A Suppressor/Avirulence Gene Combination in Hyaloperonospora arabidopsidis Determines Race Specificity in Arabidopsis thaliana

The pathosystem of Arabidopsis thaliana and diploid biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa) has been a model for investigating the molecular basis of Flor's gene-for-gene hypothesis. The isolates Hpa-Noks1 and Hpa-Cala2 are virulent on Arabidopsis accession RMX-A02 whilst an F(1) generated from a cross between these two isolates was avirulent. The F(2) progeny segregated 3,1 (avirulent, virulent), indicating a single major effect AVR locus in this pathogen. SNP-based linkage mapping confirmed a single AVR locus within a 14 kb map interval containing two genes encoding putative effectors. The Hpa-Cala2 allele of one gene, designated H. arabidopsidis cryptic1 (HAC1), encodes a protein with a signal peptide and an RxLR/dEER motif, and triggers a defense response in RMX-A02. The second gene is heterozygous in Hpa-Cala2. One allele, designated Suppressor of HAC1(Cala2) (S-HAC1(Cala2)) encodes a protein with a signal peptide and a dKEE motif with no RxLR motif; the other allele (s-hac1 (Cala2)) encodes a protein with a signal peptide, a dEEE motif and is divergent in sequence from the S-HAC1(Cala2) allele. In selfed progeny from Hpa-Cala2, dominant S-HAC1(Cala2) allele carrying progeny correlates with virulence in RMX-A02, whereas homozygous recessive s-hac1(Cala2) carrying progeny were avirulent. Genetic investigations suggested other heterozygous suppressor loci might exist in the Hpa-Cala2 genome.