Advances in Crop Science and Technology
Open Access

Osmoprotectants; Abiotic stress; Drought; Salinity; Amino acid; Carbohydrate; Polyamine; Polyol

Introduction

Plant diversity, production, and distribution are all influenced by environmental stressors. Unfavorable environmental circumstances hinder plants’ ability to grow, develop, and reproduce. Worldwide, key environmental factors that limit plant productivity include salinity, water scarcity, water logging, toxic and inadequate nutrient levels, and cold or hot conditions. Low quality irrigation water, poor cultural practices, frequent drought conditions, unpredictable weather, and overall climate change are the main causes of environmental stresses. These environmental stress factors lead to low agricultural productivity of lands and food insecurity, particularly in developing countries. The ability of plants to employ their numerous defensive mechanisms effectively determines how long they will survive these pressures. According to Khan et al. (2012) and Sharma et al. (2016), abiotic stressors inhibit plant growth through influencing a variety of biochemical and physiological processes, including photosynthesis, antioxidant systems, and hormone signaling. Plants respond intricately to these environmental pressures in order to protect themselves from harm and improve their ability to survive challenging circumstances. Abiotic pressures eventually mount a plant’s growth and development by altering several cellular and molecular processes (Bohnert et al., 1995; Shrama et al., 2019) [1-4].

Both heat and drought stress negatively impact plant development and physiology, according to a number of studies (Cui et al., 2022; Ayaz et al., 2021). Numerous physiological, biochemical, and molecular reactions to high temperature stress include stomatal closure because of low vapor pressure, which reduces the amount of carbon dioxide (CO2) available (Mathur et al., 2014; Parrotta et al., 2021). Additionally, this can harm the photosynthetic machinery and lessen photosystem activity, which lowers the photosynthetic rate (Fv/Fm) and triggers a variety of physiological reactions, including an increase in proline concentration and a decrease in chlorophyll content (Thompson et al., 2022; Mafakheri et al., 2010) [5-7].

Osmolyte

In order to react to a stress, the plant uses stress sensors, signaling pathways, and metabolism. Osmolytes are low-molecularweight molecules that are synthesized and accumulated as one such physiological reaction when a plant is exposed to stress. Osmolytes typically have no net charge at physiological pH, are readily soluble in water, do not interfere with typical metabolic processes, and are not hazardous even at high concentrations [8, 9]. These are also referred to as “compatible solutes” as a result (Slama et al., 2015). In general, osmolytes are identified by stress physiologists based on three types of data: (i) a rise in organic molecule accumulation under decreased water potential in cells; (ii) the physicochemical properties of the putative osmolyte when studied in vitro; and (iii) comparative physiology as a pointer to gain insight into whether osmolytes provide protection in desiccation-tolerant species or in dehydration-tolerant [10-12].

Major groups of osmolytes

Osmolytes, a class of phyto-protectants, can alter the solubility of water, regulate osmotic potential, maintained folded proteins, and safeguard the membrane structures in harsh climatic conditions (Yancey, 2005). Due to their ability to protect cellular components against osmotic, oxidative, and dehydration damage, these substances are known as osmoprotectants (Table 1). Osmolytes can be divided into the following groups:

Table 1: Major groups of osmolytes and its examples.

Osmolyte variety in plants

Despite the fact that the majority of osmolytes found throughout the plant kingdom have species and environmental specific osmolytes (Slama et al., 2015). The concentration or accumulation of osmolytes varies similarly depending on heredity and environmental factors. For instance, the amino acid proline appears in a variety of taxonomically different plants, whereas the quaternary ammonium complex-alanine betaine accumulates among a few species of Plumbaginaceae (Gupta and Huang, 2014). In general, plant species that have experienced ongoing environmental stress in the past have evolved to store osmolytes [13,14].

Numerous studies have shown that under abiotic stress, plants gathered sugars like trehalose, mannitol, and galactinol. Several genes are involved in the biosynthesis of these organic solutes, which helps transgenic plants develop a tolerance to abiotic stress (Taji et al., 2002) [15]. Proline accumulation is likewise one of the processes or reactions that many plants use to adapt to diverse conditions (Anjum et al., 2015, 2016; 2017). Thus, it is crucial to comprehend the mechanisms governing various activities as well as the mechanisms underpinning plants’ ability to withstand abiotic stress. Plants use phytohormones extensively in a variety of biochemical and physiological processes. For plants to be tolerant of unfavorable conditions, their involvement in reducing abiotic stress is essential (Khan et al., 2015; Tanveer et al., 2019; Shahzad et al., 2018; Khan et al., 2013; Sharma et al., 2019). It is essential to correlate the two because both osmolytes and plant hormones have been shown to play significant roles in stressful situations. This will help to clarify how phytohormones regulate osmolytes in response to abiotic stress [16,17].

Function of osmolyte in plant cell

The water intake necessary to sustain plant cell rigidity is caused by the osmolyte gradient, not the plasma membrane, which serves as an osmotic barrier. Plant cells’ cytosolic aqueous gel-based osmolyte system controls fluid balance and volume of cells. Turgor dynamics are influenced by the presence of carbohydrates like D-glucose and amino acids like L-glutamine in the cytosol [18]. According to Argiolas et al. (2016), such osmolyte complexes increase the turgor pressure needed for plant movement. Sugars support the development of plant tissues and control signaling networks that manage the transcription of genes essential for respiration, photosynthesis, and the making of starch and sugars (Hare et al., 1998). Unbound amino acids which are building blocks of proteins, contain nitrogen (such as nucleic acids). Proline also decreases cytoplasmic acidosis and maintains the NADP+ to NADPH ratios necessary for metabolism (Hare et al., 1998) [19, 20].

