The kinetics and basal levels of the transcriptome response during Effector-Triggered Immunity in Arabidopsis are mainly controlled by four immune signaling sectors

Abstract

To observe the transcriptome response during Effector-Triggered Immunity (ETI) without complications from any other pathogen factors or heterogeneously responding cell populations, we transgenically and conditionally expressed the Pseudomonas syringae effector AvrRpt2 in Arabidopsis leaves. We studied this ETI-specific, cell-autonomous transcriptome response in 16 exhaustively combinatorial genetic backgrounds for the jasmonate (JA), ethylene (ET), PAD4, and salicylate (SA) immune signaling sectors. Removal of some or all four sectors had relatively small impacts on the intensity of the overall ETI transcriptome response (1972 upregulated and 1290 downregulated genes). Yet, we found that the four signaling sectors strongly affect the kinetics of the ETI transcriptome response based on analysis of individual genes via time-course modeling and of the collective behaviors of the genes via a PCA-based method: the PAD4 sector alone and the JA;SA sector interaction (defined by the averaging model) accelerated the response, while the ET;SA sector interaction delayed it. The response acceleration by the PAD4 sector or the JA;SA sector interaction was consistent with their positive contributions to ETI measured by pathogen growth inhibition. The responsive genes overlapping between ETI and Pattern-Triggered Immunity (PTI) had distinct regulatory trends regarding the four sectors, indicating different regulatory circuits in upstream parts of ETI and PTI signaling. The basal mRNA levels of most ETI-upregulated genes, but not downregulated genes, were predominantly positively regulated by the PAD4;SA sector interaction. This detailed mechanistic decomposition of the roles of four signaling sectors allowed us to propose a potential regulatory network involved in ETI signaling.