Plant Molecular Biology

, Volume 78, Issue 1, pp 109–122

Transient MPK6 activation in response to oxygen deprivation and reoxygenation is mediated by mitochondria and aids seedling survival in Arabidopsis

  • Ruth Chang
  • Charles J. H. Jang
  • Cristina Branco-Price
  • Peter Nghiem
  • Julia Bailey-Serres
Article

DOI: 10.1007/s11103-011-9850-5

Cite this article as:
Chang, R., Jang, C.J.H., Branco-Price, C. et al. Plant Mol Biol (2012) 78: 109. doi:10.1007/s11103-011-9850-5

Abstract

Mitogen-activated protein kinases (MPKs) are regulated by diverse stresses with a reactive oxygen species (ROS) component. Here, we report the rapid and transient activation of MPK3, MPK4 and MPK6 upon oxygen deprivation as well as reoxygenation in seedlings of Arabidopsis thaliana. MPK activation peaked within 2 h of oxygen deprivation and again at a higher magnitude within 5 min of reoxygenation. MPK6 was the predominant kinase regulated by oxygen availability in both aerial and root tissue, except in mpk6 mutants, which displayed compensatory activation of MPK3. A universal consequence of oxygen deprivation in eukaryotes is inhibition of the terminal step of the mitochondrial electron transport chain (mETC). We demonstrate that treatment of seedlings with the mETC inhibitors antimycin A and potassium cyanide under normoxia promotes transient MPK6 and MPK3 activation. Confocal imaging of seedlings provided evidence that both oxygen deprivation and mETC inhibitors stimulate mitochondria-associated ROS production. We found that seedling survival of prolonged oxygen deprivation was improved in transgenics that ectopically overexpress MPK3, MPK4 and MPK6, but the induction of mRNAs associated with low oxygen acclimation responses were not markedly altered in MPK6 overexpression lines or mpk6 loss-of-function mutants. However, distinctions in MPK6 activation potential were correlated with other differences in mRNAs accumulation. Our findings suggest that oxygen deprivation and reoxygenation trigger mitochondrial ROS production to activate MPK signaling, which in turn regulate reversible processes that aid survival of transient oxygen deprivation.

Keywords

Arabidopsis thalianaAnoxiaHypoxiaMitochondrial electron transportReactive oxygen speciesSignal transductionMitogen-activated protein kinase

Abbreviations

MPK

Mitogen-activated protein kinase

ROS

Reactive oxygen species

H2O2

Hydrogen peroxide

OE

Overexpression

mETC

Mitochondrial electron transport chain

AA

Antimycin A

KCN

Potassium cyanide

MYX

Myxothiazol

FCCP

Carbonyl cyanide p-trifluoromethoxyphenyl hydrazone

RMA

Robust Multi-chip Average

DCF

Carboxy-2′,7′-dichlorofluorescein diacetate

CLSM

Confocal laser scanning microscopy

SLR

Signal log ratio

Supplementary material

11103_2011_9850_MOESM1_ESM.docx (130 kb)
Supplementary material 1 (DOCX 130 kb)
11103_2011_9850_MOESM2_ESM.xls (9.3 mb)
Supplementary material 2 (XLS 9535 kb)
11103_2011_9850_MOESM3_ESM.pdf (4.4 mb)
Supplementary material 3 (PDF 4504 kb)

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Ruth Chang
    • 1
  • Charles J. H. Jang
    • 1
  • Cristina Branco-Price
    • 1
  • Peter Nghiem
    • 1
  • Julia Bailey-Serres
    • 1
  1. 1.Department of Botany and Plant Sciences, Center for Plant Cell BiologyUniversity of CaliforniaRiversideUSA