Antioxidant and Biochemical Alterations in Sea Beet (Beta vulgaris subsp. maritime (L.) Arcang.) and Sugar Beet (Beta vulgaris L.) Exposed to Salt Stress

Document Type : Original Research

Authors
Department of Agronomy and Plant Breeding, Ilam Branch, Islamic Azad University, Ilam, Islamic Republic of Iran.
Abstract
A pot experiment was conducted using a randomized complete block design with a factorial arrangement and 3 replications. The treatments consisted of genotype (15 sea beet genotypes and two cultivated beets of one susceptible and one tolerant to stress), and salinity (four NaCl concentrations including 0, 50, 100, 200 and 400 mM) on the 35-days-old beet seedlings for 55 days. The following parameters and traits were recorded: activities of superoxide dismutase, catalase and glutathione peroxidase, malone dialdehyde, di-tyrosine, di-hydroxy guanosine, proline, and total soluble sugars. The results showed a highly significant effect of salinity treatments on the traits studied. Moreover, with increasing stress intensity, the effects of salinity on these traits increased. At least five genotypes of sea beet were clearly superior than the cultivated beet for producing a lower constitutive level of MDA, DT and 8-OH-dG destruction biomarkers, but higher activities of SOD, CAT and GPX enzymes, and proline, total soluble sugars, and glycine betaine contents were recorded under salt stress conditions. These results strongly suggest that the wild salt-tolerant sea beet possess distinct advantages over the sugar beet counterparts for protection mechanism against oxidative damage by maintaining a higher inherited and induced activity of enzymatic/ non-enzymatic antioxidant activities. Therefore, it can be concluded that under salt stress, sea beet has a significant potential for the physiological/biochemical variation in salinity tolerance, which can be exploited for improving salinity tolerance in sugar beet cultivars.

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Abbas, F.T., Mohanna, A., Al-Lahham, Gh. and Al-Jbawi, E. 2012. Osmotic adjustment in sugar beet plant under salinity stress. J. Sugar Beet. 28: 37-43.
Abd Elgawad, H., Zinta, G., Hegab, M.M., Pandey, R., Asard, H. and Abuelsoud, W. 2016. High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. Front Plant Science. 7: 1-11.
Agarwal, S. and Pandey, V., 2004. Antioxidant enzyme responses to NaCl stress in Cassia angustifolia. Biologia Plantarum. 48, 555–560.
Amirjani, M.R. 2011. Effect of salinity stress on growth, Sugar content, pigments and enzyme activity of rice. International journal of botany. 7: 73-81.
Anjorin, F.B., Adejumo, S.A., Agboola, L. and Samuel, Y.D. 2016. Proline, soluble sugar, leaf starch and relative water contents of four maize varieties in response to different. Cercetări Agronomice în Moldova. 3: 51-62.
Armion, M. 2001. The study of biochemical markers in wild beet (Beta maritima) and sugar beet (Beta vulgaris) under salt stress. M.Sc. thesis. Shiraz University.
Ashraf, M. and Foolad, M.R. 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany. 59: 206-216.
Ashrafi, E., Razmjoo, J. and Zahedi, M. 2012. The effect of salt stress on biochemical traits and relation with salt tolerant of alfalfa cultivars in field. Agronomy Journal. 108: 43-56.
Bates, I.S., Waldern, R.P. and Tear, I.D. 1973. Rapid determination of free proline for water stress studies. Journal of Plant and Soil. 39: 205-207.
Biancardi, E., Campbell, L.G., Skaracis, G.N. and de Biaggi, M., 2005. Genetics and breeding of sugar beet. Science Publishers. USA.
Biancardi, E., Panella, L.W. and Lewellen, R.T., 2012. Beta maritima, the origin of Beets. Springer.
