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Review

Role of Halotolerant Plant Growth-Promoting Rhizobacteria in Mitigating Salinity Stress: Recent Advances and Possibilities

by
Vikash Kumar
1,
Nikhil Raghuvanshi
2,
Abhay K. Pandey
3,
Abhishek Kumar
4,
Emily Thoday-Kennedy
5 and
Surya Kant
5,6,*
1
Faculty of Agricultural Science, GLA University, Mathura, Uttar Pradesh 281 406, India
2
Department of Agriculture, Deen Dayal Upadhyaya Gorakhpur University, Gorakhpur, Uttar Pradesh 273 009, India
3
Department of Mycology and Microbiology, Tea Research Association-North Bengal Regional R & D Center, Nagrakata, West Bengal 735 225, India
4
Department of Plant Pathology, Chaudhary Charan Singh Haryana Agriculture University, Hisar, Haryana 125 004, India
5
Agriculture Victoria, Grains Innovation Park, Horsham, VIC 3400, Australia
6
School of Applied Systems Biology, La Trobe University, Bundoora, VIC 3083, Australia
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(1), 168; https://doi.org/10.3390/agriculture13010168
Submission received: 21 December 2022 / Revised: 5 January 2023 / Accepted: 6 January 2023 / Published: 9 January 2023
(This article belongs to the Section Crop Production)
Browse Figures
Versions Notes

Abstract

:
Soil salinity is one of the major abiotic constraints in agricultural ecosystems worldwide. High salinity levels have negative impacts on plant growth and yield, and affect soil physicochemical properties. Salinity also has adverse effects on the distribution and abundance of soil microorganisms. Salinity problems have previously been addressed in research, but most approaches, such as breeding for salt tolerant varieties and soil amelioration, are expensive and require years of efforts. Halotolerant plant growth-promoting rhizobacteria (HT-PGPR) secrete secondary metabolites, including osmoprotectants, exopolysaccharides, and volatile organic compounds. The importance of these compounds in promoting plant growth and reducing adverse effects under salinity stress has now been widely recognised. HT-PGPR are emerging as effective biological strategies for mitigating the harmful effects of high salinity; improving plant growth, development, and yield; and remediating degraded saline soils. This review describes the beneficial effects and growth-promoting mechanisms of various HT-PGPR, which are carried out by maintaining ion homeostasis, increasing nutrient availability, and the producing secondary metabolites, osmoprotectants, growth hormones, and volatile organic compounds. Exploring suitable HT-PGPR and applications in agriculture production systems can play a crucial role in reducing the adverse impacts of salinity stress and sustainable crop productivity.

1. Introduction

Food insecurity is a growing problem globally, owing to population growth, changing climates, and declining agricultural land, which threaten sustainable agriculture [1,2]. By 2070, the world population is expected to rise from 8 billion to 10 billion people [3]. This will require more farmland to meet the increasing food demand, but environmental factors including rising temperatures, erratic rainfall patterns, drought and soil salinity already limit land suitable for agricultural production [4]. Soil salinization is a major contributor to the degradation of agricultural land and reductions in crop productivity, with salinity affecting over 800 million hectares of land or 6% of the total worldwide land area [5]. Crop growth is impeded by salinity due to the toxicity of certain ions, nutrient imbalances, and osmotic stress [6], and low levels of organic matter in the soil, all of which can amplify the unfavourable effects of salinization [7,8]. The replacement of the ions responsible for salinity, either chemically or through the addition of organic materials has been effective in the amelioration of saline soils [9]. The productivity of such saline soils can therefore be increased through the adoption of new sustainable approaches, such as the use of inorganic or organic soil amendments and salt-resistant crop varieties [10].
Based on their responses to saline conditions, plants can be separated into two categories, glycophytes and halophytes, with the majority of plant species being glycophytes, and therefore relatively intolerant to salinity [11,12]. Halophytes, salt tolerant species, have evolved specialised strategies for survival in these conditions, such as root and shoot salt exclusion, ion compartmenting into various organs, and the synthesis of compatible solutes. The metabolic capacity of plants to respond to salt stress can also be enhanced by microbial interactions [13]. Research has shown many instances where microorganism-based plant biotechnology has proven to be more effective than traditional plant breeding or genetic modification techniques, and even soil amelioration approaches in alleviating soil constraints [14]. Microbes such as halotolerant plant growth-promoting rhizobacteria (HT-PGPR) can use a wide range of metabolic and genetic strategies to assist plants in mitigating the effects of salt stress and other abiotic stresses caused by harsh environmental conditions [15,16]. HT-PGPR are able to produce a wide range of secondary metabolites that aid in plant protection and assist in maintaining growth under saline environments, for both the symbiotic plant and bacteria species [17,18]. Most of these metabolites are only formed under abiotic stress conditions and enable the plant to survive in extreme climatic conditions, by acting on vital survival mechanisms including ion transport systems and uptake of osmoprotectants (Figure 1) [19]. Associated organic compounds have recently been shown to support plants in better adapting to saline conditions [20]. This review focuses on the important roles of HT-PGPR and their secondary metabolites, which could be used as next-generation bioinoculants for salt-affected agroecosystems.

