Redox regulation and antioxidative defence in Arabidopsis leaves viewed from a systems biology perspective

Journal of Biotechnology

Volumn 129, Issue 2, 2007, Pages 229-248

  Wormuth, Dennis ^a   Heiber, Isabelle ^a   Shaikali, Jehad ^a   Kandlbinder, Andrea ^a   Baier, Margarete ^a   Dietz, Karl Josef ^a  

^a BIELEFELD UNIVERSITY   (Germany)

Author keywords

Antioxidant defence; Gene regulation; plant; Redox regulation; Signalling; Systems biology

Indexed keywords

BIOTECHNOLOGY; CROSSTALK; METABOLISM; PLANTS (BOTANY); PROTEINS; SIGNALING;

ANTIOXIDANT DEFENCE; GENE REGULATION; REDOX REGULATION; SYSTEMS BIOLOGY;

REDOX REACTIONS;

DISULFIDE; PROTEOME; THIOL;

ANTIOXIDANT ACTIVITY; ARABIDOPSIS; ARTICLE; CELL METABOLISM; MATHEMATICAL MODEL; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHOTOSYNTHESIS; PLANT LEAF; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY;

ANTIOXIDANTS; ARABIDOPSIS; GENE EXPRESSION REGULATION, PLANT; OXIDATION-REDUCTION; OXIDATIVE STRESS; PLANT LEAVES; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY;

ARABIDOPSIS;

EID: 34047244537     PISSN: 01681656     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2006.12.006     Document Type: Article

References (143)

