Control of mitochondrial function via photosynthetic redox signals

Photosynthesis Research

Volumn 79, Issue 2, 2004, Pages 133-148

  Van Lis, Robert ^a,b   Atteia, Ariane ^b,c  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c BROWN UNIVERSITY   (United States)

Author keywords

Chloroplast; Electron transport; Light regulation; Mitochondrion; Photosynthesis; Redox regulation; Redox state

Indexed keywords

EID: 1542288962     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:PRES.0000015409.14871.68     Document Type: Review

References (113)

1. Allen JF (1993) Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J Theor Biol 165: 609-631
2. Allen JF (2003) State transitions - a question of balance. Science 299: 1530-1532
3. Allen JF and Raven JA (1996) Free-radical-induced mutation vs redox regulation: costs and benefits of genes in organelles. J Mol Evol 42: 482-492
4. Allen CA, Håkansson G and Allen JF (1995a) Redox conditions specify the proteins synthesized by isolated chloroplasts and mitochondria. Redox Rep 1: 119-123
5. Allen JF, Alexciev K and Håkansson G (1995b) Photosynthesis. Regulation by redox signalling. Curr Biol 5: 869-872
6. Aro EM and Ohad I (2003) Redox regulation of thylakoid protein phosphorylation. Antioxid Redox Signal 5: 55-67
7. Azcón-Bieto J, Lambers H and Day DA (1983) Effect of photosynthesis and carbohydrate status on respiration rates and the involvement of the alternative pathway in leaf respiration. Plant Physiol 72: 598-603
8. Barber J and Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17: 61-66
9. Beardall J, Burger-Wiersma T, Rijkeboer M, Sukenik A, Lemboalle J, Dubinsky Z and Fontvielle D (1994) Studies on enhanced post-illumination respiration in microalgae. J Plankton Res 16: 1401-1410
10. Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci USA 79: 4352-4356
11. 2 assimilation in oxygenic photosynthesis: the ferredoxin-thioredoxin system. Perspective on its discovery, present status, and future development. Arch Biochem Biophys 288: 1-9
12. Budde RJ and Randall DD (1990) Pea leaf mitochondrial pyruvate dehydrogenase complex is inactivated in vivo in a light-dependent manner. Proc Natl Acad Sci USA 87: 673-676
13. Danon A and Mayfield SP (1994) Light-regulated translation of chloroplast messenger RNAs through redox potential. Science 266: 17176-17179
14. Datta N and Cashmore AR (1989) Binding of a pea nuclear protein to promoters of certain photoregulated genes is modulated by phosphorylation. Plant Cell 1: 1069-1077
15. Day DA and Wiskich JT (1995) Regulation of alternative oxidase activity in higher plants. J Bioenerg Biomembr 27: 379-385
16. Douce R and Neuburger M (1989) The uniqueness of plant mitochondria. Annu Rev Plant Physiol Plant Mol Biol 40: 371-414
17. Douce R, Bourguignon J, Neuburger M and Rébeillé F (2001) The glycine decarboxylase system: a fascinating complex. Trends Plant Sci 6: 167-176
18. Dry IB, Day D and Wiskich JT (1983) Preferential oxidation of glycine by respiratory chain of pea leaf mitochondria. FEBS Lett 158: 154-158
19. Dry IB, Moore AL, Day DA and Wiskich JT (1989) Regulation of alternative pathway activity in plant mitochondria: nonlinear relationship between electron flux and the redox poise of the quinone pool. Arch Biochem Biophys 273: 148-157
20. Dudley P, Wood CK, Pratt JR and Moore AL (1997) Developmental regulation of the plant mitochondrial matrix located HSP70 chaperone and its role in protein import. FEBS Lett 417: 321-324
21. Dutilleul C, Driscoll S, Cornic G, De Paepe R, Foyer CH and Noctor G (2003) Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol 131: 264-275
22. Escobar Galvis ML, Allen JF and Håkansson G (1998) Protein synthesis by isolated pea mitochondria is dependent on the activity of respiratory complex II. Curr Genet 33: 320-329
