Strategies to maintain redox homeostasis during photosynthesis under changing conditions

Journal of Experimental Botany

Volumn 56, Issue 416, 2005, Pages 1481-1489

  Scheibe, Renate ^a   Backhausen, Jan E ^a   Emmerlich, Vera ^a   Holtgrefe, Simone ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

Light acclimation; Malate valve; Over reduction; Oxidative stress; Photosynthesis; Poising mechanisms; Redox control; Redox homeostasis; Regulatory networks

Indexed keywords

ELECTRONS; ENERGY UTILIZATION; GENES; METABOLISM; OXIDATION; PLANTS (BOTANY); REDOX REACTIONS; SIGNALING;

ENDERGONIC PROCESSES; HOMEOSTASIS; REDUCTANTS; SIGNAL TRANSDUCTION;

PHOTOSYNTHESIS;

FERREDOXIN; THIOREDOXIN; VEGETABLE PROTEIN;

ADAPTATION; GENE EXPRESSION REGULATION; HOMEOSTASIS; LIGHT; METABOLISM; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT; REVIEW;

ADAPTATION, PHYSIOLOGICAL; FERREDOXINS; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; LIGHT; OXIDATION-REDUCTION; PHOTOSYNTHESIS; PLANT PROTEINS; PLANTS; THIOREDOXIN;

EID: 20044387599     PISSN: 00220957     EISSN: None     Source Type: Journal    
DOI: 10.1093/jxb/eri181     Document Type: Review

References (89)

