Light intensity and spectrum affect metabolism of glutathione and amino acids at transcriptional level

Autoři: Dávid Toldi aff001;  Mónika Gyugos aff003;  Eva Darko aff003;  Gabriella Szalai aff003;  Zsolt Gulyás aff003;  Krisztián Gierczik aff003;  András Székely aff003;  Ákos Boldizsár aff003;  Gábor Galiba aff003;  Maria Müller aff005;  Livia Simon-Sarkadi aff001;  Gábor Kocsy aff003
Působiště autorů: Department of Food Chemistry and Nutrition, Szent István University, Budapest, Hungary aff001;  Doctoral School for Food Sciences, Szent István University, Budapest, Hungary aff002;  Agricultural Institute, Centre for Agricultural Research, Martonvásár, Hungary aff003;  Festetics Doctoral School, Georgikon Faculty, University of Pannonia, Keszthely, Hungary aff004;  Institute of Biology, Department of Plant Sciences, University of Graz, Graz, Austria aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0227271


The effects of various light intensities and spectral compositions on glutathione and amino acid metabolism were compared in wheat. Increase of light intensity (low—normal—high) was accompanied by a simultaneous increase in the shoot fresh weight, photosynthetic activity and glutathione content. These parameters were also affected by the modification of the ratios of blue, red and far-red components (referred to as blue, pink and far-red lights) compared to normal white light. The photosynthetic activity and the glutathione content decreased to 50% and the percentage of glutathione disulfide (characterising the redox state of the tissues) in the total glutathione pool doubled in far-red light. The alterations in the level and redox state of the antioxidant glutathione resulted from the effect of light on its synthesis as it could be concluded from the changes in the transcription of the related genes. Modification of the light conditions also greatly affected both the amount and the ratio of free amino acids. The total free amino acid content was greatly induced by the increase of light intensity and was greatly reduced in pink light compared to the normal intensity white light. The concentrations of most amino acids were similarly affected by the light conditions as described for the total free amino acid content but Pro, Met, Thr, ornithine and cystathionine showed unique response to light. As observed for the amino acid levels, the expression of several genes involved in their metabolism also enhanced due to increased light intensity. Interestingly, the modification of the spectrum greatly inhibited the expression of most of these genes. Correlation analysis of the investigated parameters indicates that changes in the light conditions may affect growth through the adjustment of photosynthesis and the glutathione-dependent redox state of the tissues. This process modifies the metabolism of glutathione and amino acids at transcriptional level.

Klíčová slova:

Amino acid metabolism – Gene expression – Glutathione – Leaves – Light – Oxidation-reduction reactions – Wheat – White light


1. Foyer CH, Noctor G. Redox Regulation in Photosynthetic Organisms: Signaling, Acclimation, and Practical Implications. Antioxid Redox Signal. 2009;11: 861–905. doi: 10.1089/ars.2008.2177 19239350

2. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, et al. ROS signaling: The new wave? Trends Plant Sci. Elsevier Ltd; 2011;16: 300–309. doi: 10.1016/j.tplants.2011.03.007 21482172

3. Cook CR. A question of intervention: American policymaking in Sierra Leone and the power of institutional agenda setting. African Stud Q. 2008;10: 1–33.

4. Sarala M. Elongation of Scots pine seedlings under blue light depletion. Silva Fenn. 2010;39: 131–136. doi: 10.14214/sf.401

5. Koga R, Meng T, Nakamura E, Miura C, Irino N, Devkota HP, et al. The effect of photo-irradiation on the growth and ingredient composition of young green barley (Hordeum vulgare). Agric Sci. 2013;4: 185–194. doi: 10.4236/as.2013.44027

6. Monostori I, Heilmann M, Kocsy G, Rakszegi M, Ahres M, Altenbach SB, et al. LED Lighting—Modification of Growth, Metabolism, Yield and Flour Composition in Wheat by Spectral Quality and Intensity. Front Plant Sci. 2018;9: 1–16.

7. Lund JB, Blom TJ, Aaslyng JM. End-of-day lighting with different red/far-red ratios using light-emitting diodes affects plant growth of Chrysanthemum x morifolium Ramat. “Coral Charm”. HortScience. 2007;42: 1609–1611.

8. Kianianmomeni A. More light behind gene expression. Trends Plant Sci. Elsevier Ltd; 2014;19: 488–490. doi: 10.1016/j.tplants.2014.05.004 24928178

9. Pedmale UV, Huang SC, Zander M, Cole BJ, Hetzel J, Ljung K, et al. Cryptochromes Interact Directly with PIFs to Control Plant Growth in Limiting Blue Light. Cell. 2016;164: 233–245. doi: 10.1016/j.cell.2015.12.018 26724867

10. Pham VN, Kathare PK, Huq E. Phytochromes and Phytochrome Interacting Factors. Plant Physiol. 2018;176: 1025–1038. doi: 10.1104/pp.17.01384 29138351

11. Bouly J, Schleicher E, Dionisio-sese M, Vandenbussche F, Van Der Straeten D, Bakrim N, et al. Cryptochrome Blue Light Photoreceptors Are Activated through Interconversion of Flavin Redox States. J Biol Chem. 2007;282: 9383–9391. doi: 10.1074/jbc.M609842200 17237227

12. Biswal B, Joshi PN, Raval MK, Biswal UC. Photosynthesis, a global sensor of environmental stress in green plants: Stress signalling and adaptation. Curr Sci. 2011;101: 47–56.