23. Escoubas JM, Lomas M, LaRoche J and Falkowski PG (1995) Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 92: 10237-10241
24. Fankhauser C and Staiger D (2002) Photoreceptors in Arabidopsis thaliana: light perception, signal transduction and entrainment of the endogenous clock. Planta 216: 1-16
25. Finnegan PM, Whelan J, Millar AH, Zhang Q, Smith MK, Wiskich JT and Day DA (1997) Differential expression of the multigene family encoding the soybean mitochondrial alternative oxidase. Plant Physiol 114: 455-466
26. Flügge UI and Heldt HW (1991) Metabolite translocators of the chloroplast envelope. Annu Rev Plant Physiol Plant Mol Biol 42: 129-144
27. Forsberg J, Rosenquist M, Fraysse L and Allen JF (2001) Redox signalling in chloroplasts and mitochondria: genomic and biochemical evidence for two-component regulatory systems in bioenergetic organelles. Biochem Soc Trans 29: 403-407
28. Foyer CH, Lopez-Delgado H, Dat JF and Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100: 241-254
29. Gardeström P (1996) Interactions between mitochondria and chloroplasts. Biochim Biophys Acta 1275: 38-40
30. Gardeström P and Lernmark U (1995) The contribution of mitochondria to energetic metabolism in photosynthetic cells. J Bioenerg Biomemb 27: 415-421
31. Gemel J and Randall DD (1992) Light regulation of leaf mitochondrial pyruvate dehydrogenase complex. Plant Physiol 100: 908-914
32. Green PJ, Kay SA and Chua NH (1987) Sequence-specific interactions of a pea nuclear factor with light-responsive elements upstream of the rbcS-3A gene. EMBO J 6: 2543-2549
33. Green PJ, Yong MH, Cuozzo M, Kano-Murakami Y, Silverstein P and Chua NH (1988) Binding site requirements for pea nuclear protein factor GT-1 correlate with sequences required for light-dependent transcriptional activation of the rbcS-3A gene. EMBO J 7: 4035-4044
34. Håkansson G and Allen JF (1995) Histidine and tyrosine phosphorylation in pea mitochondria: evidence for protein phosphorylation in respiratory redox signalling. FEBS Lett 372: 238-242
35. Hare PD and Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21: 79-102
36. Hatch MD, Dröscher L, Flügge UI and Heldt HW (1984) A specific translocator for oxaloacetate transport in chloroplasts. FEBS Lett 178: 15-19
37. Hedtke B, Wagner I, Börner T and Hess WR (1999) Inter-organellar crosstalk in higher plants: impaired chloroplast development affects mitochondrial gene and transcript levels. Plant J 19: 635-643
38. Heineke D, Riens B, Grosses H, Hoferichter P and Peter U (1991) Redox transfer across the inner chloroplast envelope membrane. Plant Physiol 95: 1131-1137
39. Hoefnagel MH and Wiskich JT (1998) Activation of the plant alternative oxidase by high reduction levels of the Q-pool and pyruvate. Arch Biochem Biophys 355: 262-270
40. Hoefnagel MHN, Atkin OK and Wiskich JT (1998) Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim Biophys Acta 1366: 235-255
41. Huner NPA, Öquist G and Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 6: 224-230
42. Igamberdiev AU, Bykova NV and Garderström P (1997) Involvement of cyanide-resistant and rotenone-insensitive pathways of mitochondrial electron transport during oxidation of glycine in higher plants. FEBS Lett 412: 265-269
43. Igamberdiev AU, Hurry V, Krömer S and Garderström P (1998) The role of mitochondrial electron transport during photosynthetic induction. A study with barley (Hordeum vulgare) protoplasts incubated with rotenone and oligomycin. Physiol Plant 104: 431-439
44. Igamberdiev AU, Bykova NV, Lea PJ and Garderström P (2001a) The role of photorespiration in redox and energy balance of photosynthetic plant cells: a study with a barley mutant deficient in glycine decarboxyalse. Physiol Plant 111: 427-438
45. Igamberdiev AU, Romanovska E and Garderström P (2001b) Photorespiratory flux and mitochondrial contribution to energy and redox balance of barley leaf protoplasts in the light and during light-dark transitions. J Plant Physiol 158: 1325-1332
