The Arabidopsis WRR4A and WRR4B paralogous NLR proteins both confer recognition of multiple Albugo candida effectors
The oomycete Albugo candida causes white blister rust, an important disease of Brassica crops. Distinct races of A. candida are defined by their capacity to infect different host plant species. Each A. candida race encodes secreted proteins with a CX2 CX5 G ("CCG") motif that are polymorphic and show presence/absence variation, and are thus candidate effectors. The White Rust Resistance 4 (WRR4) locus in Arabidopsis thaliana accession Col-0 contains three genes that encode intracellular NLR immune receptors. The Col-0 alleles of WRR4A and WRR4B confer resistance to multiple A. candida races, though both WRR4A and WRR4B can be overcome by the Col-0-virulent race 4 isolate AcEx1. Comparison of CCG candidate effectors in avirulent and virulent races, and transient co-expression of CCG effectors from four A. candida races in Nicotiana sp. or A. thaliana, revealed CCG effectors that trigger WRR4A- or WRR4B- dependent hypersensitive responses (HR). We found eight WRR4A-recognized CCGs and four WRR4B-recognized CCGs, the first recognized proteins from A. candida for which the cognate immune receptors in Arabidopsis thaliana are known. This multiple recognition capacity potentially explains the broad-spectrum resistance to several A. candida races conferred by WRR4 paralogs. We further show that of five tested CCGs, three confer enhanced disease susceptibility when expressed in planta, consistent with A. candida CCG proteins being effectors.