GABA shunt deficiencies and accumulation of reactive oxygen species under UV treatments: insight from Arabidopsis thaliana calmodulin mutants

• Autorzy: AL-Quaraan N.A.
• Języki publikacji: EN

Abstrakty

EN

Environmental stimuli such as UV, paraquat, and H2O2 can induce reactive oxygen species (ROS) production and impair the cellular redox equilibrium. ROS are controlled by a complex network of ROS metabolizing enzymes and play a major signaling role in different compartments of plants cell. GABA, alanine, and glutamate are all GABA shunt-related metabolites that are accumulated in response to oxidative stress. In this study, T-DNA insertion mutants of 7 calmodulin genes (CAM) in Arabidopsis thaliana were used to determine the role of specific CaM in tolerance of plants to oxidative stress induced by ultraviolet (UVA and UVB) treatments. Seedlings growth, seeds germination, reactive oxygen species accumulation, and changes in GABA shunt metabolites levels were determined. Only cam4 mutants showed significant tolerance to UVA and UVB treatments over the other cam mutants during seed germination. Oxidative damage measured as level of MDA caused by UV treatment was found in root and shoot tissues of cam1, cam4, cam5-4, and cam6-1 of Arabidopsis cam mutants. In response to UVA treatment, the shunt metabolites accumulated in root and shoot tissues after 30 min. As a result of UVB treatment, GABA accumulated after 30 min while alanine and glutamate accumulated after 60 min only in root tissue. There was a significant increase in GABA, alanine, and glutamate levels after 30, 60, and 90 min UVA treatments in root and shoot tissue of cam1, cam3-2, cam4, cam5-1, cam5-2, cam6-1, cam7-1 mutants. On the other hand, all shunt metabolites levels were significantly accumulated in root of cam1, cam4, cam5-4, and cam6-1 and only in shoot tissue of cam5-4 and cam6-1 mutants in response to 30, 60, and 90 min UVB treatment. Our results show that cam mutants are sensitive to induced-oxidative stress in response to both UV treatments especially cam1, cam4, cam5-4, cam6-1, and cam7-1 mutants for seed germination and ROS accumulation. Accumulation of GABA shunt metabolites under induced-oxidative stress via UV treatments demonstrates that GABA shunt pathway, GABA metabolites accumulation, and Ca+2/CaM-mediating signaling mechanisms are major components of antioxidant machinery associated with ROS scavenging, H2O2 equilibrium, maintaining balance of cellular redox state, and acquiring tolerance in cellular signaling in response to UV stress in Arabidopsis seedlings.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2015
• Tom: 37
• Numer: 04
• Opis fizyczny: Article: 86 [11 p.], ref.

Twórcy

autor

AL-Quaraan N.A.

• Department of Biotechnology and Genetic Engineering, Faculty of Science and Arts, Jordan University of Science and Technology, Irbid 22110, Jordan

