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

Abstract

Globodera pallida poses a major threat to potato production, with management strategies primarily relying on genetic resistance. However, reports from multiple locations in Western Europe indicate a steady increase in virulence levels among field populations, raising major concerns about G. pallida control. The evolutionary mechanisms driving this rise in virulence are poorly understood. To investigate this, we analysed the propagation of thirteen recently isolated field populations on thirty commercial potato varieties over four independent PCN resistance tests. Our findings indicate that (1) the genetic basis of resistance in potatoes is small, with the major resistance conferred by GpaV from Solanum vernei, and (2) the wide application of GpaVvrn has led to continuous selection on standing genetic variation in G. pallida field populations. To map virulence, we propagated two field populations on a GpaVvrn-resistant variety for four consecutive generations. High-coverage whole-genome sequencing of each generation revealed that GpaVvrn-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 G. pallida virulence on a GpaVvrn-resistant potato variety but had no effect on nematode virulence on a susceptible variety. Thereby classifying Gp-pat-1 as an avirulence gene and confirming its role in the breakdown of GpaVvrn-resistance. These findings demonstrate that negative selection on the Gp-pat-1 avirulence allele by GpaVvrn-mediated resistance is driving the emergence of virulence in the G. pallida field populations used in our selection experiments. Our results therefore strongly suggest that selection on Gp-pat-1 is likely underlying the current outbreak of GpaVvrn-resistance breaking populations. Our results provide a foundation for the development of molecular diagnostic tools to monitor virulence in field populations, to enhance understanding of resistance breakdown, and to inform the sustainable deployment of resistances in the field. SIGNIFICANCE STATEMENTIn Western Europe, management of the potato cyst nematode Globodera pallida primarily relies on genetic resistances in potato plants. However, resistance-breaking populations are emerging across Western Europe. Here, we identify a single resistance locus shared by all tested resistant potato varieties. We also identify a corresponding virulence locus on a newly assembled G. pallida reference genome and identify a gene within this locus that contributes to virulence. Our findings provide critical insights into the selective pressure acting on this plant-parasitic nematode, the emergence of virulence over time, and the molecular mechanism underlying resistance breakdown. These results provide much needed insights into a highly adapted soil-borne plant-pathogen.