Understanding the roles of osmolytes for acclimatizing plants to changing environment: a review of potential mechanism

ABSTRACT

Abiotic stresses are significant environmental issues that restrict plant growth, productivity, and survival while also posing a threat to global food production and security. Plants produce compatible solutes known as osmolytes to adapt themselves in such changing environment. Osmolytes contribute to homeostasis maintenance, provide the driving gradient for water uptake, maintain cell turgor by osmotic adjustment, and redox metabolism to remove excess level of reactive oxygen species (ROS) and reestablish the cellular redox balance as well as protect cellular machinery from osmotic stress and oxidative damage. Perceiving the mechanisms how plants interpret environmental signals and transmit them to cellular machinery to activate adaptive responses is important for crop improvement programs to get stress–tolerant varieties. A large number of studies conducted in the last few decades have shown that osmolytes accumulate in plants and have strong associations with abiotic stress tolerance. Production of abundant osmolytes is needed for tolerance in many plant species. In addition, transgenic plants overexpressing genes for different osmolytes showed enhanced tolerance to various abiotic stresses. Many important aspects of their mechanisms of action are yet to be largely identified, especially regarding the relevance and relative contribution of specific osmolytes to the stress tolerance of a given species. Therefore, more efforts and resources should be invested in the study of the abiotic stress responses of plants in their natural habitats. The present review focuses on the possible roles and mechanisms of osmolytes and their association toward abiotic stress tolerance in plants. This review would help the readers in learning more about osmolytes and how they behave in changing environments as well as getting an idea of how this knowledge could be applied to develop stress tolerance in plants.

KEYWORDS:

• Osmoprotectants
• abiotic stress
• drought
• salinity
• amino acid
• carbohydrate
• polyamine
• polyol

Introduction

Abiotic stresses on plants have been rising frequently and intensely due to rapid global climate change.^1,2,3 Plant cellular and developmental processes are disrupted by various abiotic stresses throughout their lifespan.^4–17 Several abiotic stresses such as salinity, drought, light, ultraviolet radiation, temperature, and heavy metal are responsible for the increase of reactive oxygen species (ROS) levels, peroxidation of lipids, activation of antioxidant system, as well as accumulation of compatible solutes.^18–20

Plant cells usually permit the influx, sequestering and synthesis of various solutes and accumulate them for maintaining homeostasis status and keeping the cell turgid for growth and development of plants during abiotic stress conditions.^21–26 In plants, osmotic adjustment mediated by the production of osmolytes has been found to protect the cellular machinery from stresses which could confer abiotic stress tolerance.^24,27–30 The term osmolytes refers to various low molecular weight compounds or metabolites namely, sugars, polyamines, secondary metabolites, amino acids, and polyols.^31–36 These molecules also known as cytoptotectants due to their ability of protecting cell contents against abiotic stresses.^24,37,38 To cope with different stresses and protect themselves, plants have evolved complex and well–organized mechanisms.³⁹ Biosynthesis and accumulation of various osmolytes are considered one of the paramount responses of host plants for combating against oxidative as well as osmotic stress caused by various stressors. The increasing uncertainty of climate change definitely intensifies various abiotic stresses, in turn affecting a considerable damage to the agricultural world. Consequently, precise environmental adaptation approaches on target plants were developed to address the problems.⁴⁰ A number of studies have interpreted the relationship between osmolytes and their tolerance to various abiotic stresses in different crop plants either through exogenous application of osmolytes, natural accumulation, or through transgenic expression of osmolytes pathway genes that have appeared recently.^41–45

The overproduction of osmolytes is the result of various stress signaling pathways (phytohormones, mitogen activated protein (MAP) kinase, and calcium-signaling pathways). Several osmolytes and their biosynthesis have been studied in detail, such as proline, glycine betaine (GB) and mannitol.^28,46–49 Moreover, several plants have been engineered metabolically for induced osmolyte biosynthesis and those transgenic plants have displayed better survival as well as tolerance of various abiotic stresses.^{21,23,47,48,50–53}

Therefore, controlling cellular osmotic balance and ion homeostasis, i.e., intracellular transportation of water, transportation of toxic ions inside the vacuole, synthesizing osmolytes in the cytoplasm, heat shock proteins, and activation of the enzymatic as well as non–enzymatic antioxidant systems are the most important conserved mechanism that confer stress tolerance in plants.^54–56 Considering the significant roles played by the osmolytes against different abiotic stresses, the present review gathers information related to this topic focusing on conferring abiotic stress tolerance in plants.