46. Jimenez A, Hernandez JA, Del Rio LA and Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114: 275-284
47. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G and Mullineaux PS (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284: 654-657
48. Kim Y and Mayfield SP (1997) Protein disulfide isomerase as a regulator of chloroplast translational activation. Science 278: 1954-1957
49. Koch KE, Ying Z, Wu Y and Avigne WT (2000) Multiple paths of sugar-sensing and a sugar/oxygen overlap for genes of sucrose and ethanol metabolism. J Exp Bot 51: 417-427
50. Konstantinov YM, Lutsenko GN and Podsonony VA (1995) Genetic functions of isolated maize mitochondria under model changes of redox conditions. Biochem Mol Biol Int 36: 319-326
51. Konstantinov YM, Subota IY and Arziev AS (1998) Differential redox regulation by glutathione of translation in isolated mitochondria. MNL (Maize Genetics Cooperation News Letter) 72: 33
52. Konstantinov Y, Tarasenko VI and Rogozin IB (2001) Redox modulation of the activity of DNA topoisomerase I from carrot (Daucus carota) mitochondria. Dokl Biochem Biophys 377: 82-84
53. Krömer S (1995) Respiration during photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 46: 45-70
54. Krömer S, Stitt M and Heldt HW (1988) Mitochondrial oxidative phosphorylation participating in photosynthetic metabolism of a leaf cell. FEBS Lett 226: 352-356
55. Kroymann J, Schneider W and Zetsche K (1995) Opposite regulation of the copy number and the expression of plastid and mitochondrial genes by light and acetate in the green flagellate Chlorogonium. Plant Physiol 108: 1641-1646
56. Laloi C, Rayapuram N, Chartier Y, Grienenberger JM, Bonnar G and Meyer Y (2001) Identification and characterization of a mitochondrial thioredoxin system in plants. Proc Natl Acad Sci USA 98: 14144-14149
57. Lambers H (1982) Cyanide-respiration: a non-phosphorylating electron transport pathway acting as an energy overflow. Physiol Plant 55: 478-485
58. Lambers H (1985) Respiration in intact plants and tissues: its regulation and dependence on environmental factors, metabolism and invaded organisms. In: Douce R and Day DA (eds) Encyclopaedia of Plant Physiology, New Series, Higher Plant Cell Respiration, Vol 18, pp 418-473. Springer-Verlag, Berlin
59. Landschutze V, Muller-Rober B and Willmitzer L (1995) Mitochondrial citrate synthase from potato: predominant expression in mature leaves and young flower buds. Planta 196: 756-764
60. Lennon AM, Pratt J, Leach G and Moore AL (1995) Developmental regulation of respiratory activity in pea leaves. Plant Physiol 107: 925-932
61. Long JJ and Berry JO (1996) Tissue-specific and light-mediated expression of the C4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria. Plant Physiol 112: 473-482
62. Macherel D, Lebrun M, Gagnon J, Neuburger M and Douce R (1990) Primary structure and expression of H-protein, a component of the glycine cleavage system of pea leaf mitochondria. Biochem J 269: 783-789
63. Mackenzie S and McIntosh L (1999) Higher plant mitochondria. Plant Cell 11: 571-586
64. Maxwell DP, Wang Y and McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96: 8271-8276
65. Millar AH, Wiskich JT, Whelan J and Day DA (1993) Organic acid activation of the alternative oxidase of plant mitochondria. FEBS Lett 329: 259-262
66. Millenaar FF and Lambers H (2003) The alternative oxidase: in vivo regulation and function. Plant Biol 5: 2-15
67. Møller IM (2002) A new dawn for plant mitochondrial NAD(P)H dehydrogenases. Trends Plant Sci 7: 235-237
68. Moore AL, Gemel J and Randall DD (1993) The regulation of pyruvate dehydrogenase activity in pea leaf mitochondria (the effect of respiration and oxidative phosphorylation). Plant Physiol 103: 1431-1435
