Abstract
The plant hormones salicylic acid (SA), also known as plant aspirin, and jasmonic acid (JA) play major roles in the regulation of the plant immune system. In general, SA is important for defense against pathogens with a biotrophic lifestyle, whereas JA is essential for defense against insect herbivores and pathogens
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with a necrotrophic lifestyle. Antagonistic and synergistic interactions between the SA- and JA-dependent signaling pathways allow the plant to fine-tune the activation of defenses, depending on the type of attackers that they are encountering. In the model plant Arabidopsis thaliana, SA-mediated suppression of JA signaling (SA/JA crosstalk) dominates the antagonistic interaction between the two pathways. In this thesis we uncovered an important molecular mechanism underlying SA/JA crosstalk in plants. To this end, we systematically searched for targets of SA in the JA signaling pathway. Using Arabidopsis plantsthat were completely blocked in JA synthesis, we demonstrated that the antagonistic effect of SA on JA signaling must act at a target in the JA pathway downstream of JA biosynthesis. Moreover, we showed that suppression of the JA pathway by SA functions downstream of the E3 ubiquitin-ligase SCFCOI1 complex that targets JASMONATE ZIM-domain transcriptional repressor proteins (JAZs) for proteasome-mediated degradation. Analysis of the 1-kb promoter regions of genes that were induced by MeJA and suppressed by SA revealed an overrepresentation of the JA-responsive GCC-box motif in the promoters of these genes. Importantly, this motif was shown to be a sufficient element for SA-mediated suppression of JA-responsive gene expression. Furthermore, SA was shown to have a negative effect on the accumulation the GCC-box-binding AP2/ERF transcription factor ORA59, which is an activator of JA-responsive plant defense genes. Together, these data demonstrated that the SA pathway inhibits JA signaling downstream of the SCFCOI1-JAZ complex by targeting GCC-box motifs in JA-responsive promoters via a negative effect of SA on the transcriptional activator ORA59. In addition, we searched for putative SA-inducible transcriptional repressors that mediate suppression of JA-dependent transcription via the GCC-box. The GCC-box is a binding site for AP2/ERF transcription factors, and SA activated the expression of several of the AP2/ERF encoding genes, including AP2/ERFs with an EAR repression domain. However, by loss-off-function mutant analysis of several AP2/ERF genes, we showed that SA is unlikely to target the JA signaling pathway through SA-mediated activation of AP2/ERFs. Finally, we investigated the reciprocal antagonistic effect of the JA signaling pathway on the SA response using the JA-mimicking phytotoxin coronatine of the bacterial pathogen Pseudomonas syringae and MeJA as activators of the JA pathway. We observed that although exogenously applied coronatine and MeJA have both the potential to suppress SA-responsive gene expression, their ability to do so depends greatly on the environmental conditions and the developmental stage of the plant. Detailed knowledge of the plant immune signaling network and its actors will significantly increase our understanding of the ability of plants to defend themselves against the plethora of hazardous pathogens and insects in their environment, and contribute to the development of sustainable solutions for crop protection and plant health.
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