Cultivation of Tomato under Dehydration and Salinity Stress: Unravelling the Physiology and Alternative Tolerance Options

Abstract

Tomato is an important fruit vegetable in the world, as a nutritional source and an income option for a majority of resource constrained households. However, tomato supply in developing countries is often fluctuating, with high scarcity in both supply and quality during rainy season. Unlike many crops, cultivation of tomato is a challenging task during rainy season, with high pest and disease infestation. Hence, dry season is the most favorable period for tomato cultivation. However, inadequate water supply poses a yet another significant hurdle, as the crop requires high soil moisture for optimum growth. According to a landmark study by FAO, Tomato has a yield response factor of 1.05, which signifies that a smaller decline in water uptake results into a proportionally larger decline in yield. Moreover, over the years, there have been increasing reports of soil salinization, which imposes similar effects to drought stress through osmotic effects of Na+ in the soil solution and oxidative stress through excessive generation of reactive oxygen species. This chapter will dissect how tomato plants respond to these abiotic stress factors on physiological, anatomical, and molecular levels and suggest options to improve the crop’s productivity under these constraining environments.

1. Introduction

Global changes in the climate scenario undeniably pose insurmountable challenge on global food supply system. Formerly agriculturally productive lands are insidiously becoming unarable. Yet, global population is steadily increasing, projected to reach an insane 9.8 billion by 2050 [1]. Therefore, finding ways to sustain agricultural productivity in light of the prevailing and worsening climate to support the growing population is one of the current and future’s major global hurdles. Persistent droughts, extreme temperatures, soil salinization, and heat stresses have gradually become abiotic norms in the agricultural setting.

Tomato is among the most commercially important fruit vegetables globally [2, 3]. In one of the FAO’s milestone publications on crop water relations, tomato was established to have a yield response factor (Ky) of 1.05, indicating that a small decline in water uptake results into a proportionally larger yield decrease [4, 5, 6]. This substantiates the need for development of cultivars that are able to maintain yield or exhibit less yield decline under limited water conditions. Worldwide, agricultural productivity is confronted with accelerating environmental constraints such as drought and salinity. Coupled with the global changes in climate, water stress is progressively becoming a major environmental factor limiting plant growth, development, and yield [7]. Drought and salinity stress impose somewhat similar effects on growth of crop plants, as both result into reductions in soil water availability and plant water uptake capacity. When soil water potential and plant’s turgor fall below a threshold, such that normal plant functioning is perturbed, the soil is said to be droughted [8] or in a state of water stress. Some authors refer to soil as droughted when plant’s water deficiency results from evaporative demand of the atmosphere exceeding plant roots’ capacity to extract soil water [9]. It is indicated that initial reductions in shoot growth under salinity stress are due to increases in plants’ osmotic pressure due to heavy presence of salts around roots, resulting into hormonal signals that eventually reduce stomatal conductance and consequently growth [10]. These effects are similar to those generated by drought stress. Tomato (Solanum lycopersicum L.) is recognized as a crop of an immense economic importance globally [2]. What is more is that drought and soil salinity have considerable impacts on its production [11, 12]. Present understanding proves that water stress perturbs various physiological and biochemical processes [7, 13, 14, 15, 16] eliciting expression of various stress-related genes [12, 17, 18]. Therefore, in order to achieve the required knowledge for attainment of water stress tolerance, it remains imperative to couple physiological analysis’s descriptive power with biochemical, morphological, and transcriptomic analysis [19] in carefully screened and selected varieties with proven differential tolerance under drought stress.

2. Drought stress: an overview

Plant water deficit develops as its demand exceeds the supply of water. The supply is determined by the amount of water held in the soil to the depth of the crop root system. The demand for water is set by plant transpiration rate or crop evapotranspiration, which includes both plant transpiration and soil evaporation. Evapotranspiration is driven by the crop environment as well as major crop attributes such as plant architecture, leaf area, and plant development. Drought stress is often measured by the Palmer Index (the Palmer drought severity index, PDSI), a regional drought index commonly used for monitoring drought events and studying areal extent and severity of drought episodes [20]. The index uses precipitation and temperature data to study moisture supply and demand using a simple water balance model. Water moves into the plant within a physical system also known as the soil-plant-atmosphere continuum (SPAC). Here, water is driven through the plant from the soil to the atmosphere by the difference in water potential between the atmosphere (very low potential) and the soil (relatively high potential when wet).

