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Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest

Aleksandra Skirycz UGent, Hannes Claeys UGent, Stefanie De Bodt UGent, Akira Oikawa, Shoko Shinoda, Megan Andriankaja UGent, Katrien Maleux UGent, Nubia Barbosa Eloy UGent, Frederik Coppens UGent and Sang-Dong Yoo, et al. (2011) PLANT CELL. 23(5). p.1876-1888
abstract
Despite its relevance for agricultural production, environmental stress-induced growth inhibition, which is responsible for significant yield reductions, is only poorly understood. Here, we investigated the molecular mechanisms underlying cell cycle inhibition in young proliferating leaves of the model plant Arabidopsis thaliana when subjected to mild osmotic stress. A detailed cellular analysis demonstrated that as soon as osmotic stress is sensed, cell cycle progression rapidly arrests, but cells are kept in a latent ambivalent state allowing a quick recovery (pause). Remarkably, cell cycle arrest coincides with an increase in 1-aminocyclopropane-1-carboxylate levels and the activation of ethylene signaling. Our work showed that ethylene acts on cell cycle progression via inhibition of cyclin-dependent kinase A activity independently of EIN3 transcriptional control. When the stress persists, cells exit the mitotic cell cycle and initiate the differentiation process (stop). This stop is reflected by early endoreduplication onset, in a process independent of ethylene. Nonetheless, the potential to partially recover the decreased cell numbers remains due to the activity of meristemoids. Together, these data present a conceptual framework to understand how environmental stress reduces plant growth.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
DEPENDENT KINASE INHIBITORS, GENE-EXPRESSION, PROTEIN-KINASE, SALT STRESS, REGULATORY GENES, ABIOTIC STRESSES, PLANT-TISSUES, GROWTH-RESPONSE, WATER-STRESS, PROBE LEVEL DATA
journal title
PLANT CELL
Plant Cell
volume
23
issue
5
pages
1876 - 1888
Web of Science type
Article
Web of Science id
000292079800016
JCR category
PLANT SCIENCES
JCR impact factor
8.987 (2011)
JCR rank
5/189 (2011)
JCR quartile
1 (2011)
ISSN
1040-4651
DOI
10.1105/tpc.111.084160
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
1864599
handle
http://hdl.handle.net/1854/LU-1864599
date created
2011-08-01 19:33:04
date last changed
2013-02-27 12:59:21
@article{1864599,
  abstract     = {Despite its relevance for agricultural production, environmental stress-induced growth inhibition, which is responsible for significant yield reductions, is only poorly understood. Here, we investigated the molecular mechanisms underlying cell cycle inhibition in young proliferating leaves of the model plant Arabidopsis thaliana when subjected to mild osmotic stress. A detailed cellular analysis demonstrated that as soon as osmotic stress is sensed, cell cycle progression rapidly arrests, but cells are kept in a latent ambivalent state allowing a quick recovery (pause). Remarkably, cell cycle arrest coincides with an increase in 1-aminocyclopropane-1-carboxylate levels and the activation of ethylene signaling. Our work showed that ethylene acts on cell cycle progression via inhibition of cyclin-dependent kinase A activity independently of EIN3 transcriptional control. When the stress persists, cells exit the mitotic cell cycle and initiate the differentiation process (stop). This stop is reflected by early endoreduplication onset, in a process independent of ethylene. Nonetheless, the potential to partially recover the decreased cell numbers remains due to the activity of meristemoids. Together, these data present a conceptual framework to understand how environmental stress reduces plant growth.},
  author       = {Skirycz, Aleksandra and Claeys, Hannes and De Bodt, Stefanie and Oikawa, Akira and Shinoda, Shoko and Andriankaja, Megan and Maleux, Katrien and Eloy, Nubia Barbosa and Coppens, Frederik and Yoo, Sang-Dong and Saito, Kazuki and Inz{\'e}, Dirk},
  issn         = {1040-4651},
  journal      = {PLANT CELL},
  keyword      = {DEPENDENT KINASE INHIBITORS,GENE-EXPRESSION,PROTEIN-KINASE,SALT STRESS,REGULATORY GENES,ABIOTIC STRESSES,PLANT-TISSUES,GROWTH-RESPONSE,WATER-STRESS,PROBE LEVEL DATA},
  language     = {eng},
  number       = {5},
  pages        = {1876--1888},
  title        = {Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest},
  url          = {http://dx.doi.org/10.1105/tpc.111.084160},
  volume       = {23},
  year         = {2011},
}

Chicago
Skirycz, Aleksandra, Hannes Claeys, Stefanie De Bodt, Akira Oikawa, Shoko Shinoda, Megan Andriankaja, Katrien Maleux, et al. 2011. “Pause-and-stop: The Effects of Osmotic Stress on Cell Proliferation During Early Leaf Development in Arabidopsis and a Role for Ethylene Signaling in Cell Cycle Arrest.” Plant Cell 23 (5): 1876–1888.
APA
Skirycz, A., Claeys, H., De Bodt, S., Oikawa, A., Shinoda, S., Andriankaja, M., Maleux, K., et al. (2011). Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. PLANT CELL, 23(5), 1876–1888.
Vancouver
1.
Skirycz A, Claeys H, De Bodt S, Oikawa A, Shinoda S, Andriankaja M, et al. Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. PLANT CELL. 2011;23(5):1876–88.
MLA
Skirycz, Aleksandra, Hannes Claeys, Stefanie De Bodt, et al. “Pause-and-stop: The Effects of Osmotic Stress on Cell Proliferation During Early Leaf Development in Arabidopsis and a Role for Ethylene Signaling in Cell Cycle Arrest.” PLANT CELL 23.5 (2011): 1876–1888. Print.