Insights into Physiological, Biochemical and Molecular Responses in Wheat under Salt Stress

*Hari Kesh, Sunita Devi, Naresh Kumar, Ashwani Kumar, Arvind Kumar, Pooja Dhansu, Parvender Sheoran and Anita Mann*

#### **Abstract**

Globally, wheat is a major staple food crop that provides 20% of food calories for 30% of the human population. Wheat growth and production are significantly affected by salt stress at various stages and adversely affect germination, vegetative growth, stomatal conductance, photosynthesis, reproductive behavior, protein synthesis, enzymatic activity and finally hampered grain yield. Maintenance of low Na+ /K+ ratio, antioxidants and hormonal regulation, and accumulation of compatible osmolytes such as glycine betaine, proline and trehalose help the wheat genotypes to mitigate the negative effects of salt stress. Recent studies have reported various mechanisms at the physiological, biochemical and molecular levels to adapt the salinity stress in various ecologies. Salt tolerant genotypes can be developed by conventional breeding approaches and through biotechnological approaches. This chapter reviews the updates on mechanisms and recent approaches to structure the salt-tolerant and high-yielding genotypes.

**Keywords:** wheat, salt stress, ion homeostasis, conventional approaches, molecular breeding

#### **1. Introduction**

Bread wheat is a major staple food cultivated throughout the world with a global yield of 8.8 million tons [1]. Global demand for wheat is increasing day by day due to its unique features such as bio-fortified and processed products like biscuits, cookies, doughnuts, porridge and pastries [2]. However, the production and productivity of wheat have decreased due to various biotic and abiotic stresses. Different climate models estimated that wheat production could reduce by 6% due to adverse climatic conditions [3]. Among the abiotic stresses, salinity stress significantly affects the growth and production of wheat crops. Up to 40 percent yield loss worth \$ 27 billion

US annually have reported in salt-affected regions [4, 5]. Soil salinity negatively affects the morphological traits such as germination percentage, grain per spike, plant height, grain yield and harvest index [6–8]; physiological traits like relative water content, membrane stability, chlorophyll fluorescence and mineral uptake [9, 10]; biochemical traits like proline content, gluten content, protein synthesis and enzymatic activity involved in various metabolic processes [11–14]. Salinity stress disturbs the ionic balance due to the accumulation of Na+ which reduces the mineral uptake and their translocation to grains [15, 16]. Salt stress also causes the production of reactive oxygen species which hampers plant growth and development [13, 17]. Wheat grain yield reduces greatly when soil pH or electrical conductivity reaches 8.5 or 4 dS m−1. Salt stress creates a water deficit which makes it difficult for roots to draw water from their surroundings [18, 19]. Early-stage exposure to salt causes osmotic stress, which adversely affects the normal cell metabolism, stomatal opening and transpiration process. Long-term stress leads to ionic stress due to a high concentration of NaCl. Ionic stress causes chlorosis and necrosis of leaves and reduces photosynthesis and protein synthesis [20]. Irrigated water with the salt content of 2–3 g L−1 or 3–5 g L−1 reduces the grain yield of wheat by 7–13% or 13–24%, respectively [21]. To cope with these adverse effects of salt stress, plants use different mechanisms such as the exclusion of sodium ions and increase in potassium concentration, maintenance of high K+ /Na+ ratio, increased stomatal conductance and transpiration efficiency, osmotic adjustment and antioxidant defence [22–24]. Therefore, knowledge and understanding of the physiological and biochemical mechanisms are very essential for selecting and developing salt-tolerant wheat genotypes. Moreover, an integrated approach of conventional and molecular breeding can be used to improve wheat productivity and under salinity stress. Therefore, the present chapter summarizes the negative effect of salt stress, tolerance mechanism and potential breeding methods to improve the resilience in wheat.

#### **2. Effect of salt stress in wheat**

#### **2.1 Germination**

Germination is the basic and dynamic process that determines the further growth and development of plants. The seed germination process may be divided into three distinct phases. Phase one initiates with imbibition of water by dry seed, phase two causes activation of enzymatic activity and metabolic processes and phase three is a post-germination phase that includes rupturing of endosperm and radicle elongation followed by seedling establishment [25–27]. Salt stress lowers the osmotic potential of the germination medium which disrupts the normal functioning of the enzyme responsible for protein metabolism, deteriorates seed food reserves and ultimately grain yield [28]. These consequences together cause inhibition of cell expansion and cell division. Besides enzymatic imbalance, seed dormancy, hard seed coat, seed vigor and viability, temperature, moisture content and light intensity also affects the seed germination [29]. Previous studies reported that the accumulation of mucilage, callose, lignin and suberin increase the seed dormancy by limiting the permeability of water and diffusion of oxygen through the seed coat, delaying the germination process [30, 31]. Delayed and decreased germination of the wheat seed was reported at 12.5 dS m−1 salinity level [32]. Germination percentage in wheat also depends on the type of wheat i.e. spring or winter or differences in the cultivar. For example, wheat variety Kharchia 65 was found more salt-tolerant than KRL 1–9 due to its high chlorophyll content, membrane stability *Insights into Physiological, Biochemical and Molecular Responses in Wheat under Salt Stress DOI: http://dx.doi.org/10.5772/intechopen.102740*

and relative water content. Significant variation in wheat cultivars was observed for percent germination, rate of germination and germination index [33, 34]. Cultivar Shakha 93 and Shakah 94 were found positive while Masr 1 was negative for most of the germination traits under salt stress condition [35]. Similarly, Charushahi et al. [36] observed complete inhibition of germination at a high salinity rate due to limited uptake of water. High salt tolerance of Al-Hussein variety at germination stage was due to high tolerance index and chlorophyll stability at different salt concentration [37].

#### **2.2 Plant growth**

Salt stress severely affects wheat growth at both the vegetative and reproductive stages. Further, salt stress at the seedling stage may cause seedling chlorosis, necrosis or even death [38]. Early maturity under salt stress reduces the plumule length, leaf area and plant height [39]. Moreover, reduction in leaf size, number of leaves, root colonization, leaf expansion and dry matter of shoot were also noticed in wheat [40, 41]. The root is the first and most important organ of plants which is essential for the uptake of water and nutrient from the soil to maintain the growth and various developmental processes. Salinity inhibited growth of root and shoot dry weight, root length and diameter and root volume in wheat. Salinity reduces the root length and coleoptiles length and seedling establishment [42]. Otu et al. [43] reported a significant effect of increasing salinity level on root and shoot length, root fresh weight and elongation rate (**Figure 1**). A serious injuries effect in growth parameters of wheat like the relative growth rate of roots and leaves was seen under salt stress in

#### **Figure 1.**

*Effects of salinity stress on wheat morphological, physiological, biochemical traits and yield attributes.*

comparison to normal condition [44]. Many earlier studies have reported a reduction in growth parameters like root and shoot length, seedling length, leaf area, the relative growth rate of root and shoot, fresh and dry weight of root and shoot, plant height and tillering capacity at different salinity levels [45–48] (**Table 1**).


#### **Table 1.**

*Effect of salt stress on physiological, biochemical and yield attributes.*

*Insights into Physiological, Biochemical and Molecular Responses in Wheat under Salt Stress DOI: http://dx.doi.org/10.5772/intechopen.102740*

#### **2.3 Photosynthesis**

Salinity stress has severed effect of various physiological processes such as respiration, membrane stability, ion toxicity and photosynthesis. The photosynthesis process involves photosynthetic apparatus, PS-I and PS-II, electron transport chain, carbon dioxide reduction pathways. Any damage at any stage leads to a reduction in the photosynthetic efficiency of a crop plant [63]. Salinity stress greatly reduces the amount of photosynthetic pigments at different salt concentrations and it was found more in salt-sensitive genotypes than tolerant. This decreased pigment content may be a due accumulation of ions in chloroplast and the high activity of chlorophyllase enzyme [64, 65]. At the vegetative stage, salt stress affects the carbohydrate synthesis while its translocation to grains during the grain filling stage [66]. Sodium chloride treatment decreases the stomatal conductance, CO2 uptake required for carboxylation reaction and activity of RUBISCO (**Figure 1**) which ultimately reduces the photosynthetic efficiency [67]. Kafi [68] observed varied responses of wheat genotypes depending upon the growth stage, the concentration of salt and period of salt exposure. Stomatal conductance and reduced variable to maximum fluorescence were found major limiting factors affecting photosynthesis under salt stress. The toxic concentration of Na+ and Cl− in leaves, decreases the photosynthetic rate by disrupting the chlorophyll structure and PS-II [69]. Furthermore, reduced stomatal conductance decreases the electron transport chain efficiency, which results a decline in adenosine triphosphate (ATP) and nicotinamide adenine dinucleotide phosphate (NADPH) consumption in the photosynthesis process and ultimately in quantum yield of PS-II (**Table 1**). The reduction in PS-II quantum yield was more in saltsensitive genotypes under salinity condition [70]. All the physiological and biochemical processes are depending upon the accessibility of water. High salt concentration osmotic and ionic stress which lowers the water potential of wheat plants [71]. Relative water content reduced 3.5% intolerance while 6.7% in sensitive genotypes of wheat after six days of salt stress resulted a drastic decline in water use efficiency [72, 73]. In general, water stress at heading and after the anthesis stage significantly affects the productivity of wheat [74]. Salt sensitive wheat variety HD 2687 showed a higher decrease in chlorophyll content, membrane stability and relative water content under stress compared to Kharchia 65 indicating their salt-tolerant nature [50].

