Physiological and Biochemical Reactions of Some Grape Cultivars and Rootstocks Treated with Sodium Nitroprusside under Salt Stress Conditions

Document Type : Full Paper

Authors

1 Department of Horticultural Sciences, Faculty of Agriculture, University of Tehran, Karaj. Iran

2 Department of Horticultural Sciences, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran

Abstract

In order to investigate the effect of sodium nitroprusside on reducing the negative effect of salinity stress on four grape rootstocks and cultivars, a research was carried out in a factorial based on a completely randomized block design with three replications. Two-year-old rooted cuttings of all four cultivars and rootstocks (Bidaneh Sefid, Yaghouti, 140Ru and 1103P), were subjected to three levels of salinity (salinity in Cramer's nutrient solution) zero, 25 and 50 mM sodium chloride (1.3, 4.50 and 6.80 ds/m) and three levels of sodium nitroprusside (SNP) zero, 0.5 and 1 mM. The results showed that increasing salinity levels, reduced the indices of leaf relative water content and contents of chlorophyll a and b and carotenoid. Furthermore, proline, glycine betaine, soluble sugars, total phenolic, ion leakage, malondialdehyde and hydrogen peroxide increased along with increasing salinity levels. Based on the results, application of SNP, especially at a concentration of 1 mM under salt stress conditions, increased the leaf relative water content, the content of photosynthetic pigments, total phenolic, proline, glycine betaine and soluble sugars, and reduced ion leakage, malondialdehyde and hydrogen peroxide in grape cultivars and rootstocks. Use of SNP caused greater effects on ‘Bidaneh Sefid’ and ‘Yaghouti’ cultivars than the rootstocks. The results showed that ‘Bidaneh Sefid’ cultivar was sensitive to salinity, while 140Ru rootstock was more tolerant to salinity than ‘Bidaneh Sefid’ and ‘Yaghouti’ cultivars, as well as 1103P rootstock.

Keywords

Main Subjects


Extended Abstract

Introduction

 Soil and irrigation water salinity has been regarded as one of the major challenges in most of the Iran vineyards and is one of the most important environmental stresses that severely reduces the quantity and quality of economic products. To cope with this threat, selecting and producing salinity-tolerant cultivars for direct use or as rootstocks for commercial cultivars through various experiments is one of the important solutions that can be useful in the future. Tolerant cultivars and rootstocks that show good efficiency under salinity stress conditions can be used in the establishment of new gardens or as suitable parents in crossbreeding programs and controlled crossings. Other solutions include the use of compounds such as sodium nitroprusside (as a nitric oxide releaser). Nitric oxide is a biologically active molecule that plays a role in regulating many cellular functions in the plant, ranging from root growth to compensatory responses to biotic and abiotic stresses. Therefore, it seems necessary to conduct a research to investigate the mechanism of the sodium nitroprusside (SNP) effect in alleviating the negative effects of salinity stress on the growth and yield of grapes.

 

Materials and Methods

This study was conducted as a factorial in a randomized complete block design with three replications in Karaj, Iran, during 2019-2020. Treatments included four grape cultivars and rootstocks (Bidaneh Sefid, Yaghouti (native cultivars), 140Ru and 1103P), salinity stress at three levels (0, 25 and 50 mM sodium chloride) and SNP spraying at three levels (0, 0.5 and 1 mM). One-year-old rooted cuttings were transferred to 10-liter pots containing cocopeat and perlite (1:3). When plants reached the 10-leaf stage, the salinity treatments (0, 25 and 50 mM sodium chloride) were applied to the pots twice a week along with Cramer's nutrient solution (Cramer et al., 2007) through irrigation water. Simultaneous with salinity treatment, SNP treatment was applied in the form of foliar application at three levels (0, 0.5 and 1 mM SNP as nitric oxide releasing compound) one week before the onset of salinity treatment and again in another two stages with one week interval after the start of salinity treatment. Six weeks after the beginning of salinity treatment, leaves were sampled for measuring physiological and biochemical traits.

