Identifying Salt-Tolerant Chickpea Genotypes During Early Growth Stage Through Multi-Statistical Approaches and Stress Indices Under Saline Conditions

Year 2025, Volume: 31 Issue: 3, 846 - 862, 29.07.2025

Hamdi Özaktan , Zehra Tiğriğ Berk Benlioğlu , Cennet Yaman , Melike İncetekin

https://doi.org/10.15832/ankutbd.1641187

Abstract

Salinity is an important environmental factor that jeopardizes productive agriculture in our world with the increasing human population, significantly limiting the production of food products and negatively affecting the growth and development of plants. In this study, eight chickpea (Cicer arietinum L.) genotypes from Türkiye were germinated under salt stress such as sodium chloride (NaCl) and sodium sulfate (Na2SO4) at electrical conductivity levels (4, 8, 12 and 16 dS m-1) over a period of 10 days in order to evaluate seed germination, seedling morphological and mineral responses, and to determine tolerant genotypes, Salinity stress is considered as one of the major constraints in chickpea production, but our study revealed a remarkable diversity among the tested genotypes. Germination rates decreased significantly with increasing salinity levels. While germination rates of different chickpea genotypes were above 85% under control conditions, these rates varied between 21% and 91% at the highest salt treatment of 16 dS m-1 of both salts. Sodium, calcium and sulfur contents showed significant differences among the genotypes. As the salt concentrations increased, the Na/K ratio also increased. As a result, Gürdal, Aras and Katran genotypes were found to be more salt tolerant under NaCl and Na2SO4 treatments. Analysis using stress indices showed that it is an effective method to evaluate the tolerance of chickpea genotypes to salt stress. These findings can be used for future chickpea breeding programs and reclamation of saline areas.

Keywords

Cicer arientinum L. , Genotype , Salinity , Germination , Mineral content , Sodium chloride , Sodium sulfate

Project Number

FLY-2021-11306

Thanks

This study was supported by Scientific Research Projects Department of Erciyes University, Türkiye. (Project Number: FLY-2021-11306).

