Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana

Abstract

Network robustness is a crucial property of the plant immune signaling network because pathogens are under a strong selection pressure to perturb plant network components to dampen plant immune responses. Nevertheless, modulation of network robustness is an area of network biology that has rarely been explored. While two modes of plant immunity, Effector-Triggered Immunity (ETI) and Pattern-Triggered Immunity (PTI), extensively share signaling machinery, the network output is much more robust against perturbations during ETI than PTI, suggesting modulation of network robustness. Here, we report a molecular mechanism underlying the modulation of the network robustness in Arabidopsis thaliana. The salicylic acid (SA) signaling sector regulates a major portion of the plant immune response and is important in immunity against biotrophic and hemibiotrophic pathogens. In Arabidopsis, SA signaling was required for the proper regulation of the vast majority of SA-responsive genes during PTI. However, during ETI, regulation of most SA-responsive genes, including the canonical SA marker gene PR1, could be controlled by SA-independent mechanisms as well as by SA. The activation of the two immune-related MAPKs, MPK3 and MPK6, persisted for several hours during ETI but less than one hour during PTI. Sustained MAPK activation was sufficient to confer SA-independent regulation of most SA-responsive genes. Furthermore, the MPK3 and SA signaling sectors were compensatory to each other for inhibition of bacterial growth as well as for PR1 expression during ETI. These results indicate that the duration of the MAPK activation is a critical determinant for modulation of robustness of the immune signaling network. Our findings with the plant immune signaling network imply that the robustness level of a biological network can be modulated by the activities of network components.

Pathogen exploitation of an abscisic acid- and jasmonate-inducible MAPK phosphatase and its interception by Arabidopsis immunity

“…The phosphorylation status of MPK3 and MPK6 changes dynamically during pathogen infection (16)(17)(18)(19). In search of a regulator of MAPK activation during immunity, we found that an ABA-deficient mutant, aba2, shows enhanced activation of MPK3 and MPK6 after treatment with flg22, a bacterial MAMP (Fig.…”

“…Here, we show that the transcriptional induction of HAI1 and the HAI1-dependent immune suppression by COR are prevented upon ETI activation, demonstrating that ETI overcomes pathogen targeting of MAPKs. Interception of JA signaling during ETI may also be relevant to sustained MAPK activation (17), as well as to inhibition of CORmediated stomatal reopening (37).…”

“…Seedlings of A. thaliana, C. rubella, and E. salsugineum were grown on solidified half-strength Murashige and Skoog medium supplemented with 1% sucrose under a 10-h light period at 22°C. MAPK assays were carried out essentially as described (17,29). Bacterial growth assays, RT-qPCR, ChIP-qPCR, and phylogenetic analysis were performed as described (34).…”

“…A possible explanation for this observation is that ETI blocks activation of JA signaling by COR. We tested this possibility using A. thaliana lines carrying an estradiol-inducible AvrRpt2 transgene (XVE-AvrRpt2) (17). XVEAvrRpt2 seedlings were treated with estradiol for 6 h, followed by mock or COR treatment for 1 h. Induction of HAI1 and another JA-responsive gene, VSP2, was significantly lower in the wild type than in the rps2 mutant background but comparable between the wild-type and the SA-deficient sid2 mutant background (Fig.…”

Plastic Transcriptomes Stabilize Immunity to Pathogen Diversity: The Jasmonic Acid and Salicylic Acid Networks within the Arabidopsis/Botrytis Pathosystem

“…As both npr1-1 and coi1-1 block perception of SA and JA respectively, this is not caused by fungus exogenously producing the hormone to attenuate host defenses. Instead, these individual isolates suggest that these classical JA-and SA-specific transcripts can be stimulated by alternative pathways (Sato et al, 2010;Tsuda et al, 2013;Kim et al, 2014). Thus, these specific isolates can provide unique tools to query previously unrecognized defense signaling pathways.…”