Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii: (II) Involvement of the PGR5-PGRL1 pathway under anaerobic conditions

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1837, Issue 6, 2014, Pages 825-834

  Alric, Jean ^a,b  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^b University of Aix Marseille   (France)

Author keywords

Chlamydomonas reinhardtii; Electron transfer; Green algae; Photosystem I

Indexed keywords

ADENOSINE TRIPHOSPHATE; PHOTOSYNTHESIS;

ADAPTATION; ARTICLE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYLL CONTENT; ELECTRON; ELECTRON TRANSPORT; GREEN ALGA; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXYGEN TENSION; PHOTOCHEMISTRY; PHOTOSYNTHESIS; PHOTOSYNTHETIC RATE; PRIORITY JOURNAL; THYLAKOID MEMBRANE; ANAEROBIC GROWTH; KINETICS; METABOLISM; PHYSIOLOGY;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA;

ADENOSINE TRIPHOSPHATE; ANAEROBIOSIS; CHLAMYDOMONAS REINHARDTII; ELECTRONS; KINETICS; OXIDATION-REDUCTION; PHOTOSYNTHESIS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS;

EID: 84896690323     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2014.01.024     Document Type: Article

References (66)

1. J. Alric, J. Lavergne, and F. Rappaport Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii (I) aerobic conditions Biochim. Biophys. Acta 1797 1 2010 44 51
2. D.I. Arnon, M.B. Allen, and F.R. Whatley Photosynthesis by isolated chloroplasts Nature 174 4426 1954 394 396
3. D.I. Arnon, and R.K. Chain Regulation of ferredoxin-catalyzed photosynthetic phosphorylations Proc. Natl. Acad. Sci. U. S. A. 72 12 1975 4961 4965
4. J. Alric Cyclic electron flow around photosystem I in unicellular green algae Photosynth. Res. 106 1-2 2010 47 56
5. D.S. Bendall, and R.S. Manasse Cyclic photophosphorylation and electron-transport Biochim. Biophys. Acta Bioenerg. 1229 1 1995 23 38
6. P. Joliot, and A. Joliot Quantification of cyclic and linear flows in plants Proc. Natl. Acad. Sci. U. S. A. 102 13 2005 4913 4918 (Pubitemid 40471553)
7. 2 fixation by iodoacetamide stimulates cyclic electron flow and non-photochemical quenching upon far-red illumination Photosynth. Res. 115 1 2013 55 63
8. D. Crowther, and G. Hind Partial characterization of cyclic electron transport in intact chloroplasts Arch. Biochem. Biophys. 204 2 1980 568 577
9. J.D. Mills, R.E. Slovacek, and G. Hind Cyclic electron transport in isolated intact chloroplasts. Further studies with antimycin Biochim. Biophys. Acta 504 2 1978 298 309 (Pubitemid 9038357)
10. 2-fixation Biochim. Biophys. Acta 592 3 1980 495 505
11. J.P. Hosler, and C.F. Yocum Regulation of cyclic photophosphorylation during ferredoxin-mediated electron transport: effect of DCMU and the NADPH/NADP ratio Plant Physiol. 83 4 1987 965 969
12. J.F. Allen Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain Trends Plant Sci. 8 1 2003 15 19 (Pubitemid 36725962)
13. A. Courteille et al. Thioredoxin m4 controls photosynthetic alternative electron pathways in Arabidopsis Plant Physiol. 161 1 2013 508 520
14. A.P. Hertle et al. PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow Mol. Cell 49 3 2013 511 523
15. P.V. Sane, Dj Goodchil, and R.B. Park Characterization of chloroplast photosystems-1 and photosystems-2 separated by a non-detergent method Biochim. Biophys. Acta 216 1 1970 168 178
16. B. Andersson, and J.M. Anderson Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts Biochim. Biophys. Acta 593 2 1980 427 440
17. R.P. Cox, and B. Andersson Lateral and transverse organisation of cytochromes in the chloroplast thylakoid membrane Biochem. Biophys. Res. Commun. 103 4 1981 1336 1342
18. J.M. Anderson Distribution of the cytochromes of spinach chloroplasts between the appressed membranes of grana stacks and stroma-exposed thylakoid regions FEBS Lett. 138 1 1982 62 66
19. F.A. Wollman State transitions reveal the dynamics and flexibility of the photosynthetic apparatus EMBO J. 20 14 2001 3623 3630
