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.
Similar content being viewed by others
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
References
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 1797:44–51
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 98:114–120
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 34:9087–9094
Antal TK, Mattila H, Hakala-Yatkin M, Tyystjärvi T, Tyystjärvi E (2010) Acclimation of photosynthesis to nitrogen deficiency in Phaseolus vulgaris. Planta 232:887–898
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 89:3–15
Bendall DS (1982) Photosynthetic cytochromes of oxygenic organisms. Biochim Biophys Acta 683:119–151
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 59:81–93
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 43:541–547
Cleland R, Bendall D (1992) Photosystem I cyclic electron transport: measurement of ferredoxin-plastoquinone reductase activity. Photosynth Res 34:409–418
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 275:17256–17262
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 27:1229–1237
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 127:1167–1179
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 3:280–285
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 108:20820–20825
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 464:1210–1213
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 105:20546–20551
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 125:1919–1929
Johnson X, Alric J (2012) Interaction between starch breakdown, acetate assimilation, and photosynthetic cyclic electron flow in Chlamydomonas reinhardtii. J Biol Chem 287:26445–26452
Joliot P, Joliot A (2005) Quantification of cyclic and linear flows in plants. Proc Natl Acad Sci USA 102:4913–4918
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 280:34170–34177
Laźar D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct Plant Biol 33:9–30
Lennon RE (1973) Antimycin A, a piscicidal antibiotic. Adv Appl Microbiol 16:55–96
Maxwell PC, Biggins J (1976) Role of cyclic electron transport in photosynthesis as measured by the photoinduced turnover of P700 in vivo. Biochemistry 15:3975–3981
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 122:127–136
Moss DA, Bendall DS (1984) Cyclic electron transport in chloroplasts. The Q-cycle and the site of action of antimycin. Biochim Biophys Acta 767:389–395
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:e29364
Nixon PJ (2000) Chlororespiration. Phil Trans R Soc Lond B 355:1541–1547
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 78:1–15
Peltier G, Schmidt GW (1991) Chlororespiration: an adaptation to nitrogen deficiency in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 88:4791–4795
Ravenel J, Peltier G (1991) Inhibition of chlororespiration by myxothiazol and antimycin A in Chlamydomonas reinhardtii. Photosynth Res 28:141–148
Rochaix JD (2011) Regulation of photosynthetic electron transport. Biochim Biophys Acta 1807:878–886
Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PS I during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051
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 1706:250–261
Tagawa K, Tsujimoto HY, Arnon Dl (1963) Role of chloroplast ferredoxin in the energy conversion process of photosynthesis. Proc Natl Acd Sci USA 49:567–572
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 23:2619–2630
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 117:129–139
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 115–118
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Antal, T.K., Kukarskikh, G.P., Bulychev, A.A. et al. Antimycin A effect on the electron transport in chloroplasts of two Chlamydomonas reinhardtii strains. Planta 237, 1241–1250 (2013). https://doi.org/10.1007/s00425-013-1843-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-013-1843-y