses, RNA‐sequencing, and genome editing, we identified a highly RBSDVD‐resistant variety and its first functional gene.
A highly RBSDVD‐resistant variety W44 was identified through extensive evaluation of a diverse international rice panel. Seventeen quantitative trait loci (QTLs) were identified among which qRBSDV6‐1 had the largest phenotypic effect. It was finely mapped to a 0.8–1.2 Mb region on chromosome 6, with 62 annotated genes. Analysis of the candidate genes underlying qRBSDV6‐1 showed high expression of aspartic proteinase 47 (OsAP47) in a susceptible variety, W122, and a low resistance variety, W44. OsAP47 overexpressing lines exhibited significantly reduced resistance, while the knockout mutants exhibited significantly reduced SRBSDVD and RBSDVD severity. Furthermore, the resistant allele Hap1 of OsAP47 is almost exclusive to Indica, but rare in Japonica.
Results suggest that OsAP47 knockout by editing is effective for improving RBSDVD and SRBSDVD resistance. This study provides genetic information for breeding resistant cultivars.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.17961</identifier><identifier>PMID: 35015901</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Aspartic Acid Proteases ; Aspartic endopeptidase ; Aspartic proteinase ; Breeding ; Chromosome 6 ; Chromosomes ; Cultivars ; Disease ; Disease resistance ; DNA sequences ; Editing ; Gene mapping ; Gene sequencing ; Genes ; Genome-wide association studies ; Genome-Wide Association Study ; Genomes ; Identification ; Linkage disequilibrium ; Low resistance ; Oryza - genetics ; Peptide Hydrolases ; Plant Breeding ; Plant Diseases - genetics ; Proteinase ; Quantitative trait loci ; quantitative trait loci (QTLs) ; Reoviridae ; resistance variety ; Rice ; rice black‐streaked dwarf virus (RBSDV) ; RNA editing ; southern rice black‐streaked dwarf virus (SRBSDV) ; Viral diseases ; Viroses ; Virus Diseases ; Viruses</subject><ispartof>The New phytologist, 2022-03, Vol.233 (6), p.2520-2533</ispartof><rights>2022 The Authors. © 2022 New Phytologist Foundation</rights><rights>2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.</rights><rights>Copyright © 2022 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3531-e045c70df4e18a87c79cf2a2a520b59eae7957bd0e74b18c2e33fc3716de62a93</citedby><cites>FETCH-LOGICAL-c3531-e045c70df4e18a87c79cf2a2a520b59eae7957bd0e74b18c2e33fc3716de62a93</cites><orcidid>0000-0001-5884-7982 ; 0000-0001-8706-3001 ; 0000-0002-0811-5166 ; 0000-0003-3194-3290 ; 0000-0002-3736-7522</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27923,27924</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35015901$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Zhaoyun</creatorcontrib><creatorcontrib>Zhou, Lian</creatorcontrib><creatorcontrib>Lan, Ying</creatorcontrib><creatorcontrib>Li, Xuejuan</creatorcontrib><creatorcontrib>Wang, Jian</creatorcontrib><creatorcontrib>Dong, Jingfang</creatorcontrib><creatorcontrib>Guo, Wei</creatorcontrib><creatorcontrib>Jing, Dedao</creatorcontrib><creatorcontrib>Liu, Qing</creatorcontrib><creatorcontrib>Zhang, Shaohong</creatorcontrib><creatorcontrib>Liu, Zhiyang</creatorcontrib><creatorcontrib>Shi, Wenjuan</creatorcontrib><creatorcontrib>Yang, Wu</creatorcontrib><creatorcontrib>Yang, Tifeng</creatorcontrib><creatorcontrib>Sun, Feng</creatorcontrib><creatorcontrib>Du, Linlin</creatorcontrib><creatorcontrib>Fu, Hua</creatorcontrib><creatorcontrib>Ma, Yamei</creatorcontrib><creatorcontrib>Shao, Yudong</creatorcontrib><creatorcontrib>Chen, Luo</creatorcontrib><creatorcontrib>Li, Jitong</creatorcontrib><creatorcontrib>Li, Shuo</creatorcontrib><creatorcontrib>Fan, Yongjian</creatorcontrib><creatorcontrib>Wang, Yunyue</creatorcontrib><creatorcontrib>Leung, Hei</creatorcontrib><creatorcontrib>Liu, Bin</creatorcontrib><creatorcontrib>Zhou, Yijun</creatorcontrib><creatorcontrib>Zhao, Junliang</creatorcontrib><creatorcontrib>Zhou, Tong</creatorcontrib><title>An aspartic protease 47 causes quantitative recessive resistance to rice black‐streaked dwarf virus disease and southern rice black‐streaked dwarf virus disease</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
Rice black‐streaked dwarf virus disease (RBSDVD) and southern rice black‐streaked dwarf virus disease (SRBSDVD) are the most destructive viral diseases in rice. Progress is limited in breeding due to lack of resistance resource and inadequate knowledge on the underlying functional gene.