Plants often receive excessive radiation, out of which only a small fraction is used for photosynthesis (photosynthetically active radiation), while the rest is dissipated as heat and transpiration [21], this led to the term “transpirational cooling.” Transpiration functions to cool leaves relative to ambient temperatures when the environmental energy load on the plant is high, without which plant leaves could heat up to lethal temperatures [22]. When a leaf transpires, leaf water potential becomes more negative (lowers), creating a water potential gradient (pull) that drives water movement into the plant (assuming more water is available in the soil). As the soil gets drier, it is necessary that leaf water potential be reduced further in order to create the required pull to drive water into the plant leaf.

This brings a concept of osmotic adjustment (OA), defined as the net accumulation of solutes after the plant has been exposed to a predetermined rate of water deficit [23]. OA has been suggested as a prime drought stress adaptive engine in support of plant production. Osmotic adjustment (OA) and cellular compatible solute accumulation are widely recognized to have a role in plant adaptation to dehydration mainly through turgor maintenance and the protection of specific cellular functions by defined solutes. A typical leaf cell comprises a battery organic and inorganic osmolytes (osmotically active solutes), such as soluble sugars, proline, and glycine betaine, which determine the leaf osmotic potential. Relatively, osmotic potential is lower than leaf water potential, whose difference is what constitutes turgor potential, a critical determinant of cellular growth and function, devoid of which collapses the cells and wilts the leaves. A lower turgor is typified with stomata closure (as an attempt to reduce transpiration), this reduction reduces intercellular CO₂ concentration (Ci), consequently downregulating CO₂ fixation and photosynthetic assimilation [7, 24] and an increase in leaf temperature [18]. Rise in temperature may get excessive, causing heat damage to the leaf especially under hotter environments. Therefore, turgor maintenance and transpiration are two critical aspects for plants growing under dehydrated conditions. Turgor maintenance can be maintained by sustaining water uptake to keep leaf water potential higher or through accumulation of osmolytes (osmotic adjustment).

At a whole plant level, transpiration rate can be controlled by limiting total leaf area. For example, two plants growing in a pot of similar volume, a large plant will require irrigation more frequently than a smaller one. Reduction of plant size and growth rate has therefore been a key revolutionary feature for plants’ adaptation to drier environments [25]. As such, it has been observed that as water deficit becomes severe, older leaves desiccate and shed off first as an attempt to reduce leaf area and slow down on water requirement, while younger leaves maintain stomatal opening and carbon assimilation. At the crop level, the relationship between plant size and the demand for water can be extrapolated by measurement of leaf area index (LAI), which expresses total area of live leaves per unit ground surface. When LAI is high, crop evapotranspiration (ET) also increases, at least until LAI reaches a maximum threshold beyond which ET does not increase. As the crop matures and leaves senesce, LAI is reduced and so does evapotranspiration. In response to desiccation, growth regulating hormone abscisic acid (ABA) is produced in the shoot, inducing a cascade of responses such as arrested growth, stomatal closure, and reproductive failure. ABA is also produced in the root in direct response to the drying soil and its hardness as it dries. Root ABA is translocated to the shoots via the transpiration stream, eliciting stomatal closure or arrested growth before any water deficit develops in the shoot. This “hormonal or chemical root signal” may therefore serve as an “early warning system” to the plant. This results into the ABA-dependent pathway of signal transduction under drought stress. In this pathway, ABA induces novel protein synthesis, which regulates expression of numerous “ABA responsive” genes. Alternatively, ABA may also regulate stress responsive genes without novel protein synthesis. These gene products are either functional (e.g., water-channel proteins or key enzymes) or regulatory (e.g., protein kinases), and they are involved in mediating various cellular responses. Presently, thousands of “drought stress responsive genes” have been identified that are either upregulated or downregulated under dehydration.

2.1 Responses of tomato plants to drought stress

Physiologically, photosynthesis is one of the highly regulated, sensitive, and primary traits affected by drought [26, 27]. Hence, ability to maintain photosynthetic capacity under water stress deserves solemn consideration when screening for drought stress. Ueda et al. [28] observed that water and salinity stresses downregulate photosynthesis through stomatal and non-stomatal limitations. Yuan et al. [7] observed that under different water stress conditions, reasons for decline in photosynthetic rates are different; with stomatal limitations being more apparent under mild stress while non-stomatal limitations were more prevalent under moderate and severe water stress. This may suggest that severing water stress affects photosynthesis, principally via photosystem damage, inhibition of RuBISCO enzyme and other enzyme activities [29], and these non-stomatal effects may be even more apparent in sensitive cultivars. Furthermore, water stress affects photosynthesis through stomatal closure triggered by root to shoot signaling after sensing lower plant water potential. Thus, cultivars that present higher stomatal conductance under water stress conditions indicate a higher adaptability to water stress [30]. A consequence of inhibited photosynthesis is downregulation of plant growth; however, this cause-effect relationship remains difficult to entangle [31]. Under water stress, accumulation of soluble sugars and other osmolytes has been implicated in osmotic adjustment in tomatoes. Several studies have thus observed and correlated an increase in sugars and proline accumulation with drought tolerance [32, 33]. As a consequence of photosynthetic downregulation, drought stress often results into accumulation of reactive oxygen species (ROS), which damage photosynthetic machinery and cell membranes consequently resulting into cell death [13, 34]. Malondialdehyde is a widely used marker for lipid peroxidation and shows greater accumulation under abiotic stresses [7, 35]. Cell membrane stability and electrolyte leakage have also emerged as important tools in assessing membrane damage elicited by abiotic stress [36, 37].

