The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell‐to‐cell trafficking

Abstract

SummaryFrom the characterization of the recessive resistance gene, sbm1, in pea we have identified the eukaryotic translation initiation factor, eIF4E, as a susceptibility factor required for infection with the Potyvirus, Pea seedborne mosaic virus. A functional analysis of the mode of action of the product of the dominant allele revealed a novel function for eIF4E in its support for virus movement from cell-to-cell, in addition to its probable support for viral RNA translation, and hence replication. Different resistance specificities in two independent pea lines were explained by different mutations in eIF4E. On the modelled structure of eIF4E the coding changes were in both cases lying in and around the structural pocket involved in binding the 5¢-m 7 G cap of eukaryotic mRNAs.Protein expression and cap-binding analysis showed that eIF4E encoded by a resistant plant could not bind to m 7 G-Sepharose, a result which may point to functional redundancy between eIF4E and the paralogous eIF(iso)4E in resistant peas. These observations, together with related findings for other potyvirus recessive resistances, provide a more complete picture of the potyvirus life cycle.

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

“…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.…”

“…It has been noted that the eIF4E proteins encoded by the pvr1 allele from pepper and the sbm1 allele from pea, which both contain the G107R substitution, show reduced cap binding (Gao et al, 2004;Kang et al, 2005a). Recent studies have suggested that the mRNA cap structure and potyvirus VPg at least partially share the protein binding pocket structure of the eIF4E protein or its isoform eIF(iso)4E (Michon et al, 2006;Miyoshi et al, 2006).…”

“…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.…”

Cell-to-cell movement of three genera (+) ss RNA plant viruses

“…Recently, a potential link between virus accumulation and cell-to-cell movement was identified when the eukaryotic translocation factors eIF4E and eIF(iso)4E were shown to aid in virus cell-to-cell movement (Gao et al 2004). These observations correspond with earlier studies where plant mutants with eIF4E exhibit limited virus spread (Arroyo et al 1996).…”