Using genome‐wide association study (GWAS), linkage disequilibrium (LD) decay analyses, RNA‐sequencing, and genome editing, we identified a highly RBSDVD‐resistant variety and its first functional gene.
A highly RBSDVD‐resistant variety W44 was identified through extensive evaluation of a diverse international rice panel. Seventeen quantitative trait loci (QTLs) were identified among which qRBSDV6‐1 had the largest phenotypic effect. It was finely mapped to a 0.8–1.2 Mb region on chromosome 6, with 62 annotated genes. Analysis of the candidate genes underlying qRBSDV6‐1 showed high expression of aspartic proteinase 47 (OsAP47) in a susceptible variety, W122, and a low resistance variety, W44. OsAP47 overexpressing lines exhibited significantly reduced resistance, while the knockout mutants exhibited significantly reduced SRBSDVD and RBSDVD severity. Furthermore, the resistant allele Hap1 of OsAP47 is almost exclusive to Indica, but rare in Japonica.
Results suggest that OsAP47 knockout by editing is effective for improving RBSDVD and SRBSDVD resistance. This study provides genetic information for breeding resistant cultivars.</description><subject>Aspartic Acid Proteases</subject><subject>Aspartic endopeptidase</subject><subject>Aspartic proteinase</subject><subject>Breeding</subject><subject>Chromosome 6</subject><subject>Chromosomes</subject><subject>Cultivars</subject><subject>Disease</subject><subject>Disease resistance</subject><subject>DNA sequences</subject><subject>Editing</subject><subject>Gene mapping</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genome-wide association studies</subject><subject>Genome-Wide Association Study</subject><subject>Genomes</subject><subject>Identification</subject><subject>Linkage disequilibrium</subject><subject>Low resistance</subject><subject>Oryza - genetics</subject><subject>Peptide Hydrolases</subject><subject>Plant Breeding</subject><subject>Plant Diseases - genetics</subject><subject>Proteinase</subject><subject>Quantitative trait loci</subject><subject>quantitative trait loci (QTLs)</subject><subject>Reoviridae</subject><subject>resistance variety</subject><subject>Rice</subject><subject>rice black‐streaked dwarf virus (RBSDV)</subject><subject>RNA editing</subject><subject>southern rice black‐streaked dwarf virus (SRBSDV)</subject><subject>Viral diseases</subject><subject>Viroses</subject><subject>Virus Diseases</subject><subject>Viruses</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNqNkU9u1TAQhy0Eoo_CggsgS2xgkdZ_YjteVlWhSBWwAIldNHEmqtu85NXjtOqOI3AITsZJME1hgYTEbGYW33wazY-x51IcyFKH0-78QDpv5QO2kbX1VSO1e8g2QqimsrX9sseeEF0IIbyx6jHb00ZI44XcsO9HEwfaQcox8F2aMwIhrx0PsBASv1pgyjFDjtfIEwYkWieKlGEKyPPMUyy9GyFc_vj6jXJCuMSe9zeQBn4d00K8j3QnhqnnNC_5HNP0_2tP2aMBRsJn932ffX5z8un4tDr78Pbd8dFZFbTRskJRm-BEP9QoG2hccD4MChQYJTrjEdB547peoKs72QSFWg9BO2l7tAq83mevVm95xNWClNttpIDjCBPOC7XKSq9EUytT0Jd_oRfzkqZyXaGU1842WhXq9UqFNBMlHNpdiltIt60U7a_o2hJdexddYV_cG5dui_0f8ndWBThcgZs44u2_Te37j6er8id0Gag1</recordid><startdate>202203</startdate><enddate>202203</enddate><creator>Wang, Zhaoyun</creator><creator>Zhou, Lian</creator><creator>Lan, Ying</creator><creator>Li, Xuejuan</creator><creator>Wang, Jian</creator><creator>Dong, Jingfang</creator><creator>Guo, Wei</creator><creator>Jing, Dedao</creator><creator>Liu, Qing</creator><creator>Zhang, Shaohong</creator><creator>Liu, Zhiyang</creator><creator>Shi, Wenjuan</creator><creator>Yang, Wu</creator><creator>Yang, Tifeng</creator