Research Article

Growth, Physiological and Biochemical Response of Chickpea Cultivars to Different Levels of Salinity Stress

Muhammad Umer Chattha1, Muhammad Ilyas2, Imran Khan1, Athar Mahmood1, Muhammad Bilal Chattha3*, Ambreen Fatima4, Muhammad Iqbal5, Muhammad Tahir Akbar6, Muhammad Mahmood Iqbal5, Faran Muhammad7, Muhammad Talha Aslam1 and Muhammad Umair Hassan1

1Department of Agronomy, University of Agriculture, Faisalabad, 38040, Pakistan; 2University College of Dera Murad Jamali Nasirabad (LUAWMS), Pakistan; 3Department of Agronomy, Faculty of Agricultural Sciences, University of the Punjab Lahore, Pakistan; 4Department of Botany, University of Agriculture, Faisalabad, 38040, Pakistan; 5Cotton Research Institute, Multan, Pakistan; 6The Senior Scientist Soil Fertility (Field), Multan, Pakistan; 7Cereal Crops section, Agricultural Research Institute, Dera Ismail Khan-29050, Pakistan.

Received | May 04, 2022; Accepted | June 18, 2022; Published | June 28, 2022

*Correspondence | Muhammad Bilal Chattha, Department of Agronomy, Faculty of Agricultural Sciences, University of the Punjab Lahore, Pakistan; Email: [email protected]

Citation | Chattha, M.U., M. Ilyas, I. Khan, A. Mahmood, M.B. Chattha, A. Fatima, M. Iqbal, M.T. Akbar, M.M. Iqbal, F. Muhammad, M.T. Aslam and M.U. Hassan. 2022. Growth, physiological and biochemical response of chickpea cultivars to different levels of salinity stress. Pakistan Journal of Agricultural Research, 35(2): 359-365.

DOI | https://dx.doi.org/10.17582/journal.pjar/2022/35.2.359.365

Keywords | Salinity, Cultivars, Growth, Physiology, Photosynthetic pigments

Copyright: 2022 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Plants faced different stress during growth cycle which considerably reduces their growth and productivity. Salinity stress (SS) is a challenging abiotic stress which considerably reduced the seed germination, plant growth and metabolic activities (Carbajal-Vázquez et al., 2022) and productivity (Rajabi et al., 2020). The high concentration of salts induced detrimental impacts on plant physiology and disturbs the ionic homeostasis, plant hormones balance and altered plants growth and subsequent development (Azzam et al., 2022; Yuan et al., 2022). Salinity stress reduces the synthesis of chlorophyll contents, photosynthetic efficiency and it disturbs plant water relationships, membrane stability and accumulation of different osmolytes (Dustgeer et al., 2021; Rehman et al., 2021). Moreover, SS also induced the reactive oxygen (ROS) production that cause damages to plant proteins, DNA membranes and enzymes (Rehman et al., 2021). Likewise, SS reduces uptake of nutrients and disturbs plant physiological and microbial activities in rhizosphere resulting in marked reduction in production (Tavakkoli et al., 2011; Chandra et al., 2020).

Different crops have developed their own defensive systems which preserved them salinity stress. The plant response to SS largely depends on the type of genotype and amount of salts in soil (Zahra et al., 2020). Like other pulse crops chickpea is also salt sensitive and salinity stress considerably reduced the final grain yield (Khan et al., 2013). The selection and identification of cultivars that have good tolerance abilities against the salinity stress can play an important role to overcome this problem. Likewise, germination and seedling related attributes are the most important criteria to select the cultivars having good tolerance against the salt stress (Jamil and Rha, 2004). Moreover, the germination percentage and growth rate of seedlings is an imperative characteristic being used for the selection of cultivars (Saboora et al., 2006; Khayatnezhad et al., 2010).

Chickpea (Cicer arietinum L.) is an indispensible legume crop grown on 12 mha of more than 45 countries (FAOSTAT, 2010; Hirich et al., 2014). The seeds of chickpea are enriched protein source particularly for the people of developing nations (Jukanti et al., 2012). Chickpea seeds contain 5% fat, 23% protein, 47% starch, 64% carbohydrates, 7mg/100 iron, 3mg/100g zinc and 140mg/g calcium (Sanjeewa et al., 2010). In addition, chickpea also maintains the soil fertility through biological nitrogen fixation in soil (Chang et al., 2011). Cultivars varied considerably against SS, thus this research was aimed to determine the effect of SS on growth, antioxidant activities, and photosynthetic pigments of chickpea genotypes.