69. Mustilli AC and Bowler C (1997) Tuning in to the signals controlling photoregulated gene expression in plants. EMBO J 19: 5801-5806
70. Padmasree K and Raghavendra AS (1999) Response of photosynthetic carbon assimilation in mesophyll protoplasts to restriction on mitochondrial oxidative metabolism: metabolites related to the redox status and sucrose biosynthesis. Photosynth Res 62: 231-239
71. Padmasree K, Padmavati L and Raghavendra AS (2002) Essentiality of mitochondrial oxidative metabolism of photosynthesis: optimization of carbon assimilation and protection against photoinhibition. Crit Rev Biochem Mol Biol 37: 71-119
72. Peltier G and Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53: 523-550
73. Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8: 33-41
74. Pfannschmidt T, Nilsson A and Allen JF (1999a) Photosynthetic control of chloroplast gene expression. Nature 397: 625-628
75. Pfannschmidt T, Nilsson A, Tullberg A, Link G and Allen JF (1999b) Direct transcriptional control of the chloroplast genes psbA and psaAB adjusts photosynthesis to light energy distribution in plants. IUBMB Life 48: 271-276
76. Pfannschmidt T, Allen JF and Oelmüller R (2001) Principles of redox control in photosynthesis gene expression. Physiol Plant 112: 1-9
77. Pursiheimo S, Mulo P, Rintama E and Aro E-M (2001) Coregulation of light-harvesting complex II phosphorylation and lhcb mRNA accumulation in winter rye. Plant J 26: 317-327
78. Purvis AC (1997) Role of the alternative oxidase in limiting superoxide production by plant mitochondria. Physiol Plant 100: 165-170
79. Raghavendra AS, Padmasree K and Saradadevi K (1994) Inter-dependence of photosynthesis and respiration in plant cells: interactions between chloroplasts and mitochondria. Plant Sci 97: 1-14
80. Randall DD, Miernyk JA, Fang TK, Budde RJ and Schuller KA (1989) Regulation of the pyruvate dehydrogenase complexes in plants. Ann NY Acad Sci 573: 192-205
81. Reddy MM, Vani T and Raghavendra AS (1991) Light-enhanced dark respiration in mesophyll protoplasts from leaves of pea. Plant Physiol 96: 1368-1371
82. Rhoads DM, Umbach AL, Sweet CR, Lennon AM, Rauch GS and Siedow JN (1998) Regulation of the cyanide-resistant alternative oxidase of plant mitochondria. Identification of the cysteine residue involved in alpha-keto acid stimulation and intersubunit disulfide bond formation. J Biol Chem 273: 30750-30756
83. Ribas-Carbo M, Berry JA, Yakir D, Giles L, Robinson SA, Lennon AM and Siedow JN (1995) Electron partitioning between the cytochrome and alternative pathways in plant mitochondria. Plant Physiol 109: 829-837
84. Ribas-Carbo M, Lennon AM, Robinson SA, Giles L, Berry JA and Siedow JN (1997) The regulation of electron partitioning between the cytochrome and alternative pathways in soybean cotyledon and root mitochondria. Plant Physiol 13: 903-911
85. Ruelland E and Miginiac-Maslow M (1999) Regulation of chloroplast enzyme activities by thioredoxins: activation or relief from inhibition? Trends Plant Sci 4: 136-141
86. Saradadevi K and Raghavendra AS (1992) Dark respiration protects photosynthesis against photoinhibition in mesophyll protoplasts of pea (Pisum sativum). Plant Physiol 99: 1232-1237
87. 3 plants: regulation and the role of a light-activated enzyme. Physiol Plant 71: 393-400
88. Scheibe R (1991) Redox-modulation of chloroplast enzymes. A common principle for individual control. Plant Physiol 96: 1-3
89. Schürmann P and Jacquot JP (2000) Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol 51: 371-400
90. Singh KK, Shyam R and Sane PV (1996) Reactivation of photosynthesis in the photoinhibited green alga Chlamydomonas reinhardtii: role of dark respiration and of light. Photosynth Res 49: 11-20
91. Sluse FE and Jarmuszkiewicz W (2000) Activity and functional interaction of alternative oxidase and uncoupling protein in mitochondria from tomato fruit. Braz J Med Biol Res 33: 259-268
