A plant reovirus hijacks endoplasmic reticulum-associated degradation machinery to promote efficient viral transmission by its planthopper vector under high temperature conditions
In the field, many insect-borne crop viral diseases are more suitable for maintenance and spread in hot-temperature areas, but the mechanism remains poorly understood. The epidemic of a planthopper (Sogatella furcifera)-transmitted rice reovirus (southern rice black-streaked dwarf virus, SRBSDV) is...
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| creator | Yu, Xiangzhen Jia, Dongsheng Wang, Zhen Li, Guangjun Chen, Manni Liang, Qifu Zhou, Yanyan Liu, Huan Xiao, Mi Li, Siting Chen, Qian Chen, Hongyan Wei, Taiyun |
| description | In the field, many insect-borne crop viral diseases are more suitable for maintenance and spread in hot-temperature areas, but the mechanism remains poorly understood. The epidemic of a planthopper (Sogatella furcifera)-transmitted rice reovirus (southern rice black-streaked dwarf virus, SRBSDV) is geographically restricted to southern China and northern Vietnam with year-round hot temperatures. Here, we reported that two factors of endoplasmic reticulum-associated degradation (ERAD) machinery, the heat shock protein DnaJB11 and ER membrane protein BAP31, were activated by viral infection to mediate the adaptation of S. furcifera to high temperatures. Infection and transmission efficiencies of SRBSDV by S. furcifera increased with the elevated temperatures. We observed that high temperature (35°C) was beneficial for the assembly of virus-containing tubular structures formed by nonstructural protein P7-1 of SRBSDV, which facilitates efficient viral transmission by S. furcifera. Both DnaJB11 and BAP31 competed to directly bind to the tubule protein P7-1 of SRBSDV; however, DnaJB11 promoted whereas BAP31 inhibited P7-1 tubule assembly at the ER membrane. Furthermore, the binding affinity of DnaJB11 with P7-1 was stronger than that of BAP31 with P7-1. We also revealed that BAP31 negatively regulated DnaJB11 expression through their direct interaction. High temperatures could significantly upregulate DnaJB11 expression but inhibit BAP31 expression, thereby strongly facilitating the assembly of abundant P7-1 tubules. Taken together, we showed that a new temperature-dependent protein quality control pathway in the ERAD machinery has evolved for strong activation of DnaJB11 for benefiting P7-1 tubules assembly to support efficient transmission of SRBSDV in high temperatures. We thus deduced that ERAD machinery has been hitchhiked by insect-borne crop viruses to enhance their transmission in tropical climates. |
| doi_str_mv | 10.1371/journal.ppat.1009347 |
| format | Article |
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The epidemic of a planthopper (Sogatella furcifera)-transmitted rice reovirus (southern rice black-streaked dwarf virus, SRBSDV) is geographically restricted to southern China and northern Vietnam with year-round hot temperatures. Here, we reported that two factors of endoplasmic reticulum-associated degradation (ERAD) machinery, the heat shock protein DnaJB11 and ER membrane protein BAP31, were activated by viral infection to mediate the adaptation of S. furcifera to high temperatures. Infection and transmission efficiencies of SRBSDV by S. furcifera increased with the elevated temperatures. We observed that high temperature (35°C) was beneficial for the assembly of virus-containing tubular structures formed by nonstructural protein P7-1 of SRBSDV, which facilitates efficient viral transmission by S. furcifera. Both DnaJB11 and BAP31 competed to directly bind to the tubule protein P7-1 of SRBSDV; however, DnaJB11 promoted whereas BAP31 inhibited P7-1 tubule assembly at the ER membrane. Furthermore, the binding affinity of DnaJB11 with P7-1 was stronger than that of BAP31 with P7-1. We also revealed that BAP31 negatively regulated DnaJB11 expression through their direct interaction. High temperatures could significantly upregulate DnaJB11 expression but inhibit BAP31 expression, thereby strongly facilitating the assembly of abundant P7-1 tubules. Taken together, we showed that a new temperature-dependent protein quality control pathway in the ERAD machinery has evolved for strong activation of DnaJB11 for benefiting P7-1 tubules assembly to support efficient transmission of SRBSDV in high temperatures. We thus deduced that ERAD machinery has been hitchhiked by insect-borne crop viruses to enhance their transmission in tropical climates.