1. Acevedo-Hernández G.J., León P., and Herrera-Estrella L.R. Sugar and ABA responsiveness of a minimal RBCS light-responsive unit is mediated by direct binding of ABI4. Plant J. 43 (2005) 506-519
2. Alberghino L., Rossi R.L., Wanke V., Querin L., and Vanoni M. Checking cell size in budding yeast: a systems biology approach. Ital. J. Biochem. 52 (2003) 55-57
3. Alonso J.M., Stepanova A.N., Leisse T.J., Kim C.J., Chen H., Shinn P., Stevenson D.K., Zimmerman J., Barajas P., Cheuk R., Gadrinab C., Heller C., Jeske A., Koesema E., Meyers C.C., Parker H., Prednis L., Ansari Y., Choy N., Deen H., Geralt M., Hazari N., Hom E., Karnes M., Mulholland C., Ndubaku R., Schmidt I., Guzman P., Aguilar-Henonin L., Schmid M., Weigel D., Carter D.E., Marchand T., Risseeuw E., Brogden D., Zeko A., Crosby W.L., Berry C.C., and Ecker J.R. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301 (2003) 653-657
4. Asada K. The water-water-cycle in chloroplasts. Scavenging of active oxygen and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 (1999) 601-639
5. Bae H., Herman E., and Sicher R. Exogenous trehalose promotes non-structural carbohydrate accumulation and induces chemical detoxification and stress response proteins in Arabidopsis thaliana grown in liquid culture. Plant Sci. 168 (2005) 1293-1301
6. Baier M., Noctor G., Foyer C.H., and Dietz K.J. Antisense suppression of 2-cysteine peroxiredoxin in Arabidopsis specifically enhances the activities and expression of enzymes associated with ascorbate metabolism but not glutathione metabolism. Plant Physiol. 124 (2000) 823-832
7. Baier M., Ströher E., and Dietz K.J. The acceptor availability at photosystem I and ABA control nuclear expression of 2-Cys peroxiredoxin-A in Arabidopsis thaliana. Plant Cell Physiol. 45 (2004) 997-1006
8. Baier M., and Dietz K.J. Chloroplasts as source and target of cellular redox regulation, a discussion on chloroplast redox signals in the context of plant physiology. J. Exp. Bot. 56 (2005) 1449-1462
9. Baginsky S., Tiller K., Pfannschmidt T., and Link G. PTK, the chloroplast RNA polymerase-associated protein kinase from mustard (Sinapis alba), mediates redox control of plastid in vitro transcription. Plant Mol. Biol. 39 (1999) 1013-1023
10. Bartoli C.G., Pastori G.M., and Foyer C.H. Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol. 123 (2000) 335-344
11. Bartoli C.G., Yu J., Gomez F., Fernandez L., McIntosh L., and Foyer C.H. Inter-relationships between light and respiration in the control of ascorbic acid synthesis and accumulation in Arabidopsis thaliana leaves. J. Exp. Bot. 57 (2006) 1621-1631
12. Baumann U., and Juttner J. Plant thioredoxins, the multiplicity conundrum. Cell Mol. Life Sci. 59 (2002) 1042-1057
13. Blee E., and Joyard J. Envelope membranes from spinach chloroplasts are a site of metabolism of fatty acid hydroperoxides. Plant Physiol. 110 (1996) 445-454
14. Bosco C.D., Lezhneva L., Biehl A., Leister D., Strotmann H., Wanner G., and Meurer J. Inactivation of the chloroplast ATP synthase gamma subunit results in high non-photochemical fluorescence quenching and altered nuclear gene expression in Arabidopsis thaliana. J. Biol. Chem. 279 (2004) 1060-1069
15. Broin M., and Rey P. Potato plants lacking the CDSP32 plastidic thioredoxin exhibit overoxidation of the BAS1 2-cysteine peroxiredoxin and increased lipid peroxidation in thylakoids under photooxidative stress. Plant Physiol. 132 (2003) 1335-1343
16. Buchanan B.B., and Balmer Y. Redox regulation, a broadening horizon. Annu. Rev. Plant Biol. 56 (2005) 187-220
17. Cairns N.G., Pasternak M., Wachter A., Cobbett C.S., and Meyer A.J. Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis with the embryo. Plant Physiol. 141 (2006) 446-455
18. Chen Y.B., Durnford D.G., Koblizek M., and Falkowski P.G. Plastid regulation of Lhcb1 transcription in the chlorophyte alfa Dunaliella tertiolecta. Plant Physiol. 136 (2004) 3737-3750
19. Cheong Y.H., Chang H.S., Gupta R., Wang X., Zhu T., and Luan S. Transcriptional profiling reveals novel interaction between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 129 (2002) 661-677