><creator>Sun, Feng</creator><creator>Du, Linlin</creator><creator>Fu, Hua</creator><creator>Ma, Yamei</creator><creator>Shao, Yudong</creator><creator>Chen, Luo</creator><creator>Li, Jitong</creator><creator>Li, Shuo</creator><creator>Fan, Yongjian</creator><creator>Wang, Yunyue</creator><creator>Leung, Hei</creator><creator>Liu, Bin</creator><creator>Zhou, Yijun</creator><creator>Zhao, Junliang</creator><creator>Zhou, Tong</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><orcidid>https://orcid.org/0000-0001-5884-7982</orcidid><orcidid>https://orcid.org/0000-0001-8706-3001</orcidid><orcidid>https://orcid.org/0000-0002-0811-5166</orcidid><orcidid>https://orcid.org/0000-0003-3194-3290</orcidid><orcidid>https://orcid.org/0000-0002-3736-7522</orcidid></search><sort><creationdate>202203</creationdate><title>An aspartic protease 47 causes quantitative recessive resistance to rice black‐streaked dwarf virus disease and southern rice black‐streaked dwarf virus disease</title><author>Wang, Zhaoyun ; Zhou, Lian ; Lan, Ying ; Li, Xuejuan ; Wang, Jian ; Dong, Jingfang ; Guo, Wei ; Jing, Dedao ; Liu, Qing ; Zhang, Shaohong ; Liu, Zhiyang ; Shi, Wenjuan ; Yang, Wu ; Yang, Tifeng ; Sun, Feng ; Du, Linlin ; Fu, Hua ; Ma, Yamei ; Shao, Yudong ; Chen, Luo ; Li, Jitong ; Li, Shuo ; Fan, Yongjian ; Wang, Yunyue ; Leung, Hei ; Liu, Bin ; Zhou, Yijun ; Zhao, Junliang ; Zhou, Tong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3531-e045c70df4e18a87c79cf2a2a520b59eae7957bd0e74b18c2e33fc3716de62a93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Aspartic Acid Proteases</topic><topic>Aspartic endopeptidase</topic><topic>Aspartic proteinase</topic><topic>Breeding</topic><topic>Chromosome 6</topic><topic>Chromosomes</topic><topic>Cultivars</topic><topic>Disease</topic><topic>Disease resistance</topic><topic>DNA sequences</topic><topic>Editing</topic><topic>Gene mapping</topic><topic>Gene sequencing</topic><topic>Genes</topic><topic>Genome-wide association studies</topic><topic>Genome-Wide Association Study</topic><topic>Genomes</topic><topic>Identification</topic><topic>Linkage disequilibrium</topic><topic>Low resistance</topic><topic>Oryza - genetics</topic><topic>Peptide Hydrolases</topic><topic>Plant Breeding</topic><topic>Plant Diseases - genetics</topic><topic>Proteinase</topic><topic>Quantitative trait loci</topic><topic>quantitative trait loci (QTLs)</topic><topic>Reoviridae</topic><topic>resistance variety</topic><topic>Rice</topic><topic>rice black‐streaked dwarf virus (RBSDV)</topic><topic>RNA editing</topic><topic>southern rice black‐streaked dwarf virus (SRBSDV)</topic><topic>Viral diseases</topic><topic>Viroses</topic><topic>Virus Diseases</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Zhaoyun</creatorcontrib><creatorcontrib>Zhou, Lian</creatorcontrib><creatorcontrib>Lan, Ying</creatorcontrib><creatorcontrib>Li, 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Yijun</creatorcontrib><creatorcontrib>Zhao, Junliang</creatorcontrib><creatorcontrib>Zhou, Tong</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><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Zhaoyun</au><au>Zhou, Lian</au><au>Lan, Ying</au><au>Li, Xuejuan</au><au>Wang, Jian</au><au>Dong, Jingfang</au><au>Guo, Wei</au><au>Jing, Dedao</au><au>Liu, Qing</au><au>Zhang, Shaohong</au><au>Liu, Zhiyang</au><au>Shi, Wenjuan</au><au>Yang, Wu</au><au>Yang, Tifeng</au><au>Sun, Feng</au><au>Du, Linlin</au><au>Fu, Hua</au><au>Ma, Yamei</au><au>Shao, Yudong</au><au>Chen, Luo</au><au>Li, Jitong</au><au>Li, Shuo</au><au>Fan, Yongjian</au><au>Wang, Yunyue</au><au>Leung, Hei</au><au>Liu, Bin</au><au>Zhou, Yijun</au><au>Zhao, Junliang</au><au>Zhou, Tong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>An