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1009347</identifier><identifier>PMID: 33647067</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Ambient temperature ; Biodegradation ; Biology and Life Sciences ; Body temperature ; Brefeldin A ; Disease transmission ; Distribution ; Endoplasmic reticulum ; Environmental aspects ; Epidemics ; Health aspects ; Heat ; Heat shock proteins ; High temperature ; Infections ; Insects ; Low temperature ; Medicine and Health Sciences ; Membrane proteins ; Microscopy ; Mortality ; Nonstructural proteins ; Pathogens ; Physiological aspects ; Plant viruses ; Planthoppers ; Reoviruses ; Research and Analysis Methods ; Temperature tolerance ; Transmission efficiency ; Tubules ; Vectors ; Vectors (Biology) ; Viral diseases ; Viral infections ; Virus diseases of plants ; Viruses ; West Nile virus</subject><ispartof>PLoS pathogens, 2021-03, Vol.17 (3), p.e1009347-e1009347</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Yu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 Yu et al 2021 Yu et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c661t-a06ecbffe3c55c8da4a38a1bd12a88aa01b646fa2af286712f6087823683523d3</citedby><cites>FETCH-LOGICAL-c661t-a06ecbffe3c55c8da4a38a1bd12a88aa01b646fa2af286712f6087823683523d3</cites><orcidid>0000-0002-0732-9752 ; 0000-0002-6746-5211</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7951979/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7951979/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33647067$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Wang, Xiao-Wei</contributor><creatorcontrib>Yu, Xiangzhen</creatorcontrib><creatorcontrib>Jia, Dongsheng</creatorcontrib><creatorcontrib>Wang, Zhen</creatorcontrib><creatorcontrib>Li, Guangjun</creatorcontrib><creatorcontrib>Chen, Manni</creatorcontrib><creatorcontrib>Liang, Qifu</creatorcontrib><creatorcontrib>Zhou, Yanyan</creatorcontrib><creatorcontrib>Liu, Huan</creatorcontrib><creatorcontrib>Xiao, Mi</creatorcontrib><creatorcontrib>Li, Siting</creatorcontrib><creatorcontrib>Chen, Qian</creatorcontrib><creatorcontrib>Chen, Hongyan</creatorcontrib><creatorcontrib>Wei, Taiyun</creatorcontrib><title>A plant reovirus hijacks endoplasmic reticulum-associated degradation machinery to promote efficient viral transmission by its planthopper vector under high temperature conditions</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>In the field, many insect-borne crop viral diseases are more suitable for maintenance and spread in hot-temperature areas, but the mechanism remains poorly understood. The epidemic of a planthopper (Sogatella furcifera)-transmitted rice reovirus (southern rice black-streaked dwarf virus, SRBSDV) is geographically restricted to southern China and northern Vietnam with year-round hot temperatures. Here, we reported that two factors of endoplasmic reticulum-associated degradation (ERAD) machinery, the heat shock protein DnaJB11 and ER membrane protein BAP31, were activated by viral infection to mediate the adaptation of S. furcifera to high temperatures. Infection and transmission efficiencies of SRBSDV by S. furcifera increased with the elevated temperatures. We observed that high temperature (35°C) was beneficial for the assembly of virus-containing tubular structures formed by nonstructural protein P7-1 of SRBSDV, which facilitates efficient viral transmission by S. furcifera. Both DnaJB11 and BAP31 competed to directly bind to the tubule protein P7-1 of SRBSDV; however, DnaJB11 promoted whereas BAP31 