Biochemical and physiological responses of contrasting soybean genotypes to individual (Na+, Cl‾) and additive (NaCl) salts

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DOI: 10.1007/s42535-025-01331-w
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Keywords: Soybean, Sodium, Chloride, Salt stress, Biochemical responses


Abstract


Increasing soil salinity poses a detrimental impact on agriculture. Elevated sodium and chloride levels in the soil adversely affects crop plants, with sodium being a primary contributor. Recent research has also identified chloride as significant causative factor. To investigate the effects of sodium and chloride on soybean growth, in our study, we applied salt treatments on two distinct genotypes (MAUS-47 and Gujosoya-2), revealing genotype specific variations in growth reduction. The individual and combined salt treatments affected soybean growth differently, with individual sodium (Na+) alone having the most detrimental effect, followed by sodium chloride (NaCl). Each genotype exhibited distinct mechanisms to combat the individual and combined salt stress, leading to notable reductions in physiological, photosynthetic, and biochemical growth parameters. In MAUS-47, shoot and root showed a 49% and 51% increase in Cl‾ content, respectively, while Gujosoya-2 showed a 69% increase in shoot Cl‾ content and a 68% increase in root Cl‾ content, compared to their non-saline counterparts. There were significant reductions in Chl a, Chl b, and carotenoid content in Gujosoya-2 under Na-dominant salt, followed by NaCl and Cl-dominant treatments. The differential impacts of salt on gas exchange parameters were also evident in MAUS-47 and Gujosoya-2. The Gujosoya-2 genotype showed inability to recover plant growth due to inefficient photosynthetic pigment accumulation, gas exchange, antioxidant defense, osmolyte accumulation, and ion regulation. In contrast, the MAUS-47 genotype demonstrated better resilience through the expression of genotype-specific traits that supported plant growth under salinity stress. The study highlights the importance of considering role of Cl- in soybean cultivation and demonstrates the economic disadvantages of neglecting its effects. The observed differences in genotype responses to varying salt conditions underscore the significance of breeding for salinity tolerance. This study provides insights for breeders to improve salt-specific resilience in soybean.

Soybean, Sodium, Chloride, Salt stress, Biochemical responses


References


Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–208


Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287


Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227


Cao D, Li Y, Liu B, Kong F, Tran LP (2017) Adaptive mechanisms of soybean grown on salt-affected soils. Land Degrad Develop 29(4):1054–1064. https://doi.org/10.1002/ldr.2754


Chapman HD, Pratt PF (1961) Method for analysis of soil, plants and waters. University of California, Berkeley, CA


Chen L, Peng L, Ouyang W, Yao H, Ye Y, Shan Z, Cao D, Chen S, Yang Z, Huang Y, Han B, Sha A, Zhou X, Chen H (2024) Screening and identification of salt tolerance soybean varieties and germplasms. Oil Crop Sci 9(3):204–210. https://doi.org/10.1016/j.ocsci.2024.06.005


Colmenero-Flores JM, Franco-Navarro JD, Cubero-Font P, Peinado-Torrubia P, Rosales MA (2019) Chloride as a beneficial macronutrient in higher plants: new roles and regulation. Int J Mol Sci 20(19):4686. https://doi.org/10.3390/ijms20194686


Feng C, Gao H, Zhou Y, Jing Y, Li S, Yan Z, Xu K, Zhou F, Zhang W, Yang X, Hussain MA, Li H (2023) Unfolding molecular switches for salt stress resilience in soybean: recent advances and prospects for salt-tolerant smart plant production. Front Plant Sci 14:1162014. https://doi.org/10.3389/fpls.2023.1162014


Genc Y, McDonald GK, Tester M (2007) Reassessment of tissue Na+ concentration as a criterion for salinity tolerance in bread wheat. Plant Cell Environ 30:1486–1498


Grieve CM, Grattan SR (1983) Rapid assay for determination of water-soluble quaternary ammonium compounds. Plant Soil 70:303–307