 

Results and Discussion

The results of means comparison showed that the amounts of chlorophyll a, b and carotenoid in the leaves decreased under the influence of different salinity levels. According to the obtained results, SNP increased the amounts of chlorophyll a and b and total carotenoid in the studied genotypes of grape under salinity conditions. The amount of ionic leakage of the membrane of leaf cells, at different levels of salinity, was higher in Bidaneh Sefid cultivar than the other evaluated grape genotypes, so that this increase in Bidaneh Sefid cultivar increased from 25.14% (Bidaneh Sefid control) to 80.69% (50 mM sodium chloride). Furthermore, the application of SNP had a good effect on reducing the amount of malondialdehyde at both salinity levels. The effect of 1 mM SNP compared to 0.5 mM concentration had the greatest effect in reducing the amount of malondialdehyde, especially at the salinity level of 50 mM for all evaluated genotypes. The results of this research showed that salinity treatment significantly increased the amount of hydrogen peroxide. In this study, along with the increase of salinity, the amount of free oxygen radicals increased and caused lipid peroxidation of the membrane, which in turn increased the amount of ion leakage and malondialdehyde, which is consistent with the findings of other researchers (Khan et al., 2020; Hasanuzzaman et al., 2020). In this study, the amount of proline increased with the increase of salinity levels, and this increase was higher in the salinity-tolerant genotype, including 140Ru rootstock. In addition, in this study, the simultaneous application of salt stress and SNP increased the proline content of grape leaves compared to the application of salt stress alone. In this study, salinity stress significantly increased the amount of glycine-betaine in grape leaves, which has also been observed in the results of other researchers in Summer Black grape variety (Haider et al., 2019). The effect of SNP use on increasing glycine-betaine amount was more pronounced in 140Ru and 1103P rootstocks and Yaghouti cultivar than Bidaneh Sefid at different salinity levels. Interaction of salinity and SNP resulted in a significant increase in the amount of soluble sugars, so that maximum soluble sugars were observed at high salinity level and one mM SNP. According to the results of this research, SNP and salinity treatments increased the amounts of total phenolic compounds in the evaluated grape genotypes, especially in 140Ru rootstock, which is in line with the results reported by Mohammadkhani and Abbaspour (2017).

 

Conclusion

    According to the obtained results, 140Ru and 1103P rootstocks with the least decrease in photosynthetic pigments and leaf relative water content, and the most increase in the amount of compatible osmolytes and total phenolic, as well as the least increase in the amount of electrolyte leakage, malondialdehyde and hydrogen peroxide, respectively, were more tolerant to salinity. By contrast, Bidaneh Sefid cultivar was sensitive to salinity with the highest increase in the amount of ion leakage, malondialdehyde and hydrogen peroxide, as well as the highest decrease in the amount of photosynthetic pigments and leaf relative water content. Use of SNP at different levels of salinity had the best effect compared to the control treatment. In addition to being affected by different salinity levels, SNP was also influenced by the studied cultivars and rootstocks. So that the effect of 1 mM SNP was more than 0.5 mM at both salinity levels, especially 50 mM. Bidaneh Sefid and Yaghouti cultivars were more affected by SNP concentrations than the rootstocks 140Ru and 1103P.