13. Qaderi MM, Godin VJ, Reid DM. Single and combined effects of temperature and red:far-red light ratio on evening primrose (Oenothera biennis). Botany. 2015;93: 475–483.

14. Kocsy G, Tari I, Vanková R, Zechmann B, Gulyás Z, Poór P, et al. Redox control of plant growth and development. Plant Sci. 2013;211: 77–91. doi: 10.1016/j.plantsci.2013.07.004 23987814

15. Considine MJ, Foyer CH. Redox regulation of plant development. Antioxid Redox Signal. 2014;21: 1305–26. doi: 10.1089/ars.2013.5665 24180689

16. Roach T, Stöggl W, Baur T, Kranner I. Distress and eustress of reactive electrophiles and relevance to light stress acclimation via stimulation of thiol/disulphide-based redox defences. Free Radic Biol Med. 2018;122: 65–73. doi: 10.1016/j.freeradbiomed.2018.03.030 29563047

17. Heyneke E, Luschin-Ebengreuth N, Krajcer I, Wolkinger V, Müller M, Zechmann B. Dynamic compartment specific changes in glutathione and ascorbate levels in Arabidopsis plants exposed to different light intensities. BMC Plant Biol. 2013;13: 104–123. doi: 10.1186/1471-2229-13-104 23865417

18. Wildi B, Lutz C. Antioxidant composition of selected high alpine plant species from different altitudes. Plant, Cell Environ. 1996;19: 138–146. doi: 10.1111/j.1365-3040.1996.tb00235.x

19. Manivannan A, Soundararajan P, Halimah N, Ko CH, Jeong BR. Blue LED light enhances growth, phytochemical contents, and antioxidant enzyme activities of Rehmannia glutinosa cultured in vitro. Hortic Environ Biotechnol. 2015;56: 105–113. doi: 10.1007/s13580-015-0114-1

20. Bartoli CG, Tambussi EA, Diego F, Foyer CH. Control of ascorbic acid synthesis and accumulation and glutathione by the incident light red/far red ratio in Phaseolus vulgaris leaves. FEBS Lett. Federation of European Biochemical Societies; 2009;583: 118–122. doi: 10.1016/j.febslet.2008.11.034 19059408

21. Geigenberger P, Fernie AR. Metabolic Control of Redox and Redox Control of Metabolism in Plants. Antioxid Redox Signal. 2014;21: 1389–1421. doi: 10.1089/ars.2014.6018 24960279

22. Noctor G. Manipulation of Glutathione and Amino Acid Biosynthesis in the Chloroplast. Plant Physiol. 1998;118: 471–482. doi: 10.1104/pp.118.2.471 9765532

23. Davis MC, Fiehn O, Durnford DG. Metabolic acclimation to excess light intensity in Chlamydomonas reinhardtii. Plant Cell Environ. 2013;36: 1391–1405. doi: 10.1111/pce.12071 23346954

24. Mazzella MA, Zanor MI, Fernie AR, Casal JJ. Metabolic responses to red/far-red ratio and ontogeny show poor correlation with the growth rate of sunflower stems. J Exp Bot. 2008;59: 2469–2477. doi: 10.1093/jxb/ern113 18515831

25. Kim K, Kook H-S, Jang Y-J, Lee W-H, Kamala-Kannan S, Chae J-C, et al. The Effect of Blue-light-emitting Diodes on Antioxidant Properties and Resistance to Botrytis cinerea in Tomato. J Plant Pathol Microbiol. 2013;04: 1–5. doi: 10.4172/2157-7471.1000203

26. Dhakal R, Baek K-H. Metabolic alternation in the accumulation of free amino acids and γ-aminobutyric acid in postharvest mature green tomatoes following irradiation with blue light. Hortic Environ Biotechnol. 2014;55: 36–41. doi: 10.1007/s13580-014-0125-3

27. Snyder RG. Vibrational spectra of crystalline n-paraffins. II. Intermolecular effects. J Mol Spectrosc. 1961;7: 116–144. doi: 10.1016/0022-2852(61)90347-2

28. Lichtenthaler HK. Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes. Methods Enzymol. 1987;148: 350–382. doi: 10.1016/0076-6879(87)48036-1

29. Snel JFH, van Kooten O. The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res. 1990;25: 147–150. doi: 10.1007/BF00033156 24420345

