Abstract
Jasmonic acid (JA) is a critical hormonal regulator of plant growth and defense. To advance our understanding of the architecture and dynamic regulation of the JA gene regulatory network, we performed a high-resolution RNA-seq time series of methyl JA-treated Arabidopsis thaliana at 15 time points over a 16-h period. Computational analysis showed that methyl JA (MeJA) induces a burst of transcriptional activity, generating diverse expression patterns over time that partition into distinct sectors of the JA response targeting specific biological processes. The presence of transcription factor (TF) DNA binding motifs correlated with specific TF activity during temporal MeJA-induced transcriptional reprogramming. Insight into the underlying dynamic transcriptional regulation mechanisms was captured in a chronological model of the JA gene regulatory network. Several TFs, including MYB59 and bHLH27, were uncovered as early network components with a role in pathogen and insect resistance. Analysis of subnetworks surrounding the TFs ORA47, RAP2.6L, MYB59, and ANAC055, using transcriptome profiling of overexpressors and mutants, provided insights into their regulatory role in defined modules of the JA network. Collectively, our work illuminates the complexity of the JA gene regulatory network, pinpoints and validates previously unknown regulators, and provides a valuable resource for functional studies on JA signaling components in plant defense and development.
Highlights
In nature, plants are subject to attack by a broad range of harmful pests and pathogens
Genes that were significantly differentially expressed after MeJA treatment compared with mock were identified using a generalized linear model with a log link function and a negative binomial distribution. Within this model we considered both the time after treatment and the treatment itself as factors
Future use of these time-series data could include integration with additional transcriptome data across diverse environmental conditions, together with other “omics” data sets, which will aid in building a comprehensive picture of the jasmonic acid (JA) response
Summary
Plants are subject to attack by a broad range of harmful pests and pathogens. In response to pathogen or insect attack, bioactive JA-Ile is synthesized and promotes the formation of the coreceptor complex of JAZ (via its Jas domain) with CORONATINE INSENSITIVE1 (COI1), the F-box protein of the E3 ubiquitin-ligase Skip-Cullin-F-box complex SCFCOI1. Upon perception of JA-Ile, JAZ repressor proteins are targeted by SCFCOI1 for ubiquitination and subsequent proteasomal degradation (Chini et al, 2007; Thines et al, 2007; Sheard et al, 2010). This degradation leads to the release of the JAZ-mediated repression of TFs and to subsequent induction of JA-responsive gene expression
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