Bibliografia

• AL-Quraan NA, Locy RD, Singh NK (2011) Implications of paraquat and hydrogen peroxide-induced oxidative stress treatments on the GABA shunt pathway in Arabidopsis thaliana calmodulin mutants. Plant Biotech Rep 5:225–234
• AL-Quraan NA, Locy RD, Singh NK (2012) Heat and cold stresses phenotypes of Arabidopsis thaliana calmodulin mutants: regulation of gamma-aminobutyric acid shunt pathway under temperature stress. Int J Plant Biology 3(e2):9–17
• Alscher RG, Donahue JH, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 100:224–233
• Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
• Aurisano N, Bertani A, Reggiani R (1995) Involvement of calcium and calmodulin in protein and amino acid metabolism in rice roots under anoxia. Plant Cell Physiol 36:1525–1529
• Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14:93–107
• Bailly C, Benamar A, Corbineau F, Côme D (2000) Antioxidant systems in sunflower (Helianthus annuus L.) seeds as affected by priming. Seed Sci Res 10:35–42
• Bailly C, Bogatek-Leszczynska R, Côme D, Corbineau F (2002) Changes in activities of antioxidant enzymes and lipoxygenase during growth of sunflower seedlings from seeds of different vigour. Seed Sci Res 12:47–55
• Bailly C, Leymarie J, Lehner A, Rousseau S, Côme D, Corbineau F (2004) Catalase activity and expression in developing sunflower seeds as related to drying. J Exp Bot 55:475–483
• Bergmeyer HU (1983) Methods of enzymatic analysis, vol I, 2nd edn. Weinheim:Verlag Chemie, Academic Press, New York, p 427
• Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptation to environmental stresses. Plant Cell 7:1099–1111
• Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J Exp Bot 53:1367–1376
• Bouche N, Fromm H (2004) GABA in plants: just a metabolite? Trend Plant Sci 9:110–115
• Bouche N, Fait A, Bouchez D, Moller SG, Fromm H (2003) Mitochondrial succinic-semialdehyde dehydrogenase of the gamma-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proc Natl Acad Sci USA 100:6843–6848
• Bouche N, Fait A, Zik M, Fromm H (2004) The root-specific glutamate decarboxylase (gad1) is essential for sustaining gaba level in Arabidopsis. Plant Mol Biol 55:315–325
• Bouche N, Yellin A, Snedden WA, Fromm H (2005) Plantspecific calmodulin-binding proteins. Annu Rev Plant Biol 56:435–466
• Chen YL, Huang RF, Xiao YM, Lu P, Chen J, Wang XC (2004) Extracellular calmodulin-induced stomatal closure is mediated by heterotrimeric G protein and H2O2. Plant Physiol 136:4096–4103
• Coleman ST, Fang TK, Rovinsky SA, Turano FJ, Moye-Rowley WS (2001) Expression of glutamate decarboxylase homologue is required for normal oxidative stress tolerance in Saccharomyces cerevisiae. J Biol Chem 276:244–250
• Cuin TA, Shabala S (2007) Compatible solutes reduce ROS-induced potassium efflux in Arabidopsis roots. Plant Cell Environ 30:875–885
• Desikan RA, Mackerness S, Hancock JT, Neill SJ (2001) Regulation of Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172
• Dröge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95
• Du L, Poovaiah BW (2005) Ca+2/calmodulin is critical for brassinosteroid biosynthesis and plant growth. Nature 437:741–745
• Fait A, Yellin A, Fromm H (2005) GABA shunt deficiencies and accumulation of reactive oxygen intermediates: insight from Arabidopsis mutants. FEBS Lett 579:415–420
• Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364
• Foyer CH, LopezDelgado H, Dat JF, Scott IM (1997) Hydrogen peroxide-and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100:241–254
• Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. Arch Biochem Biophys 125:189–198
• Hendricks SB, Taylorson RB (1975) Breaking of seed dormancy by catalase inhibition. Proc Natl Acad Sci USA 72:306–309
• Hong ZL, Lakkineni K, Zhang ZM, Verma DPS (2000) Removal of feedback inhibition of pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136
• Hu X, Jiang M, Zhang J, Zhang A, Lin F, Tan M (2007) Calciumcalmodulin is required for abscisic acid-induced antioxidant defense and functions both upstream and downstream of H2O2 production in leaves of maize (Zea mays) plants. New Phytol 173:27–38
• Kalbina I, Strid A (2006) Supplementary ultraviolet-b irradiation reveals differences in stress responses between Arabidopsis thaliana ecotypes. Plant Cell Environ 29:754–763
• Kwon SI, Lee H, An CS (2007) Differential expression of three catalase genes in the small radish (Rhaphanus sativus L. var. sativus). Mol Cells 24:37–44
• Locy RD, Wu S-J, Bisnette J, Barger TW, McNabb D, Zik M, Fromm H, Singh NK, Cherry JH (2000) The regulation of GABA accumulation by heat stress in Arabidopsis. In: Cherry JH, Locy RD, Rychter A (eds) Plant tolerance to abiotic stresses in agriculture: role of genetic engineering. NATO advanced research workshop series in cell biology. Kluwer Academic Publishers, Dordrecht, pp 39–53