#### **2.4 Mineral uptake**

One of the most severe effects of salinity stress is the accumulation of Na<sup>+</sup> content in leaves over the control condition. A high concentration of Na+ and Cl− ions in root zone reduces the uptake of essential cationic and anionic nutrients like calcium (Ca2+), potassium (K+ ) and nitrate (No3 − ) and decreases the amount of calcium, potassium, phosphorus and magnesium (**Figure 1**) in different plant parts [75, 76]. However, the differential response was seen for Na+ concentration in winter and spring wheat. Winter-type wheat cultivars accumulate high Na<sup>+</sup> than spring type. Slat tolerant genotypes have the better ability to maintain more K<sup>+</sup> and K+ /Na+ ratios and accumulate less Na+ in their leaves [77, 78]. The findings of Hussain et al. [55] showed that the grain yield and tolerance power of wheat can be increased by enhancing Na+ / H+ type antiporter. These antiporters are responsible for the transition of Na + from the cytoplasm to apoplast [79]. Moreover, tolerant genotypes have two pore K+ channels and one selective cation channel for K permeability [80]. Reduced plant growth under salt stress may be due to the high plasma membrane injury due to Na + toxicity [48, 81]. Poor membrane stability due to the replacement of Ca2+ by Na + causes the

influx of heavy metals [82] like Zn2+ and Cu2+. Iron and manganese content were drastically reduced under salinity stress; however, this reduction was lesser in tolerant genotypes (**Table 1**). Salt sensitive cultivars like HD 2687 and WL 711 showed a significant reduction in magnesium, nitrogen, iron, manganese and an increase in zinc and copper. Kharchia 65 gave good performance due to its better nutrient uptake capacity and ion partitioning [53]. Shaaban and El-Nour [83] also reported a significant reduction in nitrogen, potassium, phosphorus, calcium, magnesium, iron, manganese concentration and uptake; this may be due to the increase in osmotic pressure of root when irrigated with saline water.

#### **2.5 Grain yield**

Grain yield in wheat depends on several agronomic and physiological traits such as tillers number, earhead length, size and number of grains, root and shoot length, chlorophyll content, membrane stability and stomatal conductance. Reduction in any of the above-mentioned traits in salt condition directly affect the grain yield of wheat. However, the percent reduction in grain yield depends on the salt concentration and tolerance power of genotypes. Hussain et al. [84] reported significant differences among the 40 genotypes of wheat under salt stress. The sensitive genotypes had fewer yields than tolerant genotypes mainly due to decreased size and number of grains and reduced tillering capacity. The tolerant genotypes produce more productive tillers, the high number of fertile spikelets and have a better capacity of photo-assimilates translocation to developing grains. Less availability of photosynthates and their translocation from source to sink (**Figure 1**) is the main reason for lower grain yield in sensitive genotypes [85, 86]. Salt stress reduced the thousand kernel weight by 20% and starch content of grains by 6% in wheat compared to control condition [87, 88]. Wheat plants grown at high salinity level 10 dSm−1 significantly reduced the spike length by 24%, the number of spikelets by 21%, thousand-grain weight by 70%, straw yield by 20% and grain yield by 67% [89] (**Table 1**). A number of previous studies also reported a significant decline in wheat grain yield with increasing levels of salinity [90–93]. Reduced grain yield under salt stress may be due to low germination percentage and small size and number of medium and small veins in leaves of wheat [94, 95]. As far as the wheat quality is concerned, carbohydrates, proteins, fibers and gluten index in grains declined significantly under salt stress [96]. Salt stress at the grain maturation stage promotes leaf senescence due to which protein deposition takes place in grains over starch [66]. A high reduction in protein content of wheat was observed in wheat than triticale [97].

#### **3. Mechanism of salt stress tolerance**

#### **3.1 Ion homeostasis**

Salinity stress causes an ionic imbalance in wheat by affecting the Na<sup>+</sup> and K<sup>+</sup> concentrations in different plant tissues. A high concentration of Na<sup>+</sup> disturbs the uptake of nutrients like K<sup>+</sup> and Ca2+ causing lesions on different plant parts with declined leaf dry weight and shoot growth. Furthermore, high concentrations of Cl<sup>−</sup> disturb the nutrient uptake by impairing anion uptake. Antagonistic effect of Cl<sup>−</sup> has been observed with nitrate and phosphate [98, 99] causing a reduction in wheat growth and yield. Under salt stress, Na<sup>+</sup> is the major cause of both ionic and osmotic stress. Thus, maintaining ionic homeostasis is very essential for plant growth and

*Insights into Physiological, Biochemical and Molecular Responses in Wheat under Salt Stress DOI: http://dx.doi.org/10.5772/intechopen.102740*

development under salinity stress. Plants maintain the ionic balance of Na<sup>+</sup> and Cl<sup>−</sup> inside the cell by removing excess salts via primary and secondary transport systems and their compartmentalization into vacuole [100]. Na<sup>+</sup> exclusion in plants can be achieved by different ion channels and transporters present in the cell membrane. Apart from being an essential micronutrient, K plays an important role in maintaining a low Na<sup>+</sup> to K<sup>+</sup> ratio. Previous studies in wheat reported a positive association of low Na<sup>+</sup> concentration in leaves with salt tolerance. Yadav et al. [93] reported that salt stress tolerance in wheat was associated with a high K<sup>+</sup> to Na<sup>+</sup> ratio in roots and shoots. Low K<sup>+</sup> to Na<sup>+</sup> ratio in the upper leaves of wheat reduces the plant growth. The high affinity potassium transported (HKT) gene family plays a major role in Na<sup>+</sup> exclusion via minimizing the entry of Na<sup>+</sup> into the roots from the soil [101]. The Nax 1 and Nax 2 genes belonging to the HKT gene gamily were initially identified in durum wheat. These genes exclude the Na<sup>+</sup> from xylem tissues and maintain its low concentration in the leaves. The Nax genes have already been utilized in the breeding program for developing the salt-tolerant genotypes in durum and hexaploid wheat. The presence of the Nax 2 gene in the durum wheat variety produced 25% more grain yield under salt stress conditions. While the presence of both Nax 1and Nax 2 in bread wheat reduces Na<sup>+</sup> concentration by 60% in leaves [102]. Salt tolerance in wheat genotypes can be achieved by down-regulation of TaHKT 2 gene [103].