Mechanism of action of osmolytes in plant cells

Abiotic stressors in plants result from environmental factors that disturb them enough to cause a reaction in them. Drought, salt, heavy metal toxicity, chilling, freezing, and heat stress are examples of abiotic stressors that are commonplace throughout the world and pose a threat to plant productivity and distribution [21].

Important osmo-protectants in plant cells

Low molecular weight hydrophilic organic molecules known as osmoprotectants play a number of roles in relation to plant defense mechanisms in a variety of environmental contexts (Nahar et al., 2016). These substances are not harmful at increasing cellular quantities, in contrast to inorganic substances (Niazian et al., 2021). Under stressful circumstances, plants buildup proline, ectoine, trehalose, polyols, fructan, and compounds with quaternary compounds (QACs), such as glycinebetaine, alanine-betaine, proline-betaine, choline-Osulfate, hydroxy-prolinebetaine, and pipecolatebetaine (Singh et al., 2015). The quantities of molecules like mannitol, GB, D-ononitol, or sorbitol generated by transgenic plants overexpressing osmoprotectant biosynthetic enzymes are too little to give protective benefits only by osmotic mass action (Huang et al., 2000) [22-25].

The major purpose of osmoprotectant accumulation in plants under salt stress is to protect cellular components by reducing ionic toxicity and maintaining cell turgor pressure through osmoregulation. These osmoprotective compounds also strengthen plants’ natural defense against free radicals by scavenging potentially harmful ROS while protecting vital antioxidative enzymes (Hasanuzzaman et al., 2014, 2019). Osmolytes also play a role in the activation of genes related to defense in response to a variety of stressors, which further emphasizes their critical role in plants (Wani et al., 2018b) [26].

Amino acids

Examples of amino acids with osmoprotective origins include proline, arginine, alanine, and aminobutyric acid (GABA; Suprasanna et al., 2014). These osmoprotectants accumulate and reduce the osmotic potential of cells during salt stress, increasing water absorption [27]. They also maintain the structural integrity of proteins and membranes (Ashraf and Foolad, 2007), act as nitrogen-storing agencies and ROS scavengers (Hayat et al., 2012), and store nitrogen. Stressed situations are indicated by the buildup of primarily proline in substantially higher proportions than other osmoprotectants. Alanine serves as a stress response molecule in plants’ defense against biotic and abiotic stresses as it is a non-proteinogenic amino acid. Furthermore, it is changed into the osmo-protective compound in various plant species (Parthasarathy et al., 2019) [30].

Proline

Glutamate and the ornithine route are the two mechanisms that can produce proline. The intermediate 1-pyrroline-5-carboxylate (P5C), which is catalyzed by 1-pyrroline-5-carboxylate synthetase (P5CS) and 1-pyrroline-5-carboxylate reductase (P5CR) in the glutamate route, is used to create proline from glutamatic acid (Dar et al., 2016). The alternative process, described by Verbruggen and Hermans (2008), involves the synthesis of proline to ornithine, which is then transaminated to pyrroline-5-carboxylate (P5C) [31]. Proline accumulation is said to help with stress tolerance in a variety of ways. It serves as a biochemical chaperone, maintaining the integrity of proteins and fostering enzyme activity (Ghosh et al., 2022). The expression of the enzyme pyrroline-5-carboxylate reductase has recently enhanced in engineered plants, resulting in an accumulation of proline [32].

Additionally, proline’s antioxidant properties have been found to be useful as reactive oxygen species scavengers (El-Badri et al., 2021). Through the constitutive expression of OsOAT genes, it has been demonstrated how crucial the ornithine path is involve in growth of rice seedlings. According to You et al. (2012), these genes are in charge of better antioxidant status, increased-OAT activity, and tolerance to osmotic stress and drought. However, due to higher expression of P5CS activity during salt stress, the Glu pathway is used more frequently than the Orn pathway. This shows that proline accumulation during osmotic adjustment is significantly influenced by the Glu route (Zhen and Ma, 2009) [33].

In Vigna aconitifolia L. under salt stress, P5CS mRNA levels dramatically increased whereas OAT mRNA levels significantly decreased, according to Delauney et al. (1993). Later, it was verified by evaluation studies looking at proline biosynthesis under salt stress by Lei et al. (2016) and Mansour and Ali (2017). It is interesting that exogenous proline administration led to various outcomes. For example, Zea mays L [34]. underwent salt stress and experienced decreased P5CS activity and increased PDH activity due to foliar proline exposure (de Freitas et al., 2018). Under salinized circumstances, Sorghum bicolor showed comparable results (de Freitas et al., 2019). Exogenous prolineprimed seed has been associated with reduced P5CS response, whereas Triticum aestivum L. PDH expression has dramatically enhanced (Rady et al., 2019). According to Deuschle et al. (2001), these elevated PDH levels shield plants from the toxicity of proline. Proline builds up and antioxidative responses to salt stress are improved in Lepidium draba when the P5CS gene is overexpressed (Pakzad et al., 2021) [35,36].

Glycine betaine (GB)

Glycine betaine (GB), an ammonium molecule that is an N-methylated by-product of glycine and is zwitterionic, neutral at physiological pH, as described by Ashraf and Foolad (2007). Chloroplasts in young tissues produce GB in large quantities to protect membrane enzymes and proteins from harmful environmental factors. Because GB is not actively broken down or metabolized in plant tissues, GB concentration is regulated by plant synthesis, transport, and dilution (Annunziata et al., 2019) [37]. Under abiotic stress situations, GB is biosynthesized as spatiotemporal (Annunziata et al., 2019). Biological stress usually starts out at minimal amounts and builds up over time in developing tissues and organs. Furthermore, unlike proline, the GB is swiftly re-translocated to younger leaves even when exogenously given to older portions. Therefore, it can be concluded that GB cannot be metabolized and is essential for protecting developing tissues (Figure 1) [38].

