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Transcriptional Dynamics of the Salicylic Acid Response and its Interplay with the Jasmonic Acid Pathway

By Richard Hickman, Marciel Pereira Mendes, Marcel C. Van Verk, Anja J.H. Van Dijken, Jacopo Di Sora, Katherine Denby, Corné M. J. Pieterse, Saskia C.M. Van Wees

Posted 24 Aug 2019
bioRxiv DOI: 10.1101/742742

The phytohormone salicylic acid (SA) is a central regulator of plant immunity. Antagonistic and synergistic actions between SA and other defense-associated hormones like jasmonic acid (JA) play key roles in determining the outcome of the plant immune response. To obtain a deep understanding of SA-mediated transcriptional reprogramming and SA/JA crosstalk, we generated a high-resolution time series of gene expression from Arabidopsis leaves treated with SA alone and a combination of SA and methyl JA (MeJA). We found that approximately one-third of the Arabidopsis genome was differentially expressed in response to SA over a 16-h period, and temporal changes in gene expression could be partitioned into 45 distinct clusters of process-specific coregulated genes, which we could link to specific cis-regulatory elements and binding of transcription factors (TFs). Integration of our expression data with information on TF-DNA binding allowed us to generate a dynamic regulatory network model of the SA response, recovering known regulators and identifying novel ones. We found larges sets of SA and MeJA-responsive genes whose expression is altered with the combined treatment. Multi-condition co-clustering of the single- and combined-hormone expression profiles revealed antagonistic and synergistic effects, and predicted underlying regulatory mechanisms. Finally, we demonstrated the utility of our dataset for the identification of novel defense regulators by demonstrating a role for ANAC061 and ANAC090 in the regulation of SA-pathway genes and defense against biotrophic pathogens. Collectively, our data provide an unprecedented level of detail about transcriptional changes during the SA response and SA/JA crosstalk, and serves as a valuable resource for functional studies on SA/JA network components in plant defense.

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