inhibited P7-1 tubule assembly at the ER membrane. Furthermore, the binding affinity of DnaJB11 with P7-1 was stronger than that of BAP31 with P7-1. We also revealed that BAP31 negatively regulated DnaJB11 expression through their direct interaction. High temperatures could significantly upregulate DnaJB11 expression but inhibit BAP31 expression, thereby strongly facilitating the assembly of abundant P7-1 tubules. Taken together, we showed that a new temperature-dependent protein quality control pathway in the ERAD machinery has evolved for strong activation of DnaJB11 for benefiting P7-1 tubules assembly to support efficient transmission of SRBSDV in high temperatures. We thus deduced that ERAD machinery has been hitchhiked by insect-borne crop viruses to enhance their transmission in tropical climates.</description><subject>Ambient temperature</subject><subject>Biodegradation</subject><subject>Biology and Life Sciences</subject><subject>Body temperature</subject><subject>Brefeldin A</subject><subject>Disease transmission</subject><subject>Distribution</subject><subject>Endoplasmic reticulum</subject><subject>Environmental aspects</subject><subject>Epidemics</subject><subject>Health aspects</subject><subject>Heat</subject><subject>Heat shock proteins</subject><subject>High temperature</subject><subject>Infections</subject><subject>Insects</subject><subject>Low temperature</subject><subject>Medicine and Health Sciences</subject><subject>Membrane proteins</subject><subject>Microscopy</subject><subject>Mortality</subject><subject>Nonstructural proteins</subject><subject>Pathogens</subject><subject>Physiological aspects</subject><subject>Plant viruses</subject><subject>Planthoppers</subject><subject>Reoviruses</subject><subject>Research and Analysis Methods</subject><subject>Temperature tolerance</subject><subject>Transmission efficiency</subject><subject>Tubules</subject><subject>Vectors</subject><subject>Vectors (Biology)</subject><subject>Viral diseases</subject><subject>Viral infections</subject><subject>Virus diseases of plants</subject><subject>Viruses</subject><subject>West Nile 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plant reovirus hijacks endoplasmic reticulum-associated degradation machinery to promote efficient viral transmission by its planthopper vector under high temperature conditions</title><author>Yu, Xiangzhen ; Jia, Dongsheng ; Wang, Zhen ; Li, Guangjun ; Chen, Manni ; Liang, Qifu ; Zhou, Yanyan ; Liu, Huan ; Xiao, Mi ; Li, Siting ; Chen, Qian ; Chen, Hongyan ; Wei, Taiyun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c661t-a06ecbffe3c55c8da4a38a1bd12a88aa01b646fa2af286712f6087823683523d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Ambient temperature</topic><topic>Biodegradation</topic><topic>Biology and Life Sciences</topic><topic>Body temperature</topic><topic>Brefeldin A</topic><topic>Disease transmission</topic><topic>Distribution</topic><topic>Endoplasmic reticulum</topic><topic>Environmental aspects</topic><topic>Epidemics</topic><topic>Health 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Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yu, Xiangzhen</au><au>Jia, Dongsheng</au><au>Wang, Zhen</au><au>Li, Guangjun</au><au>Chen, Manni</au><au>Liang, Qifu</au><au>Zhou, Yanyan</au><au>Liu, Huan</au><au>Xiao, Mi</au><au>Li, Siting</au><au>Chen, Qian</au><au>Chen, Hongyan</au><au>Wei, Taiyun</au><au>Wang, Xiao-Wei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A plant reovirus hijacks endoplasmic reticulum-associated degradation machinery to promote efficient viral transmission by its planthopper vector under high temperature conditions</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2021-03</date><risdate>2021</risdate><volume>17</volume><issue>3</issue><spage>e1009347</spage><epage>e1009347</epage><pages>e1009347-e1009347</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>In the field, many insect-borne crop viral diseases are more suitable for maintenance and spread in hot-temperature areas, but the