Combined increases in mitochondrial cooperation and oxygen photoreduction compensate for deficiency in cyclic electron flow in Chlamydomonas reinhardtii

Plant Cell

Volumn 26, Issue 7, 2014, Pages 3036-3050

  Dang, Kieu Van ^a,b,c   Plet, Julie ^a,b,c   Tolleter, Dimitri ^a,b,c,e   Jokel, Martina ^d   Cuiné, Stéphan ^a,b,c   Carrier, Patrick ^a,b,c   Auroy, Pascaline ^a,b,c   Richaud, Pierre ^a,b,c   Johnson, Xenie ^a,b,c   Alric, Jean ^a,b,c   Allahverdiyeva, Yagut ^d   Peltier, Gilles ^a,b,c  

^a IRFM   (France)

^b CNRS   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d UNIVERSITY OF TURKU   (Finland)

^e AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CARBON DIOXIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; OXYGEN; PHOTOSYSTEM I; PHOTOSYSTEM II; PROTON;

CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; ELECTRON; ELECTRON TRANSPORT; GENE INACTIVATION; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; MITOCHONDRION; MUTATION; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHOTOSYSTEM II; RADIATION RESPONSE;

ADENOSINE TRIPHOSPHATE; CARBON DIOXIDE; CHLAMYDOMONAS REINHARDTII; CHLOROPLASTS; ELECTRON TRANSPORT; ELECTRONS; GENE KNOCKOUT TECHNIQUES; LIGHT; MITOCHONDRIA; MUTATION; NADP; OXIDATION-REDUCTION; OXYGEN; PHOTOSYNTHESIS; PHOTOSYSTEM I PROTEIN COMPLEX; PHOTOSYSTEM II PROTEIN COMPLEX; PROTONS;

EID: 84907375188     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.126375     Document Type: Article

References (64)