3. Salinity stress: an overview and effects

The global consequences of the rapidly changing climate scenario imply that the environment for crop growth and development is gradually becoming unbearably altered. Soil salinization for one has victimized agriculture since time immemorial and has remained an important factor constraining worldwide crop productivity [38]. As a result, remarkable strides have been made in unmasking plants’ responses and tolerance mechanisms to salinity stress. Deposition of salts in agricultural fields is principally through rain and wind and in rare cases through weathering of rocks [39]. It is estimated that over 800 million hectares of land are saline representing more than 6% of world’s land area [31]. Spatially, soil salinity is most widespread in arid and semiarid regions in addition to sub-humid and humid climatic conditions. In most cases, these regions experience lower precipitation, yet suffer from higher evapotranspiration rates. This imbalance results into capillary transport of salts from the water table to the ground surface [40]. There are various types of salts that accumulate in the soil and water to agriculturally lethal levels. However, sodium chlorides (NaCl) are considered the most soluble and abundantly released salts, hence have been the subject of considerable research attention insofar as soil salinity is concerned. Soil salinity increases electrical conductivity of soil, hence soils are characterized as saline when its ECe is at least 4 dS/m at 25°C [41], approximately 40 mM NaCl, with about 15% exchangeable sodium [42].

Plants’ responses to soil salinity are governed by complex interactions of morphological, physiological, and biochemical processes, thereby affecting plants from seed germination, vegetative growth, reproductive development [42], and uptake of water and soil nutrients [43]. The complexity of salinity stress renders it particularly difficult to manage as it is associated with interlinked yet dissimilar effects that require different tolerance strategies. The first observable primary effect of salinity on plant growth is the reduction of water uptake capacity of plants. Usually, this effect is as a result of salts outside the roots, which increase the osmotic pressure of water making it harder for plants to take up water [31]. This osmotic component of salinity is rapid, progressing a few hours after encountering soluble salts and is characterized by decreases in new shoot growth, through reductions in leaf expansion rates, slow new leaf emergence, and lateral buds development. As a consequence of the resultant decline in soil water potential and subsequent cell dehydration, osmotic stress induces stomatal closure and a decline in photosynthetic activity that eventually chucks growth [28, 44]. In addition, soil salinity may result into ion toxicity and nutritional imbalances. Na⁺ and K⁺ compete for binding sites, due to their similarity in physicochemical properties [45], such that excess availability of Na⁺ in the growth media results into replacement of K⁺ by Na⁺ in some key biochemical reactions [42], which may become inhibitory to some enzymes [46]. It is well understood that most enzymes rely on K⁺ as a cofactor and can thus not be substituted by Na⁺. Thereby, maintaining an optimal Na⁺/K⁺ ratio has emerged a crucial aspect of salinity tolerance [47]. The ion-specific phase is relatively slow and begins when salts accumulate to lethal concentrations particularly in older leaves that have ceased expanding and eventually die. According to Munns and Tester [31], ionic stress becomes a major concern in crop plants with uncontrollable accumulation of ions in the shoots coupled with an inability to tolerate the accumulated ions. Therefore, maintenance of a lower Na⁺ accumulation in relation to essential ions such as K⁺, Mg²⁺, and Ca²⁺ is a desirable trait under salinity stress. Toxic accumulation of Na⁺ and Cl⁻ salts in the cytosol and osmotic-effect-induced reductions in water uptake result into metabolic imbalances, which in turn cause oxidative stress [48]. Meanwhile, it is widely accepted that accumulation of reaction oxygen species (ROS) accounts for a major part of damage caused to macromolecules and cellular structure by most abiotic stresses [49] suggesting that generation of ROS might be the prime cause of lethality in stressed organisms. Under optimal conditions, plants’ cellular homeostasis is dependent on a delicate balance of multiple interlinked pathways. However, water stress disrupts that balance, uncoupling the pathways resulting into transferring of high energy state electrons to oxygen, which generates reactive oxygen species [50, 51]. These include hydrogen peroxide (H₂O₂), superoxide radicles (O₂^•−), singlet oxygen (¹O₂), and hydroxyl radicles (OH^•). When their generation exceeds their scavenging, they are potentially toxic and capable of causing oxidative stress to proteins, DNA, and lipids [13, 52, 53]. Therefore, tolerance to salinity stress requires a combination of multiple strategies and mechanisms that confront osmotic stress, specific ion toxicity and scavenge reactive oxygen species.