mechanism remains poorly understood. The epidemic of a planthopper (Sogatella furcifera)-transmitted rice reovirus (southern rice black-streaked dwarf virus, SRBSDV) is geographically restricted to southern China and northern Vietnam with year-round hot temperatures. Here, we reported that two factors of endoplasmic reticulum-associated degradation (ERAD) machinery, the heat shock protein DnaJB11 and ER membrane protein BAP31, were activated by viral infection to mediate the adaptation of S. furcifera to high temperatures. Infection and transmission efficiencies of SRBSDV by S. furcifera increased with the elevated temperatures. We observed that high temperature (35°C) was beneficial for the assembly of virus-containing tubular structures formed by nonstructural protein P7-1 of SRBSDV, which facilitates efficient viral transmission by S. furcifera. Both DnaJB11 and BAP31 competed to directly bind to the tubule protein P7-1 of SRBSDV; however, DnaJB11 promoted whereas BAP31 inhibited P7-1 tubule assembly at the ER membrane. Furthermore, the binding affinity of DnaJB11 with P7-1 was stronger than that of BAP31 with P7-1. We also revealed that BAP31 negatively regulated DnaJB11 expression through their direct interaction. High temperatures could significantly upregulate DnaJB11 expression but inhibit BAP31 expression, thereby strongly facilitating the assembly of abundant P7-1 tubules. Taken together, we showed that a new temperature-dependent protein quality control pathway in the ERAD machinery has evolved for strong activation of DnaJB11 for benefiting P7-1 tubules assembly to support efficient transmission of SRBSDV in high temperatures. We thus deduced that ERAD machinery has been hitchhiked by insect-borne crop viruses to enhance their transmission in tropical climates.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33647067</pmid><doi>10.1371/journal.ppat.1009347</doi><orcidid>https://orcid.org/0000-0002-0732-9752</orcidid><orcidid>https://orcid.org/0000-0002-6746-5211</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1553-7374 |
| ispartof | PLoS pathogens, 2021-03, Vol.17 (3), p.e1009347-e1009347 |
| issn | 1553-7374 1553-7366 1553-7374 |
| language | eng |
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| source | DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central Open Access; Public Library of Science (PLoS); PubMed Central |
| subjects | Ambient temperature Biodegradation Biology and Life Sciences Body temperature Brefeldin A Disease transmission Distribution Endoplasmic reticulum Environmental aspects Epidemics Health aspects Heat Heat shock proteins High temperature Infections Insects Low temperature Medicine and Health Sciences Membrane proteins Microscopy Mortality Nonstructural proteins Pathogens Physiological aspects Plant viruses Planthoppers Reoviruses Research and Analysis Methods Temperature tolerance Transmission efficiency Tubules Vectors Vectors (Biology) Viral diseases Viral infections Virus diseases of plants Viruses West Nile virus |
| title | A plant reovirus hijacks endoplasmic reticulum-associated degradation machinery to promote efficient viral transmission by its planthopper vector under high temperature conditions |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-25T02%3A32%3A45IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20plant%20reovirus%20hijacks%20endoplasmic%20reticulum-associated%20degradation%20machinery%20to%20promote%20efficient%20viral%20transmission%20by%20its%20planthopper%20vector%20under%20high%20temperature%20conditions&rft.jtitle=PLoS%20pathogens&rft.au=Yu,%20Xiangzhen&rft.date=2021-03&rft.volume=17&rft.issue=3&rft.spage=e1009347&rft.epage=e1009347&rft.pages=e1009347-e1009347&rft.issn=1553-7374&rft.eissn=1553-7374&rft_id=info:doi/10.1371/journal.ppat.1009347&rft_dat=%3Cgale_plos_%3EA658713038%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2513689703&rft_id=info:pmid/33647067&rft_galeid=A658713038&rft_doaj_id=oai_doaj_org_article_513091722e5f4b64a688683814084165&rfr_iscdi=true |