Diversity of genetic backgrounds modulating the durability of a major resistance gene. Analysis of a core collection of pepper landraces resistant to Potato virus Y.

The evolution of resistance-breaking capacity in pathogen populations has been shown to depend on the plant genetic background surrounding the resistance genes. We evaluated a core collection of pepper (Capsicum annuum) landraces, representing the worldwide genetic diversity, for its ability to modulate the breakdown frequency by Potato virus Y of major resistance alleles at the pvr2 locus encoding the eukaryotic initiation factor 4E (eIF4E). Depending on the pepper landrace, the breakdown frequency of a given resistance allele varied from 0% to 52.5%, attesting to their diversity and the availability of genetic backgrounds favourable to resistance durability in the plant germplasm. The mutations in the virus genome involved in resistance breakdown also differed between plant genotypes, indicating differential selection effects exerted on the virus population by the different genetic backgrounds. The breakdown frequency was positively correlated with the level of virus accumulation, confirming the impact of quantitative resistance loci on resistance durability. Among these loci, pvr6, encoding an isoform of eIF4E, was associated with a major effect on virus accumulation and on the breakdown frequency of the pvr2-mediated resistance. This exploration of plant genetic diversity delivered new resources for the control of pathogen evolution and the increase in resistance durability.

Potato virus Y: a major crop pathogen that has provided major insights into the evolution of viral pathogenicity.

TAXONOMY: Potato virus Y (PVY) is the type member of the genus Potyvirus in the family Potyviridae. VIRION AND GENOME PROPERTIES: PVY virions have a filamentous, flexuous form, with a length of 730 nm and a diameter of 12 nm. The genomic RNA is single stranded, messenger sense, with a length of 9.7 kb, covalently linked to a viral-encoded protein (VPg) at the 5' end and to a 3' polyadenylated tail. The genome is expressed as a polyprotein of approximately 3062 amino acid residues, processed by three virus-specific proteases into 11 mature proteins. HOSTS: PVY is distributed worldwide and has a broad host range, consisting of cultivated solanaceous species and many solanaceous and nonsolanaceous weeds. It is one of the most economically important plant pathogens and causes severe diseases in cultivated hosts, such as potato, tobacco, tomato and pepper, as well as in ornamental plants. TRANSMISSION: PVY is transmitted from plant to plant by more than 40 aphid species in a nonpersistent manner and, in potato, by planting contaminated seed tubers. DIVERSITY: Five major clades, named C1, C2, Chile, N and O, have been described within the PVY species. In recent decades, a strong increase in prevalence of N × O recombinant isolates has been observed worldwide. A correlation has been observed between PVY phylogeny and certain pathogenicity traits. GENETIC CONTROL OF PVY: Resistance genes against PVY have been used widely in breeding programmes and deployed in the field. These resistance genes show a large diversity of spectrum of action, durability and genetic determinism. Notably, recessive and dominant major resistance genes show highly contrasting patterns of interaction with PVY populations, displaying rapid co-evolution or stable relationships, respectively.

Farther, slower, stronger: how the plant genetic background protects a major resistance gene from breakdown.

Genetic resistance provides efficient control of crop diseases, but is limited by pathogen evolution capacities which often result in resistance breakdown. It has been demonstrated recently, in three different pathosystems, that polygenic resistances combining a major-effect gene and quantitative resistance controlled by the genetic background are more durable than monogenic resistances (with the same major gene in a susceptible genetic background), but the underlying mechanisms are unknown. Using the pepper-Potato virus Y system, we examined three mechanisms that could account for the greater durability of the polygenic resistances: (i) the additional quantitative resistance conferred by the genetic background; (ii) the increase in the number of mutations required for resistance breakdown; and (iii) the slower selection of adapted resistance-breaking mutants within the viral population. The three mechanisms were experimentally validated. The first explained a large part of the variation in resistance breakdown frequency and is therefore expected to be a major determinant of resistance durability. Quantitative resistance factors also had an influence on the second mechanism by modifying the virus mutational pathways towards resistance breakdown and could also have an influence on the third mechanism by increasing genetic drift effects on the viral population. The relevance of these results for other plant-pathogen systems and their importance in plant breeding are discussed.