Overview of the Role of Rhizobacteria in Plant Salt Stress Tolerance

: Salinity is one of the main causes of abiotic stress in plants, resulting in negative effects on crop growth and yield, especially in arid and semi-arid regions. The effects of salinity on plant growth mainly generate osmotic stress, ion toxicity, nutrient deficiency, and oxidative stress. Traditional approaches for the development of salt-tolerant crops are expensive and time-consuming, as well as not always being easy to implement. Thus, the use of plant growth-promoting bacteria (PGPB) has been reported as a sustainable and cost-effective alternative to enhance plant tolerance to salt stress. In this sense, this review aims to understand the mechanisms by which PGPB help plants to alleviate saline stress, including: (i) changes in the plant hormonal balance; (ii) release of extracellular compounds acting as chemical signals for the plant or enhancing soil conditions for plant development; (iii) regulation of the internal ionic content of the plant; or iv) aiding in the synthesis of osmoprotectant compounds (which reduce osmotic stress). The potential provided by PGPB is therefore an invaluable resource for improving plant tolerance to salinity, thereby facilitating an increase in global food production and unravelling prospects for sustainable agricultural productivity.


Introduction
At present, there is scientific consensus indicating that the human production model and energetic consumption are involved in climate change [1]. The impact that this global climatic alteration causes is translated into adverse environmental conditions, such as salinity in soils, extreme temperatures, droughts, or floods, which limit the geographical distribution of plant species and crop yields [2,3]. These types of extreme processes mainly affect semi-arid and arid regions, and they have not only environmental impacts but also economic and social repercussions [2,4].
Soil salinity is the result of the accumulation of soluble salts in soils, due to natural (primary salinization) and/or anthropogenic (secondary salinization) processes, and has been defined as an important cause of loss of soil fertility, as well as agricultural productivity and sustainability [5]. A soil is saline when it presents electrical conductivity (EC) of the saturation extract (ECe) of 4 dS m −1 (approximately 40 mM NaCl) or higher at 25 °C and has an exchangeable sodium of 15% [6,7]. Although most studies have focused on the effect of NaCl as a cause of saline stress, in some areas of the planet, this stress is due to the presence of Na2SO4 [8]. The long-term accumulation of other ions, such as Ca 2+ , Mg 2+ , or C03 2-, has also been shown to have negative effects on plant productivity, when certain thresholds are exceeded [9]. In this sense, it has been estimated that 20% of cultivated it is also necessary to increase knowledge in this respect [6,7,18]. In contrast, there are other feasible and cost-effective strategies, as is the case for the application of beneficial micro-organisms that increase salt-tolerance in plants [1,17,23].
In recent years, the application of Plant Growth-Promoting Bacteria (PGPB) has been demonstrated as an effective alternative to enhance plant development and the nutritional content of various crops, even under adverse environmental conditions, such as soil salinity [10,24,[27][28][29][30][31]. These soil micro-organisms are able to improve crop water relations, alter ion homeostasis, or change phytohormone status through direct and indirect mechanisms that modulate abiotic stress regulation [1,23]. Therefore, the aim of this review is to understand the mechanisms by which PGPB help plants to alleviate saline stress.

Physiological Effects of Salinity Stress on Plants
Increased ion concentration in the soil causes salinity. Salt-affected soil includes saline soil, sodic soil, and saline-sodic soil [2]. The common cations associated with salinity are Na + , Ca 2+ , and Mg 2+ , while the common anions are Cl -, SO4 2-, and HCO3 - [22]. Among them, Na + and Clions are considered the most important, owing to their negative effects in plants and soil [1,7,16,22]. The impacts of salinity are complex, ranging from morphological, physiological, and biochemical effects on plants, to erosion and reduced soil productivity [1,7,22]. In this sense, soil salinity affects all aspects of plant growth and development (i.e., germination, vegetative growth, and reproductive development) by imposing damaging effects, involving osmotic imbalance and ionic stress. As a consequence of these primary effects, secondary stresses often occur, such as oxidative damage [1,2,7,16,22].

Osmotic Stress
Osmotic stress is a type of stress that occurs when there is an imbalance in the water balance of the plant [32]. It is said to be the first phase in the development of salt stress, which starts immediately after the accumulation of salt above a threshold level around the radicular systems, generating a water deficit in the roots [2,16,32]. Osmotic stress affects shoot and reproductive development: the expansion of leaves is reduced, new leaves emerge more slowly, senescence of older leaves occurs, fewer branches or lateral shoots form, and flowering starts earlier [1,2,16]. Radicular system architecture and development is also affected: the elongation of roots is initially diminished, and the formation of lateral roots is repressed [1,16]. Furthermore, alteration of the water balance causes stomatal closure and a reduction in gas exchange. All of the above, together with the feedback inhibition of unused photosynthates (which accumulate in plant meristems and storage organs), results in a decrease in the rate of photosynthesis [1,2,7,16].

