OPEN ACCESS ARTICLE

This Article Free via Open Access: OA OA Full Text Full Text (PDF) PPT slides of all figures Supplemental Data OA All Versions of this Article: 152/1/226    most recent pp.109.148965v1 Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via CrossRef Citing Articles via Google Scholar Google Scholar Articles by Skirycz, A. Articles by Inzé, D. Search for Related Content PubMed PubMed Citation Articles by Skirycz, A. Articles by Inzé, D. Pubmed/NCBI databases GEO DataSet Compound via MeSH Substance via MeSH Hazardous Substances DB D-MANNITOL Agricola Articles by Skirycz, A. Articles by Inzé, D. Related Collections Plant Systems Biology 2010

ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Developmental Stage Specificity and the Role of Mitochondrial Metabolism in the Response of Arabidopsis Leaves to Prolonged Mild Osmotic Stress^{1,[C],[W],[OA]}

Department of Plant Biotechnology and Genetics, Ghent University, B–9052 Ghent, Belgium (A.S., S.D.B., I.D.C., H.C., R.D.R., M.A., O.V.A., F.V.B., D.I.); Department of Plant Systems Biology, Flanders Institute for Biotechnology, B–9052 Ghent, Belgium (A.S., S.D.B., I.D.C., H.C., M.A., O.V.A., F.V.B., D.I.); and Max-Planck Institute for Molecular Plant Physiology, D–14476 Potsdam-Golm, Germany (T.O., A.R.F.)

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:β-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.

² Present address: Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Dirk Inzé (dirk.inze{at}psb.vib-ugent.be).

^[C] Some figures in this article are displayed in color online but in black and white in the print edition.

^[W] The online version of this article contains Web-only data.

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.109.148965

^* Corresponding author; e-mail dirk.inze{at}psb.vib-ugent.be.

Received October 7, 2009; accepted November 6, 2009; published November 11, 2009.

This article has been cited by other articles:

				T. C. R. Williams, M. G. Poolman, A. J. M. Howden, M. Schwarzlander, D. A. Fell, R. G. Ratcliffe, and L. J. Sweetlove A Genome-Scale Metabolic Model Accurately Predicts Fluxes in Central Carbon Metabolism under Stress Conditions Plant Physiology, September 1, 2010; 154(1): 311 - 323. [Abstract] [Full Text] [PDF]

				N. Gonzalez, S. De Bodt, R. Sulpice, Y. Jikumaru, E. Chae, S. Dhondt, T. Van Daele, L. De Milde, D. Weigel, Y. Kamiya, et al. Increased Leaf Size: Different Means to an End Plant Physiology, July 1, 2010; 153(3): 1261 - 1279. [Abstract] [Full Text] [PDF]