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Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress

Aleksandra Skirycz UGent, Stefanie De Bodt UGent, Toshihiro Obata, Inge De Clercq UGent, Hannes Claeys UGent, Riet De Rycke UGent, Megan Andriankaja UGent, Olivier Van Aken, Frank Van Breusegem UGent and Alisdair R Fernie, et al. (2010) PLANT PHYSIOLOGY. 152(1). p.226-244
abstract
When subjected to stress, plants reprogram their growth by largely unknown mechanisms. To provide insights into this process, the growth of Arabidopsis (Arabidopsis thaliana) leaves that develop under mild osmotic stress was studied. Early during leaf development, cell number and size were reduced by stress, but growth was remarkably adaptable, as division and expansion rates were identical to controls within a few days of leaf initiation. To investigate the molecular basis of the observed adaptability, leaves with only proliferating, exclusively expanding, and mature cells were analyzed by transcriptomics and targeted metabolomics. The stress response measured in growing and mature leaves was largely distinct; several hundred transcripts and multiple metabolites responded exclusively in the proliferating and/or expanding leaves. Only a few genes were differentially expressed across the three stages. Data analysis showed that proliferation and expansion were regulated by common regulatory circuits, involving ethylene and gibberellins but not abscisic acid. The role of ethylene was supported by the analysis of ethylene-insensitive mutants. Exclusively in proliferating cells, stress induced genes of the so-called "mitochondrial dysfunction regulon," comprising alternative oxidase. Up-regulation for eight of these genes was confirmed with promoter: beta-glucuronidase reporter lines. Furthermore, mitochondria of stress-treated dividing cells were morphologically distinct from control ones, and growth of plants overexpressing the alternative oxidase gene was more tolerant to osmotic and drought stresses. Taken together, our data underline the value of analyzing stress responses in development and demonstrate the importance of mitochondrial respiration for sustaining cell proliferation under osmotic stress conditions.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
TRANSCRIPTION FACTOR, DROUGHT STRESS, MODEL DATA-ANALYSIS, GENOME-WIDE ANALYSIS, PLANT-CELL-WALLS, GENE-EXPRESSION, PROBE LEVEL DATA, WATER-DEFICIT, OXIDATIVE STRESS, LEAF GROWTH
journal title
PLANT PHYSIOLOGY
Plant Physiol.
volume
152
issue
1
pages
19 pages
Web of Science type
Article
Web of Science id
000273148100018
JCR category
PLANT SCIENCES
JCR impact factor
6.451 (2010)
JCR rank
8/185 (2010)
JCR quartile
1 (2010)
ISSN
0032-0889
DOI
10.1104/pp.109.148965
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
846588
handle
http://hdl.handle.net/1854/LU-846588
date created
2010-01-29 18:39:43
date last changed
2012-09-19 14:04:00
@article{846588,
  abstract     = {When subjected to stress, plants reprogram their growth by largely unknown mechanisms. To provide insights into this process, the growth of Arabidopsis (Arabidopsis thaliana) leaves that develop under mild osmotic stress was studied. Early during leaf development, cell number and size were reduced by stress, but growth was remarkably adaptable, as division and expansion rates were identical to controls within a few days of leaf initiation. To investigate the molecular basis of the observed adaptability, leaves with only proliferating, exclusively expanding, and mature cells were analyzed by transcriptomics and targeted metabolomics. The stress response measured in growing and mature leaves was largely distinct; several hundred transcripts and multiple metabolites responded exclusively in the proliferating and/or expanding leaves. Only a few genes were differentially expressed across the three stages. Data analysis showed that proliferation and expansion were regulated by common regulatory circuits, involving ethylene and gibberellins but not abscisic acid. The role of ethylene was supported by the analysis of ethylene-insensitive mutants. Exclusively in proliferating cells, stress induced genes of the so-called {\textacutedbl}mitochondrial dysfunction regulon,{\textacutedbl} comprising alternative oxidase. Up-regulation for eight of these genes was confirmed with promoter: beta-glucuronidase reporter lines. Furthermore, mitochondria of stress-treated dividing cells were morphologically distinct from control ones, and growth of plants overexpressing the alternative oxidase gene was more tolerant to osmotic and drought stresses. Taken together, our data underline the value of analyzing stress responses in development and demonstrate the importance of mitochondrial respiration for sustaining cell proliferation under osmotic stress conditions.},
  author       = {Skirycz, Aleksandra and De Bodt, Stefanie and Obata, Toshihiro and De Clercq, Inge and Claeys, Hannes and De Rycke, Riet and Andriankaja, Megan and Van Aken, Olivier and Van Breusegem, Frank and Fernie, Alisdair R and Inz{\'e}, Dirk},
  issn         = {0032-0889},
  journal      = {PLANT PHYSIOLOGY},
  keyword      = {TRANSCRIPTION FACTOR,DROUGHT STRESS,MODEL DATA-ANALYSIS,GENOME-WIDE ANALYSIS,PLANT-CELL-WALLS,GENE-EXPRESSION,PROBE LEVEL DATA,WATER-DEFICIT,OXIDATIVE STRESS,LEAF GROWTH},
  language     = {eng},
  number       = {1},
  pages        = {226--244},
  title        = {Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress},
  url          = {http://dx.doi.org/10.1104/pp.109.148965},
  volume       = {152},
  year         = {2010},
}

Chicago
Skirycz, Aleksandra, Stefanie De Bodt, Toshihiro Obata, Inge De Clercq, Hannes Claeys, Riet De Rycke, Megan Andriankaja, et al. 2010. “Developmental Stage Specificity and the Role of Mitochondrial Metabolism in the Response of Arabidopsis Leaves to Prolonged Mild Osmotic Stress.” Plant Physiology 152 (1): 226–244.
APA
Skirycz, A., De Bodt, S., Obata, T., De Clercq, I., Claeys, H., De Rycke, R., Andriankaja, M., et al. (2010). Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress. PLANT PHYSIOLOGY, 152(1), 226–244.
Vancouver
1.
Skirycz A, De Bodt S, Obata T, De Clercq I, Claeys H, De Rycke R, et al. Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress. PLANT PHYSIOLOGY. 2010;152(1):226–44.
MLA
Skirycz, Aleksandra, Stefanie De Bodt, Toshihiro Obata, et al. “Developmental Stage Specificity and the Role of Mitochondrial Metabolism in the Response of Arabidopsis Leaves to Prolonged Mild Osmotic Stress.” PLANT PHYSIOLOGY 152.1 (2010): 226–244. Print.