92. Soole KL and Menz RI (1995) Functional molecular aspects of the NADH dehydrogenases of plant mitochondria. J Bioenerg Biomembr 27: 397-406
93. Srinivasan R and Oliver DJ (1995) Light-dependent and tissue-specific expression of the H-protein of the glycine decarboxylase complex. Plant Physiol 109: 161-168
94. Stevens FJ, Dong Li A, Salman Lateef S and Anderson LE (1997) Identification of potential inter-domain disulfides in three higher plant mitochondrial citrate synthases: paradoxical differences in redox sensitivity as compared with the animal enzyme. Photosynth Res 54: 185-197
95. Svensson AS and Rasmusson AG (2001) Light-dependent gene expression for proteins in the respiratory chain of potato leaves. Plant J 28: 73-82
96. Szibor M, Richter C and Ghafourifar P (2001) Redox control of mitochondrial functions. Antioxid Redox Signal 3: 515-523
97. Turner SR, Hellens R, Ireland R, Ellis N and Rawsthorne S (1993) The organization and expression of the genes encoding the mitochondrial glycine decarboxylase complex and serine hydroxymethyltransferase in pea (Pisum sativum). Mol Gen Genet 236: 402-408
98. Umbach AL and Siedow JN (1993) Covalent and noncovalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiol 103: 845-854
99. Umbach AL and Siedow JN (2000) The cyanide-resistant alternative oxidases from the fungi Pichia stipitis and Neurospora crassa are monomeric and lack regulatory features of the plant enzyme. Arch Biochem Biophys 378: 234-245
100. Umbach AL, Wiskich JT and Siedow JN (1994) Regulation of alternative oxidase kinetics by pyruvate and intermolecular disulfide bond redox status in soybean seedling mitochondria. FEBS Lett 348: 181-184
101. Vanlerberghe GC and McIntosh L (1994) Mitochondrial electron transport regulation of nuclear gene expression. Plant Physiol 105: 867-874
102. Vanlerberghe GC and McIntosh L (1997) Alternative oxidase: from gene to function. Ann Rev Plant Physiol Plant Mol Biol 48: 703-734
103. Vanlerberghe GC, Day DA, Wiskich JT, Vanlerberghe AE and McIntosh L (1995) Alternative oxidase activity in tobacco leaf mitochondria: dependence on tricarboxylic acid cycle-mediated redox regulation and pyruvate activation. Plant Physiol 109: 353-361
104. Vanlerberghe GC, Robson CA and Yip JY (2002) Induction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death. Plant Physiol 129: 1829-1842
105. Vauclare P, Diallo N, Bourguignon J, Macherel D and Douce R (1996) Regulation of the expression of the glycine decarboxylase complex during pea leaf development. Plant Physiol 112: 1523-1530
106. Vauclare P, Macherel D, Douce R and Bourguignon J (1998) The gene encoding T protein of the glycine decarboxylase complex involved in the mitochondrial step of the photorespiratory pathway in plants exhibits features of light-induced genes. Plant Mol Biol 37: 309-318
107. Wagner AM (1995) A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells. FEBS Lett 368: 339-342
108. Walker JL and Oliver DJ (1986) Light-induced increases in the glycine decarboxylase multienzyme complex from pea leaf mitochondria. Arch Biochem Biophys 248: 626-638
109. Walters RG, Rogers JJM, Shephard F and Horton P (1999) Acclimation of Arabidopsis thaliana to the light environment: the role of photoreceptors. Planta 209: 517-527
110. Wigge B, Krömer S and Gardeström P (1993) The redox levels and subcellular distribution of pyridine nucleotides in illuminated barley leaf protoplasts studied by rapid fractionation. Physiol Plant 88: 10-18
111. Wilson SB, Davidson GS, Thomson LM and Pearson CK (1996) Redox control of RNA synthesis in potato mitochondria. Eur J Biochem 242: 81-85
112. Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20: 3623-3630
113. Xue X, Gauthier DA, Turpin DH and Weger HG (1996) Interactions between photosynthesis and respiration in the green alga Chlamydomonas reinhardtii. Plant Physiol 112: 1005-1014