Adaptation of <i>Globodera pallida</i> to Individual Components Compromises the Durability of Pyramided Resistance in Potato

The use of resistant plants is an effective alternative to chemical products. But their sustainability is often compromised by the rapid adaptation of pathogen populations. For the cyst nematode <i>Globodera pallida</i>, a major parasite of potato, several quantitative trait loci (QTLs) conferring resistance have been identified, but their individual use could lead to resistance breakdown. Combining several resistance loci within a single potato genotype has been proposed as a strategy to improve both efficacy and durability. However, the evolutionary pathways leading to the circumvention of this pyramidal resistance remain unknown. The combination of experimental evolution, phenotyping and genome scan enabled us to study the genomic basis of <i>G. pallida</i> adaptation to individual (<i>GpaV</i> _<i>spl</i> , <i>GpaXI</i> _<i>spl</i> ) and pyramidal (<i>GpaV + XI</i> _<i>spl</i> ) resistance QTLs. Experimental evolution over 10 generations revealed that adaptation to <i>GpaV + XI</i> _<i>spl</i> pyramidal resistance was more difficult than to individual QTLs, but was nevertheless possible. Genomic analyses identified distinct regions under selection for each resistance, with a strong overlap between the adaptation to <i>GpaV</i> _<i>spl</i> and to <i>GpaV + XI</i> _<i>spl</i> , but a weaker overlap between the adaptation to <i>GpaXI</i> _<i>spl</i> and to the pyramidal resistance. Known effector genes involved in immune suppression were systematically found in the selected regions, confirming their potential role in virulence. In addition, a two-generations experiment demonstrated that prior adaptation, particularly to <i>GpaV</i> _<i>spl</i> , facilitated adaptation to pyramidal resistance. These results highlight the existence of preferential evolutionary trajectories favored by genomic proximity between nematode lineages adapted to different resistances. Our results show that pyramidal resistance can be compromised by the prior deployment of its individual components, and underline the importance of taking evolutionary pathways into account in resistance deployment.