Virulence gains in the Puccinia striiformis f. sp. tritici PstS10 lineage correlate with expression polymorphism in a candidate Avr effector

Wheat yellow rust - caused by Puccinia striiformis f. sp. tritici (Pst) - is the most damaging wheat rust in Europe, where three distinct races (Kalmar, Amboise and Benchmark) recently became prevalent. Herein, comparative genomic analysis and pathology-based race profiling showed these races evolved from diversification in the PstS10/Warrior(-) lineage. Additionally, transcriptomic profiling indicated that gain of virulence in Kalmar and Amboise Pst isolates is seemingly associated with loss of expression of a single gene, PST130_P495001; Kalmar and Amboise Pst isolates lack PST130_P495001 expression, whereas Pst isolates from Benchmark retain high expression. PST130_P495001 exhibits typical characteristics of an effector. Furthermore, examination of PST130_P495001 across global Pst isolates revealed high sequence conservation, with complete loss of expression exceptionally rare (11 of 888 Pst datasets). Pst field isolates with low PST130_P495001 expression were also found on wheat varieties with shared parentage, which only exhibited high infection levels with Kalmar-derived Pst isolates lacking PST130_P495001 expression. These findings support PST130_P495001 as a candidate avirulence effector, pending further validation once the corresponding resistance gene, likely within this shared lineage, is identified. They also suggest that loss of expression may have contributed to virulence gains in the PstS10 lineage, to overcome resistance shared by these related varieties.