Bogdanov, M.B., Flint Beal, M., McCabe, D.R., Griffin, R.M. and Matson, W.R., 1999. A carbon column-based liquid chromatography Electrochemical Approach to Routine 8-Hydroxy-2-Deoxyguanosine measurements in urine and other biologic matrices: A One-Year Evaluation of Methods. Free Radical Biology & Medicine. 27: 647-666.
Bohnert, H.J. and Jensen, R.G., 1996. Strategies for engineering water stress tolerance in plants. Trends Biotechnology. 14, 89–97.
Bor, M., Ozdemir, F. and Turkan, I., 2003. The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Science. 164, 77-84.
Caverzan, A., Casassola, A. and Brammer, S.P. 2016. Antioxidant responses of wheat plants under stress. Genet. Mol. Biol. 39: 1-6.
Chaum, S. and Kirdmanee, C. 2009. Effect of salt stress on proline accumulation, photosynthetic ability and growth characters in two maize cultivars. Pak. J. Bot. 41: 87-98.
Chen, Q., Zhang, M. and Shen, S. 2010. Effect of salt on malondialdehyde and antioxidant enzymes in seedling roots of Jerusalem artichoke (Helianthus tuberosus L.). Acta Physiologiae Plantarum, 33( 2): 273–278.
Clover, G.R.G., Smith, H. and Jaggard, K., 1998. The crop under stress. British sugar beet review. 66, 17-19.
Dhindsa, R.S., Plumb-Dhindsa, P. and Thorpe, T.A. 1981. Leaf senescence correlated with increased levels of membrane permeability, lipid peroxidation and decreased levels of superoxide dismutase and catalase. J. Exp. Bot. 32 93-101.
Dizdaroglu, M. 1993. Chemistry of free radical damage to DNA and nucleoproteins. in DNA and Free Radicals, Halliwell, B. and Aruoma, O.I. Eds., pp. 19–39, Ellis Horwood, London, UK.
Di Martino, C., Delfine, S., Pizzuto, R., Loreto, F. and Fuggi, A. 2003. Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytologist. 158: 455-463.
Francis, S.A, 2007. Development of sugar beet. Hoboken, N.J.: Blackwell Publishing Ltd.
Fridovic, I. 1986. Biological effects of the superoxide radical, Arch. Biochem. Biophys. 247: 1-11.
Gharsallah, C., Fakhfakh, H., Grubb, D. and Gorsane, F. 2016. Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AOB plants. 8: 1-21.
Gorham, J. 1995. Betaines in higher plants biosynthesis and role in stress metabolism. In: Amino Acids and Their Derivatives in Higher Plants. Cambridge University Press. Cambridge. pp 171-203.
Grattan, S.R., Grieve, C.M., 1992. Mineral element acquisition and growth response of plants grown in saline environments. Agriculture Ecological Environment. 38: 275-300.
Gzik, A., 1996. Accumulation of proline and pattern of α-amino acids in sugar beet plants in response to osmotic, water and salt stress. Environmental and Experimental Botany. 36: 29-38.
Habibollahi, N., Mahdiyeh, M. and Amirjani, M.R. 2012. Effect of salt stress on growth, proline, antioxidant enzyme activity and photosystem II efficiency in salt-sensitive and -tolerant rice cultivars. Journal of Plant Biology. 4: 85-96.
Halliwell, B. and Gutteridge, J.M.C. 1999. Free Radicals in Biology and Medicine. Oxford University Press, Oxford, UK, 3rd edition.
Hernandez, J.A. Del Rio, L.A. and Sevilla, F. 1994. Salt stress induced changes in superoxide dismutase isoenzymes in leaves and mesophyll protoplast from Vigna anguiculatea L. Walp. New Phytol. 126: 37-42.
Hopkins, W.G. and Huner, N.P.A. 2009. Introduction to Plant Physiology. Wiley.
Imlay, J.A. and Linn, S. 1988. DNA damage and oxygen radical toxicity. Science. 240 (4857): 1302–1309.
