Natural variation and functional analyses provide evidence for co‐evolution between plant eIF4E and potyviral VPg
Summary Amino acid substitutions in the eukaryotic translation initiation factor 4E (eIF4E) result in recessive resistance to potyviruses in a range of plant species, including Capsicum spp. Correspondingly, amino acid changes in the central part of the viral genome‐linked protein (VPg) are responsi...
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description | Summary
Amino acid substitutions in the eukaryotic translation initiation factor 4E (eIF4E) result in recessive resistance to potyviruses in a range of plant species, including Capsicum spp. Correspondingly, amino acid changes in the central part of the viral genome‐linked protein (VPg) are responsible for the potyvirus’s ability to overcome eIF4E‐mediated resistance. A key observation was that physical interaction between eIF4E and the VPg is required for viral infection, and eIF4E mutations that cause resistance prevent VPg binding and inhibit the viral cycle. In this study, polymorphism analysis of the pvr2‐eIF4E coding sequence in a worldwide sample of 25 C. annuum accessions identified 10 allelic variants with exclusively non‐synonymous variations clustered in two surface loops of eIF4E. Resistance and genetic complementation assays demonstrated that pvr2 variants, each with signature amino acid changes, corresponded to potyvirus resistance alleles. Systematic analysis of the interactions between eIF4E proteins encoded by the 10 pvr2 alleles and VPgs of virulent and avirulent potato virus Y (PVY) and tobacco etch virus (TEV) strains demonstrated that resistance phenotypes arose from disruption of the interaction between eIF4E and VPg, and that viral adaptation to eIF4E‐mediated resistance resulted from restored interaction with the resistance protein. Complementation of an eIF4E knockout yeast strain by C. annuum eIF4E proteins further shows that amino acid changes did not impede essential eIF4E functions. Altogether, these results argue in favour of a co‐evolutionary ‘arms race’ between Capsicum eIF4E and potyviral VPg. |
doi_str_mv | 10.1111/j.1365-313X.2008.03407.x |
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Amino acid substitutions in the eukaryotic translation initiation factor 4E (eIF4E) result in recessive resistance to potyviruses in a range of plant species, including Capsicum spp. Correspondingly, amino acid changes in the central part of the viral genome‐linked protein (VPg) are responsible for the potyvirus’s ability to overcome eIF4E‐mediated resistance. A key observation was that physical interaction between eIF4E and the VPg is required for viral infection, and eIF4E mutations that cause resistance prevent VPg binding and inhibit the viral cycle. In this study, polymorphism analysis of the pvr2‐eIF4E coding sequence in a worldwide sample of 25 C. annuum accessions identified 10 allelic variants with exclusively non‐synonymous variations clustered in two surface loops of eIF4E. Resistance and genetic complementation assays demonstrated that pvr2 variants, each with signature amino acid changes, corresponded to potyvirus resistance alleles. Systematic analysis of the interactions between eIF4E proteins encoded by the 10 pvr2 alleles and VPgs of virulent and avirulent potato virus Y (PVY) and tobacco etch virus (TEV) strains demonstrated that resistance phenotypes arose from disruption of the interaction between eIF4E and VPg, and that viral adaptation to eIF4E‐mediated resistance resulted from restored interaction with the resistance protein. Complementation of an eIF4E knockout yeast strain by C. annuum eIF4E proteins further shows that amino acid changes did not impede essential eIF4E functions. Altogether, these results argue in favour of a co‐evolutionary ‘arms race’ between Capsicum eIF4E and potyviral VPg.