Ionic Stress
According to the literature, ionic stress is defined as the combination of ion accumulation in plant shoots and an inability to tolerate the ions that have accumulated [1,2,16]. The ion toxicity phase is the second stage in the development of salt stress, which appears when the accumulation of these ions exceeds the rate of exclusion. These radicals are transported from the roots to the xylem, through which they move to the leaves, where they accumulate in vacuoles and cytoplasm to toxic levels [1]. Leaves die under these levels of ions and, if the rate of production of new leaves is less than the rate of death, the photosynthetic capacity of the plant is reduced [16]. Moreover, an excess of radical concentration, mainly Na + and Cl -, negatively affects K + uptake, due to competition between the two ions to act as substrate in low-affinity potassium uptake systems, as well as other micronutrients [1,7,24,25]. All of this results in structural and functional alterations of the cell: restraint of enzymes involved in photosynthesis and respiration, interference with vesicular trafficking, inhibited cytosolic activities, and/or chloroplast and mitochondrial toxicity [1,7,16].

Main Mechanisms of Salinity Tolerance/Resistance Induced by PGPB
The physiological effects of salinity cause significant reductions in crop productivity [1,16]; however, the application of PGPB has been shown to improve crop productivity, by reducing the physiological damage caused by high ion concentrations in the soil [1,23]. This effect is due to different mechanisms exhibited by these beneficial bacteria, which act at different levels, regulating the harmful effects of high salt concentrations [1,7,23,34,35].

Osmotic Balance (Water Homeostasis and Osmolyte Accumulation)
Osmotic stress is the first effect produced by salinity, as previously mentioned. It generates a disruption in the water balance, causing stomatal closure [2,7]. The photosynthesis rate decreases, due to an imbalance in gas exchange and leaf area reduction [1]. Additionally, photosynthate feedback inhibition occurs. The reduction of growth results in an accumulation of carbohydrates in meristems and storage organs, which otherwise would be used in proliferation and the expansion of new tissues [1,23]. Accordingly, plants need to maintain water homeostasis and preserve photosynthetic structures, with the aim to mitigate the impact of salinity. In this sense, the use of PGPB has been demonstrated as an alternative to enhance the osmotic balance, through various mechanisms (see Figure 1, Table 1). Bacterial extracellular polysaccharides or exopolysaccharides (EPS) are complex hydrated high-molecular weight organic polymers broadly distributed among bacteria [17,36], which have a fundamental roles in the defense of microbiota against stressful environmental conditions (pH or temperature), as well as adhesion to biotic and abiotic surfaces [37]. The composition and amount of ESP depend on the strain and conditions [34]. ESP also have additional functions in plant-microbe interactions. The addition of polysaccharides increases the adherence of soil particles into microaggregates and favors macropore generation, which are beneficial in improving porosity and aeration in soil ( Figure 1) [17,23,38,39]. Thus, the effects of the initial osmotic stress are diminished by binding soil particles and improving its structure [7]. It has been shown that co-inoculation of the plant growth-promoting rhizobacteria Pseudomonas mendocina and the arbuscular mycorrhizal fungus Glomus intraradices onto lettuce resulted in a high percentage of stable aggregates in soil under field conditions, due to the bacterial EPS production [40]. Moreover, according to Qurashi & Sabri [41], the effect of inoculating two bacterial strains, Halomonas variabilis HT1 and Planococcus rifietoensis RT4, onto Cicer arietinum plants subject to soil aggregation under salt stress led to enhancements in chickpea growth and soil structure.
As previously stated, salinity causes growth reduction and feedback inhibition of unused photosynthates. Micro-organisms can modulate the source-sink relationships of soluble sugars in plants, favoring osmotic adjustment and avoiding feedback photoinhibition during the salinity osmotic phase ( Figure 1) [1,42]. On one hand, plant roots are a strong carbohydrate sink, and their development can be mediated by the hormonal response (IAA) associated with the action of the microbe. On the other hand, the microbes can also consume a considerable part of these photosynthates [23]; for example, the salt resistance of two nodulated Medicago ciliaris L. lines was mediated by the maintenance of nodularsymbiotic and source-sink activities [43]. In addition, co-inoculation of Bradyrhizobium japonicum 532C, Rhizobium sp. SL42, and Hydrogenophaga sp. SL48 onto soybean plants under saline conditions improved shoot and root growth, nitrogen assimilation, and the K + /Na + ratio, which could be a consequence of nodular-symbiotic and source-sink activities [44]. Capsicum annuum L. plants co-inoculated with Azospirillum brasilense M3 and Pantoea dispersa C3 under salinity (40-120 mM NaCl) showed increases in analyzed production parameters, as related to higher stomatal conductance and photosynthesis, without changes in chlorophyll content or photosystem efficiency [45]. In the same way, inoculation with various Bacillus strains in strawberry and wheat has increased different leaf physiological parameters, such as photosynthesis or stomatal conductance [46], or productivity and nutritional content [47].
Saline stress causes a loss of intracellular water in plants [48]. Therefore, vegetal species accumulate organic osmolytes in the cytoplasm, in order to maintain the osmotic cellular state and to improve their response to such stress [34,48]. These compounds include proline, glycine, betaine, or trehalose, among others ( Figure 1) [1,23,48]. Salt-tolerant bacteria also employ this mechanism against osmotic fluctuations of the environment [34]. In addition, the biosynthesis of such osmoprotectans is quicker in bacteria than in their associated plants [1]. It has been observed that inoculation with PGPB generated an improvement of osmolytes in plants, which may be due to bacterial solutes being taken up by the roots or de novo synthesis in plants, where the PGPB have been demonstrated to be useful [1,23]. The accumulation of certain osmoprotectans (e.g., proline, betaine) has helped various vegetal species to resist salt-stress conditions in the presence of beneficial bacterial strains, such as Burkholderia [49,50], Arthrobacter [51], Azospirillum [52], Bacillus [51,53], Rhizobium, and Pseudomonas [24]. Similarly, Oryza sativa L. inoculated with Pseudomonas pseudoalcaligenes YJ1 has shown the accumulation of glycine betaine-like quaternary compounds, while co-inoculation with P. pseudoalcaligenes YJ1 and Bacillus pumilus YJ2 was also able to protect the plant from salinity [54]. It has also been shown that the use of three bacterial strains (B. megaterium MPP7, B. tequilensis MPP8, and P. putida MPP18) increased the production of proline and total soluble sugar in salt-stressed wheat plants, which also reduced electrolytic leakage and enhanced enzymatic activity for the scavenging of reactive oxygen species (ROS) [55]. In this sense, pea plant grown under salinity stress and inoculated with various PGPR (Acinetobacter bereziniae IG2, Enterobacter ludwigii IG10, and Alcaligenes faecalis IG27) showed higher proline and total soluble sugar content, as well as a reduction in oxidative damage [56]. Furthermore, the construction of Pseudomonas strain mutants for the gene coding trehalose synthase (treS) has been carried out, and the function of this bacterial mechanism in the protection of a plant (tomato) against salt stress has been reported [57].
The plant water potential is altered under high salt concentration conditions. PGPB can regulate water homeostasis by improving the hydraulic conductivity ( Figure 1) [1,23,58]. Inoculation with Bacillus megaterium B26 in maize plants under salinity (2.59 dS m −1 ) generated an enhancement in the hydraulic conductance, as related to a positive regulation of PIP-type plasma membrane aquaporins [59]. This same effect has also been observed in tropical corn plants exposed to salt stress (200 mM NaCl) and inoculated with Pantoea agglomerans SG_JW.01 rhizobacteria [60]. Furthermore, Azospirillum brasilense AZ39 inoculation produced improvements in a PIP-type aquaporin transcription for barley plants grown under saline conditions (200 mM NaCl) [61]. Sinorhizobium medicae Medicago ciliaris L.
Glycine max L.

