Planta

, Volume 237, Issue 5, pp 1241–1250 | Cite as

Antimycin A effect on the electron transport in chloroplasts of two Chlamydomonas reinhardtii strains

  • Taras K. Antal
  • Galina P. Kukarskikh
  • Alexander A. Bulychev
  • Esa Tyystjärvi
  • Tatyana Krendeleva
Original Article

Abstract

The effects of antimycin A on the redox state of plastoquinone and on electron donation to photosystem I (PS I) were studied in sulfur-deprived Chlamydomonas reinhardtii cells of the strains cc406 and 137c. We found that this reagent suppresses cyclic electron flow around PS I in the cc406 strain, whereas this inhibitory effect was completely absent in the 137c strain. In the latter strain, antimycin A induced rapid reduction of plastoquinone in the dark and considerably enhanced the rate of electron donation to P700 + in the dark. Importantly, neither myxothiazol, an inhibitor of mitochondrial respiration, FCCP, a protonophore, nor propyl gallate, an inhibitor of the plastid terminal oxidase, induced such a strong effect like antimycin A. The results indicate that in the chloroplast of the 137c strain, antimycin A has a site of action outside of the machinery of cyclic electron flow.

Keywords

Antimycin A Chlamydomonas Hydrogen Sulfur deprivation 

Abbreviations

AA

Antimycin A

DCMU3

3-(3,4-dichlorophenyl)-1,1-dimethylurea

CEF

Cyclic electron flow around PS I

FQR

Ferredoxin-quinone reductase

Chl

Chlorophyll

ETC

Electron transport chain

FCCP

Carbonylcyanide-p-trifluoromethoxyphenyl-hydrazone

Fd

Ferredoxin

FNR

Ferredoxin-NADP reductase

Mxt

Myxothyazol

MV

Methyl viologen

NDH

NADH dehydrogenase

PPFD

Photosynthetic photon flux density

PQ

Plastoquinon

Pc

Plastocyanin

PTOX

Plastid terminal oxidase

Notes

Acknowledgments

This study was supported by the Russian Federal Target Programme (8077) (TA, GK, TK). ET thanks European Regional Development Fund (Bio Refine Tech program) for financial support.