#### **3.2 Osmotic protection**

Osmotic stress due to high salt concentration reduces the water uptake, cell expansion in roots, growth and development of plants. Likewise, the accumulation of high Na in leaves affects the photosynthesis process which results in leaf chlorosis and necrosis [104]. Osmoprotectants such as sugars e.g. trehalose, sucrose and fructose, amino acids e.g. proline and pipecolic acid, quaternary ammonium compounds e.g. glycine betaine, pipecolate betaine, alanine betaine and hydroxyl pro betaine, polyols e.g. mannitol, sorbitol and inositol and polyamines e.g. spermidine, putrescine and spermine [105] acts as a defensive mechanism in plants by lowering the cell water potential, detoxifying reactive oxygen species, activating anti-oxidants activity and stabilizing normal structures of proteins and enzymes [106–108]. Production of compatible osmolytes in wheat plays an important role in providing tolerance against salt injury. Accumulation of glycine betaine in transgenic lines of wheat improves the salt tolerance by protecting the photosystem II reaction centers and oxygenevolving complex thus enhancing the photosynthetic activity [109]. Salinity stress disrupts the function of the thylakoid membrane which affects the photosynthesis process and ultimately grain yield of wheat. Glycine betaine improves salt tolerance by maintaining ionic balance, increasing osmotic adjustment and neutralizing ROS [110]. Wheat seedlings treated with showed a diminished level of malondialdehyde and an enhanced level of glutathione under salt stress [111]. Exogenous application of glycine betaine increased the activities of antioxidants such as CAT and POD to neutralize ROS damage in wheat [112]. Similarly, proline is the well-known osmolytes produced under salt stress condition [113]. Proline accumulation in wheat generally found in the cytoplasm where it acts as a shield against salt injury. Exogenous application of proline significantly enhanced the root length, seedling fresh and dry weight, photosynthetic pigments and K+ /Na+ ratio and thus efficiently sustains the wheat growth under salt stress [114, 115]. Proline acts as defending agents for electron transport chain and RIBISCO enzyme from salt stress damage and increases the CO2 assimilation rate, chlorophyll content and photosynthetic rate [116]. The sugars help

in the regulation and stabilization of the native structure of proteins and enzymes which enables their normal functioning. These sugars may contribute up to 50% of osmoregulation in leaves of glycophytes. It is reported that galactose plays a major role in ascorbic acid pathways and enhances salt tolerance in wheat [117].

#### **3.3 Antioxidants**

Salinity stress disrupts the availability of CO2 in leaves and electron transport chain in mitochondria and chloroplast due to which reactive oxygen species like singlet of oxygen (1 O2), superoxide radicle (O2 − ), hydroxyl radicle (OH− ) and hydrogen peroxide (H2O2) are produced [118, 119]. Accumulation of these ROS at high concentrations is extremely harmful to plants. Chloroplast, mitochondria and peroxisomes are the primary site of ROS production. Photosystem I and II in chloroplasts, respiratory complex I and III in mitochondria and glycolate oxidase in peroxisomes are the major source of ROS generation [120–123]. ROS cause protein oxidation, lipid peroxidation, damage to nucleic acid, inhibition of enzyme activity and programmed cell death [124]. Lipid peroxidation is caused by the oxidative burst of the cell membrane which can be estimated by the content of malondialdehyde (MDA). Lipid peroxidation increases electrolyte leakage, disturbs membrane permeability and activates the oxidation of protein and DNA. Up to 73% increase in MDA content at 300 mM and 35% increase at 100 mM have been observed when wheat plants exposed to salinity stress [52]. Plants have the natural defense system antioxidant to detoxify the harmful effect of ROS. The enzymatic antioxidants are catalase (CAT), superoxide dismutase (SOD), peroxidase (POX), ascorbate peroxidase (APX), glutathione reductase (GR), glutathione peroxidases (GPX), dehydro-ascorbate reductase (DHAR) and monodehydro-ascorbate reductase (MDHAR) while non-enzymic antioxidants are glutathione (GSH), ascorbate (AsA), tocopherol and carotenoids [124, 125]. Sairam et al. [33] reported an increased concentration of catalase in both salt-tolerant and sensitive cultivars of wheat. Mandhania et al. [126] observed enhanced activity of SOD and CAT in wheat which detoxify H2O2 and break it down as H2O and O2 under salt stress. Tolerant wheat genotypes produced a high concentration of AsA and catalase to counter the effect of salinity in comparison to sensitive genotypes [45]. Likewise, exogenous applications of ferulic acid, caffeic acid and sinapic acid up-regulate the CAT and POX activity in stresses plant of tolerant genotypes. These phenolic acids decrease the H2O2 and MDA content in roots and shoots of both sensitive (cv. HD 2329) and tolerant (cv. Kharchia local) cultivars [57].

#### **4. Approaches for salt stress tolerance**

#### **4.1 Conventional breeding**

Genetic improvement for grain yield, quality traits, biotic stress and abiotic stress including salinity stress are the major breeding objective in wheat. Different methods such as screening of genotypes, pedigree method, hybridization, genetic transformation and marker-assisted breeding have been used in for increasing salt tolerance in wheat. Target breeding for salt stress is mainly done in India and Pakistan. The salt-tolerant genotypes in India are KRL 19, KRL 1–4, KRL 210, KRL 213 and KRL 283 developed by Central Soil Salinity Research Institute, Karnal (India). Almost all the tolerant genotypes in India are developed using Kharchia 65 as donor parent.

*Insights into Physiological, Biochemical and Molecular Responses in Wheat under Salt Stress DOI: http://dx.doi.org/10.5772/intechopen.102740*

Kharchia 65 is collected from Kharchi in Pali district of Rajasthan possessing very high salinity and sodicity tolerance. KRL 1–4 developed in 1990 using the pedigree method from a cross between Kharchia 65 and WL 711 [127]. KRL 19 (PBW 255/ KRL 1–4) which can tolerate salinity up to EC 5–7 dSm−1 was released in 2000. It has yield potential in saline soil is 2.5–3.5 ton ha−1. KRL 210 (PBW 65/2\*Pastor) and KRL 213 (Cndo/r143//Ente/Mexi-2/3 *Aegilops squarrosa* (taus)/4/Weaver/5/2\*Kauz) were released in 2010 with yield potential 3.0–5.0 ton ha−1. KRL 283 (CPAN 3004/ Kharchia 65//PBW 343) was released in 2018 using bulk selection method [128] with yield potential up to 41 q ha−1. Apart from the released variety, genetic stock of salt-tolerant wheat lines i.e. KRL 35, KRL 99 and KRL 3–4 have been registered with NBPGR. Similarly, two varieties LU26S and SARC-1 were developed in Pakistan by Saline Agriculture Research Cell (SARC) at Faisalabad and one variety Sakha 8 was developed in Egypt by Agricultural Research Centre at Giza [128]. KTDH a double haploid line with good Na + exclusion ability was a product of a cross between Kharchia 65 with TW161. This line matured early and performed average under saline conditions of Spain [129].

#### **4.2 Molecular breeding**

Salt stress is a major constraint in wheat production and productivity worldwide. Salt stress causes the accumulation of Na+, Cl<sup>−</sup> ions and reactive oxygen species which disrupts the nutrient uptake, hormonal balance leads to a reduction in growth and development of wheat plants. Salt stress tolerance is a polygenic trait governed by multiple QTLs and interaction effects. Understanding the inheritance pattern of slat tolerance is the major step in developing the improved genotypes for salinity stress. Identification of QTLs with major effects helps in marker-assisted selection of salttolerant wheat genotypes. Several QTLs associated with salt tolerance-related traits have been mapped in wheat. A major QTL for salt tolerance was identified on linkage group 4DL controlling K/Na ratio in wheat [130]. To enhance the salt tolerance capacity, two major Na + exclusion genes Nax 1 and Nax 2 have been introgressed into durum wheat from *Triticum monococcum* [131, 132]. Genetic analysis mapped Nax 1 and Nax 2 locus on the long arm of linkage group 2A and 5A, respectively. Both of the genes were also introgressed into *Triticum aestivum* cv. Westonia from durum wheat and showed reduced Na + concentration in leaves [133]. In a RIL mapping population between Pasban 90 x Frontana, a total 60 QTLs for various physiological traits related to salinity tolerance has been identified on linkage group 1B, 1D, 2A, 2B, 2D, 3A, 3B, 3D, 4A, 4B, 4D, 5A, 5B, 5D, 6A, 6B, 6D, 7A, 7B and 7D. Out of these, one for chlorophyll a, three for proline content, four each for osmotic potential, superoxide dismutase, chloride content, five each for relative water content and water potential, six for membrane stability index, seven for total chlorophyll and eight for chlorophyll b [134]. Low Na+ and high K+ content in leaves is an important cellular mechanism that help the plant to withstand under salt stress condition [73, 135]. For Na content, 3 QTLs were identified by Amin and Diab [136], one by Asif et al. [137], eight by Devi et al. [138], six by Hussain et al. [104], five by Ilyas et al. [134], one by Lindsay et al. [139], four by Masoudi et al. [140] and six by Xu et al. [141]; for K content, four QTLs were detected by Amin and Diab [136], two by Devi et al. [138], five by Hussain et al. [104], four by Ilyas et al. [134], ten by Masoudi et al. [140], and eight by Xu et al. [141]; for K/Na ratio six QTLs were mapped by Amin and Diab [136], two by Asif et al. [137], four by Ilyas et al. [134], twelve by Masoudi et al. [140] and three by Xu et al. [141] (**Table 2**).