1. Allahverdiyeva, Y., Ermakova, M., Eisenhut, M., Zhang, P., Richaud, P., Hagemann, M., Cournac, L., and Aro, E.M. (2011). Interplay between flavodiiron proteins and photorespiration in Synechocystis sp. PCC 6803. J. Biol. Chem. 286: 24007-24014.
2. Allahverdiyeva, Y., Mustila, H., Ermakova, M., Bersanini, L., Richaud, P., Ajlani, G., Battchikova, N., Cournac, L., and Aro, E.M. (2013). Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proc. Natl. Acad. Sci. USA 110: 4111-4116.
3. Allen, J.F. (1975). Oxygen reduction and optimum production of ATP in photosynthesis. Nature 256: 599-600.
4. Allorent, G., et al. (2013). A dual strategy to cope with high light in Chlamydomonas reinhardtii. Plant Cell 25: 545-557.
5. Asada, K. (1999). The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 601-639.
6. Avenson, T.J., Cruz, J.A., Kanazawa, A., and Kramer, D.M. (2005). Regulating the proton budget of higher plant photosynthesis. Proc. Natl. Acad. Sci. USA 102: 9709-9713.
7. Badger, M.R. (1985). Photosynthetic oxygen-exchange. Annu. Rev. Plant Physiol. Plant Mol. Biol. 36: 27-53.
8. Beckmann, K., Messinger, J., Badger, M.R., Wydrzynski, T., and Hillier, W. (2009). On-line mass spectrometry: membrane inlet sampling. Photosynth. Res. 102: 511-522.
9. Bulté, L., Gans, P., Rebéillé, F., and Wollman, F.-A. (1990). ATP control on state transitions in vivo in Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1020: 72-80.
10. Cardol, P., Alric, J., Girard-Bascou, J., Franck, F., Wollman, F.A., and Finazzi, G. (2009). Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas. Proc. Natl. Acad. Sci. USA 106: 15979-15984.
11. Cournac, L., Latouche, G., Cerovic, Z., Redding, K., Ravenel, J., and Peltier, G. (2002). In vivo interactions between photosynthesis, mitorespiration, and chlororespiration in Chlamydomonas reinhardtii. Plant Physiol. 129: 1921-1928.
12. DalCorso, G., Pesaresi, P., Masiero, S., Aseeva, E., Schünemann, D., Finazzi, G., Joliot, P., Barbato, R., and Leister, D. (2008). A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132: 273-285.
13. Delepelaire, P., and Wollman, F.A. (1985). Correlations between fluorescence and phosphorylation changes in thylakoid membranes of Chlamydomonas reinhardtii in vivo-A kinetic analysis. Biochim. Biophys. Acta 809: 277-283.
14. Desplats, C., Mus, F., Cuiné, S., Billon, E., Cournac, L., and Peltier, G. (2009). Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts. J. Biol. Chem. 284: 4148-4157.
15. Dimon, B., Gans, P., and Peltier, G. (1988). Mass-spectrometric measurement of photosynthetic and respiratory oxygen-exchange. Methods Enzymol. 167: 686-691.
16. Duanmu, D., Miller, A.R., Horken, K.M., Weeks, D.P., and Spalding, M.H. (2009). Knockdown of limiting-CO2-induced gene HLA3 decreases HCO3-transport and photosynthetic Ci affinity in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 106: 5990-5995.
17. Eberhard, S., Finazzi, G., and Wollman, F.A. (2008). The dynamics of photosynthesis. Annu. Rev. Genet. 42: 463-515.
18. Fleischmann, M.M., Ravanel, S., Delosme, R., Olive, J., Zito, F., Wollman, F.-A., and Rochaix, J.-D. (1999). Isolation and characterization of photoautotrophic mutants of Chlamydomonas reinhardtii deficient in state transition. J. Biol. Chem. 274: 30987-30994.
19. Foyer, C.H., Neukermans, J., Queval, G., Noctor, G., and Harbinson, J. (2012). Photosynthetic control of electron transport and the regulation of gene expression. J. Exp. Bot. 63: 1637-1661.
20. Fridlyand, L.E. (1997). Models of CO2 concentrating mechanisms in microalgae taking into account cell and chloroplast structure. Biosystems 44: 41-57.
21. Harris, E.H. (1989). The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use. (San Diego, CA: Academic Press).
22. Helman, Y., Tchernov, D., Reinhold, L., Shibata, M., Ogawa, T., Schwarz, R., Ohad, I., and Kaplan, A. (2003). Genes encoding A-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr. Biol. 13: 230-235.
