Document Type : Original Article

Authors

1 Ph.D. Student Department of Agrotechnology, Faculty of Agriculture, Ferdowsi University of Mashhad, Iran

2 Assistant Professor Department of Agrotechnology, Faculty of Agriculture, Ferdowsi University of Mashhad, Iran

3 Professor, Department of Agrotechnology, Faculty of Agriculture, Ferdowsi University of Mashhad, Iran

Abstract

Introduction
The growth of chickpea plants is severely affected by salt stress, leading to a significant reduction in their performance. Therefore, identifying salt-tolerant genotypes of chickpea can greatly help improve plant resilience and enhance productivity under stressful conditions.
Materials and methods
This research was conducted with the aim of studying the salt tolerance of Kabuli chickpea genotypes under field conditions in 2021-2022. Salt stress was applied at two levels: 6 and 9 dS.m-1, along with a control level of 0.5 dS.m-1. The genotypes were evaluated based on their response to these salt stress levels. The irrigation treatments were applied uniformly and complementarily in three stages for 12 genotypes: before flowering, during flowering, and pod filling. Sodium chloride was used to induce salt stress levels. The volume of irrigation water given to each plot was measured using a water counter, and the same amount of water was considered for all treatments.
Results and discussion
The investigation demonstrated changes in the levels of secondary metabolites and leaf chlorophyll content under salt stress conditions, depending on the plant genotype. In genotypes MCC52, MCC65, MCC77, and MCC92, salt stress reduced the content of plant pigments. The reduction in chlorophyll content in plants under the influence of salt stress is associated with an increase in the activity of chlorophyll-degrading enzymes, alterations in nitrogen metabolism, and the utilization of glutamate due to its involvement in the proline synthesis pathway. Increased scavenging activity of the free radical DPPH was observed in genotypes MCC12, MCC27, MCC28, MCC72, MCC92, and MCC108 under salt stress of 9 dS.m-1. The activity of the enzyme catalase increased in most studied genotypes under 6 dS.m-1 salt stress, but decreased with the increase in stress level to 9 dS.m-1. The highest activity of the enzyme ascorbate peroxidase was observed in genotype MCC29 under 6 dS.m-1 salt stress. The decrease in the osmotic potential in plants is a consequence of cellular water conservation under stress conditions. This is because, under salt stress, the plant needs to maintain a more negative water potential in order to absorb water. Therefore, there is a greater need to increase the concentration of compatible osmolytes. Plants with higher antioxidant capacity demonstrate better resistance to oxidative stress due to their ability to detoxify free radicals. The application of salt stress at a level of 9 dS.m-1 led to a significant increase in sodium content in all genotypes compared to the control treatment. In over 65% of the studied chickpea genotypes, applying 6 dS.m-1 salt stress resulted in an increase in potassium content in the plant, while 9 dS.m-1 salt stress reduced leaf potassium content. The reduction in potassium content in plants is due to the substitution of sodium in place of potassium and calcium. The competition between potassium and sodium ions for uptake sites in the roots is one of the factors that increases sodium content and decreases potassium content. Plant dry weight increased by 25% in genotype MCC72 and more than three times in genotype MCC108 under the highest level of stress compared to the control treatment. In genotype MCC108, the application of the highest level of stress also increased seed weight in the plant by approximately 73% compared to the control treatment. With the imposition of salt stress and the decrease in water potential within the plant, the weight of the plant is affected and decreases. Additionally, due to the disruption of nutrient balance and the effects of osmotic stress, growth is reduced, and the dry weight of the aerial parts also decreases.
Conclusion
In general, the results showed that the imposition of salt stress affected the growth and physiological traits of chickpea genotypes. Seed weight and plant dry weight decreased in all genotypes under salt stress conditions of 6 dS.m-1 compared to the control treatment. The studied genotypes were able to maintain their survival and growth under salt stress conditions through various mechanisms such as increasing antioxidant compounds, preserving relative leaf water content, increasing leaf chlorophyll content, enhancing the activity of antioxidant enzymes, and increasing the content of metabolites. Generally, there was a high diversity among the studied chickpea genotypes, suggesting that their use in improving salt tolerance in chickpea plants could be beneficial.

