Susceptibility Factor BWS1 Encoded by NLR Gene Negatively Regulates SGT1-mediated Plant Immunity

On April 25, 2023, Plant Communications published online a paper entitled "An atypical NLR gene confers bacterial wilt susceptibility in Arabidopsis" by Fabienne Vailleau's team at the University of Toulouse, INRAE and CNRS, and their collaborators. This study discovered an NLR gene BWS1 involved in plant immunity that negatively regulates SGT1-mediated immune responses as a direct target of RipAC, a susceptibility factor and effector protein of plant immunity.

Currently, quantitative disease resistance (QDR) is still the most prevalent form of plant resistance in both farmland and wild environments. Previous studies have found that pathogen-associated molecular patterns (PAMP)-triggered immunity (PTI) and effector protein-triggered immunity (ETI) are not independent of each other and cannot be used to distinguish plant-pathogen interactions. It is because of QDR that researchers have a greater understanding of the role of PAMPs and effectors and of the interacting plant responses, from resistance to susceptibility. The disease resistance of plants is dynamic and continuous, and its symptoms are not simply presence/absence.

Genome-wide association studies (GWAS) can effectively decipher the genetic architecture of complex traits in plants, including QDRs. To reveal the genetic relationship between QDR and the bacterial pathogen Ralstonia solanacearum, this study first performed GWAS analysis on an Arabidopsis thaliana core collection of 25 accessions using 47 R. solanacearum type III effector (T3E) mutants to identify key pathogenicity determinants. Through preliminary analysis, the researchers decided to select four of the mutants (ripAC, ripAG, ripAQ, and ripU) for further study.

While most of the quantitative trait loci (QTL) showed high specificity for the four T3E mutants, the researchers noticed a common QTL that responded to vaccination of all four T3E mutants, and this QTL has a specific NLR allele cluster with structural variation. This study functionally confirmed that one of the NLR is a susceptibility factor in the process of plant response to R. solanacearum, and named it BWS1. The wilting symptoms developed slowly in bws1 mutant plants compared to wild type.

Overexpression of NLR genes often induces hypersensitive cell death. Through the overexpression of two BWS1 alleles, this study found that they failed to induce cell death in N. benthamiana leaves, consistent with the function of its susceptibility factor. Further characterization revealed that expression of BWS1 resulted in immunosuppression triggered by different R. solanacearum effectors, strengthening the putative role of BWS1 as a susceptibility factor. In addition, the study also demonstrated the interaction between BWS1 and RipAC, and BWS1 and SGT1. BWS1 and SGT1 can directly interact to form a BWS1-SGT1 complex, and RipAC can interact with BWS1 to inhibit the formation of the BWS1-SGT1 complex.

In conclusion, this study identified an NLR gene, BWS1, as a susceptibility factor during the plant immune response through QDR-based GWAS analysis. Mutations of this factor can effectively alleviate the development of plant disease, and at the same time, BWS1 is the direct target of T3E effector protein RipAC, which can mediate the negative regulation of SGT1-dependent immune response.

Reference:

Demirjian, C., et al. An atypical NLR gene confers bacterial wilt susceptibility in Arabidopsis. Plant Commun. (2023). https://doi.org/10.1016/j.xplc.2023.100607