Abstract
Glycinebetaine (GB) is one of the most studied and effective compatible solutes, and the exogenous application of GB can improve the tolerance of numerous plant species to various types of abiotic stresses, such as low temperature, high temperature, salt, drought and heavy metals, thereby enhancing subsequent growth and yield. In this chapter, we summarize our understanding of the research on exogenous GB under abiotic stress as an adaptive mechanism, with particular emphasis on the new insights into the molecular and physiological mechanisms involved in the exogenous GB-mediated modulation of abiotic stress tolerance in plants.
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Keywords
- Glycinebetaine
- Exogenous application
- Abiotic stress
- Antioxidative defence
- Photosynthetic machinery
- Plant hormones
- Gene expression
1 Introduction
Because of their sessile character, in the natural environment, plants are most frequently subjected to various types of abiotic stresses, such as salinity, drought, flooding, extreme temperatures, nutrient deficiency, heavy metals and high light intensities, all of which frequently exhibit decreased vegetative growth and negative impacts on crop production and reproductive capabilities (Tuteja et al. 2011; Kurepin et al. 2015; Kumar et al. 2017). One of the best-documented and most important abiotic stress-responsive mechanisms in plants is the biosynthesis and accumulation of compatible solutes (Kumar et al. 2017), such as proline, glycinebetaine, trehalose and polyols (Khan et al. 2009; Jewell et al. 2010; Giri 2011; Kumar and Khare 2015). Glycinebetaine (GB), a fully N-methyl-substituted derivative of glycine found in a large variety of microorganisms, higher plants, and animals, is one of the best-studied compatible solutes that enables plants to tolerate abiotic stress (e.g. Rhodes and Hanson 1993; Chen and Murata 2002, 2008, 2011; Takabe et al. 2006; Masood et al. 2016). GB belongs to a group of compounds collectively known as ‘compatible solutes’, small organic metabolites that are very soluble in water and nontoxic at high concentrations. Both the exogenous application and the genetically engineered biosynthesis of GB increase the tolerance of plants to abiotic stress (Chen and Murata 2002, 2008, 2011).
The exogenous application of GB can improve the tolerance of numerous plant species to various types of abiotic stresses, and it can enhance subsequent growth and yield. The GB applied to roots is usually taken up and accumulated in the cytosol, and only a small amount is translocated to chloroplasts. When applied to leaves, GB is translocated to meristematic tissues, in particular, flower buds and shoot apices, and then translocated to actively growing and expanding tissues (Mäkelä et al. 1996; Park et al. 2006). In plants, even if GB is applied to old or mature tissues, this solute reallocates to young actively growing tissues, where its protective functions are mainly required (Ladyman et al. 1980; Annunziata et al. 2019).
Due to the beneficial effects of GB, numerous experiments on the exogenous application of this compatible compound on low accumulator and non-accumulator plant species have been performed (Annunziata et al. 2019). In this chapter, we summarize and discuss the current understanding of the physiological and molecular mechanisms of exogenous GB, including the regulation of reactive oxygen species (ROS) scavenging and detoxification under stress, protection of the photosynthetic machinery, interactions and synergistic physiological effects of GB with plant hormones and metabolites and the induction of specific genes involved in stress tolerance. The future perspective of the exogenous application of GB is also discussed.
2 Exogenous Glycinebetaine Enhances Abiotic Oxidative Stress Tolerance
All forms of abiotic stress, including drought, salinity, heat, cold, nutrient deficiency, heavy metals, high light intensities and UV radiation, can cause an excessive accumulation of ROS, leading to various types of deterioration, irreparable dysfunction and cell death in plants (Ashraf 2009; Chen and Murata 2011; Ahmad et al. 2013; Kumar et al. 2017).
