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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Veröffentlicht in:The Plant journal : for cell and molecular biology 2008-04, Vol.54 (1), p.56-68
Hauptverfasser: Charron, Carine, Nicolaï, Maryse, Gallois, Jean‐Luc, Robaglia, Christophe, Moury, Benoît, Palloix, Alain, Caranta, Carole
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container_title The Plant journal : for cell and molecular biology
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creator Charron, Carine
Nicolaï, Maryse
Gallois, Jean‐Luc
Robaglia, Christophe
Moury, Benoît
Palloix, Alain
Caranta, Carole
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.
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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. 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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. 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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. 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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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