Biosynthesis and accumulation of osmolytes and their roles toward abiotic stress tolerance

Figure 1 shows the processes involved in mitigating the adverse effects of abiotic stresses. Osmolytes mitigate the adverse effect induced from abiotic stresses directly or indirectly either by maintaining membrane structure or scavenging stress-induced ROS respectfully. It has been observed that various stress response signaling pathways such as MAP kinase signaling, calcium signaling, abscisic acid (ABA) signaling, and ROS signaling synergistically lead to increased biosynthesis and/or accumulation of different osmolytes for tolerance, acclimatization and detoxification under abiotic stress conditions.⁵⁷

Figure 1. Schematic representation of overall relation between abiotic stress and osmolytes. (Upon insight of abiotic stress signal, the related signaling pathway is initiated and results in the induction of stress-responsive transcription factors (SRTFs) which consequently upregulate stress-responsive genes (SRGs) related to biosynthesis and accumulation of osmolytes such as free amino acids and their derivatives, carbohydrates and soluble sugars, polyols, polyamines, free amines to protect and make plants tolerant of encountered abiotic stresses.)

Carbohydrates and soluble sugars

It is widely accepted that the production and collection of soluble sugars directly contribute to radical scavenging, osmotic adjustment, carbon storage, and stabilization of protein structures such as Ribulose-1,5-bisphosphate carboxylase–oxygenase (RuBisCo)⁵⁸ and thus increases sugar levels when exposed to stresses.^59,60 Sugars are the main osmolytes for osmotic adjustment found in several plant species. Sugars function as osmoprotectants along with substrates for growth and regulators of gene expression during abiotic stress situations.⁶¹ Under high saline environments, some rice cultivars and Medicago species showed an increase in the total soluble sugars.^62–63 In addition, Keunen, et al.⁶⁴ concluded that disaccharides and oligosaccharides are potentially involved in plant abiotic stress tolerance.

The increase in monosaccharides in plants is associated with the initial response to drought stress while the increase in fructan believed to be associated with the delayed response.⁶⁵ In aerial tissues of Craterostigma plantagineum, sucrose accumulation has been found to be linked during the survival phase of complete tissue dehydration.^66,67 Trehalose, a disaccharide, has been found to be superior to other saccharides in conferring protection of plants under abiotic stress conditions, showed specific characteristics of reversible water absorption capacity against dehydration induced damages.^68,69 Increased level of trehalose has been also observed in drought-stressed cowpea (Vigna sinensis)⁴¹ Raffinose family oligosaccharides (RFOs) have been found to be involved in mitigating the effects including protecting cellular integrity during desiccation and imbibition and supplying substrates for energy generation during germination in response to harsh environmental conditions, namely, heat, cold, and dehydration.⁷⁰ The functions of RFOs have been examined in Arabidopsis thaliana plants under drought and cold stress conditions and mentioned that drought, high salinity, and cold-treated Arabidopsis plants gather a large amount of raffinose and galactinol, but not stachyose, proposed that raffinose and galactinol are involved in tolerance to drought, high salinity, and cold stresses, and they also act as signals to mediate abiotic stress responses.⁷¹

Thus, it is acknowledged that sugars participate in specific signal transduction mechanisms and osmotic adaptation during abiotic stress environment.⁷² It has been well documented that plants accumulate available sugars for proper metabolic functions, for example, in green gram⁷³ and pigeon pea⁷⁴ thus helping plants to tolerate waterlogged conditions. An experiment showed that sorbitol (5 and 10 mM) and trehalose (5 and 10 mM) exhibited protective roles in salt-sensitive cultivar of rice (Oryza sativa L. cv. KDML105) when exposed to salt stress (170 mM) situations.⁷⁵

Amino acids

Plant exposed to abiotic stress conditions has commonly been found to synthesize amino acids.^76,77 Among various amino acids, proline, GB and Gamma–Aminobutyric Acid (GABA) are largely associated and therefore, became the very candidate genes for genetic manipulation for improved abiotic stress tolerance.^49,78,79

