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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
Main Authors: 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
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cited_by cdi_FETCH-LOGICAL-c3531-e045c70df4e18a87c79cf2a2a520b59eae7957bd0e74b18c2e33fc3716de62a93
cites cdi_FETCH-LOGICAL-c3531-e045c70df4e18a87c79cf2a2a520b59eae7957bd0e74b18c2e33fc3716de62a93
container_end_page 2533
container_issue 6
container_start_page 2520
container_title The New phytologist
container_volume 233
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
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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, 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><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 &amp; 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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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identifier ISSN: 0028-646X
ispartof The New phytologist, 2022-03, Vol.233 (6), p.2520-2533
issn 0028-646X
1469-8137
language eng
recordid cdi_proquest_miscellaneous_2619208425
source Wiley
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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