aspartic protease 47 causes quantitative recessive resistance to rice black‐streaked dwarf virus disease and southern rice black‐streaked dwarf virus disease</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2022-03</date><risdate>2022</risdate><volume>233</volume><issue>6</issue><spage>2520</spage><epage>2533</epage><pages>2520-2533</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Summary
Rice black‐streaked dwarf virus disease (RBSDVD) and southern rice black‐streaked dwarf virus disease (SRBSDVD) are the most destructive viral diseases in rice. Progress is limited in breeding due to lack of resistance resource and inadequate knowledge on the underlying functional gene.
Using genome‐wide association study (GWAS), linkage disequilibrium (LD) decay analyses, RNA‐sequencing, and genome editing, we identified a highly RBSDVD‐resistant variety and its first functional gene.
A highly RBSDVD‐resistant variety W44 was identified through extensive evaluation of a diverse international rice panel. Seventeen quantitative trait loci (QTLs) were identified among which qRBSDV6‐1 had the largest phenotypic effect. It was finely mapped to a 0.8–1.2 Mb region on chromosome 6, with 62 annotated genes. Analysis of the candidate genes underlying qRBSDV6‐1 showed high expression of aspartic proteinase 47 (OsAP47) in a susceptible variety, W122, and a low resistance variety, W44. OsAP47 overexpressing lines exhibited significantly reduced resistance, while the knockout mutants exhibited significantly reduced SRBSDVD and RBSDVD severity. Furthermore, the resistant allele Hap1 of OsAP47 is almost exclusive to Indica, but rare in Japonica.
Results suggest that OsAP47 knockout by editing is effective for improving RBSDVD and SRBSDVD resistance. This study provides genetic information for breeding resistant cultivars.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>35015901</pmid><doi>10.1111/nph.17961</doi><tpages>2533</tpages><orcidid>https://orcid.org/0000-0001-5884-7982</orcidid><orcidid>https://orcid.org/0000-0001-8706-3001</orcidid><orcidid>https://orcid.org/0000-0002-0811-5166</orcidid><orcidid>https://orcid.org/0000-0003-3194-3290</orcidid><orcidid>https://orcid.org/0000-0002-3736-7522</orcidid></addata></record> |
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subjects | Aspartic Acid Proteases Aspartic endopeptidase Aspartic proteinase Breeding Chromosome 6 Chromosomes Cultivars Disease Disease resistance DNA sequences Editing Gene mapping Gene sequencing Genes Genome-wide association studies Genome-Wide Association Study Genomes Identification Linkage disequilibrium Low resistance Oryza - genetics Peptide Hydrolases Plant Breeding Plant Diseases - genetics Proteinase Quantitative trait loci quantitative trait loci (QTLs) Reoviridae resistance variety Rice rice black‐streaked dwarf virus (RBSDV) RNA editing southern rice black‐streaked dwarf virus (SRBSDV) Viral diseases Viroses Virus Diseases Viruses |
title | An aspartic protease 47 causes quantitative recessive resistance to rice black‐streaked dwarf virus disease and southern rice black‐streaked dwarf virus disease |
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