23. Hertle, A.P., Blunder, T., Wunder, T., Pesaresi, P., Pribil, M., Armbruster, U., and Leister, D. (2013). PGRL1 is the elusive ferredoxinplastoquinone reductase in photosynthetic cyclic electron flow. Mol. Cell 49: 511-523.
24. Hoefnagel, M.H.N., Atkin, O.K., and Wiskich, J.T. (1998). Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim. Biophys. Acta 1366: 235-255.
25. Iwai, M., Takizawa, K., Tokutsu, R., Okamuro, A., Takahashi, Y., and Minagawa, J. (2010). Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464: 1210-1213.
26. Jans, F., Mignolet, E., Houyoux, P.A., Cardol, P., Ghysels, B., Cuiné, S., Cournac, L., Peltier, G., Remacle, C., and 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.
27. Joët, T., Cournac, L., Horvath, E.M., Medgyesy, P., and 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.
28. Johnson, X., et al. (2014). Proton Gradient Regulation 5-mediated cyclic electron flow under ATP-or redox-limited conditions: a study of ΔATPase pgr5 and ΔrbcL pgr5 mutants in Chlamydomonas reinhardtii. Plant Physiol. 165: 438-452.
29. Joliot, P., and Johnson, G.N. (2011). Regulation of cyclic and linear electron flow in higher plants. Proc. Natl. Acad. Sci. USA 108: 13317-13322.
30. Karlsson, J., Ramazanov, Z., Hiltonen, T., Gardestrom, P., and Samuelsson, G. (1994). Effect of vanadate on photosynthesis and the ATP/ADP ratio in low-CO2-adapted Chlamydomonas reinhardtii cells. Planta 192: 46-51.
31. Klüghammer, C., and Schreiber, U. (2008). Saturation pulse method for assessment of energy conversion in PS I. PAM Application Notes 1: 11-14.
32. Kramer, D.M., and Evans, J.R. (2011). The importance of energy balance in improving photosynthetic productivity. Plant Physiol. 155: 70-78.
33. Krömer, S. (1995). Respiration during photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 45-70.
34. Krömer, S., and Heldt, H.W. (1991). On the role of mitochondrial oxidative phosphorylation in photosynthesis metabolism as studied by the effect of oligomycin on photosynthesis in protoplasts and leaves of barley (Hordeum vulgare). Plant Physiol. 95: 1270-1276.
35. Lemaire, C., Wollman, F.A., and Bennoun, P. (1988). Restoration of phototrophic growth in a mutant of Chlamydomonas reinhardtii in which the chloroplast atpB gene of the ATP synthase has a deletion: an example of mitochondria-dependent photosynthesis. Proc. Natl. Acad. Sci. USA 85: 1344-1348.
36. Lucker, B., and Kramer, D.M. (2013). Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability. Photosynth. Res. 117: 449-459.
37. Miura, K., Yamano, T., Yoshioka, S., Kohinata, T., Inoue, Y., Taniguchi, F., Asamizu, E., Nakamura, Y., Tabata, S., Yamato, K.T., Ohyama, K., and Fukuzawa, H. (2004). Expression profilingbased identification of CO2-responsive genes regulated by CCM1 controlling a carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol. 135: 1595-1607.
38. Millar, A.H., Whelan, J., Soole, K.L., and Day, D.A. (2011). Organization and regulation of mitochondrial respiration in plants. Annu. Rev. Plant Biol. 62: 79-104.
39. Munekage, Y., Hojo, M., Meurer, J., Endo, T., Tasaka, M., and Shikanai, T. (2002). PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110: 361-371.
40. Munekage, Y., Hashimoto, M., Miyake, C., Tomizawa, K., Endo, T., Tasaka, M., and Shikanai, T. (2004). Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429: 579-582.
41. Munekage, Y.N., Genty, B., and Peltier, G. (2008). Effect of PGR5 impairment on photosynthesis and growth in Arabidopsis thaliana. Plant Cell Physiol. 49: 1688-1698.
42. Niyogi, K.K. (2000). Safety valves for photosynthesis. Curr. Opin. Plant Biol. 3: 455-460.
43. Osmond, C.B. (1981). Photorespiration and photoinhibition. Some implications for the energetics of photosynthesis. Biochim. Biophys. Acta 639: 77-98.
44. Peers, G., Truong, T.B., Ostendorf, E., Busch, A., Elrad, D., Grossman, A.R., Hippler, M., and Niyogi, K.K. (2009). An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462: 518-521.
