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

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A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels. / van Moerkercke, Alex; Duncan, Owen; Zander, Mark; Simura, Jan; Broda, Martyna; Bossche, Robin Vanden; Lewsey, Mathew G.; Lama, Sbatie; Singh, Karam B.; Ljung, Karin; Ecker, Joseph R.; Goossens, Alain; Millar, A. Harvey; van Aken, Olivier.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 46, 2019, p. 23345-23356.

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van Moerkercke, Alex ; Duncan, Owen ; Zander, Mark ; Simura, Jan ; Broda, Martyna ; Bossche, Robin Vanden ; Lewsey, Mathew G. ; Lama, Sbatie ; Singh, Karam B. ; Ljung, Karin ; Ecker, Joseph R. ; Goossens, Alain ; Millar, A. Harvey ; van Aken, Olivier. / A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 46. pp. 23345-23356.

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TY - JOUR

T1 - A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels

AU - van Moerkercke, Alex

AU - Duncan, Owen

AU - Zander, Mark

AU - Simura, Jan

AU - Broda, Martyna

AU - Bossche, Robin Vanden

AU - Lewsey, Mathew G.

AU - Lama, Sbatie

AU - Singh, Karam B.

AU - Ljung, Karin

AU - Ecker, Joseph R.

AU - Goossens, Alain

AU - Millar, A. Harvey

AU - van Aken, Olivier

PY - 2019

Y1 - 2019

N2 - 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.

AB - 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.

KW - Jasmonic acid

KW - Mechanical stimulation

KW - Plants

KW - Touch

KW - Transcription

U2 - 10.1073/pnas.1911758116

DO - 10.1073/pnas.1911758116

M3 - Article

VL - 116

SP - 23345

EP - 23356

JO - Proceedings of the National Academy of Sciences

JF - Proceedings of the National Academy of Sciences

SN - 1091-6490

IS - 46

ER -