Materials and Methods

Experimental site

The present study was carried in wire house of Department of Agronomy, UAF. The soil was collected with spade and brought to lab and sieved in order to fill the pots. The soil was analyzed by standard procedures of Homer and Pratt (1961) and it was recognized as sandy loam with pH 7.89 and contained organic matter 0.81%, N 0.043%, P 6.98 mg kg-1 and K 195 mg kg-1.

Growth conditions

The soil collected from agronomy farm was sieved and quantity of salt (NaCl) was added into the soil according to the treatments in order to maintain the salinity levels. After that pots having size of 380.00 cm2 was filled with 5 kg soil and ten seeds sown in every pot. The pots were daily visited and irrigations were applied as per crop needs on the basis of visual observations. The weeds grown in pots were manually up-rooted and no attack of insects and disease were reported.

Experimental details

The study contained SS levels i.e., 0, 8 and 12 dsm-1 and different chickpea cultivars i.e., NIAB-2016, Bittle-2016 and Bhakar-2011. The current study was executed in completely randomized design having factorial combination.

Data collection and measurements

The mean emergence time (MGT) was measured with the procedures of Ellis and Robets (1981), whereas, the emergence index (EI) was calculated with the procedures of AOSA (1983). Moreover, T50 and final emergence percentage were calculated by the standard protocols of Farooq et al. (2005). Three plants were collected from each pot and plant height (PH) was measured and the average was taken. Similarly, the same three plants were taken, root length (RL), root fresh weight (RFW), shoot length (SL), and shoot fresh weight (SFW) was taken and the average was worked out. The concentration of total soluble proteins (TSP) was determined with the procedures of Bradford (1976). The activity of SOD was determined by the methods of Zhang (1992), whereas the POD and CAT activities were determined by the procedures of Chance and Maehly (1955) and Guan et al. (2009).

Statistical analysis

The observations on growth, physiology and biochemical characteristics were analyzed by using the analysis of variance technique (Steel et al., 1997) and LSD at 0.05 probability level was used to measure significance among mean values.

Results and Discussion

SS significantly affected all the tested germination traits (Table 1). The results indicated that maximum T50, MET, and minimum GP, and minimum EI were recorded in stronger SS (12 dsm-1), whilst minimum T50, MET, and maximum GP and EI was noticed under no salt stress (Table 1). Cultivars also behaved differently under salt stress. The results indicated that maximum T50, MET was taken by the NIAB-2016 as compared to other cultivars, while minimum T50 and MET were taken by the Bhaker-2011 (Table 1). Likewise, minimum GP and EI were also noted in Bhaker-2011 whilst maximum GP and EI were noticed in cultivar Bhaker-2011 (Table 1). The results indicated that SS the emergence and reduced the GP and EI. The delayed emergence due to SS be attributed to reduced water uptake and specific ion toxicity (SIT) which considerably increased the time to start emergence. These findings are the same as the outcomes of Munns and Tester (2008) they also noted that salt stress delayed the emergence. Salt stress increased the time MET owing to osmotic stress which resulted in a reduction in water take which consequently increased the T50 and MET. Likewise, Rajabi et al. (2020) and Ashagre et al. (2013) also noted that salt stress increased the MET. The differences among cultivars for germination traits can be the due to difference in their genetic makeup and their ability to cope with SS (Khodarahmpour et al., 2012).

The maximum plant height, RL, RFW, SL, and SFW was recorded in control conditions, whereas minimum PH, RL, RFW, SL, SFW was recorded in strong SS (12 dSm-1) (Table 2). In the case of cultivars; Bhaker-2011 performed better and had maximum PH, RL, RFW, SL and SFW whereas, NIAB-2016 had minimum PH, RL, RFW, SL and SFW (Table 2). Salt stress reduced the water uptake and nutrients translocation and therefore it considerably reduced the plant height (Hossein and Kasra, 2011). The differences amid genotypes for PH could be due to differences in the genetic makeup of plants. Previously Hassan et al. (2018) also stated that plant height is a genetic character and it differed significantly among cultivars. The reduction in RL and SL under SS might be due to the reduced availability of water owing to osmotic stress caused by SS (Sultan et al., 2021). SS decreased the RFW which could be due to a reduction in the hydrolysis of food reservoirs and its movement to growing plant parts (Gholizadeh et al., 2021).

