Abstract
Arabidopsis thaliana L. (Heynh.) plants were grown in low light (150 μmol photons m−2 s−1 and 20°C) either in short days (7.5 h photoperiod) or long days (16 h photoperiod), and then transferred into high light and low temperature (350–800 μmol photons m−2 s−1 at 12°C). Plants grown in short days responded with a rapid increase in NADP-malate dehydrogenase (EC 1.1.1.82) activation state. However, persisting overreduction revealed a new level of regulation of the malate valve. Activity measurements and Northern-blot analyses indicated that NADP-malate dehydrogenase transcript and protein levels increased within a few hours. Using macroarrays, additional changes in gene expression were identified. Transcript levels for several enzymes of glutathione metabolism and of some photosynthetic genes increased. The cellular glutathione level increased, but its redox state remained unchanged. A different situation was observed in plants grown in long-day conditions. Neither NADP-malate dehydrogenase nor glutathione content changed, but the expression of several antioxidative enzymes increased strongly. We conclude that the endogenous systems that measure day length interact with redox regulation, and override the interpretation of the signals, i.e. they redirect redox-mediated acclimation signals to allow for more efficient light usage and redox poising in short days to systems for the prevention of oxidative damages when grown under long-day conditions.
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Abbreviations
- Apx:
-
Ascorbate peroxidase
- Cat:
-
Catalase
- DTT:
-
Dithiothreitol
- GR:
-
Glutathione reductase
- GS:
-
Glutathione synthase
- LD:
-
Long day
- LHC:
-
Light-harvesting complex
- MDHAR:
-
Monodehydroascorbate reductase
- MDH:
-
Malate dehydrogenase
- NTR:
-
NADP-thioredoxin reductase
- SD:
-
Short day
- SOD:
-
Superoxide dismutase
- Trx:
-
Thioredoxin
References
Ahn JH (2002) Noncompetitive RT-PCR. In: Weigel D, Glazebrook J (eds) Arabidopsis. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 174–176
Anderson JM, Osmond CB (1987) Shade-sun responses: compromises between acclimation and photoinhibition. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 1–38
Aro EM, McCaffery S, Anderson JM (1994) Recovery from photoinhibition in peas (Pisum sativum L.) acclimated to varying growth irradiances. Plant Physiol 104:1033–1041
Backhausen JE, Scheibe R (1999) Adaptation of tobacco plants elevated CO2: influence of leaf age on changes in physiology, redox state and NADP-malate dehydrogenase activity. J Exp Bot 50:665–675
Backhausen JE, Kitzmann C, Horton P, Scheibe R (2000) Electron acceptors in isolated intact spinach chloroplasts act hierarchally to prevent over-reduction and competition for electrons. Photosynth Res 64:1–13
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
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Chen YB, Durnford DG, Koblizek M, Falkowski PG (2004) Plastid regulation of Lhcb1 transcription in the chlorophyte alga Dunaliella tertiolecta. Plant Physiol 136:3737–3750
Cheng XF, Wang ZY (2005) Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. Plant J 43:758–768
Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 78:3595–3599
Das R (2004) Photosynthesis. Regulation under varying light regimes. Science Publishers, Enfield
Del Longo OT, Gonzales CA, Pastori GM, Trippi VS (1993) Antioxidant defenses under hyperoxigenic and hyperosmotic conditions in leaves of two lines of maize with different sensitivity to drought. Plant Cell Physiol 34:1023–1028
Dodd AN, Love J, Webb AAR (2005) The plant clock shows its metal: circadian regulation of cytosolic free Ca2+. Trends Plant Sci 10:15–21
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 Physiol 115:705–715
Fey V, Wagner R, Brautigam K, Wirtzt M, Hell R, Dietzmann A, Leister D, Oelmüller R, Pfannschmidt T (2005) Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J Biol Chem 280:5318–5328
Fleming JE, Reveillaud I, Niedzwiecki A (1992) Role of oxidative stress in Drosophila aging. Mutat Res 275:267–279
Holtgrefe S, Bader KP, 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 Physiol 133:1768–1778
Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426:302–306
Jazwinski SM (1996) Longevity, genes, and aging. Science 273:54–59
Kandlbinder A, Finkemeier I, Wormuth D, Hanitsch M, Dietz K-J (2004) The antioxidant status of photosynthesising leaves under nutrient deficiency: redox regulation, gene expression and antioxidant activity in Arabidopsis thaliana. Physiol Plant 120:63–73
Kennedy BK, Austriaco NR, Zhang J, Guarente L (1995) Mutation in the silencing gene SIR4 can delay aging in S. cerevisiae. Cell 80:485–496
Koornneef M, Peeters AJM (1997) Floral transition mutants in Arabidopsis. Plant Cell Environ 20:779–784