Proline

To protect plant cells during osmotic stress situation, proline serves as compatible solute^80,81 and being a molecular chaperone, proline also acts as an antioxidant as well as ROS scavenger.^82–84 Proline accumulation might be due to a novel synthesis or decrease in degradation process or both.⁸⁵ Generally, proline is synthesized from glutamate by Δ1-pyrroline-5-carboxylate (P5C) synthetase (P5CS) and P5C reductase (P5CR) enzymes and also from ornithine pathway which is transformed into P5C/GSA (glutamate-1-semialdehyde) via ornithine-δ-aminotransferase.^30,86

In plants, under osmotic stress conditions, synthesis of proline from glutamine is the principal pathway while, under limited nitrogen, it is known that the ornithine approach works.⁸⁷ Researches have identified accelerated rate of proline biosynthesis during abiotic stress conditions which retained the low NADPH: NADP⁺ ratio, contributed to sustaining the electron flow between excitation centers of photosynthetic apparatus, stabilized the cell redox balance and lessen photoinhibition and damage of the photosynthetic apparatus in chloroplasts.⁸⁰ Proline is converted to Δ1-pyrroline-5–carboxylate (P5C) by proline dehydrogenase (PDH) and then to glutamate by P5C dehydrogenase (P5CDH) during recovery from stress. A very usual adaptive reaction to different abiotic stresses in halophytes is the increase accumulation of proline.

Being an osmoprotectant, the members of the Aizoaceae family also gather huge amounts of proline.^88–90 The salt tolerance features in Pancratium maritimum improved by stimulating the process of accumulation of the stress-protective proteins, proline.⁹¹ It has been found that proline overproduction links with halophytic behavior in some plant species with a view to conferring tolerance against salinity but did not show the complete responses for all time when exposed to extreme abiotic stress conditions. Moreover, it has recently been documented that proline mitigates the effect of both drought and heat stress situations.⁹² Under waterlogging conditions, accumulation of proline was reported and waterlogging tolerance in pigeon pea was found associated with proline accumulation.⁹³ Another experiment showed similar waterlogging tolerance in Vigna angularis.⁹⁴ Proline has been found to be associated to increase the salinity tolerance of tomato (Solanum lycopersicum L.),⁹⁵ soybean (Glycine max),^96,97 Groundnut (Arachis hypogaea L.),⁹⁸ pea (Pisum sativum),⁹⁹ sainfoin (Onobrychis viciaefolia)¹⁰⁰ and mung bean (Vigna radiata L.).¹⁰¹ Moreover, proline exhibited drought tolerance in lentil (Lens culinaris).^42,102

In addition, proline exhibited both the salinity tolerance¹⁰³ and the heavy metal tolerance particularly selenium tolerance in common bean (Phaseolus vulgaris L).¹⁰⁴

Gamma-Aminobutyric Acid (GABA)

As a non-protein amino acid, Gamma-aminobutyric acid (GABA) is reported to play a substantial role in functioning of plant when exposed to abiotic stress conditions, due to their important roles in plant osmoregulation, antioxidant defense system and act as signaling molecule.^105,106 α-ketoglutarate is the antecedent compound of GABA. Under abiotic stress conditions, α–ketoglutarate first altered by glutamate dehydrogenase to glutamate and then to GABA by glutamate decarboxylase.^106,107

Moreover, GABA averts ROS accumulation.^108,109 GABA accumulation has been found under salinity and flooding stress.^109–111 GABA alters the gene expression in various roots under saline condition. In addition, GABA activates various mechanisms associated with cascades signaling, regulation of protein degradation, hormones biosynthesis, and ROS production in Caragana intermedia (a legume shrub).¹¹² Under water deficit conditions, GABA preserved the water balance through osmotic adjustment in Nigella sativa L.¹¹³ The application of GABA increased the protein content along with the activities of glutamate decarboxylase (GAD) and diamine oxidase (DAO) in rice cultivar CSR 43 (tolerant) contrasted with Pusa 44 (susceptible) at seedling stage under 200 mM saline–alkaline stress. Subsequently, it is recommended that the increased level of endogenous GABA by exogenous GABA treatment could improve salinity stress tolerance of rice seedlings associated with GABA regulation in improving DAO activity along with proline content.¹¹⁴ Exogenous application of GABA positively facilitated polyamines biosynthesis and enhanced endogenous GABA level,¹¹⁵ significantly reduced the salt damage indices and increased plant height, chlorophyll content and the dry and fresh weights of tomato plants in response to NaCl stress.⁴⁵ GABA treatment well accumulates the content of endogenous GABA and proline, which was found to be useful to protect peach fruit suffering from chilling injury.¹¹⁶ Exogenous supply of GABA enhanced drought tolerance through the maintenance of membrane stability in perennial ryegrass (Lolium perenne) and black pepper.^117,118

