biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 61:791-796, 2017 | DOI: 10.1007/s10535-017-0729-4

Diurnal changes of subcellular glutathione content in Arabidopsis thaliana

B. Zechmann1,*
1 Center for Microscopy and Imaging, Baylor University, Waco, USA

The aim of this study was to investigate diurnal changes of subcellular glutathione content in leaves of Arabidopsis thaliana by immunohistochemistry and quantitative transmission electron microscopy. The results revealed major diurnal changes in glutathione content. The highest content was found within 2 - 3 h of exposure to light (increase of 489 % in mitochondria, 318 % in plastids, 857 % in nuclei, 511 % in peroxisomes, and 900 % in the cytosol when compared to that during darkness), followed by a strong drop (49 % in mitochondria and the cytosol, 53 % in plastids, 68 % in nuclei, 38 % in peroxisomes) within the next 1 - 2 h. Glutathione content was 67 % lower in mitochondria, 76 % in plastids, 73 % in nuclei, 50 % in peroxisomes, and 68 % in the cytosol at the end of the light period which lasted for 8 h when compared to highest content. Lowest glutathione content was found in most cell compartments at the very end of the dark period. In context with previous studies it could be concluded that low glutathione content at the end of the dark period was caused by lack of glycine and cysteine due to lack of photorespiration and decreased sulfur uptake and assimilation during darkness. The rapid increase of glutathione content observed within 3 h of light was most probably caused by a strong increase in glutathione synthesis triggered by increased glycine and cysteine content. The strong drop of glutathione after that period was most probably due to elevated glutathione degradation rate or increased use of glutathione for phytochelatin synthesis.

Keywords: antioxidants; chloroplasts; cytosol; mitochondria; peroxisomes; transmission electron microscopy
Subjects: glutathione; subcellular localization; diurnal course; chloroplasts; mitochondria; peroxisomes; cytosol

Received: July 16, 2016; Revised: January 6, 2017; Accepted: February 7, 2017; Published: December 1, 2017  Show citation

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Zechmann, B. (2017). Diurnal changes of subcellular glutathione content in Arabidopsis thaliana. Biologia plantarum61(4), 791-796. doi: 10.1007/s10535-017-0729-4
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References