Maintaining of higher stomatal conductance
Higher dry weight and K + /Na + ratio [45] Bacillus licheniformis, Bacillus subtilis, and Bacillus sp.

Fragaria x ananassa
Maintaining of higher stomatal conductance and transpiration rate Enhanced growth, yield, and fruit quality [46] Bacillus aquimaris Triticum aestivum L.
Accumulation of osmoprotectans (proline and sugars) Increased plant biomass, water homeostasis, and soil aggregate stability [53] Rhizobium sp. and Pseudomonas sp. Zea mays L.
Accumulation of osmoprotectans (trehalose) and ACC deaminase production Higher root and shoot length, total dry weight, and chlorophyll content [57] Bacillus megaterium Zea Mays L.
Transcriptional changes in ion transporter genes (HKT and NHX-type) and hormonal changes (IAA and ABA) Decreased Na + accumulation and increased productivity parameters [63] Pseudomonas simiae Glycine max L.
Transcriptional changes in phosphatase activity and accumulation of osmoprotectans (proline) Increased biomass and water content [65] Brachybacterium sp., Brevibacterium sp., and Haererohalobacter sp.

Water homeostasis and IAA plant accumulation
Higher productivity variables and nutrient content [66] Pseudomonas putida Gossypium hirsutum L.
Hormonal changes and accumulation of polyphenols Higher plant length, weight, and ion uptake [68] Azospirillum brasilense Zea mays L.
Transcriptional changes in plant growth genes Higher K + /Na + ratio [69] Rhizobium sp. and Pseudomonas sp. Zea mays L.
EPS production, accumulation of osmoprotectans (proline), and raised antioxidant enzyme activities Higher shoot biomass, water content, and K + /Na + ratio [72] Pseudomonas sp. and Bacillus sp. Glycine max L.
ESP, ACC deaminase and IAA production, and accumulation of osmoprotectans (proline) Enhanced plant biomass, water content, and photosynthesis activity [73] Halomonas maura and Ensifer meliloti Medicago sativa L.
Accumulation of osmoprotectans (proline and soluble sugars) Increased biomass, weight, and leaf nutrients

