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A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels
Friday, 2019/11/22 | 08:01:23

Alex Van Moerkercke, Owen Duncan, Mark Zander, Jan Šimura, Robin Vanden Bossche,  G. Lewsey, Sbatie Lama, Karam B. Singh, Joseph R. Ecker,  A. Harvey Millar, and Olivier Van Aken

PNAS November 12, 2019 116 (46) 23345-23356

Significance

Plants are continuously exposed to mechanical manipulation by wind, rain, neighboring plants, animals, and human activities. These mechanical stimuli cause short-term molecular changes and long-term developmental effects, affecting flowering time, pathogen defence, and plant architecture. Using water spray to simulate rain, we show that jasmonic acid-signaling factors mediate rapid gene-expression changes. Nearly 300 genes are regulated by MYC2/MYC3/MYC4 transcription factors, particularly affecting the most highly responsive genes. This is controlled by induced binding and activation of water spray-inducible promoters by MYC2. We have identified a core MYC2 “regulon,” including many secondary transcription factors that in turn activate downstream promoters, creating a hierarchical transcriptional network. Finally, we demonstrate that spray-induced jasmonate accumulation is transcriptionally regulated by a MYC2/MYC3/MYC4-controlled positive-feedback loop.

Abstract

Mechanical stimuli, such as wind, rain, and touch affect plant development, growth, pest resistance, and ultimately reproductive success. Using water spray to simulate rain, we demonstrate that jasmonic acid (JA) signaling plays a key role in early gene-expression changes, well before it leads to developmental changes in flowering and plant architecture. The JA-activated transcription factors MYC2/MYC3/MYC4 modulate transiently induced expression of 266 genes, most of which peak within 30 min, and control 52% of genes induced >100-fold. Chromatin immunoprecipitation-sequencing analysis indicates that MYC2 dynamically binds >1,300 promoters and trans-activation assays show that MYC2 activates these promoters. By mining our multiomic datasets, we identified a core MYC2/MYC3/MYC4-dependent “regulon” of 82 genes containing many previously unknown MYC2 targets, including transcription factors bHLH19 and ERF109. bHLH19 can in turn directly activate the ORA47 promoter, indicating that MYC2/MYC3/MYC4 initiate a hierarchical network of downstream transcription factors. Finally, we also reveal that rapid water spray-induced accumulation of JA and JA-isoleucine is directly controlled by MYC2/MYC3/MYC4 through a positive amplification loop that regulates JA-biosynthesis genes.

 

See https://www.pnas.org/content/116/46/23345

Figure 1: The MYC2/MYC3/MYC4-dependent water spray-transcriptome. (A and B) Summary of the RNA-seq experiment in Col-0 (A) and myc234 mutant (B) lines in untreated seedlings (UT) and seedlings 25 min (25m) after mechanical stimulation by water spray. (A) 77.6% of the genes are up-regulated (sprayUP) after 25 min in Col-0, of which 10.5% encode TFs. (B) Of the fraction of genes affected by the myc234 mutations, 88.3% show reduced inducibility after water spray; 85.7% are up-regulated by spray, and 16.9% encode TFs. (CE) Heat maps representing normalized levels of water spray-responsive transcripts in Col-0 and the myc234 mutant sampled 25 min after waterspray (25m) and untouched (UT). Scale bars represent linear fold-changes normalized to Col-0 untreated as 1. (C) Heat map of all 266 myc234-dependent spray transcripts. Inset represents transcripts more than 100-fold induced by spray treatment in Col-0. (D) Heat map of selected MYC2/MYC3/MYC4-dependent transcripts related to JA-signaling and biosynthesis. (E) Heat map of the top 20 spray-inducible TF genes in Col-0 and their transcript abundance in myc234 after touch. TF genes that are significantly altered (at least 2-fold, P < 0.05) in myc234 after spray (myc234 25m) compared to Col-0 (Col-0 25m) are indicated in bold and blue.

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