References

• Abdelaal S M S, Moussa K F, Ibrahim A H, Mohamed E S, Kucher D E, Savin I & Abdel-Fattah M K (2021). Mapping Spatial Management Zones of Salt-Affected Soils in Arid Region: A Case Study in the East of the Nile Delta, Egypt. Agronomy 11(12): 2510. https://doi.org/10.3390/AGRONOMY11122510
• Abrol I (1986). Salt-affected soils: problems and prospects in developing countries. CAB Digital Library. https://www.cabidigitallibrary.org/doi/full/10.5555/19881923285
• Ahmed S, Ahmed S, Roy S K, Woo S H, Sonawane K D & Shohael A M (2019). Effect of salinity on the morphological, physiological and biochemical properties of lettuce (Lactuca sativa L.) in Bangladesh. Open Agriculture 4(1): 361–373. https://doi.org/10.1515/OPAG-2019 0033/HTML
• Anuradha S & Seeta Ram Rao S (2001). Effect of brassinosteroids on salinity stress induced inhibition of seed germination and seedling growth of rice (Oryza sativa L.). Plant Growth Regulation 33(2): 151–153. https://doi.org/10.1023/A:1017590108484
• 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. https://doi.org/10.1016/J.PLAPHY.2020.08.042
• Assareh M H, Rasouli B & Amiri B (2010). Effects of NaCl and Na2SO4 on germination and initial growth phase of Halostachys caspica. Desert 15: 119–125
• Atieno J, Li Y, Langridge P, Dowling K, Brien C, Berger B, Varshney R K & Sutton T (2017). Exploring genetic variation for salinity tolerance in chickpea using image-based phenotyping. Scientific Reports 7(1): 1–11. https://doi.org/10.1038/s41598-017-01211-7
• Bouslama M & Schapaugh W T (1984). Stress tolerance in soybean, part 1: Evaluation of three screening techniques for heat and drought tolerance. Crop Science 24(5): 933–937. https://doi.org/10.2135/cropsci1984.0011183X002400050026x
• Causin H F, Bordón D A E & Burrieza H (2020). Salinity tolerance mechanisms during germination and early seedling growth in Chenopodium quinoa Wild. genotypes with different sensitivity to saline stress. Environmental and Experimental Botany, 172, 103995. https://doi.org/10.1016/J.ENVEXPBOT.2020.103995
• Chen X J, Min D H, Yasir T A & Hu Y G (2012). Evaluation of 14 morphological, yield-related and physiological traits as indicators of drought tolerance in Chinese winter bread wheat revealed by analysis of the membership function value of drought tolerance (MFVD). Field Crops Research 137: 195–201
• Clarke J M, De Pauw R M & Townley-Smith T M (1992). Evaluation of methods for quantification of drought tolerance in wheat. Crop Science 32: 732–737
• Dadbakhsh A, Yazdansepas A & Ahmadizadeh M (2011). Study drought stress on yield of wheat (Triticum aestivum L.) genotypes by drought tolerance indices. Advances in Environmental Biology 5(7): 1804–1810
• Dadshani S, Sharma R C, Baum M, Ogbonnaya F C, León J & Ballvora A (2019). Buğdayda tuz stresine tepkinin çok boyutlu değerlendirmesi. PLoS One, 14(9), e0222659.
• Dehnavi A R, Zahedi M, Ludwiczak A, Perez S C & Piernik A (2020). Effect of Salinity on Seed Germination and Seedling Development of Sorghum (Sorghum bicolor (L.) Moench) Genotypes. Agronomy 10(6): 859. https://doi.org/10.3390/AGRONOMY10060859
• del Carmen Martínez-Ballesta M, Egea-Gilabert C, Conesa E, Ochoa J, Vicente M J, Franco J A, Bañon S, Martínez J J & Fernández J A (2020). The Importance of Ion Homeostasis and Nutrient Status in Seed Development and Germination. Agronomy 10(4): 504. https://doi.org/10.3390/AGRONOMY10040504
• Farshadfar E & Elyasi P (2012). Screening quantitative indicators of drought tolerance in bread wheat (Triticum aestivum) landraces. European Journal of Experimental Biology 2(3): 577–584
• Farshadfar E & Javadinia J (2011). Evaluation of chickpea (Cicer arietinum L.) genotypes for drought tolerance. Seed and Plant Improvement Journal 27(4): 517–537
• Farshadfar E & Sutka J (2002). Multivariate analysis of drought tolerance in wheat substitution lines. Cereal Research Communications 31: 33–39
• Fernandez G C J (1992). Effective selection criteria for assessing plant stress tolerance. In Kuo C G (Ed.), Adaptation of Food Crops to Temperature and Water Stress (pp. 257–270). International Symposium, Taiwan.