Ion Homeostasis (Regulation of Ion Content)
Salinity causes Na + , Cl -, Ca 2+ , Mg 2+ , SO3 2-, or CO3 2-accumulation, which results in the ion toxicity phase. Ionic stress occurs under prolonged exposure to high salt concentrations, when the influx of these ions overcomes the rate of exclusion [1,16]. Plants initially compartmentalize the excessive salts in vacuoles, avoiding their accumulation in the cytosol and intracellular spaces, which limits photosynthesis and respiration [1]. Elevated Na + concentrations affect K + -dependent process, where the replacement of K + by Na + in biochemical reactions results in protein conformation changes and synthesis [7,76]. It has also been observed that there is a dependence between the reduction of productivity and the ionic balance, determined by the K + :Na + , Mg 2+ :Na + , and Ca 2+ :Na + ratios [9]. Soil microorganisms have been reported to maintain ion homeostasis, which must benefit plant growth and tolerance during salinity [23,77]; however, these studies have focused on NaCl saline stress, but not other ions involved in saline stress.
Maintaining a high K + /Na + ratio is one of the ways by which PGPB can regulate toxic ion homeostasis, thus reducing the accumulation of Na + and Clin leaves, boosting ion exclusion by the root, or modulating the expression of ion transporters [1,23]. High-affinity K + transporters (HKT) are plasma membrane proteins that mediate Na + transport in plants, preventing the build-up of high concentrations of Na ions in shoots by excluding to the roots (Figure 1) [49,76]. It has been shown that inoculation with rhizobacteria modulates the expression of these types of transporters. The B. subtilis GB03 strain conferred salt tolerance Puccinellia tenuiflora Scribn. & Merr., by enhancing selective absorption of K + over Na + and (down-and up-)regulating the expression of HKT-family genes in roots and shoots, such as HKT1 or HKT2 [62]. Furthermore, the expression of ion affinity transporters (ZmHKT1, ZmNHX1, ZMNHX2, and ZmNHX3) has also been up-regulated in Zea mays L. after exposure to salt stress and inoculation with Kocuria rhizophila Y1, resulting in protection of the plant against salinity [63]. Thus, tissue-specific regulation of HKT-type genes in plant-microbe interactions is necessary for toxic ion homeostasis in salt-stressed plants [49,62,76]. Moreover, there are other enzymes that act as sodium antiporters, such as Salt Overlay Sensitive (SOS) genes, which can help the plants to cope with salinity stress [55]. In this sense, inoculation with three bacterial strains (B. megaterium MPP7, B. tequilensis MPP8, and P. putida MPP18) on wheat plants grown under saline conditions revealed the higher expression of SOS1 and SOS4 genes, which were associated with a higher relative water content and photosynthetic pigments in wheat seedlings [55].
PGPB can also reduce the accumulation of Na + and Clions, by regulating the exchange of macro-and micro-nutrients [1]. First, microbial activities, such as Pi (inorganic phosphate) solubilization or siderophore production, may make these nutrients more accessible to plants ( Figure 1) [23,77]. Second, inoculation with PGPB can induce the upregulation of proteins related to phosphatase activity (associated with Pi solubilization). As Vaishnav et al. [64] have reported, Pseudomonas simiae AU treatment in soybean plants under salt stress increased the expression of VSP (vegetative storage protein) in plants, which had preponderant roles in acid phosphatase activity. In this sense, water-stressed lettuce plants colonised by the Pseudomonas mendocina Palleroni strain also increased acid phosphatase activity, among other effects, thus alleviating oxidative stress in plants [65]. Three bacterial strains, belonging to Brachybacterium, Brevibacterium, and Haererohalobacter genera, improved productivity variables of peanut plants under 100 mM NaCl, as well as K + /Na + ratio and Ca 2+ , phosphorus, and nitrogen content [66]. Moreover, a P. putida strain increased the absorption of Mg 2+ , K + , and Ca 2+ in cotton plants grown under saline conditions (3.5 g salt/kg soil), and decreased the uptake of Na + ; plant growth was also enhanced after its application [67]. According to Rojas-Tapias et al. [62], maize plants grown under saline conditions (2.93 and 5.85 g NaCl/kg soil) and treated with two Azotobacter chroococcum strains showed an enhancement in Na + exclusion and K + uptake, as well as polyphenol and chlorophyll content, with respect to uninoculated controls. Another free-living nitrogen-fixing rhizobacteria also significantly improved the K + /Na + ratio in a salt-sensitive maize cultivar, by restricting Na + uptake and selectively increasing K + and Ca 2+ [69]. In addition, NaCl-affected maize (100 mM), co-inoculated with Rhizobium and Pseudomonas, exhibited some positive adaptative responses to such stress, such as an increase in proline content or the selective absorption of K + ions [24]. Exopolysaccharide (EPS) production also provides a way in which microbes can reduce the uptake of toxic ions in plants. These compounds act as a physical barrier around the root system, preventing the effects of the ion toxicity phase [17,35,77]. EPS bind cations, including Na + , and thereby decrease the accessibility of toxic ions available for plant uptake, reducing the salinity stress by diminishing its transfer to leaves (Figure 1) [7,17,23,35]. According to Ashraf et al. and Talebi Atouei et al. [70,71], wheat plants affected by salinity and treated with EPS-producing bacteria showed increases in growth parameters and alteration of nutrient uptake, by diminishing Na + concentration and boosting the absorption of K + and Ca 2+ . Similarly, a plant growth-promoting rhizobacteria (P. mendocina), in combination with an arbuscular mycorrhizal fungus (G. intraradices), colonised lettuce plants, which presented higher concentrations of foliar K + and lower amounts of Na + under saline conditions [72]. The inoculation with other exopolysaccharide-producing rhizobacteria also indicated the important role that they play in alleviating saline stress conditions in different crops, such as soybean, wheat, alfalfa, or pistachio [47,[73][74][75].

