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The effect of calcium on the antioxidant systems in the halophyte Cakile maritima under salt stress

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Abstract

The purpose of the current investigation was to study the effect of Ca2+ (0, 3.5 and 20 mM concentrations) on the antioxidant systems in the halophyte Cakile maritima under NaCl stress (0, 100, 200 and 400 mM NaCl). Plants treated with both moderate calcium (3.5 mM) and salt levels (100 mM) showed the maximum growth, and the addition of 20 mM calcium to the nutrient media did not significantly reduce the growth under the moderate salt treatment. The absence of calcium associated with high salt concentration induced a strong reduction of biomass production. The tolerance of C. maritima at moderate salinity and calcium was related with the lowest values of the parameters indicative of oxidative stress (malondialdehyde, electrolyte leakage and hydrogen peroxide concentration). This was accompanied with a higher peroxidase, superoxide dismutase, ascorbate peroxidase, monodehydroascorbate reductase, dehydroascorbate reductase and glutathione reductase activities. In contrast, in the absence of calcium, those enzymes showed the lowest activities under all salt treatments. As a whole, it can be noticed that salt tolerance was improved by moderate calcium concentration; however, the absence of calcium has a drastic effect on C. maritima.

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Abbreviations

ASC:

Ascorbate

CAT:

Catalase

DHAR:

Dehydroascorbate reductase

EL:

Electrolyte leakage

GR:

Glutathione reductase

GSH:

Reduced glutathione

MDA:

Malondialdehyde

MDHAR:

Monodehydroascorbate reductase

POX:

Peroxidase

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

TAC:

Total antioxidant capacity

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • Al-Harbi AR (1995) Growth and nutrient composition of tomato and cucumber seedlings as affected by sodium chloride salinity and supplemental calcium. J Plant Nutr 18:1403–1416

    Article  CAS  Google Scholar 

  • Arrigoni O, Dipierro S, Borracino G (1981) Ascorbate free radical reductase: a key enzyme of the ascorbic acid system. FEBS Lett 125:242–244

    Article  CAS  Google Scholar 

  • Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  CAS  PubMed  Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 227–287

    Google Scholar 

  • Banuls J, Legaz F, Primo-Millo E (1991) Salinity–calcium interactions on growth and ionic concentration of Citrus plants. Plant Soil 133:39–46

    Article  CAS  Google Scholar 

  • Bowler C, Van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cachorro P, Ortiz A, Cerda A (1993) Effects of saline stress and calcium on lipid composition in bean roots. Phytochemistry 32:1131–1136

    Article  CAS  Google Scholar 

  • Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    Article  CAS  Google Scholar 

  • Cano A, Hernandez-Ruiz J, Garcia-Canovas F, Acosta M, Arnao MB (1998) An end-point method for estimation of the total antioxidant activity in plant material. Phytochem Anal 9:196–202

    Article  CAS  Google Scholar 

  • Cramer G, Lauchli RA, Polito VS (1985) Displacement of Ca2+ by Na+ from the plasmalemma of root cells. A primary response to salt stress. Plant Physiol 79:207–211

    Article  CAS  PubMed  Google Scholar 

  • Cramer GR, Lauchli A, Epstein E (1986) Effects of NaCl and CaCl2 on ion activities in complex nutrient solutions and root growth of cotton. Physiol Plant 81:792–797

    Article  CAS  Google Scholar 

  • Dalton DA, Baird LM, Langeberg L, Taugher CY, Anyan WR, Vance CV, Sarath G (1993) Subcellular localization of oxygen defense enzymes in soybean (Glycine max L. Merr) root nodules. Plant Physiol 102:481–489

    CAS  PubMed  Google Scholar 

  • Davy AJ, Scott R, Cordazzo CV (2006) Biological flora of the British Isles: Cakile maritima. Scop J Ecol 94:695–711

    Article  Google Scholar 

  • De Azevedo Neto AD, Prisco JT, Enéas-Filho J, Braga de Abreu CE, Gomes-Filho E (2005) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94

    Article  Google Scholar 

  • Debez A, Ben Hamed K, Grignon C, Abdelly C (2004) Salinity effects on germination, growth, and seed production of the halophyte Cakile maritima. Plant Soil 262:179–189

    Article  CAS  Google Scholar 

  • Debez A, Saadaoui D, Ramani B, Ouerghi Z, Koyro HW, Huchzermeyer B, Abdelly C (2006) Leaf H+-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity. Environ Exp Bot 57:285–295

    Article  CAS  Google Scholar 

  • Delumeau O, Morère-le Paven MC, Montrichard F, Laval Martin DL (2000) Effects of short-term NaCl stress on calmodulin-dependent NAD kinase activity in two species of tomato. Plant Cell Environ 23:329–336

    Article  CAS  Google Scholar 

  • Di Baccio D, Tognetti R, Sebastiani L, Vitagliano C (2003) Responses of Populus deltoides_Populus nigra (Populus_euramericana) clone I-214 to high zinc concentrations. New Phytol 159:443–452

    Article  CAS  Google Scholar 

  • Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    Article  CAS  Google Scholar 