At present, many studies have shown that the exogenous application of GB on plants enhances oxidative stress tolerance (e.g. Park et al. 2006; Hoque et al. 2007, 2008; Farooq et al. 2008a, b; Hossain et al. 2010, 2011a, b, 2014; Anjum et al. 2012; Hu et al. 2012; Hasanuzzaman et al. 2014; Yildirim et al. 2015; Kumar et al. 2017). Ma et al. (2004) found that exogenous GB application ameliorated the water status of and improved the antioxidant enzyme activities in water-stressed wheat (Triticum aestivum L.) seedlings. Moreover, in fine rice (Oryza sativa), the exogenous application of GB significantly enhanced drought tolerance by altering the level of ROS and malondialdehyde (MDA), increasing the activities of enzyme antioxidants and promoting seedling growth (Farooq et al. 2008b). Additionally, in two maize (Zea mays L.) cultivars, prolonged drought stress increased lipid peroxidation, whereas GB treatment significantly reduced oxidative damage, as indicated by lower MDA levels. Importantly, GB-treated plants maintained higher antioxidant enzyme activity than did non-GB-treated plants in the course of drought stress, which ultimately enhanced the growth and yield of maize (Anjum et al. 2012). Furthermore, Molla et al. (2014) also demonstrated that the exogenous application of GB resulted in a significant increase in the glutathione (GSH) content and maintenance of the high activities of glutathione S-transferase (GST) and glyoxalase I (Gly I) enzymes, with a simultaneous reduction in glutathione disulfide (GSSG) and hydrogen peroxide (H2O2) levels in lentil (Lens culinaris) seedlings compared to control plants under drought stress, indicating that exogenous GB application enhances drought stress tolerance by limiting H2O2 accumulation and increasing the activities of the antioxidant and glyoxalase systems (Molla et al. 2014).
Additionally, the protective roles of GB in modulating cold-, heat- and salinity-induced oxidative stress tolerance have also been well documented in plants. Park et al. (2006) showed that after the exogenous application of GB on tomato (Solanum lycopersicum) plants, the level of catalase activity and expression of the catalase gene (CAT1) were higher, and the H2O2 levels were lower in GB-treated plants than in control plants during 2 days of chilling treatment, indicating that GB may participate in the induction of H2O2-detoxifying antioxidant systems, namely, enhanced catalase expression and catalase activity, when the plants were exposed to chilling stress (Park et al. 2006). Moreover, seed treatments with GB in hybrid maize reduced membrane electrolyte leakage (EL) and maintained higher tissue water contents, antioxidant enzyme activities and carbohydrate metabolism (Farooq et al. 2008a). Furthermore, under cold stress, the exogenous application of GB showed a protective effect on tea buds by regulating the formation of methylglyoxal (MG) and lipid peroxidation and by activating or protecting some antioxidant and glyoxalase pathway enzymes (Kumar and Yadav 2009).
Similar effects were also observed in plants under heat stress. Sorwong and Sakhonwasee (2015) reported that the foliar application of GB enhanced heat stress tolerance in marigold (Calendula officinalis) cultivars by reducing the levels of H2O2, superoxide and MDA, indicating that GB may be involved in the induction of ROS detoxification, thereby mitigating the effect of heat stress on marigolds. Similarly, salinity stress inhibited the growth and development of most plants as a result of the overproduction of ROS, whereas exogenous GB ameliorated the detrimental effect of salinity stress on plants. Hoque et al. (2007) revealed that exogenous GB enhances salinity-induced oxidative stress tolerance in cultured tobacco (Nicotiana tabacum) (BY-2) cells by modulating the activities of ascorbate-glutathione (AsA-GSH) cycle enzymes and GST, glutathione peroxidase (GPX) and glyoxalase system enzymes activities and reducing protein oxidation (Hoque et al. 2008). In addition, compared with control plants, in mung bean seedlings under salinity stress, the exogenous application of GB resulted in a conspicuous increase in the GSH content and the maintenance of a high glutathione redox state and higher activities of correlative enzymes involved in the ROS and methylglyoxal (MG) detoxification system, with a simultaneous decrease in the GSSG content and the levels of H2O2 and lipid peroxidation, suggesting that GB provides a protective action against salt-induced oxidative damage by activating antioxidant defence and MG detoxification systems and reducing the levels of H2O2 and lipid peroxidation (Hossain and Fujita 2010). Moreover, Nawaz and Ashraf (2010) found that compared with control maize plants, in two maize genotypes, the exogenous application of GB, as a modulator of salt tolerance, prominently enhanced the activities of superoxide dismutase (SOD), catalase (CAT) and peroxidase (POD). Furthermore, compared with control plants, in perennial ryegrass (Lolium perenne) under salinity stress, the exogenous application of GB enhances salinity stress tolerance by reducing the content of EL, MDA, and proline and increasing the vertical shoot growth rate (VSGR), relative water content (RWC), relative transpiration rate (Tr), chlorophyll (Chl) content and activities of SOD, CAT and ascorbate peroxidase (APX) (Hu et al. 2012). Recently, Kotb and Elhamahmy (2014) showed that long-term exogenous GB application at a suitable concentration (50 mM) on bread wheat under saline soil conditions significantly increased enzymatic antioxidant activities, total chlorophylls, leaf osmotic potential and the K+ contents in leaves and grain, thereby alleviating the oxidative stress damage of salinity stress, reflected by improving the growth and productivity of bread wheat plants. In addition, Hasanuzzaman et al. (2014) found that the exogenous application of GB on rice seedlings enhanced salinity-induced oxidative stress tolerance by the upregulation of the ROS and MG detoxification pathways. Similarly, in lettuce (Lactuca sativa L.) plants, exogenous foliar applications of GB mitigated the deleterious effects of salt stress by reducing membrane permeability and the MDA and H2O2 content (Yildirim et al. 2015).