Glycine betaine

Glycine betaine, an important osmolyte, has widely been accumulated in plants and other microorganisms.^119,120 Physiological studies have demonstrated that the increased level of accumulation of GB is linked with the degree of tolerance.¹²¹ In case of osmoregulation, it significantly plays a vital role in effective protection against several abiotic stresses such as salinity, drought, and extreme heat stress.^28,49,120

Choline and glycine are the two substrates which produces GB.¹²² In several plants, animals and microorganisms, there are two-enzyme pathway involved in the conversion of choline to GB. By the double step oxidation of choline through the toxic intermediate betaine aldehyde, GB is formed. These processes are catalyzed by choline monooxygenase (CMO) and NAD⁺–dependent betaine aldehyde dehydrogenase (BADH) in higher plants, and these enzymes are confined inside stroma of the chloroplasts.

The biosynthesis of GB can be induced with stress. The concentration of GB greatly lies between 40 and 400 μ mol (g DW)⁻¹ depending on the plant species.^119,120 In several crop plants, comprising sugar beet (Beta vulgaris), spinach (Spinacia oleracea), barley (Hordeum vulgare), wheat (Triticum aestivum) and sorghum (Sorghum bicolor), GB is known to add more GB than sensitive genotypes in response to abiotic stresses.^119,123,124 Transgenic plants with the increased level genes associated with GB synthesis, exhibited improved production of GB thus showed better tolerance to salt, cold, drought, ultraviolet light or high temperature stress.¹¹⁹ GB might be involved in preventing accumulation of ROS, protecting membrane, and photosynthetic machinery, and activating several genes associated with stress.^120,125 The ROS detoxification by GB as well as the reduced accumulation of ROS in transgenic plants under drought stress condition has been reported and even very lower concentration of GB provides tolerance to abiotic stress conditions.^126,127 It is also mentioned that GB enhanced the activity of photosystem-II leading to improved abiotic stress tolerance.¹²⁶ It is reported that exogenous application of GB to lower- or non-accumulating plants helps in reducing adverse effects of abiotic stresses.⁹³ Moreover, GB improved photosynthesis and reduced oxidative damages with a view to conferring heavy metal stress particularly cadmium in Gossypium hirsutum L.¹²⁸

GB treatment enhanced the antioxidant enzyme activity, reduced ROS accumulation and thus exhibiting tolerance against chilling injury in Crataegus monogyna.¹²⁹ Foliar application of GB increased both the salinity and drought tolerance in soybean (Glycine max).^96,97 Salinity tolerance in response to GB has also been observed in mung bean (Vigna radiata L.),¹⁰¹ green bean (Phaseolus vulgaris L),¹³⁰ and soybean (Glycine max).^131,132

Polyols (Sugar alcohols)

Polyols such as glycerol, mannitol, sorbitol, ononitol and pinitols etc. act as ROS scavengers, thus prevents lipid peroxidation and subsequently reduce cell damage. In general, myo-inositol, D-pinitol, and D-ononitol have the ability of scavenging hydroxyl radicals.¹³³ Under salinity stress, with the overexpression of enzymes like NADPH dependent mannitol 1–phosphate dehydrogenase in tobacco and Arabidopsis, plays essential role in the synthesis of mannitol thus provides potential tolerance.^134,135 It is found that mannitol produced in a considerable amount in Apium graveolens under abiotic stress conditions.¹³⁶ Polyols have been found to synthesize with regard to freezing stress acting as osmoprotectants in halophytic plants, algae, and some insects.¹³⁶

Glucose-6-phosphate, on the other hand, serves as the precursor for the synthesis of several metabolites which provides protection against stresses revealed that polyols serve dual purposes both against stress protection as well as in maintenance of cells redox control.

