title: Transient MPK6 activation in response to oxygen deprivation and reoxygenation is mediated by mitochondria and aids seedling survival in Arabidopsis.
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.
authors.affiliation: Department of Botany and Plant Sciences, Center for Plant Cell Biology, University of California, Riverside, CA 92521, USA.
authors.forename: Ruth
authors.initials: R
authors.lastname: Chang
authors.forename: Charles J H
authors.initials: CJ
authors.lastname: Jang
authors.forename: Cristina
authors.initials: C
authors.lastname: Branco-Price
authors.forename: Peter
authors.initials: P
authors.lastname: Nghiem
authors.forename: Julia
authors.initials: J
authors.lastname: Bailey-Serres
mesh_terms: D000693:Anaerobiosis; D000968:Antimycin A / Q000494:pharmacology; D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D016000:Cluster Analysis; D004579:Electron Transport / Q000187:drug effects; D004789:Enzyme Activation / Q000187:drug effects; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D015151:Immunoblotting; D018613:Microscopy, Confocal; D008928:Mitochondria / Q000187:drug effects / Q000378:metabolism*; D020929:Mitogen-Activated Protein Kinase Kinases / Q000235:genetics / Q000378:metabolism; D020928:Mitogen-Activated Protein Kinases / Q000235:genetics / Q000378:metabolism*; D009154:Mutation; D020411:Oligonucleotide Array Sequence Analysis; D010100:Oxygen / Q000378:metabolism* / Q000494:pharmacology; D030821:Plants, Genetically Modified; D011190:Potassium Cyanide / Q000494:pharmacology; D017382:Reactive Oxygen Species / Q000378:metabolism; D036226:Seedlings / Q000187:drug effects / Q000254:growth & development / Q000378:metabolism*; D059467:Transcriptome
chemical_list: D029681:Arabidopsis Proteins; D017382:Reactive Oxygen Species; D000968:Antimycin A; C458516:AtMPK3 protein, Arabidopsis; C436292:AtMPK4 protein, Arabidopsis; C436293:MPK6 protein, Arabidopsis; D020928:Mitogen-Activated Protein Kinases; D020929:Mitogen-Activated Protein Kinase Kinases; D011190:Potassium Cyanide; D010100:Oxygen
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