Abstract
The thiol tripeptide, glutathione (GSH) is an essential redox metabolite in plant cells but little information is available concerning GSH partitioning between the cytosol and nucleus. In this article we discuss the evidence concerning the distribution of GSH between the nucleus and the cytosol. The glutathione redox potential was similar in the nucleus and cytosol of developing radicles of Arabidopsis thaliana seeds after germination. However, in the arrested embryonic root meristem of the root meristemless 1 (rml1) mutant that have less than 5 % GSH of the wild type, GSH was predominantly localised in the nuclei. This was also the case in wild type roots treated with the auxin transport inhibitor, N-1-napthylphthalamic acid (NPA), which have decreased root glutathione levels. GSH was co-localised with nuclear DNA at G1 and G2 in A. thaliana cultures in which the cell cycle was synchronised. The functions of GSH are considered in terms of cell cycle regulation and the regulation of gene expression.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld JP (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22:376–391
Burhans WC, Heintz NH (2009) The cell cycle is a redox cycle: linking phase-specific targets to cell fate. Free Radic Biol Med 47:1282–1293
Cairns NG, Pasternak M, Wachter A, Cobbett CS, Meyer AJ (2006) Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiol 141:446–455
Cheng JC, Seeley KA, Sung ZR (1995) RML1 and RML2, Arabidopsis genes required for cell-proliferation at the root-tip. Plant Physiol 107:365–376
Cobbett CS, May MJ, Howden R, Rolls B (1998) The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in gamma-glutamylcysteine synthetase. Plant J 16:73–78
Diaz-Vivancos P, Dong Y-P, Ziegler K, Markovic J, Pallardó FV, Pellny TK, Verrier P, Foyer CH (2010a) Recruitment of glutathione into the nucleus during cell proliferation adjusts whole cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defence shield. Plant J 64:825–838
Diaz-Vivancos P, Wolff T, Markovic J, Pallardó FV, Foyer CH (2010b) A nuclear glutathione cycle within the cell cycle. Biochem J 431:169–178
GarcÃa-Giménez JL, Markovic J, Dasà F, Queval G, Schnaubelt D, Foyer CH, Pallardó FV (2013) Nuclear glutathione. Biochim Biophys Acta 1830:3304–3316
Han Y, Chaouch S, Mhamdi A, Queval G, Zechmann B, Noctor G (2013a) Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H2O2 to activation of salicylic acid accumulation and signaling. Antioxid Redox Signal 18:2106–2121
Han Y, Mhamdi A, Chaouch S, Noctor G (2013b) Regulation of basal and oxidative stress-triggered jasmonic acid-related gene expression by glutathione. Plant Cell Environ 36:1135–1146
Himanen K, Boucheron E, Vanneste S, de Almeida EJ, Inzé D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14:2339–2351
Howden R, Andersen CR, Goldsbrough PB, Cobbett CS (1995) A cadmium-sensitive, glutathione-deficient mutant of Arabidopsis thaliana. Plant Physiol 107:1067–1073
Koprivova A, Mugford ST, Kopriva S (2010) Arabidopsis root growth dependence on glutathione is linked to auxin transport. Plant Cell Rep 29:1157–1167
Markovic J, Borrás C, Ortega A, Sastre J, Viña J, Pallardó FV (2007) Glutathione is recruited into the nucleus in early phases of cell proliferation. J Biol Chem 282:20416–20424
Markovic J, Mora NJ, Broseta AM, Gimeno A, de-la-Concepción N, Viña J, Pallardó FV (2009) Nuclear GSH depletion impairs cell proliferation in 3T3 fibroblasts. PLoS One 29, e6413
Maughan S, Foyer CH (2006) Engineering and genetic approaches to modulating the glutathione network in plants. Physiol Plant 126:382–397
Maughan SC, Pasternak M, Cairns N, Kiddle G, Brach T, Jarvisb R, Haasc F, Nieuwlanda J, Limb B, Müllerc C, Salcedo-Sorae E, Krusec C, Orseld M, Hellc R, Millerd AJ, Braye P, Foyer CH, Murray JAH, Meyerc AJ, Cobbettb CS (2010) Plant homologs of the Plasmodium falciparum chloroquine-resistance transporter, PfCRT, are required for glutathione homeostasis and stress responses. Proc Natl Acad Sci U S A 107:2331–2336
Meister A (1988) Glutathione metabolism and its selective modification. J Biol Chem 263:17205–17208
Menon SG, Goswami PC (2007) A redox cycle within the cell cycle: ring in the old with the new. Oncogene 26:1101–1109