Some stress tolerant plants showed a higher amount of cyclitols than mannitol and sorbitol. The genes involved in the synthesis of the cyclitols and modulation of their regulation can be important traits in developing abiotic stress-tolerant crops. It has been perceived that myoinositol converted into osmoprotectants D-ononitol and D-pinitol by a dual-step pathway which is primarily regulated by abiotic stress conditions.^137–140

Polyamines

Polyamines, a nitrogenous compounds, are ubiquitous in every alive cells and have been specified to take part in various cellular mechanisms.^141–148 Several types of polyamines such as diamine putrescine, triamine spermidine, and tetramine spermine play important role in the mitigating mechanism against extreme environmental stresses.^149–151 Accumulation of polyamines, for example, homospermine and cadaverine has been well documented in different plant tissues during normal developmental phases as well as during abiotic stresses. Their genetic actions have been ascribed to their cationic behavior which permits them to act together with all the negatively charged cellular components such as DNA, RNA, phospholipids and proteins.^{145,152–154} The beneficial role of polyamines is in their ability to block ion channels (hence, achieve osmotic adjustment by means of inorganic ions) and in ROS scavenging.

An elevation in the putrescine level has been reported during chilling stress in Arabidopsis.¹⁵⁵ Similar results has been reported in the case of wheat under cold hardening.¹⁵⁶ Exogenous spermidine treatment in both salt-sensitive and salt-tolerant rice cultivar shows recovery against salinity stress-induced plasma membrane injury.¹⁵⁷ Spermine on the other hand, inhibits DNA oxidative degradation carried out by hydroxyl radical in Mesembryanthemum crystallinum, thus ensuring the functions of polyamine as a potential ROS scavenger osmolytes.¹⁵⁸ Exogenous application of spermidine and putrescine increased the postharvest shelf‐life of Capsicum annuum L,⁴⁴ and improved grain filling and drought tolerance in wheat.¹⁵⁹ Putrescine treatment improved water content of leaf, dry matter accumulation, antioxidant activities and decreased cell injuries in Thymus vulgaris L. under water stress situations.¹⁶⁰ Putrescine, spermidine, and spermine were showed to increase drought tolerance¹⁶¹ by increasing soluble protein content, relative water content, chlorophyll value, net photosynthetic rate and salinity tolerance in mung bean (Vigna radiata L.).¹⁶² It is reported that putrescine exhibited salinity tolerance in pigeon pea (Cajanus cajan) by modulating anabolic and catabolic enzyme activities responsible for putrescine biosynthesis.¹⁶³

Bioengineering: Osmolyte induced stress tolerances

Bioengineering of osmolytes biosynthetic and metabolic genes has paved the pathway for comprehensive investigation regarding significance of osmolytes during abiotic stress responses.³⁸ The improved level of compatible nontoxic osmolytes, radical scavengers, and other transgene produces has been confirmed with the abiotic stress tolerance.⁵⁶ Advancement in the process of cellular and molecular biological tools has made it realistic to clone potential osmolyte biosynthetic genes and transfer them into required crop plants.¹⁶⁴ It is mentioned that overproduction of proline synthesis genes improved drought stress tolerance in tobacco plants.⁵⁰ A list of transgenic plants engineered to osmolyte-synthesizing or metabolic genes and their tolerance to stresses have been presented in Table 1. Overexpression of MfMIPS1 (Medicago falcate myo-inositol phosphate synthase) in tobacco resulted enriched resistance to abiotic stresses namely, cold, drought and salinity in transgenic tobacco plants.¹⁶⁵ Similar tolerances has been reported in the transgenic sweet potato plant which expresses betaine aldehyde dehydrogenase (BADH) gene.¹⁶⁶ Transgenic Brassica plants containing choline oxidase (codA) gene showed improved resistance to multiple abiotic stresses due to increased glycinebetaine accumulation.¹⁶⁴ In addition, several studies stated that otsA (trehalose-6-phosphate synthase) and otsB (trehalose-6-phosphate phosphatase) genes from E. coli showed more drought tolerance than controls in raising transgenic tobacco plants.^69,167

Table 1. Overexpression of osmolytes biosynthetic genes in transgenic plants showing stress tolerance

