Simultaneous mutations in translation initiation factors eIF4E and eIF(iso)4E are required to prevent pepper veinal mottle virus infection of pepper.
Capsicum resistance to Pepper veinal mottle virus (PVMV) results from complementation between the pvr2 and pvr6 resistance genes: recessive alleles at these two loci are necessary for resistance, whereas any dominant allele confers susceptibility. In line with previous results showing that pvr2 resistance alleles encode mutated versions of the eukaryotic translation initiation factor 4E (eIF4E), the involvement of other members of the eIF4E multigenic family in PVMV resistance was investigated. It was demonstrated that pvr6 corresponds to an eIF(iso)4E gene, predicted to encode the second cap-binding isoform identified in plants. Comparative genetic mapping in pepper and tomato indicated that eIF(iso)4E maps in the same genomic region as pvr6. Sequence analysis revealed an 82 nt deletion in eIF(iso)4E cDNAs from genotypes with the pvr6 resistance allele, leading to a truncated protein. This deletion was shown to co-segregate with pvr6 in doubled haploid and F(2) progeny. Transient expression in a PVMV-resistant genotype of eIF(iso)4E derived from a genotype with the pvr6(+) susceptibility allele resulted in loss of resistance to subsequent PVMV inoculation, confirming that pvr6 encodes the translation factor eIF(iso)4E. Similarly, transient expression of eIF4E from a genotype with the pvr2(+)-eIF4E susceptibility allele also resulted in loss of resistance, demonstrating that wild-type eIF4E and eIF(iso)4E are susceptibility factors for PVMV and that resistance results from the combined effect of mutations in the two cap-binding isoforms. Thus, whilst most potyviruses specifically require one eIF4E isoform to perform their replication cycle, PVMV uses either eIF4E or eIF(iso)4E for infection of pepper.
Ruffel
Sandrine
S
INRA, Genetics and Breeding of Fruits and Vegetables, Domaine St Maurice, BP 94, F-84143 Montfavet, France.
Gallois
Jean-Luc
JL
INRA, Genetics and Breeding of Fruits and Vegetables, Domaine St Maurice, BP 94, F-84143 Montfavet, France.
Moury
Benoît
B
Plant Pathology, Domaine St Maurice, BP 94, F-84143 Montfavet, France.
Robaglia
Christophe
C
Laboratoire de Génétique et Biophysique des Plantes, CEA-CNRS-Université Aix-Marseille II, Faculté des Sciences de Luminy, F-13009 Marseille, France.
Palloix
Alain
A
INRA, Genetics and Breeding of Fruits and Vegetables, Domaine St Maurice, BP 94, F-84143 Montfavet, France.
Caranta
Carole
C
INRA, Genetics and Breeding of Fruits and Vegetables, Domaine St Maurice, BP 94, F-84143 Montfavet, France.
D000483:Alleles; D000595:Amino Acid Sequence; D001483:Base Sequence; D002212:Capsicum / Q000235:genetics* / Q000821:virology*; D002874:Chromosome Mapping; D018744:DNA, Plant / Q000235:genetics; D039561:Eukaryotic Initiation Factor-4E / Q000235:genetics*; D017343:Genes, Plant; D005816:Genetic Complementation Test; D005838:Genotype; D008969:Molecular Sequence Data; D009154:Mutation; D010935:Plant Diseases / Q000821:virology; D010940:Plant Proteins / Q000235:genetics*; D017800:Potyvirus / Q000472:pathogenicity* / Q000502:physiology; D020033:Protein Isoforms / Q000235:genetics; D039381:RNA Cap-Binding Proteins / Q000235:genetics*; D017384:Sequence Deletion; D017386:Sequence Homology, Amino Acid; D012689:Sequence Homology, Nucleic Acid; D014779:Virus Replication
D018744:DNA, Plant; D039561:Eukaryotic Initiation Factor-4E; D010940:Plant Proteins; D020033:Protein Isoforms; D039381:RNA Cap-Binding Proteins