Barley stripe mosaic virus γb Protein Subverts Autophagy to Promote Viral Infection by Disrupting the ATG7-ATG8 Interaction
Autophagy is a conserved defense strategy against viral infection. However, little is known about the counterdefense strategies of plant viruses involving interference with autophagy. Here, we show that γb protein from Barley stripe mosaic virus (BSMV), a positive single-stranded RNA virus, directly...
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Veröffentlicht in: | The Plant cell 2018-07, Vol.30 (7), p.1582-1595 |
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description | Autophagy is a conserved defense strategy against viral infection. However, little is known about the counterdefense strategies of plant viruses involving interference with autophagy. Here, we show that γb protein from Barley stripe mosaic virus (BSMV), a positive single-stranded RNA virus, directly interacts with AUTOPHAGY PROTEIN7 (ATG7). BSMV infection suppresses autophagy, and overexpression of γb protein is sufficient to inhibit autophagy. Furthermore, silencing of autophagy-related gene ATG5 and ATG7 in Nicotiana benthamiana plants enhanced BSMV accumulation and viral symptoms, indicating that autophagy plays an antiviral role in BSMV infection. Molecular analyses indicated that γb interferes with the interaction of ATG7 with ATG8 in a competitive manner, whereas a single point mutation in γb, Tyr29Ala (Y29A), made this protein deficient in the interaction with ATG7, which was correlated with the abolishment of autophagy inhibition. Consistently, the mutant BSMVY29A virus showed reduced symptom severity and viral accumulation. Taken together, our findings reveal that BSMV γb protein subverts autophagy-mediated antiviral defense by disrupting the ATG7-ATG8 interaction to promote plant RNA virus infection, and they provide evidence that ATG7 is a target of pathogen effectors that functions in the ongoing arms race of plant defense and viral counterdefense. |
doi_str_mv | 10.1105/tpc.18.00122 |
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However, little is known about the counterdefense strategies of plant viruses involving interference with autophagy. Here, we show that γb protein from Barley stripe mosaic virus (BSMV), a positive single-stranded RNA virus, directly interacts with AUTOPHAGY PROTEIN7 (ATG7). BSMV infection suppresses autophagy, and overexpression of γb protein is sufficient to inhibit autophagy. Furthermore, silencing of autophagy-related gene ATG5 and ATG7 in Nicotiana benthamiana plants enhanced BSMV accumulation and viral symptoms, indicating that autophagy plays an antiviral role in BSMV infection. Molecular analyses indicated that γb interferes with the interaction of ATG7 with ATG8 in a competitive manner, whereas a single point mutation in γb, Tyr29Ala (Y29A), made this protein deficient in the interaction with ATG7, which was correlated with the abolishment of autophagy inhibition. Consistently, the mutant BSMVY29A virus showed reduced symptom severity and viral accumulation. Taken together, our findings reveal that BSMV γb protein subverts autophagy-mediated antiviral defense by disrupting the ATG7-ATG8 interaction to promote plant RNA virus infection, and they provide evidence that ATG7 is a target of pathogen effectors that functions in the ongoing arms race of plant defense and viral counterdefense.