Responses of Spinacia oleracea L. cv. Matador Plants to Various Abiotic Stresses Such as Cadmium Metal Toxicity, Drought and Salinity

Year 2021, Volume: 35 Issue: 1, 103 - 117, 01.06.2021

Aysegul Akpınar Asuman Cansev Deniz Acun

Abstract

Spinacia oleracea L. cv. Matador plants produced in many regions are exposed to many abiotic
stresses from drought to metal toxicity. In this study, the effects of drought (control: 100% field capacity (FC),
D1: 50% FC and D2: no-watering), salinity (100 and 200 mM NaCl) and cadmium (Cd; 100 and 200 µM CdCl2)
metal toxicity, which are among the most common abiotic stress factors, on spinach plants were determined at the cellular level. There was not determined any alterations along 10 days’ drought, salinity and Cd stress in dry and fresh weights of spinach plants grown in plant growth chamber, in which there is a 16-hour photoperiod under a light intensity of 1200 lux at 24°C/20°C (day/night). However, all treatments caused oxidative stress. Cd treatments were more structurally damaging than drought and salinity treatments. In drought and salinity treatments, chlorophyll content and dry weight did not change despite the increased superoxide dismutase (SOD) and catalase (CAT) activities. The highest values in SOD activity were obtained at D2-drought treatment and 200 mM salinity treatment. SOD activity determined in Cd treatments was also increased compared to control, but this increase was lower than the other treatments. Thus, it can be considered that CAT enzyme is primarily scavenger of reactive oxygen species (ROS) in spinach plants under Cd stress. As a results, spinach plants had an ability to cope with this stresses. The different responses of spinach seedlings to various stress factors provide for estimate of the plant's powerful physiological mechanism. In the continuation of this study, it is recommended to conduct molecular studies and to investigate of the cellular responses to long-term stress on Spinacia oleracea L. cv. Matador plants, which we found to be tolerant to short-term stresses.

Keywords

Spinacia oleracea L. cv. Matador, abiotic stress, antioxidative defence system, drought, salinity, cadmium

Supporting Institution

Bilecik Şeyh Edebali Üniversitesi

Project Number

2019-02.BŞEÜ.11-04

Thanks

Thank to the Scientific Research Projects Council of Bilecik Şeyh Edebali University, Turkey for supporting this study (Project Number 2019-02.BŞEÜ.11-04)

Tuzluluk, Kuraklık, Kadmiyum Metal Toksitesi gibi Çeşitli Abiyotik Streslere Matador Çeşidi Spinacia oleracea L. nın Verdiği Yanıtlar

Abstract

Birçok bölgede üretilen Matador çeşidi Spinacia oleracea L. bitkisi, kuraklıktan metal toksisitesine kadar
birçok abiyotik strese maruz kalmaktadır. Bu çalışmada Matador çeşidi ıspanak bitkilerinde en yaygın abiyotik stres faktörlerinden kuraklık (kontrol: %100 tarla kapasitesi, D1: %50 tarla kapasitesi ve D2: tam kuraklık koşulları), tuzluluk (100 ve 200 mM NaCl) ve kadmiyum (Cd; 100 ve 200 µΜ CdCl2) metal toksisitesinin hücresel düzeyde etkileri belirlenmiştir. Elde edilen sonuçlarda 10 günlük kuraklık, tuzluluk ve Cd stresi boyunca 24°C/20°C'de (gündüz/gece) 1200 lüks ışık yoğunluğu altında 16 saatlik fotoperiyodun bulunduğu bitki büyüme odasında yetiştirilen Matador çeşidi ıspanak bitkilerinin kuru ve yaş ağırlıklarında herhangi bir değişiklik tespit edilmemiştir. Bununla birlikte, tüm stres uygulamaları oksidatif strese neden olmuştur. Cd uygulamalarının, ıspanak bitkilerinde kuraklık ve tuzluluk uygulamalarına göre yapısal olarak daha zarar verici olduğu tespit edilmiştir. Kuraklık ve tuzluluk uygulamalarında, klorofil içeriği ve kuru ağırlık, artan süperoksit dismütaz (SOD) ve katalaz (CAT) aktivitesine rağmen değişmemiştir. SOD aktivitesinde en yüksek değerler, D2-kuraklık uygulamasında ve 200 mM konsantrasyonunda tuzluluk uygulamasında elde edilmiştir. Cd uygulamalarında belirlenen SOD aktivitesi de kontrole göre artmıştır ancak bu artış, diğer uygulamalardan daha düşüktür. Bu nedenle, Matador çeşidi ıspanak bitkilerinde Cd stresi altında CAT enziminin esas olarak reaktif oksijen türleri (ROS) nin temizleyicisi olduğu düşünülebilir. Sonuç olarak, Matador çeşidi ıspanak bitkilerinin bu streslerle başa çıkma yeteneği vardır. Çeşitli stres faktörlerine ıspanak fidelerinin verdiği farklı yanıtlar, bitkinin güçlü fizyolojik mekanizmasının tahminini sağlar. Bu çalışmanın devamında, kısa süreli streslere toleranslı olduğunu tespit ettiğimiz Matador çeşidi Spinacia oleracea L. üzerinde moleküler çalışmaların yapılması ve uzun vadeli strese hücresel tepkilerin araştırılması önerilmektedir.

