Glycine betaine affects the antioxidant system and ion accumulation and reduces salinity-induced damage in safflower seedlings

Authors

  • Farnaz Alasvandyari Department of Agronomy and Plant Breeding, Agriculture College, Vali-e-Asr University of Rafsanjan
  • Batool Mahdavi Department of Agronomy and Plant Breeding, Agriculture College, Vali-e-Asr University of Rafsanjan
  • Shahab Madah Hosseini Department of Agronomy and Plant Breeding, Agriculture College, Vali-e-Asr University of Rafsanjan

Keywords:

enzyme activity, germination, glycine betaine, safflower, salt stress

Abstract

Safflower (Carthamus tinctorius L.) is an important oilseed crop, usually grown on a small scale and in salt-affected soils. Salinity stress can cause oxidative damage to plants. Upregulation of the antioxidant defense system induced by glycine betaine (GlyBet) alleviates the damaging effects of oxidative stress in plants. In the present investigation, seeds were treated with 0, 10, 30 and 60 mM of GlyBet solutions. Germination and the primary growth of the seedling were examined using sodium chloride salt (NaCl) at 0 (non-stress), 50, 100 and 150 mM concentrations. The obtained results indicate that at 50 and 100 mM NaCl, priming with 30 and 60 mM GlyBet increased root and shoot lengths compared to the control (0 mM). In addition, at all stress levels, priming with 60 mM GlyBet led to lower malondialdehyde, total soluble sugars and proline contents than in control seedlings. Priming with GlyBet increased catalase (CAT), superoxide dismutase (SOD) enzyme activities and protein content, while it reduced the activity of peroxidase (POD) under salinity stress. In addition, priming with GlyBet reduced the Na+/K+ ratio of seedlings and increased K+ under all salinity stress levels. Priming with 60 mM GlyBet also reduced the Na+ content under 150 mM NaCl. Together, these results show that 60 mM GlyBet had the most pronounced effect on tolerance to salinity stress in safflower seedling. The GlyBet-increased tolerance to salt in safflower was mainly related to increased CAT and SOD activities, and the prevention of cell membrane damage as a result of reduced lipid peroxidation and improved ion homeostasis under salinity stress condition.

DOI: 10.2298/ABS160216089A

Received: February 16, 2016; Revised: April 25, 2016; Accepted: May 23, 2016; Published online: October 21, 2016

How to cite this article: Alasvandyari F, Mahdavi B, Hosseini Shahab M. Glycine betaine affects the antioxidant system and ion accumulation and reduces salinity-induced damage in safflower seedlings. Arch Biol Sci. 2017;69(1):139-47.

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Author Biography

Batool Mahdavi, Department of Agronomy and Plant Breeding, Agriculture College, Vali-e-Asr University of Rafsanjan

Department of Agronomy and Plant Breeding, Agriculture College, Vali-e-Asr University of Rafsanjan

References

Munns R, Tester M. Mechanisms of salinity tolerance. Ann Rev Plant Biol. 2008;59:651-81.

Greenway H, Munns R. Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol. 1980;70:303-7.

Ahmad S, Ahmad R, Ashraf MY, Ashraf M, Waraich EA. Sunflower (Helianthus annuus L.) response to drought stress at germination and growth stages. Pak J Bot. 2009;41(2):647-54.

Albuquerque FMCD, Carvalho NMD. Effect of type of environmental stress on the emergence of sunflower (Helianthus annuus L.), soybean (Glycine max (L.) Merril) and maize (Zea mays L.) seeds with different levels of vigor. Seed Sci Technol. 2003;31:465-7.

Hoque MA, Okuma E, Banu MNA, Nakamura Y, Shimoishi Y, Murata Y. Exogenous proline mitigates the detrimental effects of salt stress more than the betaine by increasing antioxidant enzyme activities. J Plant Physiol. 2007;164:553-61.

Hare PD, Cress WA, Van-Staden J. Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 1998;21(6):535-53.

Sakamoto A, Murata N. Genetic engineering of GlyBet synthesis in plants: current status and implications for enhancement of stress tolerance. J Exp Bot. 2000;51:81-8.

Saneoka H, Nagasaka C, Hahn DT, Yang WJ, Premachandra GS, Joly RJ, Rhodes D. Salt tolerance of GlyBet-deficient and -containing maize lines. Plant Physiol. 1995;107:631-8.