Figure 1: Schematic representation of Plant response to various abiotic stress factors.

Sugars

Carbohydrates such sugars (including sucrose, fructose, and trehalose) and starch build up during salt stress (Parida et al., 2004). These sugars are important because they act as an osmoprotectant and a ROS scavenger to reduce salt stress. Additionally, it has been noted that as salt stress levels rise, lowering sugar levels (such as fructans and sucrose) rise dramatically as well (Kerepesi and Galiba, 2000; Gangola and Ramadoss, 2018) [39,40].

Sugar alcohol

Sugar alcohols such as pinitol, mannitol, myo-inositol, and sorbitol play a vital role in lowering stress-related diseases by altering the osmotic equilibrium. These also have a strong polyol reputation. Myo-inositol and pinitol are cyclic, but mannitol and sorbitol have a linear structure. Their buildup in plants is thought to serve a variety of purposes, including osmotic adjustment, ROS regulation, and molecular chaperons, according to Upadhyay et al. (2015) and Bhattacharya and Kundu (2020) [41]. A sugar alcohol called mannitol is created when the enzyme mannose-6-phosphate reductase reacts with a combination of glucose and fructose to produce both mannitol and gluconic acid. According to Kaya et al. (2013), mannitol helps with osmotic balance and removes oxygen radicals generated by stress. An osmoprotectant called sorbitol is created during photosynthesis (Wu et al., 2020). Zhou et al. (2003) converted sorbitol-6-phosphate into sorbitol by dephosphorylating sorbitol-6-phosphatase. As an osmolyte, d-ononitol, a sugar alcohol, prevents water loss in plants that are under drought stress [42]. Tobacco was able to manufacture more D-ononitol and show greater resistance to salt and drought by adding the myoinositol O-methyltransferase gene (Vinocur and Altman, 2005).Pinitol is a byproduct of the methylation of myo-inositol and is found in a number of halophytic organisms. As a consequence of ononitol epimerization, pinitol is also created (Sengupta et al., 2008; Slama et al., 2015; Dumschott et al., 2019) [43].

Inositol

Numerous plants produce the sugar-like carbohydrate known as inositol, or more specifically, myo-inositol (Valluru & Van den Ende, 2011; Nisa et al., 2016). Pinitol, galactinol, and ononitol are some of its derivatives that function as osmoprotectants in a number of ways (Handa et al., 2018). Additionally, it controls the manufacture of phytic acid, auxin, and plant defense mechanisms (Hazra et al., 2019) [44]. In two different mechanisms, inositol and other related compounds are proposed to demonstrate salt tolerance: (1) by protecting the interior of cells from ROS, and (2) by preserving cell turgor stress. The generation of the polar compound (inositol) is a two-step metabolic process way that starts the enzymatic transformation of the sugar d-6-P into myoinositol- 1-P stimulated by myo-inositol-1-P synthase (Majumder et al., 1997), accompanied by the dephosphorylation of myo-inositol-1-P resulting to generate myoinositol which further generates distinctive inositol-containing materials including the phospholipids (Dastidar et al., 2006) [45].

Polyamines

Low molecular weight nitrogen-containing substances known as polyamines (PAs) are found in several cellular compartments. The three plant growth substances spermidine (Spd), putrescine (Put), and spermine (Spm) are the most prevalent PAs detected in plants (Bano et al., 2020). Canavalamine, homospermidine, cadaverine, and 1, 3-diamino propane is among the additional PAs that can be made from amino acids. The most common forms of PAs are free or coupled with phenolic chemicals, macromolecules, or both. putrescine (Put), spermidine (Spd), and spermine (Spm) are the most abundant PA that can be formed from arginine with the help of N-carbamoyl putrescine and agmatine (Urano et al., 2003) [46]. The synthase enzyme also transforms this putrescine into spermine and spermidine. Out of these polyamines, putrescine is the one that accumulates most in saline environments. Due to their polyanionic nature, they engage with the outer layer of the membrane and assist in maintaining the membrane structure (Gill and Tuteja, 2010a) [47]. Polyamines’ main roles, according to Kuznetsov et al. (2007), Mustafavi et al. (2018), and Chen et al. (2019), are osmotic regulation, hydroxyl radical scavenging through altering the activity of enzymes and ammonia detoxification. According to Li and He (2012), Spd level may serve as a marker of one’s ability to tolerate salt. Exogenous Spd treatment enhanced growth of plants by increasing photosynthesis and reactive oxygen metabolism in the presence of salinity stress (Meng et al., 2015; Baniasadi et al., 2018) [48-50]. The expression of polyamine biosynthetic enzymes like spermidine synthase (SPDS), arginine decarboxylase (ADC), ornithine decarboxylase (ODC), and S-adenosyl methionine decarboxylase (SAMDC) is utilized in a variety of transgenic techniques to improve stress tolerance (Gill and Tuteja, 2010a). Following validation of the subpar performance of transgenic plants altered with PA synthesis genes (Urano et al., 2004; Marco et al., 2015), regulation of PAs becomes critical in salt-stressed plants. Brassica napus L. is capable of reducing the negative effects of salt thanks to up-regulated expression of Calvin-cycle-related genes mediated by PAs (ElSayed et al., 2022) (Figure 2) [51-53].

Figure 2: Schematic representation of abiotic stress and osmolyte (Pathway is initiated as results in induction of stress responsive transcriptional factors (SRTFs) that up regulate the stress responsive genes (SRGs) related to biosynthesis and accumulation of osmolytes.

