Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-25T00:57:03.465Z Has data issue: false hasContentIssue false

Cloning and characterization of γ-glutamylcysteine synthetase in the salt- and oxidative stress-tolerant wild tomato species Solanum pennellii under abiotic stresses

Published online by Cambridge University Press:  13 April 2016

Waseim Barriah*
Affiliation:
Department of Life Sciences, Ben Gurion University of the Negev, Beer Sheva 84105, Israel Qasemi Research Center, Al-Qasemi Academy, P.O. Box 124, Baqa El-Gharbia 30100, Israel
Naim Najami
Affiliation:
Institute of Applied Research, Affiliated with University of Haifa, The Galilee Society, P.O. Box 437, Shefa-Amr 20200, Israel The Academic Arab College for Education, 22 Hachashmal St., P.O. Box 8349, Haifa 33145, Israel
Hilal Zaid*
Affiliation:
Qasemi Research Center, Al-Qasemi Academy, P.O. Box 124, Baqa El-Gharbia 30100, Israel Faculty of Arts and Sciences, Arab American University Jenin, P.O. Box 240, Jenin, Palestine
*
*Corresponding authors. E-mail: barriah@post.bgu.ac.il; hilalz@qsm.ac.il
*Corresponding authors. E-mail: barriah@post.bgu.ac.il; hilalz@qsm.ac.il

Abstract

The wild species of tomato Solanum pennellii (Lpa) is more tolerant to salt-induced oxidative stress than the cultivated species Solanum lycopersicum (Lem), due to the increase of several antioxidative metabolites and enzymes in this species under stress. The increase of reduced glutathione (GSH), one of these metabolites, in NaCl-treated Lpa, is due at least partly to the elevation of γ-glutamylcysteine synthetase (γ-ECS). Introgression line IL 8–3, which was found to include the Lpa orthologue of the γ-ECS gene (Lpa γ-ECS) in Lem's genetic background, was used to assign this gene to chromosome 8 and to assess its relative contribution to the effective antioxidative response of Lpa to stress. The growth of IL 8–3 and Lem plants responded similarly to NaCl and cadmium (Cd) stresses. In both genotypes, GSH and H2O2 levels responded also similarly to NaCl stress. NaCl and Cd stresses affected similarly the transcription of the γ-ECS gene in leaves of both IL 8–3 and Lpa plants. The effect of buthionine sulfoximine (BSO), a competitive inhibitor of the γ-ECS enzyme, on γ-ECS transcription was also similar in these two genotypes. Taken together, these results suggest that γ-ECS orthologues differ mainly in the regulation of their transcription and not at the post-transcriptional or translational levels. The mutation(s) led to these differences in the response of the two orthologues to the salinity and heavy metal stresses are expected to occur in a cis-regulatory element(s) located relatively close to γ-ECS.