Transgenic plant	Gene and gene source	Gene product	Osmolytes	References
Rice (Oryza sativa)	Cod A from spinach and Arthrobacter	Choline oxidase	Glycine betaine	^Citation168,Citation169
Wheat (Triticum aestivum L.)	MtlD from E. coli	Mannitol-1-phosphate dehydrogenase	Mannitol	^Citation170
Tomato (Solanum lycopersicum)	TPS1 from Saccharomyces cerevisiae	Treahalose-6- phosphate synthase	Trehalose	^Citation171
Arabidopsis	P5CS1 from Arabidopsis thaliana	Pyrroline-5- carboxylate synthetase	Proline	^Citation172
	TPS1-TPS2 from Saccharomyces cerevisiae	Treahalose-6- phosphate synthase	Trehalose	^Citation173,Citation174
Tobacco (Nicotiana tabacum L.)	CDH and BADH from E. coli	Choline dehydrogenase and betaine aldehyde dehydrogenase	Glycine betaine	^Citation175,Citation176
	BvCMO from Beta vulgaris	Choline monooxygenase	Glycine betaine	^Citation177
	BADH from Spinacia oleracea and Oryza sativa	Betaine aldehyde dehydrogenase	Glycine betaine	^Citation178,Citation179
	P5CS from Vigna Aconitifolia	Pyrroline-5- carboxylate synthetase	Proline	^Citation50,Citation135
	MtlD from E. coli	Mannitol-1-phosphate dehydrogenase	Mannitol	^Citation135
	TPP and TPS1 from Saccharomyces cerevisiae	Trehalose-6- phosphate phosphatize and treahalose-6- phosphate synthase	Trehalose	^Citation180,Citation181

Using the yeast, TPS1 gene in tomato plants had shown improved tolerance possibly by the carbohydrate alterations generated by trehalose biosynthetic pathway.¹⁷¹ Altered cultured tobacco cell lines with ectA, ectB and ectC showed higher resistance to mannitol-induced osmotic stress with the control of the constitutive CaMV 35S promoter¹⁸² and showed enhanced nitrogen supply to leaves by enhancing transpiration and by protecting RuBisCO proteins.¹⁸³ mentioned that transgenic plant lines of Petunia hybrida showed improved tolerance to drought stress which have been developed by 1-pyrroline-5-carboxylate synthetase genes (AtP5CS gene taken from Arabidopsis thaliana L. or OsP5CS gene from Oryza sativa L.) and they accumulated higher proline.¹⁸⁴ The transgenic wheat plants (VaP5CS from Vigna aconitifolia) showed increased tolerances to drought stress as well.¹⁸⁵ Abiotic stress conditions namely, salt, poly ethylene glycine, abscisic acid, and heat stresses showed overexpression of P5CR in Arabidopsis. Moreover, overexpression of proline P5CR increased proline accumulation in soybean (Glycine max L. Merr. cv. Ibis) exhibiting better drought tolerance.^186,187 It is documented that maize inbred line DH4866 which was transformed with the betA gene encoding choline dehydrogenase accumulated increased level of GB and showed improved drought stress tolerance.

The potential parameters for drought tolerance are improved osmotic adjustment, reduced ion leakage, lipid membrane peroxidation, and improved level of relative water content when plants exposed to stress conditions.¹⁸⁸ Experiment shows that transgenic cotton developed by introducing CMO gene (AhCMO) replicated from Atriplex hortensis accumulated higher GB than those of non-transgenic plants in both at general and salinity stress (150 mM NaCl). Transformed wheat with the betA gene has shown tolerance to salt stress.¹⁸⁹ Moreover, overexpression of betaine by the influence of betaine aldehyde dehydrogenase (BADH) through chloroplast genetic engineering demonstrate to be a vital approach with a view to conferring salt tolerance on preferred crops.^190,191 In addition, tobacco plants which were introduced with BADH gene for betaine aldehyde dehydrogenase showed the capability of producing GB in chloroplasts conferring salinity stress.