20. O. Vallon et al. Lateral redistribution of cytochrome b6/f complexes along thylakoid membranes upon state transitions Proc. Natl. Acad. Sci. U. S. A. 88 18 1991 8262 8266 (Pubitemid 21915337)
21. G. Forti et al. In vivo changes of the oxidation-reduction state of NADP and of the ATP/ADP cellular ratio linked to the photosynthetic activity in Chlamydomonas reinhardtii Plant Physiol. 132 3 2003 1464 1474 (Pubitemid 36872895)
22. G. Finazzi et al. Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii EMBO Rep. 3 3 2002 280 285 (Pubitemid 34269523)
23. G. Finazzi et al. Nonphotochemical quenching of chlorophyll fluorescence in Chlamydomonas reinhardtii Biochemistry 45 5 2006 1490 1498 (Pubitemid 43214814)
24. G. Finazzi et al. State transitions, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii Biochim. Biophys. Acta 1413 3 1999 117 129 (Pubitemid 29507551)
25. G. Finazzi, and G. Forti Metabolic flexibility of the green alga Chlamydomonas reinhardtii as revealed by the link between state transitions and cyclic electron flow Photosynth. Res. 82 3 2004 327 338 (Pubitemid 40032965)
26. G. Finazzi et al. Photoinhibition of Chlamydomonas reinhardtii in state 1 and state 2: damages to the photosynthetic apparatus under linear and cyclic electron flow J. Biol. Chem. 276 25 2001 22251 22257
27. G. Finazzi The central role of the green alga Chlamydomonas reinhardtii in revealing the mechanism of state transitions J. Exp. Bot. 56 411 2005 383 388 (Pubitemid 40263285)
28. H. Takahashi et al. Cyclic electron flow is redox-controlled but independent of state transition Nat. Commun. 4 2013 1954
29. M. Iwai et al. Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis Nature 464 7292 2010 1210 1213
30. D. Strand, A. Livingston, and D. Kramer Do state transitions control CEF1 in higher plants? Photosynthesis Research for Food, Fuel and the Future 2013 Springer Berlin/Heidelberg 286 289
31. B. Lucker, and D.M. Kramer Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability Photosynth. Res. 117 1-3 2013 449 459
32. P. Joliot, and A. Joliot Cyclic electron flow in C3 plants Biochim. Biophys. Acta 1757 5-6 2006 362 368 (Pubitemid 43993840)
33. X. Johnson, and J. Alric Interaction between starch breakdown, acetate assimilation, and photosynthetic cyclic electron flow in Chlamydomonas reinhardtii J. Biol. Chem. 287 31 2012 26445 26452
34. X. Johnson, and J. Alric Central carbon metabolism and electron transport in Chlamydomonas reinhardtii: metabolic constraints for carbon partitioning between oil and starch Eukaryot. Cell 12 6 2013 776 793
35. L. Houille-Vernes et al. Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas Proc. Natl. Acad. Sci. U. S. A. 108 51 2011 20820 20825
36. F. Jans et al. A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas Proc. Natl. Acad. Sci. U. S. A. 105 51 2008 20546 20551
37. D. Tolleter et al. Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii Plant Cell 23 7 2011 2619 2630
38. D.A. Moss, and D.S. Bendall Cyclic electron-transport in chloroplasts - the Q-cycle and the site of action of antimycin Biochim. Biophys. Acta 767 3 1984 389 395
39. X. Johnson et al. PGR5-mediated Cyclic Electron Flow under ATP- or Redox-limiting Conditions, a Study of Pgr5 ΔATPase and Pgr5 ΔrbcL Mutants in Chlamydomonas reinhardtii Plant Physiol. 2014 (accepted in revised form)
40. D. Leister, and T. Shikanai Complexities and protein complexes in the antimycin A-sensitive pathway of cyclic electron flow in plants Front. Plant Sci. 4 2013 161
41. P. Cardol et al. Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas Proc. Natl. Acad. Sci. U. S. A. 106 37 2009 15979 15984
42. N. Depege, S. Bellafiore, and J.D. Rochaix Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas Science 299 5612 2003 1572 1575 (Pubitemid 36297706)
43. G. Peers et al. An ancient light-harvesting protein is critical for the regulation of algal photosynthesis Nature 462 7272 2009 518 521
