The P2 protein of wheat yellow mosaic virus acts as a viral suppressor of RNA silencing in Nicotiana benthamiana to facilitate virus infection
Wheat yellow mosaic virus (WYMV) causes severe viral wheat disease in Asia. The WYMV P1 protein encoded by RNA2 has viral suppressor of RNA silencing (VSR) activity to facilitate virus infection, however, VSR activity has not been identified for P2 protein encoded by RNA2. In this study, P2 protein...
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| creator | Chen, Dao Zhang, Hui‐Ying Hu, Shu‐Ming He, Zheng Wu, Yong Qi Zhang, Zong‐Ying Wang, Ying Han, Cheng‐Gui |
| description | Wheat yellow mosaic virus (WYMV) causes severe viral wheat disease in Asia. The WYMV P1 protein encoded by RNA2 has viral suppressor of RNA silencing (VSR) activity to facilitate virus infection, however, VSR activity has not been identified for P2 protein encoded by RNA2. In this study, P2 protein exhibited strong VSR activity in Nicotiana benthamiana at the four‐leaf stage, and point mutants P70A and G230A lost VSR activity. Protein P2 interacted with calmodulin (CaM) protein, a gene‐silencing associated protein, while point mutants P70A and G230A did not interact with it. Competitive bimolecular fluorescence complementation and competitive co‐immunoprecipitation experiments showed that P2 interfered with the interaction between CaM and calmodulin‐binding transcription activator 3 (CAMTA3), but the point mutants P70A and G230A could not. Mechanical inoculation of wheat with in vitro transcripts of WYMV infectious cDNA clone further confirmed that VSR‐deficient mutants P70A and G230A decreased WYMV infection in wheat plants compared with the wild type. In addition, RNA silencing, temperature, ubiquitination and autophagy had significant effects on accumulation of P2 protein in N. benthamiana leaves. In conclusion, WYMV P2 plays a VSR role in N. benthamiana and promotes virus infection by interfering with calmodulin‐related antiviral RNAi defense.
Summary statement
Wheat yellow mosaic virus P2 protein exerts VSR activity in Nicotiana benthamiana by interfering with the CaM–CAMTA3 interaction to facilitate virus efficient systemic infection. |
| doi_str_mv | 10.1111/pce.15041 |
| format | Article |
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Summary statement
Wheat yellow mosaic virus P2 protein exerts VSR activity in Nicotiana benthamiana by interfering with the CaM–CAMTA3 interaction to facilitate virus efficient systemic infection.</description><identifier>ISSN: 0140-7791</identifier><identifier>ISSN: 1365-3040</identifier><identifier>EISSN: 1365-3040</identifier><identifier>DOI: 10.1111/pce.15041</identifier><identifier>PMID: 39016637</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Asia ; Autophagy ; Calmodulin ; Calmodulin - genetics ; Calmodulin - metabolism ; CaM ; CAMTA3 ; Complementation ; Deficient mutant ; environment ; fluorescence ; gene silencing ; Immunoprecipitation ; in vitro transcript inoculation ; Infections ; Inoculation ; Leaves ; Nicotiana - genetics ; Nicotiana - virology ; Nicotiana benthamiana ; p1 Protein ; Plant Diseases - genetics ; Plant Diseases - virology ; Plant Leaves - genetics ; Plant Leaves - metabolism ; Plant Leaves - virology ; Plant viruses ; Potyviridae - physiology ; precipitin tests ; Proteins ; Ribonucleic acid ; RNA ; RNA Interference ; RNA viruses ; RNA-mediated interference ; temperature ; Triticum - genetics ; Triticum - metabolism ; Triticum - virology ; Ubiquitination ; Viral Proteins - genetics ; Viral Proteins - metabolism ; Viruses ; VSR ; Wheat ; Wheat yellow mosaic virus ; WYMV</subject><ispartof>Plant, cell and environment, 2024-12, Vol.47 (12), p.4543-4556</ispartof><rights>2024 The Author(s). published by John Wiley & Sons Ltd.