Ionic tolerance

A well-known strategy allowing agricultural plants to tolerate salinity is the exclusion of ions, especially Na+, from the shoot [54]. Due to the ease of conducting experiments, this mechanism has drawn the greatest attention. Many crops, including wheat (Forster, 2001; Munns and James, 2003), rice (Zhu et al., 2001; Lee et al., 2003), barley (Wei et al., 2003; Garthwaite et al., 2005), and Medicago (Sibole et al., 2003), have shown a significant connection between exclusion and salt tolerance. With this technique, Na+ and Cl-penetrate the plant’s roots and quickly travel to the shoot by the process of transpiration. In order to avoid these ions from accumulating in the shoot system, the roots filter out the majority of the Na+ and Cl dissolving in the soil solution [55-60]. As a result, the plant may survive in saline soil indefinitely since the concentration of salt in the shoot as a whole never exceeds that in the soil. Because the concentration of Na+ and Cl ions is far higher in the shoot than in the roots, this boosts the plant’s tolerance to salt. The sodium and other ion concentrations in the various layers of wheat root were assessed by Lauchli et al. (2008Additionally, the first line of defense against sodium uptake is the SOS1 antiporter, which is located to the root epidermis (specifically at the root tip, where roots are undifferentiated) (Assaha et al., 2017) (Figure 3) [61-65].

Figure 3: Schematic diagram of salt overlay sensitive (SOS) pathways. (Pooja Singh et al., 2022).

Bioengineering: Osmolyte induced stress tolerances

The relevance of osmolytes during abiotic stress responses has been well investigated thanks to bioengineering of the genes responsible for osmolytes’ biosynthesis and metabolism (Groppa and Benavides, 2008). Abiotic stress tolerance has been used to confirm the increased level of compatible nontoxic osmolytes, radical scavengers, and other transgenic products (Vinocur and Altman, 2005) [66-68]. Due to advancements in biochemical and cell biology techniques, it is now possible to clone potential osmolyte biosynthetic genes and transfer them into essential crop plants (Wang et al., 2003). According to Cortina and Culianez-Macia (2005), the trehalose biosynthetic pathway alters carbohydrates, which may explain why tomato plants with the TPS1 gene displayed higher tolerance when utilized with yeast [69,70]. Engineered tobacco cell lines containing ect A, ect B, and ect C showed improved resistance to mannitol-induced osmotic stress, which is linked to the constitutive CaMV 35S promoter (Nakayama et al., 2000) [71,72]. By boosting transpiration and safeguarding RuBisCO proteins, they also showed increased nitrogen delivery to leaves (Moghaieb et al., 2006). Revealed that engineered plant lines of Petunia hybrida were created using 1-pyrroline-5-carboxylate synthetase genes (AtP5CS gene obtained from Arabidopsis thaliana L [73,74]. or OsP5CS gene derived from Oryza sativa L.) that showed improved tolerance to conditions of drought and accumulated additional proline. Greater tolerance to drought stress was also seen in transgenic wheat plants (VaP5CS from Vigna aconitifolia) (Vendruscolo et al., 2007) [75-79]. P5CR was overexpressed in Arabidopsis under abiotic stress conditions such as salt, polyethylene glycine, abscisic acid, and heat stress. Furthermore, proline P5CR expression in soybean (Glycine max L. Merr. cv. Ibis) with greater endurance to drought resulted in increased accumulation of proline (Simon et al., 2006; Mwenye et al., 2016) [80]. It is reported that the choline dehydrogenase (betA)-producing choline dehydrogenase (DH4866) genetically engineered line of maize showed higher GB storage and stress caused by drought resistance [81-84]. In plants exposed to stress conditions, improved osmotic adjustment, reduced ion leakage, lipid membrane peroxidation, and improved level of relative water content are potential indications of drought resistance (Lv S et al., 2007) [85-90]. A research study shows that under both ordinary and salt stress (150 mM NaCl), transgenic cotton produced by introducing the CMO gene (AhCMO) replicated from Atriplex hortensis collected more GB than nontransgenic plants. The betA gene has been introduced into wheat, and this wheat has shown resistance to salt stress (He et al., 2010). Furthermore, it has been demonstrated that chloroplast genetic engineering’s overexpression of betaine under the direction of betaine aldehyde dehydrogenase (BADH) is a key tactic for providing salt tolerance to particular crops (Kumar et al., 2004; Fitzgerald et al., 2009). Additionally, tobacco plants that had the BADH gene for betaine aldehyde dehydrogenase added to them had the ability to produce GB in chloroplasts that induced salt stress [91-94].

Conclusions and Perspectives

The positive impacts of osmolytes have on plants as well as their ability to boost abiotic stress tolerance were highlighted in this review study. One possibility for achieving the second environmentally friendly goal, which is to end hunger, is to increase both the quantity and the quality of agricultural crops through the synthesis of osmolytes and their stress-reduction properties. However, other economically successful crops, such as wheat, maize, and barley, do not produce higher amounts of osmolytes. Comparatively to susceptible genotypes, only stress tolerant genotypes within a species accrue levels of osmolytes high enough to deal with stress. As a result, numerous studies have demonstrated that exogenous osmolyte treatment can compensate for osmolyte accumulation deficiencies and improve plant growth. Exogenously given osmolytes help plants fight against environmental stress more effectively than unfed plants do, even within the same accumulating species. Furthermore, exogenous administration of a particular osmolyte or mixtures of osmolytes reduces the negative effects of a particular stress state in cells. In order to help a particular crop deal with a particular stress, researchers have advised exogenous administration of a particular osmolyte. A number of studies have shown that the biosynthetic and regulatory genes from various sources have been effectively used to create transgenic plants that are more resistant to stress and have the capacity to accumulate osmolytes in a timely manner. The numerous potential genes for the osmolyte synthesis pathway can be advantageous for a variety of crop plants. Due to the quick worldwide changes in the climate, research must focus on utilizing the benefits of osmolyte-mediated crop enhancement to assist the worldwide supply of food. Improvements in gene implantation and manipulation may facilitate the development of super crops by enhancing their capacity to retain osmolytes for greater production and to ensure life under various stress conditions.