20. Chiu W., Baker M.L., and Almo S.C. Structural biology of cellular machines. Trends Cell Biol. 16 (2006) 144-150
21. Collin V., Lamkemeyer P., Miginiac-Maslow M., Hirasawa M., Knaff D.B., Dietz K.J., and Issakidis-Bourguet E. Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type. Plant Physiol. 136 (2004) 4088-4095
22. Conklin P.L., Williams E.H., and Last R.L. Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc. Natl. Acad. Sci. USA 93 (1996) 9970-9974
23. Couee I., Sulmon C., Gouesbet G., and El Amrani A. Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J. Exp. Bot. 57 (2006) 449-459
24. Cross J.V., and Templeton D.J. Oxidative stress inhibits MEKK1 by site-specific glutatinylation in the ATP-binding domain. Biochem. J. 381 (2004) 675-683
25. Desikan R., Mackerness S.A.H., Hancock J.T., and Neill S.J. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127 (2001) 159-172
26. Despres C., DeLong C., Glaze S., Liu E., and Fobert P.R. The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12 (2000) 279-290
27. Despres C., Chubak C., Rochon A., Clark R., Bethune T., Desveaux D., and Fobert P.R. Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 15 (2003) 2181-2191
28. Dietz K.J. Redox control, redox signaling, and redox homeostasis in plant cells. Int. Rev. Cytol. 228 (2003) 141-193
29. Dietz K.J. Plant peroxiredoxins. Annu. Rev. Plant Biol. 54 (2003) 93-107
30. Dietz K.J., Jacob S., Oelze M.L., Laxa M., Tognetti V., de Miranda S.M., Baier M., and Finkemeier I. The function of peroxiredoxins in plant organelle redox metabolism. J. Exp. Bot. 57 (2006) 1697-1709
31. Dietz K.J., Neimanis S., and Heber U. Rate limiting factors in leaf photosynthesis. II. Electron transport. Biochim. Biophys. Acta 767 (1984) 444-450
32. Eicks M., Maurino V., Knappe S., Flügge U.I., and Fischer K. The plastidic pentose phosphate translocator represents a link between the cytosolic and the plastidic pentose phosphate pathways in plants. Plant Physiol. 128 (2002) 512-522
33. Escoubas J.-M., Lomas M., LaRoche S., Stutios L.M., Angell N.A., Mindrions M., Cho R.J., Oefner P.J., Davis R.W., and Ausubel F.M. Light intensity regulation of cab gene transcription is signalled by the redox state of the plastoquinone pool. Proc. Natl. Acad. Sci. USA 92 (1995) 10237-10241
34. Fey V., Wagner R., Brautigam K., Wirtz M., Hell R., Dietzmann A., Leister D., Oelmüller R., and Pfannschmidt T. Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J. Biol. Chem. 280 (2005) 5318-5328
35. Finkemeier I., Goodman M., Lamkemeyer P., Kandlbinder A., Sweetlove L.J., and Dietz K.J. The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J. Biol. Chem. 280 (2005) 12168-12180
36. Forti G., and Elli G. Stimulation of photophosphorylation by ascorbate as a function of light intensity. Plant Physiol. 112 (1996) 1509-1511
37. Foyer C.H. Prospects for enhancement of the soluble antioxidants, ascorbate and glutathione. BioFactors 25 (2001) 75-78
38. Foyer C.H., and Noctor G. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17 (2005) 1866-1875
39. Francke C., Siezen R.J., and Teusink B. Reconstructing the metabolic network of a bacterium from its genome. Trends Microbiol. 13 (2005) 550-558
40. Fryer M.J., Oxborough K., Mullineaux P.M., and Baker N.R. Imaging of photo-oxidative stress responses in leaves. J. Exp. Bot. 53 (2002) 1249-1254
41. Fryer M.J., Ball L., Oxborough K., Karpinski S., Mullineaux P.M., and Baker N.R. Control of Ascorbate peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J. 33 (2003) 691-705
42. Gadjev I., Vanderauwera S., Gechev T.S., Laloi C., Minkov I.N., Shulaev V., Apel K., Inzé D., Mittler R., and Van Breusegem F. Transcriptomic footprints disclose specificity of reactive oxygen species signalling in Arabidopsis. Plant Physiol. 141 (2006) 436-445
43. Giegé P., Sweetlove L.J., Cognat V., and Leaver C.J. Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell 17 (2005) 1497-1512
44. Gilles-Gonzalez M.A., and Gonzalez G. Heme-based sensors, defining characteristics, recent developments, and regulatory hypotheses. J. Inorg. Biochem. 99 (2005) 1-22
45. Goldschmidt E.E., and Huber S.C. Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiol. 99 (1992) 1443-1448