3.1 Tolerance mechanisms to salinity stress

As a result of the widespread nature of salinity stress, plants have developed multiple mechanisms and strategies to confront salinity stress. Tolerance to salinity stress falls within three main categories; osmotic tolerance, ion exclusion, and tissue tolerance (Figure 1). A yet fourth tolerance strategy pertains to tolerance to oxidative stress elicited by excessive generation of ROS. Osmotic stress inhibits ability of plants to take up water due to excessive presence of salts around the roots. Thereby first mechanism, termed osmotic tolerance, is targeted at sustaining water uptake in plants and ensuring a well-hydrated leaf status of plants to maintain key metabolic activities such as photosynthesis. This is regulated by long distance signals that reduce shoot growth [54] way before Na⁺ accumulates to the shoots. ROS and Ca²⁺ waves are speculated to be involved in the long-distance signaling under osmotic tolerance [55]. One important mechanism through which plants confront osmotic stress is through accumulation of solutes to balance extra osmotic pressure generated in the soil solution to maintain turgor [18]. This can be achieved by excluding saline ions from accumulating in the shoots and principally relying on accumulation of organic osmolytes such as sugars, proline, glycine betaine, etc. However, controversy sparks from this strategy as it comes with a larger trade-off in the form of energy cost [56]. That notwithstanding, this strategy is employed particularly among glycophytes through selective uptake of ions by roots, excluding uptake of Na⁺ and Cl⁻, preferentially loading K⁺ in the xylem vessels, and controlling Na⁺ loading and unloading of Na⁺ from the xylem in the upper part of the roots, stems, and petiole [10]. Cognizant of the energy cost of synthesizing organic solutes for osmotic adjustment, some plants, mostly halophytes, rely on accumulation of Na⁺ as a cheap osmoticum. This way, the plants transport Na⁺ to the shoots to levels bearable and sequester them into vacuoles so as not to interfere with key cytosolic metabolic activities [57]. Works leading to the discovery of tissue tolerance as a strategy in plants were inspired by an earlier finding that in vitro, halophytic enzymes were not any more tolerant to high salt than those of glycophytic plants [58, 59]. Besides, several species have reported higher tissue Na⁺ concentrations in leaves that are still functioning [60, 61]. When Na⁺/Cl⁻ accumulates in the vacuole, K⁺ and organic solutes must accumulate in the cytoplasm to balance the osmotic pressure of ions in the vacuole. Common organic osmolytes in tomatoes are proline [62] and soluble sugars [24, 63].

Figure 1.

A summary of mechanisms of salinity tolerance in tomato plants.

All these compounds are found under both drought and salt stress and accumulate in higher levels in plants adapted to such environments. Under salt stress, their accumulation reflects more of an osmotic response than salt-specific (ionic) response. This strategy is termed tissue tolerance and in tomatoes, it is aided by Na⁺/H⁺ antiporters NHX, isoforms SlNHX3 and SlNHX4 [64]. It is important to note that plants transpire 30–70% more water than is used for cell expansion [10]. Salts carried in the transpiration stream are deposited in leaves as the water evaporates, gradually building up to toxic levels. In older leaves, salt toxicity becomes much higher than younger leaves since they are no longer expanding and cannot dilute incoming salts. Eventually, the salt concentration becomes high enough to kill the cells. Hence, some plants rely on Na⁺ exclusion, to reduce the rate at which salt accumulates in transpiring organs. This can be achieved through (1) root cells and can selectively avoid uptake of Na⁺ (2) preferentially loading of K⁺ into the xylem at the expense of Na⁺ and (3) unloading of Na⁺ from the xylem, this is aided in tomato by high-affinity K⁺ transporters (SlHKT1;2). Being a glycophytic plant, tomato is less efficient in sequestering Na⁺ in the vacuoles but relies predominantly on exclusion of Na⁺ from the leaves.