1. Anjum SA, Ashraf U, Tanveer M, Khan I, Hussain S, et al. (2017) (b) Drought Induced Changes in Growth, Osmolyte Accumulation and Antioxidant Metabolism of Three Maize Hybrids. Front Plant Sci 8: 69.

Google Scholar, Crossref, Indexed at

2. Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, et al. (2015) (a) Cadmium toxicity in Maize (Zea mays L.): Consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ Sci Pollut Res 22: 17022-17030.

Google Scholar, Crossref, Indexed at

3. Anjum SA, Tanveer M, Hussain S, Shahzad B, Ashraf U, et al. (2016) (c)  Osmoregulation and antioxidant production in maize under combined cadmium and arsenic stress. Environ Sci Pollut Res 23: 11864-11875.

Google Scholar, Crossref, Indexed at

4. Annunziata MG, Ciarmiello LF, Woodrow P, Dell’ Aversana E, Carillo P, et al. (2019) Spatial and temporal profile of glycine betaine accumulation in plants under abiotic stresses. Front Plant Sci 10: 1-13.

Google Scholar, Crossref, Indexed at

5. Argiolas A, Puleo GL, Sinibaldi E, Mazzolai B (2016) Osmolyte cooperation affects turgor dynamics in plants. Scientific Reports 6: 30139.

Google Scholar, Crossref, Indexed at

6. Ashraf MFMR, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59: 206-216.

Google Scholar

7. Assaha DV, Ueda A, Saneoka H, Al-Yahyai R, Yaish MW, et al. (2017) The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Front Physiol 8:509.

Google Scholar, Crossref, Indexed at

8. Ayaz A, Huang H, Zheng M, Zaman W, Li D, et al. Molecular Cloning and Functional Analysis of GmLACS2-3 Reveals It’s Involvement in Cutin and Suberin Biosynthesis along with Abiotic Stress Tolerance. Int J Mol Sci 22:  9175.

Google Scholar

9. Baniasadi F, Saffari VR, Moud AAM (2018) Physiological and growth responses of Calendula officinalis L. plants to the interaction effects of polyamines and salt stress. Sci Horticult 234: 312-317.

Google Scholar

10. Bhattacharya S, Kundu A (2020) Sugars and sugar polyols in overcoming environmental stresses in Protective Chemical Agents in the Amelioration of Plant Abiotic Stress. Eds. A. Roychoudhury and DK Tripathi (Hoboken, NJ: John Wiley and Sons) 71-101.

Google Scholar, Crossref, Indexed at

11. Bohnert HJ, Nelson DE, Jensen RG (2019) Adaptations to Environmental Stresses. Plant Cell 7: 1099-1111.

Google Scholar

12. Chen D, Shao Q, Yin L, Younis A, Zheng B (2019) Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci 9:1945.

Google Scholar, Crossref, Indexed at

13. Cortina C, Culianez-Macia FA (2005) Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci 169:75-82.

Google Scholar

14. Cui Y,  Ouyang S,  Zhao Y, Tie L, Shao C,  et al. (2022) Plant responses to high temperature and drought: A bibliometrics analysis. Front Plant Sci 13: 1052660.

Google Scholar, Crossref, Indexed at

15. Dar MI, Naikoo MI, Rehman F, Naushin F, Khan FA, et al. (2016) Proline accumulation in plants: roles in stress tolerance and plant development,” in Osmolytes and Plants Acclimation to Changing Environment: Emerging Omics Technologies. eds. N. Iqbal, R. Nazar and N. A. Khan (New Delhi: Springer), 155- 166.

Google Scholar

16. Dastidar KG, Maitra S, Goswami L, Roy D, Das KP, et al.(2006) An insight into the molecular basis of salt tolerance of L-myo-inositol 1-P synthase (PcINO1) from Porteresiacoarctata (Roxb.) Tateoka, a halophytic wild rice. Plant Physiol 140: 1279-1296.

Google Scholar, Crossref, Indexed at

17. de Freitas PAF, de Souza Miranda R, Marques EC, Prisco JT, Gomes-Filho E, et  al.  (2018) Salt tolerance induced by exogenous proline in maize is related to low oxidative damage and favorable ionic homeostasis. J Plant Growth Regul 37: 911-924.

Google Scholar

18. Delauney AJ, Hu CA, Kishor PB, Verma DP (1993) Cloning of ornithine delta-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem 268: 18673-18678.

Google Scholar, Indexed at

19. Dumschott K, Dechorgnat J, Merchant A (2019) Water deficit elicits a transcriptional response of genes governing D-pinitol biosynthesis in soybean (Glycine max). Int J Mol Sci 20:2411.

Google Scholar Crossref, Indexed at

20. Ejaz S, Sajjad H, Muhammad AA, Shakeel A (2019) Application of Osmolytes in Improving Abiotic Stress Tolerance in Plant. Plant growth and regulation 1:1-58.

Google Scholar

21. El-Badri AM, Batool M, Wang Z, Khatab A, Sherif A, et al. (2021) Antioxidative and metabolic contribution to salinity stress responses in two rapeseed cultivars during the early seedling stage. Antioxidants 10:1227.

Google Scholar, Crossref, Indexed at

22. ElSayed AI, Mohamed AH, Rafudeen MS, Omar AA, Awad MF,et  al. (2022) Polyamines mitigate the destructive impacts of salinity stress by enhancing photosynthetic capacity, antioxidant defense system and upregulation of Calvin cycle-related genes in rapeseed (Brassica napus L.). Saudi J Biol Sci 29: 3675-3686.