46. Grant C.M., MacIver F.H., and Dawes I.W. Glutathione synthetase is dispensable for growth under both normal and oxidative stress conditions in the yeast Saccharomyces cerevisiae due to an accumulation of the dipeptide gamma-glutamylcysteine. Mol. Biol. Cell 8 (1997) 1699-1707
47. Hagedorn P.H., Flyvbjerg H., and Moller I.M. Modelling NADH turnover in plant mitochondria. Physiol. Plant 120 (2004) 370-385
48. Halliwell B. How to characterize an antioxidant: an update. Biochem. Soc. Symp. 61 (1994) 73-101
49. Heine G.F., Hernández J.M., and Grotewold E. Two cysteines in plant R2R3 MYB domains participate in redox-dependent DNA binding. J. Biol. Chem. 279 (2004) 37878-37885
50. Henmi K., Demura T., Tsuboi S., Fukuda H., Iwabuchi M., and Ogawa K. Change in the redox state of glutathione regulates differentiation of tracheary elements in Zinnia cells and Arabidopsis roots. Plant Cell Physiol. 46 (2005) 1757-1765
51. Hisabori T., Hara S., Fujii T., Yamazaki D., Hosoya-Matsuda N., and Motohashi K. Thioredoxin affinity chromatography: a useful method for further understanding the thioredoxin network. J. Exp. Bot. 56 (2005) 1463-1468
52. Holmgren A., and Åslund F. Glutaredoxin. Meth. Enzymol. 252 (1995) 283-292
53. Horling F., Lamkemeyer P., König J., Finkemeier I., Kandlbinder A., Baier M., and Dietz K.J. Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiol. 131 (2003) 317-325
54. Hunt L., Lerner F., and Ziegler M. NAD-new roles in signalling and gene regulation in plants. New Phytol. 163 (2004) 31-44
55. Jacob C., Giles G.I., Giles N.M., and Sies H. Sulfur and selenium, the role of oxidation state in protein structure and function. Angew. Chem. Int. Ed. Engl. 42 (2003) 4742-4758
56. Jacquot J.P., Lancelin J.M., and Meyer Y. Thioredoxins: structure and function in plant cells. New Phytol. 136 (1997) 543-570
57. Junge W. Physical aspects of light harvesting, electron transport and electrochemical potential generation in photosynthesis of green plants. In: Pirson A., and Zimmermann M.H. (Eds). Encyclopedia of Plant Physiology: Photosynthesis I (1977), Springer Publ., Berlin 59-93
58. Kachroo A., Lapchyk L., Fukushige H., Hildebrand D., Klessig D., and Karchroo P. Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell 15 (2003) 2952-2965
59. Kandlbinder A., Finkemeier I., Wormuth D., Hanitzsch M., and Dietz K.J. The antioxidant status of photosynthesizing leaves under nutrient deficiency, redox regulation, gene expression and antioxidant activity in Arabidopsis thaliana. Physiol. Plant 120 (2004) 63-73
60. Karpinski S., Escobar C., Karpinska B., Creissen G., and Mullinaux P.M. Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9 (1997) 627-640
61. Karpinski S., Reynolds H., Karpinska B., Wingsle G., Creissen G., and Mullineaux P. Systemic signalling and acclimation in response to excess excitation energy in Arabidopsis. Science 284 (1999) 654-657
62. 2+ binding motifs. Plant Cell 10 (1998) 255-266
63. Kiddle G., Pastori G.M., Bernard S., Pignocchi C., Antoniw J., Verrier P.J., and Foyer C.H. Effects of leaf ascorbate content on defense and photosynthesis gene expression in Arabidopsis thaliana. Antioxid. Redox Signal. 5 (2003) 23-32
64. Klatt P., and Lamas S. Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur. J. Biochem. 267 (2000) 4928-4944
65. Kliebenstein D.J., Monde R.A., and Last R.L. Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol. 118 (1998) 637-650
66. Knoop V. The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr. Genet. 46 (2004) 123-139
67. Kolbe A., Oliver S.N., Fernie A.R., Stitt M., van Dongen J.T., and Geigenberger P. Combined transcript and metabolite profiling of Arabidopsis leaves reveals fundamental effects of the thiol-disulfide status on plant metabolism. Plant Physiol. 141 (2006) 412-422
68. König J., Baier M., Horling F., Kahmann U., Harris G., Schürmann P., and Dietz K.J. The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proc. Natl. Acad. Sci. USA 99 (2002) 5738-5743
69. Lamkemeyer P., Laxa M., Collin V., Li W., Finkemeier I., Schottler M.A., Holtkamp V., Tognetti V.B., Issakidis-Bourguet E., Kandlbinder A., Weis E., Miginiac-Maslow M., and Dietz K.J. Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J. 45 (2006) 968-981