Synthesis of Phytohormones
Phytohormones are synthesized by plants in response to salt stress, such as indole-3acetic acid (IAA), abscisic acid (ABA), or ethylene. These substances alter plant metabolism, morphology, biomass production, and other mechanisms [23,77]. Moreover, soil bacteria may directly alter the plant hormonal balance, by producing exogenous phytohormones. Thus, changes in hormonal signalling arising from plant-microbe interactions are considered as a mechanism for plant soil salinity tolerance ( Figure 2) [1,23,77].

Indole-3-Acetic Acid
IAA is the major auxin, which plays an important role in plant growth and development. Rhizobacteria can produce this metabolite by multiple synthesis pathways, most of which are L-tryptophan-dependent, which is present in root exudates [1,17]. The IAA hormone is involved in many vegetal processes, including cell division, elongation, differentiation, apical dominance, phototropism, and gravitropism [34,77,78]. At optimal levels, IAA may result in beneficial effects, but excessive amounts of this auxin can cause toxicity, as has been revealed by assessing the action mode of some phytopathogens [1,78]. Several studies have shown that the foliar application of exogenous IAA to various crops (maize, sorghum, and pea plants) induced alleviation of salt stress, through the modulation of photosynthesis rate, water use efficiency, Na + accumulation, or weight measurements [58,79,80]. This higher auxin content may contribute to maintaining root and leaf growth, which are important limiting factors under this abiotic stress condition.
Furthermore, the use of auxin-producing PGPB has been shown to minimise crop yield loss due to salinity. Yao et al., [67] have reported that salt-stressed cotton plants inoculated with IAA-producing P. putida increased in growth parameters with IAA content. The auxin content in shoots and roots of Arachis hypogaea L. plants was increased through the application of IAA-producing PGPB strains under salinity (100 mM NaCl), whose effects also positively affected various growth parameters [66]. In addition, the inoculation of salt-stressed wheat plants with a salt-tolerant and IAA-producing Azospirillum strain exhibited enhancements in production parameters, including weight, chlorophyll, and micronutrient concentration [81]. The inoculation of salt-stressed wheat plants with Streptomyces (with the ability to produce IAA) also improved growth and development parameters [82].
In this sense, it has been shown that there is a correlation between bacterial IAA production and plant hormone status modification, which has positive effects on plant growth and development ( Figure 2). Thus, both the use of exogenous IAA and inoculation with an IAA-deficient mutant (A. brasilense Sp245 indole pyruvate decarboxylase -ipdCmutant, generating only 10% of wild-type auxin production), showed that the growth response of Phaseolus vulgaris L. roots is related to a differential response to the bacterially produced auxin, in terms of root dry weight, nodule number, and the number of basal roots formed during germination [83].