Type
Research Article
Copyright
Copyright © NIAB 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bailey-Serres, J and Mittler, R (2006) The roles of reactive oxygen species in plant cells. Plant Physiology 141: 311311.CrossRefGoogle ScholarPubMed
Bashandy, T, Guilleminot, J, Vernoux, T, Caparros-Ruiz, D, Ljung, K, Meyer, Y and Reichheld, JP (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22: 376391.CrossRefGoogle ScholarPubMed
Brigelius-Flohé, R and Maiorino, M (2013) Glutathione peroxidases. Biochimica et Biophysica Acta 1830: 32893303.CrossRefGoogle ScholarPubMed
Caverzan, A, Passaia, G, Rosa, SB, Ribeiro, CW, Lazzarotto, F and Margis-Pinheiro, M (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genetics and Molecular Biology (Suppl.) 35: 10111019.CrossRefGoogle ScholarPubMed
Cobbett, CS, May, MJ, Howden, R and Rolls, B (1998) The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in gamma-glutamylcysteine synthetase. Plant Journal 16: 7378.CrossRefGoogle ScholarPubMed
Cuypers, A, Plusqui, M, Remans, T, Jozefczak, M, Keunen, E, Gielen, H, Opdenakker, K, Nair, AR, Munters, E and Artois, TJ (2010) Cadmium stress: an oxidative challenge. Biometals 23: 927940.CrossRefGoogle ScholarPubMed
Eshed, Y and Zamir, D (1994) A genomic library of Lycopersicon pennellii in esculentum: a tool for fine mapping of genes. Euphytica 9: 175179.CrossRefGoogle Scholar
Eshed, Y and Zamir, D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141: 11471162.CrossRefGoogle ScholarPubMed
Ferretti, M, Destro, T, Tosatto, SE, La Rocca, N, Rascio, N and Masi, A (2009) Gamma-glutamyl transferase in the cell wall participates in extracellular glutathione salvage from the root apoplast. New Phytologist 181: 115126.CrossRefGoogle ScholarPubMed
Foyer, CH and Halliwell, B (1976) The presence of glutathione and glutathione reductase in chloroplast: a proposed role in ascorbic acid metabolism. Planta 133: 2125.CrossRefGoogle ScholarPubMed
Foyer, CH and Noctor, G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17: 18661875.CrossRefGoogle ScholarPubMed
Foyer, CH and Noctor, G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiology 155: 218.CrossRefGoogle ScholarPubMed
Frendo, P, Mathieu, C, Van de Sype, G, Herouart, D and Puppo, A (1999) Characterisation of a cDNA encoding gamma-glutamylcysteine synthetase in Medicago truncatula. Free Radical Research 31(Suppl): S213S218.CrossRefGoogle ScholarPubMed
Gomez, LD, Noctor, G, Knight, MR and Foyer, CH (2004) Regulation of calcium signaling and gene expression by glutathione. Journal of Experimental Botany 55: 18511859.CrossRefGoogle ScholarPubMed
Griffith, OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Analytical Biochemistry 106: 207212.CrossRefGoogle ScholarPubMed
Hoagland, DR and Arnon, DI (1950) The water-culture method for growing plants without soil. In: California Agricultural Experiment Station Circular 347. Berkeley, CA: The College of Agriculture, University of California, pp. 139.Google Scholar
Jozefczak, M, Remans, T, Vangronsveld, J and Cuypers, A (2012) Glutathione is a key player in metal-induced oxidative stress defenses. International Journal of Molecular Science 13: 31453175.CrossRefGoogle ScholarPubMed
Kocsy, G, von Ballmoos, P, Suter, M, Ruegsegger, A, Galli, U, Szalai, G, Galiba, G and Brunold, C (2000) Inhibition of glutathione synthesis reduces chilling tolerance in maize. Planta 211: 528536.CrossRefGoogle ScholarPubMed
Lauchli, A (1984) Salt exclusion: an adaptation of legumes for crops and pastures under saline conditions. In: Staples, RC and Toenniessen, GH (eds) Salinity Tolerance in Plants: Strategies for Crop Improvement. New York: John Wiley & Sons, Inc., pp. 171187.Google Scholar
Mittler, R, Vanderauwera, S, Gollery, M and van Breusegem, F (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9: 490498.CrossRefGoogle ScholarPubMed
Mittova, V, Tal, M, Guy, M and Volokita, M (2002a) Response of the cultivated tomato and its wild salt tolerance relative Lycopersicon pennellii to salt-dependent oxidative stress: increase activities of antioxidant enzymes in root plastids. Free Radical Research 36: 195202.CrossRefGoogle Scholar
Mittova, V, Tal, M, Volokita, M and Guy, M (2002b) Salt-stress induces upregulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species. Physiologia Plantarum 115: 393400.CrossRefGoogle Scholar
Mittova, V, Tal, M, Volokita, M and Guy, M (2003a) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii . Plant Cell & Environment 26: 845856.CrossRefGoogle ScholarPubMed
Mittova, V, Theodoulou, FL, Kiddle, G, Gomez, L, Volokita, M, Tal, M, Foyer, CH and Guy, M (2003b) Coordinate induction of glutathione biosynthesis and glutathione metabolizing enzymes is correlated with salt tolerance in tomato. FEBS Letters 554: 417421.CrossRefGoogle ScholarPubMed
Mittova, V, Guy, M, Tal, MV and olokita, M (2004) Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii . J Exp Bot 55: 11051113.CrossRefGoogle ScholarPubMed
Noctor, G, Gomez, L, Vanacker, H and Foyer, CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. Journal of Experimental Botany 53: 12831304.CrossRefGoogle Scholar
Ogawa, K (2005) Glutathione-associated regulation of plant growth and stress responses. Antioxidants & Redox Signaling 7: 973981.CrossRefGoogle ScholarPubMed
Seth, CS, Remans, T, Keunen, E, Jozefczak, M, Gielen, H, Opdenakker, K, Weyens, N, Vangronsveld, J and Cuypers, A (2012) Phytoextraction of toxic metals: a central role for glutathione. Plant Cell & Environ ment 35: 334346.CrossRefGoogle ScholarPubMed
Shalata, A, Mittova, V, Volokita, M, Guy, M and Tal, M (2001) Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the root antioxidative system. Physiologia Plantarum 112: 487494.CrossRefGoogle ScholarPubMed
Smeets, K, Opdenakker, K, Remans, T, van Sanden, S, van Belleghem, F, Semane, B, Horemans, N, Guisez, Y, Vangronsveld, J and Cuypers, A (2009) Oxidative stress-related responses at transcriptional and enzymatic levels after exposure to Cd or Cu in a multipollution context. Journal of Plant Physiology 166: 19821992.CrossRefGoogle ScholarPubMed
Soltaninassab, SR, Sekhar, KR, Meredit, MJ and Freeman, ML (2000) Multi-faceted regulation of γ-glutamylcysteine synthetase. Journal of Cell Physiology 182: 163170.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Vestergaard, CL, Flyvbjerg, H and Møller, IM (2012) Intracellular signaling by diffusion: can waves of hydrogen peroxide transmit intracellular information in plant cells? Frontiers in Plant Science 3: 115.CrossRefGoogle ScholarPubMed
Wolff, S (1994) Ferrous ion oxidation in presence of ferric ion indicator xylenol orange for measurement of hydroperoxides. Methods in Enzymology 233: 182189.CrossRefGoogle Scholar
Supplementary material: File

Barriah supplementary material

Barriah supplementary material 1

Download Barriah supplementary material(File)
File 118.6 KB