70. Laxa M., König J., Dietz K.J., and Kandlbinder A. Role of the cysteinyl residues in Arabidopsis thaliana cyclophilin CYP20-3 in peptidyl-prolyl cis-trans isomerase and redox-related function. Biochem. J. 401 (2007) 287-297
71. Legen J., Kemp S., Krause K., Profanter B., Herrmann R.G., and Maier R.M. Comparative analysis of plastid transcription profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription machineries. Plant J. 31 (2002) 171-188
72. Leister D., and Schneider A. From genes to photosynthesis in Arabidopsis thaliana. Int. Rev. Cytol. 228 (2003) 31-83
73. Li X.P., Bjorkman O., Shih C., Grossman A.R., Rosenquist M., Jansson S., and Niyogi K.K. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403 (2000) 391-395
74. Luwe M. Antioxidants in the apoplast and symplast of beech (Fagus sylvatica L.) leaves: seasonal variation and responses to changing ozone concentrations in air. Plant Cell Environ. 19 (1996) 321-328
75. Mano J., Hideg E., and Asada K. Ascorbate in thylakoid lumen functions as an alternative electron donor to photosystem II and photosystem I. Arch. Biochem. Biophys. 429 (2004) 71-80
76. Mehler A. Studies on the reaction of illuminated chloroplasts I. Mechanisms of the reduction of oxygen and other Hill reagents. Arch. Biochem. Biophys. 33 (1951) 65-77
77. Meinhard M., and Grill E. Hydrogen peroxide is a regulator of ABI1, a protein phosphatase 2C from Arabidopsis. FEBS Lett. 508 (2001) 443-446
78. Meinhard M., Rodriguez P.L., and Grill E. The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta 214 (2002) 775-782
79. Meskauskiene R., Nater M., Goslings D., Kessler F., op den Camp R., and Apel K. FLU, a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 98 (2001) 12826-12831
80. Meyer A.J., and Fricker M.D. Direct measurement of glutathione in epidermal cells of intact Arabidopsis roots by two-photon laser scanning microscopy. J. Microsc. 198 (2000) 174-181
81. Millar A.H., Day D.A., and Whelan J. Mitochondrial biogenesis and function in Arabidopsis. In: Somerville C.R., and Meyerowitz E.M. (Eds). The Arabidopsis Book (2004), American Society of Plant Biologists, Rockville, MD doi:10.1199/tab.0009
82. Mittler R., Vanderauwera S., Gollery M., and Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 9 (2004) 490-498
83. Moran P.J., and Thompson G.A. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol. 125 (2001) 1074-1085
84. Mullineaux P., and Karpinski S. Signal transduction in response to excess light, getting out of the chloroplast. Curr. Opin. Plant Biol. 5 (2002) 43-48
85. Mullineaux P.M., and Rausch T. Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynth. Res. 86 (2005) 459-474
86. Munekage Y., Takeda S., Endo T., Jahns P., Hashimoto T., and Shikanai T. Cytochrome b(6)f mutation specifically affects thermal dissipation of absorbed light energy in Arabidopsis. Plant J. 28 (2001) 351-359
87. 2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13 (2001) 2513-2523
88. Mustacchi R., Hohmann S., and Nielsen J. Yeast systems biology to unravel the network of life. Yeast 23 (2006) 227-238
89. Nielsen J., and Oliver S. The next wave in metabolome analysis. Trends Biotechnol. 23 (2005) 544-546
90. Noctor G., and Foyer C.H. Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 (1998) 249-279
91. Nunes-Nesi A., Carrari F., Lytovchenko A., Smith A.M., Loureiro M.E., Ratcliffe R.G., Sweetlove L.J., and Fernie A.R. Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol. 137 (2005) 611-622
92. Ogawa K. Glutathione-associated regulation of plant growth and stress responses. Antioxid. Redox Signal. 7 (2005) 973-981
93. Okamuro J.K., Caster B., Villarroel R., Van Montagu M., and Jofuku K.D. The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc. Natl. Acad. Sci. USA 94 (1997) 7076-7081
94. Oliver S.G. From genomes to systems, the path with yeast. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 361 (2006) 477-482
95. op den Camp R.G., Przybyla D., Ochsenbein C., Laloi C., Kim C., Danon A., Wagner D., Hideg E., Gobel C., Feussner I., Nater M., and Apel K. Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15 (2003) 2320-2332