Hayashi H, Alia Sakamoto A, Nonaka H, Chen THH, Murata N. Enhanced germination under high-salt conditions of seeds of transgenic Arabidopsis with a bacterial gene (codA) for choline oxidase. J Plant Res. 1998;111:357-62.

Gadallah MMA. Effects of proline and GlyBet on Vicia faba responses to salt stress. Plant Biol. 1999;42:249-57.

Mansour MMF. Protection of plasma membrane of onion epidermal cells by GlyBet and proline against NaCl stress. Plant Physiol Biochem. 1998;36(10):767-72.

Rahman MS, Miyake H, Takeoka Y. Effects of exogenous GlyBet on growth and ultra-structure of salt-stressed rice seedlings (Oryza sativa L.). Plant Prod Sci. 2002;5:33-44.

Ma Q, Wang W, Li Y, Li D, Zou Q. Alleviation of photo-inhibition in drought-stresses wheat (Triticum aestivum) by foliar-applied GlyBet. Plant Physiol. 2006;163:165-75.

Hu L, Hu T, Zhang X, Pang H, Fu J. Exogenous GlyBet ameliorates the adverse effect of salt stress on perennial ryegrass. J Amer Sooc Hort Sci. 2012;137(1):38-46.

Bassil ES, Kaffka SR. Response of safflower (Carthamus tinctorius L.) to saline soils and irrigation: II. Crop response to salinity. Agricult Water Manag. 2002;54(1):67-80.

Perry LM. Medicinal plants of east and Southeast Asia: Attributed properties and uses. Cambridge, UK: MIT Press; 1980.

Singh V, Nimbkar N. Safflower (Carthamus tinctorius L.). In: Singh RJ, editor. Genetic resources, chromosome engineering and crop improvement. Vol 4: Oilseed Crops. Boca Raton: CRC Press; 2006. p. 167-94.

Ramana S, Biswas AK, Kundu S, Saha JK, Yadava RBR. Effect of distillery effluent on seed germination in some vegetable crops. Bioresour Technol. 2002;82:273-5.

Bates LS, Waldern RP, Teave ID. Rapid determination of free proline for water stress studies. Plant Soil. 1973;39:205-7.

Heath RL, Packer L. Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys. 1968;125(1):189-98.

Dubois M, Gilles KA, Hamilton JK, Reber PA, Smith F. Colorimetric method for determination of sugars and related substances. Annu Chem. 1956;28(3):350-6.

Bradford, MM. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of proteindye-binding. Annu Biochem. 1976;72:248-54.

Cakmak I, Marschner H. Enhanced superoxide radical production in roots of zinc-deficient plants. J Exp Bot. 1988;39:1449-60.

Pandolfini T, Gabbrielli R, Comparini C. Nickel toxicity and peroxidase activity in seedlings of Triticum aestivum L. Plant Cell Environ. 1992;15:719-25.

Giannopolitis CN, Ries SK. Superoxide dismutases occurrence in higher plants. Plant Physiol. 1977;59(2):309-14.

Shafi M, Bakht J, Khan MJ, Khan MA. Effect of salinity and ion accumulation of wheat genotypes. Pak J Bot. 2010;42(6):4113-21.

Sharma SK, Grag OP. Salinity induced changes in plant growth and activities of glutamate dehydrogenase, aspartate and alanine amino-transferases in wheat. Indian J Plant Physi. 1985;28:407-12.

Taamalli W, Abz L, Youssef NB, Miled DDB, Zarrouk M. Lipid breakdown in sunflower (Helianthus annuus L.) seeds during post germinative growth under salt-stress. Riv Ital Sostanze Gr. 2004;81:90-7.

Jamil M, Lee DB, Jung KY, Ashraf M, Lee SC, Rha ESh. Effect of salt (NaCl) stress on germination and early seedling growth of four vegetables species. Cent Eur Agric. 2006;7:273-82.

Iqbal N, Ashraf MY. Does seed treatment with GlyBet improve germination rate and seedling growth of sunflower (Helianthus annuus L.) under osmotic stress. Pak J Bot. 2006;38(5):1641-8.

Kausar N, Nawaz Kh, Hussain Kh, Bhatti KhH, Siddiqi EH, Talla A. Effect of exogenous applications of GlyBet on growth and gaseous exchange attributes of two maize (Zea mays L.) cultivars under saline conditions. World Appl Scis J. 2014;29(12):1559-65.