  • Edwards EA, Rawsthorne S, Mullineaux PM (1990) Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 180:278–284

    Article  CAS  Google Scholar 

  • Epstein E (1961) The essential role of calcium in selective cation transport by plant cells. Plant Physiol 36:437–444

    Article  CAS  PubMed  Google Scholar 

  • Evans NH, McAins MR, Hetherigton AM (2001) Calcium oscillation in higher plants. Curr Opin Plant Biol 4:415–420

    Article  CAS  PubMed  Google Scholar 

  • Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. Quart Rev Biol 61:313–337

    Article  Google Scholar 

  • Foyer CH, Halliwell B (1976) Presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  Google Scholar 

  • Foyer CH, Leandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92:696–717

    Article  CAS  Google Scholar 

  • Frew J, Jones P, Scholes G (1983) Spectrophotometric determination of hydrogen peroxide and organic hydroperoxides at low concentrations in aqueous solution. Anal Chim Acta 155:130–150

    Article  Google Scholar 

  • Gao XY, Yang GP, Xu ZQ, Xu FC (1999) Effect of calcium on anti-oxidant enzymes of lipid peroxidation of soybean leaves under water stress. J South China Agric Univ 2:58–62

    Google Scholar 

  • Gong M, Chen SN, Song YQ, Li ZG (1997) Effects of calcium and calmodulin on intrinsic heat tolerance in relation to antioxidant systems in maize seedlings. Aust J Plant Physiol 150:615–621

    CAS  Google Scholar 

  • Hachicha M, Job JO, Mtimet A (1994) Les sols salés et la salinisation en Tunisie. Sols de Tunisie 5:271–341

    Google Scholar 

  • Hepler PK, Wayne RO (1985) Calcium and Plant development. Annu Rev Plant Physiol 36:397–439

    Article  CAS  Google Scholar 

  • Hernandez JA, Aguilar AN, Portillo B, Gomez EL, Beneyto JM, Garcia-Legaz MF (2003) The effect of calcium on the antioxidant enzymes from salt-treated loquat and anger plants. Funct Plant Biol l30:1127–1137

    Article  Google Scholar 

  • Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. Commonwealth Bureau of Horticulture Teach. com.22

  • Jain M, Mathur G, Koul S, Sarin NB (2001) Ameliorative effects of proline on salt stress-induced lipid peroxidation in cell lines of groundnut (Arachis hypogaea L.). Plant Cell Rep 20:463–468

    Article  CAS  Google Scholar 

  • Jimenez A, Hernandez JA, del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate–glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284

    CAS  PubMed  Google Scholar 

  • Kauss H (1987) Some aspects of calcium-dependent regulation in plant metabolism. Annu Rev Plant Physiol 38:47–72

    Article  CAS  Google Scholar 

  • Koyro HW (2006) Effect of salinity on growth, photosynthesis, water relations and solute composition of the potential cash crop halophyte Plantago coronopus (L.). Environ Exp Bot 56:136–146

    Article  CAS  Google Scholar 

  • Lee JH, Hossner LR, Attrep M Jr, Kung KS (2002) Uptake and translocation of plutonium in two plant species using hydroponics. Environ Pollut 117:61–68

    Article  CAS  PubMed  Google Scholar 

  • Li M, Wang GX, Lin JS (2003) Application of external calcium in improving the PEG-induced water stress tolerance in liquorice cells. Bot Bull Acad Sin 44:275–284

    CAS  Google Scholar 

  • Lieth H, Moschenko M, Lohmann M, Koyro HW, Hamdy A (1999) Halophyte uses in different climates. I. Ecological and ecophysiological studies. Backhuys Publishers, Leiden, p 258

    Google Scholar 

  • Lin CC, Kao CH (1995) NaCl stress in rice seedlings: the influence of calcium on root growth. Bot Bull Acad Sin 36:41–45

    CAS  Google Scholar 

  • Martinez-Ballesta MC, Martinez V, Carvajal M (2000) Regulation of water channel activity in whole roots of melon plants grown under saline conditions. Aust J Plant Physiol 27:685–691

    Google Scholar 

  • McAinsh MR, Clayton H, Mansfield TA, Hetherington AM (1996) Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiol 111:1031–1042

    CAS  PubMed  Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymic function for erythrocuprein. J Biol Biochem 244:6049–6055

    CAS  Google Scholar 

  • Muscolo A, Sidari M, Panccio MR (2003) Tolerance of Kikuyu grass to long term salt stress in associated with induction of antioxidant defences. Plant Growth Regul 41:57–62

    Article  CAS  Google Scholar 

  • Nandwal AS, Godara M, Sheokand S, Kamboj DV, Kundu BS, Kuhad MS, Kumar B, Sharma SK (2000) Salinity induced changes in plant water status, nodule functioning and ionic distribution in phenotypically differing genotypes of Vigna radiata L. J Plant Physiol 156:350–359

    CAS  Google Scholar 

  • Noctor G, Foyer C (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Mol Biol 49:249–279