Guan Z, Chen S, Chen F, Liu Z, Fang W, Tang J (2012) Comparison of stress effect of NaCl, Na+ and Cl‾ on two Chrysanthemum species. Acta Hortic 937:369–375


Guan RX, Guo XY, Qu Y, Zhang ZW, Bao LG, Ye RY, Chang RZ, Qiu LJ (2023) Salt tolerance in soybeans: focus on screening methods and genetics. Plants 28(1):97. https://doi.org/10.3390/plants13010097


Hanin M, Ebel C, Ngom M, Laplaze L, Masmoud K (2016) New insights on plant salt tolerance mechanisms and their potential use for breeding. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01787


Hasanuzzaman M, Raihan MRH, Masud AAC, Rahman K, Nowroz F, Rahman M, Nahar K, Fujita M (2021) Regulation of reactive oxygen species and antioxidant defense in plants under salinity. Int J Mol Sci 22(17):9326. https://doi.org/10.3390/ijms22179326


He Y, Chen Y, Yu CL, Lu KX, Jiang QS, Fu JL, Wang GM, Jiang DA (2016) Photosynthesis and yield traits in different soybean lines in response to salt stress. Photosynthetica 54(4):630–635


Hemeda HM, Klein BP (1990) Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. J Food Sci 55:184–186


Hossain MS, Dietz K (2016) Tuning of redox regulatory mechanisms, reactive oxygen species and redox homeostasis under salinity stress. Front PlantSci 7:548


Huang Y, Chen L, Zhen A, Liu ZX, Lei B, Kong QS, Bie ZL (2015) Effects of iso-osmotic Na+, Cl‾ and NaCl stress on the plant growth and physiological parameters of grafted cucumber. Acta Hortic 1086:153–160


Jiang L, Xiao M, Huang R, Wang J (2025) The regulation of ROS and phytohormones in balancing crop yield and salt tolerance. Antioxidants 14(1):63. https://doi.org/10.3390/antiox14010063


Jogeswar G, Pallela R, Jakka NM, Reddy PS, Rao JV, Sreeniwasulu N, Kavi Kishor PB (2006) Antioxidative response in different sorghum species under short term salinity stress. Acta Phy Planta 28:465–475


Kamyab-Talesh F, Mousavi SF, Asadi R, Rezaei M, Khaledian MR (2014) Evaluation of some rice cultivars response to salinity stress using resistance indices. Arch Agron Soil Sci 60:1303–1314. https://doi.org/10.1080/03650340.2014.891730


Kesawat MS, Satheesh N, Kherawat BS, Kumar A, Kim HU, Chung SM, Kumar M (2023) Regulation of Reactive Oxygen Species during Salt Stress in Plants and Their Crosstalk with Other Signaling Molecules-Current Perspectives and Future Directions. Plants (Basel) 14;12(4):864. https://doi.org/10.3390/plants12040864


Khare T, Kumar V, Kavi Kishor PB (2014) Na+ and Cl‾ ions show additive effects under NaCl stress on induction of oxidative stress and the responsive antioxidative defense in rice. Protoplasma 252:1149–1165


Kumar V, Khare T (2016) Differential growth and yield responses of salt-tolerant and susceptible rice cultivars to individual (Na+ and Cl‾) and additive stress effects of NaCl. Acta Physiol Plant. https://doi.org/10.1007/s11738-016-2191-x


Li B, Tester M, Gilliham M (2017) Chloride on the Move. TRPLSC 1508


Lowry OH, Rosenbrough NJ, Far AL, Randall RJ (1951) Protein measurement with the folin-phenol reagent. J Biol Chem 193:265–275


Massa D, Magán JJ, Montesano FF, Tzortzakis N (2020) Minimizing water and nutrient losses from soilless cropping in Southern Europe. Agric Water Manage 1(241):106395


Morán-Diez ME, Tranque E, Bettiol W, Monte E, Hermosa R (2020) Differential response of tomato plants to the application of three Trichoderma species when evaluating the control of Pseudomonas syringae populations. Plants 9(5):626