Menon SG, Sarsour EH, Spitz DR, Higashikubo R, Sturm M, Zhang H, Goswami PC (2003) Redox regulation of the G1 to S phase transition in the mouse embryo fibroblast cell cycle. Cancer Res 63:2109–2117
Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, Hell R (2007) Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52:973–986
Mullineaux PM, Rausch T (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynth Res 86:459–474
Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J Exp Bot 53:1283–1304
Noctor G, Queval G, Mhamdi A, Chaouch S, Foyer CH (2011) Glutathione. In: Millar H (ed) The Arabidopsis book 9. American Society of Plant Biologists, Rockville, pp 1–32
Noctor G, Mhamdi A, Queval G, Chaouch S, Han Y, Neukermans J, Foyer CH (2012) Glutathione functions in plants: an integrated overview. Plant Cell Environ 35:454–484
Pallardó FV, Markovic J, Garcia JL, Viña J (2009) Role of nuclear glutathione as a key regulator of cell proliferation. Mol Asp Med 30:77–85
Pasternak M, Lim B, Wirtz M, Hell R, Cobbett CS, Meyer AJ (2008) Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J 53:999–1012
Pellny TK, Locato V, Vivancos PD, Markovic J, De Gara L, Pallardo FV, Foyer CH (2009) Pyridine nucleotide cycling and control of intracellular redox state in relation to poly (ADP-ribose) polymerase activity and nuclear localisation of glutathione during exponential growth of Arabidopsis cells in culture. Mol Plant 2:442–456
Potters G, De Gara L, Asard H, Horemans H (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiol Biochem 40:537–548
Reichheld JP, Khafif M, Riondet C, Droux M, Bonnard G, Meyer Y (2007) Inactivation of thioredoxin reductases reveals a complex interplay between thioredoxin and glutathione pathways in Arabidopsis development. Plant Cell 19:1851–1865
Rennenberg H (1982) Glutathione metabolism and possible biological roles in higher-plants. Phytochemistry 21:2771–2781
Schnaubelt D, Queval G, Dong Y, Diaz-Vivancos P, Makgopa ME, Howell G, De Simone A, Bai J, Hannah MA, Foyer CH (2015) Low glutathione regulates gene expression and the redox potentials of the nucleus and cytosol in Arabidopsis thaliana. Plant Cell Environ. 38:266–279. doi:10.1111/pce.12252
Shanmugam V, Tsednee M, Yeh KC (2012) Zinc tolerance induced by iron 1 reveals the importance of glutathione in the cross-homeostasis between zinc and iron in Arabidopsis thaliana. Plant J 69:1006–10017
Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, Van Montagu M, Inze D, May MJ, Sung ZR (2000) The root meristemless1/cadmium sensitive2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12:97–110
Wachter A, Wolf S, Steininger H, Bogs J, Rausch T (2005) 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
Yu X, Pasternak T, Eiblmeier M, Ditengou F, Kochersperger P, Sun J, Wang H, Rennenberg H, Teale W, Paponov I, Zhou W, Li C, Li X, Palmea K (2013) Plastid-localized glutathione reductase 2–regulated glutathione redox status is essential for Arabidopsis root apical meristem maintenance. Plant Cell 25:4451–4468
Zechmann B, Mauch F, Sticher L, Müller M (2008) Subcellular immunocytochemical analysis detects the highest concentrations of glutathione in mitochondria and not in plastids. J Exp Bot 59:4017–4027
Zechmann B, Koffler BE, Russell SD (2011) Glutathione synthesis is essential for pollen germination in vitro. BMC Plant Biol 11:54
Acknowledgements
This work was funded by EU FP7: KBBE-2012-6-311840 (ECOSEED: ADS). PDV acknowledges the CSIC and the Spanish Ministry of Economy and Competitiveness for his ‘Ramon & Cajal’ research contract, co-financed by FEDER funds. YPD thanks the China Scholarship Council (China) for a scholarship.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
De Simone, A., Dong, Y., Vivancos, P.D., Foyer, C.H. (2015). GSH Partitioning Between the Nucleus and Cytosol in Arabidopsis thaliana . In: De Kok, L., Hawkesford, M., Rennenberg, H., Saito, K., Schnug, E. (eds) Molecular Physiology and Ecophysiology of Sulfur. Proceedings of the International Plant Sulfur Workshop. Springer, Cham. https://doi.org/10.1007/978-3-319-20137-5_4
Download citation
DOI: https://doi.org/10.1007/978-3-319-20137-5_4
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-20136-8
Online ISBN: 978-3-319-20137-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)