Keywords

Spinacia oleracea L. cv. Matador, abiyotik stres, antioksidatif savunma sistemi, kuraklık, tuzluluk, kadmiyum

Project Number

2019-02.BŞEÜ.11-04

References

• Ahmad, Z., Ahmad Waraich, E., Akhtar, S., Anjum, S., Ahmad, T., Mahboob, W., Hafeez, O.A., Tapera, T., Labuschagne, M. and Rizwan, M. 2018. Physiological responses of wheat to drought stress and its mitigation approaches. Acta Physiologiae Plantarum 40:80.
• Alia, N., Sardar, K., Said, M., Salam, K. Sadia, A., Sadaf, S., Toqeer, A. and Miklas, S. 2015. Toxicity and Bioaccumulation of Heavy Metals in Spinach (Spinacia oleracea) Grown in a Controlled Environment. Int. J. Environ. Res. Public Health. 12: 7400-7416.
• Anjum, N.A., Umar, S., Iqbal, M. and Khan, N.A. 2011. Cadmium causes oxidative stress in mung bean by affecting the antioxidant enzyme system and ascorbate-glutathione cycle metabolism. Russ J Plant Physiol. 58(1): 92-99.
• Ardıç, M., Sekmen, A.H., Türkan, I., Tokur, S. and Ozdemir, F., 2009. The Effects of Boron Toxicity on Root Antioxidant Systems of Two Chickpea (Cicer arietinum L.) Cultivars. Plant Soil, 314: 99-108.
• Arefian, M. and Shafaroudi, S.M. 2015. Physiological and gene expression analysis of extreme chickpea (Cicer arietinum L.) genotypes in response to salinity stress. Acta Physiologia Plantarum 37: 193.
• Arora, R., Pitchay, D.S. and Bearce, B.C. 1998. Water‐stress‐induced heat tolerance in geranium leaf tissues: A possible linkage through stress proteins? Physiologia Plantarum 103 (1): 24-34.
• Arslan, H., Güleryüz, G., Akpınar, A., Kırmızı, S., Seven Erdemir, Ü. and Güçer, Ş. 2014. Responses of Ruderal Verbascum olympicum Boiss. (Scrophulariaceae) Growing under Cadmium Stress. CLEAN – Soil, Air, Water 42(6): 824-835.
• Atafar, Z., Mesdaghinia, A., Nouri, J., Homaee, M., Yunesian, M., Ahmadimoghaddam, M. and Hossein Mahvi, A. 2010. Effect of fertilizer application on soil heavy metal concentration. Environ. Monit. Assess. 160: 83- 89.
• Bagheri, R., Bashir, H., Ahmad, J., Baig, A. and Qureshi, M.I. 2013. Effect of cadmium on leaf proteome of Spinacia oleracea (spinach). Int J. Agric Food Sci. Technol. 4:33-36.
• Bagheri, R., Ahmad, J., Bashir, H., Iqbal, M. and Qureshi, M.I. 2017. Changes in rubisco, cysteine-rich proteins and antioxidant system of spinach (Spinacia oleracea L.) due to sulphur deficiency, cadmium stress and their combination. Protoplasma, 254: 1031-1043.
• Bandurska, H. and Jozwiak, W. 2010. A comparison of the effects of drought on proline accumulation and peroxidases activity in leaves of Festuca rubral L. and Lolium perenne L. Dept. Plant Physiol. 2: 111-116.
• Bartels, D. and Sunkar, R. 2005. Drought and Salt Tolerance in Plants. Critical Reviews in Plant Sciences, 24:23-58.
• Bayram Erdoğan, S. 2018. Su Stresi ve Bitkilerde Su Stresine Bağlı Fizyolojik Değişimler. Tralleis Elektronik Dergisi 3(2): 219-228.