Muchate NS, Nikalje GC, Rajurkar NS, Suprasanna P, Nikam TD (2016) Plant salt stress: adaptive responses, tolerance mechanism and bioengineering for salt tolerance. Bot Rev. https://doi.org/10.1007/s12229-016-9173-y


Munns R, Husain S, Rivelli AR, James R, Condon AG, Lindsay M, Lagudah ES, Schachtman DP, Hare RA (2002) Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits. Plant Soil 247:93–105


Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681


Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxide in spinach chloroplasts. Plant Cell Physiol 22:867–880


Nikalje GC, Nikam TD, Suprasanna P (2017a) Looking at halophytic adaptation to high salinity through genomics landscape. Curr Genom 18:6


Nikalje GC, Srivastava AK, Pandey GK, Penna S (2017b) Halophytes in biosaline agriculture: mechanism, utilization and value addition. Land Degrad Dev. https://doi.org/10.1002/ldr.2819


Nikalje GC, Mirajkar SJ, Nikam TD, Suprasanna P (2018) Multifarious role of ROS in halophytes: signaling and defence. In: Zargar and Zargar (Eds.) Abiotic stress mediated sensing and signaling in plants: An omics perspective. Springer. https://doi.org/10.1007/978-981-10-7479-0_7


Negrao S, Schmockel SM, Tester M (2017) Evaluating physiological responses of plants to salinity stress. Ann Bot 119(1):1–11


Patil PP, Ghane SG, Barmukh RB, Teixeira JAS, Nikam TD (2010) Differential response of Niger (Guizotia abyssinica Cass.) cultivars to salinity stress in relation to seed germination, oxidative stress, osmotic adjustment and antioxidant enzyme activities. Plant Stress 4:56–63


Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Envir Sci Pollut Res 22:4056–4075


Phang TH, Shao GH, Lam HM (2008) Salt tolerance in soybean. J Integr Plant Biol 50:1196–1212


Rabhi M, Castagna A, Remorini D, Scattino C, Smaoui A, Ranieri A, Abdelly C (2012) Photosynthetic response to salinity in two obligate halophytes: Sesuvium portulacastrum and Tecticornia indica. South Afr J Bot 79:39–47


Rahman MA, Thomson MJ, Shah-E-Alam M, de Ocampo M, Egdane J, Ismail AM (2016) Exploring novel genetic sources of salinity tolerance in rice through molecular and physiological characterization. Ann Bot 117:1083–1097


Raza MA, Saeed A, Munir H, Ziaf K, Shakeel A, Saeed N, Munawar A, Rehman F (2017) Screening of tomato genotypes for salinity tolerance based on early growth attributes and leaf inorganic osmolytes. Arch Agro Soil Sci 63:4


Rosales MA, Franco-Navarro JD, Peinado-Torrubia P, Díaz-Rueda P, Álvarez R, Colmenero-Flores JM (2020) Chloride improves nitrate utilization and NUE in plants. Front Plant Sci 11:442. https://doi.org/10.3389/fpls.2020.00442


Savchenko T, Tikhonov K (2021) Oxidative Stress-Induced Alteration of Plant Central Metabolism. Life (Basel), 1;11(4):304. https://doi.org/10.3390/life11040304


Shelke DB, Pandey M, Nikalje GC, Zaware BN, Suprasanna P, Nikam TD (2017) Salt responsive physiological, photosynthetic and biochemical attributes at early seedling stage for screening soybean genotypes. Plant Physiol Biochem 118:519–528


Shelke DB, Nikalje GC, Chambhare MR, Zaware BN, Suprasanna P, Nikam TD (2019a) Na+ and Cl‾ induce differential physiological, biochemical responses and metabolite modulations in vitro in contrasting salt-tolerant soybean genotypes. 3 Biotech 9:91


