Advanced

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

Skirycz, Aleksandra; De Bodt, Stefanie; Obata, Toshihiro; De Clercq, Inge; Claeys, Hannes; De Rycke, Riet Maria; Andriankaja, Megan; Van Aken, Olivier LU ; Van Breusegem, Frank and Fernie, Alisdair R, et al. (2010) In Plant Physiology 152(1). p.44-226
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... (More)

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.

(Less)
Please use this url to cite or link to this publication:
author
, et al. (More)
(Less)
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Arabidopsis, Arabidopsis Proteins, Cell Wall, Gene Expression Regulation, Plant, Mannitol, Mitochondria, Osmosis, Plant Leaves, Seedlings, Stress, Physiological, Time Factors, Water
in
Plant Physiology
volume
152
issue
1
pages
19 pages
publisher
American Society of Plant Biologists
external identifiers
  • scopus:73249116031
ISSN
1532-2548
DOI
10.1104/pp.109.148965
language
English
LU publication?
no
id
3bb965fd-0416-42c4-87d7-b4aa2c672106
date added to LUP
2017-05-09 10:09:04
date last changed
2018-11-18 04:54:25
@article{3bb965fd-0416-42c4-87d7-b4aa2c672106,
  abstract     = {<p>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.</p>},
  author       = {Skirycz, Aleksandra and De Bodt, Stefanie and Obata, Toshihiro and De Clercq, Inge and Claeys, Hannes and De Rycke, Riet Maria and Andriankaja, Megan and Van Aken, Olivier and Van Breusegem, Frank and Fernie, Alisdair R and Inzé, Dirk},
  issn         = {1532-2548},
  keyword      = {Arabidopsis,Arabidopsis Proteins,Cell Wall,Gene Expression Regulation, Plant,Mannitol,Mitochondria,Osmosis,Plant Leaves,Seedlings,Stress, Physiological,Time Factors,Water},
  language     = {eng},
  number       = {1},
  pages        = {44--226},
  publisher    = {American Society of Plant Biologists},
  series       = {Plant Physiology},
  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},
}