45. Peltier, G., and Thibault, P. (1985). Oxygen uptake in the light in Chlamydomonas. Evidence for persistent mitochondrial respiration. Plant Physiol. 79: 225-230.
46. Peltier, G., Tolleter, D., Billon, E., and Cournac, L. (2010). Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth. Res. 106: 19-31.
47. Petroutsos, D., Terauchi, A.M., Busch, A., Hirschmann, I., Merchant, S.S., Finazzi, G., and Hippler, M. (2009). PGRL1 participates in iron-induced remodeling of the photosynthetic apparatus and in energy metabolism in Chlamydomonas reinhardtii. J. Biol. Chem. 284: 32770-32781.
48. Ravenel, J., Peltier, G., and Havaux, M. (1994). The cyclic electron pathways around photosystem-I in Chlamydomonas reinhardtii as determined in vivo by photoacoustic measurements of energy storage. Planta 193: 251-259.
49. Rumeau, D., Bécuwe-Linka, N., Beyly, A., Louwagie, M., Garin, J., and Peltier, G. (2005). New subunits NDH-M,-N, and-O, encoded by nuclear genes, are essential for plastid Ndh complex functioning in higher plants. Plant Cell 17: 219-232.
50. Rutherford, A.W., Osyczka, A., and Rappaport, F. (2012). Backreactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O(2). FEBS Lett. 586: 603-616.
51. Scheibe, R. (2004). Malate valves to balance cellular energy supply. Physiol. Plant. 120: 21-26.
52. Schreiber, U., Schliwa, U., and Bilger, W. (1986). Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10: 51-62.
53. Shen, W., Wei, Y., Dauk, M., Tan, Y., Taylor, D.C., Selvaraj, G., and Zou, J. (2006). Involvement of a glycerol-3-phosphate dehydrogenase in modulating the NADH/NAD+ ratio provides evidence of a mitochondrial glycerol-3-phosphate shuttle in Arabidopsis. Plant Cell 18: 422-441.
54. Sultemeyer, D., Biehler, K., and Fock, H.P. (1993). Evidence for the contribution of pseudocyclic photophosphorylation to the energy requirement of the mechanism for concentrating inorganic carbon in Chlamydomonas. Planta 189: 235-242.
55. Suorsa, M., Järvi, S., Grieco, M., Nurmi, M., Pietrzykowska, M., Rantala, M., Kangasjärvi, S., Paakkarinen, V., Tikkanen, M., Jansson, S., and Aro, E.-M. (2012). PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24: 2934-2948.
56. Takahashi, H., Clowez, S., Wollman, F.-A., Vallon, O., and Rappaport, F. (2013). Cyclic electron flow is redox-controlled but independent of state transition. Nat. Commun. 4: 1954.
57. Terashima, M., Petroutsos, D., Hüdig, M., Tolstygina, I., Trompelt, K., Gäbelein, P., Fufezan, C., Kudla, J., Weinl, S., Finazzi, G., and Hippler, M. (2012). Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex. Proc. Natl. Acad. Sci. USA 109: 17717-17722.
58. Tikkanen, M., Grieco, M., Kangasjärvi, S., and Aro, E.M. (2010). Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol. 152: 723-735.
59. Tolleter, D., et al. (2011). Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 23: 2619-2630.
60. Vicente, J.B., Gomes, C.M., Wasserfallen, A., and Teixeira, M. (2002). Module fusion in an A-type flavoprotein from the cyanobacterium Synechocystis condenses a multiple-component pathway in a single polypeptide chain. Biochem. Biophys. Res. Commun. 294: 82-87.
61. Wollman, F.A., and Delepelaire, P. (1984). Correlation between changes in light energy distribution and changes in thylakoid membrane polypeptide phosphorylation in Chlamydomonas reinhardtii. J. Cell Biol. 98: 1-7.
62. Yamano, T., Tsujikawa, T., Hatano, K., Ozawa, S., Takahashi, Y., and Fukuzawa, H. (2010). Light and low-CO2-dependent LCIBLCIC complex localization in the chloroplast supports the carbonconcentrating mechanism in Chlamydomonas reinhardtii. Plant Cell Physiol. 51: 1453-1468.
63. Zhang, P., Allahverdiyeva, Y., Eisenhut, M., and Aro, E.-M. (2009). Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803. PLoS ONE 4: e5331.
64. Zhang, P., Eisenhut, M., Brandt, A.M., Carmel, D., Silén, H.M., Vass, I., Allahverdiyeva, Y., Salminen, T.A., and Aro, E.M. (2012). Operon flv4-flv2 provides cyanobacterial photosystem II with flexibility of electron transfer. Plant Cell 24: 1952-1971.