  1. Buwalda, F., Stulen, I., De Kok, L.J., Kuiper, P.J.C.: Cysteine, c-glutamylcysteine and glutathione contents of spinach leaves as affected by darkness and application of excess sulfur. II. Glutathione accumulation in detached leaves exposed to H2S in the absence of light is stimulated by the supply of glycine to the petiole. - Physiol. Plant. 80: 196-204, 1990. Go to original source...
  2. Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Chetrit, P., Foyer, C.H., Paepe, R.: Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. - Plant Cell 15: 1212-1226, 2003. Go to original source...
  3. Forde, B.G., Lea, P.J.: Glutamate in plants: metabolism, regulation, and signaling. - J. exp. Bot. 58: 2339-2358, 2007. Go to original source...
  4. Foyer, C.H., Noctor, G.: Stress-triggered redox signalling: what's in pROSpect? - Plant Cell Environ. 39: 951-964, 2016. Go to original source...
  5. Höller, K., Király, L., Künstler, A., Müller, M., Gullner, G., Fattinger, M., Zechmann, B.: Enhanced glutathione metabolism is correlated with sulfur induced resistance in Tobacco mosaic virus-infected genetically susceptible Nicotiana tabacum plants. - Mol. Plant-Microbe Interact. 23: 1448-1459, 2011. Go to original source...
  6. Huseby, S., Koprivova, A., Lee, B.R., Shaha, S., Mithen, R., Wold, A.B., Bengtsson, G.B., Kopriva, S.: Diurnal and light regulation of sulphur assimilation and glucosinolate biosynthesis in Arabidopsis. - J. exp. Bot. 64: 1039-1048, 2013. Go to original source...
  7. Király, L., Künstler, A., Höller, K., Fattinger, M., Juhász, C., Müller, M., Gullner, G., Zechmann B.: Sulfate supply influences compartment specific glutathione metabolism and confers enhanced resistance to Tobacco mosaic virus during a hypersensitive response. - Plant Physiol. Biochem. 59: 44-54, 2012. Go to original source...
  8. Kocsy, G., Tari, I., Vankova, R., Zechmann, B., Gulyas, Z., Poor, P., Galiba, G.: Redox control of plant growth and development. - Plant Sci. 211: 77-91, 2013. Go to original source...
  9. Luschin-Ebengreuth, N., Zechmann, B.: Compartment specific investigations of antioxidants and hydrogen peroxide in leaves of Arabidopsis thaliana during dark induced senescence. - Acta Physiol. Plant. 38: 133, 2016. Go to original source...
  10. Massi, A., Ghisi, R., Ferretti, M.: Measuring low-molecularweight thiols by detecting the fluorescence of their SBDderivatives: application to studies of diurnal and UV-B induced changes in Zea mays L. - J. Plant Physiol. 159: 499-507, 2002. Go to original source...
  11. Maughan, S.C., Pasternak, M., Cairns, N., Kiddle, G., Brach, T., Jarvis, R., Haas, F., Nieuwlanda, J., Lim, B., Mueller, C., Salcedo-Sorae, E., Kruse, C., Orsel, M., Hell, R., Miller, A.J., Bray, P., Foyer, C.H., Murray, A.H., Meyer, A., Cobbett, C.S.: Plant homologs of the Plasmodium falciparum chloroquine resistance transporter PfCRT are required for glutathione homeostasis and stress responses. - Proc. nat. Acad. Sci. USA 107: 2331-2336, 2010. Go to original source...
  12. Noctor, G., Arisi, A.C.M., Jouanin, L., Foyer, C.H.: Photorespiratory glycine enhances glutathione accumulation in both the chloroplastic and cytosolic compartments. - J. exp. Bot. 50: 1157-1167, 1999. Go to original source...
  13. Noctor, G., Arisi, A.C., Jouanin, L., Valadier, M.H., Rouc, Y., Foyer C. H.: Light-dependent modulation of foliar glutathione synthesis and associated amino acid metabolism in poplar overexpressing c-glutamylcysteine synthetase. - Planta 202: 357-369, 1997. Go to original source...
  14. Polle, A.: Dissecting the superoxide dismutase-ascorbateglutathione pathway in chloroplasts by metabolic modeling: computer simulations as a step towards flux analysis. - Plant Physiol. 126: 445-462, 2001. Go to original source...
  15. Queval, G., Jaillard, D., Zechmann, B., Noctor G.: Increased intracellular H2O2 availability preferentially drives glutathione accumulation in vacuoles and chloroplasts. - Plant Cell Environ. 34: 21-32, 2011. Go to original source...
  16. Schupp, R., Rennenberg, H.: Diurnal changes in the glutathione content of spruce needles (Picea abies L.). - Plant Sci. 57: 113-117, 1988. Go to original source...
  17. Seth, C.S., Remans, T., Keunen, E., Jozefczak, M., Gielen, H., Opdenakker, K., Weyens, N., Vangronsveld, J., Cuypers, A.: Phytoextraction of toxic metals: a central role for glutathione. - Plant Cell Environ. 35: 334-346, 2012. Go to original source...
  18. Spoel, S.H., Loake, G.J.: Redox-based protein modifications: the missing link in plant immune signalling. - Curr. Opin. Plant Biol. 14: 358-364, 2011. Go to original source...
  19. Spoel, S.H., Van Ooijen, G.: Circadian redox signaling in plant immunity and abiotic stress. - Antioxid. Redox Signal. 20: 3024-3039, 2014. Go to original source...
  20. Valero, E., González-Sánchez, M.I., Macià, H., García-Carmona, F.: Computer simulation of the dynamic behavior of the glutathione-ascorbate redox cycle in chloroplasts. - Plant Physiol. 149: 1958-1969, 2009. Go to original source...
  21. Valero, E., Macià, H., Fuente, I., Hernandez, J.A., Gonzales-Sanchez, M.I., Garcia-Carmona, F.: Modeling the ascorbate-glutathione cycle in chloroplasts under light/dark conditions. - BMC Systems Biol. 10: 11, 2016. Go to original source...
  22. Van Ooijen, G., Millar, A.J.: Non-transcriptional oscillators in circadian timekeeping. - Trends Biochem. Sci. 37: 484-492, 2012. Go to original source...
  23. Wachter, A., Wolf, S., Steininger, H., Bogs, J., Rausch, T.: Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. - Plant J. 41: 15-30, 2005. Go to original source...
  24. Zechmann, B.: Compartment specific importance of glutathione during abiotic and biotic stress. - Front. Plant Sci. 5: 566, 2014. Go to original source...
  25. Zechmann, B., Mauch, F., Sticher, L., Müller, M.: Subcellular immunocytochemical analysis detects the highest concentrations of glutathione in mitochondria and not in plastids. - J. exp. Bot. 59: 4017-4027, 2008a. Go to original source...
  26. Zechmann. B., Müller, M.: Subcellular compartmentation of glutathione in dicotyledonous plants. - Protoplasma 246: 15-24, 2010. Go to original source...
  27. Zechmann, B., Müller, M., Zellnig, G.: Modified levels of cysteine affect glutathione metabolism in plant cells. - In Khan, N.A., Singh S., Umar S. (ed.): Sulfur Assimilation and Abiotic Stress in Plants. Pp. 193-206. Springer-Verlag, Berlin - Heidelberg 2008b. Go to original source...
  28. Zechmann, B., Zellnig, G., Urbanek-Krajnc, A., Müller, M.: Artificial elevation of glutathione affects symptom development in ZYMV-infected Cucurbita pepo L. plants. - Arch. Virol. 152: 747-762, 2007. Go to original source...




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