Autophagy plays an antiviral defence role against tomato spotted wilt orthotospovirus and is counteracted by viral effector NSs
Autophagy, an intracellular degradation process, has emerged as a crucial innate immune response against various plant pathogens, including viruses. Tomato spotted wilt orthotospovirus (TSWV) is a highly destructive plant pathogen that infects over 1000 plant species and poses a significant threat t...
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| Veröffentlicht in: | Molecular plant pathology 2024-10, Vol.25 (10), p.e70012-n/a |
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| creator | Zhang, Xingwang Hong, Hao Yan, Jiaoling Yuan, Yulong Feng, Mingfeng Liu, Qinhai Zhao, Yanxiao Yang, Tongqing Huang, Shen Wang, Chunli Zhao, Ruizhen Zuo, Wenyu Liu, Suyu Ding, Zixuan Huang, Changjun Zhang, Zhongkai Kundu, Jiban Kumar Tao, Xiaorong |
| description | Autophagy, an intracellular degradation process, has emerged as a crucial innate immune response against various plant pathogens, including viruses. Tomato spotted wilt orthotospovirus (TSWV) is a highly destructive plant pathogen that infects over 1000 plant species and poses a significant threat to global food security. However, the role of autophagy in defence against the TSWV pathogen, and whether the virus counteracts this defence, remains unknown. In this study, we report that autophagy plays an important role in antiviral defence against TSWV infection; however, this autophagy‐mediated defence is counteracted by the viral effector NSs. Transcriptome profiling revealed the up‐regulation of autophagy‐related genes (ATGs) upon TSWV infection. Blocking autophagy induction by chemical treatment or knockout/down of ATG5/ATG7 significantly enhanced TSWV accumulation. Notably, the TSWV nucleocapsid (N) protein, a major component of the viral replication unit, strongly induced autophagy. However, the TSWV nonstructural protein NSs was able to effectively suppress N‐induced autophagy in a dose‐dependent manner. Further investigation revealed that NSs inhibited ATG6‐mediated autophagy induction. These findings provide new insights into the defence role of autophagy against TSWV, a representative segmented negative‐strand RNA virus, as well as the tospoviral pathogen counterdefence mechanism.
Autophagy plays an important role in antiviral defence against tomato spotted wilt orthotospovirus (TSWV) infection. However, the TSWV NSs is able to effectively suppress N‐induced autophagy in a dose‐dependent manner. |
| doi_str_mv | 10.1111/mpp.70012 |
| format | Article |
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Autophagy plays an important role in antiviral defence against tomato spotted wilt orthotospovirus (TSWV) infection. However, the TSWV NSs is able to effectively suppress N‐induced autophagy in a dose‐dependent manner.</description><identifier>ISSN: 1464-6722</identifier><identifier>EISSN: 1364-3703</identifier><identifier>DOI: 10.1111/mpp.70012</identifier><identifier>PMID: 39350560</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>antiviral defence ; Autophagy ; Chemical treatment ; Cloning ; counterdefence ; Defense ; dose response ; Flowers & plants ; Food plants ; Food security ; Gene regulation ; Genes ; Glycoproteins ; Immune response ; Infections ; Innate immunity ; Nicotiana - genetics ; Nicotiana - immunology ; Nicotiana - virology ; nonstructural protein NSs ; nucleocapsid ; nucleocapsid protein ; Nucleocapsids ; Original ; Orthotospovirus ; Pathogens ; Plant Diseases - immunology ; Plant Diseases - virology ; plant pathogens ; plant pathology ; Plant species ; Plant viruses ; Proteins ; replicon ; RNA polymerase ; RNA viruses ; Solanum lycopersicum - genetics ; Solanum lycopersicum - immunology ; Solanum lycopersicum - virology ; species ; Tomatoes ; Tospovirus - pathogenicity ; Tospovirus - physiology ; transcriptome ; Transcriptomes ; TSWV ; viral nonstructural proteins ; Viral Nonstructural Proteins - genetics ; Viral Nonstructural Proteins - metabolism ; virus replication ; Viruses ; Wilt</subject><ispartof>Molecular plant pathology, 2024-10, Vol.25 (10), p.e70012-n/a</ispartof><rights>2024 The Author(s). published by British Society for Plant Pathology and John Wiley & Sons Ltd.</rights><rights>2024 The Author(s). Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.