Google Scholar, Crossref, Indexed at

23. Fitzgerald TL, Waters DLE, Henry RJ (2009) Betaine aldehyde dehydrogenase in plants. Plant Biol 11:119-130.

Google Scholar, Crossref, Indexed at

24. Forster B (2001) Mutation genetics of salt tolerance in barley: an assessment of Golden promise and other semi-dwarf mutants. Euphytica 120: 317-328.

Google Scholar

25. Gangola MP, Ramadoss BR (2018) Sugars play a critical role in abiotic stress tolerance in plants in Biochemical, Physiological and Molecular Avenues for Combating Abiotic Stress Tolerance in Plants. ed. S. H. Wani (Amsterdam, The Netherlands: Academic Press) 17-38.

Google Scholar, Crossref, Indexed at

26. Garthwaite AJ, von Bothmer R, Colmer TD (2005) Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and cl−into the shoots. J Exp Bot 56: 2365-2378.

Google Scholar, Crossref, Indexed at

27. Ghosh UK, Islam MN, Siddiqui MN, Cao X, Khan MAR, et al. (2022) Proline, a multifaceted signalling molecule in plant responses to abiotic stress: understanding the physiological mechanisms. Plant Biol 24: 227-239.

Google Scholar, Crossref, Indexed at

28. Gill SS, Tuteja N (2010a) Polyamines and abiotic stress tolerance in plants. Plant Signal. Behav 5: 26-33.

Google Scholar, Crossref, Indexed at

29. Groppa M, Benavides M (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35.

Google Scholar, Crossref, Indexed at

30. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. International Journal of Genomics 2014: 701596.

Google Scholar, Crossref, Indexed at

31. Handa N, Kohli SK, Kaur R, Sharma A, Kumar V, et al. (2018) Role of compatible solutes in enhancing antioxidative defense in plants exposed to metal toxicity” in Plants Under Metal and Metalloid Stress. eds. M. Hasanuzzaman, K. Nahar and M. Fujita (Singapore: Springer) 207-228.

Google Scholar

32. Hare PD, Cress WA, van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant, Cell and Environment 21: 535-553.

Google Scholar

33. Hasanuzzaman M, Alam MM, Rahman A, Hasanuzzaman M, Nahar K, et al. (2014) Exogenous proline and glycine betaine mediated upregulation of antioxidant defense andglyoxalyase systems provides better protection against salt-induced oxidative stress in two rice (Oryza sativa L.) varieties. Biomed Res Int 757219.

Google Scholar, Crossref, Indexed at

34. Hasanuzzaman M, Anee TI, Bhuiyan TF, Nahar K, Fujita M (2019) Emerging role of osmolytes in enhancing abiotic stress tolerance in rice in Advances in Rice Research for Abiotic Stress Tolerance. eds. M. Hasanuzzaman, M. Fujita, K. Nahar and J. K. Biswas (Amsterdam: Woodhead Publications) 677-708.

Google Scholar, Crossref, Indexed at

35. Hazra A, Dasgupta N, Sengupta C, Das S (2019) MIPS: functional dynamics in evolutionary pathways of plant kingdom. Genomics 111:1929-1945.

Google Scholar, Crossref, Indexed at

36. He C, Yang A, Zhang W, Gao Q, Zhang J (2010) Improved salt tolerance of transgenic wheat by introducing betA gene for glycine betaine synthesis. Plant Cell, Tissue and Organ Culture (PCTOC). 101:65-78.

Google Scholar, Crossref, Indexed at

37. Huang J, Hirji R, Adam L, Rozwadowski KL, Hammerlindl JK, et al. (2000) Genetic engineering of glycinebetaine production toward enhancing stress tolerance in plants: metabolic limitations. Plant Physiol. 122: 747-756.

Google Scholar, Crossref, Indexed at

38. Kaya C, Sonmez O, Aydemir S, Ashraf M, Dikilitas M, et al. (2013) Exogenous application of mannitol and thiourea regulates plant growth and oxidative stress responses in salt-stressed maize (Zea mays L.). J Plant Interact 8: 234-241.

Google Scholar, Crossref, Indexed at

39. Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40: 482-487.

Google Scholar

40. Khan MI, Iqbal N, Masood A, Per TS, Khan NA, et al. (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal Behav 8: e26374

Google Scholar, Crossref, Indexed at

41. Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA, et al. (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6: 462.

Google Scholar, Crossref, Indexed at

42. Khan MIR, Iqbal N, Masood A, Khan NA (2012) Variation in Salt Tolerance of Wheat Cultivars: Role of Glycinebetaine and Ethylene. Pedosphere 22: 746-754.

Google Scholar

43. Kumar S, Dhingra A, Daniell H (2004) Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confer enhanced salt tolerance. Plant Physiol 136:2843-2854.

Google Scholar, Crossref, Indexed at

44. Kuznetsov V, Shorina M, Aronova E, Stetsenko L, Rakitin V, et al. (2007) NaCl-and ethylene-dependent cadaverine accumulation and its possible protective role in the adaptation of the common ice plant to salt stress. Plant Sci 172:363-370.

Google Scholar

45. Lauchli A, James AR, Huang XC, McCully M, Munns R, et al.  (2008) Cell-specific localization of Na+ in roots of durum wheat and possible control points for salt exclusion. Plant Cell Environ. 31: 1565-1574.

Google Scholar, Crossref, Indexed at

46. Lee KS, Choi WY, Ko JC, Kim TS, Gregorio GB, et al. (2003) Salinity tolerance of japonica and indica rice (Oryza sativa L.) at the seedling stage. Planta 216: 1043-1046.