1. Allen JF. 2002. Plastoquinone redox control of chloroplast thylakoid protein phosphorylation and distribution of excitation energy between photosystems: discovery, background, implications. Photosynthesis Research 73, 139-148.
2. Anderson JM, Osmond CB. 1987. Shade-sun responses: compromises between acclimation and photoinhibition. In: Kyle DJ, Osmond CB, Amtzen CJ, eds. Photoinhibition. Amsterdam: Elsevier, 1-36.
3. Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373-399.
4. Arrigoni O, De Tullio MC. 2002. Ascorbic acid: much more than just an antioxidant. Biochimica et Biophysica Acta 1569, 1-9.
5. Asada K. 2000. The water-water cycle as alternative photon and electron sinks. Philosophical Transactions of the Royal Society London B 355, 1419-1431.
6. Avenson TJ, Kanazawa A, Cruz JA, Takizawa K, Ettinger WE, Kramer DM. 2005. Integrating the proton circuit into photosynthesis: progress and challenges. Plant, Cell and Environment 28, 97-109.
7. Backhausen JE, Emmerlich A, Holtgrefe S, Horton P, Nast G, Roggers JJM, Müller-Röber B, Scheibe R. 1998. Transgenic potato plants with altered expression levels of chloroplast NADP-malate dehydrogenase: interactions between photosynthetic electron transport and malate metabolism in leaves and in isolated intact chloroplasts. Planta 207, 105-114.
8. Backhausen JE, Kitzmann C, Horton P, Scheibe R. 2000. Electron acceptors in isolated intact spinach chloroplasts act hierarchically to prevent competition for electrons. Photosynthesis Research 64, 1-13.
9. 2: influence of leaf age on changes in physiology, redox states and NADP-malate dehydrogenase activity. Journal of Experimental Botany 50, 665-675.
10. Bailey S, Walters RG, Jansson S, Horton P. 2001. Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213, 794-801.
11. Buchanan BB. 1984. The ferredoxin/thioredoxin system: a key element in the regulatory function of light in photosynthesis. Bioscience 34, 378-383.
12. Cao S, Xu Q, Cao Y, Qian K, An K, Zhu Y, Binzeng H, Zhao H, Kuai B. 2005. Loss-of-function mutations in DET2 gene lead to an enhanced resistance of oxidative stress in Arabidopsis. Physiologia Plantarum 123, 57-66.
13. Chen WJ, Zhu T. 2004. Networks of transcription factors with roles in environmental stress response. Trends in Plant Science 9, 591-596.
14. Chow WS, Melis A, Anderson JM. 1990. Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photossynthesis. Proceedings of the National Academy of Sciences, USA 87, 7502-7506.
15. Cotgreave IA, Gerdes RG. 1998. Recent trends in glutathione biochemistry - glutathione-protein interactions: a molecular link between oxidative stress and cell proliferation? Biochemical and Biophysical Research Communications 242, 1-9.
16. Corbesier L, Coupland G. 2005. Photoperiodic flowering of Arabidopsis: integrating genetic and physiological approaches to characterization of the floral stimulus. Plant, Cell and Environment 28, 54-66.
17. Dai S, Schwendtmayer C, Schünemann P, Ramaswamy S, Eklund H. 2000. Redox signaling in chloroplasts: cleavage of disulfides by an iron-sulfur cluster. Science 287, 655-658.
18. Davies DD. 1986. The fine control of cytosolic pH. Physiologia Plantarum 67, 702-706.
19. De Gara L. 2004. Ascorbate and plant growth: from germination to cell death. In: Asard H, May JM, Smirnoff N, eds. Vitamin C function and biochemistry in animals and plants. Oxford, UK: Bios Scientific Publishers, 83-95.
20. Dietz K-J. 2003. Redox control, redox signaling, and redox homeostasis in plant cells. International Review of Cytology 228, 141-193.
21. Dutilleul C, Garmier M, Noctor G, Mathieu C, Chétrit P, Foyer CH, de Paepe R. 2003. Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capactiy, and determine stress resistance through altered signaling and diurnal regulation. The Plant Cell 15, 1212-1226.
22. Emmerlich V, Linka N, Reinhold T, Hurth MA, Traub M, Martinoia E, Neuhaus HE. 2003. The plant homolog to the human sodium/dicarboxylic cotransporter is the vacuolar malate carrier. Proceedings of the National Academy of Sciences, USA 100, 11122-11126.
23. Faske M, Backhausen JE, Sendker M, Singer-Bayrle M, Scheibe R, von Schaewen A. 1997. Transgenic tobacco plants expressing pea chloroplast Nmdh cDNA in sense and antisense orientation: effects on NADP-malate dehydrogenase level, stability of transformants, and plant growth. Plant Physiology 115, 705-715.
24. Faske M, Holtgrefe S, Ocheretina O, Meister M, Backhausen JE, Scheibe R. 1995. Redox equilibria between the regulatory thiols of light/dark-modulated chloroplast enzymes and dithiothreitol: fine-tuning by metabolites. Biochimica et Biophysica Acta 1247, 135-142.
25. Felle HH. 2001. pH: signal and messenger in plant cells. Plant Biology 3, 577-591.
26. Fernie AR, Carrari F, Sweetlove LJ. 2004. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Current Opinion in Plant Biology 7, 254-261.
27. Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz K-J. 2005. The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. Journal of Biological Chemistry 280, 12168-12180.
28. Foyer CH, Noctor G. 2000. Oxygen processing in photosynthesis: regulation and signalling. New Phytologist 146, 359-388.