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/j.1365-313X.2008.03407.x</identifier><identifier>PMID: 18182024</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Alleles ; Amino Acid Substitution ; Amino acids ; Botany ; Capsicum ; Capsicum - genetics ; Capsicum - metabolism ; Capsicum annuum ; DNA, Plant - genetics ; Eukaryotes ; Eukaryotic Initiation Factor-4E - chemistry ; Eukaryotic Initiation Factor-4E - genetics ; Eukaryotic Initiation Factor-4E - metabolism ; eukaryotic translation initiation factor 4E ; Evolution, Molecular ; Evolutionary biology ; Flowers & plants ; Genetic Variation ; Genetics ; Genomics ; Life Sciences ; Microbiology and Parasitology ; Plant Diseases - virology ; Plant pathology ; Plant Proteins - chemistry ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants genetics ; Potato virus Y ; Potyvirus ; Potyvirus - genetics ; Potyvirus - metabolism ; Potyvirus - pathogenicity ; recessive virus resistance ; Solanum tuberosum ; Tobacco etch virus ; Vegetal Biology ; viral genome‐linked protein ; Viral Proteins - genetics ; Viral Proteins - metabolism ; Virology</subject><ispartof>The Plant journal : for cell and molecular biology, 2008-04, Vol.54 (1), p.56-68</ispartof><rights>2008 The Authors</rights><rights>Journal compilation © 2008 Blackwell Publishing Ltd and the Society for Experimental Biology</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5647-132820655a1793258efcf037d214f896999cb394356bcce3368d69f8cc6c017c3</citedby><cites>FETCH-LOGICAL-c5647-132820655a1793258efcf037d214f896999cb394356bcce3368d69f8cc6c017c3</cites><orcidid>0000-0003-0451-1740 ; 0000-0003-3081-1034 ; 0000-0002-0861-909X ; 0000-0003-0281-9936</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%2Fj.1365-313X.2008.03407.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1365-313X.2008.03407.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18182024$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02667924$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Charron, Carine</creatorcontrib><creatorcontrib>Nicolaï, Maryse</creatorcontrib><creatorcontrib>Gallois, Jean‐Luc</creatorcontrib><creatorcontrib>Robaglia, Christophe</creatorcontrib><creatorcontrib>Moury, Benoît</creatorcontrib><creatorcontrib>Palloix, Alain</creatorcontrib><creatorcontrib>Caranta, Carole</creatorcontrib><title>Natural variation and functional analyses provide evidence for co‐evolution between plant eIF4E and potyviral VPg</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary
Amino acid substitutions in the eukaryotic translation initiation factor 4E (eIF4E) result in recessive resistance to potyviruses in a range of plant species, including Capsicum spp. Correspondingly, amino acid changes in the central part of the viral genome‐linked protein (VPg) are responsible for the potyvirus’s ability to overcome eIF4E‐mediated resistance. A key observation was that physical interaction between eIF4E and the VPg is required for viral infection, and eIF4E mutations that cause resistance prevent VPg binding and inhibit the viral cycle. In this study, polymorphism analysis of the pvr2‐eIF4E coding sequence in a worldwide sample of 25 C. annuum accessions identified 10 allelic variants with exclusively non‐synonymous variations clustered in two surface loops of eIF4E. Resistance and genetic complementation assays demonstrated that pvr2 variants, each with signature amino acid changes, corresponded to potyvirus resistance alleles. Systematic analysis of the interactions between eIF4E proteins encoded by the 10 pvr2 alleles and VPgs of virulent and avirulent potato virus Y (PVY) and tobacco etch virus (TEV) strains demonstrated that resistance phenotypes arose from disruption of the interaction between eIF4E and VPg, and that viral adaptation to eIF4E‐mediated resistance resulted from restored interaction with the resistance protein. Complementation of an eIF4E knockout yeast strain by C. annuum eIF4E proteins further shows that amino acid changes did not impede essential eIF4E functions. Altogether, these results argue in favour of a co‐evolutionary ‘arms race’ between Capsicum eIF4E and potyviral VPg.