**Table 2.**

*QTLs associated with salt tolerance related traits in wheat.*

*Insights into Physiological, Biochemical and Molecular Responses in Wheat under Salt Stress DOI: http://dx.doi.org/10.5772/intechopen.102740*

#### **4.3 Salt-tolerant gens**

One of the approaches to improve salinity tolerance is the identification of genes playing a significant role in the tolerance mechanism. Till now massive information about tolerant gens, transcription factors that are either up-regulated or downregulated have been identified using genomic or trancriptomics approaches. There is increasing evidence for the involvement of dehydrin and expansion proteins, transcription factors like TaSRG, TaMYB2A, TaNAC29, TdERF1 and Sodium antiporter, transporters and vacuolar pyrophosphatase in the salt stress response in wheat [145–147]. Some of the examples of salt-responsive genes are listed in **Table 3**.


#### **Table 3.**

*Genes conferring salt tolerance in wheat.*

These transcription factors can change the gene expression by specific binding in the promoter region of a large number of genes. Rong et al. [146] characterized the function of ethylene response factor TaERF3 and observed that overexpression of TaERF3 improved the salt and drought tolerance in wheat. Electrophoretic mobility shift assay showed that TaERF3 protein interacted with the GCC-box present in the promoters of seven TaERF3-activated stress-related genes, suggesting that TaERF3 positively regulated wheat adaptation responses to salt and drought stress through the activation of stress-related genes. Similarly, Up-regulation of bZIP genes was found insensitive and down-regulation in tolerant cultivar of wheat under salinity stress [158]. Overexpression of TaEXPA2 an -expansin gene of wheat provides salt tolerance in transgenic lines of tobacco. The enhanced salt tolerance was associated with improved relative water content, selective ion absorption and increased antioxidant activity. Moreover, ABA signaling positively participated in regulating theTaEXPA2-enhanced salt stress tolerance but how ABA participates in regulating salt stress tolerance needs to be studied further [157].

## **Author details**

Hari Kesh1 , Sunita Devi1 , Naresh Kumar1 , Ashwani Kumar1 \*, Arvind Kumar1 , Pooja Dhansu2 , Parvender Sheoran1 and Anita Mann1

1 ICAR – Central Soil Salinity Research Institute, Karnal, India

2 ICAR – Sugarcane Breeding Research Institute, Regional Center, Karnal, India

\*Address all correspondence to: ashwani.kumar1@icar.gov.in

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Insights into Physiological, Biochemical and Molecular Responses in Wheat under Salt Stress DOI: http://dx.doi.org/10.5772/intechopen.102740*

#### **References**

[1] FAO. Food Outlook—Biannual Report on Global Food Markets: June 2020. Food Outlook. 2020;**1**. DOI: 10.4060/ca9509en

[2] Nawaz F, Majeed S, Ahmad KS, Hamid A, Shabbir RN, Aqib M, et al. Use of osmolytes in improving abiotic stress tolerance to wheat (*Triticum aestivum* L.). In: Wheat Production in Changing Environments. Singapore: Springer; 2019. pp. 497-519

[3] Asseng S, Ewert F, Martre P, Rötter RP, Lobell DB, Cammarano D, et al. Rising temperatures reduce global wheat production. Nature Climate Change. 2015;**5**:143-147

[4] Qadir M, Quillérou E, Nangia V, Murtaza G, Singh M, Thomas RJ, et al. Economics of salt-induced land degradation and restoration. Natural Resources Forum. 2014;**38**:282-295

[5] Munns R, Gilliham M. Salinity tolerance of crops—What is the cost? The New Phytologist. 2015;**208**:668-673

[6] Kumar A, Sharma SK, Lata C, Devi R, Kulshrestha N, Krishnamurthy SL, et al. Impact of water deficit (salt and drought) stress on physiological, biochemical and yield attributes on wheat (*Triticum aestivum)* varieties. Indian Journal of Agricultural Sciences. 2018;**88**:1624-1632

[7] Datir S, Singh N, Joshi I. Effect of NaCl-induced salinity stress on growth, osmolytes and enzyme activities in wheat genotypes. Bulletin of Environmental Contamination and Toxicology. 2020;**104**:351-357

[8] Soni S, Kumar A, Sehrawat N, Kumar A, Kumar N, Mann A. Effect of saline irrigation on plant water traits,

photosynthesis and ionic balance in durum wheat genotypes. Saudi Journal of Biological Sciences. 2021;**28**:2510-2517

[9] Shoresh M, Spivak M, Bernstein N. Involvement of calcium-mediated effects on ROS metabolism in the regulation of growth improvement under salinity. Free Radical Biology & Medicine. 2011;**51**:1221-1234

[10] Jamshidi GK, Riahi-Madvar A, Rezaee F, Pakzad R, Jadid Bonyad F, Ghazizadeh AM. Effect of salinity stress on enzymes activity, ions concentration, oxidative stress parameters, biochemical traits, content of sulforaphane, and CYP79F1 gene expression level in *Lepidium draba* plant. Journal of Plant Growth Regulation. 2019;**6**:1-20

[11] Szabados L, Savouré A. Proline: A multifunctional amino acid. Trends in Plant Science. 2010;**15**:89-97

[12] Hasanuzzaman M, Alam M, Rahman A, Hasanuzzaman M, Nahar K, Fujita M. Exogenous proline and glycine betaine mediated upregulation of antioxidant defense and glyoxalase systems provides better protection against salt-induced oxidative stress in two rice (*Oryza sativa* L.) varieties. BioMed Research International. 2014:757219

[13] Soni S, Kumar A, Sehrawat N, Lata C, Kumar A, Kumar N, et al. Variability of durum wheat genotypes in terms of physio-biochemical traits against salinity stress. Cereal Research Communications. 2021;**49**:45-54

[14] Sheoran P, Kumar A, Sharma R, Prajapat K, Kumar A, Barman A, et al. Quantitative dissection of salt tolerance for sustainable wheat production

in sodic agro-ecosystems through farmers' participatory approach: An Indian experience. Sustainability. 2021;**13**(6):3378

[15] Arif Y, Singh P, Siddiqui H, Bajguz A, Hayat S. Salinity induced physiological and biochemical changes in plants: An omic approach towards salt stress tolerance. Plant Physiology and Biochemistry. 2020;**156**:64-77. DOI: 10.1016/j.plaphy.2020.08.042

[16] Sharma PC, Kumar A, Mann A. Physiology of salinity tolerance in Crop plants. In: Minhas PS, Yadav RK, Sharma PC, editors. Managing Soil Salinity. Karnal: ICAR; 2021. pp. 331-356

[17] Luo MB, Liu F. Salinity-induced oxidative stress and regulation of antioxidant defense system in the marine macroalga *Ulva Prolifera*. Journal of Experimental Marine Biology and Ecology. 2011;**409**:223-228

[18] Sairam RK, Srivastava GC. Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Science. 2002;**162**:897-904

[19] Goudarzi M, Pakniyat H. Salinity causes increase in proline and protein contents and peroxidase activity in wheat cultivars. Journal of Applied Sciences. 2009;**9**(2):348-353

[20] Woodrow P, Ciarmiello LF, Annunziata MG, Pacifico S, Iannuzzi F, Mirto A, et al. Durum wheat seedling responses to simultaneous high light and salinity involve a fine reconfiguration of amino acids and carbohydrate metabolism. Physiologia Plantarum. 2017;**159**:290-312

[21] Alzahrani O, Abouseadaa H, Abdelmoneim TK, Alshehri MA, Mohamed EM, El-Beltagi HS, et al. Agronomical, physiological and molecular evaluation reveals superior salt-tolerance in bread wheat through salt-induced priming approach. Notulae Botanicae Horti Agro botanici Cluj-Napoca. 2021;**49**:12310-12310

[22] Rahman MA, Chikushi J, Yoshida S, Yahata H, Yasunaga E. Effect of high air temperature on grain growth and yields of wheat genotypes differing in heat tolerance. Journal of Agricultural Meteorology. 2005;**60**:605-608

[23] Chahine K, Sourour A, Youssef T, Hajer S. Salinity effect on plant growth at the seedling stage of durum wheat (*Triticum durum Desf*.). Journal of Plant Breeding and Crop Science. 2013;**5**:20-25