 

Table 1: Effect of different levels of salinity stress on germinations traits of chickpea cultivars.

Salinity stress	TSE (days)	MET (days)	EI (EI)	T50 (days)	FEP (%)
S1 (control)	7.2B	12.1C	74.6A	9.6A	93.0A
S2 (8 dsm-1)	9.4A	12.8B	61.7B	10.7B	76.2B
S3 (12 dsm-1)	10.0A	13.6A	51.9C	11.3C	63.7C
LSD≤0.05P	0.68	0.63	1.46	0.54	1.83
Cultivars (CV)
CV1 (NIAB-2016)	9.8A	13.3A	59.0C	11.1A	70.8C
CV2 (Bittle-2016)	9.3A	13.0B	62.2B	10.7A	76.7B
CV3 (Bhakar-2011)	8.6B	12.1C	66.9A	9.0B	85.4A
LSD≤0.05P	0.68	0.63	1.46	0.54	1.83
S × CV
S1× CV1	8.3	12.7	71.3	10.0cd	87.0c
S1× CV2	8.3	12.3	73.7	9.7de	93.0b
S1× CV3	7.7	11.3	78.7	9.0d	99.0a
S2× CV1	10.0	13.3	59.0	11.3ab	69.3e
S2× CV2	9.7	13.0	61.3	11.0b	74.7d
S2× CV3	8.7	12.0	64.7	9.7de	84.7c
S3× CV1	10.7	14.0	46.7	12.0a	56.0g
S3× CV2	10.0	13.7	51.7	11.3ab	62.3f
S3× CV3	9.3	13.0	57.3	10.7bc	72.7d
LSD≤0.05P	NS	NS	NS	0.93	3.16

TSE: time to start emergence; MET: mean emergence time; EI: emergence index; T50: time to 50% emergence; FEP: final emergence percentage. Means having different letters showing significance at 0.05 P.

 

The results indicated that SS imposed a negative impact on photosynthetic pigments (Table 3). In the case of cultivars, Bhakar-2011 had maximum values for chlorophyll and carotenoid contents whereas the NIAB-2016 had maximum values for the aforementioned photosynthetic pigments (Table 3). In the present study, salinity stress considerably reduced the photosynthetic pigments (Table 2). The excessive concentration of Na+ owing to salinity stress causes the production of ROS that denatures enzymes required for the synthesis of chlorophyll contents thereby substantially reduced the chlorophyll contents (Alzahib et al., 2021).

 

Table 2: Effect of different levels of salinity stress on growth attributes of chickpea cultivars.

Salinity stress	PH (cm)	RL (cm)	RFW (g)	SL (cm)	SFW (g)
S1 (control)	68.2A	7.7A	0.45A	16.66A	5.52A
S2 (8 dsm-1)	56.2B	6.2B	0.45AB	14.29B	4.81B
S3 (12 dsm-1)	51.8C	4.8C	0.42B	12.99C	4.34C
LSD≤0.05P	1.83	0.22	0.026	0.86	0.47
Cultivars (CV)
CV1 (NIAB-2016)	57.1B	5.9C	0.37C	14.02B	4.54B
CV2 (Bittle-2016)	58.4AB	6.6A	0.49A	14.52A	4.86AB
CV3 (Bhakar-2011)	67.7A	6.3B	0.46B	15.39A	5.27A
LSD≤0.05P	1.83	0.22	0.026	0.86	0.47
S × CV
S1× CV1	63.7	6.9c	0.38	15.73	4.68cd
S1× CV2	65.0	8.4a	0.44	16.53	5.68ab
S1× CV3	76.0	7.8b	0.54	17.70	6.20a
S2× CV1	58.3	6.1de	0.44	13.60	4.77cd
S2× CV2	56.7	6.0e	0.46	14.40	4.50cd
S2× CV3	53.7	6.5d	0.44	14.87	5.17bc
S3× CV1	49.3	4.6g	0.29	12.73	4.18d
S3× CV2	53.7	5.3f	0.59	12.63	4.39cd
S3× CV3	52.3	4.6g	0.39	13.60	4.44cd
LSD≤0.05P	NS	0.39	NS	NS	0.82

PH: Plant height; RL: root length; RFW: root fresh weight; SFW: shoot fresh weight. Means having different letters showing significance at 0.05 P.