</rights><rights>2024 The Author(s). Plant, Cell & Environment published by John Wiley & Sons Ltd.</rights><rights>2024. This article is published under http://creativecommons.org/licenses/by-nc/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-c2761-7ef2725cbab8f82c8b91cd721e1132dfbeaa58281980d439e001ae56571ac1fd3</cites><orcidid>0000-0002-1584-7170</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fpce.15041$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fpce.15041$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39016637$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Dao</creatorcontrib><creatorcontrib>Zhang, Hui‐Ying</creatorcontrib><creatorcontrib>Hu, Shu‐Ming</creatorcontrib><creatorcontrib>He, Zheng</creatorcontrib><creatorcontrib>Wu, Yong Qi</creatorcontrib><creatorcontrib>Zhang, Zong‐Ying</creatorcontrib><creatorcontrib>Wang, Ying</creatorcontrib><creatorcontrib>Han, Cheng‐Gui</creatorcontrib><title>The P2 protein of wheat yellow mosaic virus acts as a viral suppressor of RNA silencing in Nicotiana benthamiana to facilitate virus infection</title><title>Plant, cell and environment</title><addtitle>Plant Cell Environ</addtitle><description>Wheat yellow mosaic virus (WYMV) causes severe viral wheat disease in Asia. The WYMV P1 protein encoded by RNA2 has viral suppressor of RNA silencing (VSR) activity to facilitate virus infection, however, VSR activity has not been identified for P2 protein encoded by RNA2. In this study, P2 protein exhibited strong VSR activity in Nicotiana benthamiana at the four‐leaf stage, and point mutants P70A and G230A lost VSR activity. Protein P2 interacted with calmodulin (CaM) protein, a gene‐silencing associated protein, while point mutants P70A and G230A did not interact with it. Competitive bimolecular fluorescence complementation and competitive co‐immunoprecipitation experiments showed that P2 interfered with the interaction between CaM and calmodulin‐binding transcription activator 3 (CAMTA3), but the point mutants P70A and G230A could not. Mechanical inoculation of wheat with in vitro transcripts of WYMV infectious cDNA clone further confirmed that VSR‐deficient mutants P70A and G230A decreased WYMV infection in wheat plants compared with the wild type. In addition, RNA silencing, temperature, ubiquitination and autophagy had significant effects on accumulation of P2 protein in N. benthamiana leaves. In conclusion, WYMV P2 plays a VSR role in N. benthamiana and promotes virus infection by interfering with calmodulin‐related antiviral RNAi defense.
Summary statement
Wheat yellow mosaic virus P2 protein exerts VSR activity in Nicotiana benthamiana by interfering with the CaM–CAMTA3 interaction to facilitate virus efficient systemic infection.</description><subject>Asia</subject><subject>Autophagy</subject><subject>Calmodulin</subject><subject>Calmodulin - genetics</subject><subject>Calmodulin - metabolism</subject><subject>CaM</subject><subject>CAMTA3</subject><subject>Complementation</subject><subject>Deficient mutant</subject><subject>environment</subject><subject>fluorescence</subject><subject>gene silencing</subject><subject>Immunoprecipitation</subject><subject>in vitro transcript inoculation</subject><subject>Infections</subject><subject>Inoculation</subject><subject>Leaves</subject><subject>Nicotiana - genetics</subject><subject>Nicotiana - virology</subject><subject>Nicotiana benthamiana</subject><subject>p1 Protein</subject><subject>Plant Diseases - genetics</subject><subject>Plant Diseases - virology</subject><subject>Plant Leaves - genetics</subject><subject>Plant Leaves - metabolism</subject><subject>Plant Leaves - virology</subject><subject>Plant viruses</subject><subject>Potyviridae - physiology</subject><subject>precipitin tests</subject><subject>Proteins</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA