A new eIF4E1 allele characterized by RNAseq data mining is associated with resistance to potato virus Y in tomato albeit with a low durability

Abstract

Allele mining on susceptibility factors offers opportunities to find new sources of resistance among crop wild relatives for breeding purposes. As a proof of concept, we used available RNAseq data to investigate polymorphisms among the four tomato genes encoding translation initiation factors [eIF4E1 and eIF4E2, eIFiso4E and the related gene new cap-binding protein(nCBP)] to look for new potential resistance alleles to potyviruses. By analysing polymorphism among RNAseq data obtained for 20 tomato accessions, 10 belonging to the cultivated type Solanum lycopersicum and 10 belonging to the closest related wild species Solanum pimpinellifolium, we isolated one new eIF4E1 allele, in the S. pimpinellifolium LA0411 accession, which encodes a potential new resistance allele, mainly due to a polymorphism associated with an amino acid change within eIF4E1 region II. We confirmed that this new allele, pot12, is indeed associated with resistance to potato virus Y, although with a restricted resistance spectrum and a very low durability potential. This suggests that mutations occurring in eIF4E region II only may not be sufficient to provide efficient and durable resistance in plants. However, our study emphasizes the opportunity brought by RNAseq data to mine for new resistance alleles. Moreover, this approach could be extended to seek for putative new resistance alleles by screening for variant forms of susceptibility genes encoding plant host proteins known to interact with viral proteins.

Good Riddance? Breaking Disease Susceptibility in the Era of New Breeding Technologies

“…Yet, evidence seems inconclusive. Additional elF4E1 alleles have been identified in wild tomato species, albeit with a limited resistance spectrum [81]. Conversely, in chili peppers (Capsicum annuum), many variants confer resistance and are thought to have originated from loci under positive selection.…”

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

“…Even if the exact mechanism(s) involved in eIF4E ‐mediated resistance are still unclear (Wang and Krishnaswamy, ), it has been shown that the viral genome linked protein (VPg) can interact with eIF4E, mimicking the 5’ cap structure of messenger RNAs (mRNAs). In addition, potyviruses can evolve towards resistance breaking through the acquisition of mutations that either restore compatibility of their VPg with the host mutant eIF4E or allow an interaction with another member of the eIF4E family (Charron et al , ; Gallois et al , , ; Lebaron et al , ; Takakura et al , ).…”

Mimicking natural polymorphism in eIF4E by CRISPR‐Cas9 base editing is associated with resistance to potyviruses

“…Interestingly, the eif4e1 KO eIF4E1 W69L plants' responses to both isolates were not homogenous, with seven plants showing full resistance and nine plants showing full susceptibility. This difference may be caused by resistance breaking, as previously shown for other eIF4E‐based alleles (Charron et al ., ; Lebaron et al ., ). On the contrary, both eif4e1 KO eIF4E1 T80DS81D and eif4e1 KO eIF4E1 N176K plants displayed full resistance to the No.…”

“…The independent selection of these mutations in pepper and in pea provides a compelling argument for their contribution to potyvirus resistance (Charron et al ., ). Interestingly, the G114R mutation located in Region II was not sufficient to provide efficient resistance, similar to equivalent mutations in the same region in the Solanum pimpinellifolium LA0411 resistance allele (Lebaron et al ., ). T80D‐S81D and G114R are substitutions that are frequently isolated in resistance alleles in pepper, tomato and pea, and appear to be under positive selection (Cavatorta et al ., ; Moury et al ., ).…”