[24] Rahman A, Nahar K, Hasanuzzaman M, Fujita M. Calcium supplementation improves Na<sup>+</sup> /K+ ratio, antioxidant defense and glyoxalase systems in salt-stressed rice seedlings. Frontiers in Plant Science. 2016;**7**:609. DOI: 10.3389/fpls.2016.00609

[25] Weitbrecht K, Müller K, Leubner MG. First off the mark: Early seed germination. Journal of Experimental Botany. 2011;**62**(10):3289-3309

[26] Chamorro D, Luna B, Ourcival JM, Kavgac A, Sirca C, Mouillot F, et al. Germination sensitivity to water stress in four shrubby species across the Mediterranean Basin. Plant Biology. 2017;**19**:23-31. DOI: 10.1111/plb.12450

[27] Kumari A, Kaur R. Evaluation of benzyl-butyl phthalate induced germination and early growth vulnerability to barley seedlings (Hordeumvulgare L.). Indian Journal of Ecology. 2018;**45**:174-177

[28] Hasanuzzaman M, Nahar K, Fujita M, Ahmad P, Chandna R, et al. *Insights into Physiological, Biochemical and Molecular Responses in Wheat under Salt Stress DOI: http://dx.doi.org/10.5772/intechopen.102740*

Enhancing plant productivity under salt stress: Relevance of poly-omics. In: Ahmad P, Azooz MM, Prasad MNV, editors. Salt Stress in Plants: Omics, Signaling and Responses. Berlin, Germany: Springer; 2013. pp. 113-156. DOI: 10.1007/978-1-4614-6108-1\_6

[29] Wahid A, Farooq M, Basra SMA, Rasul E, Siddique KHM. Germination of seeds and propagules under salt stress. In: Pessarakli M, editor. Handbook of Plant and Crop Stress. 3rd ed. Boca Raton: CRC Press; 2011. pp. 321-337

[30] Beisson F, Li Y, Bonaventure G, Mike P, Ohlrogge JB. The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. Plant Cell. 2007;**19**:351-368. DOI: 10.1105/tpc.106.048033

[31] Yang XJ, Baskin J, Baskin CC, Huang ZY. More than just a coating: Ecological importance, taxonomic occurrence and phylogenetic relationships of seed coat mucilage. Perspectives in Plant Ecology. 2012;**14**:434-442. DOI: 10.1016/j. ppees.2012.09.002

[32] Akbarimoghaddam H, Galavi M, Ghanbari A, Panjehkeh N. Salinity effects on seed germination and seedling growth of bread wheat cultivars. Trakia Journal of Sciences. 2011;**9**:43-50

[33] Sairam RK, Rao KV, Srivastava GC. Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Science. 2002;**163**:1037-1046. DOI: 10.1016/ S0168-9452(02)00278-9

[34] Badridze G, Weidner A, Asch F, Börner A. Variation in salt tolerance within a Georgian wheat germplasm collection. Genetic Resources and Crops Evolution. 2009;**56**:1125-1130

[35] Kandil A, Sharief A, Elokda M. Germination and seedling characters of different wheat cultivars under salinity stress. Journal of Basic & Applied Sciences. 2012;**8**:585-596

[36] Charushahi V, Bargali K, Bargali SS. Influence of seed size and salt stress on seed germination and seedling growth of wheat (*Triticum aestivum*). Indian Journal of Agricultural Sciences. 2015;**85**(9):1134-1137

[37] Alwan AA, Hussein KA, Jaddoa KA. Effect of sodium chloride on response of two wheat cultivars (*Triticum aestivum* L.) at germination and early seedling stages. International Journal of Applied Agricultural Sciences. 2015;**1**:60-65

[38] Goyal E, Amit SK, Singh RS, Mahato AK, Chand S. Transcriptome profiling of the salt-stress response in *Triticum aestivum* cv. Kharchia Local. Scientific Reports. 2016;**6**:1-14

[39] Ahmed IM, Cao F, Zhang M, Chen X, Zhang G, Wu F. Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys. PLoS One. 2013;**8**:e77869. DOI: 10.1371/journal. pone.0077869

[40] Bacilio M, Rodriguez H, Moreno M, Hernandez JP, Bashan Y. Mitigation of salt stress in wheat seedlings by a gfptagged *Azospirillum lipoferum*. Biology and Fertility of Soils. 2004;**40**:188-193

[41] El-Hendawy SE, Ruan Y, Hu Y, Schmidhalter U. A comparison of screening criteria for salt tolerance in wheat under field and environment controlled conditions. Journal of Agronomy and Crop Science. 2009;**49**:1-9

[42] Bera AK, Pati MK, Bera A. Bassionolide ameliorates adverse effect on salt stress on germination and seedling growth of rice. Indian Journal of Plant Physiology. 2006;**11**:182-189

[43] Otu H, Celiktas V, Duzenli S, Hossain A, El Sabagh A. Germination and early seedling growth of five durum wheat cultivars (*Triticum durum* Desf.) is affected by different levels of salinity. Fresenius Environmental Bulletin. 2018;**27**:7746-7757

[44] Guo R, Yang Z, Li F, Yan C, Zhong X, et al. Comparative metabolic responses and adaptive strategies of wheat (*Triticum aestivum* L.) to salt and alkali stress. BMC Plant Biology. 2015;**15**:170. DOI: 10.1186/s12870-015-0546-x

[45] Athar HUR, Khan A, Ashraf M. Exogenously applied ascorbic acid alleviates salt-induced oxidative stress in wheat. Environmental and Experimental Botany. 2007;**63**:224-231. DOI: 10.1016/j. envexpbot.2007.10.018

[46] Afzal I, Rauf S, Basra SMA, Murtaza G. Halopriming improves vigor, metabolism of reserves and ionic contents in wheat seedlings under salt stress. Plant, Soil and Environment. 2008;**54**:382-388

[47] Datta JK, Nag S, Banerjee A, Mondal NK. Impact of salt stress on five varieties of Wheat (*Triticum aestivum* L.) cultivars under laboratory condition. Journal of Applied Sciences and Environmental Management. 2009;**13**:93-97

[48] Saddiq MS, Iqbal S, Hafeez MB, Ibrahim AM, Raza A, et al. Effect of salinity stress on physiological changes in winter and spring wheat. Agronomy. 2021;**11**:4. DOI: 10.3390/ agronomy11061193

[49] Poustini K, Siosemardeh A. Ion distribution in wheat cultivars in

response to salinity stress. Field Crops Research. 2004;**85**:25-133

[50] Sairam RK, Srivastava GC, Agarwal S, Meena RC. Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biologia Plantarum. 2005;**49**:85-91

[51] Wahid A, Perveen M, Gelani S, Basra SMA. Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. Journal of Plant Physiology. 2007;**164**:283-294. DOI: 10.1016/j. jplph.2006.01.005

[52] Hasanuzzaman M, Hossain MA, Fujita M. Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnology Reports. 2011;**5**:353-365. DOI: 10.1007/ s11816-011-0189-9

[53] Lekshmy S, Sairam RK, Kushwaha SR. Effect of long-term salinity stress on growth and nutrient uptake in contrasting wheat genotypes. Indian Journal of Plant Physiology. 2013;**18**:344-353

[54] Qiu Z, Guo J, Zhu A, Zhang L, Zhang M. Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicology and Environmental Safety. 2014;**104**:202-208

[55] Hussain B, Khan AS, Ali Z. Genetic variation in wheat germplasm for salinity tolerance at seedling stage: Improved statistical inference. Turkish Journal of Agriculture and Forestry. 2015;**39**:182-192

[56] Tian F, Wang W, Liang C, Wang X, Wang G, Wang W. Overaccumulation

*Insights into Physiological, Biochemical and Molecular Responses in Wheat under Salt Stress DOI: http://dx.doi.org/10.5772/intechopen.102740*

of glycine betaine makes the function of the thylakoid membrane better in wheat under salt stress. The Crop Journal. 2016;**174**:1-10

[57] Kaur H, Bhardwaj RD, Grewal SK. Mitigation of salinity-induced oxidative damage in wheat (*Triticum aestivum* L.) seedlings by exogenous application of phenolic acids. Acta Physiologiae Plantarum. 2017;**39**:1-15

[58] Sadak MS. Physiological role of trehalose on enhancing salinity tolerance of wheat plant. Bulletin of the National Research Centre. 2019;**43**:1-10. DOI: 10.1186/s42269-019-0098

