Natural variation anf functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg
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.
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dig-cirad-fr-5816312022-04-21T07:50:30Z http://agritrop.cirad.fr/581631/ http://agritrop.cirad.fr/581631/ Natural variation anf functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Charron Carine, Nicolaï Maryse, Gallois Jean-Luc, Robaglia Christophe, Moury Benoit, Palloix Alain, Caranta Carole. 2008. Plant Journal, 54 (1) : 56-68.https://doi.org/10.1111/j.1365-313X.2008.03407.x <https://doi.org/10.1111/j.1365-313X.2008.03407.x> Researchers Natural variation anf functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg Charron, Carine Nicolaï, Maryse Gallois, Jean-Luc Robaglia, Christophe Moury, Benoit Palloix, Alain Caranta, Carole eng 2008 Plant Journal H20 - Maladies des plantes F30 - Génétique et amélioration des plantes 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. article info:eu-repo/semantics/article Journal Article info:eu-repo/semantics/publishedVersion http://agritrop.cirad.fr/581631/1/Charron_2008_Plant%20Journal.pdf text Cirad license info:eu-repo/semantics/restrictedAccess https://agritrop.cirad.fr/mention_legale.html https://doi.org/10.1111/j.1365-313X.2008.03407.x 10.1111/j.1365-313X.2008.03407.x info:eu-repo/semantics/altIdentifier/doi/10.1111/j.1365-313X.2008.03407.x info:eu-repo/semantics/altIdentifier/purl/https://doi.org/10.1111/j.1365-313X.2008.03407.x info:eu-repo/semantics/dataset/purl/http://www.ncbi.nlm.nih.gov/nuccore/EU106863.1 info:eu-repo/semantics/dataset/purl/http://www.ncbi.nlm.nih.gov/nuccore/EU106865.1 info:eu-repo/semantics/dataset/purl/http://www.ncbi.nlm.nih.gov/nuccore/EU106864.1 info:eu-repo/semantics/dataset/purl/http://www.ncbi.nlm.nih.gov/nuccore/NM_001324970.1 |
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| tag |
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| language |
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| topic |
H20 - Maladies des plantes F30 - Génétique et amélioration des plantes H20 - Maladies des plantes F30 - Génétique et amélioration des plantes |
| spellingShingle |
H20 - Maladies des plantes F30 - Génétique et amélioration des plantes H20 - Maladies des plantes F30 - Génétique et amélioration des plantes Charron, Carine Nicolaï, Maryse Gallois, Jean-Luc Robaglia, Christophe Moury, Benoit Palloix, Alain Caranta, Carole Natural variation anf functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg |
| description |
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. |
| format |
article |
| topic_facet |
H20 - Maladies des plantes F30 - Génétique et amélioration des plantes |
| author |
Charron, Carine Nicolaï, Maryse Gallois, Jean-Luc Robaglia, Christophe Moury, Benoit Palloix, Alain Caranta, Carole |
| author_facet |
Charron, Carine Nicolaï, Maryse Gallois, Jean-Luc Robaglia, Christophe Moury, Benoit Palloix, Alain Caranta, Carole |
| author_sort |
Charron, Carine |
| title |
Natural variation anf functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg |
| title_short |
Natural variation anf functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg |
| title_full |
Natural variation anf functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg |
| title_fullStr |
Natural variation anf functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg |
| title_full_unstemmed |
Natural variation anf functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg |
| title_sort |
natural variation anf functional analyses provide evidence for co-evolution between plant eif4e and potyviral vpg |
| url |
http://agritrop.cirad.fr/581631/ http://agritrop.cirad.fr/581631/1/Charron_2008_Plant%20Journal.pdf |
| work_keys_str_mv |
AT charroncarine naturalvariationanffunctionalanalysesprovideevidenceforcoevolutionbetweenplanteif4eandpotyviralvpg AT nicolaimaryse naturalvariationanffunctionalanalysesprovideevidenceforcoevolutionbetweenplanteif4eandpotyviralvpg AT galloisjeanluc naturalvariationanffunctionalanalysesprovideevidenceforcoevolutionbetweenplanteif4eandpotyviralvpg AT robagliachristophe naturalvariationanffunctionalanalysesprovideevidenceforcoevolutionbetweenplanteif4eandpotyviralvpg AT mourybenoit naturalvariationanffunctionalanalysesprovideevidenceforcoevolutionbetweenplanteif4eandpotyviralvpg AT palloixalain naturalvariationanffunctionalanalysesprovideevidenceforcoevolutionbetweenplanteif4eandpotyviralvpg AT carantacarole naturalvariationanffunctionalanalysesprovideevidenceforcoevolutionbetweenplanteif4eandpotyviralvpg |
| _version_ |
1758025077252685824 |