• Belmecheri-Cherifi, H., Albacete, A., Martínez-Andújar, C., Pérez-Alfocea, F. and Abrous-Belbachir, O. 2019. The growth impairment of salinized fenugreek (Trigonella foenum-graecum L.) plants is associated to changes in the hormonal balance. Journal of Plant Physiology 232: 311-319.
• Bender Özenç, D. and Şenlikoğlu, G. 2017. Kompost ve azotlu gübre uygulamasının ıspanak bitkisinin (Spinacia oleracea L.) gelişimi üzerine etkileri. Akademik Ziraat Dergisi Cilt:6 Özel Sayı: 227-234.
• Beuchamp, C. and Fridovich, I. 1971. Superoxide dismutase; improved assays and an assay applicable to acrylamide gels, Anal. Biochem. 44: 276-287.
• Blokhina, O., Virolainen, E. and Fagerstedt, K.V. 2003. Antioxidants, Oxidative Damage and Oxygen Deprivation Stress: a Review. Annals of Botany 91: 179-194.
• Boojar, M.M.A. and Goodarzi, F. 2007. The copper tolerance strategies and the role of antioxidative enzymes in three plant species grown on copper mine. Chemosphere 67(11): 2138-47.
• Dhongade, S. and Nandkar, P.B. 2011. The phytotoxicity of heavy metals on growth and metal uptake by spinach. Agr. Biol. Res. 27: 78–90.
• Dixit, V., Pandey, V. and Shyam, R. 2001. Differential oxidative responses to cadmium in roots and leaves of pea (Pisum sativum L cv. Azad). J. Exp. Bot. 52:1101-1109.
• Du, S.T., Liu, Y., Zhang, P., Liu, H.J., Zhang, X.Q. and Zhang, R.R. 2015. Atmospheric application of trace amounts of nitric oxide enhances tolerance to salt stress and improves nutritional quality in spinach (Spinacia oleracea L.). Food Chemistry 173: 905-911.
• FAO. 2018. Food and Agriculture Organization of the United Nations, Rome, Italy.
• Farooq, M., Wahid, A., Kobayashi, N., Fujita, D. and Basra, S.M.A. 2009. Plant drought stress: effects, mechanisms and management. Agronomy for Sustain. Dev. 29: 185-212.
• Gulen, H. and Eris, A. 2003. Some Physiological Changes in Strawberry (Fragaria × ananassa cv. camarosa) Plants Under Heat Stress. J. Hort. Sci. Biotech. 78: 894-898.
• Hina, K., Kanwal, S.S., Arshad, M. and Gul, I. 2019. Effect of Cadmium (Cd) Stress on Spinach (Spinacea oleracea) and Its Retention Kinetics in Soil in Response to Organic Amendments. Pak. J. Agri. Sci. Vol. 56(1): 179-185.
• Hossain, M.A., Piyatida, P., Teixeira da Silva, J.A. and Fujita, M. 2012. Molecular Mechanism of Heavy Metal Toxicity and Tolerance in Plants: Central Role of Glutathione in Detoxification of Reactive Oxygen Species and Methylglyoxal and in Heavy Metal Chelation. Journal of Botany, http://dx.doi.org/10.1155/2012/872875, sf. 37.
• Jaleel se, C.A., Manivannan, P., Wahid, A., Farooq, M., Somasundaram, R. and Panneerselvam, R. 2009. Drought stress in plants: a review on morphological characteristics and pigments composition. International Journal of Agriculture and Biology 11 (1): 100-105.
• Kaya, C., Higgs, D. and Kırnak, H. 2001. The Effects of High Salinity (NaCl) and Supplementary Phosphorus and Potassium on Physiology and Nutrition Development of Spinach. Bulg. J. Plant Physiol. 27(3–4): 47-59.
• Khan, N.A. and Singh, S. (Eds.) 2008. Abiotic Stress and Plant Responses. IK International Publishing House Pvt. Ltd., New Delhi, pp. 1-299.
