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ETHYLENE RESPONSE FACTOR6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis

Marieke Dubois, Aleksandra Skirycz UGent, Hannes Claeys, Katrien Maleux UGent, Stijn Dhondt UGent, Stefanie De Bodt UGent, Robin Vanden Bossche UGent, Liesbeth De Milde UGent, Takeshi Yoshizumi, Minami Matsui, et al. (2013) PLANT PHYSIOLOGY. 162(1). p.319-332
abstract
Leaf growth is a complex developmental process that is continuously fine-tuned by the environment. Various abiotic stresses, including mild drought stress, have been shown to inhibit leaf growth in Arabidopsis (Arabidopsis thaliana), but the underlying mechanisms remain largely unknown. Here, we identify the redundant Arabidopsis transcription factors ETHYLENE RESPONSE FACTOR5 (ERF5) and ERF6 as master regulators that adapt leaf growth to environmental changes. ERF5 and ERF6 gene expression is induced very rapidly and specifically in actively growing leaves after sudden exposure to osmotic stress that mimics mild drought. Subsequently, enhanced ERF6 expression inhibits cell proliferation and leaf growth by a process involving gibberellin and DELLA signaling. Using an ERF6-inducible overexpression line, we demonstrate that the gibberellin-degrading enzyme GIBBERELLIN 2-OXIDASE6 is transcriptionally induced by ERF6 and that, consequently, DELLA proteins are stabilized. As a result, ERF6 gain-of-function lines are dwarfed and hypersensitive to osmotic stress, while the growth of erf5erf6 loss-of-function mutants is less affected by stress. Besides its role in plant growth under stress, ERF6 also activates the expression of a plethora of osmotic stress-responsive genes, including the well-known stress tolerance genes STZ, MYB51, and WRKY33. Interestingly, activation of the stress tolerance genes by ERF6 occurs independently from the ERF6-mediated growth inhibition. Together, these data fit into a leaf growth regulatory model in which ERF5 and ERF6 form a missing link between the previously observed stress-induced 1-aminocyclopropane-1-carboxylic acid accumulation and DELLA-mediated cell cycle exit and execute a dual role by regulating both stress tolerance and growth inhibition.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
SALT-STRESS, TRANSCRIPTION FACTOR, HIGH-SALINITY STRESS, PROBE LEVEL DATA, SIGNAL-TRANSDUCTION, CELL-PROLIFERATION, DROUGHT STRESS, ABIOTIC STRESS, PLANT-GROWTH, OSMOTIC-STRESS
journal title
PLANT PHYSIOLOGY
Plant Physiol.
volume
162
issue
1
pages
319 - 332
Web of Science type
Article
Web of Science id
000318547900024
JCR category
PLANT SCIENCES
JCR impact factor
7.394 (2013)
JCR rank
6/199 (2013)
JCR quartile
1 (2013)
ISSN
0032-0889
DOI
10.1104/pp.113.216341
project
Biotechnology for a sustainable economy (Bio-Economy)
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
4098736
handle
http://hdl.handle.net/1854/LU-4098736
date created
2013-07-09 15:50:40
date last changed
2016-12-19 15:46:50
@article{4098736,
  abstract     = {Leaf growth is a complex developmental process that is continuously fine-tuned by the environment. Various abiotic stresses, including mild drought stress, have been shown to inhibit leaf growth in Arabidopsis (Arabidopsis thaliana), but the underlying mechanisms remain largely unknown. Here, we identify the redundant Arabidopsis transcription factors ETHYLENE RESPONSE FACTOR5 (ERF5) and ERF6 as master regulators that adapt leaf growth to environmental changes. ERF5 and ERF6 gene expression is induced very rapidly and specifically in actively growing leaves after sudden exposure to osmotic stress that mimics mild drought. Subsequently, enhanced ERF6 expression inhibits cell proliferation and leaf growth by a process involving gibberellin and DELLA signaling. Using an ERF6-inducible overexpression line, we demonstrate that the gibberellin-degrading enzyme GIBBERELLIN 2-OXIDASE6 is transcriptionally induced by ERF6 and that, consequently, DELLA proteins are stabilized. As a result, ERF6 gain-of-function lines are dwarfed and hypersensitive to osmotic stress, while the growth of erf5erf6 loss-of-function mutants is less affected by stress. Besides its role in plant growth under stress, ERF6 also activates the expression of a plethora of osmotic stress-responsive genes, including the well-known stress tolerance genes STZ, MYB51, and WRKY33. Interestingly, activation of the stress tolerance genes by ERF6 occurs independently from the ERF6-mediated growth inhibition. Together, these data fit into a leaf growth regulatory model in which ERF5 and ERF6 form a missing link between the previously observed stress-induced 1-aminocyclopropane-1-carboxylic acid accumulation and DELLA-mediated cell cycle exit and execute a dual role by regulating both stress tolerance and growth inhibition.},
  author       = {Dubois, Marieke and Skirycz, Aleksandra and Claeys, Hannes and Maleux, Katrien and Dhondt, Stijn and De Bodt, Stefanie and Vanden Bossche, Robin and De Milde, Liesbeth and Yoshizumi, Takeshi and Matsui, Minami and Inz{\'e}, Dirk},
  issn         = {0032-0889},
  journal      = {PLANT PHYSIOLOGY},
  keyword      = {SALT-STRESS,TRANSCRIPTION FACTOR,HIGH-SALINITY STRESS,PROBE LEVEL DATA,SIGNAL-TRANSDUCTION,CELL-PROLIFERATION,DROUGHT STRESS,ABIOTIC STRESS,PLANT-GROWTH,OSMOTIC-STRESS},
  language     = {eng},
  number       = {1},
  pages        = {319--332},
  title        = {ETHYLENE RESPONSE FACTOR6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis},
  url          = {http://dx.doi.org/10.1104/pp.113.216341},
  volume       = {162},
  year         = {2013},
}

Chicago
Dubois, Marieke, Aleksandra Skirycz, Hannes Claeys, Katrien Maleux, Stijn Dhondt, Stefanie De Bodt, Robin Vanden Bossche, et al. 2013. “ETHYLENE RESPONSE FACTOR6 Acts as a Central Regulator of Leaf Growth Under Water-limiting Conditions in Arabidopsis.” Plant Physiology 162 (1): 319–332.
APA
Dubois, Marieke, Skirycz, A., Claeys, H., Maleux, K., Dhondt, S., De Bodt, S., Vanden Bossche, R., et al. (2013). ETHYLENE RESPONSE FACTOR6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis. PLANT PHYSIOLOGY, 162(1), 319–332.
Vancouver
1.
Dubois M, Skirycz A, Claeys H, Maleux K, Dhondt S, De Bodt S, et al. ETHYLENE RESPONSE FACTOR6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis. PLANT PHYSIOLOGY. 2013;162(1):319–32.
MLA
Dubois, Marieke, Aleksandra Skirycz, Hannes Claeys, et al. “ETHYLENE RESPONSE FACTOR6 Acts as a Central Regulator of Leaf Growth Under Water-limiting Conditions in Arabidopsis.” PLANT PHYSIOLOGY 162.1 (2013): 319–332. Print.