Google Scholar, Crossref, Indexed at

47. Lei P, Xu Z, Liang J, Luo X, Zhang Y, et al. (2016) Poly (γ-glutamic acid) enhanced tolerance to salt stress by promoting proline accumulation in Brassica napus L. Plant Growth Regul 78: 233-241.

Google Scholar, Crossref, Indexed at

48. Li Y, He J (2012) Advance in metabolism and response to stress of polyamines in plant. Acta Agric. Boreali Sinica 27: 240-245.

Google Scholar

49. Lv S, Yang A, Zhang K, Wang L, Zhang J, et al. (2007) Increase of glycinebetaine synthesis improves drought tolerance in cotton. Mol Breed 20:233-248.

Google Scholar, Crossref, Indexed at

50. Mafakheri A, Siosemardeh A, Bahramnejad B, Struik PC, Sohrabi E, et al. (2010) Effect of drought stress on yield, proline and chlorophyll contents in three chickpea cultivars. Aust J Crop Sci 4: 580-585.

Google Scholar

51. Majumder AL, Johnson MD, Henry SA (1997) 1L-myo-inositol1-phosphate synthase. Biochim Biophys Acta 1348: 245-256.

Google Scholar, Crossref, Indexed at

52. Mansour MMF, Ali EF (2017) Evaluation of proline functions in saline conditions. Phytochemistry 140: 52-68.

Google Scholar, Crossref, Indexed at

53. Marco F, Bitrián M, Carrasco P, Alcázar R, Tiburcio AF, et al. (2015) Polyamine biosynthesis engineering as a tool to improve plant resistance to abiotic stress in Genetic Manipulation in Plants for Mitigation of Climate Change. eds. P. Jaiwal, R. Singh and O. Dhankher (New Delhi: Springer) 103-116.

Google Scholar

54. Mathur S, Agrawal D, Jajoo A (2014) Photosynthesis: Response to high temperature stress. J Photochem Photobiol B Biol 137:116-126.

Google Scholar, Crossref, Indexed at

55. Meng D, Hou L, Yang S (2015) Exogenous polyamines alleviating salt stress on peanuts (Arachis hypogaea) grown in pots. Chin J Plant Eco 39: 1209-1215.

Google Scholar

56. Moghaieb REA, Tanaka N, Saneoka H, Murooka Y, Ono H, et al. (2006) Characterization of salt tolerance in ectoine-transformed tobacco plants (Nicotiana tabaccum): photosynthesis, osmotic adjustment, and nitrogen partitioning. Plant Cell Environ 29:173-182.

Google Scholar, Crossref, Indexed at

57. Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil 253: 201-218.

Google Scholar, Crossref, Indexed at

58. Mustafavi SH, Badi HN, Sękara A, Mehrafarin A, Janda T, et al. (2018) Polyamines and their possible mechanisms involved in plant physiological processes and elicitation of secondary metabolites. Acta Physiol Plant 40:102.

Google Scholar

59. Mwenye OJ, Van Rensburg L, Van Biljon A, Van der Merwe R (2016) The role of proline and root traits on selection for drought-stress tolerance in soybeans: a review. S Afr J Plant Soil 33:245-256.

Google Scholar, Crossref, Indexed at

60. Nahar K, Hasanuzzaman M, Fujita M (2016) Roles of Osmolytes in plant adaptation to drought and salinity in Osmolytes and Plants Acclimation to Changing Environment: Emerging Omics Technologies. eds. N. Iqbal, R. Nazar and N. A. Khan (New Delhi: Springer) 37-68.

Google Scholar

61. Nakayama H, Yoshida K, Ono H, Murooka Y, Shinmyo A, et al. (2000) Ectoine, the compatible solute of Halomonas elongata, confers hyperosmotic tolerance in cultured tobacco cells. Plant Physiol 122:1239-1247.

Google Scholar, Crossref, Indexed at

62. Niazian M, Sadat-Noori SA, Tohidfar M, Mortazavian SMM, Sabbatini P (2021) Betaine aldehyde dehydrogenase (BADH) vs. Flavodoxin (Fld): two important genes for enhancing plants stress tolerance and productivity. Front. Plant Sci. 12:695110.

Google Scholar Crossref, Indexed at

63. Nisa ZU, Chen C, Yu Y, Chen C, Mallano A I, et al. (2016) Constitutive overexpression of myoinositol-1-phosphate synthase gene (GsMIPS2) from Glycine soja confers enhanced salt tolerance at various growth stages in Arabidopsis. J Northeast Agric Univ 23:28-44.

Google Scholar, Crossref, Indexed at

64. Pakzad R, Goharrizi KJ, Riahi-Madvar A, Amirmahani F, Mortazavi M, et al. (2021) Identification of Lepidium draba Δ1-pyrroline-5-carboxylate Synthetase (P5CS) and assessment of its expression under NaCl stress: P5CS identification in L. draba plant. P Natl A Sci India 91:195-203.

Google Scholar

65. Parida AK, Das AB, Mohanty P (2004) Investigations on the antioxidative defense responses to NaCl stress in a mangrove, Bruguiera parviflora: differential regulations of isoforms of some antioxidative enzymes. Plant Growth Regul 42: 213-226.

Google Scholar, Crossref, Indexed at

66. Parrotta L, Aloisi I, Faleri C, Romi M, Del Duca S, et al. (2020) Chronic heat stress affects the photosynthetic apparatus of Solanum lycopersicum L. cv Micro-Tom Plant Physiol Biochem 154:463-475.

Google Scholar, Crossref, Indexed at

67. Rady MM, Elrys AS, El-Maati MFA, Desoky ESM (2019) Interplaying roles of silicon and proline effectively improve salt and cadmium stress tolerance in Phaseolus vulgaris plant. Plant Physiol. Bioch. 139: 558-568.