• Khan, M.U., Malik, R.N., Muhammad, S., Ullah, F. and Qadir, A. 2015. Health risk assessment of consumption of heavy metals in market food crops from Sialkot and Gujranwala districts, Pakistan. Human Ecol Risk Assess: An Int Journal, 21: 327-337.
• Karapınar, H.S. and Kılıçel, F. 2020. Determination of Some Toxic Element (Cr, Cd, Cu and Pb) Levels in Cumin and Cinnamon Aromatic Plants Frequently Used as Foodstuff. Bursa Uludag Üniv. Ziraat Fak. Derg. 34(Özel Sayı/Special Issue), s.1-8.
• Khorasaninejad, S., Mousavi, A., Soltanloo, H., Hemmati, K. and Khalighi, A. 2011. The effect of drought stress on growth parameters, essential oil yield and constituent of Peppermint (Mentha piperita L.). Journal of Medicinal Plants Research 5(22): 5360-5365.
• Lester, C., Moller, N. and Hammerum, A. 2004. Conjugal Transfer of Aminoglycoside and Macrolide Resistance between Enterococcus faecium Isolates in The Intestine of Streptomycin-Treated Mice. Feems Microbiol. Lett, 235: 385-391.
• Liang, W., Ma, X., Wan, P. and Liu, L. 2018. Plant salt-tolerance mechanism: a review. Biochemical and Biophysical Research Communications 495(1): 286-291.
• Liu, L., Zhang, X. and Zhong, T. 2015. Pollution and health risk assessment of heavy metals in urban soil in China. Human Ecol Risk Assess: An Int J. doi:10.1080/10807039.2015.1078226.
• Lombardi, L.L. and Sebastiani, L. 2005. Copper toxicity in Prunus cerasifera: Growth and antioxidant enzymes responses of in vitro grown plants. Plant Science 168: 797-802.
• Mahajan, S. and Tuteja, N. 2005. Cold, salinity and drought stress: an overview. Arch Biochem Biophys 444: 139-158.
• Minhas, P., Rane, J. and Pasala, R.K. 2017. Abiotic Stresses in Agriculture: An Overview. Abiotic Stress Management for Resilient Agriculture Book, pp. 3-8.
• Mishra, S., Srivastava, S., Tripathi, R.D., Govindarajan, R., Kuriakose, S.V. and Prasad, M.N.V. 2006. Phytochelatin Syhthesis and Response of Antioxidants During Cadmium Stres in Bacopa monnieri L. Plant Physiology and Biochemistry 44: 25-37.
• Mohan, B.S. and Hosetti, B.B. 2006. Phytotoxicity of cadmium on the physiological dynamics of Salvinia natans L. grown in macrophyte ponds. Journal of Environmental Biology 27(4): 701-704.
• Nezhadahmadi, A., Hossain Prodhan, Z. and Faruq, G. 2013. Drought Tolerance in Wheat. Hindawi Publishing Corporation The Scientific World Journal Volume 2013, Article ID 610721, 12 pages http://dx.doi.org/10.1155/2013/610721.
• Noctor, G., Mhamdi, A. and Foyer, C.H. 2014. The Roles of Reactive Oxygen Metabolism in Drought: Not So Cut and Dried. Plant Physiology 164: 1636-1648.
• Osakabe, Y., Osakabe, K., Shinozaki, K. and Tran, L.S.P. 2014. Response of plants to water stress. Front. Plant Sci. 5, 86. https://doi.org/10.3389/fpls.2014.00086.
• Petropoulos, S.A., Daferera, D., Polissiou, M.G. and Passam, H.C. 2008. The effect ofwater deficit stress on the growth, yield and composition of essential oils ofparsley. Sci. Hortic. 115: 393-397.