The protective roles of GB have also been reported in plants subjected to nitrogen deficiency and cadmium (Cd) stress. Under nitrogen stress conditions, the exogenous application of GB was beneficial for improving the endogenous nitrogen status (Bowman and Rohringer 1970) and thereby enhancing photosynthesis and activating the antioxidant defence system in plants (Ashraf and Foolad 2007; Hoque et al. 2008). Additionally, the exogenous application of varying doses of GB on maize plants resulted in a significant decrease in lipid peroxidation and the intercellular CO2 concentration (Ci), while an increase in the content of leaf total nitrogen and endogenous GB, net photosynthetic rate (Pn), and SOD, CAT, phosphoenolpyruvate carboxylase (PEPCase) and ribulose-1,5-bisphosphate carboxylase (RuBPCase) activities were observed under nitrogen stress (Zhang et al. 2014). Cd is a highly toxic environmental pollutant that can produce excessive ROS, resulting in cellular damage through the oxidation of membrane lipids, proteins and nucleic acids (Flora 2009; De Maria et al. 2013; Lou et al. 2015). Nevertheless, many researchers have demonstrated that exogenous GB ameliorates the adverse effect of Cd stress on plants. Hossain et al. (2010) showed that compared to control plants, the exogenous application of GB on mung bean (Vigna radiata L.) seedlings enhanced Cd tolerance by decreasing H2O2 and MDA levels and enhancing the activities of the relative enzymes involved in ROS and MG detoxification systems. Moreover, Duman et al. (2011) concluded that the use of exogenous GB on an aquatic plant (Lemna gibba L.) relieved the deleterious effects of Cd stress by reducing both ROS and MDA levels, as well as enhancing photosynthetic activity, endogenous proline accumulation and antioxidant enzyme activities. Furthermore, compared with control plants, exogenous applications of GB on perennial ryegrass resulted in alleviating the detrimental effect of Cd stress by elevating SOD, CAT and POD activities and higher stress-responsive gene expression (Lou et al. 2015).
From the above reports, it has become clear that GB performs a pivotal function in maintaining ROS levels by modulating the activities of correlative enzymes involved in ROS scavenging and detoxification and the glyoxalase system under various abiotic stresses.
3 Exogenous Glycinebetaine Protects Photosynthetic Machinery Under Abiotic Stress
One of the physiological processes greatly affected by abiotic stress in plants is photosynthesis, and within the photosynthetic machinery, photosystem II (PSII) is the most vulnerable and crucial component that bears the brunt of abiotic stress (Nishiyama et al. 2006; Takahashi and Murata 2008; Nishiyama and Murata 2014; Gururani et al. 2015).