دولتی‌بانه، حامد (1395). بررسی تغییرپذیری‌های عناصر غذایی، ویژگی‌های رشدی و فیزیولوژیک در چند رقم و دورگه بین‌گونه‌ای انگور در شرایط تنش شوری ناشی از سدیم کلرید. علوم باغبانی ایران، 47(1)، 33-44.‎
طاهری، سحر؛ سعیدیسر، سکینه؛ مسعودیان، ناهید؛ عبادی، مصطفی و رودی، بستان (1399). نقش محافظتی مولکولی و بیوشیمیایی نیتروپروسید سدیم در گوجه فرنگی (Lycopersicon esculentum Mill.) تحت تنش شوری. مجله فیزیولوژی گیاهی، 11(1)، 3465-3472.
طحانیان، حمید. رضا (1397). ارزیابی مکانیسم­های فیزیولوژیکی و مولکولی تحمل برخی پایه­های درون و بین گونه‌ای انگور به شوری و کلروز ناشی از آهک. رساله دکتری، دانشگاه تهران، تهران.
عزیزی، حسین؛ حسنی، عباس؛ صدقیانی، میر حسن؛ عباسپور، ناصر و دولتی بانه، حامد (2017). تأثیر محلول‌پاشی سیلیکات پتاسیم و سولفات روی بر برخی ویژگی‌های فیزیولوژیک دو رقم انگور در شرایط تنش شوری. علوم باغبانی ایران، 47(4)، 797-810.‎
محمدخانی، نیر و عباسپور، ناصر (1397). اثر شوری بر سیستم آنتی­اکسیدانی در ده ژنوتیپ انگور. فیزیولوژی گیاهی، 8(1 )، 2247-2255.
مینازاده، راضیه؛ کریمی، روح الله و محمد پرست، بهروز (1397). اثر تغذیه برگی سولفات‌ پتاسیم بر شاخص‌های مورفو-فیزیولوژیکی انگور تحت تنش ‌شوری . نشریه زیست‌شناسی گیاهی ایران، 10 (3)، 83-106.
یوسفی، مهری؛ ناصری، لطفعلی و زارع نهندی، فریبرز (1398). اثرات نیتریک ‌اکسید با بهبود تحمل شوری در پایه­های گلابی با تنظیم محتوای پلی آمین. مجله فیزیولوژی گیاهی، 10(1)، 3023-3033.
 