 

The concentration of TSP and anti-oxidant activities was significantly enhanced under SS. The maximum TSP, SOD, POD and CAT activities were noted in high level of salt stress, whilst minimum TSP and antioxidant activities were noted in normal conditions (Table 4). Amongst cultivars Bhaker-2011 had maximum TSP and antioxidant activities were activities, whereas the cultivar NIAB-2016 had minimum TSP and antioxidant activities were (Table 4). The increase in protein under salt stress can be ascribed to increase in protein synthesis and conversation of nitrogen in proteins (Ashraf, 2003). The anti-oxidant activities were considerably increased under the SS, likewise, Sultan et al. (2021) also found a marked increase in SOD activity under salt stress. Likewise, Khan et al. (2022) noted a significant increase in SOD and CAT are considerably increased under the activity under salt stress.

 

Table 3: Effect of different levels of salinity stress on photosynthetic attributes of chickpea cultivars.

Salinity stress	Chlorophyll a	Chlorophyll b	Carotenoids
S1 (control)	9.67A	3.41A	0.69A
S2 (8 dsm-1)	7.61B	2.45B	0.58B
S3 (12 dsm-1)	6.62C	1.76C	0.59B
LSD≤0.05P	0.28	0.16	0.02
Cultivars (CV)
CV1 (NIAB-2016)	6.76C	2.32B	0.60B
CV2 (Bittle-2016)	7.82B	2.61A	0.61B
CV3 (Bhakar-2011)	9.32A	2.69A	0.65A
LSD≤0.05P	1.83	0.16	0.02
S × CV
S1× CV1	8.43	3.10c	0.65b
S1× CV2	9.53	3.40b	0.66b
S1× CV3	11.03	3.73a	0.77a
S2× CV1	6.40	2.23e	0.57cd
S2× CV2	7.47	2.57d	0.59cd
S2× CV3	8.97	2.55d	0.58cd
S3× CV1	5.43	1.62f	0.57cd
S3× CV2	6.47	1.86f	0.59cd
S3× CV3	7.97	1.78f	0.61c
LSD≤0.05P	NS	0.28	0.03

Means having different letters showing significance at 0.05 P.

 

Table 4: Effect of different levels of salinity stress on soluble proteins and anti-oxidant activities of chickpea cultivars.

Salinity stress	TSP (mg/g FW)	SOD (U/mg FW)	POD (U/µg protein)	CAT (U/mg protein)
S1 (control)	69.39B	53.83C	6.08C	30.49B
S2 (8 dsm-1)	70.08B	168.83B	15.77B	53.77A
S3 (12 dsm-1)	72.46A	236.79A	18.16A	55.24A
LSD≤0.05P	1.68	2.01	0.88	1.50
Cultivars (CV)
CV1 (NIAB-2016)	69.10B	147.33C	12.12B	42.86B
CV2 (Bittle-2016)	69.88B	151.66B	12.47B	47.64A
CV3 (Bhakar-2011)	72.94A	160.47A	15.41A	49.0A
LSD≤0.05P	1.68	2.01	0.88	1.50
S × CV
S1× CV1	67.60	50.27	4.87f	26.0
S1× CV2	68.80	52.97	6.27ef	31.20
S1× CV3	71.77	58.27	7.10e	33.57
S2× CV1	68.70	162.07	14.50d	50.03
S2× CV2	69.63	169.63	14.40d	55.10
S2× CV3	71.90	174.80	18.40b	56.17
S3× CV1	71.00	229.67	17.0bc	51.83
S3× CV2	71.20	232.37	16.73c	56.63
S3× CV3	75.17	248.33	20.73a	57.27
LSD≤0.05P	NS	3.49	1.53	NS

TSP: total soluble proteins; SOD: superoxide dismutase; POD: peroxidase; CTA: catalase. Means having different letters showing significance at 0.05 P.