    Article  CAS  Google Scholar 

  • Owens S (2001) Salt of the earth. EMBO Rep 2:877–879

    CAS  PubMed  Google Scholar 

  • Paranhos A, Fernandez-Jarrago J, Corchete P (1994) Relationship between active oxygen species and cardenolide production in cell cultures of Digitalis thapsi: effect of calcium restriction. New Physiol 141:51–60

    Article  Google Scholar 

  • Parida AK, Das AB, Mohanty P (2004) Investigations on the antioxidative defence responses to NaCl stress in a mangrove, Bruguiera parviflora: differential regulations of isoforms of some antioxidative enzymes. Plant Growth Regul 42:213–226

    Article  CAS  Google Scholar 

  • Pietrobon DF, Virgilio O, Pozzea T (1990) Structural and functional aspects of calcium homeostasis in eukaryotic cells. Eur J Biochem 193:559–622

    Article  Google Scholar 

  • Price AH, Taylor A, Ripley SJ, Griffiths A, Trewavas AJ (1994) Oxidative signals in Tobacco increase cytosolic calcium. Plant Cell 6:1301–1310

    Article  CAS  PubMed  Google Scholar 

  • Rains D, Epstein E (1967) Sodium absorption by barley roots. Its mediation by mechanisms 2 of alkali cation transport. Plant Physiol 42:319–323

    Article  CAS  PubMed  Google Scholar 

  • Ranieri A, Petacco F, Castagna A, Soldatini GF (2000) Redox state and peroxidase system in sunflower plants exposed to ozone. Plant Sci 159:159–168

    Article  CAS  PubMed  Google Scholar 

  • Rozema J, Flowers T (2008) Cultivation of salt-tolerant crops can help address the threats of irreversible global salinization of fresh water and soils. Science 322:1478–1479

    Article  CAS  PubMed  Google Scholar 

  • Schaedle M, Bassham J (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012

    Article  CAS  PubMed  Google Scholar 

  • Shim IS, Yukie M, Akihiro Y, Dea-Wook K, Kenji U (2003) Inhibition of catalase activity by oxidative stress and its relationship to salicylic acid accumulation in plants. Plant Growth Regul 39:285–292

    Article  CAS  Google Scholar 

  • Shu MY, Fan MQ (2000) Effect of osmotic stress and calcium on membrane-lipid peroxidation and the activity of defense enzymes in fir seedling. Forest Res 4:391–396

    Google Scholar 

  • Tanaka K, Takeuchi E, Kubo A, Sakaki T, Haraguchi K, Kawamura Y (1991) Two immunologically different isozymes of ascorbate peroxidase from spinach leaves. Arch Biochem Biophys 286:371–375

    Article  CAS  PubMed  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  Google Scholar 

  • Trofimova MS, Andreev IM, Kuznetsov VV (1999) Calcium is involved in regulation of the synthesis of HSPs in suspension-cultured sugar beet cells under hyperthermia. Physiol Plant 105:67–73

    Article  CAS  Google Scholar 

  • Wang GX, Yang CD, Liang HG (1989) Changes in SOD activity and MDA content during the development of broad bean leaves. Acta Phytophysiol Sin 15:13–17

    CAS  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defense in C3 plants. EMBO J 16:4806–4816

    Article  CAS  PubMed  Google Scholar 

  • Yasar F (2007) Effects of salt stress on ion and lipid peroxidation content in green Beans genotypes. Asian J Chem 19:1165–1169

    CAS  Google Scholar 

  • Yokoi S, Bressan RA, Hasegawa PM (2002) Salt stress tolerance of plants. Jircas working report 25–33

  • Zarrouk M, El Almi H, Ben Youssef N, Sleimi N, Smaoui A, Ben Miled D, Abdelly C (2003) Lipid composition of local halophytes seeds: Cakile maritima, Zygophyllum album and Crithmum maritimum. In: Lieth H (ed) Cash crop halophytes: recent studies. 10 years after the Al Ain. Kluwer Academic Publishers Group, The Netherlands, pp 121–126

    Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Tunisian Ministry of Higher Education, Scientific research and Technology (LR02CB02).

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Authors and Affiliations

  1. Laboratoire d’Adaptation des Plantes aux Stress Abiotiques, CBBC, BP 901, 2050, Hammam-Lif, Tunisia

    Nader Ben Amor, Wided Megdiche & Chedly Abdelly

  2. Department of Plant Stress Biology and Pathology, Centro de Edafología y Biología Aplicada del Segura, Consejo Superior de Investigaciones Cientificas (CSIC), Apdo. 164, 30100, Murcia, Spain

    Ana Jiménez & Francisca Sevilla

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  1. Nader Ben Amor
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  2. Wided Megdiche
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  3. Ana Jiménez
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  4. Francisca Sevilla
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  5. Chedly Abdelly
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Correspondence to Chedly Abdelly.

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Communicated by M. Horbowicz.

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Ben Amor, N., Megdiche, W., Jiménez, A. et al. The effect of calcium on the antioxidant systems in the halophyte Cakile maritima under salt stress. Acta Physiol Plant 32, 453–461 (2010). https://doi.org/10.1007/s11738-009-0420-2

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  • DOI: https://doi.org/10.1007/s11738-009-0420-2

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