• Fischer K S & Wood G (1981). Breeding and selection for drought tolerance in tropical maize. Symposium on Principles and Methods in Crop Improvement for Drought Resistance with Emphasis on Rice, IRRI, Philippines.
• Fischer R A & Maurer R (1978). Drought resistance in spring wheat cultivars. Australian Journal of Agricultural Research 29: 897–912
• Ghazali G E B (2020). Suaeda vermiculata Forssk. ex J.F. Gmel.: Structural Characteristics and Adaptations to Salinity and Drought: A Review. International Journal of Scientific & Engineering Research. https://doi.org/10.18483/ijsc.2268
• Hossain A B S, Sears A G, Cox T S & Paulsen G M (1999). Desiccation tolerance and its relationship to assimilate partitioning in winter wheat. Crop Science 30: 622–627
• Iqbal R M (2003). NaCl ve Na altında yetiştirilen buğdayın yaprak alanı ve iyon içeriği. Pakistan Journal of Biological Sciences 6: 1512–1514
• Iqbal S, Hussain S, Qayyaum M et al. (2020). The response of maize physiology under salinity stress and its coping strategies. In Akbar Hossain (Ed.), Plant Stress Physiology. IntechOpen.
• Isayenkov S V & Maathuis F J M (2019). Plant salinity stress: Many unanswered questions remain. Frontiers in Plant Science, 10, 80. https://doi.org/10.3389/fpls.2019.00080
• Joshi J & Kavane A (2024). Estimation of salinity stress tolerant level of chickpea cultivars (Cicer arietinum) using seed germination experiment followed by good agricultural practices. Springer Journal of Botany 37(1): 421–425. https://doi.org/10.1007/s42535-02300579-4
• K Abass Al-Hamzawi, M. (2007). Effect of sodium chloride and sodium sulfate on growth, and ions content in faba-bean (Vicia faba). J Kerbala Univ 3(2): 152-163
• Kaur G, Sanwal S, Sehrawat N, Kumar A, Kumar N & Mann A (2022). Assessing the effect of salinity stress on root and shoot physiology of chickpea genotypes using hydroponic technique. Indian Journal of Genetics and Plant Breeding 81(4): 92–95. https://doi.org/10.31742/ISGPB.81.4.12
• Khan H, Gul R, Khan N U, Naz R, Shah S, Asim N & Latif A (2018). Role of selection indices in ascertaining high yielding drought stress tolerant chickpea (Cicer arietinum L.). Journal of Animal & Plant Sciences 28(2)
• Knight H & Knight M R (2001). Abiotic stress signaling pathways specificity and cross-talk. Trends in Plant Science, 6: 262–267
• Kotula L, Clode P L, De J, Cruz Jimenez L & Colmer T D (2019). Salinity tolerance in chickpea is associated with the ability to 'exclude' Na from leaf mesophyll cells. Journal of Experimental Botany 70(18): 4991–5002. https://doi.org/10.1093/jxb/erz241
• Kumar S, Li G, Yang J, Huang X, Ji Q, Liu Z, Ke W & Hou H (2021). Effect of Salt Stress on Growth, Physiological Parameters, and Ionic Concentration of Water Dropwort (Oenanthe javanica) Cultivars. Frontiers in Plant Science, 12. https://doi.org/10.3389/FPLS.2021.660409
• Kundu V, Sarkar M & Kundagrami S (2023). Screening of chickpea (Cicer arietinum L.) germplasms under salt stress. Journal of Eco-Friendly Agriculture. https://doi.org/10.48165/jefa.2023.18.02.11
• Kurunc A, Aslan G, Karaca C, Tezcan A, Turgut K, Karhan M, Kaplan B (2020). Stevia rebaudiana Bertoni'nin tuz kaynağı ve sulama suyu tuzluluğunun büyüme, verim ve kalite parametreleri üzerine etkileri. Bilim Horticul, 270, 109458.
• medicinal plant Laghmouchi Y, Belmehdi O, Bouyahya A, Skali Senhaji N & Abrini J (2017). Effect of temperature, salt stress and pH on seed germination of Origanum compactum. https://doi.org/10.1016/J.BCAB.2017.03.002
• Lamba K, Kumar M, Singh V, Chaudhary L, Sharma R, Yashveer S & Dalal M S (2023). Heat stress tolerance indices for identification of the heat tolerant wheat genotypes. Scientific Reports 13(1): 10842
• Lavrenko S, Lavrenko N & Lykhovyd P V (2019). Effect of degree of salinity on seed germination and initial growth of chickpea (Cicer arietinum). Biosystems Diversity 27(2): 101–105. https://doi.org/10.15421/011914
• Li W, Zhang H, Zeng Y, Xiang L, Lei Z, Huang Q et al. (2020). A salt tolerance evaluation method for sunflower (Helianthus annuus L.) at the seed germination stage. Scientific Reports 10(1): 10626