</rights><rights>2024. 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><cites>FETCH-LOGICAL-c3672-fc43c419ca24c1e8e97eb6d352aee8d9fbfed30f94231c6c66e4ddc82f7766973</cites><orcidid>0000-0003-3131-8743 ; 0000-0003-1259-366X</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/PMC11442783/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11442783/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1411,11541,27901,27902,45550,45551,46027,46451,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39350560$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Xingwang</creatorcontrib><creatorcontrib>Hong, Hao</creatorcontrib><creatorcontrib>Yan, Jiaoling</creatorcontrib><creatorcontrib>Yuan, Yulong</creatorcontrib><creatorcontrib>Feng, Mingfeng</creatorcontrib><creatorcontrib>Liu, Qinhai</creatorcontrib><creatorcontrib>Zhao, Yanxiao</creatorcontrib><creatorcontrib>Yang, Tongqing</creatorcontrib><creatorcontrib>Huang, Shen</creatorcontrib><creatorcontrib>Wang, Chunli</creatorcontrib><creatorcontrib>Zhao, Ruizhen</creatorcontrib><creatorcontrib>Zuo, Wenyu</creatorcontrib><creatorcontrib>Liu, Suyu</creatorcontrib><creatorcontrib>Ding, Zixuan</creatorcontrib><creatorcontrib>Huang, Changjun</creatorcontrib><creatorcontrib>Zhang, Zhongkai</creatorcontrib><creatorcontrib>Kundu, Jiban Kumar</creatorcontrib><creatorcontrib>Tao, Xiaorong</creatorcontrib><title>Autophagy plays an antiviral defence role against tomato spotted wilt orthotospovirus and is counteracted by viral effector NSs</title><title>Molecular plant pathology</title><addtitle>Mol Plant Pathol</addtitle><description>Autophagy, an intracellular degradation process, has emerged as a crucial innate immune response against various plant pathogens, including viruses. Tomato spotted wilt orthotospovirus (TSWV) is a highly destructive plant pathogen that infects over 1000 plant species and poses a significant threat to global food security. However, the role of autophagy in defence against the TSWV pathogen, and whether the virus counteracts this defence, remains unknown. In this study, we report that autophagy plays an important role in antiviral defence against TSWV infection; however, this autophagy‐mediated defence is counteracted by the viral effector NSs. Transcriptome profiling revealed the up‐regulation of autophagy‐related genes (ATGs) upon TSWV infection. Blocking autophagy induction by chemical treatment or knockout/down of ATG5/ATG7 significantly enhanced TSWV accumulation. Notably, the TSWV nucleocapsid (N) protein, a major component of the viral replication unit, strongly induced autophagy. However, the TSWV nonstructural protein NSs was able to effectively suppress N‐induced autophagy in a dose‐dependent manner. Further investigation revealed that NSs inhibited ATG6‐mediated autophagy induction. These findings provide new insights into the defence role of autophagy against TSWV, a representative segmented negative‐strand RNA virus, as well as the tospoviral pathogen counterdefence mechanism.
Autophagy plays an important role in antiviral defence against tomato spotted wilt orthotospovirus (TSWV) infection. However, the TSWV NSs is able to effectively suppress N‐induced autophagy in a dose‐dependent manner.</description><subject>antiviral defence</subject><subject>Autophagy</subject><subject>Chemical treatment</subject><subject>Cloning</subject><subject>counterdefence</subject><subject>Defense</subject><subject>dose response</subject><subject>Flowers & plants</subject><subject>Food plants</subject><subject>Food security</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Glycoproteins</subject><subject>Immune response</subject><subject>Infections</subject><subject>Innate immunity</subject><subject>Nicotiana - genetics</subject><subject>Nicotiana - immunology</subject><subject>Nicotiana - virology</subject><subject>nonstructural protein NSs</subject><subject>nucleocapsid</subject><subject>nucleocapsid protein</subject><subject>Nucleocapsids</subject><subject>Original</subject><subject>Orthotospovirus</subject><subject>Pathogens</subject><subject>Plant Diseases - immunology</subject><subject>Plant Diseases - virology</subject><subject>plant pathogens</subject><subject>plant pathology</subject><subject>Plant species</subject><subject>Plant viruses</subject><subject>Proteins</subject><subject>replicon</subject><subject>RNA