Keywords

Main Subjects

Abdolinejad, R., Shekafandeh. A., 2014. Salt stress-induced changes in leaf antioxidant activity, proline and protein content in ‘Shah Anjir’and ‘Anjir Sabz’fig seedlings. International Journal of Horticultural Science and Technology. 1, 121-129. https://doi.org/10.22059/ijhst.2014.52782
Abe, N., Murata, T., Hirota, A., 1998. Novel DPPH radical scavengers, bisorbicillinol and demethyltrichodimerol, from a fungus. Bioscience, Biotechnology and Biochemistry. 6, 661-666. https://doi.org/10.1271/bbb.62.661
Abogadallah, G.M., 2010. Antioxidative defense under salt stress. Plant Signal Behavior, 5, 369-374. https://doi.org/10.4161/psb.5.4.10873
Adil, H.I., Cetin, H.I., Yener, M.E., Bayindirh, A., 2007. Subcritical (carbon dioxide + ethanol) extraction of polyphenols from apple and peach pomaces, and determination of the antioxidant activities of the extracts. The Journal of Supercritical Fluids. 43, 55-63. https://doi.org/10.1016/j.supflu.2007.04.012
Al-Amier, H., Craker, L.E., 2007. In vitro selection for stress tolerant spearmint. In: Janick J., Whipkey, A., (eds.), Issues in new crops and new uses. ASHS Press, Alexandria, VA. pp. 306-310
Alhasnawi, A.N., Kadhimi, A.A., Isahak, A., Mohamad, A., Doni, F., Yusoff, W.W., Zain, C.M., 2014. Salinity stress in plant and an important antioxidant enzyme. Life Science Journal. 11, 913-920. https://doi.org/10.7537/marslsj111014.143
Aliabadi-Farahani, H., Valadabadi, S.A., Daneshian, J., Khalvati, M.A., 2009. Evaluation changing of essential oil of balm (Melissa officinalis L.) under water deficit stress conditions. Journal of Medicinal Plant Research. 3, 329-333. https://doi.org/10.5897/JMPR.9000606
AliDinar, H.M., Ebert, G., Ludders, P., 1999. Growth, Chlorophyll Content, Photosynthesis and Water Relations in Guava (Psidium guajava L.) Under Salinity and Different Nitrogen Supply. Gartenbauwissenschaft. 64, 54-59.
Ashraf, M., Foolad, M.R., 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany. 59, 206–216. https://doi.org/10.1016/j.envexpbot.2005.12.006
Ashraf, M., Ozturk, M., Athar, H.R., 2008. Salinity and Water Stress: Improving Crop Efficiency. Springer, Netherlands.
Bates, L.S., Waldren, R.P., Teare, I.D., 1973. Rapid determination of free proline for water-stress studies. Plant and Soil. 39, 205-207. https://doi.org/10.1007/BF00018060
Bray, E.A., 1997. Plant responses to water deficit. Trends in Plant Science. 2, 48–54.
Bybordi, A., 2012. Study effect of salinity on some physiologic and morphologic properties of two grape cultivars. Life Science Journal, 9, 1092-1101. https://doi.org/10.7537/marslsj090412.166
Cakmak, I., Kirkby, E.A., 2008. Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiologia Plantarum. 133, 692-704. https://doi.org/10.1111/j.1399-3054.2007.01042.x
Caverzan, A., Casassola, A., Brammer, S.P., 2016. Antioxidant responses of wheat plants under stress. Genetic molecular and Biology. 39, 1-6. https://doi.org/10.1590/1678-4685-GMB-2015-0109
Chartzoulakis, K., Klapaki, G., 2000. Response of two greenhouse pepper hybrids to NaCl salinity during different growth stages. Scientia Horticulturae. 86, 247-260. https://doi.org/10.1016/S0304-4238(00)00151-5
Cicek, N., Cakirlar, H., 2002. The effect of salinity on some physiological parameters in two maize cultivars. Bulgican Journal Plant Physiology. 28, 66-74.