29. Foyer CH, Noctor G. 2003. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiologia Plantarum 119, 355-364.
30. Fujita Y, Murakami A, Ohki K. 1987. Regulation of photosystem composition in the cyanobacterial photosynthesic system: the regulation occurs in response to the redox state of the electron pool located between the two photosystems. Plant and Cell Physiology 28, 283-292.
31. Gardeström P, Igamberdiev AU, Raghavendra AS. 2002. Mitochondrial functions in the light and significance to carbon-nitrogen interactions. In: Foyer CH, Noctor G, eds. Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism. Dordrecht, Boston, London: Kluwer Academic Publishers, 152-172.
32. Golding AJ, Finazzi G, Johnson GN. 2004. Reduction of the thylakoid electron transport chain by stromal reductants: evidence for activation of cyclic electron transport upon dark adaptation or under drought. Planta 220, 356-363.
33. +-dependent isocitrate dehydrogenase: evidence implicating this enzyme in the redox activation of the alternative oxidase. Plant Cell Physiology 45, 1413-1425.
34. 3 plants. Photosynthesis Research 73, 223-231.
35. Hirasawa M, Ruelland E, Schepens I, Issakidis-Bourguet E, Miginiac-Maslow M, Knaff DB. 2000. Oxidation-reduction properties of the regulatory disulfides of sorghum chloroplast nicotinamide adenine dinucleotide phosphate-malate dehydrogenase. Biochemistry 39, 3344-3350.
36. Holt NE, Fleming GR, Niyogi KK. 2004. Toward an understanding of the mechanism of non-photochemical quenching in green plants. Biochemistry 43, 8281-8289.
37. Holtgrefe S, Bader HP, Horton P, Scheibe R, von Schaewen A, Backhausen JE. 2003. Decreased content of leaf ferredoxin changes electron distribution and limits photosynthesis in transgenic potato plants. Plant Physiology 133, 1768-1778.
38. Huner NPA, Maxwell DP, Gray GR, Savitch LV, Krol M, Ivanov AG, Falk S. 1996. Sensing environmental temperature change through imbalances between energy supply and energy consumption: redox state of photosystem II. Physiologia Plantarum 98, 358-364.
39. Huner NPA, Öquist G, Sarhan F. 1998. Energy balance and acclimation to light and cold. Trends in Plant Science 3, 224-230.
40. Ito H, Iwabuchi M, Ogawa K. 2003. The sugar-metabolic enzymes aldolase and triose-phosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: detection using biotinylated glutathione. Plant and Cell Physiology 44, 655-660.
41. Ivanov B, Khorobrykh S. 2003. Participation of photosynthetic electron transport in production and scavenging of reactive oxygen species. Antioxidants and Redox Signaling 5, 43-53.
42. Johnson GN. 2003. Thiol regulation of the thylakoid electron transport chain: a missing link in the regulation of photosynthesis? Biochemistry 42, 3040-3044.
43. 3 plants: fact or artefact? Journal of Experimental Botany 56, 407-416.
44. König J, Baier M, Horling F, Harris G, Schürmann P, Dietz K-J. 2002. The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proceedings of the National Academy of Sciences, USA 99, 5738-5743.
45. Koornneef M, Alonso-Blanco C, Peeters AJM, Soppe W. 1998. Genetic control of flowering time in Arabidopsis. Annual Reviews of Plant Phyisology and Plant Molecular Biology 49, 345-370.
46. Kramer DM, Avenson TJ, Edwards GE. 2004. Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends in Plant Science 9, 349-357.
47. Krömer S, Scheibe R. 1996. Function of the chloroplastic malate valve for respiration during photosynthesis. Biochemical Society Transactions 24, 761-766.
48. Laloi C, Apel K, Danon A. 2004. Reactive oxygen signalling: the latest news. Current Opinion in Plant Biology 7, 323-328.
49. Lance C, Rustin P. 1984. The central role of malate in plant metabolism. Physiologie Végétale 22, 625-641.
50. Marchand C, Le Maréchal P, Meyer Y, Miginiac-Maslow M, Issakidis-Bourguet E, Decottignies P. 2004. New targets of Arabidopsis thioredoxins revealed by proteomic analysis. Proteomics 4, 2696-2706.
51. Martinsuo P, Pursiheimo S, Aro E-M, Rintamäki E. 2003. Dithiol oxidant and disulfide reductant dynamically regulate the phosphorylation of light-harvesting complex II proteins in thylakoid membranes. Plant Physiology 133, 37-46.
52. Masters CH, Reid S, Don M. 1987. Glycolysis: new concepts in an old pathway. Molecular and Cellular Biochemistry 76, 3-14.
53. Mathieu Y, Guern J, Pean M, Pasquier C, Beloeil J-C, Lallamand J-Y. 1986. Cytoplasmic pH regulation in Acer pseudoplatanus cells. II. Possible mechanisms involved in pH regulation during acid-load. Plant Physiology 82, 846-852.
54. May MJ, Vernoux T, Leaver C, Van Montagu M, Inzé D. 1998. Glutathione homeostasis in plants: implications for environmental sensing and plant development. Journal of Experimental Botany 49, 649-667.
55. Meyer Y, Verdoucq L, Vignols F. 1999. Plant thioredoxins and glutaredoxins: identity and putative roles. Trends in Plant Science 4, 388-394.
56. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405-410.
57. Mullineaux P, Karpinski S. 2002. Signal transduction in response to excess light: getting out of the chloroplast. Current Opinion in Plant Biology 5, 43-48.
58. 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.