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.18.00122</identifier><identifier>PMID: 29848767</identifier><language>eng</language><publisher>England: American Society of Plant Biologists</publisher><subject>Accumulation ; Antiviral activity ; Autophagy ; Barley ; Disruption ; Effectors ; Infections ; Nicotiana - metabolism ; Nicotiana - virology ; Pathogens ; Phagocytosis ; Plant Proteins - metabolism ; Plant virus diseases ; Plant viruses ; Plant Viruses - genetics ; Plant Viruses - metabolism ; Plant Viruses - pathogenicity ; Point mutation ; Protein Binding ; Proteins ; Ribonucleic acid ; RNA ; RNA viruses ; RNA, Viral - genetics ; Viral infections ; Viruses</subject><ispartof>The Plant cell, 2018-07, Vol.30 (7), p.1582-1595</ispartof><rights>American Society of Plant Biologists</rights><rights>2018 American Society of Plant Biologists. All rights reserved.</rights><rights>Copyright American Society of Plant Biologists Jul 2018</rights><rights>2018 American Society of Plant Biologists. All rights reserved. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c434t-b1374ab375dede8ffadb2cb37d732d67989329c443cc4ba0699118c81ba261a03</citedby><orcidid>0000-0002-4423-6045 ; 0000-0003-2003-9466 ; 0000-0003-3082-2462 ; 0000-0002-1032-6800 ; 0000-0003-1603-5526 ; 0000-0003-4133-1263 ; 0000-0001-7561-5008 ; 0000-0002-6790-1044 ; 0000-0003-0684-5584 ; 0000-0002-1584-7170</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/90024058$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/90024058$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,27901,27902,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29848767$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Meng</creatorcontrib><creatorcontrib>Zhang, Yongliang</creatorcontrib><creatorcontrib>Xie, Xialin</creatorcontrib><creatorcontrib>Yue, Ning</creatorcontrib><creatorcontrib>Li, Jinlin</creatorcontrib><creatorcontrib>Wang, Xian-Bing</creatorcontrib><creatorcontrib>Han, Chenggui</creatorcontrib><creatorcontrib>Yu, Jialin</creatorcontrib><creatorcontrib>Liu, Yule</creatorcontrib><creatorcontrib>Li, Dawei</creatorcontrib><title>Barley stripe mosaic virus γb Protein Subverts Autophagy to Promote Viral Infection by Disrupting the ATG7-ATG8 Interaction</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>Autophagy is a conserved defense strategy against viral infection. However, little is known about the counterdefense strategies of plant viruses involving interference with autophagy. Here, we show that γb protein from Barley stripe mosaic virus (BSMV), a positive single-stranded RNA virus, directly interacts with AUTOPHAGY PROTEIN7 (ATG7). BSMV infection suppresses autophagy, and overexpression of γb protein is sufficient to inhibit autophagy. Furthermore, silencing of autophagy-related gene ATG5 and ATG7 in Nicotiana benthamiana plants enhanced BSMV accumulation and viral symptoms, indicating that autophagy plays an antiviral role in BSMV infection. Molecular analyses indicated that γb interferes with the interaction of ATG7 with ATG8 in a competitive manner, whereas a single point mutation in γb, Tyr29Ala (Y29A), made this protein deficient in the interaction with ATG7, which was correlated with the abolishment of autophagy inhibition. Consistently, the mutant BSMVY29A virus showed reduced symptom severity and viral accumulation. Taken together, our findings reveal that BSMV γb protein subverts autophagy-mediated antiviral defense by disrupting the ATG7-ATG8 interaction to promote plant RNA virus infection, and they provide evidence that ATG7 is a target of pathogen effectors that functions in the ongoing arms race of plant defense and viral counterdefense.