Under no-stress conditions, exogenous glycinebetaine can improve the growth, CO2 assimilation and PSII photochemistry of maize plants, and the enhanced CO2 assimilation rate may be explained by the increased stomatal conductance (Yang and Lu 2006). It is now evident that exogenous glycinebetaine can also play a pivotal role in protecting the photosynthetic machinery in plants under various stressful conditions, which is considered to be one of the major mechanisms of attaining relief from abiotic stress (Chen and Murata 2011; Masood et al. 2016; Kurepin et al. 2017). Exogenous GB application improves CO2 assimilation under drought stress (Mäkelä et al. 1998, 1999; Xing and Rajashekar 1999) and salinity stress (Mäkelä et al. 1998, 1999; Lopez et al. 2002). The exogenous application of GB increased the relative area of starch granules in salt-stressed tomato leaflets and the relative area of plastoglobuli in GB-treated tomato plants under drought stress (Mäkelä et al. 2000). Furthermore, the application of GB on spinach leaves alleviated the photodamage of photosystem I (PSI) submembrane particles by minimizing the alteration in photochemical activity and chlorophyll-protein complexes under cold stress conditions (Rajagopal and Carpentier 2003). Foliar-applied GB also prevented photoinhibition in wheat under freezing (Allard et al. 1998) and drought stresses (Ma et al. 2006). Yang and Lu (2005) observed that the exogenous application of GB on maize plants improved photosynthesis by improving stomatal conductance and PSII efficiency. Similarly, in salt-stressed wheat plants, the application of GB mitigated the adverse effects on photosynthetic capacity by favouring the net CO2 fixation rate, increasing stomatal conductance and protecting the photosynthetic pigments in wheat cultivars (Raza et al. 2006). In another study, the foliar application of GB increased chlorophyll content, gas exchange and photosynthesis, alleviated the deleterious effect of drought on Hill reaction activities and improved the modified lipid composition of the thylakoid membranes in drought-stressed wheat cultivars (Zhao et al. 2007). When tobacco is subjected to low-temperature stress, the exogenous application of GB to plant roots could protect violaxanthin de-epoxidase and enhance non-radiative energy dissipation (NPQ), thereby improving the function of the thylakoid membrane (Wang et al. 2008).
Moreover, pretreating rice plants with GB maintained a higher net photosynthetic rate and CO2 assimilation rate compared with those of control plants during drought stress (Farooq et al. 2008b). Analogously, foliar-applied GB maintained water-use efficiency and pigments and increased plant height and the net photosynthetic rate when rice plants were exposed to salt stress (Cha-um and Kirdmanee 2010). Under heat stress, Oukarroum et al. (2012) reported that the foliar application of GB on barley (Hordeum vulgare L.) plants mitigated thermal stress by protecting the oxygen-evolving complex and increasing the energy connectivity between the PSII antennae to increase the stability of the system PSII, thereby reinforcing the heat tolerance in GB-treated plants. In salt-stressed canola plants, foliar-applied GB improved the water-use efficiency, photosynthetic CO2 fixation and stomatal conductance while protecting the oxygen-evolving centre of PSII and maintaining the activity of PSII (Athar et al. 2015). Furthermore, Gupta and Thind (2015) found that the exogenous application of GB on bread wheat plants prominently improved their photosynthetic performance due to more utilization of glutathione and high levels of ascorbic acid in wheat flag leaves under drought stress, indicating the role of nonenzymatic antioxidants in sustaining photosynthetic efficiency and yield stability under prolonged field drought stress conditions. Stepien et al. (2016) clearly demonstrated that the foliar application of exogenous GB could significantly mitigate the adverse effects of aluminium (Al) stress in cucumber (Cucumis sativus L. cv. Wisconsin) seedlings by protecting the photosynthetic apparatus components, leading to improved electron transport, gas exchange and enzymatic CO2 fixation.
The exogenous application of GB plays a role in protecting the photosynthetic machinery in plants via improving the CO2 assimilation rate and chlorophyll content, as well as ameliorating the negative effect of photodamage and maintaining thylakoid membrane stabilization during various types of abiotic stresses.
4 Interactions of Exogenous Glycinebetaine with Plant Hormones and Metabolites Under Abiotic Stress
During the life span of plants, plant hormones are synthesized in very minute quantities, and these compounds regulate the development and growth of plants and play pivotal roles under various types of abiotic stresses (Masood et al. 2012, 2016; Khan et al. 2013, 2015; Khan and Khan 2014; Asgher et al. 2014, 2015). Many scientists have suggested that the interactions of exogenous GB, plant hormones, and metabolites can be beneficial to plants in abiotic stress tolerance (Yang et al. 2012; Aldesuquy et al. 2012; Yildirim et al. 2015; Gupta and Thind 2019).
The foliar application of either GB or abscisic acid (ABA) on creeping bentgrass (Agrostis stolonifera) and Kentucky bluegrass (Poa pratensis) similarly suppresses membrane EL and the accumulation of MDA and increases the activities of APX, POD, and SOD during prolonged periods of drought or salinity stress, indicating that the foliar application of ABA or GB could mitigate physiological damage in turfgrass under drought or salt stress (Yang et al. 2012). Similarly, in a recent study of wheat under water deficit conditions, the application of either salicylic acid (SA) or GB similarly increased grain yield; nevertheless, their co-application was more pronounced than the application of either applied alone due to the repairing effect of the provided chemicals on the growth and metabolism of wheat plants under drought stress (Aldesuquy et al. 2012).