Koornneef M, Alonso-Blanco C, Peeters AJM, Soppe W (1998) Genetic control of flowering time in Arabidopsis. Annu Rev Plant Physiol Plant Mol Biol 49:345–370
Kurepa J, Smalle J, Van Montagu M, Inzé D (1998) Oxidative stress tolerance and longevity in Arabidopsis: the late-flowering mutant gigantea is tolerant to paraquat. Plant J 14:759–764
Lohmann JU, Weigel D (2002) Building beauty: The genetic control of floral patterning. Dev Cell 2:135–142
Madueno F, Ruiz Garcia L, Salinas J, Zapater JM (1996) Genetic interactions that promote the floral transition in Arabidopsis. Semin Cell Dev Biol 7:401–407
Martin GM, Austad SN, Johnson TE (1996) Genetic analysis of aging: the role of oxidative damage and environmental stresses. Nat Genet 13:25–34
May MJ, Vernoux T, Leaver C, van Montagu M, Inzé D (1998) Glutathione homeostasis in plants: Implications for environmental sensing and plant development. J Exp Bot 49:649–667
Murakami S, Johnson TE (1996) A genetic pathway conferring life extension and resistance to UV stress in Caenorhabditis elegans. Genetics 143:1207–1218
Murchie EH, Hubbart S, Peng S, Horton P (2005) Acclimation of photosynthesis to high irradiance in rice: gene expression and interactions with leaf development. J Exp Bot 56:449–460
Ogawa K, Hatano-Iwasaki A, Yanagida M, Iwabuchi M (2004) Level of glutathione is regulated by ATP-dependent ligation of glutamate and cysteine through photosynthesis in Arabidopsis thaliana: mechanism of strong interaction of light intensity with flowering. Plant Cell Physiol 45:1–8
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of the accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents. Biochim Biophys Acta 975:384–394
Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 130:1109–1120
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbour Laboratory Press, Cold Spring Harbour
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. Aust J Plant Physiol 27:253–264
Savitch LV, Barker-Astrom 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
Scheibe R (2004) Malate valves to balance cellular energy supply. Physiol Plant 120:21–26
Scheibe R, Jacquot JP (1983) NADP regulates the light activation of NADP-dependent malate dehydrogenase. Planta 157:548–553
Scheibe R, Stitt M (1988) Comparison of NADP-malate dehydrogenase activation, QA reduction and O2 evolution in spinach leaves. Plant Physiol Biochem 26:473–481
Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S (2005) Strategies to maintain redox homeostasis during changing conditions. J Exp Bot 56:1481–1489
Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU (2003) Dissection of floral induction pathways using global expression analysis. Development 130:6001–6012
Schönfeld C, Wobbe L, Borgstadt R, Kienast A, Nixon PJ, Kruse O (2004) The nucleus-encoded protein MOC1 is essential for mitochondrial light acclimation in Chlamydomonas reinhardtii. J Biol Chem 279:50366–50374
Schulte M, von Ballmoos P, Rennenberg H, Herschbach C (2002) Live-long growth of Quercus ilex L. at natural CO2 springs acclimates sulfur, nitrogen and carbohydrate metabolism of the progeny to elevated CO2. Plant Cell Environ 25:1715–1727
Schultz TF, Kay SA (2003) Circadian clocks in daily and seasonal control of development. Science 301:326–328
Schupp R, Rennenberg H (1988) Diurnal changes in the glutathione concentration of spruce needles (Picea abies L.). Plant Sci 57:113–117
von Schaewen A, Langenkämper G, Graeve K, Wenderoth I, Scheibe R (1995) Molecular characterization of the plastidic glucose-6-phosphate dehydrogenase from potato in comparison to its cytosolic counterpart. Plant Physiol 109:1327–1335
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
Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447
Yanagida M, Nino M, Iwabuchi M, Ogawa K (2004) Reduced glutathione is a novel regulator of vernalization-induced bolting in the rosette plant Eustoma grandiflorum. Plant Cell Physiol 45:129–137
Acknowledgements
The authors thank H. Rennenberg and M. Eiblmeyer (Universitaet Freiburg, Germany) for their help with the method of glutathione determination. Further thanks are due to S. Klocke for her help with performing the experiments, and R. Brockmann for the frustrating job of measuring the NADP-MDH activities in Arabidopsis plants grown in mixed SD and LD conditions. We finally thank H. Wolf-Wibbelmann and S. Steinbach for excellently growing the plant material. This work was financially supported by a grant from the Deutsche Forschungsgemeinschaft (FOR 387, TP1 and TP3).
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Becker, B., Holtgrefe, S., Jung, S. et al. Influence of the photoperiod on redox regulation and stress responses in Arabidopsis thaliana L. (Heynh.) plants under long- and short-day conditions. Planta 224, 380–393 (2006). https://doi.org/10.1007/s00425-006-0222-3
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DOI: https://doi.org/10.1007/s00425-006-0222-3