[59] Liu X, Chen D, Yang T, Huang F, Fu S, Li L. Changes in soil labile and recalcitrant carbon pools after land-use change in a semi-arid agro-pastoral ecotone in Central Asia. Ecological Indicators. 2020;**110**:105925. DOI: 10.1016/j.ecolind.2019.105925

[60] Mohsin SM, Hasanuzzaman M, Parvin K, Fujita M. Pretreatment of wheat (*Triticum aestivum* L.) seedlings with 2, 4-D improves tolerance to salinity-induced oxidative stress and methylglyoxal toxicity by modulating ion homeostasis, antioxidant defenses, and glyoxalase systems. Plant Physiology and Biochemistry. 2020;**152**:221-231

[61] Nassar R, Kamel HA, Ghoniem AE, Alarcón JJ, Sekara A, et al. Physiological and anatomical mechanisms in wheat to cope with salt stress induced by seawater. Plants. 2020;**9**:237. DOI: 10.3390/ plants9020237

[62] Cuong DM, Kwon SJ, Nguyen BV, Chun SW, Kim JK, Park SU. Effect of salinity stress on phenyl propanoid genes expression and related gene expression in wheat sprout. Agronomy. 2020;**10**:390

[63] Ashraf M, Harris PJC. Photosynthesis under stressful environments:

An overview. Photosynthetica. 2013;**51**:163-190. DOI: 10.1007/ s11099-013-0021-6(2013)

[64] Chookhampaeng S. The effect of salt stress on growth, chlorophyll content proline content and antioxidative enzymes of pepper (*Capsicum annuum* L.) seedling. European Journal of Scientific Research. 2011;**49**:103-109

[65] Abedini M. Physiological responses of wheat plant to salinity under different concentrations of Zn. Acta Biologica Szegediensis. 2016;**60**:9-16

[66] Fernandez-Figares I, Marinetto J, Royo C, Ramos JM, Del Moral LG. Amino-acid composition and protein and carbohydrate accumulation in the grain of triticale grown under terminal water stress simulated by a senescing agent. Journal of Cereal Science. 2000;**32**:249-258. DOI: 10.1006/ jcrs.2000.0329

[67] Shafi M, Zhang G, Bakht J, Khan MA, Islam UE, Khan MD, et al. Effect of cadmium and salinity stresses on root morphology of wheat. Pakistan Journal of Botany. 2010;**42**:2747-2754

[68] Kafi M. The effects of salinity and light on photosynthesis, respiration and chlorophyll fluorescence in salt-tolerant and salt sensitive wheat (*Triticum aestivum* L.) cultivars. Journal of Agricultural Science and Technology. 2009;**11**:535-547

[69] Chen TH, Murata N. Glycine betaine protects plants against abiotic stress: Mechanisms and biotechnological applications. Plant, Cell and Environment. 2011;**34**:1-20

[70] El-Hendawy SE, Hassan WM, Al-Suhaibani NA, et al. Comparative performance of multivariable agrophysiological parameters for detecting salt tolerance of wheat cultivars under simulated saline field growing conditions. Frontiers in Plant Science. 2017;**8**:435

[71] Qamar H, Ilyas M, Jan SA, Mustafa HSB, Arshad A, Yar MS, et al. Recent trends in molecular breeding and biotechnology for the genetic improvement of Brassica species against drought stress. Fresenius Environmental Bulletin. 2020;**29**:19-25

[72] Zhang X, Shi Z, Tian Y, Zhou Q, Cai J, Dai T, et al. Salt stress increases content and size of gluten in macropolymers in wheat grain. Food Chemistry. 2016;**197**:516-521. DOI: 10.1016/j.foodchem.2015.11.008

[73] Gil-Muñoz F, Pérez-Pérez JG, Quiñones A, Primo-Capella A, Cebolla J, Ángeles Forner-Giner M, et al. A cross population between D. Kaki and D. Virginiana shows high variability for saline tolerance and improved salt stress tolerance. Plos One. 2020;**15**:e0229023. DOI: 10.1371/journal.pone.0229023

[74] Barutcular C, Yildirim M, Koc M, Akinci C, Topta I, Albayrak O, et al. Evaluation of SPAD chlorophyll in spring wheat genotypes under different environments. Fresenius Environmental Bulletin. 2016;**25**:1258-1266

[75] Munns R. Comparative physiology of salt and water stress. Plant, Cell and Environment. 2002;**25**:239-250

[76] Esechie HA, Al-Saidi A, Al-Khanjari S. Effect of sodium chloride salinity on seedling emergence in chickpea. Journal of Agronomy and Crop Science. 2002;**188**:155-160

[77] Saddiq MS, Afzal I, Basra SM, Ali Z, Ibrahim AM. Sodium exclusion is a reliable trait for the improvement of salinity tolerance in bread wheat.

Archives of Agronomy and Soil Science. 2018;**64**:272-284

[78] Elkelish AA, Soliman MH, Alhaithloul HA, El-Esawi MA. Selenium protects wheat seedlings against salt stress-mediated oxidative damage by up-regulating antioxidants and osmolytes metabolism. Plant Physiology and Biochemistry. 2019;**137**:144-153

[79] Munns R, Tester M. Mechanism of salinity tolerance. Annual Review of Plant Biology. 2008;**59**:651- 681. DOI: 10.1146/annurev. arplant.59.032607.092911

[80] Shabala S, Pottosin I. Regulation of potassium transport in plants under hostile conditions: Implications for abiotic and biotic stress tolerance. Physiologia Plantarum. 2014;**151**:257-279

[81] Loutfy N, Sakuma Y, Gupta DK. Modifications of water status, growth rate and antioxidant system in two wheat cultivars as affected by salinity stress and salicylic acid. Journal of Plant Research. 2020;**133**:549-570

[82] Di Donato RJ, Roberts LA, Sanderson T, Eisley RB, Walker EL. Arabidopsis yellow stripe-like 2 (YSL2): A metal-regulated gene encoding a plasma membrane transporter of nicotianamine–metal complexes. The Plant Journal. 2004;**39**:403-414

[83] Shaaban Mahmoud M, Abou El-Nour EAA. Nutritional status and growth of wheat plants grown under salinity stress conditions as responded to different nitrogen sources. American Journal of Plant Physiology. 2013;**8**:32-40

[84] Hussain S, Hussain S, Ali B, Ren X, Chen X, et al. Recent progress in understanding salinity tolerance in plants: Story of Na<sup>+</sup> /K+ balance and beyond. Plant Physiology and

*Insights into Physiological, Biochemical and Molecular Responses in Wheat under Salt Stress DOI: http://dx.doi.org/10.5772/intechopen.102740*

Biochemistry. 2021;**160**:250-256. DOI: 10.1016/j.plaphy.2021.01.029

[85] Arfan M, Athar HR, Ashraf M. Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in differently adapted spring wheat cultivated under salt stress. Journal of Plant Physiology. 2007;**6**:685-694

[86] Dugasa T, Abebie B, Tomer RPS, Barnabas J. Tolerance of *Triticum aestivum* L. (Bread wheat) varieties for growth yield in high salinity soils of Ethiopia. International Journal of Science and Research. 2016;**5**:139-153

[87] Dadshani S, Sharma RC, Baum M, Ogbonnaya FC, Léon J, Ballvora A. Multidimensional evaluation of response to salt stress in wheat. PLoS One. 2019;**14**:e0222659. DOI: 10.1371/journal. pone.0222659

[88] Jamal Y, Shafi M, Bakht J, Arif M. Seed priming improves salinity tolerance of wheat varieties. Pakistan Journal of Botany. 2011;**43**:2683-2686

[89] Kalhoro NA, Rajpar I, Kalhoro SA, Ali A, Raza S, Ahmed M, et al. Effect of salts stress on the growth and yield of wheat (Triticumaestivum L.). American Journal of Plant Sciences. 2016;**7**:2257-2271

[90] Chinnusamy V, Jagendorf A, Zhu JK. Understanding and improving salt tolerance in plants. Crop Science. 2005;**45**:437-448. DOI: 10.2135/ cropsci2005.0437

[91] Asgari HR, Cornelis W, Damme PV. Salt stress effect on wheat (*Triticum aestivum* L.). growth and leaf ion concentrations. International Journal of Plant Production. 2012;**6**:195-208

[92] Afzal I, Basra SMA, Cheema MA, Farooq M, Jafar MZ, Shahid M, et al.

