Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress.
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.
Skirycz
Aleksandra
A
Department of Plant Biotechnology and Genetics, Ghent University, B-9052 Ghent, Belgium.
De Bodt
Stefanie
S
Obata
Toshihiro
T
De Clercq
Inge
I
Claeys
Hannes
H
De Rycke
Riet
R
Andriankaja
Megan
M
Van Aken
Olivier
O
Van Breusegem
Frank
F
Fernie
Alisdair R
AR
Inzé
Dirk
D
D017360:Arabidopsis / Q000187:drug effects* / Q000254:growth & development*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D002473:Cell Wall; D018506:Gene Expression Regulation, Plant / Q000502:physiology; D008353:Mannitol / Q000494:pharmacology; D008928:Mitochondria / Q000378:metabolism*; D009995:Osmosis; D018515:Plant Leaves / Q000166:cytology / Q000187:drug effects / Q000502:physiology*; D036226:Seedlings; D013312:Stress, Physiological / Q000187:drug effects / Q000502:physiology*; D013997:Time Factors; D014867:Water / Q000378:metabolism
D029681:Arabidopsis Proteins; D014867:Water; D008353:Mannitol