 

Conclusions and Recommendations

The increase in salt stress linearly decreased the germination, growth, and photosynthetic pigments however, salinity significantly increased antioxidant activities. Cultivars behaved differently in terms of salt stress tolerance. Cultivar Bhakker-2016 is characterized as the most tolerant cultivar owing to better germination, growth, and antioxidant activities as compared to other cultivars. Therefore, the cultivar, Bhakker-2016 can be used in future breeding programs to develop salt-tolerant cultivars.

Novelty Statement

Cultivars varied considerably against salinity stress, thus this research was aimed to characterize the best salt tolerant cultivars.

Author’s Contribution

Muhammad Umer Chattha: Conceived and planned the experiment and write the original draft.

Muhammad Ilyas: Review and editing

Imran Khan: Conceived and planned the experiment and write the original draft.

Ambreen Fatima: Helped in Data collection

Athar Mahmood, Muhammad Bilal Chattha, Muhammad Iqbal, Muhammad Tahir Akbar, Muhammad Mahmood Iqbal, Faran Muhammad, Muhammad Talha Aslam and Muhammad Umair Hassan: Reviewed and edited the manuscript.

Conflict of interest

The authors have declared no conflict of interest.

References

Alzahib, R.H., H.M. Migdadi, A.A. Al-Ghamdi, M.S. Alwahibi, A.A. Ibrahim, and W.A. Al-Selwey. 2021. Assessment of morpho-physiological, biochemical and antioxidant responses of tomato landraces to salinity stress. Plants, 10(4): 696. https://doi.org/10.3390/plants10040696

Ashagre, H., H.A. Ibrahim, E. Fasika, and F. Temesgen. 2013. Effect of salinity stress on germination and seedling vigour of chickpea (Cicer arietinum L.). Acad. J. Agric. Res., 9: 161-166.

Ashraf, M., 2003. Relationships between leaf gas exchange characteristics and growth of differently adapted populations of blue panic grass (Panicum antidotale Retz.) under salinity or waterlogging. Plant Sci., 165: 69-75. https://doi.org/10.1016/S0168-9452(03)00128-6

Association of Official Seed Analysts, 1983. Seed Vigor testing handbook. 1st Edition, AOSA, East Lasing, 88.

Azzam, R.C., S. Safi-naz Zaki, A. Atif, Bamagoos, Mostafa, M. Rady, and F.H. Alharby. 2022. Soaking maize seeds in zeatin-type cytokinin biostimulators improves salt tolerance by enhancing the antioxidant system and photosynthetic efficiency. Plants, 11(8): 1004. https://doi.org/10.3390/plants11081004

Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3

Carbajal-Vázquez V.H., F.C. Gómez-Merino, E.G. Alcántar-González, P. Sánchez-García, and L.I. Trejo-Téllez. 2022. Titanium increases the antioxidant activity and macronutrient concentration in tomato seedlings exposed to salinity in hydroponics. Plants, 11(8): 1036. https://doi.org/10.3390/plants11081036

Chandra, P., P. Dhuli, P. Verma, A. Singh, M. Choudhary, K. Prajapat, A.K. Rai, and R.K. Yadav. 2020. Culturable microbial diversity in the rhizosphere of different biotypes under variable salinity. Trop. Ecol., 61: 291-300. https://doi.org/10.1007/s42965-020-00089-3

Chang Y.W., I. Alli, Y. Konishi, and E. Ziomek. 2011. Characterization of protein fractions from chickpea (Cicer arietinum L.) and oat (Avena sativa L.) seeds using proteomic techniques. Int. Food Res. J., 44: 3094-3104. https://doi.org/10.1016/j.foodres.2011.08.001

Chance, B., and A.C. Maehly. 1955. Assay of catalase and pemxides. Methods Enzymol., 2: 764-775. https://doi.org/10.1016/S0076-6879(55)02300-8

Dustgeer, Z., M.F. Seleiman, I. Khan, M.U. Chattha, B.A. Alhammad, R.S. JALAL, and M.U. Hassan. 2021. Glycine-betaine induced salinity tolerance in maize by regulating the physiological attributes, antioxidant defense system and ionic homeostasis. Notulae Bot. Hortic. Agrobot. Cluj-Napoca, 49(1): 12248-12248. https://doi.org/10.15835/nbha49112248

Ellis, R.A. and E.H. Roberts. 1981. The quantification of ageing and survival in orthodox seeds. Seed Sci. Tech., 9: 373-409.

