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Activation of cyclic electron flow by hydrogen peroxide in vivo

  1. David M. Kramera,b,e,2
  1. aPlant Research Laboratory and
  2. Departments of bPlant Biology and
  3. eBiochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824;
  4. cSchool of Molecular Biosciences and
  5. dInstitute for Biological Chemistry, Washington State University, Pullman, WA 99164; and
  6. fInstitute of Developmental and Molecular Biology of Plants, Plant Molecular Physiology and Biotechnology Group, Heinrich-Heine-Universität, Cluster of Excellence on Plant Sciences (CEPLAS), 40225 Düsseldorf, Germany

  1. Edited by Bob B. Buchanan, University of California, Berkeley, CA, and approved March 9, 2015 (received for review September 23, 2014)

Significance

Cyclic electron flow around photosystem I (CEF) is critical for balancing the energy budget of photosynthesis, but its regulation is not well understood. Our results provide evidence that hydrogen peroxide, which is produced as a result of imbalances in chloroplast redox state, acts as a signaling agent to activate CEF in higher plants in vivo.

Abstract

Cyclic electron flow (CEF) around photosystem I is thought to balance the ATP/NADPH energy budget of photosynthesis, requiring that its rate be finely regulated. The mechanisms of this regulation are not well understood. We observed that mutants that exhibited constitutively high rates of CEF also showed elevated production of H2O2. We thus tested the hypothesis that CEF can be activated by H2O2 in vivo. CEF was strongly increased by H2O2 both by infiltration or in situ production by chloroplast-localized glycolate oxidase, implying that H2O2 can activate CEF either directly by redox modulation of key enzymes, or indirectly by affecting other photosynthetic processes. CEF appeared with a half time of about 20 min after exposure to H2O2, suggesting activation of previously expressed CEF-related machinery. H2O2-dependent CEF was not sensitive to antimycin A or loss of PGR5, indicating that increased CEF probably does not involve the PGR5-PGRL1 associated pathway. In contrast, the rise in CEF was not observed in a mutant deficient in the chloroplast NADPH:PQ reductase (NDH), supporting the involvement of this complex in CEF activated by H2O2. We propose that H2O2 is a missing link between environmental stress, metabolism, and redox regulation of CEF in higher plants.

Footnotes

  • ↵1Present address: Department of Biology, Portland Community College, Portland, OR 97219.

  • ↵2To whom correspondence should be addressed. Email: kramerd8{at}msu.edu.

  • Author contributions: D.D.S., A.K.L., M.S.-C., J.E.F., V.G.M., and D.M.K. designed research; D.D.S., A.K.L., M.S.-C., and J.E.F. performed research; D.D.S., A.K.L., M.S.-C., and J.E.F. analyzed data; and D.D.S., A.K.L., and D.M.K. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1418223112/-/DCSupplemental.

Freely available online through the PNAS open access option.

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