Interference</subject><subject>RNA viruses</subject><subject>RNA-mediated interference</subject><subject>temperature</subject><subject>Triticum - genetics</subject><subject>Triticum - metabolism</subject><subject>Triticum - virology</subject><subject>Ubiquitination</subject><subject>Viral Proteins - genetics</subject><subject>Viral Proteins - metabolism</subject><subject>Viruses</subject><subject>VSR</subject><subject>Wheat</subject><subject>Wheat yellow mosaic virus</subject><subject>WYMV</subject><issn>0140-7791</issn><issn>1365-3040</issn><issn>1365-3040</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNqFkVFr1TAYhoMo7ji98A9IwBt30S1f0jbp5TjMKYw5ZF6XNP3iyWiT2qQ7nD_hbzZn5-iFIIaQpOXJA29eQt4CO4c8LiaD51CxEp6RFYi6KgQr2XOyYlCyQsoGTsirGB8Yyz9k85KciIZBXQu5Ij_vN0jvOJ3mkNB5GizdblAnusNhCFs6hqidoY9uXiLVJuUlz_23HmhcpmnGGMO8v_f19pJGN6A3zn-n2XXrTEhOe0079Gmjx6dzCtRq4waXdMKj2HmLJrngX5MXVg8R3xz3U_Lt49X9-lNx8-X68_rypjBc1lBItFzyynS6U1Zxo7oGTC85IIDgve1Q60pxBY1ifSkazMk1VnUlQRuwvTglHw7enPvHgjG1o4smR9YewxJbAVUJStRl_X-UKZCKKVVl9P1f6ENYZp-DZCEXTS1KvheeHSgzhxhntO00u1HPuxZYu--zzX22T31m9t3RuHQj9n_I3wVm4OIAbPPL7_5tau_WVwflL94UqfA</recordid><startdate>202412</startdate><enddate>202412</enddate><creator>Chen, Dao</creator><creator>Zhang, Hui‐Ying</creator><creator>Hu, Shu‐Ming</creator><creator>He, Zheng</creator><creator>Wu, Yong Qi</creator><creator>Zhang, Zong‐Ying</creator><creator>Wang, Ying</creator><creator>Han, Cheng‐Gui</creator><general>Wiley Subscription Services, 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>7QP</scope><scope>7ST</scope><scope>C1K</scope><scope>SOI</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-1584-7170</orcidid></search><sort><creationdate>202412</creationdate><title>The P2 protein of wheat yellow mosaic virus acts as a viral suppressor of RNA silencing in Nicotiana benthamiana to facilitate virus infection</title><author>Chen, Dao ; Zhang, Hui‐Ying ; Hu, Shu‐Ming ; He, Zheng ; Wu, Yong Qi ; Zhang, Zong‐Ying ; Wang, Ying ; Han, Cheng‐Gui</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c2761-7ef2725cbab8f82c8b91cd721e1132dfbeaa58281980d439e001ae56571ac1fd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Asia</topic><topic>Autophagy</topic><topic>Calmodulin</topic><topic>Calmodulin - genetics</topic><topic>Calmodulin - metabolism</topic><topic>CaM</topic><topic>CAMTA3</topic><topic>Complementation</topic><topic>Deficient mutant</topic><topic>environment</topic><topic>fluorescence</topic><topic>gene silencing</topic><topic>Immunoprecipitation</topic><topic>in vitro transcript inoculation</topic><topic>Infections</topic><topic>Inoculation</topic><topic>Leaves</topic><topic>Nicotiana - genetics</topic><topic>Nicotiana - virology</topic><topic>Nicotiana benthamiana</topic><topic>p1 Protein</topic><topic>Plant Diseases - genetics</topic><topic>Plant Diseases - virology</topic><topic>Plant Leaves - genetics</topic><topic>Plant Leaves - metabolism</topic><topic>Plant Leaves - virology</topic><topic>Plant viruses</topic><topic>Potyviridae - physiology</topic><topic>precipitin tests</topic><topic>Proteins</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA Interference</topic><topic>RNA viruses</topic><topic>RNA-mediated interference</topic><topic>temperature</topic><topic>Triticum - genetics</topic><topic>Triticum - metabolism</topic><topic>Triticum - virology</topic><topic>Ubiquitination</topic><topic>Viral Proteins - genetics</topic><topic>Viral Proteins - metabolism</topic><topic>Viruses</topic><topic>VSR</topic><topic>Wheat</topic><topic>Wheat yellow mosaic virus</topic><topic>WYMV</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Dao</creatorcontrib><creatorcontrib>Zhang, Hui‐Ying</creatorcontrib><creatorcontrib>Hu, Shu‐Ming</creatorcontrib><creatorcontrib>He, Zheng</creatorcontrib><creatorcontrib>Wu, Yong