A complex eIF4E locus impacts the durability of va resistance to Potato virus Y in tobacco

Abstract

Summary Many recessive resistances against potyviruses are mediated by eukaryotic translation initiation factor 4E (eIF4E). In tobacco, the va resistance gene commonly used to control Potato virus Y (PVY) corresponds to a large deletion affecting the eIF4E‐1 gene on chromosome 21. Here, we compared the resistance durability conferred by various types of mutations affecting eIF4E‐1 (deletions of various sizes, frameshift or nonsense mutations). The ‘large deletion’ genotypes displayed the broadest and most durable resistance, whereas frameshift and nonsense mutants displayed a less durable resistance, with rapid and frequent apparition of resistance‐breaking variants. In addition, genetic and transcriptomic analyses revealed that resistance durability is strongly impacted by a complex genetic locus on chromosome 14, which contains three other eIF4E genes. One of these, eIF4E‐3 , is rearranged as a hybrid gene between eIF4E‐2 and eIF4E‐3 ( eIF4E‐ 2‐3 ) in the genotypes showing the most durable resistance, while eIF4E‐2 is differentially expressed between the tested varieties. RNA‐seq and quantitative reverse transcriptase‐polymerase chain reaction experiments demonstrated that eIF4E‐2 expression level is positively correlated with resistance durability. These results suggest that besides the nature of the mutation affecting eIF4E‐1 , three factors linked with a complex locus may potentially impact va durability: loss of an integral eIF4E‐3 , presence of eIF4E‐ 2‐3 and overexpression of eIF4E‐2. This latter gene might act as a decoy in a non‐productive virus–plant interaction, limiting the ability of PVY to evolve towards resistance breaking. Taken together, these results show that va resistance durability can in large part be explained by complex redundancy effects in the eIF4E gene family.

Plant Molecular Responses to Potato Virus Y: A Continuum of Outcomes from Sensitivity and Tolerance to Resistance

“…Naturally existing resistant versions of eIF4E differ from the susceptible form of the protein by only one to five amino acid changes, near the VPg-binding region (reviewed by [95]). The tobacco isoform eIF4E-2 expression level is positively correlated with resistance durability and might act as a decoy, limiting the ability of PVY to evolve towards resistance breaking [96]. Nevertheless, resistance-breaking strains of PVY, carrying a mutation in the VPg, that overcome this type of resistance, were identified.…”

Development of a PVY Resistant Flue-Cured Tobacco Line via EMS Mutagenesis of eIF4E

“…The feasibility of this approach has been demonstrated in N. tabacum, where stop codon mutations (W50* and W53*) have been introduced in exon 1 of eIF4E1-S in the PVY susceptible burley tobacco line BB16NN [22]. Both of these EMS-induced nonsense mutations lead to the synthesis of C-terminal truncated eIF4E1-S proteins, which confer resistance to PVY O and PVY N isolates [22,33] but reduced resistance to PVY isolates of the C clade [33].…”

“…Tolerance to RB PVY variants varies with the virus isolates [34][35][36][37] and mutation types affecting eIF4E genes, such as eIF(iso)4E-T and eIF(iso)4E-S [38]. A recent study characterized the differences in resistance durability, in which mutants harboring a large deletion at the eIF4E1-S locus on chromosome 21 displayed the most durable resistance, whereas those carrying frameshift and nonsense mutations displayed less durable resistance and were associated with frequent emergence of RB PVY isolates [33]. Additionally, genetic and transcriptomic analyses conducted by Michel et al [33] indicated that resistance durability was correlated with a complex genetic locus on chromosome 14 that contained three other eIF4E copies (eIF4E-2-4).…”

“…A recent study characterized the differences in resistance durability, in which mutants harboring a large deletion at the eIF4E1-S locus on chromosome 21 displayed the most durable resistance, whereas those carrying frameshift and nonsense mutations displayed less durable resistance and were associated with frequent emergence of RB PVY isolates [33]. Additionally, genetic and transcriptomic analyses conducted by Michel et al [33] indicated that resistance durability was correlated with a complex genetic locus on chromosome 14 that contained three other eIF4E copies (eIF4E-2-4). However, in this study, we did not observe the breakage of resistance against PVY isolates, possibly because a limited number of isolates were assayed.…”

Translational gene regulation in plants: A green new deal

“…In this way, the plant can stay one step ahead of the virus even though its rate of sequence change and the rate with which new alleles spread through the population are far slower than that of the virus. In favor of this hypothesis, the allelic diversity of eIF4E genes explains different degrees of resistance durability in tobacco (Michel et al, 2019). Specifically, a resistance breaking strain of potato virus Y with a mutation in its VPg switched its preference from the eIF4E1 paralog toward an eIFiso4E paralog in its tobacco host (Takakura, Udagawa, Shinjo, & Koga, 2018).…”