FAOSTAT, 2010. Agriculture production. Food and Agriculture Organization of the United Nations. http://faostat.fao.org/site/339/default.aspx. Accessed 30/08/2012.

Farooq, M., S.M.A. Basra, K. Hafeez and N. Ahmad. 2005. Thermal hardening: A new seed vigor enhancement tool in rice. Acta Bot. Sin., 47: 187-192. https://doi.org/10.1111/j.1744-7909.2005.00031.x

Gholizadeh, F., G. Mirzaghaderi, S. Danish, M. Farsi, and S.H. Marashi. 2021. Evaluation of morphological traits of wheat varieties at germination stage under salinity stress. PLoS One, 16(11): e0258703. https://doi.org/10.1371/journal.pone.0258703

Guan, Y.J. J. Hu, X.J. Wang, and C. Shao. 2009. Seed priming with chitosan improves maize germination and seedling growth in relation to physiological changes under low temperature stress. Zhejiang Univ. Sci. B, 10: 427-433. https://doi.org/10.1631/jzus.B0820373

Hassan, M.U., M.U. Chattha, A. Mahmood and S.T. Shahi. 2018. Performace of sorghum cultivars for biomass quality and bio-methane production grown in semiarid area of Pakistan. Environ. Sci. Pollut. Res., 1: 1-8.

Hirich A, R. Ragab, R. Choukr-Allah, and A. Rami. 2014. The effect of deficit irrigation with treated wastewater on sweet corn: experimental and modelling study using SALTMED model. Irrig. Sci., 32: 205-219. https://doi.org/10.1007/s00271-013-0422-0

Homer, C.D., and P.E. Pratt. 1961. Methods of analysis for soils, plants and waters. University of California. Agric. Sci. Publications, Berkeley.

Hossein, A.F. and M. Kasr. 2011. Effect of hydropriming on seedling vigour in basil (Ocimum basilicum L.) under salinity conditions. Adv. Environ. Biol., 5: 828-833.

Khan, I., H. Zafar, M.U. Chattha, A. Mahmood, R. Maqbool, F. Athar, M.A. Alahdal, B. Farhana, F. Mahmood, and M.U. Hassan. 2022. Seed priming with different agents mitigate alkalinity induced oxidative damage and improves maize growth. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 50(1): 12615-12615. https://doi.org/10.15835/nbha50112615

Jamil, M. and E.S. Rha. 2004. The effect of salinity (NaCl) on the germination and seedling of sugar beet (Beta vulgaris L.) and cabbage (Brassica oleracea capitata L.). Korean J. Plant Res., 7: 226-232.

Jukanti, A.K., P.M. Gaur, C.L.L. Gowda, and R.N. Chibbar. 2012. Nutritional quality and health benefits of chickpea (Cicer arietinum L.): A review. Br. J. Nutr., 108(S1): S11-S26. https://doi.org/10.1017/S0007114512000797

Khan, S., J. Iqbal and M. Saeed. 2013. Comparative study of grain yield and biochemical traits of different rice varieties grown under saline and normal conditions. J. Anim. Plant Sci., 23: 575-588.

Khan, I., Muhammad, A., Chattha, M.U., Skalicky, M., Chattha, M.B., Ayub, M.A., Anwar, M.R., Soufan, W., Hassan, M.U., Rahman, M.A. and Brestic, M., 2022. Mitigation of Salinity-Induced Oxidative Damage, Growth, and Yield Reduction in Fine Rice by Sugarcane Press Mud Application. Frontiers in Plant Science, 13. 13:840900.

