{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,12]],"date-time":"2026-10-12T03:32:47Z","timestamp":1791775967203,"version":"4.3.4"},"reference-count":16,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2026,7,17]],"date-time":"2026-07-17T00:00:00Z","timestamp":1784246400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000040","name":"Agriculture and Agri-Food Canada","doi-asserted-by":"publisher","award":["J-002838"],"award-info":[{"award-number":["J-002838"]}],"id":[{"id":"10.13039\/501100000040","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000040","name":"Agriculture and Agri-Food Canada","doi-asserted-by":"publisher","award":["J-003395"],"award-info":[{"award-number":["J-003395"]}],"id":[{"id":"10.13039\/501100000040","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000040","name":"Agriculture and Agri-Food Canada","doi-asserted-by":"publisher","award":["J-003896"],"award-info":[{"award-number":["J-003896"]}],"id":[{"id":"10.13039\/501100000040","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"\n The tomato\n Tm-2<\/jats:italic>\n \n 2<\/jats:italic>\n <\/jats:sup>\n gene is a highly effective, and durable resistance gene in agriculture that has protected tomato production against viruses of the\n Tobamovirus<\/jats:italic>\n genus, such as tomato mosaic virus (ToMV) and tobacco mosaic virus (TMV) for over 60 years. This dominant\n R<\/jats:italic>\n gene, originally sourced from wild tomato species (\n Solanum peruvianum<\/jats:italic>\n ), acts by recognizing the viral movement protein (MP) and triggering an immune response, often resulting in extreme resistance (ER). However, this durable protection is challenged by a recently emerged new tobamovirus named tomato brown rugose fruit virus (ToBRFV,\n Tobamovirus fructirugosum<\/jats:italic>\n ). ToBRFV-encoded MP is responsible for ER breakdown. Here, we present evidence that while ToBRFV can evade\n Tm-2<\/jats:italic>\n \n 2<\/jats:italic>\n <\/jats:sup>\n -mediated ER,\n Nicotiana benthamiana<\/jats:italic>\n and tomato plants carrying\n Tm-2<\/jats:italic>\n \n 2<\/jats:italic>\n <\/jats:sup>\n still remain partially resistant to ToBRFV. We show that ToBRFV MP is recognized by and interacts with Tm-2\n 2<\/jats:sup>\n to trigger an attenuated hypersensitive response. Moreover, we discover that overexpression of Tm-2\n 2<\/jats:sup>\n can enhance resistance to ToBRFV. These findings demonstrate the practical value of\n Tm-2<\/jats:italic>\n \n 2<\/jats:italic>\n <\/jats:sup>\n in ongoing resistance breeding programs and open a potential avenue to restore\n Tm-2<\/jats:italic>\n \n 2<\/jats:italic>\n <\/jats:sup>\n immunity through upregulation of\n Tm-2<\/jats:italic>\n \n 2<\/jats:italic>\n <\/jats:sup>\n expression.\n <\/jats:p>","DOI":"10.1371\/journal.ppat.1014380","type":"journal-article","created":{"date-parts":[[2026,7,17]],"date-time":"2026-07-17T17:42:02Z","timestamp":1784310122000},"page":"e1014380","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":3,"title":["The durable resistance gene Tm-22 remains partially resistant to tomato brown rugose fruit virus"],"prefix":"10.1371","volume":"22","author":[{"given":"Shaokang","family":"Zhang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark A.","family":"Bernards","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2233-0652","authenticated-orcid":true,"given":"Aiming","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2026,7,17]]},"reference":[{"issue":"9","key":"ppat.1014380.ref001","doi-asserted-by":"crossref","first-page":"1262","DOI":"10.1111\/mpp.13229","article-title":"Tomato brown rugose fruit virus: An emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide","volume":"23","author":"S Zhang","year":"2022","journal-title":"Mol Plant Pathol"},{"issue":"1","key":"ppat.1014380.ref002","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1146\/annurev-virology-111821-122847","article-title":"Breaking boundaries: The perpetual interplay between tobamoviruses and plant immunity","volume":"10","author":"Z Spiegelman","year":"2023","journal-title":"Annu Rev Virol"},{"key":"ppat.1014380.ref003","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1146\/annurev-phyto-021622-120703","article-title":"Tomato brown rugose fruit virus pandemic","volume":"61","author":"NM Salem","year":"2023","journal-title":"Annu Rev Phytopathol"},{"issue":"4","key":"ppat.1014380.ref004","doi-asserted-by":"crossref","first-page":"530","DOI":"10.3390\/v16040530","article-title":"Plant Immunity against tobamoviruses","volume":"16","author":"X