• Liang W, Ma X, Wan P & Liu L (2018). Plant salt-tolerance mechanism: A review. Biochemical and Biophysical Research Communications, 495(1): 286–291. https://doi.org/10.1016/J.BBRC.2017.11.043
• Lin C S, Binns M R & Lefkovitch L P (1986). Stability analysis: where do we stand? Crop Science 26: 894–900
• Ludwig M, Wilmes P & Schrader S (2018). Measuring soil sustainability via soil resilience. Science of The Total Environment 626: 1484 1493. https://doi.org/10.1016/J.SCITOTENV.2017.10.043
• Mann A et al. (2019). Physiological response of chickpea (Cicer arietinum L.) at early seedling stage under salt stress conditions. Legume Research - An International Journal 42(5).
• Meena H P, Kumar J & Ramesh M (2014). Evaluation of the reaction of chickpea (Cicer arietinum L.) genotypes to drought conditions using various stress tolerance indices. Legume Research - An International Journal 37(5): 453–459
• Mertens D (2005). AOAC official method 975.03. Metal in plants and pet foods. Official Methods of Analysis, 18th edn. Horwitz W & Latimer G W (Eds), pp. 3–4
• Moosavi S S, Samadi Y B, Naghavi M R, Zali A A, Dashti H & Pourshahbazi A (2008). Introduction of new indices to identify relative drought tolerance and resistance in wheat genotypes. Desert 12: 165–178
• Mukami A, Ng’etich A, Syombua E, Oduor R & Mbinda W (2020). Varietal differences in physiological and biochemical responses to salinity stress in six finger millet plants. Physiology and Molecular Biology of Plants 26(8): 1569–1582. https://doi.org/10.1007/S12298-020 00853-8
• Munns R & Tester M (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology 59: 651–681. https://doi.org/10.1146/ANNUREV.ARPLANT.59.032607.092911
• Naseer M N, Rahman F U, Hussain Z, Khan I A, Aslam M M, Aslam A, Waheed H, Khan A U & Iqbal S (2022). Effect of Salinity Stress on Germination, Seedling Growth, Mineral Uptake and Chlorophyll Contents of Three Cucurbitaceae Species. Brazilian Archives of Biology and Technology, 65, e22210213. https://doi.org/10.1590/1678-4324-2022210213
• Navada S, Vadstein O, Gaumet F, Tveten A K, Spanu C, Mikkelsen Ø & Kolarevic J (2020). Biofilms remember: Osmotic stress priming as a microbial management strategy for improving salinity acclimation in nitrifying biofilms. Water Research, 176, 115732. https://doi.org/10.1016/J.WATRES.2020.115732 Nayyar H (2003). Calcium as environmental sensors in plants. Current Science India 84: 7–10
• Okumuş O, Uzun S & Özaktan H (2023). Investigation of Some Forage Peas (Pisum arvense L.) in terms of Seed Yield under Kayseri Conditions. International Journal of Agricultural and Natural Sciences 3(16): 316–321
• Ozaktan H & Doymaz A (2022). Mineral composition and technological and morphological performance of beans as influenced by organic seaweed-extracted fertilizers applied in different growth stages. Journal of Food Composition and Analysis 114 pp
• Ozaktan H, Uzun S, Uzun O & Yasar Ciftci C (2023). Assessment of Agro-Morphological Traits of Common Bean Genotypes Grown Under Organic Farming Conditions with Multi-Variate Analyses and Applications. Gesunde Pflanzen 75(3): 515–523
• Özaktan H, Çiftçi C Y, Kaya M D, Uzun S, Uzun O & Akdogan G (2018). Chloride salts inhibit emergence and seedling growth of chickpea rather than germination. Legume Research, 41(1): 60–66
• Özaktan H, Kıbık G & Erol O (2022). Yeni Nohut (Cicer arietinum L.) Çeşitlerinin Kayseri Koşullarında Agro-morfolojik Özelliklerinin Belirlenmesi. Erciyes Tarım ve Hayvan Bilimleri Dergisi 5(2): 62–70
• Pan T, Liu M, Kreslavski V D, Zharmukhamedov S K, Nie C, Yu M, Kuznetsov V V, Allakhverdiev S I & Shabala S (2021). Non-stomatal limitation of photosynthesis by soil salinity. Critical Reviews in Environmental Science and Technology 51(8): 791–825. https://doi.org/10.1080/10643389.2020.1735231
• Pessarakli M & Szabolcs I (2016). Soil salinity and sodicity as particular plant/crop stress factors. Handbook of Plant and Crop Stress, Third Edition, 3–21. https://doi.org/10.1201/9781351104609-1