96. Oswald O., Martin T., Dominy P.J., and Graham I.A. Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc. Natl. Acad. Sci. USA 98 (2001) 2047-2052
97. Pastori G.M., Kiddle G., Antoniw J., Bernard S., Veljovic-Jovanovic S., Verrier P.J., Noctor G., and Foyer C.H. Leaf vitamin C contents modulate plant defence transcripts and regulate genes that control development through hormone signaling. Plant Cell 15 (2003) 939-951
98. Pena-Ahumanda A., Kahmann U., Dietz K.J., and Baier M. Regulation of peroxiredoxin expression versus expression of Halliwell-Asada-cycle enzymes during early seedling development of Arabidopsis thaliana. Photosynthesis Res. 89 (2006) 99-112
99. Perez-Ruiz J.M., Spinola M.C., Kirchsteiger K., Moreno J., Sahrawy M., and Cejudo F.J. Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage. Plant Cell 18 (2006) 2356-2368
100. Pfannschmidt T., Milsson A., and Allen J.F. Photosynthetic control of chloroplast gene expression. Nature 397 (1999) 625-628
101. Pfannschmidt T., Allen J.E., and Oelmüller R. Principles of redox control in photosynthetic gene expression. Physiol. Plant 112 (2001) 1-9
102. Pfannschmidt T. Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci. 8 (2003) 33-41
103. Piippo M., Allahverdiyeva Y., Paallarinen V., Suoranta U.M., Battchikova N., and Aro E.M. Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol. Genomics 25 (2006) 142-152
104. Polle A. Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modelling. Computer simulations as a step towards flux analysis. Plant Physiol. 126 (2001) 445-462
105. Potters G., Horemanns N., Cauberg R.J., and Asard H. Ascorbate and dehydroascorbate influence cell cycle progression in a tobacco cell suspension. Plant Physiol. 124 (2000) 17-20
106. Potters G., Horemanns N., Bellone S., Caubergs R.J., Trost P., Guisez Y., and Asard H. Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism. Plant Physiol. 134 (2004) 1479-1487
107. Renne P., Dressen U., Hebbeker U., Hille D., Flügge U.I., Westhoff P., and Weber A.P. The Arabidopsis mutant dct is deficient in the plastid glutamate/malate translocator DiT2. Plant J. 35 (2003) 316-331
108. Rook F., and Bevan M. Genetic approaches to understanding sugar response pathways. J. Exp. Bot. 54 (2003) 1-7
109. Rossel J.B., Wilson I.W., and Pogson B.J. Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol. 130 (2002) 1109-1120
110. Rossel J.B., Walter P.B., Hendrickson L., Chow W.S., Poole A., Mullineaux P.M., and Pogson B.J. A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. Plant Cell Environ. 29 (2006) 269-281
111. Rouhier N., Gelhaye E., and Jacquot J.P. Glutaredoxin-dependent peroxiredoxin from poplar: protein-protein interaction and catalytic mechanism. J. Biol. Chem. 277 (2002) 13609-13614
112. Rouhier N., Gelhaye E., and Jacquot J.P. Plant glutaredoxins, still mysterious reducing systems. Cell Mol. Life Sci. 61 (2004) 1266-1277
113. Rouhier N., Villarejo A., Srivastava M., Gelhaye E., Keech O., Droux M., Finkemeier I., Samuelsson G., Dietz K.J., Jacquot J.P., and Wingsle G. Identification of plant glutaredoxin targets. Antioxid. Redox Signal. 7 (2005) 919-929
114. Sakamoto A., Okumura T., Kaminaka H., Sumi K., and Tanaka K. Structure and differential response to abscisic acid of two promoters for the cytosolic copper/zinc-superoxide dismutase genes, SodCc1 and SodCc2, in rice protoplasts. FEBS Lett. 358 (1995) 62-66
115. Santos M., Gousseau H., Lister C., Foyer C.H., Creissen G., and Mullineaux P. Cytosolic ascorbate peroxidase from Arabidopsis thaliana L. is encoded by a small multigene family. Planta 198 (1996) 64-69
116. Schafer F.Q., and Buettner G.R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 30 (2001) 1191-1212
117. Scheibe R. Redox-modulation of chloroplast enzymes: a common principle for individual control. Plant Physiol. 96 (1991) 1-3
118. Scheibe R., Backhausen J.E., Emmerlich V., and Holtgrefe S. Strategies to maintain redox homeostasis during photosynthesis under changing conditions. J. Exp. Bot. 56 (2005) 1481-1489