Islam, M. M., Hoque, M. A., Okuma, E., Banu, M. N. A., Shimoishi, Y., Nakamura, Y. and Murata, Y. 2009. Exogenous proline and glycine betaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. Journal Plant Physiology. 166: 1587-1597.
Jenks, M.A. and Hasegawa, P.M. 2014. Plant abiotic stress. John Wiley & Sons.
Liu, T., Van Staden, J. and Cress, W.A. 2000. Salinity induced nuclear and DNA degradation in meristematic cells of soybean (Glycine max (L.)) roots. Plant Growth Regulation. 30 (1): 49–54.
Madhava, K.V. and Sresty, T.V.S. 2000. Antioxidative parameters in the seedlings of pigeon pea in response to Zn and Ni stresses. Plant Science. 157: 113-128.
Maheshwari, R. and Dubey, R.S. 2009. Nickel-induced oxidative stress and the role of antioxidant defense in rice seedlings. Plant Growth Regulation. 59 (1): 37–49.
Meriga, B., Reddy, B.K., Rao, K.R., Reddy, L.A. and Kishor, P.B.K. 2004. Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). Journal of Plant Physiology. 161 (1): 63–68.
Mittal, R. and Dubey, R.S. 1991. Behaviour of peroxidases in rice: changes in enzymatic activity and isoforms in relation to salt tolerance. Plant Physiology and Biochemistry. 29: (1) 31–40.
Mohammadkhani, N. and Heidari, R. 2008. Drought-induced accumulation of soluble sugars and proline in two maize varieties. World applied sciences journal. 3: 448-453.
Moharramnejad, S. and Valizadeh, M. 2015. Variation of pigment content and antioxidant enzyme activities in pinto bean (Phaseolus vulgaris L.) seedlings under salt stress. Journal of Crop Ecophysiology. 9: 153-166.
Mosaddek Ahmed, I., Cao, F., Zhang, M., Chen, X., Zhang, G. and Wu, F. 2013. Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys. PLOS One. 8: 1-14.
Movafegh, S., Razeghi Jadid, R. and Kiabi, S. 2012. Effect of salinity stress on chlorophyll content, proline, water-soluble carbohydrate, germination, growth and dry weight of three seedling barley (Hordeum vulgare L.) cultivars. Journal of Stress Physiology and Biochemistry. 8: 157-168.
Nemati, I., Moradi, F., Gholizadeh, S., Esmaeili, M.A. and Bihamta, M.R. 2011. The effect of salinity stress on ions and soluble sugars distribution in leaves, leaf sheaths, and roots of rice (Oryza sativa L.) seedlings. Plant, soil and environment. 57: 26-33.
Noctor, G. and Foyer, C.H. 1998. Ascorbate and glutathione: keeping active oxygen under control, Annual Review of Plant Biology. 49: 249–279.
Orhanl, H., Vermeulen, N.P.E., Tump, C., Zappey, H. and Meerman, J.H.N. 2004. Simultaneous determination of tyrosine, phenylalanine and deoxyguanosine oxidation products by liquid chromatography-tandem mass spectrometry as non- invasive biomarkers for oxidative damage. J. Chromato. B. 799: 245-254.
Paglia, D.E. and Valentine, W.N. 1997. Studies on the qualitative characterization of glutathione peroxidase. J. Lab. Med. 70: 158-168.
Pareek, A., Sopory, S.K., Bohnert, H.J. and Govindjee, A., 2010. Abiotic stress adaptation in plants: physiological, molecular and genomic foundation. Springer.
Pessarakli, M., 2010. Handbook of plant and crop stress. CRC Press.
Poustini, K., Siosemardeh, A. and Ranjbar, M. 2007. Proline accumulation as a response to salt stress in 30 wheat (Triticum aestivum L.) cultivars differing in salt tolerance. Genetic Resources and Crop Evolution. 54: 925-934.
Qayyum, A., Razzaq, A., Ahmad, M. and Jenks, M.A. 2011. Water stress causes differential effects on germination indices, total soluble sugar and proline content in wheat (Triticum aestivum L.) genotypes. African Journal of Biotechnology. 10: 14038-114045.
