The Arabidopsis WRR4A and WRR4B paralogous NLR proteins both confer recognition of multiple Albugo candida effectors

Abstract

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 CX 2 CX 5 G ('CCG') motif that are polymorphic and show presence/absence variation, and are therefore candidate effectors.The White Rust Resistance 4 (WRR4) locus in Arabidopsis thaliana accession Col-0 contains three genes that encode intracellular nucleotide-binding domain leucine-rich repeat immune receptors. The Col-0 alleles of WRR4A and WRR4B confer resistance to multiple A. candida races, although 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 coexpression 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.We found eight WRR4A-recognised CCGs and four WRR4B-recognised CCGs, the first recognised proteins from A. candida for which the cognate immune receptors in A. thaliana are known. This multiple recognition capacity potentially explains the broad-spectrum resistance to several A. candida races conferred by WRR4 paralogues. 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.

ATR2Cala2 from Arabidopsis‐infecting downy mildew requires 4 TIR‐NLR immune receptors for full recognition

“…As before, CCG28 was recognized by WRR4A, which served as a positive control (Fig. 2c) (Redkar et al ., 2023). Thus, our genetic investigations and bombardment experiments are consistent with A2C3 Cala2 being the avirulence determinant ATR2 Cala2 , and we hence refer to A2C3 Cala2 as ATR2 Cala2 .…”

“…NLR activation results in an elevated immune response, characterized by generation of reactive oxygen species, cell wall fortification, activation of defence‐associated genes and a localized cell death known as the hypersensitive response (HR) (Spoel & Dong, 2012). Many cases of matching R and Avr genes have been described (Bernoux et al ., 2011; Césari et al ., 2014; Ma et al ., 2020; Redkar et al ., 2023). However, in some examples, disease resistance against a pathogen isolate or recognition of an Avr protein requires the coordinate function of pairs of NLR genes (Eitas & Dangl, 2010).…”

WRR4B contributes to a broad‐spectrum disease resistance against powdery mildew in Arabidopsis

“…WRR4B was first characterized as an R gene against the white rust pathogen A. candida (Cevik et al., 2019 ). Four different CCG effector proteins in Ac2V have been found to be recognized by WRR4B , triggering the HR in a WRR4B ‐dependent manner in Arabidopsis and N. benthamiana (Redkar et al., 2023 ). The genome and transcriptome of O. heveae strain HO‐73 have been sequenced, revealing that 133 candidate effector proteins are present in this strain.…”

Conserved effector families of Phytophthora species drive NLR-mediated nonhost resistance in plants

“…Similar with our study, several cases of conserved effectors in both adapted and non-adapted pathogens which are recognized by similar NLRs have been reported. For instance, various CCG effectors conserved in Albugo candida races are recognized by Arabidopsis WRR4A and WRR4B 53 , Avramr1/3 homologs of multiple Phytophthora species are recognized by Rpi-amr1/3 18,52 , and multiple effector families of Pseudomonas syringae pathovars are recognized by corresponding Arabidopsis NLRs 17 . In this context, we anticipate that the homologous NLRmediated recognition of conserved effectors between the closely related plant and pathogen species would also be applied beyond the Solanaceae plants and Phytophthora species.…”