Google Scholar, Crossref, Indexed at

68. Sengupta S, Patra B, Ray S, Majumder AL (2008) Inositol methyl transferase from a halophytic wild rice, PorteresiacoarctataRoxb. (Tateoka): regulation of pinitol synthesis under abiotic stress. Plant Cell Environ 30: 1442-1459.

Google Scholar, Crossref, Indexed at

69. Shahzad B, Tanveer M, Che Z, Rehman A, Cheema SA, et al. (2018)Role of 24-epibrassinolide (EBL) in mediating heavy metal and pesticide induced oxidative stress in plants: A review. Ecotoxicol Environ Saf 147:935-944.

Google Scholar, Crossref, Indexed at

70. Sharma A, Soares C, Sousa B, Martins M, Kumar V, et al. (2019) Nitric oxide-mediated regulation of oxidative stress in plants under metal stress: A review on molecular and biochemical aspects. Physiol Plant 19: 334-474.

Google Scholar, Crossref, Indexed at

71. Sharma A,  Shahzad B,  Rehman A,  Bhardwaj R,  Landi M, et al. Response of Phenylpropanoid Pathway and the Role of Polyphenols in Plants under Abiotic Stress. Molecules 24:2452.

Google Scholar, Crossref, Indexed at

72. Sibole JV, Cabot C, Poschenrieder C, and Barceló J (2003) Efficient leaf partitioning, an overriding condition for abscisic acid-controlled stomatal and leaf growth responses to NaCl salinization in two legumes. J Exp Bot 54: 2111-2119.

Google Scholar, Crossref, Indexed at

73. Simon-Sarkadi L, Kocsy G, Varhegyi A, Galiba G, Ronde JA, et al. (2006) Stress-induced changes in the free amino acid composition in transgenic soybean plants having increased proline content. Biologia Plantarum 50:793-796.

Google Scholar

74. Singh M, Kumar J, Singh S, Singh VP,  Prasad SM, et al.  (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Biotechnol 14: 407-426.

Google Scholar, Crossref, Indexed at

75. Slama I, Abdelly C, Bouchereau A, Flowers T, Savoure A, et al. (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot 115: 433-447.

Google Scholar

76. Slama I, Abdelly C, Bouchereau A, Flowers T, Savoure A, et al. (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Annals of Botany 115: 433-447.

Google Scholar, Crossref, Indexed at

77. Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, et al. (2002) Important roles of drought-and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29: 417-426.

Google Scholar, Crossref, Indexed at

78. Tanveer M, Shahzad B, Sharma A, Khan EA (2019) 24-Epibrassinolide application in plants: An implication for improving drought stress tolerance in plants. Plant Physiol Biochem 135: 295-303.

Google Scholar, Crossref, Indexed at

79. Thompson A, Conley M, Herritt M, Thorp K (2022) Response of upland cotton (Gossypium hirsutum L.) leaf chlorophyll content to high heat and low-soil water in the Arizona low desert. Photosynthetica 60: 280-292.

Google Scholar

80. Upadhyay RS, Meena M, Prasad V, Zehra A, Gupta VK, et al. (2015) Mannitol metabolism during pathogenic fungal–host interactions under stressed conditions. Front Microbiol 6:1019.

Google Scholar, Crossref, Indexed at

81. Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, et al (2003) Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ 26: 1917-1926.

Google Scholar, Crossref, Indexed at

82. Urano K, Yoshiba Y, Nanjo T, Ito T, Yamaguchi-Shinozaki K, et al. (2004) Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem Biophys Res Commun 313: 369-375.

Google Scholar, Crossref, Indexed at

83. Valluru R, Van den Ende W (2011) Myo-inositol and beyond-emerging networks under stress. Plant Sci 181: 387-400.

Google Scholar, Crossref, Indexed at

84. Vendruscolo ECG, Schuster I, Pileggi M, Scapim CA, Molinari HBC, et al. (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J Plant Physiol 164:1367-1376.

Google Scholar, Crossref, Indexed at

85. Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35: 753-759.

Google Scholar, Crossref, Indexed at

86. Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotech 16: 123-132.

Google Scholar, Crossref, Indexed at

87. Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1-14.

Google Scholar

88. Wani SH, Tripathi P, Zaid A, Challa GS, Kumar A, et al. (2018b) Transcriptional regulation of osmotic stress tolerance in wheat (Triticum aestivum L.). Plant Mol Bio 97: 469-487.

Google Scholar, Crossref, Indexed at

89. Wei W, Bilsborrow PE, Hooley P, Fincham DA, Lombi E, et al. (2003) Salinity induced differences in growth, ion distribution and partioning in barley between the cultivar Maythorpean its derivated mutant Golden promise. Plant Soil 250: 183-191.

Google Scholar, Crossref, Indexed at

90. Wu F, Chi Y, Jiang Z, Xu Y, Xie L, et al. (2020) Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 578: 577581.

Google Scholar, Crossref, Indexed at

91. You J, Hu H, Xiong L (2012) An ornithine δ-aminotransferase gene OsOAT confers drought and oxidative stress tolerance in rice. Plant Sci 197: 59-69.

Google Scholar, Crossref, Indexed at

92. Zhen WB, Ma QH (2009) Proline metabolism in response to salt stress in common reed [Phragmites australis (Cav.) Trin. Ex Steud]. Bot Mar 52: 341-347.

Google Scholar, Crossref, Indexed at

93. Zhou R, Cheng L, Wayne R (2003) Purification and characterization of sorbitol-6-phosphate phosphatase from apple leaves. Plant Sci 165: 227-232.

Google Scholar, Crossref, Indexed at

94. Zhu GY, Kinet JM, Lutts S (2001) Characterization of rice (Oryza sativa L.) F3 populations selected for salt resistance. I. Physiological behaviour during vegetative growth. Euphytica 121:251-263.

Google Scholar, Indexed at