Rao, A., Ahmad, S.D., Sabir, S.M., Awan, S., Shah, A.H., Khan, M.F., Khan, S.A., Shafique, S., Arif, S., Abbas, S.R. and Gohar, M. 2013. Antioxidant activity and lipid peroxidation of selected wheat cultivars under salt stress. Journal of Medicinal Plants Research. 7: 155-164.
Sairam, R.K., Rao, K.V. and Srivastava, G.C. 2002. Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Science. 163, 1037-1046.
Shabala, S. 2012. Plant stress physiology. CABI Publishing.
Shah, K., Kumar, R.G., Verma, S. and Dubey, R.S. 2001. Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Science. 161(6): 1135–1144.
Sharma, P. and Dubey, R.S. 2005. Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regulation. 46 (3): 209–221.
Shlegil, H.G. 1986. Die verwertung organgischer souren durch chlorella lhncht. Journal of Plant Sciences. 41: 47-51.
Sayfzadeh, S. and Rashidi, M. 2011. Response of antioxidant enzymes activities of Sugar beet to drought stress. ARPN Journal of Agricultural and Biological Science. 6: 27-33.
Srivastava, S. and Dubey, R.S. 2011. Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regulation. 1–16.
Taiz, L. and Zeiger, E. 2018. Plant physiology. Sinauer Associates, Sunderland.
Tohidi-Moghadam, H.R., Shirani-Rad, A.H., Nour-Mohammadi, G., Habibi, D., Mashhadi-Akbar-Boojar, M. 2009. Effect of superabsorbent application on antioxidant enzyme activities in canola (Brassica napus L.) cultivars under water stress conditions. American Journal of Agricultural and Biological Sciences. 4: 215-223.
Tsuboi, H., Kouda, K., Takeuchi, H., et al., 1998. 8-Hydroxydeoxyguanosine in urine as an index of oxidative damage to DNA in the evaluation of atopic dermatitis. British Journal of Dermatology. 138(6): 1033–1035.
Tuteja, N. and Singh, G.S. 2012. Plant acclimation to environmental stress‌. Springer.
von Boguslawski, E. 1984. Zur Geschichte der Beta-Rübe als Kulturpfl anze bis zum Beginn des 19. Jahrhundert. Institut für Zuckerrübenforschung, Göttingen, Berlin, Germany.
Wang, Y., Stevanato, P., Yu, L., Zhao, H., Sun, X., Sun, F., Li, J. and Geng, G., 2017. The physiological and metabolic changes in sugar beet seedlings under different levels of salt stress. Journal of plant research. 28: 10-26.
Wu, G.Q., Feng, R.J. and Shui, Q.Z., 2016. Effect of osmotic stress on growth and osmolytes accumulation in sugar beet (Beta vulgaris L.) plants. Plant Soil Environ. 62: 189-194.
Yamauchi, Y., Furutera, A., Seki, K., Toyoda, Y., Tanaka, K. and Sugimoto, Y. 2008. Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants. Plant Physiology and Biochemistry. 46 (8-9): 786–793.
Yancey, P.H., Clark, M.E., Hand, S.C., Bowlus, R.D. and Somero, G.N., 1982. Living with water stress: Evolution of osmolyte systems. Science. 217: 1214-1223.
Yang, W.J., Rich, P.J., Axtell, J.D., Wood, K.V., Bonham, C.C., Ejeta, G., Mickelbart, M.V. and Rhodes, D. 2003. Genotypic variation for glycine betaine in sorghum. Crop Science. 43: 162-169.
Zaefyzadeh, M., Quliyev, R.A., Babayeva, S.M. and Abbasov, M.A. 2009. The effect of the interaction between genotypes and drought stress on the superoxide dismutase and chlorophyll content in durum wheat landraces. Turkish Journal of Biology. 33(1): 1–7.