REFERENCES
Adnan, M. Y., Hussain, T., Asrar, H., Hamed, A., Gul, B., Nielsen, B., & Khan, M. A. (2016). Desmostachya bipinnata manages photosynthesis and oxidative stress at moderate salinity. Flora, 225, 1–9.
Ahmed, F. F., Abdel-Aal, A. M. K. A., Mervat, A., & Ahmed, S. E. A. (2015). Tolerance of some grapevine cultivars to salinity and calcium carbonate in the soil. Stem Cell, 6, 45-64.
Akcin, A., & Yalcin, E. (2016). Effect of salinity stress on chlorophyll, carotenoid content, and proline in Salicornia prostrata Pall. and Suaeda prostrata Pall. subsp. prostrata (Amaranthaceae). Brazilian Journal of Botany, 39, 101-106.
Alam, H., Khattak, J. Z., Ksiksi, T. S., Saleem, M. H., Fahad, S., Sohail, H., Ali, Q., Zamin, M., El‐Esawi, M. A., Saud, S., & Jiang, X. (2021). Negative impact of long‐term exposure of salinity and drought stress on native Tetraena mandavillei L. Physiologia Plantarum, 172(2), 1336-1351.
Arif, Y., Singh, P., Siddiqui, H., Bajguz, A., & Hayat, S. (2020). Salinity induced physiological and biochemical changes in plants: An omic approach towards salt stress tolerance. Plant Physiology and Biochemistry, 156, 64-77.
Azizi, H., Hassani, A., Sadaghiani, M., Abbaspour, N., & Doulati-Baneh, H. (2017). Effect of foliar application of potassium silicate and zinc sulphate on some physiological parameters of two grapevine cultivars under salt stress conditions. Iranian Journal of Horticultural Science, 47(4), 797-810. (In Persian).
Cramer, G. R., Ergül, A., Grimplet, J., Tillett, R. L., Tattersall, E. A., Bohlman, M. C., Vincent, D., Sonderegger, J., Evans, J., Osborne, C., & Quilici, D. (2007). Water and salinity stress in grapevines: Early and late changes in transcript and metabolite profiles. Functional & Integrative Genomics, 7, 111-134.
Doulati-Baneh, H. (2016). Salinity effects on plant tissue nutritional status as well as growth and physiological factors in some cultivars and interspecies hybrids of grape. Iranian Journal of Horticultural Science, 47(1), 33-44. (In Persian).
Duan, P., Ding, F., Wang, F., & Wang, B. S. (2007). Priming of seeds with nitric oxide donor sodium nitroprusside (SNP) alleviates the inhibition on wheat seed germination by salt stress. Zhi wu Sheng li yu fen zi Sheng wu xue xue bao. Journal of Plant Physiology and Molecular Biology, 33(3), 244-250.
Fàbregas, N., & Fernie, A. R. (2019). The metabolic response to drought. Journal of Experimental Botany, 70(4), 1077-1085.
Fancy, N. N., Bahlmann, A. K., & Loake, G. J. (2017). Nitric oxide function in plant abiotic stress. Plant, Cell & Environment, 40(4), 462-472.
Fozouni, M., Abbaspour, N., & Baneh, H. D. (2012). Short term response of grapevine grown hydroponically to salinity: Mineral composition and growth parameters. Vitis, 51(3), 95-101.
Ghadakchiasl, A., Mozafari, A. A., & Ghaderi, N. (2017). Mitigation by sodium nitroprusside of the effects of salinity on the morpho-physiological and biochemical characteristics of Rubus idaeus under in vitro conditions. Physiology and Molecular Biology of Plants, 23, 73-83.
Gohari, G., Mohammadi, A., Akbari, A., Panahirad, S., Dadpour, M. R., Fotopoulos, V., & Kimura, S. (2020). Titanium dioxide nanoparticles (TiO2 NPs) promote growth and ameliorate salinity stress effects on essential oil profile and biochemical attributes of Dracocephalum moldavica. Scientific Reports, 10(1), 1-14.
Grieve, C. M., & Grattan, S. R. (1983). Rapid assay for determination of water soluble quaternary ammonium compounds. Plant and Soil, 70, 303-307.
Haider, M. S., Jogaiah, S., Pervaiz, T., Yanxue, Z., Khan, N., & Fang, J. (2019). Physiological and transcriptional variations inducing complex adaptive mechanisms in grapevine by salt stress. Environmental and Experimental Botany, 162, 455-467.
Hand, M. J., Taffouo, V. D., Nouck, A. E., Nyemene, K. P., Tonfack, B., Meguekam, T. L., & Youmbi, E. (2017). Effects of salt stress on plant growth, nutrient partitioning, chlorophyll content, leaf relative water content, accumulation of osmolytes and antioxidant compounds in pepper (Capsicum annuum L.) cultivars. Not Bot Horti Agrobot Cluj Napoca, 45, 481–490.
