Soft selective sweeps in fungicide resistance evolution: recurrent mutations without fitness costs in grapevine downy mildew

Abstract

Adaptation produces hard or soft selective sweeps depending on the supply of adaptive genetic polymorphism. The evolution of pesticide resistance in parasites is a striking example of rapid adaptation that can shed light on selection processes. Plasmopara viticola, which causes grapevine downy mildew, forms large populations, in which resistance has rapidly evolved due to excessive fungicide use. We investigated the pathways by which fungicide resistance has evolved in this plant pathogen, to determine whether hard or soft selective sweeps were involved. An analysis of nucleotide polymorphism in 108 field isolates from the Bordeaux region revealed recurrent mutations of cytb and CesA3 conferring resistance to quinone outside inhibiting (QoI) and carboxylic acid amide (CAA) fungicides, respectively. Higher levels of genetic differentiation were observed for nucleotide positions involved in resistance than for neutral microsatellites, consistent with local adaptation of the pathogen to fungicide treatments. No hitchhiking was found between selected sites and neighbouring polymorphisms in cytb and CesA3, confirming multiple origins of resistance alleles. We assessed resistance costs, by evaluating the fitness of the 108 isolates through measurements of multiple quantitative pathogenicity traits under controlled conditions. No significant differences were found between sensitive and resistant isolates, suggesting that fitness costs may be absent or negligible. Our results indicate that the rapid evolution of fungicide resistance in P. viticola has involved a soft sweep.

A time‐course investigation of resistance to the carboxylic acid amide mandipropamid in field populations of Plasmopara viticola treated with anti‐resistance strategies

“…The fluctuations in the allelic composition at the PvCesA3 ‐1105 codon were observed in all the plots, indicating that the pathogen population changes over time in a manner that is independent of the treatment but probably influenced by the environment and/or changes in the fitness properties of the strains harboring these alleles. In a recent study, carried out on an large number of isolates with different allelic compositions at the PvCesA3 ‐1105 codon, no differences in fitness costs were found between the molecular profiles associated with sensitivity and resistance to CAAs . The authors, however, did not completely exclude the presence of fitness costs, suggesting that they could be better estimated by considering the whole life cycle of the pathogen.…”

“…Sensitivity monitoring is required as a consequence of the combined risks from the interaction of the individual components of resistance, such as fungicide risk, the polycyclic nature of the pathogen, sexual reproduction and the intensive application of the CAA fungicides in most vineyards. Currently, P. viticola strains resistant to CAAs have been detected in Japan, India and European countries including Italy and France . The CAA class was chosen in the present study because it is under strong selection pressure and the resistance mechanism is well established and has interesting features linked to the inheritance traits.…”

“…Homozygous strains carrying the wild‐type allele PvCesA3 ‐1105G and heterozygous strains carrying the PvCesA3 ‐1105G allele and the resistant alleles PvCesA3 ‐1105S/V express a sensitive phenotype to CAAs, whereas homozygous strains with either the PvCesA3 ‐1105S or PvCesA3 ‐1105V allele are phenotypically resistant. Recently, CAA‐resistant heterozygous strains bearing the PvCesA3 ‐1105S and PvCesA3 ‐1105V alleles were identified . Sensitivity monitoring through molecular quantification of CAA resistance allele frequency provides useful information on the population composition; however, it is difficult to interpret the results given the recessive inheritance of resistance.…”

“…Currently, P. viticola strains resistant to CAAs have been detected in Japan, India and European countries including Italy and France. [20][21][22][23] The CAA class was chosen in the present study because it is under strong selection pressure and the resistance mechanism is well established and has interesting features linked to the inheritance traits. CAA fungicides inhibit cellulose biosynthesis 24 and the molecular mechanism of resistance relies on G1105S and G1105V mutations in the cellulose synthase PvCesA3 gene.…”

“…Recently, CAA-resistant heterozygous strains bearing the PvCesA3-1105S and PvCesA3-1105V alleles were identified. 23 Sensitivity monitoring through molecular quantification of CAA resistance allele frequency provides useful information on the population composition; 26 however, it is difficult to interpret the results given the recessive inheritance of resistance. As a consequence, bioassays and molecular analysis are both needed to estimate the risk of practical field resistance.…”