Concurrent evolution of resistance and tolerance to potato virus Y in Capsicum annuum revealed by genome-wide association.

Lucie Tamisier,Caroline Djian‐Caporalino,Marion Szadkowski,Judith Hirsch,Alain Palloix,Benoit Moury,Grégory Girardot

doi:10.1111/mpp.13157

Abstract

We performed a genome‐wide association study of pepper (Capsicum annuum) tolerance to potato virus Y (PVY). For 254 pepper accessions, we estimated the tolerance to PVY as the coefficient of regression of the fresh weight (or height) of PVY‐infected and mock‐inoculated plants against within‐plant virus load. Small (strongly negative) coefficients of regression indicate low tolerance because plant biomass or growth decreases sharply as virus load increases. The tolerance level varied largely, with some pepper accessions showing no symptoms or fairly mild mosaics, whereas about half (48%) of the accessions showed necrotic symptoms. We found two adjacent single‐nucleotide polymorphisms (SNPs) at one extremity of chromosome 9 that were significantly associated with tolerance to PVY. Similarly, in three biparental pepper progenies, we showed that the induction of necrosis on PVY systemic infection segregated as a monogenic trait determined by a locus on chromosome 9. Our results also demonstrate the existence of a negative correlation between resistance and tolerance among the cultivated pepper accessions at both the phenotypic and genetic levels. By comparing the distributions of the tolerance‐associated SNP alleles and previously identified PVY resistance‐associated SNP alleles, we showed that cultivated pepper accessions possess favourable alleles for both resistance and tolerance less frequently than expected under random associations, while the minority of wild pepper accessions frequently combined resistance and tolerance alleles. This divergent evolution of PVY resistance and tolerance could be related to pepper domestication or farmer's selection.

Highlights

To avoid or mitigate the harmful effects of pests and pathogens, plants have developed two main lines of defence: resistance and tolerance (Råberg et al, 2007)
A previous genome-wide association study (GWAS) performed on the pepper core-collection identified seven single-nucleotide polymorphisms (SNPs) linked to pepper resistance to potato virus Y (PVY), using compressed mixed linear model (CMLM) and multilocus mixed model (MLMM) (Tamisier et al, 2020)
Many studies have focused on analysing plant resistance to parasites, providing us with an in-depth understanding of its molecular and physiological mechanisms and how it evolves

Summary

| INTRODUCTION

To avoid or mitigate the harmful effects of pests and pathogens, plants have developed two main lines of defence: resistance and tolerance (Råberg et al, 2007). A previous GWAS performed on the pepper core-collection identified seven SNPs linked to pepper resistance to PVY, using CMLM and MLMM (Tamisier et al, 2020) These SNPs were associated with the number of primary infection foci in the inoculated leaves (effective population size of PVY at the inoculation step) and/or the viral load at the systemic level and were localized on chromosomes 4 (positions 1,151,249, 1,151,254, and 340,333 bp), 6 (positions 234,142,995 and 234,143,013 bp), 9 (position 58,056,303 bp), and 12 (position 235,513,719 bp). Other co-segregations of resistance and tolerance-associated alleles did not differ significantly between cultivated and wild accessions after Bonferroni correction but a trend similar to that above was observed for association of the other resistance SNPs with the tolerance SNP at position 251,247,298 bp of chromosome 9. These analyses could suffer from a lack of statistical power because of the small number of wild accessions

| DISCUSSION

Findings

| EXPERIMENTAL PROCEDURES