A Rare Recombination in the Phytophthora sojae Genome Allows the Redefinition of a Major Avirulence Gene

Significant yield losses in soybean production are imputable to Phytophthora root and stem rot (PRR) caused by Phytophthora sojae. Resistance to PRR relies on resistance genes (Rps) that recognize key effectors from the pathogen, which are encoded by avirulence genes (Avr). Key Avr haplotypes can be monitored in natural P. sojae populations and exploited to predict which resistance gene can be deployed to provide protection to the soybean crop. In this study, we reassessed the identity of the avirulence gene whose protein product is recognized by Rps6. Following extensive soil sampling and single-spore isolation of a large population of P. sojae, we found two salient isolates carrying a rare recombination between the closely linked effectors Avr3c and Avr4/6. Using a PCR assay and molecular markers, we showed that only allelic variations at the Avr3c locus were in perfect association with the phenotypes of the isolates on Rps3c, Rps4 and Rps6 resistance. Consistent with these findings, a soybean protoplast cell-death assay further showed that only Avr3c, and not Avr4/6, triggered Rps6-dependent recognition. Furthermore, whole-genome resequencing and de novo assembly of the two isolates revealed the full extent of this genomic rearrangement. Together, these results establish Avr3c as the bona fide avirulence gene corresponding to Rps6 and offer a more reliable target for the pathotyping of P. sojae, which ultimately leads to a better deployment of resistant soybean cultivars.