A natural recessive resistance gene against potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E)

Abstract

SummaryWe show here that the pvr2 locus in pepper, conferring recessive resistance against strains of potato virus Y (PVY), corresponds to a eukaryotic initiation factor 4E (eIF4E) gene. RFLP analysis on the PVY-susceptible and resistant pepper cultivars, using an eIF4E cDNA from tobacco as probe, revealed perfect map cosegregation between a polymorphism in the eIF4E gene and the pvr2 alleles, pvr2 1 (resistant to PVY-0) and pvr2 2 (resistant to PVY-0 and 1). The cloned pepper eIF4E cDNA encoded a 228 amino acid polypeptide with 70-86% nucleotide sequence identity with other plant eIF4Es. The sequences of eIF4E protein from two PVY-susceptible cultivars were identical and differed from the eIF4E sequences of the two PVY-resistant cultivars Yolo Y (YY) (pvr2 1 ) and FloridaVR2 (F) (pvr2 2 ) at two amino acids, a mutation common to both resistant genotypes and a second mutation specific to each. Complementation experiments were used to show that the eIF4E gene corresponds to pvr2. Thus, potato virus X-mediated transient expression of eIF4E from susceptible cultivar Yolo Wonder (YW) in the resistant genotype YY resulted in loss of resistance to subsequent PVY-0 inoculation and transient expression of eIF4E from YY (resistant to PVY-0; susceptible to PVY-1) rendered genotype F susceptible to PVY-1. Several lines of evidence indicate that interaction between the potyvirus genome-linked protein (VPg) and eIF4E are important for virus infectivity, suggesting that the recessive resistance could be due to incompatibility between the VPg and eIF4E in the resistant genotype.

Functional Dissection of Naturally Occurring Amino Acid Substitutions in eIF4E That Confers Recessive Potyvirus Resistance in Plants

“…The eIF4E protein encoded by the pvr1 allele (eIF4E-pvr1) contains amino acid changes T51A, P66T, and G107R, eIF4E-pvr1 1 contains amino acid changes V67E and L79R, and eIF4E-pvr1 2 contains amino acid changes V67E, L79R, and D109N compared with eIF4E-Pvr1 þ (Ruffel et al, 2002;Kang et al, 2005a). To understand the biochemical effect of each amino acid substitution in eIF4E, we generated novel alleles of eIF4E, which contain each amino acid substitution separately, as shown in Figure 1C.…”

“…In plants, a number of alleles at the eIF4E locus conferring resistance against multiple viruses in the family Potyviridae and at least one virus in the family Tombusviridae have been discovered recently. These include pvr1 in pepper (Ruffel et al, 2002;Kang et al, 2005a), mo1 in lettuce (Nicaise et al, 2003), sbm1 in pea (Gao et al, 2004), pot-1 in tomato (Ruffel et al, 2005), rym4/5 in barley (Stein et al, 2005), and nsv in melon (Nieto et al, 2006). It is striking to note that the critical amino acid substitution in eIF4E-pvr1, G107R, also exists at the homologous sites in several other recessive resistance genes: mo1 and sbm1 in lettuce and pea, respectively.…”

“…The efficacy of this resistance, which typically manifests as recessive inheritence, is evidenced by the prominence of recessive resistance to plant viruses relative to that of other pathogen classes (Provvidenti and Hampton, 1992;Keller et al, 1998;Robaglia and Caranta, 2006). This defense strategy appears to be particularly widely observed at the eIF4E locus where resistance to multiple RNA phytopathogenic viruses occurs in numerous plant families, including pvr1 in Capsicum (Ruffel et al, 2002;Kang et al, 2005a), mo1 in lettuce (Lactuca sativa; Nicaise et al, 2003), sbm1 in pea (Pisum sativum; Gao et al, 2004), pot-1 in tomato (Solanum lycopersicum; Ruffel et al, 2005), rym4/5 in barley (Hordeum vulgare; Stein et al, 2005), and nsv in melon (Cucumis melo; Nieto et al, 2006). In addition to these naturally existing genes, lsp1 and cum1 resistance alleles created via mutagenesis in Arabidopsis thaliana also encode eIF4E (Lellis et al, 2002;Yoshii et al, 2004).…”

Biotech Potatoes in the 21st Century: 20 Years Since the First Biotech Potato

“…One such example is the eIF4E gene that has been found to be associated with virus resistance in many plant species (Nicaise et al 2003;Gao et al 2004;Yoshii et al 2004;Kang et al 2005;Kanyuka et al 2005;Stein et al 2005;Nieto et al 2006Nieto et al , 2007Ibiza et al 2010;Naderpour et al 2010;Piron et al 2010), including resistance to potato virus Y in potato, tomato, and pepper (Ruffel et al 2002(Ruffel et al , 2005Cavatorta et al 2011;Duan et al 2012). Variants of eIF4E confer resistance to PVY in the potato wild species relatives S. chacoense, S. demissum, and S. etuberosum , permitting the eventual use of this gene in future biotech potato varieties.…”

“…Instead, it is a host protein required for proper translation of the viral genomic RNA. Mutations within eIF4E render the protein unusable by the virus and therefore the virus is unable to replicate within the plant cell (Ruffel et al 2002). In pepper and tomato, eIF4E-mediated resistance is inherited in a recessive manner (Ruffel et al 2002(Ruffel et al , 2005.…”