Seed priming: A shotgun approach for alleviation of salt stress in wheat. International Journal of Agriculture and Biology. 2013;**15**:1199-1203

[93] Yadav S, Solanki YPS, Singh V, Yashveer S, Kesh H. Assessment of diversity for yield and its component traits in F2 population of wheat (*Triticum aestivum* L.) under salinity conditions. Applied Biological Research. 2018;**20**:256-261

[94] Singh KN, Chatrath R. Salinity tolerance. In: Reynolds MP, Ortiz-Monasterio JJ, McNab A, editors. Application of Physiology in Wheat Breeding. Mexico: CIMMYT; 2001. pp. 101-110

[95] Hu YC, Schmidhalter U. Drought and salinity. A comparison of their effects on mineral nutrition of plants. Journal of Plant Nutrition and Soil Science. 2007;**168**:541-549

[96] Katerji N, Van Hoorn JW, Fares C, Hamdy A, Mastrorilli M, Oweis T. Salinity effect on grain quality of two durum wheat varieties differing in salt tolerance. Agricultural Water Management. 2005;**75**:85-91

[97] Darvey NL, Naeem H, Gustafson JP. Triticale: Production and utilization. In: Klup K, Ponte J, editors. Handbook of Cereal Science and Technology. 2nd ed. New York: Marcel Dekker; 2000

[98] Abdelgadir EM, Oka M, Fujiyama H. Characteristics of nitrate uptake by plants under salinity. Journal of Plant Nutrition. 2005;**28**:33-46. DOI: 10.1081/PLN-200042156

[99] Massa D, Mattson NS, Lieth HJ. Effects of saline root environment (NaCl) on nitrate and potassium uptake kinetics for rose plants: A Michaelis– Menten modelling approach. Plant and

Soil. 2009;**318**:101-115. DOI: 10.1007/ s11104-008-9821-z

[100] Li J, Li X, Guo L, Lu F, Feng X, He K, et al. A subgroup of MYB transcription factor genes undergoes highly conserved alternative splicing in Arabidopsis and rice. Journal of Experimental Botany. 2006;**57**:1263-1273

[101] Tester M, Davenport R. Na<sup>+</sup> tolerance and Na+ transport in higher plants. Annals of Botany. 2003;**91**:503e527

[102] James RA, Davenport RJ, Munns R. Physiological characterization of two genes for Na<sup>+</sup> exclusion in durum wheat, Nax1 and Nax21. Plant Physiology. 2006;**142**:1537-1547. DOI: 10.1104/ pp.106.086538

[103] Singh A, Bhushan B, Gaikwad K, Yadav OP, Kumar S, Rai RD. Induced defence responses of contrasting bread wheat genotypes under differential salt stress imposition. Indian Journal of Biochemistry & Biophysics. 2015;**52**:75-85

[104] Hussain B, Lucas SJ, Ozturk L, Budak H. Mapping QTLs conferring salt tolerance and micronutrient concentrations at seedling stage in wheat. Scientific Reports. 2017;**7**:15662

[105] Wang Y, Nii N. Changes in chlorophyll, ribulosebisphosphate carboxylase-oxygenase, glycine betaine content, photosynthesis and transpiration in *Amaranthus tricolor* leaves during salt stress. The Journal of Horticultural Science and Biotechnology. 2000;**75**:623-627. DOI: 10.1080/14620316.2000.11511297

[106] Bose J, Rodrigo-Moreno A, Shabala S. ROS homeostasis in halophytes in the context of salinity stress tolerance. Journal of Experimental Botany. 2014;**65**:1241-1257. DOI: 10.1093/ jxb/ert430

[107] Blum A. Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant, Cell and Environment. 2017;**40**:4e10

[108] Farooq M, Nawaz A, Chaudhry MAM, Indrasti R, Rehman A. Improving resistance against terminal drought in bread wheat by exogenous application of proline and gammaaminobutyric acid. Journal of Agronomy and Crop Science. 2017;**203**:464-472

[109] Tian F, Wang W, Liang C, Wang X, Wang G, Wang W. Over accumulation of glycine betaine makes the function of the thylakoid membrane better in wheat under salt stress. The Crop Journal. 2017;**5**(1):73-82

[110] Liang C, Zhang XY, Luo Y, Wang GP, Zou Q, Wang W. Over accumulation of glycine betaine alleviates the negative effects of salt stress in wheat. Russian Journal of Plant Physiology. 2009;**56**(3):370-376

[111] Salama KH, Mansour MMF, Al-Malawi HA. Glycinebetaine priming improves salt tolerance of wheat. Biologia. 2015;**70**:1334-1339

[112] Raza SH, Athar HR, Ashraf M, Hameed A. Glycine betaine-induced modulation of antioxidant enzymes activities and ion accumulation in two wheat cultivars differing in salt tolerance. Environmental and Experimental Botany. 2007;**60**:368-376

[113] Rady MM, Kuşvuran A, Alharby HF, Alzahrani Y, Kuşvuran S. Pretreatment with proline or an organic bio-stimulant induces salt tolerance in wheat plants by improving antioxidant redox state and enzymatic activities and reducing the oxidative stress. Journal of Plant Growth Regulation. 2019;**38**:449-462

*Insights into Physiological, Biochemical and Molecular Responses in Wheat under Salt Stress DOI: http://dx.doi.org/10.5772/intechopen.102740*

[114] Ashraf M, Foolad MR. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany. 2007;**59**:206-216. DOI: 10.1016/j. envexpbot.2005.12.006

[115] Mahboob W, Khan MA, Shirazi MU. Induction of salt tolerance in wheat (*Triticum aestivum* L.) seedlings through exogenous application of proline. Pakistan Journal of Botany. 2016;**48**:861-867

[116] Hamilton EW, Heckathorn SA. Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiology. 2001;**126**:1266-1274

[117] Darko E, Gierczik K, Hudak O, Forgo P, Pal M, Turkosi E, et al. Differing metabolic responses to salt stress in wheat-barley addition lines containing different 7H chromosomal fragments. PLoS One. 2017;**12**:1-20. DOI: 10.1371/ journal.pone.0174170

[118] Farissi M, Aziz F, Bouizgaren A, Ghoulam C. Legume-rhizobia symbiosis under saline conditions: Agrophysiological and biochemical aspects of tolerance. International Journal of Innovative Science and Research. 2014;**11**:96-104

[119] Navarro-Yepes J, Burns M, Anandhan A, Khalimonchuk O, Del Razo LM, Quintanilla-Vega B, et al. Oxidative stress, redox signaling, and autophagy: Cell death versus survival. Antioxidants and Redox Signaling. 2014;**21**:66-85. DOI: 10.1089/ ars.2014.5837

[120] Huang S, Van Aken O, Schwarzländer M, Belt K, Millar AH. The roles of mitochondrial reactive oxygen

species in cellular signaling and stress responses in plants. Plant Physiology. 2016;**171**:1551-1559

[121] Kerchev P, Waszczak C, Lewandowska A, Willems P, Shapiguzov A, Li Z. Lack of *GLYCOLATE OXIDASE1*, but not *GLYCOLATE OXIDASE2*, attenuates the photorespiratory phenotype of CATALASE2- deficient Arabidopsis. Plant Physiology. 2016;**171**:1704-1719

[122] Singh A, Kumar A, Yadav S, Singh IK. Reactive oxygen species-mediated signaling during abiotic stress. Plant Gene. 2019;**18**:100-173

[123] Hasanuzzaman M, Bhuyan M, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, et al. Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator. Antioxidants. 2020;**9**:681

[124] Hossain MA, Hoque TS, Zaid A, Wani SH, Mostofa MG, Henry R. Targeting the ascorbate-glutathione pathway and the glyoxalase pathway for genetic engineering of abiotic stress-tolerance in rice. In: Hossain MA, Hassan KM, Iftekharuddaula A, Kumar A, Henry R, editors. Molecular Breeding for Rice Abiotic Stress Tolerance and Nutritional Quality. Hoboken, NJ: Wiley-Blackwell; 2021. pp. 398-427. DOI: 10.1002/9781119633174.ch21

[125] Sachdev S, Ansari SA, Ansari MI, Fujita M, Hasanuzzaman M. Abiotic stress and reactive oxygen species: Generation, signaling, and defense mechanisms. Antioxidants. 2021;**10**:277

[126] Mandhania S, Madan S, Sawhney V. Antioxidant defense mechanism under salt stress in wheat seedlings. Biologia Plantarum. 2006;**50**:227-231

[127] Hollington PA. Technological breakthroughs in screening/breeding wheat varieties for salt tolerance. In: Proceedings of the National Conference 'Salinity Management in Agriculture. Karnal, India: CSSRI; 2000. pp. 273-289

