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A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels

van Moerkercke, Alex LU ; Duncan, Owen ; Zander, Mark ; Simura, Jan ; Broda, Martyna ; Bossche, Robin Vanden ; Lewsey, Mathew G. ; Lama, Sbatie LU ; Singh, Karam B. and Ljung, Karin , et al. (2019) In Proceedings of the National Academy of Sciences of the United States of America 116(46). p.23345-23356
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... (More)

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.

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publication status
published
subject
keywords
Jasmonic acid, Mechanical stimulation, Plants, Touch, Transcription
in
Proceedings of the National Academy of Sciences of the United States of America
volume
116
issue
46
pages
12 pages
publisher
National Acad Sciences
external identifiers
  • pmid:31662474
  • scopus:85074754543
ISSN
0027-8424
DOI
10.1073/pnas.1911758116
language
English
LU publication?
yes
id
b8d8394a-d408-45ee-886c-011c8ffdfbb2
date added to LUP
2019-11-29 12:10:59
date last changed
2020-07-08 05:08:19
@article{b8d8394a-d408-45ee-886c-011c8ffdfbb2,
  abstract     = {<p>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 &gt;100-fold. Chromatin immunoprecipitation-sequencing analysis indicates that MYC2 dynamically binds &gt;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.</p>},
  author       = {van Moerkercke, Alex and Duncan, Owen and Zander, Mark and Simura, Jan and Broda, Martyna and Bossche, Robin Vanden and Lewsey, Mathew G. and Lama, Sbatie and Singh, Karam B. and Ljung, Karin and Ecker, Joseph R. and Goossens, Alain and Millar, A. Harvey and van Aken, Olivier},
  issn         = {0027-8424},
  language     = {eng},
  number       = {46},
  pages        = {23345--23356},
  publisher    = {National Acad Sciences},
  series       = {Proceedings of the National Academy of Sciences of the United States of America},
  title        = {A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels},
  url          = {http://dx.doi.org/10.1073/pnas.1911758116},
  doi          = {10.1073/pnas.1911758116},
  volume       = {116},
  year         = {2019},
}