polymerase</subject><subject>RNA viruses</subject><subject>Solanum lycopersicum - genetics</subject><subject>Solanum lycopersicum - immunology</subject><subject>Solanum lycopersicum - virology</subject><subject>species</subject><subject>Tomatoes</subject><subject>Tospovirus - pathogenicity</subject><subject>Tospovirus - physiology</subject><subject>transcriptome</subject><subject>Transcriptomes</subject><subject>TSWV</subject><subject>viral nonstructural proteins</subject><subject>Viral Nonstructural Proteins - genetics</subject><subject>Viral Nonstructural Proteins - metabolism</subject><subject>virus replication</subject><subject>Viruses</subject><subject>Wilt</subject><issn>1464-6722</issn><issn>1364-3703</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp1kU1rFTEUhoNYbHt14R-QgBu7uG2-JplZSSl-QasFdR1yk5N7p8xMxiRTmZV_3VynLSo0BHJInjyc5EXoJSWntIyzfhxPFSGUPUFHlEux5orwp6UWpZaKsUN0nNJNIVTDqmfokDe8IpUkR-jX-ZTDuDPbGY-dmRM2Q5m5vW2j6bADD4MFHEMH2GxNO6SMc-hNDjiNIWdw-GfbZRxi3oUcyl65OO0tDrcJ2zANGaKxe3Az48UK3oPNIeLPX9NzdOBNl-DF3bpC39-_-3bxcX355cOni_PLteXlAWtvBbeCNtYwYSnU0CjYSMcrZgBq1_iNB8eJbwTj1EorJQjnbM28UlI2iq_Q28U7TpsenIUhl1b0GNvexFkH0-p_T4Z2p7fhVlMqBFM1L4Y3d4YYfkyQsu7bZKHrzABhSprTitdCkfL1K_T6P_QmTHEo7ysUoxURXNSFOlkoG0NKEfxDN5Tofa665Kr_5FrYV3-3_0DeB1mAswUoccD8uElfXV8vyt_2d7B5</recordid><startdate>202410</startdate><enddate>202410</enddate><creator>Zhang, Xingwang</creator><creator>Hong, Hao</creator><creator>Yan, Jiaoling</creator><creator>Yuan, Yulong</creator><creator>Feng, Mingfeng</creator><creator>Liu, Qinhai</creator><creator>Zhao, Yanxiao</creator><creator>Yang, Tongqing</creator><creator>Huang, Shen</creator><creator>Wang, Chunli</creator><creator>Zhao, Ruizhen</creator><creator>Zuo, Wenyu</creator><creator>Liu, Suyu</creator><creator>Ding, Zixuan</creator><creator>Huang, Changjun</creator><creator>Zhang, Zhongkai</creator><creator>Kundu, Jiban Kumar</creator><creator>Tao, Xiaorong</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><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>3V.</scope><scope>7QL</scope><scope>7QO</scope><scope>7T7</scope><scope>7U9</scope><scope>7X2</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M0K</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-3131-8743</orcidid><orcidid>https://orcid.org/0000-0003-1259-366X</orcidid></search><sort><creationdate>202410</creationdate><title>Autophagy plays an antiviral defence role against tomato spotted wilt orthotospovirus and is counteracted by viral effector NSs</title><author>Zhang, Xingwang ; Hong, Hao ; Yan, Jiaoling ; Yuan, Yulong ; Feng, Mingfeng ; Liu, Qinhai ; Zhao, Yanxiao ; Yang, Tongqing ; Huang, Shen ; Wang, Chunli ; Zhao, Ruizhen ; Zuo, Wenyu ; Liu, Suyu ; Ding, Zixuan ; Huang, Changjun ; Zhang, Zhongkai ; Kundu, Jiban Kumar ; Tao, Xiaorong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3672-fc43c419ca24c1e8e97eb6d352aee8d9fbfed30f94231c6c66e4ddc82f7766973</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>antiviral defence</topic><topic>Autophagy</topic><topic>Chemical treatment</topic><topic>Cloning</topic><topic>counterdefence</topic><topic>Defense</topic><topic>dose response</topic><topic>Flowers & plants</topic><topic>Food plants</topic><topic>Food security</topic><topic>Gene regulation</topic><topic>Genes</topic><topic>Glycoproteins</topic><topic>Immune response</topic><topic>Infections</topic><topic>Innate immunity</topic><topic>Nicotiana - genetics</topic><topic>Nicotiana - immunology</topic><topic>Nicotiana - virology</topic><topic>nonstructural protein NSs</topic><topic>nucleocapsid</topic><topic>nucleocapsid protein</topic><topic>Nucleocapsids</topic><topic>Original</topic><topic>Orthotospovirus</topic><topic>Pathogens</topic><topic>Plant Diseases - immunology</topic><topic>Plant Diseases - virology</topic><topic>plant pathogens</topic><topic>plant pathology</topic><topic>Plant species</topic><topic>Plant viruses</topic><topic>Proteins</topic><topic>replicon</topic><topic>RNA polymerase</topic><topic>RNA viruses</topic><topic>Solanum lycopersicum - genetics</topic><topic>Solanum lycopersicum - immunology</topic><topic>Solanum lycopersicum - virology</topic><topic>species</topic><topic>Tomatoes</topic><topic>Tospovirus - pathogenicity</topic><topic>Tospovirus - physiology</topic><topic>transcriptome</topic><topic>Transcriptomes</topic><topic>TSWV</topic><topic>viral