Physiological links among alternative electron transport pathways that reduce and oxidize plastoquinone in Arabidopsis

Plant Journal

Volumn 63, Issue 3, 2010, Pages 458-468

  Okegawa, Yuki ^a,b,c   Kobayashi, Yoshichika ^a   Shikanai, Toshiharu ^b  

^a KYUSHU UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c KYOTO SANGYO UNIVERSITY   (Japan)

Author keywords

chloroplast; immutans; plastid terminal oxidase; PSI cyclic electron transport; redox regulation; variegation

Indexed keywords

ARABIDOPSIS; CHLOROPLAST DEVELOPMENT; CYCLIC ELECTRON TRANSPORT; DOUBLE MUTANTS; ELECTRON TRANSPORT; IN-VIVO; MATURE LEAVES; PHOTOSYSTEM I; PLASTOQUINONE; PQ POOL; PROTON GRADIENT; REDOX REGULATION; TERMINAL OXIDASE; THYLAKOID MEMBRANES;

CHLOROPHYLL; ELECTRON TRANSITIONS; ELECTRON TRANSPORT PROPERTIES; OXYGEN; PHOTOSYNTHESIS; PLANTS (BOTANY);

TRANSPORTATION ROUTES;

ARABIDOPSIS;

PLASTOQUINONE;

ARABIDOPSIS; ELECTRON TRANSPORT; GENETICS; METABOLISM; MUTATION; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF;

ARABIDOPSIS; ELECTRON TRANSPORT; MUTATION; OXIDATION-REDUCTION; PHOTOSYNTHESIS; PLANT LEAVES; PLASTOQUINONE;

EID: 77954912134     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04252.x     Document Type: Article

References (48)