• Ludewig F, Hüser A, Fromm H, Beauclair L, Bouché N (2008) Mutants of GABA transaminase (POP2) suppress the severe phenotype of succinic semialdehyde dehydrogenase (ssadh) mutants in Arabidopsis. PLoS One 3(10) e3383:1–10
• Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R (2007) Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiol 144:1777–1785
• Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trend Plant Sci 7:405–410
• Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trend Plant Sci 9:490–498
• Moller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591
• Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:472–497
• Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to paraquatinduced photooxidative stress and to nitric oxide-induced cell death. Plant J 38:940–953
• Neill SJ, Desikan RA, Hancock JT (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395
• Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359
• Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279
• Oracz K, El-Maarouf BH, Farrant JM, Cooper K, Belghazi M, Job C, Job D, Corbineau F, Bailly C (2007a) ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. Plant J 50:452–465
• Oracz K, Bailly C, Gniazdowska A, Côme D, Corbineau F, Bogatek R (2007b) Induction of oxidative stress by sunflower phytotoxins in germinating mustard seeds. J Chem Ecol 33:251–264
• Oracz K, El-Maarouf BH, Kranner I, Bogatek R, Corbineau F, Bailly C (2009) The mechanisms involved in seed dormancy alleviation by hydrogen cyanide unravel the role of reactive oxygen species as key factors of cellular signaling during germination. Plant Physiol 150:494–505
• Oracz K, Voegele A, Tarkowská D, Jacquemoud D, Turecková V, Urbanová T, Strnad M, Sliwinska E, Leubner-Metzger G (2012) Myrigalone A inhibits Lepidium sativum seed germination by interference with gibberellin metabolism and apoplastic superoxide production required for embryo extension growth and endosperm rupture. Plant Cell Physiol 53:81–95
• Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Signal 8:1757–1764
• Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74
• Reggiani R, Cantu CA, Brambilla I, Bertani A (1988) Accumulation and interconversion of amino acids in rice roots under anoxia. Plant Cell Physiol 29:981–987
• Rentel MC, Knight MR (2004) Oxidtaive stress-induced calcium signaling in Arabidopsis. Plant Physiol 135:1471–1479
• Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species: contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357–366
• Rogozhin VV, Kuriliuk TT, Filippova NP (2000) Change in the reaction of the antioxidant system of wheat sprouts after Uvirradiation of seeds [article in Russian]. Biofizika 45:730–736
• Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signal triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014
• Serraj R, Shelp BJ, Sinclair T (1998) Accumulation of gammaaminobutyric acid in nodulated soybean in response to droughtstress. Physiol Plant 102:79–86
• Shelp BJ, Walton CS, Snedden WA, Tuin LG, Oresnik IJ, Layzell DB (1995) GABA shunt In developing soybean seeds is associated with hypoxia. Physiol Plant 94:219–228
• Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trend Plant Sci 4:446–452
• Simontacchi M, Caro A, Fraga CG, Puntarulo S (1993) Oxidative stress affects [alpha]-tocopherol content in soybean embryonic axes upon imbibition and following germination. Plant Physiol 103:949–953
• Snedden WA, Koutsia N, Baum G, Fromm H (1996) Activation of a recombinant Petunia glutamate decarboxylase by calcium/calmodulin binding domain. J Biol Chem 271:4148–4153
• Turano FJ, Fang TK (1998) Characterization of two glutamate decarboxylase cDNA clones from Arabidopsis. Plant Physiol 117:1411–1421
• Vranova E, Inze D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236
• Yang T, Poovaiah BW (2002) Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proc Natl Acad Sci USA 99:4097–4102
• Yevtushenko DP, McLean MD, Peiris S, Van Cauwenberghe OR, Shelp BJ (2003) Calcium/calmodulin activation of two divergent glutamate decarboxylases from tobacco. J Exp Bot 54:2001–2002
• Zhang G, Bown AW (1997) The rapid determination of gammaaminobutyric acid. Phytochemistry 44:1007–1009
• Zik M, Arazi T, Snedden WA, Fromm H (1998) Two isoforms of glutamate decarboxylase in Arabidopsis are regulated by calcium/calmodulin and differ in organ distribution. Plant Mol Biol 37:967–975

Identyfikatory

DOI

10.1007/s11738-015-1836-5