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

Abstract

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 deeper 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), sampled at 14 time points over a 16-h period. We found that approximately one-third of the Arabidopsis genome was differentially expressed in response to SA, and temporal changes in gene expression could be partitioned into 45 distinct clusters of process-specific coregulated genes, linked 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 gene regulatory network model of the SA response, recovering known regulators and identifying novel ones. We found that 12% of SA-responsive genes and 69% of the MeJA-responsive genes exhibited antagonistic or synergistic expression levels in the combination treatment. Multi-condition co-clustering of the single-and combined-hormone expression profiles predicted underlying regulatory mechanisms in signal integration. Finally, we identified the TFs ANAC061 and ANAC090 as negative regulators 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, serving as a valuable resource for systems-level network studies and functional plant defense studies.

Multiple levels of crosstalk in hormone networks regulating plant defense

“…Such an approach facilitates our understanding of the temporal information flow through the different sectors of the individual hormone regulatory networks, including the interactions with sectors of other hormone networks. This approach was taken for JA (Hickman et al ., 2017; Zander et al ., 2020), the JA mimic phytotoxin (of P. syringae ) coronatine (Attaran et al ., 2014), SA (Hickman et al ., 2019), ET (Chang et al ., 2013) and ABA (Song et al ., 2016), which followed up on seminal time series papers studying responses to pathogen infection (Windram et al ., 2012; Lewis et al ., 2015).…”

“…An important role for MYC2 and MYC3 in modulation of other hormone pathways was demonstrated by the finding that 37–59% of genes that are annotated as being part of other hormone signaling pathways were bound by MYC2 and MYC3 and that their transcription responded to the MeJA treatment. Furthermore, the JA‐induced transcriptional repressor STZ was predicted to suppress genes from several other hormone pathways, including the SA, gibberellin (GA) and brassinosteroid (BR) pathways (Hickman et al ., 2019; Zander et al ., 2020).…”

“…In a follow‐up paper of the Hickman et al . (2017) paper on individual MeJA treatment, another part of the same experiment was reported, for which plants received a single SA treatment or a combination treatment of MeJA with SA (Hickman et al ., 2019). The single SA treatment had a greater impact on the transcriptome than the single MeJA treatment, affecting the expression of more genes and having more prolonged effects.…”

“…The classical example of crosstalk in defense regulation is that between the SA and JA pathways. Antagonism between these two pathways is the most studied and prevalent form, although large‐scale additive and synergistic interactions have been described as well (Hickman et al ., 2019). Additionally, the ERF branch and the MYC branch of the JA pathway have been reported to repress each other (Pieterse et al ., 2012; Gimenez‐Ibanez and Solano, 2013; Wasternack and Hause, 2013).…”

Transcriptional reprogramming during effector/flg22-triggered immune is independent of defense phytohormone signaling networks

“…Genome-wide transcriptional profiling has become an instrumental resource and is widely in plant immunity researches (Attaran et al, 2014;Lewis et al, 2015;Hickman et al, 2017;Hillmer et al, 2017;Mine et al, 2018;Hickman et al, 2019;Zhang et al, 2020a). Many genes related to plant defense are initially identified through traditional differential expression approaches.…”