Zheng","year":"2024","journal-title":"Viruses"},{"issue":"5","key":"ppat.1014380.ref005","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1023\/A:1025434519282","article-title":"Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-2(2) from Lycopersicon esculentum","volume":"52","author":"FC Lanfermeijer","year":"2003","journal-title":"Plant Mol Biol"},{"issue":"4","key":"ppat.1014380.ref006","doi-asserted-by":"crossref","first-page":"2399","DOI":"10.1104\/pp.16.01512","article-title":"Antiviral resistance protein Tm-22 functions on the plasma membrane","volume":"173","author":"T Chen","year":"2017","journal-title":"Plant Physiol"},{"issue":"8","key":"ppat.1014380.ref007","doi-asserted-by":"crossref","first-page":"838","DOI":"10.1111\/mpp.13318","article-title":"Activation of Tm-22 resistance is mediated by a conserved cysteine essential for tobacco mosaic virus movement","volume":"24","author":"H Hak","year":"2023","journal-title":"Mol Plant Pathol"},{"issue":"4","key":"ppat.1014380.ref008","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1008475","article-title":"Plant NLR immune receptor Tm-22 activation requires NB-ARC domain-mediated self-association of CC domain","volume":"16","author":"J Wang","journal-title":"PLoS Pathog"},{"issue":"9","key":"ppat.1014380.ref009","doi-asserted-by":"crossref","first-page":"1024","DOI":"10.1094\/MPMI-01-21-0023-R","article-title":"The tomato brown rugose fruit virus movement protein overcomes Tm-22 resistance in tomato while attenuating viral transport","volume":"34","author":"H Hak","year":"2021","journal-title":"Mol Plant Microbe Interact"},{"issue":"11","key":"ppat.1014380.ref010","doi-asserted-by":"crossref","first-page":"1347","DOI":"10.1111\/mpp.13115","article-title":"Identification of genetic determinants of tomato brown rugose fruit virus that enable infection of plants harbouring the Tm-22 resistance gene","volume":"22","author":"Z-Y Yan","year":"2021","journal-title":"Mol Plant Pathol"},{"issue":"3","key":"ppat.1014380.ref011","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1093\/mp\/sss153","article-title":"Tm-22 confers different resistance responses against tobacco mosaic virus dependent on its expression level","volume":"6","author":"H Zhang","year":"2013","journal-title":"Mol Plant"},{"issue":"4","key":"ppat.1014380.ref012","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1046\/j.1365-313X.2002.01297.x","article-title":"Tobacco Rar1, EDS1 and NPR1\/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus","volume":"30","author":"Y Liu","year":"2002","journal-title":"Plant J"},{"issue":"1","key":"ppat.1014380.ref013","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1094\/MPMI-07-25-0095-R","article-title":"Single Amino acid change at two conserved residues in tomato brown rugose fruit virus coat protein compromises virion assembly and viral systemic infection","volume":"39","author":"S Zhang","year":"2026","journal-title":"Mol Plant Microbe Interact"},{"issue":"9","key":"ppat.1014380.ref014","doi-asserted-by":"crossref","first-page":"1369","DOI":"10.1016\/j.molp.2024.07.010","article-title":"Proxitome profiling reveals a conserved SGT1-NSL1 signaling module that activates NLR-mediated immunity","volume":"17","author":"D Zhang","year":"2024","journal-title":"Mol Plant"},{"issue":"11","key":"ppat.1014380.ref015","doi-asserted-by":"crossref","first-page":"1398","DOI":"10.1094\/MPMI-21-11-1398","article-title":"High level expression of a virus resistance gene, RCY1, confers extreme resistance to Cucumber mosaic virus in Arabidopsis thaliana","volume":"21","author":"K-T Sekine","year":"2008","journal-title":"Mol Plant Microbe Interact"},{"issue":"11","key":"ppat.1014380.ref016","doi-asserted-by":"crossref","first-page":"3392","DOI":"10.1007\/s11427-025-3026-7","article-title":"Engineering resistance genes against tomato brown rugose fruit virus","volume":"68","author":"J Wang","year":"2025","journal-title":"Sci China Life Sci"}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1014380","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,17]],"date-time":"2026-07-17T17:42:07Z","timestamp":1784310127000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1014380"}},"subtitle":[],"editor":[{"given":"Ying","family":"Wang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2026,7,17]]},"references-count":16,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2026,7,17]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1014380","relation":{},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,17]]}}}