References

  1. Alric J, Lavergne J, Rappaport F (2010) Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii (I) aerobic conditions. Biochim Biophys Acta 1797:44–51PubMedGoogle Scholar
  2. Antal TK, Lindblad P (2005) Production of H2 by sulphur-deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp. PCC 6803 during dark incubation with methane or at various extracellular pH. J Appl Microbiol 98:114–120PubMedCrossRefGoogle Scholar
  3. Antal TK, Volgusheva AA, Kukarskih GP, Krendeleva TE, Rubin AB (2009) Relationships between H2 photoproduction and different electron transport pathways in sulfur-deprived Chlamydomonas reinhardtii. Int J Hydrogen Energy 34:9087–9094CrossRefGoogle Scholar
  4. Antal TK, Mattila H, Hakala-Yatkin M, Tyystjärvi T, Tyystjärvi E (2010) Acclimation of photosynthesis to nitrogen deficiency in Phaseolus vulgaris. Planta 232:887–898PubMedCrossRefGoogle Scholar
  5. Antal TK, Krendeleva TE, Rubin AB (2011) Acclimation of green algae to sulfur deficiency stress: underlying mechanisms and application for hydrogen production. Appl Microbiol Biotechnol 89:3–15PubMedCrossRefGoogle Scholar
  6. Bendall DS (1982) Photosynthetic cytochromes of oxygenic organisms. Biochim Biophys Acta 683:119–151CrossRefGoogle Scholar
  7. Bukhov NG, Wiese C, Neimanis S, Heber U (1999) Heat sensitivity of chloroplasts and leaves: leakage of protons from thylakoids and reversible activation of cyclic electron transport. Photosynth Res 59:81–93CrossRefGoogle Scholar
  8. Chemeris YuK, Shenderova LV, Venediktov PS (1996) Chloroplast respiration in Chlorella pyrenoidosa CALU-175: effects of nitrogen deficiency, exogenous glucose, and elevated temperature. Rus Plant Physiol 43:541–547Google Scholar
  9. Cleland R, Bendall D (1992) Photosystem I cyclic electron transport: measurement of ferredoxin-plastoquinone reductase activity. Photosynth Res 34:409–418CrossRefGoogle Scholar
  10. Cournac L, Redding K, Ravenel J, Rumeau D, Josse EM, Kuntz M, Peltier G (2000) Electron flow between PS II and oxygen in chloroplasts of PS I deficient algae is mediated by a quinol oxidase involved in chlororespiration. J Biol Chem 275:17256–17262PubMedCrossRefGoogle Scholar
  11. Cournac L, Mus F, Bernard L, Guedeney G, Vignais P, Peltier G (2002) Limiting steps in hydrogen production in Chlamydomonas reinhardtii and Synechocystis PCC 6803 as analyzed by light-induced gas exchange transients. Int J Hydrog Energy 27:1229–1237CrossRefGoogle Scholar
  12. Cruz JA, Salbilla BA, Kanazawa A, Kramer DM (2001) Inhibition of plastocyanin to P(700)(+) electron transfer in Chlamydomonas reinhardtii by hyperosmotic stress. Plant Physiol 127:1167–1179PubMedCrossRefGoogle Scholar
  13. Finazzi G, Rappaport F, Furia A, Fleischmann M, Rochaix JD, Zito F, Forti G (2002) Involvement of state transition in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii. EMBO Rep 3:280–285PubMedCrossRefGoogle Scholar
  14. Houille-Vernes L, Rappaport F, Wollman F-A, Alric J, Johnson X (2011) Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. Proc Natl Acad Sci USA 108:20820–20825PubMedCrossRefGoogle Scholar
  15. Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–1213PubMedCrossRefGoogle Scholar
  16. Jans F, Mignolet E, Houyoux P-A, Cardol P, Ghysels B, Cuink S, Cournac L, Peltier G, Remacle C, Franck F (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci USA 105:20546–20551PubMedCrossRefGoogle Scholar
  17. Joët T, Cournac L, Horvath EM, Medgyesy P, Peltier G (2001) Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around photosystem I. Plant Physiol 125:1919–1929PubMedCrossRefGoogle Scholar
  18. Johnson X, Alric J (2012) Interaction between starch breakdown, acetate assimilation, and photosynthetic cyclic electron flow in Chlamydomonas reinhardtii. J Biol Chem 287:26445–26452PubMedCrossRefGoogle Scholar
  19. Joliot P, Joliot A (2005) Quantification of cyclic and linear flows in plants. Proc Natl Acad Sci USA 102:4913–4918PubMedCrossRefGoogle Scholar
  20. Kruse O, Rupprecht J, Bader K, Thomas-Hall S, Schenk PM, Finazzi G, Hankamer B (2005) Improved photobiological H2 production in engineered green algal cells. J Biol Chem 280:34170–34177PubMedCrossRefGoogle Scholar
  21. Laźar D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct Plant Biol 33:9–30CrossRefGoogle Scholar
  22. Lennon RE (1973) Antimycin A, a piscicidal antibiotic. Adv Appl Microbiol 16:55–96PubMedCrossRefGoogle Scholar
  23. Maxwell PC, Biggins J (1976) Role of cyclic electron transport in photosynthesis as measured by the photoinduced turnover of P700 in vivo. Biochemistry 15:3975–3981PubMedCrossRefGoogle Scholar
  24. Melis A, Zhang L, Forestier M, Ghirardi M, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122:127–136PubMedCrossRefGoogle Scholar
  25. Moss DA, Bendall DS (1984) Cyclic electron transport in chloroplasts. The Q-cycle and the site of action of antimycin. Biochim Biophys Acta 767:389–395CrossRefGoogle Scholar
  26. Nguyen AV, Toepel J, Burgess S, Uhmeyer A, Blifernez O, Doebbe A, Hankamer B, Nixon P, Wobbe L, Kruse O (2011) Time-course global expression profiles of Chlamydomonas reinhardtii during photo-biological H2 production. PLoS ONE 6:e29364PubMedCrossRefGoogle Scholar
  27. Nixon PJ (2000) Chlororespiration. Phil Trans R Soc Lond B 355:1541–1547CrossRefGoogle Scholar
  28. Oja V, Eichelmann H, Peterson RB, Rasulov B, Laisk A (2003) Deciphering the 820 nm signal: redox state of donor side and quantum yield of photosystem I in leaves. Photosynth Res 78:1–15PubMedCrossRefGoogle Scholar
  29. Peltier G, Schmidt GW (1991) Chlororespiration: an adaptation to nitrogen deficiency in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 88:4791–4795PubMedCrossRefGoogle Scholar
  30. Ravenel J, Peltier G (1991) Inhibition of chlororespiration by myxothiazol and antimycin A in Chlamydomonas reinhardtii. Photosynth Res 28:141–148CrossRefGoogle Scholar
  31. Rochaix JD (2011) Regulation of photosynthetic electron transport. Biochim Biophys Acta 1807:878–886PubMedCrossRefGoogle Scholar
  32. Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PS I during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051PubMedCrossRefGoogle Scholar
  33. Schansker G, Toth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta 1706:250–261PubMedCrossRefGoogle Scholar
  34. Tagawa K, Tsujimoto HY, Arnon Dl (1963) Role of chloroplast ferredoxin in the energy conversion process of photosynthesis. Proc Natl Acd Sci USA 49:567–572CrossRefGoogle Scholar
  35. Tolleter D, Ghysels B, Alric J, Petroutsos D, Tolstygina I, Krawietz D, Happe T, Auroy P, Adriano JM, Beyly A, Cuiné S, Plet J, Reiter IM, Genty B, Cournac L, Hippler M, Peltier G (2011) Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 23:2619–2630PubMedCrossRefGoogle Scholar
  36. Wykoff DD, Davies JP, Melis A, Grossman A (1998) The effects of phosphorus and sulfur deprivation on photosynthetic electron transport in Chlamydomonas reinhardtii. Plant Physiol 117:129–139PubMedCrossRefGoogle Scholar
  37. Yerkes CT, Crofts AR (1995) Antimycin inhibits qE-quenching by a protonophoric mechanism. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol 3. Kluwer Academic Publishers, Dordrecht, pp 115–118Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Taras K. Antal
    • 1
  • Galina P. Kukarskikh
    • 1
  • Alexander A. Bulychev
    • 1
  • Esa Tyystjärvi
    • 2
  • Tatyana Krendeleva
    • 1
  1. 1.Biological FacultyMoscow State UniversityMoscowRussia
  2. 2.Department of Biochemistry and Food Chemistry Molecular Plant BiologyUniversity of TurkuTurkuFinland

Personalised recommendations