Integrated Multi-omic Framework of the Plant Response to Jasmonic Acid

Abstract

Understanding the systems-level actions of transcriptional responses to hormones provides insight into how the genome is reprogrammed in response to environmental stimuli. Here, we investigate the signaling pathway of the hormone jasmonic acid (JA), which controls a plethora of critically important processes in plants and is orchestrated by the transcription factor (TF) MYC2 and its closest relatives in Arabidopsis thaliana. We generated an integrated framework of the response to JA that spans from the activity of master and secondary-regulatory TFs, through gene expression outputs and alternative splicing to protein abundance changes, protein phosphorylation and chromatin remodeling. We integrated time series transcriptome analysis with (phospho)proteomic data to reconstruct gene regulatory network models. These enable us to predict previously unknown points of crosstalk from JA to other signaling pathways and to identify new components of the JA regulatory mechanism, which we validated through targeted mutant analysis. These results provide a comprehensive understanding of how a plant hormone remodels cellular functions and plant behavior, the general principles of which provide a framework for analysis of cross-regulation between other hormone and stress signaling pathways.