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

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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.
Keywords
STRESS RESPONSES, PLANT-RESPONSE, ARABIDOPSIS, MYC2, TOUCH, GROWTH, ACID, IDENTIFICATION, MITOCHONDRIAL, ACTIVATION, mechanical stimulation, touch, jasmonic acid, plants, transcription

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Citation

Please use this url to cite or link to this publication:

MLA
Van Moerkercke, Alex, et al. “A MYC2/MYC3/MYC4-Dependent Transcription Factor Network Regulates Water Spray-Responsive Gene Expression and Jasmonate Levels.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 116, no. 46, Natl Acad Sciences, 2019, pp. 23345–56.
APA
Van Moerkercke, A., Duncan, O., Zander, M., Simura, J., Broda, M., Vanden Bossche, R., … Van Aken, O. (2019). A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 116(46), 23345–23356.
Chicago author-date
Van Moerkercke, Alex, Owen Duncan, Mark Zander, Jan Simura, Martyna Broda, Robin Vanden Bossche, Mathew G. Lewsey, et al. 2019. “A MYC2/MYC3/MYC4-Dependent Transcription Factor Network Regulates Water Spray-Responsive Gene Expression and Jasmonate Levels.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 116 (46): 23345–56.
Chicago author-date (all authors)
Van Moerkercke, Alex, Owen Duncan, Mark Zander, Jan Simura, Martyna Broda, Robin Vanden Bossche, Mathew G. Lewsey, Sbatie Lama, Karam B. Singh, Karin Ljung, Joseph R. Ecker, Alain Goossens, A. Harvey Millar, and Olivier Van Aken. 2019. “A MYC2/MYC3/MYC4-Dependent Transcription Factor Network Regulates Water Spray-Responsive Gene Expression and Jasmonate Levels.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 116 (46): 23345–23356.
Vancouver
1.
Van Moerkercke A, Duncan O, Zander M, Simura J, Broda M, Vanden Bossche R, et al. A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2019;116(46):23345–56.
IEEE
[1]
A. Van Moerkercke et al., “A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels,” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 116, no. 46, pp. 23345–23356, 2019.
@article{8637084,
  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.},
  author       = {Van Moerkercke, Alex and Duncan, Owen and Zander, Mark and Simura, Jan and Broda, Martyna and Vanden Bossche, Robin 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},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keywords     = {STRESS RESPONSES,PLANT-RESPONSE,ARABIDOPSIS,MYC2,TOUCH,GROWTH,ACID,IDENTIFICATION,MITOCHONDRIAL,ACTIVATION,mechanical stimulation,touch,jasmonic acid,plants,transcription},
  language     = {eng},
  number       = {46},
  pages        = {23345--23356},
  publisher    = {Natl Acad Sciences},
  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},
  volume       = {116},
  year         = {2019},
}

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