The Eukaryotic Translation Initiation Factor 4E Controls Lettuce Susceptibility to the PotyvirusLettuce mosaic virus 

Abstract

The eIF4E and eIF(iso)4E cDNAs from several genotypes of lettuce (Lactuca sativa) that are susceptible, tolerant, or resistant to infection by Lettuce mosaic virus (LMV; genus Potyvirus) were cloned and sequenced. Although Ls-eIF(iso)4E was monomorphic in sequence, three types of Ls-eIF4E differed by point sequence variations, and a short in-frame deletion in one of them. The amino acid variations specific to Ls-eIF4E(1) and Ls-eIF4E(2) were predicted to be located near the cap recognition pocket in a homology-based tridimensional protein model. In 19 lettuce genotypes, including two near-isogenic pairs, there was a strict correlation between these three allelic types and the presence or absence of the recessive LMV resistance genes mo1(1) and mo1(2). Ls-eIF4E(1) and mo1(1) cosegregated in the progeny of two separate crosses between susceptible genotypes and an mo1(1) genotype. Finally, transient ectopic expression of Ls-eIF4E restored systemic accumulation of a green fluorescent protein-tagged LMV in LMV-resistant mo1(2) plants and a recombinant LMV expressing Ls-eIF4E degrees from its genome, but not Ls-eIF4E(1) or Ls-eIF(iso)4E, accumulated and produced symptoms in mo1(1) or mo1(2) genotypes. Therefore, sequence correlation, tight genetic linkage, and functional complementation strongly suggest that eIF4E plays a role in the LMV cycle in lettuce and that mo1(1) and mo1(2) are alleles coding for forms of eIF4E unable or less effective to fulfill this role. More generally, the isoforms of eIF4E appear to be host factors involved in the cycle of potyviruses in plants, probably through a general mechanism yet to be clarified.

Arabidopsis thaliana class II poly(A)-binding proteins are required for efficient multiplication of turnip mosaic virus

“…Requirement for eIF4E/4G or eIF(iso)4E/4G isomers depends on the virus being studied, as A. thaliana knockout plants for eIF(iso)4E or eIF(iso)4G1/2 genes are resistant to TuMV, lettuce mosaic virus and plum pox virus infection, while disruption of eIF4E1 or eIF4G results in resistance to clover yellow vein virus (Decroocq et al, 2006; Duprat et al, 2002;Lellis et al, 2002;Nicaise et al, 2007;Sato et al, 2005). These results were also confirmed in multiple plant species with the identification of eIF4E and eIF4G isoforms as recessive resistance gene products against potyviruses (Gao et al, 2004;Kang et al, 2005;Nicaise et al, 2003; Ruffel et al, 2002Ruffel et al, , 2005. Together, these results are indicative of an essential link between potyvirus replication and components of the translation initiation complex.…”

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.…”

“…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.…”