Ethylene (ACC-Deaminase)
Ethylene is commonly known as a stress hormone, due to its synthesis in response to abiotic and biotic stress in plants [77]. This organic compound is regarded as an inhibitor of root growth and formation, also negatively influencing plant development as a whole [35,42]. Aminocyclopropane-1-carboxylate (ACC) is the precursor of ethylene biosynthesis, which can be transported specifically to stressed organs, where is converted into ethylene by the ACC oxidase enzyme [42,77]. PGPB influence the ethylene cycle in plants by inhibiting its production, which happens because rhizobacteria can secrete ACC deaminase, an enzyme which converts ACC into ammonia and α-ketobutyrate; possible sources of carbon and nitrogen for bacteria [1,34]. In this context, ACC deaminase-containing PGPB may mitigate stress symptoms and boost plant development, by reducing the levels of this stress hormone and preventing the associated growth inhibition (Figure 2) [34,35,84].
Many studies have shown that ACC deaminase-producing bacteria can diminish the ethylene inhibition due to salinity. Maize inoculated with Pseudomonas and Enterobacter strains under saline conditions demonstrated that ACC deaminase synthesized by these bacteria led to improvements in plant growth parameters and nutrient absorption, such as higher K + /Na + ratios and NPK uptake [85]. Barnawal et al. [84] have reported a correlation between the protection of Trigonella plants against osmotic stress and reduced levels of ACC, due to inoculation with ACC deaminase-containing rhizobacteria (Bacillus and Ensifer), which also generated improvements in growth and plant-microbe interaction. Achromobacter piechaudii inoculation increased the nutrient uptake (P and K), as well as the fresh and dry weights of tomato seedlings grown in the presence of up to 172 mM NaCl salt, and diminished ethylene production [86]. Three ACC deaminase-producing halotolerant bacteria (Brevibacterium, Bacillus, and Zhihengliuela) have been evaluated, in terms of improving red pepper growth under salt stress. Inoculation with these strains reduced ethylene production and enhanced plant development and nutrient acquisition [87]. The correlation between ACC deaminase production and protection against salt stress has been demonstrated in various reports. Thus, the inoculation of groundnut plants with an ACC deaminase-producing P. fluorescens strain enhanced their saline resistance and the yield of the plant, as compared with other strains lacking this activity [88]. In this sense, Orozco-Mosqueda et al. [51] and Ali et al. [89] have reported that ACC deaminase-deficient mutants (mutated at acdS) inoculated on salt-stressed tomato plants performed worse, in terms of different production parameters, compared to wild-type strains.
Furthermore, there exist microbes which are capable of producing both IAA and ACC deaminase. As previously noted, IAA induces cell division and root growth, and the ACC deaminase produced by these bacteria hydrolyse the excess ACC, as well as promoting plant development [1,35]. Therefore, the combined action of both phytohormones can also help the plant to cope with adverse environmental conditions. For example, IAA-and ACC deaminase-producing Pantoea dispersa led to improved production parameters in salt-affected Cicer arietinum L. plants (150 mM NaCl). These effects were associated with a higher K + /Na + ratio, chlorophyll content, and relative leaf water content [90].

Abscisic Acid (ABA)
Abscisic acid (ABA) is another phytohormone involved in the plant response to abiotic and biotic stresses, mainly in protection against drought, salt stress, and toxic metals [91]. Under osmotic stress, ABA is produced in roots, and then can be translocated into leaves. It is involved in stomatal closure (reducing transpiration and maintaining water potential), the growth and emergence of roots (enhancing water uptake), and ion homeostasis [77,91]. Many PGPB can alter the ABA status in plants, acting as modulators of plant ABA content and, thus, allowing for the management of salt stress.
Some reports have exhibited that PGPB inoculation prevents ABA accumulation in plants (Figure 2). According to Yao et al. [67], cotton plants inoculated with P. putida Rs198 showed biomass enhancements and salt tolerance, induced by higher nutrient uptake and lower ABA production. In this sense, the inoculation of cucumber plants with Burkholderia, Promicromonospora, and Acinetobacter strains under salt and drought stress were revealed to be effective, with consequent increases in biomass, chlorophyll, water, and ion content. These treated plants also presented down-regulation of ABA, compared with uninoculated controls [92]. Additionally, Belimov et al. [93] conducted inoculation trials in tomato plants (using wild-type and negative mutants in ABA), with two ABA metabolizing rhizobacteria, in which it was observed that microbial inoculation decreased ABA concentration in roots and leaves, and altered plant development under saline conditions. Further, B. aryabhattai ATL29 and A. woluwensis ATL43 strains inoculated on salt-stressed soybean plants caused an enhancement in plant growth productive parameters, as associated with a reduction in ABA endogenous levels and the expression of GmNARK genes (related to the induction of ABA production) [94]. Finally, K. rhizophila Y1 inoculation protected maize from salt stress by regulating plant hormones: IAA (positively) and ABA (negatively). This study indicated that strain Y1 inoculation reduced ABA content markedly, in comparison with non-inoculated treatments, under salt stress treatment; these results being associated with the down-regulation of ZmNCED1 (the key gene for ABA synthesis) [63].
On the other hand, other studies have found that PGPB treatments improved ABA content in plants ( Figure 2). Thus, Salomon et al. [95] have indicated that Bacillus and Pseudomonas strains (ABA-producing) act as stress alleviators in Vitis vinifera L., by inducing ABA synthesis and, so, reducing water losses. In another report, Cohen et al. [96] proposed that an ABA-producing Azospirillum lipoferum strain reversed the negative effects caused by osmotic stress in maize plants, even using ABA synthesis inhibitors. These results were correlated with ABA levels assessed by GC-EIMS. Furthermore, inoculation of maize plants with B. pumilis positively modulated the ABA content in leaves, while increases in water content, photosynthetic pigments, and osmotic potential were also recorded. This established the great potential of this bacterium for formulations to alleviate osmotic stress [97]. In this way, the evidence seems to indicate that PGPB are capable of modifying ABA levels, optimizing their function and regulation (which are already complex), while presenting different levels, according to the stage of development of the plant [98,99].

