The potato cyst nematode Globodera pallida overcomes major potato resistance through selection on standing variation at a single locus

Globodera pallida poses a major threat to potato production, with management strategies primarily relying on genetic resistance. However, increasing virulence in field populations across Western Europe raises major concerns for G. pallida control. To investigate the evolutionary mechanisms driving this rise in virulence, we propagated 13 field populations on 30 commercial potato varieties. Our findings indicate that the genetic basis of resistance in potatoes is small, with the major resistance conferred by GpaV from Solanum vernei. The wide application of GpaV_vrn has led to continuous selection on standing genetic variation in G. pallida. To map virulence, we propagated two field populations on a GpaV_vrn-resistant variety for five generations. High-coverage whole-genome sequencing of each generation revealed that GpaV_vrn-mediated selection acted on a single locus of a newly assembled G. pallida Rookmaker reference genome. Examination of this virulence-associated locus identified Gp-pat-1 as a candidate gene. Silencing Gp-pat-1 increased virulence on a GpaV_vrn-resistant variety but had no effect on nematode virulence on a susceptible variety, classifying Gp-pat-1 as an avirulence gene. Our findings show that GpaV_vrn-mediated negative selection on Gp-pat-1 is driving the emergence of virulence and improves our understanding of resistance breakdown and the evolutionary dynamics of nematode adaptation in the field.