</description><subject>Accumulation</subject><subject>Antiviral activity</subject><subject>Autophagy</subject><subject>Barley</subject><subject>Disruption</subject><subject>Effectors</subject><subject>Infections</subject><subject>Nicotiana - metabolism</subject><subject>Nicotiana - virology</subject><subject>Pathogens</subject><subject>Phagocytosis</subject><subject>Plant Proteins - metabolism</subject><subject>Plant virus diseases</subject><subject>Plant viruses</subject><subject>Plant Viruses - genetics</subject><subject>Plant Viruses - metabolism</subject><subject>Plant Viruses - pathogenicity</subject><subject>Point mutation</subject><subject>Protein Binding</subject><subject>Proteins</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA viruses</subject><subject>RNA, Viral - genetics</subject><subject>Viral infections</subject><subject>Viruses</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkcuKFDEUhgtRnIvu3CoBNy6sNrfKZTPQjjoODCg4iruQpFLdaaoqZZJqaJi38j18JjPTY6NucuH7-DmHv6qeIbhACDZv8mQXSCwgRBg_qI5RQ3CNpfj-sLwhhTVlDTqqTlLawOJwJB9XR4VTwRk_rm7e6ti7HUg5-smBISTtLdj6OCfw66cBn2PIzo_gy2y2LuYElnMO01qvdiCHWzoUDr75qHtwOXbOZh9GYHbgnU9xnrIfVyCvHVheX_C6HKJY2UV95z2pHnW6T-7p_X1aff3w_vr8Y3316eLyfHlVW0porg0inGpDeNO61omu063BtvxbTnDLuBSSYGkpJdZSoyGTEiFhBTIaM6QhOa3O9rnTbAbXWjfmMq-aoh903KmgvfqXjH6tVmGrGJSMQVwCXt0HxPBjdimrwSfr-l6PLsxJYUi5xLhBtKgv_1M3YY5jWa9YghEhKUfFer23bAwpRdcdhkFQ3daqSq0KCXVXa9Ff_L3AQf7TYxGe74VNyiEeuIQQU9gI8hsr-qng</recordid><startdate>20180701</startdate><enddate>20180701</enddate><creator>Yang, Meng</creator><creator>Zhang, Yongliang</creator><creator>Xie, Xialin</creator><creator>Yue, Ning</creator><creator>Li, Jinlin</creator><creator>Wang, Xian-Bing</creator><creator>Han, Chenggui</creator><creator>Yu, Jialin</creator><creator>Liu, Yule</creator><creator>Li, Dawei</creator><general>American Society of Plant Biologists</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>4T-</scope><scope>7QO</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4423-6045</orcidid><orcidid>https://orcid.org/0000-0003-2003-9466</orcidid><orcidid>https://orcid.org/0000-0003-3082-2462</orcidid><orcidid>https://orcid.org/0000-0002-1032-6800</orcidid><orcidid>https://orcid.org/0000-0003-1603-5526</orcidid><orcidid>https://orcid.org/0000-0003-4133-1263</orcidid><orcidid>https://orcid.org/0000-0001-7561-5008</orcidid><orcidid>https://orcid.org/0000-0002-6790-1044</orcidid><orcidid>https://orcid.org/0000-0003-0684-5584</orcidid><orcidid>https://orcid.org/0000-0002-1584-7170</orcidid></search><sort><creationdate>20180701</creationdate><title>Barley stripe mosaic virus γb Protein Subverts Autophagy to Promote Viral Infection by Disrupting the ATG7-ATG8 Interaction</title><author>Yang, Meng ; Zhang, Yongliang ; Xie, Xialin ; Yue, Ning ; Li, Jinlin ; Wang, Xian-Bing ; Han, Chenggui ; Yu, Jialin ; Liu, Yule ; Li, Dawei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c434t-b1374ab375dede8ffadb2cb37d732d67989329c443cc4ba0699118c81ba261a03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Accumulation</topic><topic>Antiviral activity</topic><topic>Autophagy</topic><topic>Barley</topic><topic>Disruption</topic><topic>Effectors</topic><topic>Infections</topic><topic>Nicotiana - metabolism</topic><topic>Nicotiana - virology</topic><topic>Pathogens</topic><topic>Phagocytosis</topic><topic>Plant Proteins - metabolism</topic><topic>Plant virus diseases</topic><topic>Plant viruses</topic><topic>Plant Viruses - genetics</topic><topic>Plant Viruses - metabolism</topic><topic>Plant Viruses - pathogenicity</topic><topic>Point mutation</topic><topic>Protein Binding</topic><topic>Proteins</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA viruses</topic><topic>RNA, Viral - genetics</topic><topic>Viral infections</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Meng</creatorcontrib><creatorcontrib>Zhang, Yongliang</creatorcontrib><creatorcontrib>Xie, Xialin</creatorcontrib><creatorcontrib>Yue, Ning</creatorcontrib><creatorcontrib>Li, Jinlin</creatorcontrib><creatorcontrib>Wang, Xian-Bing</creatorcontrib><creatorcontrib>Han, Chenggui</creatorcontrib><creatorcontrib>Yu, Jialin</creatorcontrib><creatorcontrib>Liu, Yule</creatorcontrib><creatorcontrib>Li, Dawei</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Docstoc</collection><collection>Biotechnology