</description><subject>Alleles</subject><subject>Amino Acid Substitution</subject><subject>Amino acids</subject><subject>Botany</subject><subject>Capsicum</subject><subject>Capsicum - genetics</subject><subject>Capsicum - metabolism</subject><subject>Capsicum annuum</subject><subject>DNA, Plant - genetics</subject><subject>Eukaryotes</subject><subject>Eukaryotic Initiation Factor-4E - chemistry</subject><subject>Eukaryotic Initiation Factor-4E - genetics</subject><subject>Eukaryotic Initiation Factor-4E - metabolism</subject><subject>eukaryotic translation initiation factor 4E</subject><subject>Evolution, Molecular</subject><subject>Evolutionary biology</subject><subject>Flowers & plants</subject><subject>Genetic Variation</subject><subject>Genetics</subject><subject>Genomics</subject><subject>Life Sciences</subject><subject>Microbiology and Parasitology</subject><subject>Plant Diseases - virology</subject><subject>Plant pathology</subject><subject>Plant Proteins - chemistry</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants genetics</subject><subject>Potato virus Y</subject><subject>Potyvirus</subject><subject>Potyvirus - genetics</subject><subject>Potyvirus - metabolism</subject><subject>Potyvirus - pathogenicity</subject><subject>recessive virus resistance</subject><subject>Solanum tuberosum</subject><subject>Tobacco etch virus</subject><subject>Vegetal Biology</subject><subject>viral genome‐linked protein</subject><subject>Viral Proteins - genetics</subject><subject>Viral Proteins - metabolism</subject><subject>Virology</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkctu1DAUhi1ERYeWV0AWC6QuEnyLLwsWVdXSolHbRYvYWR7HgYwy8WAnaWfHI_CMPAn2zKhI3YAXx7fv_D7HPwAQoxKn8WFZYsqrgmL6tSQIyRJRhkT5-ALMni5eghlSHBWCYXIIXse4RAgLytkrcIgllgQRNgPx2gxjMB2cTGjN0Poemr6GzdjbvEkXJoVNdBGug5_a2kGXY28dbHyA1v_--ctNvhu3uQs3PDjXw3Vn-gG6qwt2vtVb-2EztfmdL7ffjsFBY7ro3uznI3B_cX53dlnMbz5dnZ3OC1txJgpMSSqSV5XBQlFSSdfYBlFRE8waqbhSyi6oYrTiC2sdpVzWXDXSWm5Tp5YegZOd7nfT6XVoVyZstDetvjyd63yGCOdCETbhxL7fsanLH6OLg1610bou9eH8GDWXGCFB_g0SxBSSTCTw3TNw6ceQPjMxmFbJMSwTJHeQDT7G4JqnOjHS2Wq91NlRnR3V2Wq9tVo_ptS3e_1xsXL138S9twn4uAMe2s5t_ltY391-ziv6BxTKt1c</recordid><startdate>200804</startdate><enddate>200804</enddate><creator>Charron, Carine</creator><creator>Nicolaï, Maryse</creator><creator>Gallois, Jean‐Luc</creator><creator>Robaglia, Christophe</creator><creator>Moury, Benoît</creator><creator>Palloix, Alain</creator><creator>Caranta, Carole</creator><general>Blackwell Publishing Ltd</general><general>Wiley</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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7U9</scope><scope>H94</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0003-0451-1740</orcidid><orcidid>https://orcid.org/0000-0003-3081-1034</orcidid><orcidid>https://orcid.org/0000-0002-0861-909X</orcidid><orcidid>https://orcid.org/0000-0003-0281-9936</orcidid></search><sort><creationdate>200804</creationdate><title>Natural variation and functional analyses provide evidence for co‐evolution between plant eIF4E and potyviral VPg</title><author>Charron, Carine ; Nicolaï, Maryse ; Gallois, Jean‐Luc ; Robaglia, Christophe ; Moury, Benoît ; Palloix, Alain ; Caranta, Carole</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5647-132820655a1793258efcf037d214f896999cb394356bcce3368d69f8cc6c017c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Alleles</topic><topic>Amino Acid Substitution</topic><topic>Amino acids</topic><topic>Botany</topic><topic>Capsicum</topic><topic>Capsicum - genetics</topic><topic>Capsicum - metabolism</topic><topic>Capsicum annuum</topic><topic>DNA, Plant - genetics</topic><topic>Eukaryotes</topic><topic>Eukaryotic Initiation Factor-4E - chemistry</topic><topic>Eukaryotic Initiation Factor-4E - genetics</topic><topic>Eukaryotic Initiation Factor-4E - metabolism</topic><topic>eukaryotic translation initiation factor 4E</topic><topic>Evolution, Molecular</topic><topic>Evolutionary biology</topic><topic>Flowers & plants</topic><topic>Genetic Variation</topic><topic>Genetics</topic><topic>Genomics</topic><topic>Life Sciences</topic><topic>Microbiology and Parasitology</topic><topic>Plant Diseases - virology</topic><topic>Plant pathology</topic><topic>Plant Proteins - chemistry</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants genetics</topic><topic>Potato virus Y</topic><topic>Potyvirus</topic><topic>Potyvirus - genetics</topic><topic>Potyvirus - metabolism</topic><topic>Potyvirus - pathogenicity</topic><topic>recessive virus resistance</topic><topic>Solanum tuberosum</topic><topic>Tobacco etch virus</topic><topic>Vegetal