Cross-talk in plant defense signaling: Antagonism between salicylate and jasmonate pathways in Arabidopsis

Abstract

Plants are equipped with an array of defense mechanisms to protect themselves against herbivorous insects and microbial pathogens. Some are pre-existing while others are only activated upon insect attack or pathogen invasion. However, induced defense responses entail fitness costs. Therefore, plants possess elaborate regulatory mechanisms that efficiently coordinate activation of attacker-specific defenses. A major focus in plant defense signaling research is to uncover key mechanisms by which plants tailor their responses to different attackers, and to investigate how plants cope with simultaneous interactions with multiple aggressors. The phytohormones salicylic acid (SA) and jasmonic acid (JA) play a major role in the regulation of induced defense mechanisms against biotrophic pathogens and insect herbivores, respectively. Cross-talk between SA and JA defense signaling pathways is thought to allow fine-tuning of the defense response to the attacker encountered. In Arabidopsis, pharmacological experiments revealed that SA exerts a strong antagonistic effect on JA-responsive genes, such as PLANT DEFENSIN1.2 (PDF1.2), indicating that the SA pathway can be prioritized over the JA pathway. This antagonistic effect of SA on JA signaling is a robust phenomenon: It is conserved among Arabidopsis accessions, and JA-responsive gene expression is readily suppressed by SA for several days, even when triggered by very low doses of SA. Time interval studies revealed that SA has a window of opportunity to suppress MeJA-responsive gene expression, and that this time interval correlates with the SA-induced redox change in the plant tissue. Thus, redox modulation is likely to play a central role in the regulatory mechanism underlying SA/JA cross-talk. Analysis of the Arabidopsis mutant npr1, impaired in SA signal transduction, revealed that the antagonistic effect of SA on JA signaling requires the regulatory protein NPR1. Nuclear localization of NPR1, which is essential for SA-mediated defense gene expression, is not required for suppression of JA-responsive genes, indicating that cross-talk between SA and JA is modulated through a function of NPR1 in the cytosol. TGA transcription factors are similarly required for both SA-dependent gene expression and SA-mediated suppression of JA signaling. However, TGA factors are unlikely to exert their effect through direct interaction with the promoter of JA-responsive genes such as PDF1.2, as removal of the TGA binding site in this promoter did not affect cross-talk. Promoter analysis of SA-suppressed, MeJA-inducible cross-talk genes revealed enrichment of the I box and the GCC box motif. Site-directed mutagenesis of the I box motif in the PDF1.2 promoter did not affect suppression of this gene by SA, indicating that the I box is not essential in mediating cross-talk. The role of the GCC box in cross-talk regulation should be further elucidated. This motif is required for MeJA-responsiveness in the PDF1.2 promoter, and thus provides an attractive target for SA-mediated suppression. Collectively, this work provides novel insight into how plants regulate their defense response upon attack by multiple aggressors, and may prove valuable for the development of novel strategies for crop protection.