3.2 Screening techniques for drought and salinity tolerance

In view of the devastating effects of drought and salinity coupled with sensitivity of this agronomically important crop, it is substantiated to develop cultivars that are able to maintain yield or exhibit less yield decline under these environments. Such breeding goals can be aided with proper screening and selection for water stress-tolerant cultivars. Various techniques and parameters have been derived from screening for drought tolerance [65, 66]. A classical approach to investigating plants’ responses to abiotic stresses is to use two genotypes with contrasting tolerance reputations. Some have argued that this approach is narrow, hence have advocated for the broadening of these types of analyses by using several genotypes before speculating about a species’ performance [67]. Furthermore, when selecting a few contrasting genotypes, it is necessary to take into account the potential variability of the trait under study within the population, especially crops and plants with determinate and indeterminate growth habits such as tomato. In such cases, derivation of salt tolerance indices obtained as relative decreases in plant biomass by comparing plant biomass of stressed and control plants [68] is imperative. Stress susceptibility index (SSI) serves as a reliable measure of sensitivity to stress as it considers the intensity of stress and performance ratio between stress and their respective controls [69]. That notwithstanding, screening techniques need to be supplemented with other techniques to increase their reliability. Cluster analysis is one dependable tool that allows self-grouping of cultivars into groups of similar characteristics and has been widely used as a screening tool in tomato [24, 65, 66]. For reference to a variety of screening methods and their merits, refer to [70].

4. Salinity and water stress: where is the synergy?

Firstly, it is important to understand that plants’ responses to salinity stress occur in two distinct temporal phases [71]: a rapid response to the increase in external osmotic pressure, and a slower response due to the accumulation of Na⁺ in leaves. Hence, in order to correctly dissect the physiological mechanisms associated with salinity tolerance of plants, it is necessary to first identify whether their growth is being limited by the osmotic effect of the salt in the soil or the toxic effect of the salt within the plant. According to [31], in the first few hours occurring immediately after plant roots are exposed to a saline media, plant’s shoot growth is considerably reduced, largely as a result of osmotic effect of salts “outside” the plant roots. Evidently, plants experience a lower rate of leaf expansion, slower emergency of newer leaves, and slower development of lateral buds consequently forming fewer branches and lateral shoots. It is important to note that shoot growth is far much sensitive to the osmotic effects than root growth. This phenomenon is also common in drying soils under drought conditions. It has been suggested that reduction in leaf area development relative to root growth would decrease the water use by the plant, thus allowing it to conserve soil moisture and prevent an escalation in the salt concentration in the soil [31]. Relatively, it is the osmotic stress component of salinity stress that exhibits both an immediate and greater effect on growth than the ionic stress. The latter is manifested much later and lesser. Ionic effects of salinity stress are only higher either at very high salinity levels or in extremely sensitive species such as rice whose ability to control Na⁺ transport is limited.

Now, the question may remain as to whether these osmotic responses are salt and species-specific. Experiments in maize [72, 73], rice [74] as well as wheat and barley [75] have all recorded rapid and transient reductions in leaf expansion rates after a sudden increase in salinity. Likewise, similar changes were reported when plants are exposed to KCl, mannitol, or polyethylene glycol (PEG) [76]. These results are indicative that the responses are neither salt- nor species-specific. This first phase growth reduction is quickly apparent and is due to the salt outside the roots. It is essentially a water stress or osmotic phase, for which there is surprisingly little genotypic variation. The growth reduction is presumably regulated by hormonal signals coming from the roots. It is from this point of view that salinity stress synonymizes drought stress, hence the usage of the term “physiological drought” by some authors [62, 77]. Figure 2 shows this synergy, drought-specific responses involve synthesis of ABA and induction of ABA responsive genes involved in synthesis of water channels, enzymes, and protein kinases.

Figure 2.

The synergy of drought and salinity stresses. Osmotic stress and oxidative stress are common links of both salinity and drought stress, whereas salt specific response is ionic toxicity (Na⁺ and Cl⁻) and drought-specific responses include synthesis of ABA in either shoots or roots that trigger expression of ABA responsive genes.

