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*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

72 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)109-122
Number of pages14
JournalPlant Molecular Biology
Volume78
Issue number1-2
DOIs
Publication statusPublished - 01 Jan 2012
Externally publishedYes

Keywords

  • Anoxia
  • Arabidopsis thaliana
  • Hypoxia
  • Mitochondrial electron transport
  • Mitogen-activated protein kinase
  • Reactive oxygen species
  • Signal transduction

ASJC Scopus subject areas

  • Agronomy and Crop Science
  • Genetics
  • Plant Science

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