Genome scans on experimentally evolved populations reveal candidate regions for adaptation to plant resistance in the potato cyst nematode Globodera pallida.

Improving resistance durability involves to be able to predict the adaptation speed of pathogen populations. Identifying the genetic bases of pathogen adaptation to plant resistances is a useful step to better understand and anticipate this phenomenon. Globodera pallida is a major pest of potato crop for which a resistance QTL, GpaVvrn , has been identified in Solanum vernei. However, its durability is threatened as G. pallida populations are able to adapt to the resistance in few generations. The aim of this study was to investigate the genomic regions involved in the resistance breakdown by coupling experimental evolution and high-density genome scan. We performed a whole-genome resequencing of pools of individuals (Pool-Seq) belonging to G. pallida lineages derived from two independent populations having experimentally evolved on susceptible and resistant potato cultivars. About 1.6 million SNPs were used to perform the genome scan using a recent model testing for adaptive differentiation and association to population-specific covariables. We identified 275 outliers and 31 of them, which also showed a significant reduction in diversity in adapted lineages, were investigated for their genic environment. Some candidate genomic regions contained genes putatively encoding effectors and were enriched in SPRYSECs, known in cyst nematodes to be involved in pathogenicity and in (a)virulence. Validated candidate SNPs will provide a useful molecular tool to follow frequencies of virulence alleles in natural G. pallida populations and define efficient strategies of use of potato resistances maximizing their durability.

Adaptation to the most abundant host genotype in an agricultural plant-pathogen system--potato late blight.

This study investigated local adaptation of Phytophthora infestans populations, the causal agent of potato late blight, to two susceptible potato cultivars, each grown for a number of years and over large areas in separate French regions. We measured aggressiveness (quantitative pathogenicity) of each pathogen population to sympatric and allopatric hosts in a reciprocal cross-inoculation experiment. There was no evidence for specific host adaptation in this pathosystem. At both local and regional scales, the distribution of aggressiveness fits a pattern of adaptation to the most common host genotype. Our observations support the theoretical predictions that large pathogen dispersal rates and genetic drift, revealed by the comparisons of the genotypic structures of the populations tested, can lead to a local adaptation pattern detectable only at a large spatial scale. The unravelling of adaptive patterns at different spatial scales can be used for a more efficient management of the disease.

Does selection by resistant hosts trigger local adaptation in plant-pathogen systems?

Understanding the consequences of selection by host resistance on pathogen population structure provides useful insights into the dynamics of host-parasite co-evolution processes and is crucial for effective disease management through resistant cultivars. We tested general vs. local population adaptation to host cultivars, by characterizing a French collection of Phytophthora infestans (the causal organism of potato late blight) sampled during two consecutive years on cultivars exhibiting various levels of resistance. Local populations were structured by the host for virulence (qualitative pathogenicity) but also for aggressiveness (quantitative pathogenicity). All populations had a low genotypic diversity for amplified fragment length polymorphisms (AFLPs), and presumably consisted of a few closely related clonal lineages. No correlation was detected between pathogenicity traits and AFLP genotypes. The data support the hypothesis of general adaptation for aggressiveness, to which directional selection for virulence is superimposed when race-specific resistance is introduced.