Cornic, C., Massacci, A., 1996 Leaf photosynthesis under drought stress. In: Baker, N.R. (ed.), Photosynthesis and Environment. pp. 347-366. Kluwer Academic Publish.
Dere, S., Gines, T., Sivaci, R., 1998. Spectrophotometric determination of chlorophyll a, b and total carotenoid contents of some algae species using different solvents. Turkish Journal of Botany 22, 13-17.
Dkhil, B.B., Denden, M., 2010. Salt stress induced changes in germination, sugars, starch and enzyme of carbohydrate metabolism in Abelmoschuses culentus L. (Moench.) seeds. African Journal of Agricultural Research. 5, 408-415. https://doi.org/10.5897/AJAR.9000614
Fallah, A., Farahmanfar, E., Moradi, F., 2015. Effect of salt stress on some morphophysiological characters of two rice culitivars during different growth stages at greenhouse. Applied Field Crops Research. 28, 175-182. [In Persian with English abstract]. https://doi.org/10.22092/aj.2015.105720.
FAOSTAT. 2021. Rome. Available online: https://www.fao.org/faostat/es/#data/QCL (accessed on 17 December 2021).
Firoozeh, R., Khavarinejad, R., Najafi, F., Saadatmand, S., 2019. Effects of gibberellin on contents of photosynthetic pigments, proline, phenol and flavonoid in savory plants (Satureja hortensis L.) under salt stress. Journal of Plant Research (Iranian Journal of Biology). 31, 894-908. [In Persian with English abstract]. http://dorl.net/dor/20.1001.1.23832592.1397.31.4.12.4.
Flowers, T. J., Flowers, S.A., 2005. Why does salinity pose such a different problem for plant breeders? Agricultural Water Management. 78, 15-24. https://doi.org/10.1016/j.agwat.2005.04.015
Garratt, L.C., Janagoudar, B.S., Lowe, K.C., Anthony, P., Power, J. B., Davey, M.R., 2002. Salinity tolerance and antioxidant status in cotton cultures. Free Radical Biology and Medicine 33, 502-511. https://doi.org/10.1016/S0891-5849(02)00838-9
Hassani Moghadam, E., Esna-Ashari, M., Rezainejad, A., 2015. Effect of drought stress on some physiological characteristics in six commercial iranian pomegranate (Punica granatum L.) Cultivars. 7, 1-11. [In Persian with English abstract].
Heidari, A., Toorchi, M., Bandehagh, A., Shakiba, M.R., 2011. Effect of NaCl stress on growth, water relations, organic and inorganic osmolytes accumulation in sunflower (Helianthus annuus L.) lines. Universal Journal of Environmental Research and Technology. 1, 351-362.
James, R.A., Caemmerer, S.V., Condon, A.G., Zwart, A.B., Munns, R., 2008. Genetic variation in tolerance to the osmotic stress component of salinity stress in durum wheat. Functional Plant Biology 35, 111-123. https://doi.org/10.1071/FP07234
Jukanti A.K, G.P., 2012. Nutritional quality and health benefits of chickpea (Cicer arietinum L): a review. British Journal of Nutrition. 108, 11-26. https://doi.org/10.1017/S0007114512000797
Kibria, M.G., Hossain, M.A., Murata, Y., Hoque, M.A., 2017. Antioxidant defense mechanisms of salinity tolerance in rice genotypes. rice science. 24, 155-162. https://doi.org/10.1016/j.rsci.2017.05.001
Kochaki, A., Zand, A., Banayan Aval, M., Rezvanimoghadam, P., Mahdavi Damghani, A, Jami Al-Ahmadi, M., Vesal, S.R., 2015. Plant Ecophysiology. Ferdowsi University of Mashhad Press. pp 271. [In Persian].
Koyro, H.W., 2000. Effect of high NaCl-salinity on plant growth, leaf morphology and ion composition in leaf tissues of Beta vulgaris ssp. Maritima. Journal of Applied Botany and Food Quality. 74, 67-73.