Shelke DB, Nikalje GC, Nikam TD, Maheshwari P, Punita DL, Rao KRSS, Kavi Kishor PB, Suprasanna P (2019b) Chloride (Cl‾) uptake, transport, and regulation in plant salt tolerance. In: Roychoudhury A and Tripathi D (eds) Molecular plant abiotic stress: biology and biotechnology, 1st edn, pp. 241–268. https://doi.org/10.1002/9781119463665.ch13


Shelke DB, Chambhare MR, Nikalje GC, Nikam TD (2023) Improvement of soybean crop for yield, stress tolerance, and Value-Added products using a Transgenic approach. Adv Agric 8166928:26. https://doi.org/10.1155/2023/8166928


Singh D, Singh CK, Kumari S, Tomar RS, Karwa S, Singh R, Raja BS, Sarkar SK, Pal M (2017) Discerning morpho-anatomical, physiological and molecular multiformity in cultivated and wild genotypes of lentil with reconciliation to salinity stress. PLoS ONE 12(5):e0177465


Smith IK, Vierheller TL, Thurne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5,5_-dithiobis (2-nitrobenzoic acid). Anal Biochem 175:408–413


Srivastava S, Srivastava S (2020) Prescience of endogenous regulation in Arabidopsis thaliana by Pseudomonas putida MTCC 5279 under phosphate starved salinity stress condition. Sci Rep 10(1):1–5


Suprasanna P, Nikalje GC, Rai AN (2016) Osmolyte Accumulation and implications in plant abiotic stress tolerance In: Osmolytes and plants acclimation to changing environment: Emerging omics technologies Springer India. Pp 1–12


Tavakkoli E, Fatehi F, Rengasamy P, McDonald GK (2012) A comparison of hydroponic and soil-based screening methods to identify salt tolerance in the field in barley. J Exp Bot. https://doi.org/10.1093/jxb/ers085


Tavakkoli E, FoadFatehi SC, Rengasamy P, Glenn KM (2011) Additive effects of Na+ and Cl‾ ions on barley growth under salinity stress. J Exp Bot 62:2189–2203


Tavakkoli E, Rengasamy P, Mcdonald GK (2010) High concentrations of Na+ and Cl‾ ions in soil solution have simultaneous detrimental effects on growth of Faba bean under salinity stress. J Exp Bot 61:4449–4459


Teakle NL, Tyerman SD (2010) Mechanisms of Cl– transport contributing to salt tolerance. Plant Cell Environ 33:566–589


Teshome DT, Zharare GE, Naidoo S (2020) The threat of the combined effect of biotic and abiotic stress factors in forestry under a changing climate. Front Plant Sci 30:11:1874


Wang L, Jia-Yang X, Jia W, Chen Z, Zi-Cheng X (2020) Chloride salinity in a chloride-sensitive plant: focusing on photosynthesis, hormone synthesis and transduction in tobacco. Plant Physiol Biochem 153:119–130. https://doi.org/10.1016/j.plaphy.2020.05.021


Watanabe S, Kojima K, Ide Y, Sasaki S (2000) Effect of saline and osmotic stress on proline and sugar accumulation in Populus eupharatica in vitro. Plant Cell Tissue Organ Cult 63:199–206


Witham FH, Blaydes DF, Devlin RM (1971) Experiments in plant physiology. Van Nostrand, New York, p 245


Wu D, Shen Q, Cai S, Chen Z, Dai F, Zhang G (2013) Ionomic responses and correlations between elements and metabolites under salt stress in wild and cultivated barley. Plant Cell Physiol 54(12):1976–1988


Yu TF, Hou ZH, Wang HL, Chang SY, Song XY, Zheng WJ, Zheng L, Wei JT, Lu ZW, Chen J, Zhou YB, Chen M, Sun SL, Jiang QY, Jin LG, Ma YZ, Xu ZS (2024) Soybean steroids improve crop abiotic stress tolerance and increase yield. Plant Biotechnol J 22(8):2333–2347. https://doi.org/10.1111/pbi.14349

 


Author Information


Department of Botany, Savitribai Phule Pune University, Pune, India