Research Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Plant cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Meng</au><au>Zhang, Yongliang</au><au>Xie, Xialin</au><au>Yue, Ning</au><au>Li, Jinlin</au><au>Wang, Xian-Bing</au><au>Han, Chenggui</au><au>Yu, Jialin</au><au>Liu, Yule</au><au>Li, Dawei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Barley stripe mosaic virus γb Protein Subverts Autophagy to Promote Viral Infection by Disrupting the ATG7-ATG8 Interaction</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2018-07-01</date><risdate>2018</risdate><volume>30</volume><issue>7</issue><spage>1582</spage><epage>1595</epage><pages>1582-1595</pages><issn>1040-4651</issn><eissn>1532-298X</eissn><abstract>Autophagy is a conserved defense strategy against viral infection. However, little is known about the counterdefense strategies of plant viruses involving interference with autophagy. Here, we show that γb protein from Barley stripe mosaic virus (BSMV), a positive single-stranded RNA virus, directly interacts with AUTOPHAGY PROTEIN7 (ATG7). BSMV infection suppresses autophagy, and overexpression of γb protein is sufficient to inhibit autophagy. Furthermore, silencing of autophagy-related gene ATG5 and ATG7 in Nicotiana benthamiana plants enhanced BSMV accumulation and viral symptoms, indicating that autophagy plays an antiviral role in BSMV infection. Molecular analyses indicated that γb interferes with the interaction of ATG7 with ATG8 in a competitive manner, whereas a single point mutation in γb, Tyr29Ala (Y29A), made this protein deficient in the interaction with ATG7, which was correlated with the abolishment of autophagy inhibition. Consistently, the mutant BSMVY29A virus showed reduced symptom severity and viral accumulation. Taken together, our findings reveal that BSMV γb protein subverts autophagy-mediated antiviral defense by disrupting the ATG7-ATG8 interaction to promote plant RNA virus infection, and they provide evidence that ATG7 is a target of pathogen effectors that functions in the ongoing arms race of plant defense and viral counterdefense.</abstract><cop>England</cop><pub>American Society of Plant Biologists</pub><pmid>29848767</pmid><doi>10.1105/tpc.18.00122</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-4423-6045</orcidid><orcidid>https://orcid.org/0000-0003-2003-9466</orcidid><orcidid>https://orcid.org/0000-0003-3082-2462</orcidid><orcidid>https://orcid.org/0000-0002-1032-6800</orcidid><orcidid>https://orcid.org/0000-0003-1603-5526</orcidid><orcidid>https://orcid.org/0000-0003-4133-1263</orcidid><orcidid>https://orcid.org/0000-0001-7561-5008</orcidid><orcidid>https://orcid.org/0000-0002-6790-1044</orcidid><orcidid>https://orcid.org/0000-0003-0684-5584</orcidid><orcidid>https://orcid.org/0000-0002-1584-7170</orcidid><oa>free_for_read</oa></addata></record> |
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source | Jstor Complete Legacy; Oxford University Press Journals All Titles (1996-Current); MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
subjects | Accumulation Antiviral activity Autophagy Barley Disruption Effectors Infections Nicotiana - metabolism Nicotiana - virology Pathogens Phagocytosis Plant Proteins - metabolism Plant virus diseases Plant viruses Plant Viruses - genetics Plant Viruses - metabolism Plant Viruses - pathogenicity Point mutation Protein Binding Proteins Ribonucleic acid RNA RNA viruses RNA, Viral - genetics Viral infections Viruses |
title | Barley stripe mosaic virus γb Protein Subverts Autophagy to Promote Viral Infection by Disrupting the ATG7-ATG8 Interaction |
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