Khayatnezhad, M., R. Gholamin, S.H. Jamaati-e-Somarin and R. Zabihi-Mahmoodabad. 2010. Effects of peg stress on corn cultivars (Zea mays L.) at germination stage. World Appl. Sci. J., 11: 504-506.

Khodarahmpour, Z., M. Ifar and M. Motamedi. 2012. Effects of NaCl salinity on maize (Zea mays L.) at germination and early seedling stage. Afr. J. Biotechnol., 11: 298-304. https://doi.org/10.5897/AJB11.2624

Li, W., and Q. Li. 2017. Effect of environmental salt stress on plants and the molecular mechanism of salt stress tolerance. Int. J. Environ. Sci. Nat. Res., 7: 555714. https://doi.org/10.19080/IJESNR.2017.07.555714

López-Bellido, R.J., L. López-Bellido, J. Benítez-Vega, V. Muñoz-Romero, F.J. López-Bellido, and R. Redondo. 2011. Chickpea and faba bean nitrogen fixation in a Mediterranean rainfed Vertisol: Effect of the tillage system. Eur. J. Agron., 34(4): 222-230. https://doi.org/10.1016/j.eja.2011.01.005

Munns, R. and M. Tester. 2008. Mechanism of salinity tolerance. Annu. Rcv. Plant Biol., 59: 651-681. https://doi.org/10.1146/annurev.arplant.59.032607.092911

Rajabi D.A., M. Zahedi, A. Ludwiczak, S. Cardenas Perez, and A. Piernik. 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

Saboora, A., K. Kiarostami, F. Behroozbayati, and S. Hajihashemi. 2006. Salinity (NaCl) tolerance of wheat genotypes at germination and early seedling growth. Pak. J. Biol. Sci., 9(11): 2009-2021. https://doi.org/10.3923/pjbs.2006.2009.2021

Sanjeewa, W.T., J.P. Wanasundara, Z. Pietrasik, and P.J. Shand. 2010. Characterization of chickpea (Cicer arietinum L.) flours and application in low-fat pork bologna as a model system. Int. Food Res. J., 43(2): 617-626. https://doi.org/10.1016/j.foodres.2009.07.024

Steel, R.G.D., J.H. Torrie, and D.A. Dicky. 1997. Principles and procedures of statistics, a biometrical approach, 3rd ed. McGraw Hill, Inc. Book Co. New York, NY, USA. pp. 352-358.

Sultan, I., I. Khan, M.U. Chattha, M.U. Hassan, L. Barbanti, R. Calone, M. Ali, S. Majid, M.A. Ghani, M. Batool and W. Izzat. 2021. Improved salinity tolerance in early growth stage of maize through salicylic acid foliar application. Ital. J. Agron., 16(3): 1810. https://doi.org/10.4081/ija.2021.1810

Tavakkoli, E., F. Fatehi, S. Coventry, P. Rengasamy, and G.K. McDonald. 2011. Additive effects of Na+ and Cl− ions on barley growth under salinity stress. J. Exp. Bot., 62: 2189-2203. https://doi.org/10.1093/jxb/erq422

Rehman, H., H.F. Alharby, A.A. Bamagoos, M.T. Abdelhamid, and M.M. Rady. 2021. Sequenced application of glutathione as an antioxidant with an organic biostimulant improves physiological and metabolic adaptation to salinity in wheat. Plant Physiol. Biochem., 158: 43-52. https://doi.org/10.1016/j.plaphy.2020.11.041

Yuan, J.Q., D.W. Sun, Q. Lu, L. Yang, H.W. Wang, and X.X. Fu. 2022. Responses of Physiology, Photosynthesis, and Related Genes to Saline Stress in Cornus hongkongensis subsp, tonkinensis (WP Fang) QY Xiang. Plants, 11(7): 940. https://doi.org/10.3390/plants11070940

Zahra, N., Z.A. Raza, and S. Mahmood. 2020. Effect of salinity stress on various growth and physiological attributes of two contrasting maize genotypes. Braz. Arch. Biol. Technol., 63. https://doi.org/10.1590/1678-4324-2020200072

Zhang, X., 1992. The measurement and mechanism of lipid peroxidation and SOD, POD and CAT activities in biological system. Research methodology of crop physiology. Agriculture Press, Beijing. pp. 208-211.