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

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.

适应性演化可产生硬选择清扫（hard selective sweep）与软选择清扫（soft selective sweep）两种模式，具体取决于适应性遗传多态性的供应情况。寄生虫的抗药性演化是快速适应性演化的典型范例，可为解析选择过程提供关键视角。引发葡萄霜霉病的葡萄霜霉菌（Plasmopara viticola）种群规模庞大，受杀菌剂过量使用的影响，其抗药性已快速演化。本研究针对该植物病原菌的杀菌剂抗药性演化路径展开探究，以明确其抗药性演化是否涉及硬选择清扫或软选择清扫模式。对采自波尔多地区的108株野外分离株进行核苷酸多态性分析后发现，细胞色素b基因（cytb）与纤维素合酶3基因（CesA3）分别存在可赋予菌株对醌外抑制剂（QoI）类与羧酸酰胺（CAA）类杀菌剂抗性的反复突变。相较于中性微卫星位点，与抗性相关的核苷酸位点呈现出更高水平的遗传分化，这与该病原菌针对杀菌剂处理的本地适应性演化结果相符。在细胞色素b基因与纤维素合酶3基因的受选择位点与邻近多态性位点之间未检测到遗传搭车现象，这证实了抗性等位基因存在多重起源。本研究通过在可控条件下测定108株分离株的多项定量致病性性状，以此评估抗药性的适合度代价。敏感菌株与抗性菌株之间未发现显著性状差异，这表明抗药性的适合度代价可能不存在或可忽略不计。本研究结果表明，葡萄霜霉菌（P. viticola）杀菌剂抗药性的快速演化涉及软选择清扫模式。