Other Molecules Synthesized by Rhizobacteria
Certain bacterial mechanisms for modulating salt stress in plants are related to the secretion of extracellular molecules, such as volatile organic compounds or other organic compounds [1,34]. These substances act as inter-organismal signals, which affect plant behaviour by manipulating response pathways and regulatory functions, eliciting positive effects against stress conditions [100,101], and several species are able to produce some which can alleviate osmotic and salinity stress ( Table 2).

Volatile Organic Compounds (VOCs)
Volatile Organic Compounds (VOCs) are carbon-containing chemical substances with low molecular masses and boiling points, which can be emitted by rhizobacteria [1,79]. It has been reported that microbial volatiles can induce resistance to diseases and stimulate plant growth [79,102]. Other studies have indicated the effect of these substances in relieving salt stress in plants ( Figure 2). The application of a putative P. simiae VOCs blend to soybean (under 100 mM NaCl) decreased the Na + concentration in roots, and increased proline and chlorophyll content. Molecular analysis confirmed that this effect was induced by protein transcription changes [64]. Vaishnav et al. [103] has also found that two VOCs-namely, 4-nitroguaiacol and quinoline-promote soybean seed germination under 100 mM NaCl stress. Accordingly, Mentha x piperita L. plants grown under different NaCl levels (0 to 100 mM) were exposed to B. amyloliquefaciens GB03 VOCs (acetoin being the main one). This counteracted the negative effects of salinity, also causing a reduction in the endogenous levels of ABA in the plant [104].

Polyamines
Polyamines (PAs) are aliphatic amines with great antioxidant potential, which play an important role in plant development and abiotic stress response, by regulating antioxidant enzymes and genetic activities, as well as ROS homeostasis ( Figure 2). Spermidine, spermine, and putrescine are the most significant polyamines [1,101]. It has been shown that exogenous PA application can induce tolerance to salinity, but more exhaustive studies of the effects on plants of the PAs secreted by PGPR are necessary. For example, spermidine secreted by B. amyloliquefaciens SQR9 caused a decrease in the effects of oxidative damage, a reduction of Na + toxicity, and an inhibition of ABA accumulation in Zea mays L. plants. These resulted in plant salt tolerance enhancement, which was confirmed through the construction of mutants [105,106]. Moreover, tomato plants grown under osmotic stress and inoculated with B. megaterium TG1-E1 accumulated a higher level of arginine, a precursor in the synthesis of polyamines (e.g., spermidine, spermine, or putrescine) [107].

Bacteriocins and Lipo-Chitooligosaccharides
Bacteriocins are ribosomally synthesized peptides secreted by bacteria, which are bactericidal and/or bacteriostatic against organisms closely related to the producer, and active at low concentrations [1,108]. These molecules are used as a competitive advantage in the ecological niche. The use of bacteriocins, such as Thuricin, has been focused in the food industry and medicines, but also has agricultural potential [108]. Lipo-chitooligosaccharides (LCOs) are molecules produced by microbes that trigger their symbiotic interactions with plants [109]. Among them, Nod-factors (NFs) are secreted by rhizobacteria in response to flavonoids in root exudates, which initiate nodule formation [1,110]. For example, LCOs extracted from B. diazoefficiens USDA 110 and from R. tropici CIAT 889, in conjunction with various rhizobacterial strains (Bradyrhizobium and Azospirullum), have been shown to enhance grain quality and nodule formation in soybean [111]. Furthermore, NFs can positively affect plant growth, even under abiotic stresses ( Figure 2) [110,112,113]. Thuricin 17 (Th17), isolated from B. thuringiensis NEB17, has been shown to be a plant growth promoter under saline stress conditions, applied alone or in conjunction with Bradyrhizobium japonicum 532C LCOs. Brassica napus L. plants treated with Th17 showed a positive response under saline and temperature stress conditions, causing a higher biomass production and root development [113]. In this sense, the application of B. thuringiensis NEB17 Th17 and B. japonicum 532C LCOs to salt-stressed soybean (100 mM NaCl) altered the plant proteome, by positively regulating proteins involved in photosynthesis, metabolism, and stress-related pathways, such as: PEP carboxylase, rubisco oxygenase large subunit, glutathione-S-transferase (with antioxidant activity), and LEA proteins (involved in cellular dehydration tolerance) [110]. Thus, Th17 and LCO can manipulate the plant proteome profile and improve its physiological tolerance to salinity [110,112]. IAA production Higher root weight, and number of roots and nodules [83] Pseudomonas fluorescens and Enterobacter aerogenes Zea mays L. ACC deaminase production Increased plant height, biomass, K + /Na + ratio, and NPK uptake [85] Bacillus subtilis and Ensifer meliloti Trigonella foenum-graecum L.
ACC deaminase production Improved plant weight with lower ACC concentration [84] Achromobacter piechaudii Solanum lycopersicum L.
ACC deaminase production Increased fresh and dry weight, and P and K uptake [86] Brevibacterium iodinum, Bacillus licheniformis, and Zhihengliuela alba Capsicum annuum L.
Accumulation of osmoprotectans (trehalose) and ACC deaminase production Higher root and shoot length, total dry weight, and chlorophyll content [57] Pseudomonas fluorescens and Pseudomonas migulae Solanum lycopersicum L.
ACC deaminase production Higher biomass, chlorophyll content, and number of flowers and buds [89] Pantoea dispersa Cicer arietinum L.

