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, Hannes Claeys, Stefanie de Bodt, Akira Oikawa, Shoko Shinoda, Megan Andriankaja, Katrien Maleux, Nubia Barbosa Eloy, Frederik Coppens, Sang-Dong Yoo, Kazuki Saito, Dirk Inzé

Research output: Contribution to journalArticle

130 Citations (Scopus)

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 endore duplication 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.

Original languageEnglish
Pages (from-to)1876-1888
Number of pages13
JournalPlant Cell
Volume23
Issue number5
DOIs
Publication statusPublished - 2011 May 1
Externally publishedYes

Fingerprint

Osmotic Pressure
leaf development
osmotic stress
Cell Cycle Checkpoints
Arabidopsis
ethylene
cell cycle
cell proliferation
Cell Cycle
Cell Proliferation
Plant Leaves
cyclin-dependent kinase
Cyclin-Dependent Kinases
cells
Growth
growth retardation
Arabidopsis thaliana
Cell Count
plant growth
agriculture

ASJC Scopus subject areas

  • Plant Science
  • Cell Biology

Cite this

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. / Skirycz, Aleksandra; Claeys, Hannes; de Bodt, Stefanie; Oikawa, Akira; Shinoda, Shoko; Andriankaja, Megan; Maleux, Katrien; Eloy, Nubia Barbosa; Coppens, Frederik; Yoo, Sang-Dong; Saito, Kazuki; Inzé, Dirk.

In: Plant Cell, Vol. 23, No. 5, 01.05.2011, p. 1876-1888.

Research output: Contribution to journalArticle

Skirycz, A, Claeys, H, de Bodt, S, Oikawa, A, Shinoda, S, Andriankaja, M, Maleux, K, Eloy, NB, Coppens, F, Yoo, S-D, Saito, K & Inzé, D 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, vol. 23, no. 5, pp. 1876-1888. https://doi.org/10.1105/tpc.111.084160
Skirycz, Aleksandra ; Claeys, Hannes ; de Bodt, Stefanie ; Oikawa, Akira ; Shinoda, Shoko ; Andriankaja, Megan ; Maleux, Katrien ; Eloy, Nubia Barbosa ; Coppens, Frederik ; Yoo, Sang-Dong ; Saito, Kazuki ; Inzé, Dirk. / 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. In: Plant Cell. 2011 ; Vol. 23, No. 5. pp. 1876-1888.
@article{56b409817c9c4e899a6bb191387282fd,
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",
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 endore duplication 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 = "Aleksandra Skirycz and Hannes Claeys and {de Bodt}, Stefanie and Akira Oikawa and Shoko Shinoda and Megan Andriankaja and Katrien Maleux and Eloy, {Nubia Barbosa} and Frederik Coppens and Sang-Dong Yoo and Kazuki Saito and Dirk Inz{\'e}",
year = "2011",
month = "5",
day = "1",
doi = "10.1105/tpc.111.084160",
language = "English",
volume = "23",
pages = "1876--1888",
journal = "Plant Cell",
issn = "1040-4651",
publisher = "American Society of Plant Biologists",
number = "5",

}

TY - JOUR

T1 - Pause-and-stop

T2 - The effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest

AU - Skirycz, Aleksandra

AU - Claeys, Hannes

AU - de Bodt, Stefanie

AU - Oikawa, Akira

AU - Shinoda, Shoko

AU - Andriankaja, Megan

AU - Maleux, Katrien

AU - Eloy, Nubia Barbosa

AU - Coppens, Frederik

AU - Yoo, Sang-Dong

AU - Saito, Kazuki

AU - Inzé, Dirk

PY - 2011/5/1

Y1 - 2011/5/1

N2 - 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 endore duplication 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.

AB - 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 endore duplication 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.

UR - http://www.scopus.com/inward/record.url?scp=79959839056&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79959839056&partnerID=8YFLogxK

U2 - 10.1105/tpc.111.084160

DO - 10.1105/tpc.111.084160

M3 - Article

VL - 23

SP - 1876

EP - 1888

JO - Plant Cell

JF - Plant Cell

SN - 1040-4651

IS - 5

ER -