Hao, G. P., Du, X. H., & Shi, R. J. (2007). Exogenous nitric oxide accelerates soluble sugar, proline and secondary metabolite synthesis in Ginkgo biloba under drought stress. Zhi wu Sheng li yu fen zi Sheng wu xue xue bao. Journal of Plant Physiology and Molecular Biology, 33(6), 499-506.
Hasanuzzaman, M., Bhuyan, M. B., Zulfiqar, F., Raza, A., Mohsin, S. M., Mahmud, J. A., Fujita, M., & Fotopoulos, V. (2020). Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator. Antioxidants, 9(8), 681.
Hashmat, S., Shahid, M., Tanwir, K., Abbas, S., Ali, Q., Niazi, N. K., Akram, M. S., Saleem, M. H., & Javed, M. T. (2021). Elucidating distinct oxidative stress management, nutrient acquisition and yield responses of Pisum sativum L. fertigated with diluted and treated wastewater. Agricultural Water Management, 247, 106720.
Heath, R. L., & Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125(1), 189-198.
Hesami, M., Tohidfar, M., Alizadeh, M., & Daneshvar, M. H. (2020). Effects of sodium nitroprusside on callus browning of Ficus religiosa: An important medicinal plant. Journal of Forestry Research, 31, 789-796.
Kamanga, R. M., Echigo, K., Yodoya, K., Mekawy, A. M. M., & Ueda, A. (2020). Salinity acclimation ameliorates salt stress in tomato (Solanum lycopersicum L.) seedlings by triggering a cascade of physiological processes in the leaves. Scientia Horticulturae, 270, 109434.
Khan, I., Raza, M. A., Awan, S. A., Shah, G. A., Rizwan, M., Ali, B., Tariq, R., Hassan, M. J., Alyemeni, M. N., Brestic, M., & Zhang, X. (2020). Amelioration of salt induced toxicity in pearl millet by seed priming with silver nanoparticles (AgNPs): The oxidative damage, antioxidant enzymes and ions uptake are major determinants of salt tolerant capacity. Plant Physiology and Biochemistry, 156, 221-232.
Khanna-Chopra, R., Semwal, V. K., Lakra, N., & Pareek, A. (2019). Proline–A key regulator conferring plant tolerance to salinity and drought. In Hasanuzzaman, M., Fujita, M., Oku, H. & Tofazzal Islam, M. (Eds), Plant tolerance to environmental stress, (pp. 59-80). CRC Press.
Khoshbakht, D., Asghari, M. R., & Haghighi, M. (2018). Effects of foliar applications of nitric oxide and spermidine on chlorophyll fluorescence, photosynthesis and antioxidant enzyme activities of citrus seedlings under salinity stress. Photosynthetica, 56, 1313-1325.
Kim, Y., Mun, B. G., Khan A. L., Waqas, M., Kim, H. H., Shahzad, R., Lmran, M., Yan, B. W., & Lee, L. J. (2018). Regulation of reactive oxygen and nitrogen species by salicylic acid in rice plants under salinity stress conditions. PLoS One, 13 (3), 1–20.
Kumar, K., Manigundan, K., & Amaresan, N. (2017). Influence of salt tolerant Trichoderma spp. on growth of maize (Zea mays) under different salinity conditions. Journal Basic Microbiol, 57, 141–150.
Letey, J., Hoffman, G. J., Hopmans, J. W., Grattan, S., Suarez, D. L., Corwin, D. L., Oster, J. D., Wu, L., & Amrhein, C. (2011). Evaluation of soil salinity leaching requirement guidelines. A Gricultural Water Management, 98 (4), 502-506.
Lichtenthaler, H. K., & Buschmann, C. (2001). Chlorophylls and carotenoids: Measurement and characterization by UV‐VIS spectroscopy. Current Protocols in Food Analytical Chemistry, 1(1), F4-3.
Luttes, S., Kinet, J. M., & Bouharmont, J. (1995). Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. Journal of Experimental Botany, 46,1843-1852.
Minazadeh, R., Karimi, R., & Mohammadparast, B. (2018). The effect of foliar nutrition of potassium sulfate on morpho-physiological indices of grapevine under salinity stress. Iranian Journal of Plant Biology, 10(3), 83-106. (In Persian).
Mohammadkhani, N., & Abbaspour, N. (2017). Effects of salinity on antioxidant system in ten grape genotypes. Iranian Journal of Plant Physiology, 8(1), 2247-2255. (In Persian).
Mohammadkhani, N., Heidari, R., & Abbaspour, N. (2013). Effects of salinity on antioxidant system in four grape (Vitis vinifera L.) genotypes. Vitis, 52(3), 105-110.
Munns, R., & Tester, M. (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology, 59(1), 651-681.
Munns, R., Day, D. A., Fricke, W., Watt, M., Arsova, B., Barkla, B. J., Bose, J., Byrt, C. S., Chen, Z. H., Foster, K. J., & Gilliham, M. (2020). Energy costs of salt tolerance in crop plants. New Phytologist, 225(3), 1072-1090.