• Pessoa L G M, Freire M B G do S, Green C H M, Miranda M F A, Filho J C d A & Pessoa W R L S (2022). Assessment of soil salinity status under different land-use conditions in the semiarid region of Northeastern Brazil. Ecological Indicators, 141, 109139. https://doi.org/10.1016/J.ECOLIND.2022.109139
• Peterson A & Murphy K (2015). Ova kinoa çeşitlerinin sodyum klorür ve sodyum sülfat tuzluluğuna toleransı. Mahsul Bilimi, 55, 331–338.
• Pushpavalli R, Krishnamurthy L, Thudi M, Gaur P M, Rao M V, Siddique K H M, Colmer T D, Turner N C, Varshney R K & Vadez V (2015). Two key genomic regions harbour QTLs for salinity tolerance in ICCV 2 × JG 11 derived chickpea (Cicer arietinum L.) recombinant inbred lines. BMC Plant Biology, 15(1): 1–15. https://doi.org/10.1186/S12870-015-0491-8
• Reich M, Aghajanzadeh T, Parmar S, Hawkesford M J & De Kok L J (2018). Calcium ameliorates the toxicity of sulfate salinity in Brassica rapa. Journal of Plant Physiology 231: 1–8
• Rengasamy P (2010). Osmotic and ionic effects of various electrolytes on the growth of wheat. Australian Journal of Soil Research 48: 120124
• Rosielle A A & Hamblin J (1981). Theoretical aspects of selection for yield in stress and non-stress environments. Crop Science 21: 943–946
• Sandhu D, Cornacchione M V & Ferreira J F S (2017). Variable salinity responses of 12 alfalfa genotypes and comparative expression analyses of salt-response genes. Scientific Reports, 7, 42958. https://doi.org/10.1038/srep42958
• Sarita, Mehrotra S, Dimkpa C O & Goyal V (2023). Survival mechanisms of chickpea (Cicer arietinum) under saline conditions. Plant Physiology and Biochemistry, 205: 108168. https://doi.org/10.1016/J.PLAPHY.2023.108168
• Stavi I, Thevs N & Priori S (2021). Soil Salinity and Sodicity in Drylands: A Review of Causes, Effects, Monitoring, and Restoration Measures. Frontiers in Environmental Science, 9, 712831. https://doi.org/10.3389/FENVS.2021.712831
• Toderich K N, Mamadrahimov A A, Khaitov B B, Karimov A A, Soliev A A, Nanduri K R & Shuyskaya E V (2020). Differential impact of salinity stress on seeds minerals, storage proteins, fatty acids, and squalene composition of new Quinoa genotype, grown in hyper-arid desert environments. Frontiers in Plant Science, 11, 607102. https://doi.org/10.3389/fpls.2020.607102
• Toklu F, Gupta D, Sen, Karaköy T & Özkan H (2021). Bioactives and Nutraceuticals in Food Legumes: Nutritional Perspective. In Breeding for Enhanced Nutrition and Bio-Active Compounds in Food Legumes (pp. 229–245). https://doi.org/10.1007/978-3-030-59215-8_10
• Tounsi S, Feki K, Hmidi D, Masmoudi K & Brini F (2017). Salt stress reveals differential physiological, biochemical and molecular responses in T. monococcum and T. durum wheat genotypes. Physiology and Molecular Biology of Plants 23(3): 517–528. https://doi.org/10.1007/s12298-017-0457-4
• Voisin T, Erriguible A & Aymonier C (2019). Influence of multiphasic systems on salt(s) solubility in supercritical water: the case of NaCl and NaCl-Na2SO4. The Journal of Supercritical Fluids 152, 104567
• Wang J, Zhao Y G, Pang H C, Zhang L & Li Y Y (2016). Grain shape as a predictor of salt tolerance in sunflower. Agronomy Journal 108: 2280–2288 salinity stress
• Yuan Y (2011). Multiple imputation using SAS software. Journal of Statistical Software, 45, 1–25.
• Zeeshan M, Lu M, Sehar S, Holford P & Wu F (2020). Comparison of biochemical, anatomical, morphological, and physiological responses to in wheat and barley genotypes differing in salinity tolerance. Agronomy 10(1): 127. https://doi.org/10.3390/agronomy10010127
• Zehra A, Gul B, Ansari R & Khan M A (2012). Role of calcium in alleviating effect of salinity on germination of Phragmites karka seeds. South African Journal of Botany, 78, 122–128.
• Zhang Q & Dai W (2019). Plant Response to Salinity Stress. In Stress Physiology of Woody Plants (pp. 155–173). https://doi.org/10.1201/9780429190476-7
• Zörb C, Geilfus C M & Dietz K J (2019). Salinity and crop yield. Plant Biology 21: 31–38. https://doi.org/10.1111/PLB.12884