Katsuhara M, Otsuka T, Ezaki B. Salt stress-induced lipid peroxidation is reduced by glutathione S-transferase, but this reduction of lipid peroxides is not enough for a recovery of root growth in Arabidopsis. Plant Sci. 2005;169:369-73.

Erdal SC, Cakirlar H. Impact of salt stress on photosystem II efficiency and antioxidant enzyme activities of safflower (Carthamus tinctorius L.) cultivars. Turk J Biol. 2014;38:549-60.

Hala M, El-Bassiouny S, Bekheta MA. Effect of salt stress on relative water content, lipid peroxidation, polyamines, amino acids and ethylene of two Wheat cultivars. J Agric Biol. 2005;3:363-8.

Neumann PM. The role of cell wall adjustment in plant resistance to water deficits. Crop Sci. 2001;35:1258-66.

Yazici I, Türkan I, Sekmen A, Demiral T. Salinity tolerance of Purslane (Portulaca oleracea L.) is achieved by enhanced antioxidant system, lower level of lipid peroxidation and proline accumulation. Environ Exp Bot. 2007;61:49-57.

Gill PK, Sharma AD, Singh P, Bhullar SS. Osmotic stress induced changes in germination, growth and soluble sugar contents of Sorghum bicolor (L.) Moench seeds under various abiotic stresses. Plant Physiol. 2002;128:12-25.

Demiral T, Türkan I. Does exogenous GlyBet affect antioxidative system of rice seedlings under NaCl treatment? J Plant Physiol. 2004;161:1089-100.

Heuer B. Influence of exogenous application of proline and GlyBet on growth of salt-stressed tomato plants. Plant Sci. 2003;165:693-9.

Ibrahim AH, Aldesuquy HS. Induction of increased water stress tolerance in Sorghum bicolor plants by glycine betaine and shikimic acid treatment. Phyton. 2003;43:351-63.

Aldesuquy HS, Abo-Hamed SA, Abbas MA, Elhakem AH. Effect of glycine betaine and salicylic acid on growth and productivity of droughted wheat cultivars. I. Osmolytes in relation to osmotic adjustment and grain yield. J Environ Sci. 2009;37:13-3.

Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol. 2004;55:373-99.

Lee DH, Kim YS, Lee CB. The inductive responses of the antioxidant enzymes by salt stress in rice (Oryza sativa L.). J Plant Physiol. 2001;158:737-45.

Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002;7:405-10.

Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI. Photoinhibition of photosystem II under environmental stress. Biochem Biophys Acta. 2007;1767:414-21.

Hernandez JA, Campillo A, Jimenez A, Alacon JJ, Sevilla F. Response of antioxidant systems and leaf water relations to NaCl stress in pea plants. New Phytol. 1999;141:241-51.

Meneguzzo S, Navari-Izzo F, Izzo R. Antioxidative responses of shoots and roots of wheat to increasing NaCl concentrations. J Plant Physiol. 1999;155:274-80.

Sairam RK, Srivastava GC. Changes in antioxidant activity in subcellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci. 2002;162:897-904.

Kaya C, Sönmez O, Aydemir S, Dikilitas M. Mitigation effects of GlyBet on oxidative stress and some key growth parameters of maize exposed to salt stress. Turk J Agric For. 2013;37:188-94.

Chen THH, Murata N. GlyBet: an effective protectant against abiotic stress in plants. Trends Plant. 2008;13:499-505.

Cuin TA, Shabala S. Exogenously supplied compatible solutes rapidly ameliorate NaCl-induced potassium efflux from barley roots. Plant Cell Physiol. 2005;46:1924-33.

Cuin TA, Shabala S. Amino acids regulates salinity-induced potassium efflux in barley root epidermis. Planta. 2007;225:753-61.

Sobahan MA, Arias CR, Okuma E, Shimoishi Y, Nakamura Y, Hirai Y, Mori IC, Murata Y. Exogenous proline and GlyBet suppress apoplastic flow to reduce Na+ uptake in rice seedlings. Biosci Biotech Bioch. 2009;73:2037-42.

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Published

2017-03-07

How to Cite

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Alasvandyari F, Mahdavi B, Madah Hosseini S. Glycine betaine affects the antioxidant system and ion accumulation and reduces salinity-induced damage in safflower seedlings. Arch Biol Sci [Internet]. 2017Mar.7 [cited 2022Jan.19];69(1):139-47. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/157

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