Downregulation of ABA genes
Increased biomass, and chlorophyll, water, and ion (K and P) content [92] Rhodococcus sp. and Novosphingobium sp.
Metabolizing ABA Decreased ABA concentration in roots and leaves, and altered plant development [93] Bacillus aryabhattai and Arthrobacter woluwensis Glycine max L. Reduction in ABA endogenous levels and downregulation of ABA genes Increased fresh and dry weight, length, and chlorophyll content [94] Kocuria rhizophila Zea mays L.
Transcriptional changes in ion transporter genes (HKT and NHX-type) and hormonal changes (IAA and ABA) Decreased Na + accumulation and increased productivity parameters [63] Bacillus licheniformis and Pseudomonas fluorescens Vitis vinifera L.
ABA production and accumulation in plants Diminished plant water loss rate [95] Azospirillum lipoferum Zea mays L. ABA, IAA, and gibberellins production Reversed negative effects caused by osmotic stress [96] Bacillus pumilis Zea mays L. ABA production and accumulation in leaves Increased water content, photosynthetic pigments, and osmotic potential [97] Other molecules synthesized by rhizobacteria Pseudomonas simiae Glycine max L. Transcriptional changes in phosphatase activity, accumulation of osmoprotectans (proline), and VOCs production Higher weight and length, and K + /Na + ratio [64] Pseudomonas psimiae Glycine max L. VOCs production and transcriptional changes in phosphatase activity Promoted seed germination [103] Bacillus amyloliquefaciens Mentha x piperita L.
VOCs production and reduction of ABA endogenous levels Higher total chlorophyll content, and better morphological characteristics [104] Bacillus amyloliquefaciens Zea mays L. Polyamine production (spermidine) Decreased oxidative damage and Na + toxicity, and inhibiton of ABA accumulation in plants [105,106] Bacillus megaterium Solanum lycopersicum L.

Production of polyamine precursors
Osmotic stress resistance [107] Bradyrhizobium japonicum and Bacillus thuringiensis Brassica napus L.
Lipo-chitooligosaccharide and bacteriocin production Affected plant growth, architecture, and biomass [113] Bradyrhizobium japonicum and Bacillus thuringiensis Glycine max L. Lipo-chitooligosaccharide and bacteriocin production Changes in the proteome during seed germination [110]

Conclusions
Soil salinity is one of the main causes of abiotic stress in plants, as it generates not only environmental, but also economic and social problems. Crop yields can be reduced by the effects of salinity in plants (e.g., osmotic stress, ion toxicity, nutrient deficiency, and oxidative stress) and soils (loss of structure and fertility). In this sense, the use of plant growth-promoting bacteria (PGPB) has been reported as a sustainable and cost-effective alternative to increase plant tolerance to salt stress. Stress adaptation of plants is induced by the microbiota, through: i) changes in plant hormonal balance (e.g., IAA and ABA production, or inhibition of ethylene synthesis); ii) the release of extracellular compounds that act as chemical signals for the plant (e.g., LCOs, PAs, and/or VOCs), or enhancers that improve the soil conditions for plant development (e.g., EPS or Bacteriocins); iii) regulating the internal ionic content of the plant (e.g., inducing ion transporters or regulating the exchange of macro and micronutrients); and iv) facilitating the synthesis of osmoprotectant compounds that reduce osmotic stress (e.g., soluble sugars, proline, betaine, or trehalose).
Despite the studies carried out on these mechanisms to date, there exist other beneficial effects of soil microbiota that remain unknown, making it necessary to identify them, in order to optimise the use of PGPB in agronomic systems. Moreover, it is important to bear in mind that the action of these mechanisms is not individual, but that the same micro-organism may induce different effects in the plant.
Therefore, the potential that PGPB provide is an incalculable resource favouring the salt tolerance and, thereby, reducing the effects of soil salinity in crops. In this line, many studies have shown that inoculation with halotolerant bacteria can lead to salinity alleviation in plants, but not all of them have investigated the mechanisms underlying these effects. Furthermore, the range of micro-organisms capable of growing in saline conditions and promoting plant development is very wide. For all of these reasons, there exists a need for a deeper understanding and knowledge of plant-micro-organism interactions and the PGPB mechanisms which mitigate salt stress in plants.

Conflicts of Interest:
The authors declare no conflict of interest.