4.1 Comparative osmotic responses to salt and drought stress

Plants growing under salt stress are faced with three prime costs; (1) the cost of excluding Na⁺ from uptake by roots, (2) the cost of compartmentalizing/sequestering Na⁺ in the vacuole, and (3) that of excreting the salt through salt glands. In tomatoes, the latter cost is of less importance as tomatoes do not have the salt glands. Under drought stress, the prime cost is to synthesize organic osmolytes, a far much higher cost. While it remains unclear whether plants growing under saline media produce lesser organic solutes compared with those growing under non-saline media, a comparison of four tomato genotypes growing under PEG and NaCl at an isotonic solution, much greater accumulation of soluble sugars was observed under PEG than NaCl [78]. Correspondingly, the tomato plants growing under NaCl grew much better than under the isotonic PEG solution. This result suggests the higher cost of synthesizing organic osmolytes in tomatoes on growth, hence it may follow that plants growing under saline conditions grow faster than under non-saline media. However, this conclusion may not be overarching, as equivocal results have been obtained in other species, notably [10].

5. Learning from tomato wild relatives

Despite that tomato remains sensitive to drought and salt stress, the genus Solanum has extensive wealth of genetic variation existing in wild relatives. Tomato, for example, has a number of wild relatives with remarkable reputation for tolerance to drought and salt stress, such as Solanum pennellii, S. habrochaites, S. pimpinellifolium, S. hirsutum, Lycopersicum chillense, and L. peruvianum. As such, they represent a valuable system in which to study local adaptation to drought and salt stress. A number of comparative studies have been conducted to evaluate physiological and molecular responses of cultivated tomato (S. lycopersicum) in comparison with wild relatives. For example, Egea et al. [17] reported substantial physiological differences, with the wild relative Sp leaves showing greater ability to avoid water loss and oxidative damage under drought stress. Similar results were also found in another wild relative S. habrochaites under root-chilling-induced water stress, in which Sh exhibited higher shoot turgor through enhanced stomata closure relative to cultivated tomato, which failed to close stomata and consequently wilted [79]. QTL mapping revealed a single QTL coincidental with the gene or genes contributing to shoot turgor maintenance under root chilling residing on chromosome 9 region that have been associated with abiotic stress tolerance in cultivated tomato. Under salinity stress, another study showed that Sp was able to reduce water loss by regulating transpiration through reduced stomatal density and aperture [18]. Furthermore, Sp leaves had larger and more turgid cells occupied by a giant vacuole, which was associated with higher water and Na⁺ accumulation. On Na⁺ homeostasis, the wild relative had higher expression of SpHKT1;2 and SpSOS1, which played an important role in Na⁺ translocation from root to shoot, and therefore, in the determination of the included behavior in the wild species, which was in concordance with the higher transcript levels of Na⁺ vacuolar transporters SpNHX3 and SpNHX4 in Sp leaves. An association study in 94 genotypes of S. pimpinellifolium to identify variations linked to salt tolerance traits (physiological and yield traits under salt stress) in four candidate genes identified five SNP/Indels in DREB1A and VP1.1 genes that explained substantially, phenotypic variation for various salt tolerance traits [80].

6. Improving salt and drought tolerance in tomato

Salinity stress affects many aspects of physiology and biochemistry of plants and, subsequently, yield. Growing knowledge and advances in molecular techniques provide room and opportunity for quicker enhancement of salt tolerance in tomatoes. Even though genetic transformation could become a powerful tool in plant breeding, it is necessary to integrate the growing knowledge from plant physiology with molecular breeding techniques. Notwithstanding the many relatively salt tolerant wild relatives of the cultivated tomato, it has proved difficult to enrich elite lines with genes from wild species that confer tolerance because of the large number of genes involved, most of them with small effect in comparison to the environment [81]. Critical in breeding for salt and drought tolerance is the need for the new cultivars to be both tolerant and maintain attributes of higher yield and quality shown by modern cultivars. Hypothetically, susceptible but productive cultivars should be converted to tolerant cultivars, while maintaining all the very valuable characters current cultivars possess, making the introduction of genes conveying salt tolerance to elite cultivars by transformation an attractive option. However, the problem of drought and salt tolerance is complex and multigenic, requiring a battery of strategies. Instead, scientists have resorted to a range of cultural techniques, each contributing to a small extent to allow plants to withstand better the deleterious effects of salt.

For many years to recent, it was believed that salt tolerance was solely a factor of expression of genetic information counteracting effects of stress [82]. However, present understanding tells that plants can improve their physiological ability and adapt to severe stresses when pretreated (PT) with mild stress, a phenomenon termed acclimation [61, 83, 84, 85] as shown in Figure 3. During the plant response and acclimation to abiotic stress, important changes in biochemistry and physiology take place and many genes are activated, leading to accumulation of numerous proteins involved in abiotic stress tolerance. Benefits of acclimation to salinity stress have been linked to improved growth via effective vacuolar Na⁺ sequestration [61], improved survival rates [84], and reduced shoot Na⁺ accumulation [62, 85, 86]. The successful adaptation of cell lines to salinity suggests that a genetic potential for salt tolerance is present in cells of plants from which the lines were derived and that exposure of the cells to salt triggers the expression of this information.