nonstructural proteins</topic><topic>Viral Nonstructural Proteins - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular plant pathology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Xingwang</au><au>Hong, Hao</au><au>Yan, Jiaoling</au><au>Yuan, Yulong</au><au>Feng, Mingfeng</au><au>Liu, Qinhai</au><au>Zhao, Yanxiao</au><au>Yang, Tongqing</au><au>Huang, Shen</au><au>Wang, Chunli</au><au>Zhao, Ruizhen</au><au>Zuo, Wenyu</au><au>Liu, Suyu</au><au>Ding, Zixuan</au><au>Huang, Changjun</au><au>Zhang, Zhongkai</au><au>Kundu, Jiban Kumar</au><au>Tao, Xiaorong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Autophagy plays an antiviral defence role against tomato spotted wilt orthotospovirus and is counteracted by viral effector NSs</atitle><jtitle>Molecular plant pathology</jtitle><addtitle>Mol Plant Pathol</addtitle><date>2024-10</date><risdate>2024</risdate><volume>25</volume><issue>10</issue><spage>e70012</spage><epage>n/a</epage><pages>e70012-n/a</pages><issn>1464-6722</issn><eissn>1364-3703</eissn><abstract>Autophagy, an intracellular degradation process, has emerged as a crucial innate immune response against various plant pathogens, including viruses. Tomato spotted wilt orthotospovirus (TSWV) is a highly destructive plant pathogen that infects over 1000 plant species and poses a significant threat to global food security. However, the role of autophagy in defence against the TSWV pathogen, and whether the virus counteracts this defence, remains unknown. In this study, we report that autophagy plays an important role in antiviral defence against TSWV infection; however, this autophagy‐mediated defence is counteracted by the viral effector NSs. Transcriptome profiling revealed the up‐regulation of autophagy‐related genes (ATGs) upon TSWV infection. Blocking autophagy induction by chemical treatment or knockout/down of ATG5/ATG7 significantly enhanced TSWV accumulation. Notably, the TSWV nucleocapsid (N) protein, a major component of the viral replication unit, strongly induced autophagy. However, the TSWV nonstructural protein NSs was able to effectively suppress N‐induced autophagy in a dose‐dependent manner. Further investigation revealed that NSs inhibited ATG6‐mediated autophagy induction. These findings provide new insights into the defence role of autophagy against TSWV, a representative segmented negative‐strand RNA virus, as well as the tospoviral pathogen counterdefence mechanism.
Autophagy plays an important role in antiviral defence against tomato spotted wilt orthotospovirus (TSWV) infection. However, the TSWV NSs is able to effectively suppress N‐induced autophagy in a dose‐dependent manner.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>39350560</pmid><doi>10.1111/mpp.70012</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-3131-8743</orcidid><orcidid>https://orcid.org/0000-0003-1259-366X</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1464-6722 |
| ispartof | Molecular plant pathology, 2024-10, Vol.25 (10), p.e70012-n/a |
| issn | 1464-6722 1364-3703 |
| language | eng |
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| source | MEDLINE; Wiley Online Library Open Access; DOAJ Directory of Open Access Journals; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | antiviral defence Autophagy Chemical treatment Cloning counterdefence Defense dose response Flowers & plants Food plants Food security Gene regulation Genes Glycoproteins Immune response Infections Innate immunity Nicotiana - genetics Nicotiana - immunology Nicotiana - virology nonstructural protein NSs nucleocapsid nucleocapsid protein Nucleocapsids Original Orthotospovirus Pathogens Plant Diseases - immunology Plant Diseases - virology plant pathogens plant pathology Plant species Plant viruses Proteins replicon RNA polymerase RNA viruses Solanum lycopersicum - genetics Solanum lycopersicum - immunology Solanum lycopersicum - virology species Tomatoes Tospovirus - pathogenicity Tospovirus - physiology transcriptome Transcriptomes TSWV viral nonstructural proteins Viral Nonstructural Proteins - genetics Viral Nonstructural Proteins - metabolism virus replication Viruses Wilt |
| title | Autophagy plays an antiviral defence role against tomato spotted wilt orthotospovirus and is counteracted by viral effector NSs |
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