Kumar, S., Beena, A.S., Awana, M., Singh, A., 2017. Physiological, biochemical, epigenetic and molecular analyses of wheat (Triticum aestivum) genotypes with contrasting salt tolerance. Frontiers in Plant Science. 8, 1151. https://doi.org/10.3389/fpls.2017.01151
Maliro, M.F.A., McNeil, D.L., Redden, B., Kollmorgen, J.F., Pittock, C., 2008. Sampling strategies and screening of chickpea (Cicer arietinum L.) germplasm for salt tolerance. Genetic Resources and Crop Evolution. 55: 53-63. https://doi.org/10.1007/s10722-007-9214-9
Masoumzadeh, B.M., Imani, A.A., Khayamaim, S., 2012. Salinity stress effect on proline and chlorophyll rate in four beet cultivars. Scholars Research Library. 3, 5453-5456.
Mittler, R., Vanderauwera, S., Gollery, M., Van Breusegem, F., 2004. Reactive oxygen gene network of plant. Trends in Plant Science. 9, 490-498. https://doi.org/10.1016/j.tplants.2004.08.009
Parida, A.K., Das, A.B., 2005. Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety. 60, 324-349. https://doi.org/10.1016/j.ecoenv.2004.06.010
Parvaiz, A., Stayawati, S., 2008. Salt stress and phyto-biochemical responses of plants – a review. Plant, Soil and Environment. 54, 89–99. https://doi.org/10.17221/2774-PSE
Pinheiro, C., Chaves, M.M., Ricardo, C.P., 2001. Alterations in carbon and nitrogen metabolism induced by water deficit in the stems and leaves of Lupinus albus L. Journal of Experimental Botany. 52, 1063-70. https://doi.org/10.1093/jexbot/52.358.1063
Rafael, M., Enez-Díaz, J., Castillo, P., Jimenez-Gasco, M.D.M., Landa, B., Navas-Cortes, J.A., 2015. Fusarium wilt of chickpeas: Biology, ecology and management. Crop Protection. 23, 1-12.
Rahnama, A., James, R.A., Poustini, K., Munns, R., 2010. Stomatal conductance as a screen for osmotic stress tolerance in durum wheat growing in saline soil. Functional Plant Biology. 37, 255-269. https://doi.org/10.1016/j.cropro.2015.02.023
Rahnemoun, H., Shekari, F., Dejampour, J., Khorshidi, M.B., 2013. Salinity effects on some morphological and biochemical changes of almond. Journal of Crops Improvement. 15, 179-192. [In Persian with English abstract]. https://doi.org/10.22059/jci.2013.36108
Rajabi Dehnavi, A., Zahedi, M., 2020. Effects of foliar application of different ascorbic acid concentrations on the response of sorghum to salinity. Plant Process and Function. 9, 223-241. [In Persian with English abstract]. http://dorl.net/dor/20.1001.1.23222727.1399.9.35.13.4
Redouane, E., Mohamed, N., 2015. Adaptive response to salt stress in sorghum (Sorghum bicolor). American Eurasian Journal of Agricultural and Environmental Sciences. 15, 1351-1360. https://doi.org/10.5829/idosi.aejaes.2015.15.7.12683
Sabaghpour, S.H., 2001. Major diseases of chickpea In Iran. In proceeding of symposium on Grain Legumes in the Mediterranean. Agriculture, (LEGUMED), 25-27 October 2001. Rabat, Morocoo.
Sabir, P., Ashraf, M., Hussain, M., Jamil, A., 2009. Relationship of photosynthetic pigments and water relations with salt tolerance of proso millet (Panicum miliaceum L.) accessions. Pakistan Journal of Botany, 41, 2957-2964. https://doi.org/41(6): 2957-2964,2009
Shahid, M. A., Balal, R. M., Pervez, M. A., 2012. Differential response of pea (Pisum sativum L.) genotypes to salt stress in relation to the growth, physiological attributes antioxidant activity and organic solutes. Australian Journal of Crop Science. 6, 828-838.