59. Nedbal L, Březina V, Adamec F, Štys D, Oja V, Laisk A, Govindjee. 2003. Negative feedback regulation is responsible for the non-linear modulation of photosynthetic activity in plants and cyanobacteria exposed to a dynamic light environment. Biochimica et Biophysica Acta 1607, 5-17.
60. Neill S, Desikan R, Hancock J. 2002. Hydrogen peroxide signalling. Current Opinion in Plant Biology 5, 388-395.
61. Niyogi KK. 1999. Photoprotection revisited: genetic and molecular approaches. Annual Reviews in Plant Physiology and Plant Molecular Biology 50, 333-359.
62. Noctor G, Dutilleul C, De Paepe R, Foyer CH. 2004. Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon/nitrogen metabolism. Journal of Experimental Botany 55, 49-57.
63. 3 plants: a predominant role for photorespiration? Annals of Botany 89, 841-850.
64. Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AMO, Ehlers Loureiro M, Ratcliffe RG, Sweetlove LJ, Fernie AR. 2005. Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiology 137, 611-622.
65. Padmasree K, Padmavathi L, Raghavendra AS. 2002. Essentiality of mitochondrial oxidative metabolism for photosynthesis: optimization of carbon assimilation and protection against photoinhibition. Critical Reviews in Biochemistry and Molecular Biology 37, 71-119.
66. Polle A. 1996. Mehler reaction: friend or foe in photosynthesis? Botanica Acta 109, 84-89.
67. Puppo A, Groten K, Bastian F, Carzaniga R, Soussi M, Lucas MM, de Felipe MR, Harrison J, Vanacker H, Foyer CH. 2004. Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytologist 165, 683-701.
68. Rajagopal S, Bukhov NG, Tajmir-Riahi H, Carpentier R. 2003. Control of energy dissipation and photochemical activity in photosystem I by NADP-dependent reversible conformational changes. Biochemistry 42, 11839-11845.
69. Renné P, Dreßen U, Hebbeker U, Hille A, Flügge U-I, Westhoff P, Weber APM. 2003. The Arabidopsis mutant dct is deficient in the plastidic glutamate/malate translocator DiT2. The Plant Journal 35, 316-331.
70. Sakano K. 1998. Revision of biochemical pH-stat: involvement of alternative pathway metabolisms. Plant Cell Physiology 39, 467-473.
71. Sakano K, Kiyota S, Yazaki Y. 1998. Degradation of endogenous organic acids induced by Pi uptake in Catharanthus roseus cells: involvement of the biochemical pH-stat. Plant and Cell Physiology 39, 615-619.
72. Savitch LV, Barker-Åstrom J, Ivanov AG, Hurry V, Öquist G, Huner NPA, Gardeström P. 2001. Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma. Planta 214, 295-303.
73. Savitch LV, Massacci A, Gray GR, Huner NPA. 2000. Acclimation to low temperature or high light mitigates sensitivity to photoinhibition: roles of the Calvin cycle and the Mehler reaction. Australian Journal of Plant Physiology 27, 253-264.
74. Scheibe R. 2001. Redox-modulation of chloroplast enzymes. A common principle for individual control. Plant Physiology 96, 1-3.
75. Scheibe R. 2004. Malate valves to balance cellular energy supply. Physiologia Plantarum 120, 21-26.
76. 2 evolution in spinach leaves. Plant Physiology and Biochemistry 26, 473-481.
77. Schürmann P, Jacquot J-P. 2000. Plant thioredoxin system revisited. Annual Reviews of Plant Physiology and Plant Molecular Biology 51, 371-400.
78. Shi Y, Shi Y. 2004. Metabolic enzymes and coenzymes in transcription: a direct link between metabolism and transcription? Trends in Genetics 20, 445-452.
79. Takahashi S, Seki M, Ishida J, et al. 2004. Monitoring the expression profiles of genes induced by hyperosmotic, high salinity, and oxidative stress and abscisic acid treatment in Arabidopsis cell culture using a full-length cDNA microarray. Plant Molecular Biology 56, 29-55.
80. Taniguchi M, Taniguchi Y, Kawasaki M, Takeda S, Kato T, Sato S, Tabata S, Miyake H, Sugiyama T. 2002. Identifying and characterizing plastidic 2-oxoglutarate/malate and dicarboxylate transporters in Arabidopsis thaliana. Plant, Cell and Environment 43, 706-717.
81. Vanlerberghe GC, McIntosh L. 1992. Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiology 100, 115-119.
82. Van Lis R, Atteia A. 2004. Control of mitochondrial function via photosynthetic redox signals. Photosynthesis Research 79, 133-148.
83. Walters RG. 2005. Towards an understanding of photosynthetic acclimation. Journal of Experimental Botany 56, 435-447.
84. Walters RG, Rogers JJM, Shephard F, Horton P. 1999. Acclimation of Arabidopsis thaliana to the light environment: the role of photoreceptors. Planta 209, 517-527.
85. Wendehenne D, Durner J, Klessig DF. 2004. Nitric oxide: a new player in plant signalling and defense responses. Current Opinion in Plant Biology 7, 449-455.
86. Wingate VPM, Lawton MA, Lamb CJ. 1988. Glutathione causes a massive and selective induction of plant defense genes. Plant Physiology 87, 206-210.
87. Winkel BSJ. 2004. Metabolic channeling in plants. Annual Review of Plant Biology 55, 23-39.
88. Zentgraf U, Jobst J, KoIb D, Rentsch D. 2004. Senescence-related gene expression profiles of rosette leaves of Arabidopsis thaliana: leaf age versus plant age. Plant Biology 6, 178-183.
89. Zhang Q, Moore CS, Soole KL, Wiskich JT. 2003. Over-reduction of cultured tobacco cells mediates changes in respiratory activities. Physiologia Plantarum 119, 183-191.