119. Schneider A., Hausler R.E., Kolukisaoglu U., Kunze R., van der Graaff E., Schwacke R., Catoni E., Desimone M., and Flügge U.I. An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. Plant J. 32 (2002) 685-699
120. Schopfer P., Plachy C., and Frahry G. Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiol. 125 (2001) 1591-1602
121. Schürmann P., and Jacquot J.P. Plant thioredoxin systems revised. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51 (2000) 371-400
122. Seki M., Ishida J., Narusaka M., Fujita M., Nanjo T., Umezawa T., Kamiya A., Nakajima M., Enju A., Sakurai T., Satou M., Akiyama K., Yamaguchi-Shinozaki K., Carninci P., Kawai J., Hayashizaki Y., and Shinozaki K. Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct. Integr. Genomics 2 (2002) 282-291
123. Strand A., Asami T., Alonso J., Ecker J.R., and Chory J. Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrin IX. Nature 421 6918 (2003) 79-83
124. Streb P., Feierabend J., and Bligny R. Resistance to photoinhibition of photosystem II and catalase and antioxidative protection in high mountain plants. Plant Cell Environ. 20 (1997) 1030-1040
125. Ströher E., and Dietz K.J. Concepts and approaches towards understanding the cellular redox proteome. Plant Biol. 8 (2006) 407-418
126. Susek R.E., Ausubel F.M., and Chory J. Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74 (1993) 787-799
127. Taniguchi M., Taniguchi Y., Kawasaki M., Takeda S., Kato T., Sato S., Tabata S., Miyake H., and Sugiyama T. Identifying and characterizing plastidic 2-oxoglutarate/malate and dicarboxylate transporters in Arabidopsis thaliana. Plant Cell Physiol. 43 (2002) 706-717
128. Thimm O., Blasing O., Gibon Y., Nagel A., Meyer S., Kruger P., Selbig J., Muller L.A., Rhee S.Y., and Stitt M. MAPMAN, a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37 (2004) 914-939
129. Trebst A., Depka B., and Hollander-Czytko H. A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhardtii. FEBS Lett. 516 (2002) 156-160
130. Tyystjärvi E., Hakala M., and Sarvikas P. Mathematical modelling of the light response curve of photoinhibition of photosystem II. Photosynth Res. 84 (2005) 21-27
131. Ülker B., and Somssich I.E. WRKY transcription factors, from DNA binding towards biological function. Curr. Opin. Plant Biol. 7 (2004) 491-498
132. Veljovic-Jovanovic S.D., Pignocchi C., Noctor G., and Foyer C.H. Low ascorbic acid in the vtc1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol. 127 (2001) 426-435
133. Vernoux T., Wilson R.C., Seeley K.A., Reichheld J.P., Muroy S., Brown S., Maughan S.C., Cobbett C.S., Van Montagu M., Inzé D., May M.J., and Sung Z.R. The ROOT MERISTEMLESS/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12 (2000) 97-110
134. Wang S.M., Lue W.I., Yu T.S., Long J.H., Wang C.H., Eimert K., and Chen J. Characterisation of ADG1, an Arabidopsis locus encoding for ADG pyrophosphorylase small subunit, demonstrates that the presence of the small subunit is required for large subunit stability. Plant J. 13 (1998) 63-70
135. Wheeler G.L., Jones M.A., and Smirnoff N. The biosynthetic pathway of vitamin C in higher plants. Nature 393 (1998) 365-369
136. 2 and is indispensable for stress defence in C-3 plants. EMBO J. 16 (1997) 4806-4816
137. Wilson K.E., and Huner N.P. The role of growth rate, redox-state of the plastoquinone pool and the trans-thylakoid delta pH in photoacclimation of Chlorella vulgaris to growth irradiance and temperature. Planta 212 (2000) 93-102
138. Wolosiuk R.A., and Buchanan B.B. Thioredoxin and glutathione regulate photosynthesis in chloroplasts. Nature 266 (1977) 565-567
139. 2 availability. BMC Plant Biol. 6 (2006) 15
140. Xing T., and Jordan M. Genetic engineering of plant signal transduction mechanisms. Plant Mol. Biol. 18 (2000) 309-318
141. Zhang X., Zhang L., Dong F., Gao J., Galbraith D.W., and Song C.-P. Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol. 126 (2001) 1438-1448
142. Zimmermann P., Hirsch-Hoffmann M., Hennig L., and Gruissem W. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136 (2004) 2621-2632
143. Zimmermann P., Hennig L., and Gruissem W. Gene-expression analysis and network discovery using Genevestigator. Trends Plant Sci. 10 (2005) 407-409