[128] Sharma SK. Success Stories on Development, Spread and Impact of Salt-Tolerant Varieties of Rice, Wheat and Mustard in India. Karnal: Central Soil Salinity Research Institute; 2010

[129] Hollington PA, Royo A, Miller TE, Quarrie SA, Mahmood A, et al. The use of doubled haploid breeding techniques to develop wheat varieties for saline areas. In: Proceedings of the 3rd Congress of the European Society of Agronomy. Netherlands; 1994. pp. 156-157

[130] Dubcovsky J, María GS, Epstein E, Luo MC, Dvořák J. Mapping of the K+ / Na+ discrimination locus Kna1 in wheat. Theoretical and Applied Genetics. 1996;**92**:448-454

[131] Munns R, James RA. Screening methods for salinity tolerance: A case study with tetraploid wheat. Plant and Soil. 2003;**253**:201-218

[132] James RA, Munns R, Von Caemmerer S, Trejo C, Miller C, Condon T. Photosynthetic capacity is related to the cellular and subcellular partitioning of Na+ , K+ and Cl− in salt-affected barley and durum wheat. Plant, Cell and Environment. 2006;**29**:2185-2197. DOI: 10.1111/j.1365-3040.2006.01592.x

[133] James RA, Blake C, Byrt CS, Munns R. Major genes for Na<sup>+</sup> exclusion, *Nax1* and *Nax2* (wheat *HKT1; 4* and *HKT1; 5*) decrease Na+ accumulation in bread wheat leaves under saline and waterlogged conditions. Journal of Experimental Botany. 2011;**62**:2939-2947. DOI: 10.1093/jxb/err003

[134] Ilyas N, Amjid MW, Saleem MA, Khan W, Wattoo FM, Rana RM, et al. Quantitative trait loci (QTL) mapping for physiological and biochemical attributes in a Pasban90/Frontana recombinant inbred lines (RILs) population of wheat (*Triticum aestivum*) under salt stress condition. Saudi Journal of Biological Sciences. 2020;**27**:341-351

[135] Mbarki S, Sytar O, Zivcak M, et al. Anthocyanins of coloured wheat genotypes in specific response to salt stress. Molecules. 2018;**23**:1518

[136] Amin AYMAN Y, Diab AA. QTL mapping of wheat (Triticumaestivum L.) in response to salt stress. International Journal of Bio Technology and Research. 2013;**3**:47-60

[137] Asif MA, Garcia M, Tilbrook J, Brien C, Dowling K, Berger B, et al. Identification of salt tolerance QTL in a wheat RIL mapping population using destructive and non-destructive phenotyping. Functional Plant Biology. 2021;**48**:131-140

[138] Devi R, Ram S, Rana V, Malik VK, Pande V, Singh GP. QTL mapping for salt tolerance associated traits in wheat (*Triticum aestivum* L.). Euphytica. 2019;**215**:1-23

[139] Lindsay MP, Lagudah ES, Hare RA, Munns R. A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Functional Plant Biology. 2004;**31**:1105-1114. DOI: 10.1071/FP04111

[140] Masoudi B, Mardi M, Hervan EM, et al. QTL mapping of salt tolerance traits with different effects at the seedling stage of bread wheat. Plant Molecular Biology Reporter. 2015;**33**:1790-1803. DOI: 10.1007/s11105-015-0874-x

[141] Xu YF, An DG, Liu DC, et al. Mapping QTLs with epistatic effects *Insights into Physiological, Biochemical and Molecular Responses in Wheat under Salt Stress DOI: http://dx.doi.org/10.5772/intechopen.102740*

and QTL 9 treatment interactions for salt tolerance at seedling stage of wheat. Euphytica. 2012;**186**:233-245. DOI: 10.1007/s10681-012-0647-7

[142] Batool N, Ilyas N, Shahzad A, Hauser BA, Arshad M. Quantitative trait loci (QTLs) mapping for salt stress tolerance in wheat at germination stage. Pakistan Journal of Agricultural Sciences. 2018;**55**:47-55

[143] Ghaedrahmati M, Mardi M, Naghavi MR, et al. Mapping QTLs associated with salt tolerance related traits in seedling stage of wheat (*Triticum aestivum* L.). Journal of Agricultural Science and Technology. 2014;**16**:1413-1428

[144] Ma L, Fengzhou E, Huo N. Genetic analysis of salt tolerance in a recombination inbred population of wheat. Euphytica. 2007;**153**:109-117

[145] Mao X, Jia D, Li A, Zhang H, Tian S, Zhang X, et al. Transgenic expression of TaMYB2A confers enhanced tolerance to multiple abiotic stresses in Arabidopsis. Functional and Integrative Genomics. 2011;**11**:445-465

[146] Rong W, Qi L, Wang A, Ye X, Du L, Liang H, et al. The ERF transcription factor Ta ERF 3 promotes tolerance to salt and drought stresses in wheat. Plant Biotechnology Journal. 2014;**12**:468-479

[147] Makhloufi E, Yousfi FE, Pirrello J, Bernadac A, Ghorbel A, Bouzayen M. TdERF1, an ethylene response factor associated with dehydration responses in durum wheat (*Triticum turgidum* L. subsp. durum). Plant Signaling and Behaviour. 2015;**10**(10):e1065366

[148] Brini F, Hanin M,

Mezghani I, Berkowitz GA, Masmoudi K. Overexpression of wheat Na+ /H+ antiporter TNHX1 and H+-pyrophosphatase

TVP1 improve salt-and drought-stress tolerance in Arabidopsis thaliana plants. Journal of Experimental Botany. 2007;**58**:301-308

[149] Khoudi H, Nouri-Khemakhem A, Gouiaa S, Masmoudi K. Optimization of regeneration and transformation parameters in tomato and improvement of its salinity and drought tolerance. African Journal of Biotechnology. 2009;**8**(22)

[150] Zhou W, Li Y, Zhao BC, Ge RC, Shen YZ, Wang G, et al. Overexpression of TaSTRG gene improves salt and drought tolerance in rice. Journal of Plant Physiology. 2009;**166**:1660-1671

[151] Huang X, Zhang Y, Jiao B, Chen G, Huang S, Guo F, et al. Overexpression of the wheat salt tolerance-related gene TaSC enhances salt tolerance in Arabidopsis. Journal of Experimental Botany. 2012;**63**:5463-5473

[152] Han Y, Xiu Li A, Li F, Rong ZM, Wang W. Characterization of a wheat (*Triticum aestivum* L.) expansin gene, TaEXPB23, involved in the abiotic stress response and phytohormone regulation. Plant Physiology and Biochemistry. 2012;**54**:49-58

[153] Xu Z, Wang C, Xue F, Zhang H, Ji W. Wheat NAC transcription factor TaNAC29 is involved in response to salt stress. Plant Physiology and Biochemistry. 2015;**96**:356-363

[154] Gouiaa S, Khoudi H. Co-expression of vacuolar Na<sup>+</sup> /H+ antiporter and H+ -pyrophosphatase with an IRESmediated dicistronic vector improves salinity tolerance and enhances potassium biofortification of tomato. Phytochemistry. 2015;**117**:537-546

[155] Zaidi I, Ebel C, Belgaroui N, Ghorbel M, Amara I, Hanin M. The wheat MAP kinase phosphatase 1 alleviates salt stress and increases antioxidant activities in Arabidopsis. Journal of Plant Physiology. 2016;**193**:12-21

[156] Zhang M, Zhang GQ, Kang HH, Zhou SM, Wang W. TaPUB1, a putative E3 ligase gene from wheat, enhances salt stress tolerance in transgenic *Nicotiana benthamiana*. Plant & Cell Physiology. 2017;**58**:1673-1688

[157] Chen Y, Han Y, Kong X, Kang H, Ren Y, Wang W. Ectopic expression of wheat expansin gene TaEXPA2 improved the salt tolerance of transgenic tobacco by regulating Na<sup>+</sup> /K+ and antioxidant competence. Physiologia Plantarum. 2017;**159**(2):161-177

[158] Johnson RR, Wagner RL, Verhey SD, Walker-Simmons MK. The abscisic acid-responsive kinase PKABA1 interacts with a seed-specific abscisic acid response element-binding factor, TaABF, and phosphorylates TaABF peptide sequences. Plant Physiology. 2002;**130**:837-846

#### **Chapter 11**