Pandey, S., Fartyal, D., Agarwal, A., Shukla, T., James, D., Kaul, T., Negi, Y. K., Arora, S., & Reddy, M. K. (2017). Abiotic stress tolerance in plants: Myriad roles of ascorbate peroxidase. Front, Plant Science, 8, 581.
Paquin, R., & Lechasseur, P. (1979). Observationssur une methode de dosage de la proline libre les extraits de plantes. Canad, Journal  Botany, 57, 1851-1854.
Safdar, H., Amin, A., Shafiq, Y., Ali, A., Yasin, R., Shoukat, A., Hussan, M. U., & Sarwar, M. I. (2019). A review: Impact of salinity on plant growth. Nat Science,17, 34–40.
Sarropoulou, V., & Maloupa, E. (2017). Effect of the NO donor “sodium nitroprusside”(SNP), the ethylene inhibitor “cobalt chloride”(CoCl 2) and the antioxidant vitamin E “α-tocopherol” on in vitro shoot proliferation of Sideritis raeseri Boiss. & Heldr. subsp. raeseri. Plant Cell, Tissue and Organ Culture (PCTOC), 128, 619-629.
Sharma, R., Bhardwaj, R., Thukral, A. K., Al-Huqail, A. A., Siddiqui, M. H., & Ahmad, P. (2019a). Oxidative stress mitigation and initiation of antioxidant and osmoprotectant responses mediated by ascorbic acid in (Brassica juncea L.) subjected to copper (II) stress. Ecotoxicol. Environ. Saf, 182, 109436.
Sharma, A., Shahzad, B., Rehman, A., Bhardwaj, R., Landi, M., & Zheng, B. (2019b). Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules, 24(13), 2452.
Sheligl, H. Q. (1986). Die verwertung orgngischer souren durch chlorella lincht. Planta Journal, 47-51.
Siddiqui, M. H., Alamri, S., Alsubaie, Q. D., Ali, H. M., Khan, M. N., Al-Ghamdi, A., & Alsadon, A. (2020). Exogenous nitric oxide alleviates sulfur deficiency-induced oxidative damage in tomato seedlings. Nitric Oxide, 94, 95–107.
Silva, K. S., Tabaldi, L. A., Rossato, L. V., Cavichioli, B. M., Basilio, V. B., & Machado, S. L. O. (2019). Contents of pigments and activity of antioxidant enzymes in rice plants pre-treated with sodium nitroprusside and exposed to clomazone. Planta Daninha, 37.
Singleton, V. L., & Rossi, J. A. (1965). Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American journal of Enology and Viticulture, 16(3), 144-158.
Sofy, M. R., Elhawat, N., & Alshaal, T. (2020). Glycine betaine counters salinity stress by maintaining high K+/Na+ ratio and antioxidant defense via limiting Na+ uptake in common bean (Phaseolus vulgaris L.). Ecotoxicology and Environmental Safety, 200, 110732.
Sohrabi, S., Ebadi, A., Jalali, S., & Salami, S. A. (2017). Enhanced values of various physiological traits and VvNAC1 gene expression showing better salinity stress tolerance in some grapevine cultivars as well as rootstocks. Scientia Horticulturae, 225, 317-326.
Taheri, S., Saeidisar, S., Masoudian, N., Ebadi, M., & Roudi, B. (2020). Molecular and biochemical protective roles of sodium nitroprusside in tomato (Lycopersicon esculentum Mill.) under salt stress. Iranian Journal of Plant Physiology, 11(1), 3465-3472. (In Persian).
Tahanian, H. R. (2019). Molecular and physiological evaluation on tolerance of some within and between species of grapevine rootstocks to salinity and lime-induced chlorosis. Ph.D. Thesis, University of Tehran, Tehran. (In Persian).
Turner, N. C. (1981). Techniques and experimental approaches for the measurement of plant water status. Plant Soil, 58, 339-366.
Velikova, V., Yordanov, I., & Edreva, A. J. P. S. (2000). Oxidtive stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Science, 151(1), 59-66.
Walker, R. R., Blackmore, D. H., Gong, H., Henderson, S. W., Gilliham, M., & Walker, A. R. (2018). Analysis of the salt exclusion phenotype in rooted leaves of grapevine (Vitis spp.). Australian Journal of Grape and Wine Research, 24, 317–326.
Yousefi, M., Naseri, L., & Zaare-Nahandi, F. (2019). Nitric oxide ameliorates salinity tolerance in Pyrodwarf pear (Pyrus communis) rootstocks by regulating polyamine content. Iranian Journal of Plant Physiology, 10(1), 3023-3033. (In Persian).
Zhang, X., Walker, R. R., Stevens, R. M., & Prior, L. D. (2002). Yield salinity relationships of different grapevine (Vitis vinifera L. ) scion- rootstock combinations. Australian Journal of Grape and Wine Research, 8(3), 150-156.
Zheng, C., Jiang, D., Liu, F., Dai, T., Liu, W., Jing, Q., & Cao, W. (2009). Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environmental and Experimental Botany, 67(1), 222-227.