Yildirim et al. (2015) reported that compared to control plants, the foliar application of GB on lettuce plants mitigated the deleterious effect of salt stress by alleviating stomatal conductance, water status, plant nutrient uptake and soluble sugar content and elevating the concentrations of gibberellin (GA), SA and indole acetic acid (IAA) . Additionally, another study demonstrated that the foliar application of 100 mM GB on 19 wheat genotypes resulted in a higher total soluble sugar content under drought stress, whereas the starch content was reduced in GB-treated plants during anthesis. Furthermore, GB application also led to a decline in the activity of leaf sucrose phosphate synthase and sucrose synthase at both tillering and anthesis stages, confirming that exogenous applications of GB could alter the levels of the various sugar components that coordinate the drought response of selected wheat genotypes, resulting in grain yield benefit under prolonged field drought stress (Gupta and Thind 2019).
5 Exogenous Glycinebetaine Induces Specific Gene Expression
GB in the micromolar range, either after the uptake of exogenous GB in plants or as a result of its genetically engineered synthesis, can confer tolerance to several types of stresses (Einset et al. 2007; Chen and Murata 2008, 2011).
Allard et al. (1998) demonstrated that the exogenous application of GB enhanced the freezing tolerance of wheat plants. Immunoblot analysis revealed that WCOR410, a low-temperature-inducible protein, was accumulated in the presence of GB, and the ultimate level depended on the concentration of GB. Similarly, northern blotting analysis also illustrated that GB treatment resulted in the induction of a subset of low-temperature-responsive genes, such as WCOR410 and WCOR413, indicating that GB elevated the freezing tolerance of plants by inducing the expression of low-temperature-responsive genes. In tomato plants, after the exogenous application of GB, the level of catalase activity and expression of the catalase gene (CAT1) were higher than those in control plants during 2 days of chilling treatment, suggesting that GB may increase catalase expression and catalase activity when the plants were exposed to chilling stress (Park et al. 2006). Additionally, the exogenous application of GB on both the leaves and roots of Arabidopsis thaliana resulted in the upregulated expression of the genes in roots, including those for membrane-trafficking components, NADP-dependent ferric reductase, transcription factors and ROS-scavenging enzymes, suggesting that GB may confer chilling tolerance to plants by activating the expression of a number of stress-tolerance genes (Einset et al. 2007, 2008). Furthermore, compared to controls, exogenous GB application on tomato seeds under high-temperature stress resulted in elevated levels of heat-shock genes, such as MT-sHSP, HSP70 and HSC70, and accumulated HSP70 protein (Li et al. 2011).
Consequently, based on previous research on the concentrations of GB and testimony of its effects on gene expression, it is reasonable to postulate that, at least in part, the effects of GB might be ascribed to the induction and activation of the expression of stress-tolerance genes (Einset et al. 2007; Chen and Murata 2008, 2011). Further studies on the identification of GB-inducible genes and the functions of their products will advance our understanding of the GB-enhanced tolerance in plants under abiotic stress.
6 Conclusion and Future Perspectives
The exogenous application of GB can improve the tolerance of numerous plant species to various types of abiotic stresses, and due to its multiple functions, the possible mechanisms of the exogenous GB-induced tolerance of plants to various types of abiotic stresses include but are not limited to (i) the regulation of ROS scavenging and detoxification under stress, (ii) the protection of the photosynthetic machinery, (iii) interactions with plant hormones and metabolites and (iv) the induction of specific genes whose products are involved in stress tolerance.
Although research on the improvement of plant resistance by GB has made great progress, more in-depth studies are needed to reveal subtler regulatory roles for GB in modulating abiotic stress tolerance. For instance, why specific genes are direct targets of GB and whether GB could modulate the tolerance of plants under biotic stress, as well as how to use GB more effectively to develop crops with enhanced tolerance to multiple environmental stresses in the field.
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Acknowledgements
This work was supported by the National Natural Science Foundation of China (31470341, 31870216) and the State Key Basic Research and Development Plan of China (2015CB150105).
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Zhang, T., Yang, X. (2019). Exogenous Glycinebetaine-Mediated Modulation of Abiotic Stress Tolerance in Plants: Possible Mechanisms. In: Hossain, M., Kumar, V., Burritt, D., Fujita, M., Mäkelä, P. (eds) Osmoprotectant-Mediated Abiotic Stress Tolerance in Plants. Springer, Cham. https://doi.org/10.1007/978-3-030-27423-8_6
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