Figure 3.

A schematic of acclimation in tomato plants, wherein seedlings’ previous exposure to a mild level of stress (salt or drought) primes tomato plants to exhibit faster and stronger responses to subsequent lethal stresses.

In tomato, success stories of acclimation have been reported through seedling pretreatment with NaCl [62, 87], pre-exposure to salicylic acid [88, 89], and seed priming with NaCl [82]. Another study by Gémes et al. [90] showed that pretreatment of tomato plants with salicylic acid attenuated oxidative stress by reducing H₂O₂ generation under salt stress, suggesting a cross talk between salicylic acid and salt-stress-induced ROS. H₂O₂ is considered functional link of cross-tolerance to various stressors, as also reported in rice under saline-alkaline stress [86]. Szepesi [91] found that salicylic acid pretreatment improved the acclimation of tomato plants to tolerance levels comparable to that of tomato’s wild relative L. pennellii, a wild relative with a high reputation for stress tolerance. Humic acids pretreatment of tomato seedlings has also been explored and showed that seedlings primed by humic acids minimized the salinity stress by changing ion balance, promoting plasma membrane proton pumps activity and enhancing photosynthesis rate and plant growth [92].

Plant adaptation to abiotic stress has also been observed under drought stress. For example, a study by [93] showed that multiple exposures to drought stress trained transcriptional responses in Arabidopsis. In the study, it was shown that during recurring dehydration stresses, Arabidopsis plants displayed transcriptional stress memory demonstrated by an increase in the rate of transcription and elevated transcript levels of a subset of the stress-response genes (trainable genes). Four distinct types of dehydration stress memory genes in Arabidopsis thaliana have been further identified [94]. These observations of altered plants’ subsequent responses following pre-exposure to various abiotic stresses by improving resistance to future exposures, have led to the concept of “stress memory” implying that during subsequent exposures, plants provide responses that are different from those during their first encounter with the stress. While these phenomena have not been reported in tomato, yet they might represent a general feature of plant stress-response systems and could lead to novel approaches for increasing the flexibility of a plant’s ability to respond to the environment. In tomato, it has been shown that a moderate water deficit applied 10 days after anthesis induced acclimation to a subsequent more severe drought stress [95]. Similar results have also been reported in wheat [96]. It has been reported that plants exposed to one stress may show tolerance to other stresses, displaying a concept of cross-tolerance [86, 97, 98]. It is hypothesized that drought pretreatment could increase the tolerance to the osmotic effect, the main effect induced by salinity when moderate salt levels are used. This has been observed in tomato plants previously exposed to a drought stress pretreatment, which subsequently grew better than non-pretreated plants after 21 days of salt treatment [99]. Similar findings were reported by [100], who found improved salt tolerance of tomato plants following seedling pretreatment with PEG, a chemical drought (osmotic) stress simulator. This illustrates a concept of induced cross-tolerance (Figure 4), in which prior exposure to one stress induces tolerance to another stress, as opposed to inherent cross-tolerance that manifests itself as genetic correlation of gene expression under different stresses (Figure 4).

Figure 4.

A schematic of cross-tolerance. Plants may exhibit inherent cross-tolerance, manifesting itself as genetic correlation of gene expression under different stresses. Cross-tolerance may also be induced by previous exposure to one stress that may develop tolerance to another stress compared with plants without prior exposure to any stress.

Plant adaptation to stresses is a complex process, involving numerous physiological and biochemical changes. The key components in a typical stress-response relationship involve stress stimulus, perception of stress by signals, expression of stress-induced genes, and resultant changes at morphological, biochemical, and physiological levels [98]. The signaling and response pathways have been reported to overlap during exposure to different abiotic stresses, including reactive oxygen species (ROS), hormones, protein kinase cascades, and calcium gradients as common elements [101]. In a case of cross-tolerance, it has been suggested that specific proteins are induced by one kind of stress and are involved in the protection against other kinds of stress [97, 98], although a common mechanism has not been found.