Biology</topic><topic>viral genome‐linked protein</topic><topic>Viral Proteins - genetics</topic><topic>Viral Proteins - metabolism</topic><topic>Virology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Charron, Carine</creatorcontrib><creatorcontrib>Nicolaï, Maryse</creatorcontrib><creatorcontrib>Gallois, Jean‐Luc</creatorcontrib><creatorcontrib>Robaglia, Christophe</creatorcontrib><creatorcontrib>Moury, Benoît</creatorcontrib><creatorcontrib>Palloix, Alain</creatorcontrib><creatorcontrib>Caranta, Carole</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Charron, Carine</au><au>Nicolaï, Maryse</au><au>Gallois, Jean‐Luc</au><au>Robaglia, Christophe</au><au>Moury, Benoît</au><au>Palloix, Alain</au><au>Caranta, Carole</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Natural variation and functional analyses provide evidence for co‐evolution between plant eIF4E and potyviral VPg</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2008-04</date><risdate>2008</risdate><volume>54</volume><issue>1</issue><spage>56</spage><epage>68</epage><pages>56-68</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>Summary
Amino acid substitutions in the eukaryotic translation initiation factor 4E (eIF4E) result in recessive resistance to potyviruses in a range of plant species, including Capsicum spp. Correspondingly, amino acid changes in the central part of the viral genome‐linked protein (VPg) are responsible for the potyvirus’s ability to overcome eIF4E‐mediated resistance. A key observation was that physical interaction between eIF4E and the VPg is required for viral infection, and eIF4E mutations that cause resistance prevent VPg binding and inhibit the viral cycle. In this study, polymorphism analysis of the pvr2‐eIF4E coding sequence in a worldwide sample of 25 C. annuum accessions identified 10 allelic variants with exclusively non‐synonymous variations clustered in two surface loops of eIF4E. Resistance and genetic complementation assays demonstrated that pvr2 variants, each with signature amino acid changes, corresponded to potyvirus resistance alleles. Systematic analysis of the interactions between eIF4E proteins encoded by the 10 pvr2 alleles and VPgs of virulent and avirulent potato virus Y (PVY) and tobacco etch virus (TEV) strains demonstrated that resistance phenotypes arose from disruption of the interaction between eIF4E and VPg, and that viral adaptation to eIF4E‐mediated resistance resulted from restored interaction with the resistance protein. Complementation of an eIF4E knockout yeast strain by C. annuum eIF4E proteins further shows that amino acid changes did not impede essential eIF4E functions. Altogether, these results argue in favour of a co‐evolutionary ‘arms race’ between Capsicum eIF4E and potyviral VPg.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>18182024</pmid><doi>10.1111/j.1365-313X.2008.03407.x</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-0451-1740</orcidid><orcidid>https://orcid.org/0000-0003-3081-1034</orcidid><orcidid>https://orcid.org/0000-0002-0861-909X</orcidid><orcidid>https://orcid.org/0000-0003-0281-9936</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Alleles Amino Acid Substitution Amino acids Botany Capsicum Capsicum - genetics Capsicum - metabolism Capsicum annuum DNA, Plant - genetics Eukaryotes Eukaryotic Initiation Factor-4E - chemistry Eukaryotic Initiation Factor-4E - genetics Eukaryotic Initiation Factor-4E - metabolism eukaryotic translation initiation factor 4E Evolution, Molecular Evolutionary biology Flowers & plants Genetic Variation Genetics Genomics Life Sciences Microbiology and Parasitology Plant Diseases - virology Plant pathology Plant Proteins - chemistry Plant Proteins - genetics Plant Proteins - metabolism Plants genetics Potato virus Y Potyvirus Potyvirus - genetics Potyvirus - metabolism Potyvirus - pathogenicity recessive virus resistance Solanum tuberosum Tobacco etch virus Vegetal Biology viral genome‐linked protein Viral Proteins - genetics Viral Proteins - metabolism Virology |
title | Natural variation and functional analyses provide evidence for co‐evolution between plant eIF4E and potyviral VPg |
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