Effector-Triggered Immune Response in Arabidopsis thaliana Is a Quantitative Trait

Abstract

We identified loci responsible for natural variation in Arabidopsis thaliana (Arabidopsis) responses to a bacterial pathogen virulence factor, HopAM1. HopAM1 is a type III effector protein secreted by the virulent Pseudomonas syringae strain Pto DC3000. Delivery of HopAM1 from disarmed Pseudomonas strains leads to local cell death, meristem chlorosis, or both, with varying intensities in different Arabidopsis accessions. These phenotypes are not associated with differences in bacterial growth restriction. We treated the two phenotypes as quantitative traits to identify host loci controlling responses to HopAM1. Genome-wide association (GWA) of 64 Arabidopsis accessions identified independent variants highly correlated with response to each phenotype. Quantitative trait locus (QTL) mapping in a recombinant inbred population between Bur-0 and Col-0 accessions revealed genetic linkage to regions distinct from the top GWA hits. Two major QTL associated with HopAM1-induced cell death were also associated with HopAM1-induced chlorosis. HopAM1-induced changes in Arabidopsis gene expression showed that rapid HopAM1-dependent cell death in Bur-0 is correlated with effector-triggered immune responses. Studies of the effect of mutations in known plant immune system genes showed, surprisingly, that both cell death and chlorosis phenotypes are enhanced by loss of EDS1, a regulatory hub in the plant immune-signaling network. Our results reveal complex genetic architecture for response to this particular type III virulence effector, in contrast to the typical monogenic control of cell death and disease resistance triggered by most type III effectors.

Diverse mechanisms of resistance to Pseudomonas syringae in a thousand natural accessions of Arabidopsis thaliana

“…Therefore, HopAM1 recognition in Xan‐2 and Xan‐5 seems to be involved in a weak ETI‐like response. A quantitative nature of the cell death response after HopAM1 bacterial delivery was recently reported in 98 Arabidopsis accessions (Iakovidis et al ., ). However, even though deletion of hopAM1 slightly increased bacterial growth in strong ETI‐like accession Bur‐0 (an accession evaluated in our screen that, unlike Xan‐2 and Xan‐5, was susceptible to Pst DC3000 infection), no correlation was found between the accelerated cell death response and disease resistance, as the same effect of increased bacterial growth for a strain lacking hopAM1 was observed after infection of both Col‐0 and Bur‐0 (Iakovidis et al ., ).…”

TIR-only protein RBA1 recognizes a pathogen effector to regulate cell death inArabidopsis

“…Pto DC3000 containing HopBA1 is still growth restricted on Col-0, indicating a decoupling of cell death and disease resistance. Decoupling of cell death and disease resistance has been previously reported (47)(48)(49). HopBA1 is not present naturally in Pto DC3000, so better understanding its contribution to disease resistance might require future studies in its endogenous strains (P. syringae pv.…”

The genetic background modulates the intensity of Rpv3‐dependent downy mildew resistance in grapevine

“…ETI has long been considered a monogenic trait in model species, a notion recently challenged by Iakovidis et al. (). These authors showed that cell death in 98 accessions of Arabidopsis in the response to a Pseudomonas syringae effector has a quantitative nature, exhibiting variation in timing of appearance and strength of the response.…”