Transgenic plants resulted significantly better seedling growth having greater ribulose 1, 5 bisphosphate carboxylase, and phosphoenolpyruvate compared to the wild type.¹⁷⁹ Under salinity stress, transgenic rice plants overexpress trehalose synthesis genes (otsA and otsB), accumulated higher trehalose content and showed higher photosynthetic capacity, decreased photooxidative damage, as well as improved ion uptake and partitioning during salt stress.¹⁹² In transgenic potato plant using the yeast TPS1 gene showed improved tolerance against drought stress compared to the wild type.¹⁹³ Rice OsTPP1 and OsTPP2 were transiently induced for conferring chilling, salinity and drought stress and external applications of ABA enhanced abiotic stress tolerance of rice plants.^194,195 Several studies stated that transgenic Arabidopsis plants overexpressing TPS1¹⁹⁶ and tomato transgened with yeast TPS1 gene revealed to be drought tolerant.^171,197 Abebe, et al.¹⁷⁰ reported that ectopic expression of the mtlD gene from Escherichia coli for the accumulation of mannitol ensured improved tolerance to water as well as salinity stress in wheat Similar results has been observed under salinity and drought conditions which meaningfully increased mannitol transport activity and OeMaT1 expression, thus conferring olive trees to survive under salinity and drought by coordinating mannitol transport with cellular metabolism.¹⁹⁸

Research showed that engineered Nicotiana tabacum and Populus tomentosa accumulates mannitol by introducing Escherichia coli mannitol-1-phosphate dehydrogenase (mltD) resulted in better salt-tolerant plants.^199,200 Research also showed that tobacco plant transformed with imt1 added significantly higher D–ononitol and showed enhanced tolerance against drought and salt stress conditions.²⁰¹ Tobacco plant engineered with sacB gene for levansucrase has been showed enhanced drought tolerance.²⁰² In transgenic rice with overexpressed ADC gene from Datura stramonium accumulates higher amount of putrescine exhibiting tolerant to drought stress.^203,204 It is mentioned that SAMDC gene of tritordeum was introduced in rice plants which accelerated a three- to fourfold increase in the level of spermidine and thus conferring salt tolerance.¹⁴⁴ found that overexpressed SAMDC gene of Arabidopsis in tobacco plants exhibit tolerance toward multiple stress.²⁰⁵ Overexpression of SPDS (spermidine synthase) from Cucurbita ficifolia in Arabidopsis manifested a wide spectrum of tolerance toward chilling, freezing, salinity, hyperosmosis, drought stress.²⁰⁶ Overexpression of SAMDC from Dianthus caryophyllus in transgenic tobacco manifested a wide spectrum of tolerance toward salinity, chilling and oxidative stress.²⁰⁶

It has been found that overexpression of apple MdSPDS1 gene in European pear (Pyrus communis L.) increases the tolerance to multiple abiotic stresses by altering polyamine level.²⁰⁷ Similarly, transgenic eggplants with oat ADC gene displayed an upsurge in tolerance toward drought, salinity, low, high temperature, and heavy metal stress.²⁰⁸ Thus, to mitigate the ever-increasing demand of food crops across the world, transgenic approach involving osmolytes biosynthetic genes is considered as a proficient strategy to improve crop tolerance to stress.

Conclusions and perspectives

This review article highlighted various positive influences of osmolytes on plants together with the ability to induce abiotic stress tolerance. The synthesis and stress mitigation roles of osmolytes could be considered as a promising tool to improve the quality and quantity of agricultural crops which ultimately contribute to achieving sustainable development goal number two, that is, zero hunger. According to several studies, the biosynthesis and regulatory genes from different sources have been successfully exploited for generating stress-tolerant transgenic plants which have better capability to rapidly accumulate satisfactory amounts of osmolytes. The different candidate genes for the osmolyte biosynthesis pathway can be utilized for better survival of several crop plants. Due to rapid global climate change, researches need to focus on utilizing the benefits of osmolyte-mediated crop improvement to contribute in global food security. Advancements in gene insertion and manipulation might improve the generation of super crops using super genes from different sources by boosting their ability to accumulate osmolytes for better yield as well as ensure survival under various stress conditions. Many approaches including biochemical and transgenic have been put forward to develop stress tolerance or resistance in plants, although most of them have been found partially successful. Further researches need to be conducted for exploring the actual signaling behavior of different osmolytes in many cases where it is still largely unrevealed for increasing our knowledge of the actual mechanisms for plant abiotic stress tolerance and adaptation. With the exogenous application of osmolytes, the frequency of field research for a wide range of globally important crops needs to be substantially increased along with cost-effectiveness in mitigating various abiotic stresses.

Acknowledgments

Authors acknowledge Ministry of Science and Technology, People’s Republic of Bangladesh for financial support regarding this study.

Disclosure statement

Authors declare no conflict of interest.

Additional information

Funding

This work was supported by the Ministry of Science and Technology, Government of the People’s Republic of Bangladesh.