1. Aluru, M.R. Rodermel, S.R. (2004) Control of chloroplast redox by the IMMUTANS terminal oxidase. Physiol. Plant. 120, 4 11.
2. Aluru, M.R., Yu, F., Fu, A. Rodermel, S. (2006) Arabidopsis variegation mutants: new insights into chloroplast biogenesis. J. Exp. Bot. 57, 1871 1881.
3. Aluru, M.R., Stessman, D.J., Spalding, M.H. Rodermel, S.R. (2007) Alterations in photosynthesis in Arabidopsis lacking IMMUTANS, a chloroplast terminal oxidase. Photosynth. Res. 91, 11 23.
4. Arnon, D.I. (1949) Copper enzyme in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24, 1 15.
5. Baerr, J.N., Thomas, J.D., Taylor, B.G., Rodermel, S.R. Gray, G.R. (2005) Differential photosynthetic compensatory mechanisms exist in the immutans mutant of Arabidopsis thaliana. Physiol. Plant. 124, 390 402.
6. Bennoun, P. (1982) Evidence for a respiratory chain in the chloroplast. Proc. Natl Acad. Sci. USA, 79, 4352 4356.
7. Burrows, P.A., Sazanov, L.A., Svab, Z., Maliga, P. Nixon, P.J. (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J. 17, 868 876.
8. Carol, P., Stevenson, D., Bisanz, C., Breitenbach, J., Sandmann, G., Mache, R., Coupland, G. Kuntz, M. (1999) Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell, 11, 57 68.
9. Cournac, L., Redding, K., Ravenel, J., Rumeau, D., Josse, E.M., Kuntz, M. Peltier, G. (2000) Electron flow between photosystem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration. J. Biol. Chem. 275, 17256 17262.
10. DalCorso, G., Pesaresi, P., Masiero, S., Aseeva, E., Schünemann, D., Finazzi, G., Joliot, P., Barbato, R. 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.
11. Desplats, C., Mus, F., Cuine, S., Billon, E., Cournac, L. Peltier, G. (2009) Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts. J. Biol. Chem. 284, 4148 4157.
12. Endo, T., Shikanai, T., Takabayashi, A., Asada, K. Sato, F. (1999) The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett. 457, 5 8.
13. Genty, B., Briantais, J.M. Baker, N.R. (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta, 990, 87 92.
14. Hashimoto, M., Endo, T., Peltier, G., Tasaka, M. Shikanai, T. (2003) A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. Plant J. 36, 541 549.
15. Heyno, E., Gross, C.M., Laureau, C., Culcasi, M., Pietri, S. Krieger-Liszkay, A. (2009) Plastid alternative oxidase (PTOX) promotes oxidative stress when overexpressed in tobacco. J. Biol. Chem. 284, 31174 31180.
16. Joët, T., Genty, B., Josse, E.M., Kuntz, M., Cournac, L. Peltier, G. (2002) Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J. Biol. Chem. 277, 31623 31630.
17. Josse, E.M., Simkin, A.J., Gaffe, J., Laboure, A.M., Kuntz, M. Carol, P. (2000) A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol. 123, 1427 1436.
18. A redox state and excitation energy fluxes. Photosynth. Res. 79, 209 218.
19. Krause, G.H. Weis, E. (1991) Chlorophyll fluorescence and photosynthesis - the basics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 313 349.
20. Lennon, A.M., Prommeenate, P. Nixon, P.J. (2003) Location, expression and orientation of the putative chlororespiratory enzymes, Ndh and IMMUTANS, in higher-plant plastids. Planta, 218, 254 260.
21. Long, T.A., Okegawa, Y., Shikanai, T., Schmidt, G.W. Covert, S.F. (2008) Conserved role of proton gradient regulation 5 in the regulation of PSI cyclic electron transport. Planta, 228, 907 918.
22. Mi, H.L., Endo, T., Ogawa, T. Asada, K. (1995) Thylakoid membrane-bound, NADPH-specific pyridine nucleotide dehydrogenase complex mediates cyclic electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 36, 661 668.
23. Miyake, C. Asada, K. (1994) Ferredoxin-dependent photoreduction of the monodehydroascorbate radical in spinach thylakoids. Plant Cell Physiol. 35, 539 549.
24. Miyake, C., Amako, K., Shiraishi., N. Sugimoto, T. (2009) Acclimation of tobacco leaves to high light intensity drives the plastoquinone oxidation system - relationship among the fraction of open PSII centers, non-photochemical quenching of Chl fluorescence and the maximum quantum yield of PSII in the dark. Plant Cell Physiol. 50, 730 743.
25. Munekage, Y., Hojo, M., Meurer, J., Endo, T., Tasaka, M. Shikanai, T. (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell, 110, 361 371.
26. Munekage, Y., Hashimoto, M., Miyake, C., Tomizawa, K., Endo, T., Tasaka, M. Shikanai, T. (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature, 429, 579 582.
27. Niyogi, K.K. (2000) Safety valves for photosynthesis. Curr. Opin. Plant Biol. 3, 455 460.
28. Ogawa, T. (1991) A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC6803. Proc. Natl Acad. Sci. USA, 88, 4275 4279.
29. Okegawa, Y., Long, T.A., Iwano, M., Takayama, S., Kobayashi, Y., Covert, S.F. Shikanai, T. (2007) A balanced PGR5 level is required for chloroplast development and optimum operation of cyclic electron transport around photosystem I. Plant Cell Physiol. 48, 1462 1471.
30. Okegawa, Y., Kagawa, Y., Kobayashi, Y. Shikanai, T. (2008) Characterization of factors affecting the activity of photosystem I cyclic electron transport in chloroplasts. Plant Cell Physiol. 49, 825 834.
31. Peltier, G. Cournac, L. (2002) Chlororespiration. Annu. Rev. Plant Biol. 53, 523 550.
32. Peng, L., Shimizu, H. Shikanai, T. (2008) The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis. J. Biol. Chem. 283, 34873 34879.
33. Peng, L., Fukao, Y., Fujiwara, M., Takami, T. Shikanai, T. (2009) Efficient operation of NAD(P)H dehydrogenase requires the supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell, 21, 3623 3640.
34. Pesaresi, P., Hertle, A., Pribil, M. et al. (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell, 21, 2402 2423.
35. Redei, G.P. (1963) Somatic instability caused by a cysteine-sensitive gene in Arabidopsis. Science, 139, 767 769.
36. Rizhsky, L., Hallak-Herr, E., Van Breusegem, F., Rachmilevitch, S., Barr, J.E., Rodermel, S., Inze, D. Mittler, R. (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J. 32, 329 342.
37. Rosso, D., Ivanov, A.G., Fu, A. et al. (2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis during steady-state photosynthesis. Plant Physiol. 142, 574 585.
38. Rosso, D., Bode, R., Li, W., Krol, M., Saccon, D., Wang, S., Schillaci, L.A., Rodermel, S.R., Maxwell, D.P. Hüner, N.P. (2009) Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1, and var2. Plant Cell, 21, 3473 3492.
39. Rumeau, D., Peltier, G. Cournac, L. (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ. 30, 1041 1051.
40. Schägger, H. von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368 379.
41. Shikanai, T. (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu. Rev. Plant Biol. 58, 199 217.
42. Shikanai, T., Endo, T., Hashimoto, T., Yamada, Y., Asada, K. Yokota, A. (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc. Natl Acad. Sci. USA, 95, 9705 9709.
43. Stepien, P. Johnson, G.N. (2009) Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol. 149, 1154 1165.
44. Streb, P., Josse, E.M., Gallouet, E., Baptist, F., Kuntz, M. Cornic, G. (2005) Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant species Ranunculus glacialis. Plant Cell Environ. 28, 1123 1135.
45. Tagawa, K., Tsujimoto, H.Y. Arnon, D.I. (1963) Role of chloroplast ferredoxin in the energy conversion process of photosynthesis. Proc. Natl Acad. Sci. USA, 49, 567 572.
46. Tsuyama, M. Kobayashi, Y. (2009) Reduction of the primary donor P700 of photosystem I during steady-state photosynthesis under low light in Arabidopsis. Photosynth. Res. 99, 27 47.
47. Wetzel, C.M., Jiang, C.Z., Meehan, L.J., Voytas, D.F. Rodermel, S.R. (1994) Nuclear-organelle interactions: the immutans variegation mutant of Arabidopsis is plastid autonomous and impaired in carotenoid biosynthesis. Plant J. 6, 161 175.
48. Wu, D., Wright, D.A., Wetzel, C., Voytas, D.F. Rodermel, S. (1999) The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell, 11, 43 55.