Aside from the use of pretreatments, another route for enhancing salt and drought stress tolerance in tomato would be to graft cultivars on to rootstocks able to reduce the effect of external salt or drought on the shoot. This strategy could also provide the opportunity to growers of combining good shoot characters with good root characters. In tomato, grafting has previously been used to limit soil-borne and vascular diseases such as Fusarium. Over the years, application of grafting technique has been widened across various uses such as improving yield, fruit quality, low and high temperature as well as Fe chlorosis as outlined in [81]. In Citrus spp., for example, the positive effect of rootstock is related to the ability of the rootstock to exclude chloride [102, 103]. However, grafting has rarely been used to increase the productivity of vegetables growing under adverse conditions. In tomato, a commercial tomato cultivar Jaguar as scion has been grafted onto roots derived from the same genotype (J/J) or other cultivars’ root stocks that increased fruit yield by more than 60% under salinity stress by regulating the transport of Na⁺ and Cl⁻ throughout the plant growth cycle, even after 90 days of salt treatment [104]. Similar results have also been reported by [105], further revealing that rootstock effect on the tomato salinity response depends on the shoot genotype. Furthermore, [106] also found higher improvements in vegetative growth as well as yield in a commercial tomato cultivar grafted on tomato wild relatives coupled with changes in morphological, physiological, and molecular attributes. The results suggest that the saline ion accumulation in leaves is predominantly controlled by the genotype of the rootstock, providing an alternative way of enhancing salt tolerance in tomato – quicker and least costly.

An observation has been made that acclimation ability to abiotic stress in tomatoes is dependent on degree of tolerance of the cultivar such that more salt-sensitive cultivars benefit more from the acclimation process than tolerant cultivars [62, 87].

7. Concluding remarks

Despite being a crop of considerable agronomic importance, tomato remains a sensitive crop to droughts and salinity stress. Cultivation under these environments is an extremely challenging task; hence, it is imperative to develop tomato cultivars resistant to these adverse conditions. This, however, requires an understanding of their physiological and molecular mechanisms underpinning tolerance. This chapter has dissected in detail the key physiological and molecular changes that take place under both drought and salinity. These two stresses, albeit being distinct, pose considerable similarities and affect tomato growth in significantly comparable manners. The chapter also drew learning points from tomato’s wild relatives that present the required variation for development of tolerant cultivated varieties. However, development of tolerant cultivars is often a long and costly endeavor and subject to country-specific regulatory frameworks. Moreover, considering the multigenic nature of drought and salt tolerance trait, the chapter suggests exploration of some quicker options that promote adaptation to adverse environments. In tomato, options such as acclimation, cross-tolerance, and grafting have proved effective in developing tolerance to abiotic and in some cases, biotic stress conditions (Table 1). These may provide some required short-term yield gains when cultivating tomato under adverse environmental conditions.

Pretreatment	Abiotic stress	Crop species	Target stress factor	Studies
NaCl	Salinity	O. sativa L.	Osmotic, ionic	[85, 86, 107, 108, 109]
		S. lycopersicum L.	Osmotic, ionic	[62, 82, 87]
		Z. mays L.	Osmotic, ionic	[83]
		P. sativum L.	Osmotic, ionic	[61]
		G. max L. merr	Osmotic, ionic	[84]
		V. radiata L.	Osmotic, oxidative	[110]
Salicylic acid	Salinity	S. lycopersicum L.	Ionic	[88, 89]
	Alkaline	S. lycopersicum L.	Ionic, oxidative	[111]
Silicon	Alkaline	S. lycopersicum L.	Ionic, oxidative	[111]
ABA	Salinity	O. sativa L.	Osmotic, ionic	[112, 113]
	Alkali	O. sativa L.	Osmotic, ionic, oxidative	[114, 115]
Gibberellins	Salinity	P. vulgaris L.	Oxidative	[116]
Cytokinin	Saline-alkaline	O. sativa L.	Osmotic	[117]
	Salinity	Lolium perenne	Oxidative, ionic	[118]
	Salinity	V. faba	Oxidative, ionic, osmotic	[119]
NaHCO3	Saline-alkaline	S. cereale L.	Osmotic, oxidative	[120]
Drought	Drought	S. lycopersicum L.	Osmotic	[95]
	Drought	T. aestivum	Osmotic	[96]
	Salinity	S. lycopersicum L.	Osmotic	[99, 100]
Repeated drought	Drought	A. Thaliana	Oxidative	[93, 94]
H2O2	Salinity	T. aestivum L.	Oxidative	[121]
	Salinity	H. vulgare L.	Oxidative	[122]
	Salinity	Z. mays L.	Oxidative, osmotic	[123]
	Saline-alkaline	O. sativa L.	Oxidative	[86]
Grafting	Salinity	S. lycopersicum L.	Ionic	[104, 105, 106]

Table 1.

List of some cultural techniques that have been used to enhance drought and salt tolerance in tomato and other crops.

Conflict of interest

The authors declare no conflict of interest.