30. Kocsy G, Szalai G, Vágújfalvi A, Stéhli L, Orosz G, Galiba G. Genetic study of glutathione accumulation during cold hardening in wheat. Planta. 2000;210: 295–301. doi: 10.1007/PL00008137 10664136

31. Kranner I, Grill D. Determination of glutathione and glutathione disulphide in lichens: A comparison of frequently used methods. Phytochemical Analysis. 19967: 24–28. doi: 10.1002/(SICI)1099-1565(199601)7:1<24::AID-PCA277>3.0.CO;2-2

32. Gulyás Z, Simon-Sarkadi L, Badics E, Novák A, Mednyánszky Z, Szalai G, et al. Redox regulation of free amino acid levels in Arabidopsis thaliana. Physiol Plant. 2017;159: 264–276. doi: 10.1111/ppl.12510 27605256

33. Boldizsár Á, Vanková R, Novák A, Kalapos B, Gulyás Z, Pál M, et al. The mvp2 mutation affects the generative transition through the modification of transcriptome pattern, salicylic acid and cytokinin metabolism in Triticum monococcum. J Plant Physiol. 2016;202: 21–33. doi: 10.1016/j.jplph.2016.07.005 27450491

34. YAO X yang, LIU X ying, XU Z gang, JIAO X lei. Effects of light intensity on leaf microstructure and growth of rape seedlings cultivated under a combination of red and blue LEDs. J Integr Agric. 2017;16: 97–105. doi: 10.1016/S2095-3119(16)61393-X

35. Abdel-Ghany SE. Two P-Type ATPases Are Required for Copper Delivery in Arabidopsis thaliana Chloroplasts. Plant Cell Online. 2005;17: 1233–1251. doi: 10.1105/tpc.104.030452 15772282

36. Gruszeckia WI, Wardak A, Maksymiec W. The effect of blue light on electron transport in photosystem II reconstituted in planar bilayer lipid membrane. J Photochem Photobiol B Biol. 1997;39: 265–268. doi: 10.1016/S1011-1344(97)00014-6

37. Gallé Á, Czékus Z, Bela K, Horváth E, Ördög A, Csiszár J, et al. Plant Glutathione Transferases and Light. Front Plant Sci. 2019;9: 1–12. doi: 10.3389/fpls.2018.01944 30687349

38. Kolbe A. Combined Transcript and Metabolite Profiling of Arabidopsis Leaves Reveals Fundamental Effects of the Thiol-Disulfide Status on Plant Metabolism. Plant Physiol. 2006;141: 412–422. doi: 10.1104/pp.106.081208 16648214

39. Yang D, Seaton DD, Krahmer J, Halliday KJ. Photoreceptor effects on plant biomass, resource allocation, and metabolic state. PNAS. 2016;113: 7667–7672. doi: 10.1073/pnas.1601309113 27330114

40. Ramesh SA, Tyerman SD, Gilliham M, Xu B. γ-Aminobutyric acid (GABA) signalling in plants. Cellular and Molecular Life Sciences. 2017. pp. 1577–1603. doi: 10.1007/s00018-016-2415-7 27838745

41. Forde BG, Lea PJ. Glutamate in plants: Metabolism, regulation, and signalling. J Exp Bot. 2007;58: 2339–2358. doi: 10.1093/jxb/erm121 17578865

42. Suzuki A, Rioual S, Lemarchand S, Godfroy N, Roux Y, Boutin JP, et al. Regulation by light and metabolites of ferredoxin-dependent glutamate synthase in maize. Physiol Plant. 2001;112: 524–530. doi: 10.1034/j.1399-3054.2001.1120409.x 11473712

43. Szabados L, Savouré A. Proline: a multifunctional amino acid. Trends Plant Sci. 2010;15: 89–97. doi: 10.1016/j.tplants.2009.11.009 20036181

44. Krishnan N, Dickman MB, Becker DF. Proline modulates the intracellular redox environment and protects mammalian cells against oxidative stress. Free Radic Biol Med. 2008;44: 671–681. doi: 10.1016/j.freeradbiomed.2007.10.054 18036351

45. Takahashi T, Kakehi JI. Polyamines: Ubiquitous polycations with unique roles in growth and stress responses. Ann Bot. 2010;105: 1–6. doi: 10.1093/aob/mcp259 19828463

46. Winter G, Todd CD, Trovato M, Forlani G, Funck D. Physiological implications of arginine metabolism in plants. Front Plant Sci. 2015;6: 1–14.

47. Ros R, Muñoz-Bertomeu J, Krueger S. Serine in plants: biosynthesis, metabolism, and functions. Trends Plant Sci. 2014;19: 564–569. doi: 10.1016/j.tplants.2014.06.003 24999240

48. Ouyang F, Mao J, Wang J, Zhang S, Li Y. Transcriptome Analysis Reveals that Red and Blue Light Regulate Growth and Phytohormone Metabolism in Norway Spruce [Picea abies (L.) Karst.]. PLoS One. 2015; 1–19. doi: 10.1371/journal.pone.0127896 26237749

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