Qi</creatorcontrib><creatorcontrib>Zhang, Zong‐Ying</creatorcontrib><creatorcontrib>Wang, Ying</creatorcontrib><creatorcontrib>Han, Cheng‐Gui</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Environment Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Plant, cell and environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Dao</au><au>Zhang, Hui‐Ying</au><au>Hu, Shu‐Ming</au><au>He, Zheng</au><au>Wu, Yong Qi</au><au>Zhang, Zong‐Ying</au><au>Wang, Ying</au><au>Han, Cheng‐Gui</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The P2 protein of wheat yellow mosaic virus acts as a viral suppressor of RNA silencing in Nicotiana benthamiana to facilitate virus infection</atitle><jtitle>Plant, cell and environment</jtitle><addtitle>Plant Cell Environ</addtitle><date>2024-12</date><risdate>2024</risdate><volume>47</volume><issue>12</issue><spage>4543</spage><epage>4556</epage><pages>4543-4556</pages><issn>0140-7791</issn><issn>1365-3040</issn><eissn>1365-3040</eissn><abstract>Wheat yellow mosaic virus (WYMV) causes severe viral wheat disease in Asia. The WYMV P1 protein encoded by RNA2 has viral suppressor of RNA silencing (VSR) activity to facilitate virus infection, however, VSR activity has not been identified for P2 protein encoded by RNA2. In this study, P2 protein exhibited strong VSR activity in Nicotiana benthamiana at the four‐leaf stage, and point mutants P70A and G230A lost VSR activity. Protein P2 interacted with calmodulin (CaM) protein, a gene‐silencing associated protein, while point mutants P70A and G230A did not interact with it. Competitive bimolecular fluorescence complementation and competitive co‐immunoprecipitation experiments showed that P2 interfered with the interaction between CaM and calmodulin‐binding transcription activator 3 (CAMTA3), but the point mutants P70A and G230A could not. Mechanical inoculation of wheat with in vitro transcripts of WYMV infectious cDNA clone further confirmed that VSR‐deficient mutants P70A and G230A decreased WYMV infection in wheat plants compared with the wild type. In addition, RNA silencing, temperature, ubiquitination and autophagy had significant effects on accumulation of P2 protein in N. benthamiana leaves. In conclusion, WYMV P2 plays a VSR role in N. benthamiana and promotes virus infection by interfering with calmodulin‐related antiviral RNAi defense.
Summary statement
Wheat yellow mosaic virus P2 protein exerts VSR activity in Nicotiana benthamiana by interfering with the CaM–CAMTA3 interaction to facilitate virus efficient systemic infection.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>39016637</pmid><doi>10.1111/pce.15041</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-1584-7170</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Asia Autophagy Calmodulin Calmodulin - genetics Calmodulin - metabolism CaM CAMTA3 Complementation Deficient mutant environment fluorescence gene silencing Immunoprecipitation in vitro transcript inoculation Infections Inoculation Leaves Nicotiana - genetics Nicotiana - virology Nicotiana benthamiana p1 Protein Plant Diseases - genetics Plant Diseases - virology Plant Leaves - genetics Plant Leaves - metabolism Plant Leaves - virology Plant viruses Potyviridae - physiology precipitin tests Proteins Ribonucleic acid RNA RNA Interference RNA viruses RNA-mediated interference temperature Triticum - genetics Triticum - metabolism Triticum - virology Ubiquitination Viral Proteins - genetics Viral Proteins - metabolism Viruses VSR Wheat Wheat yellow mosaic virus WYMV |
| title | The P2 protein of wheat yellow mosaic virus acts as a viral suppressor of RNA silencing in Nicotiana benthamiana to facilitate virus infection |
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