Heterozygosity Plays a Key Role in Pathogenicity of Hyaloperonospora arabidopsidis

Fungal and oomycete pathogens are causal agents of many important plant diseases affecting crops that are staple foods for human and livestock. These pathogens secrete thousands of effector molecules to manipulate plants for their own advantage. A class of cytoplasmic effectors from oomycete pathogens contain RxLR and dEER motifs that enable translocation of these effectors into the host cell. Using the Hyaloperonospora arabidopsidis-Arabidopsis thaliana system, we investigated how a new avirulent F1 isolate arose from virulent parents. We employed pathogen genetics, next generation sequencing and genome mapping, and showed that one of the parent isolates, Hpa-Cala2, contains a gene coding for an effector, designated HAC1Cala2, with a canonical signal peptide and RXLR/dEER motif, which can trigger defence in an Arabidopsis accession. However, in the same locus, there are putative heterozygous effectors, designated S-HAC1Cala2 and s-hac1 Cala2, with a signal peptide and a dKEE or dEEE motif, respectively, but no canonical RXLR motif. The presence of these effectors enables Hpa-Cala2 to be virulent on the Arabidopsis accession, indicating that the heterozygous nature of Cala2 plays an important role in the suppression/avoidance of plant defence. Further bioinformatic investigations suggested that other heterozygous loci might exist in the genome of other Hpa isolates.