, Volume 224, Issue 2, pp 380–393 | Cite as

Influence of the photoperiod on redox regulation and stress responses in Arabidopsis thaliana L. (Heynh.) plants under long- and short-day conditions

  • Beril Becker
  • Simone Holtgrefe
  • Sabrina Jung
  • Christina Wunrau
  • Andrea Kandlbinder
  • Margarete Baier
  • Karl-Josef Dietz
  • Jan E. Backhausen
  • Renate Scheibe
Original Article


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 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.


Glutathione Light acclimation Malate valve Oxidative stress Photoperiod Redox regulation 



Ascorbate peroxidase






Glutathione reductase


Glutathione synthase


Long day


Light-harvesting complex


Monodehydroascorbate reductase


Malate dehydrogenase


NADP-thioredoxin reductase


Short day


Superoxide dismutase





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).


  1. 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 174–176Google Scholar
  2. 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 1–38Google Scholar
  3. Aro EM, McCaffery S, Anderson JM (1994) Recovery from photoinhibition in peas (Pisum sativum L.) acclimated to varying growth irradiances. Plant Physiol 104:1033–1041PubMedGoogle Scholar
  4. 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 50:665–675CrossRefGoogle Scholar
  5. 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 64:1–13PubMedCrossRefGoogle Scholar
  6. 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 213:794–801PubMedCrossRefGoogle Scholar
  7. 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 72:248–254PubMedCrossRefGoogle Scholar
  8. Chen YB, Durnford DG, Koblizek M, Falkowski PG (2004) Plastid regulation of Lhcb1 transcription in the chlorophyte alga Dunaliella tertiolecta. Plant Physiol 136:3737–3750PubMedCrossRefGoogle Scholar
  9. 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 43:758–768PubMedCrossRefGoogle Scholar
  10. Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 78:3595–3599Google Scholar
  11. Das R (2004) Photosynthesis. Regulation under varying light regimes. Science Publishers, EnfieldGoogle Scholar
  12. 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 34:1023–1028Google Scholar
  13. Dodd AN, Love J, Webb AAR (2005) The plant clock shows its metal: circadian regulation of cytosolic free Ca2+. Trends Plant Sci 10:15–21PubMedCrossRefGoogle Scholar
  14. 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 115:705–715PubMedCrossRefGoogle Scholar
  15. 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 280:5318–5328PubMedCrossRefGoogle Scholar
  16. Fleming JE, Reveillaud I, Niedzwiecki A (1992) Role of oxidative stress in Drosophila aging. Mutat Res 275:267–279PubMedGoogle Scholar
  17. 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 133:1768–1778PubMedCrossRefGoogle Scholar
  18. Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426:302–306PubMedCrossRefGoogle Scholar
  19. Jazwinski SM (1996) Longevity, genes, and aging. Science 273:54–59PubMedCrossRefGoogle Scholar
  20. 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 120:63–73PubMedCrossRefGoogle Scholar
  21. Kennedy BK, Austriaco NR, Zhang J, Guarente L (1995) Mutation in the silencing gene SIR4 can delay aging in S. cerevisiae. Cell 80:485–496PubMedCrossRefGoogle Scholar
  22. Koornneef M, Peeters AJM (1997) Floral transition mutants in Arabidopsis. Plant Cell Environ 20:779–784CrossRefGoogle Scholar
  23. Koornneef M, Alonso-Blanco C, Peeters AJM, Soppe W (1998) Genetic control of flowering time in Arabidopsis. Annu Rev Plant Physiol Plant Mol Biol 49:345–370PubMedCrossRefGoogle Scholar
  24. 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 14:759–764PubMedCrossRefGoogle Scholar
  25. Lohmann JU, Weigel D (2002) Building beauty: The genetic control of floral patterning. Dev Cell 2:135–142PubMedCrossRefGoogle Scholar
  26. Madueno F, Ruiz Garcia L, Salinas J, Zapater JM (1996) Genetic interactions that promote the floral transition in Arabidopsis. Semin Cell Dev Biol 7:401–407CrossRefGoogle Scholar
  27. Martin GM, Austad SN, Johnson TE (1996) Genetic analysis of aging: the role of oxidative damage and environmental stresses. Nat Genet 13:25–34PubMedCrossRefGoogle Scholar
  28. 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 49:649–667CrossRefGoogle Scholar
  29. Murakami S, Johnson TE (1996) A genetic pathway conferring life extension and resistance to UV stress in Caenorhabditis elegans. Genetics 143:1207–1218PubMedGoogle Scholar
  30. 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 56:449–460PubMedCrossRefGoogle Scholar
  31. 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 45:1–8PubMedCrossRefGoogle Scholar
  32. 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 975:384–394CrossRefGoogle Scholar
  33. Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 130:1109–1120PubMedCrossRefGoogle Scholar
  34. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbour Laboratory Press, Cold Spring HarbourGoogle Scholar
  35. 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 27:253–264Google Scholar
  36. 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 214:295–303PubMedCrossRefGoogle Scholar
  37. Scheibe R (2004) Malate valves to balance cellular energy supply. Physiol Plant 120:21–26PubMedCrossRefGoogle Scholar
  38. Scheibe R, Jacquot JP (1983) NADP regulates the light activation of NADP-dependent malate dehydrogenase. Planta 157:548–553CrossRefGoogle Scholar
  39. Scheibe R, Stitt M (1988) Comparison of NADP-malate dehydrogenase activation, QA reduction and O2 evolution in spinach leaves. Plant Physiol Biochem 26:473–481Google Scholar
  40. Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S (2005) Strategies to maintain redox homeostasis during changing conditions. J Exp Bot 56:1481–1489PubMedCrossRefGoogle Scholar
  41. 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 130:6001–6012PubMedCrossRefGoogle Scholar
  42. 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 279:50366–50374PubMedCrossRefGoogle Scholar
  43. 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 25:1715–1727CrossRefGoogle Scholar
  44. Schultz TF, Kay SA (2003) Circadian clocks in daily and seasonal control of development. Science 301:326–328PubMedCrossRefGoogle Scholar
  45. Schupp R, Rennenberg H (1988) Diurnal changes in the glutathione concentration of spruce needles (Picea abies L.). Plant Sci 57:113–117CrossRefGoogle Scholar
  46. 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 109:1327–1335CrossRefGoogle Scholar
  47. Walters RG, Rogers JJM, Shephard F, Horton P (1999) Acclimation of Arabidopsis thaliana to the light environment: the role of photoreceptors. Planta 209:517–527PubMedCrossRefGoogle Scholar
  48. Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447PubMedCrossRefGoogle Scholar
  49. 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 45:129–137PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Beril Becker
    • 1
  • Simone Holtgrefe
    • 1
  • Sabrina Jung
    • 1
  • Christina Wunrau
    • 1
  • Andrea Kandlbinder
    • 2
  • Margarete Baier
    • 2
  • Karl-Josef Dietz
    • 2
  • Jan E. Backhausen
    • 1
  • Renate Scheibe
    • 1
  1. 1.Pflanzenphysiologie, Fachbereich Biologie/ChemieUniversität OsnabrückOsnabrückGermany
  2. 2.Lehrstuhl für Biochemie und Physiologie der Pflanzen, Fakultät für BiologieUniversität BielefeldBielefeldGermany

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