44. P. Delepelaire, and F.A. Wollman Correlations between fluorescence and phosphorylation changes in thylakoid membranes of Chlamydomonas reinhardtii in vivo: a kinetic analysis Biochim. Biophys. Acta Bioenerg. 809 2 1985 277 283 (Pubitemid 15019069)
45. F.A. Wollman, and P. Delepelaire Correlation between changes in light energy distribution and changes in thylakoid membrane polypeptide phosphorylation in Chlamydomonas reinhardtii J. Cell Biol. 98 1 1984 1 7 (Pubitemid 14220460)
46. I.D. Kuntz, and M. Calvin Kinetic studies of the two light reactions in photosynthesis Photochem. Photobiol. 4 3 1965 537 548
47. K. Takizawa et al. The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf Biochim. Biophys. Acta 1767 10 2007 1233 1244 (Pubitemid 47498308)
48. C.A. Sacksteder, and D.M. Kramer Dark-interval relaxation kinetics (DIRK) of absorbance changes as a quantitative probe of steady-state electron transfer Photosynth. Res. 66 1-2 2000 145 158 (Pubitemid 32540456)
49. C.A. Sacksteder et al. The proton to electron stoichiometry of steady-state photosynthesis in living plants: a proton-pumping Q cycle is continuously engaged Proc. Natl. Acad. Sci. U. S. A. 97 26 2000 14283 14288 (Pubitemid 32016568)
50. P. Joliot, and A. Joliot Cyclic electron transfer in plant leaf Proc. Natl. Acad. Sci. U. S. A. 99 15 2002 10209 10214 (Pubitemid 34831197)
51. J.A. Cruz et al. Contribution of electric field (Delta psi) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into Delta psi and Delta pH by ionic strength Biochemistry 40 5 2001 1226 1237 (Pubitemid 32142884)
52. T.J. Avenson, J.A. Cruz, and D.M. Kramer Modulation of energy-dependent quenching of excitons in antennae of higher plants Proc. Natl. Acad. Sci. U. S. A. 101 15 2004 5530 5535 (Pubitemid 38481191)
53. C. Klughammer, K. Siebke, and U. Schreiber Continuous ECS-indicated recording of the proton-motive charge flux in leaves Photosynth. Res. 117 1-3 2013 471 487
54. D.I. Arnon Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris Plant Physiol. 24 1 1949 1 15
55. P.J. Neale, and A. Melis Algal photosynthetic membrane complexes and the photosynthesis-irradiance curve: a comparison of light-adaptation responses in Chlamydomonas reinhardtii (CHLOROPHYTA)1 J. Phycol. 22 4 1986 531 538
56. P. Joliot, and R. Delosme Flash-induced 519 nm absorption change in green algae Biochim. Biophys. Acta Bioenerg. 357 2 1974 267 284
57. Y.V. Bolychevtseva et al. Effects of oxygen and photosynthesis carbon cycle reactions on kinetics of P700 redox transients in cyanobacterium Arthrospira platensis cells Biochemistry (Mosc) 72 3 2007 275 281
58. B. Ghysels et al. Function of the chloroplast hydrogenase in the microalga Chlamydomonas: the role of hydrogenase and state transitions during photosynthetic activation in anaerobiosis PLoS One 8 5 2013 e64161
59. L. Bulté et al. ATP control on state transitions in vivo in Chlamydomonas reinhardtii Biochim. Biophys. Acta Bioenerg. 1020 1 1990 72 80
60. G. Peltier, and P. Thibault O(2) uptake in the light in Chlamydomonas: evidence for persistent mitochondrial respiration Plant Physiol. 79 1 1985 225 230
61. D.F. Sueltemeyer, K. Klug, and H.P. Fock Effect of photon fluence rate on oxygen evolution and uptake by Chlamydomonas reinhardtii suspensions grown in ambient and CO(2)-enriched air Plant Physiol. 81 2 1986 372 375
62. P.C. Maxwell, and J. Biggins Role of cyclic electron-transport in photosynthesis as measured by photoinduced turnover of P-700 in vivo Biochemistry 15 18 1976 3975 3981
63. K. Brettel, and W. Leibl Electron transfer in photosystem I Biochim. Biophys. Acta 1507 1-3 2001 100 114 (Pubitemid 33001515)
64. P. Horton et al. Regulation of phosphorylation of chloroplast membrane polypeptides by the redox state of plastoquinone FEBS Lett. 125 2 1981 193 196
65. J.F. Allen et al. Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems Nature 291 1981 25 29
66. M. Hirasawa et al. Oxidation-reduction properties of chloroplast thioredoxins, ferredoxin:thioredoxin reductase, and thioredoxin f-regulated enzymes Biochemistry 38 16 1999 5200 5205