Shobeiri, S., K. Ghassemi-Golezani, A. Golechin and J. Saba., 2007. Effect of water limitation on growth and yield of three chickpea cultivars in Zanjan. Journal of Agricultural Sciences and Natural Resources. 14, 32-43. [In Persia].
Singleton, V.L., Rossi, J.A., 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture. 16, 144-158. https://doi.org/10.5344/ajev.1965.16.3.144
Smart, R.E., Bingham, G.E., 1974. Rapid estimates of relative water content. Plant Physiology. 53, 258-260. https://doi.org/10.1104/pp.53.2.258
Soori, N., Bakhshi, D., Rezaei Nejad, A., Faizian, M., 2019. Effect of salinity stress on some physiological characteristics and photosynthetic parameters of several Iranian commercial pomegranate genotypes. Plant Process and Function. 8, 155-170. [In Persian with English abstract].
Srinivas, N.D., Rashmi, K.R., Raghavarao, K.S.M.S., 1999. Extraction and purification of a plant peroxidase by aqueous two-phase extraction coupled with gel filtration. Process Biochemistry. 35, 43-48. https://doi.org/10.1016/S0032-9592(99)00030-8
Tari, I., Laskay, G., Takacs, Z., Poor, P., 2013. Response of sorghum to abiotic stresses: A review. Journal of Agronomy and Crop Science. 199, 264-274. https://doi.org/10.1111/jac.12017
Turner, N., Colmer, T., Quealy, J., Pushpavalli, R., Krishnamurthy, L., Kaur, J., Singh, G., Siddique, K., Vadez, V., 2013. Salinity tolerance and ion accumulation in chickpea (Cicer arietinum L.) subjected to salt stress. Plant and Soil. 365, 347-361. https://doi.org/10.1007/s11104-012-1387-0
Vafadar, Z., Rahimmalek, M., Sabzalian, M.R., Nikbakht, A., 2018. Effect of salt stress and harvesting time on morphological and physiological characteristics of Myrtle (Myrthus communis). Plant Process and Function. 7, 33-44. http://dorl.net/dor/20.1001.1.23222727.1397.7.23.18.1
Velikova, V., Yordanov, I., Edreva, A., 2000. Oxidative stress and some antioxidant systems in acid raintreated bean plants. Protective role of exogenous polyamines. Plant Science. 151, 59-66. https://doi.org/10.1016/S0168-9452(99)00197-1
Wang, C.J., Yang, W., Wang, C., Gu, C., Niu, D.D., Liu, H.X., Wang, Y.P. and Guo, J.H., 2012. Induction of drought tolerance in cucumber plants by a consortium of three plant growth promoting rhizobacterium strains. Plos One, 7, 1-12. https://doi.org/10.1371/journal.pone.0052565
Yamaguchi, K., Mori, H., Nishimura, M., 1995. A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. Plant Cell Physiology. 36, 1157-1162. https://doi.org/10.1093/oxfordjournals.pcp.a078862
Yamaguchi, T., Blumwald, E., 2005. Developing salt-tolerant crop plants: challenges and opportunities. Trends in Plant Science. 12, 615-620. https://doi.org/10.1016/j.tplants.2005.10.002
Zarandi-Miandoab, L., Chaparzadeh, N., Fekri Shali, H., 2019. Interactive effects of salinity and magnesium on water and ionic relations of Zygophillum fabago L. Journal of Plant Research (Iranian Journal of Biology). 32, 72-85. [In Persian with English abstract].  https://dor.isc.ac/dor/20.1001.1.23832592.1398.32.1.18.1
Zarei, M., Azizi M., Rahemi, M., Tehranifar, A., 2016. Assessment of salinity tolerance of three fig cultivars based on growth and physiological factors and ions distribution. Iranian Journal of Horticultural Science and Technology. 17, 247-260. [In Persian with English abstract]. https://dor.isc.ac/dor/20.1001.1.16807154.1395.17.2.10.8