• Pinto, F.R., Mourato, M.P., Sales, J.R., Moreira, I.N. and Martins, L.L. 2017. Oxidative stress response in spinach plants induced by cadmium. Journal of Plant Nutrition 40(2): 268-276.
• Rahdari, P., Hosseini, S.M. and Tavakoli, S. 2012. The studying effect of drought stress on germination, proline, sugar, lipid, protein and chlorophyll content in purslane (Portulaca oleracea L.) leaves. Journal of Medicinal Plants Research 6(9): 1539-1547.
• Rezakhani, L., Golchin, A. and Samavat, S. 2013. Effect of different rates of Cd on growth and chemical composition of spinach. Int Res J Appl Basic Sci. 7: 1136-1140.
• Roberts, T.L. 2014. Cadmium and Phosphorous Fertilizers: The Issues and the Science. Procedia Engineering “SYMPHOS 2013”, 2nd International Symposium on Innovation and Technology in the Phosphate Industry, 83: 52-59.
• Schützendübel, A., Nikolova, P., Rudolf, C. and Polle, A. 2002. Cadmium and H2O2-induced oxidative stress in Populus canescens roots, Plant Physiol. Biochem. 40: 577-584.
• Sertkaya, G. 2015. Investigation of some viruses in lettuce and spinach fields in Hatay province of Turkey. Ziraat Fakültesi Dergisi 20(1): 7-12.
• Seven, S. and Sağlam, S. 2020. Investigation on the relationship between salinity stress and epibrassinolide in spinach (Spinacia oleracea L. cv. Matador) seedlings. Cumhuriyet Science Journal 41(1): 131-138.
• Taiz, L. and Zeiger, E. 2002. Plant Physiology. 3rd Ed. Sinauer Publishers Inc. Massachusetts.
• Tuteja, N. 2007. Mechanisms of high salinity tolerance in plants. Meth Enzymol. 428: 419-438.
• Upadhyay, R.K. and Panda, S.K. 2009. Copper-induced growth inhibition, oxidative stress and ultrastructural alterations in freshly grown water lettuce (Pistia stratiotes L.). C. R. Biologies 332: 623-632.
• Xu, C. and Leskovar, D.I. 2015. Effects of A. nodosum seaweed extracts on spinach growth, physiology and nutrition value under drought stress. Sci. Hort. 183: 39-47.
• Verma, P., George, K.V., Singh, H.V. and Singh, R.N. 2007. Modeling cadmium accumulation in radish, carrot, spinach and cabbage. Appl Mathem Mod. 31: 1652-1661.
• Wang, J., Li, W., Zhang, C. and Ke, S. 2010. Physiological Responses and Detoxific Mechanisms to Pb, Zn, Cu and Cd in Young Seedling of Paulownia fortunei. Journal of Environmental Sciences 22(12): 1916-1922.
• Yurtyeri, T., Cemek, B. and Ünlükara, A. 2014. Response of Spinach to Different Water Stress Conditions in Greenhouse Indoor and Outdoor Conditions. 12.Culture technique Symposium, 21–23 May, Tekirdağ, Turkey, pp. 331-336.
• Younis, U., Malik, S.A., Rizwan, M., Farooq Qayyum, M., Ok, Y.S., Raza Shah, M.H., Rehman, R.A. and Ahmad, N. 2016. Biochar enhances the cadmium tolerance in spinach (Spinacia oleracea) through modification of Cd uptake and physiological and biochemical attributes. Environ Sci Pollut Res. 23:21385- 21394.
• Zaeifizade, M. and Goliov, R. 2009. The Effect of the Interaction between Genotypes and Drought Stress on the Superoxide Dismutase and Chlorophyll Content in Durum Wheat Landraces. Turk. J. Boil. 33: 1-7.