2. HT-PGPR: Diversity and Their Effect on Crop Production

The use of HT-PGPR has recently emerged as a viable solution to issues associated with increasing soil salinity in agricultural lands [21]. These halophilic and halotolerant microorganisms are already adapted to thrive in salty environments [22] and through symbiotic relationships with associated plant species, they can influence host plant survival, root development, and growth (Figure 2) [23]. HT-PGPR can not only recognise and react to signal molecules secreted by plant roots, but also secrete a diverse range of signalling molecules that influence plant behaviour. These microbes also synthesis beneficial molecules including siderophores, phytohormones, volatile organic compounds (VOCs), exopolysaccharides (EPS), and other metabolites, along with solubilising nutrients such as phosphorus (P), zinc (Zn), and potassium (K) (Figure 2) [14,15]. These metabolites can assist plants through a wide range of biochemical, physiological, and molecular responses, including preserving ionic homeostasis through Na+/K+ transporters, enhancing water capacity, and activating SOS (Salt-Overly Sensitive) genes [24,25], together with acting as osmoprotectants, antioxidants, and compatible solutes. This three-tiered interwoven action–cumulation association between HT-PGPR and plant salt stress responses includes the existence of the bacteria itself in hyperosmotic conditions, the induction of salt-resistance in crops, and the improvement of soil quality [26] (Figure 1). Crop salt stress has been found to be reduced by several HT-PGPR species, including Azospirillum, Arhrobacter, Burkholderia, Alcaligenes, Bacillus, Enterobacter, Klebsiella, Microbacterium, Streptomyces, Pseudomonas, Pantoea, and Rhizobium [27]. These species may occur naturally around crop species or can be isolated from native halophytic plants.
Wheat inoculated with HT-PGPR Enterobacter cloacae, Pseudomonas putida, Pseudomonas fluorescens, and Serratia ficaria, then cultivated in naturally saline fields (ECe = 15 dSm−1), had increased germination rates, percentage, and index by 51%, 43%, and 123%, respectively, in comparison to the nontreated controls, along with increased yield [28]. Another study found that the shoot and root fresh and dry biomass weights of Brassica juncea, cultivated in saline conditions (ECe = 12 dSm−1), significantly increased after inoculation with salt-tolerant Pseudomonas azotoformans JMM15 and Pseudomonas argentinensis HMM57 strains [29]. Additionally, an F-11 halotolerant Staphylococcus jettensis F1 increased the dry biomass of Zea mays by a factor of three when plants were grown under 200 mM saline stress [30]. Pseudomonas putida performed best among strains tested under high salinity (15 dSm−1), increasing plant height by 52%, root length by 60%, grain output by 76%, 100-grain weight by 19%, and straw yield by 67%, in wheat compared to the uninoculated crop [31]. Although it has been shown that HT-PGPR may improve crop production (in salt-affected soil) and reduce salinity stress, there is still much to learn about the interactions and processes that take place between plants and microorganisms under multidimensional stresses like salinity.

3. HT-PGPR and Their Effects in Mitigating Salt Stress in Crops

HT-PGPR provide plants with resistance to salt stress through several key processes. One such process is the regulation of the salt overly sensitive (SOS) pathway, which is involved in salt influx/efflux across membranes, through metabolites and associated gene expression patterns. It has been shown that the SOS1 gene is directly regulated by metabolites such as EPS, VOCs, and suitable solutes (i.e., proline, glycine betaines, and trehalose) [25], which also direct stress regulation in SOS genes [3], HKT1 transporter (high-affinity K) expression [32], and other genes implicated in the reduction in salt stress, i.e., ethylene biosynthesis and antioxidant protein encoding genes [33,34]. Examples of the beneficial effects of HT-PGPR, along with how they help plants cope with saline conditions in different plants, are reviewed and presented in Table 1. The following sections further discuss the importance and beneficial aspects of HT-PGPR, how metabolites are biosynthesised or promoted by HT-PGPR, and the role of these mechanisms in improving plant salinity tolerance.

4. Plant Growth-Promoting Mechanisms by HT-PGPR

4.1. HT-PGPR Mediated Increased Availability of Soil Nutrients

Reduced bioavailability of nutrients due to altered physicochemical properties is a common problem of salinity stress [69,70,71]. The composition and level of salinity, the concentration of nutrients, and environmental conditions all have an impact on the interaction between mineral nutrition and salinity [72]. Continuous applications of chemical fertilisers can be a temporary solution to address these issues, but pose environmental risks, reduces soil health, and, paradoxically, can increase soil salinity [73]. Therefore, the use of beneficial microorganisms to enhance nutrient bioavailability, rather than chemical amendments, is potentially a more environmentally friendly and sustainable approach to crop production [74].
Nitrogen (N) is necessary for plant growth and productivity, as it is primarily involved in the synthesis of enzymes, proteins, RNA, and DNA within plant cells [75]. High chloride (Cl−) content, and therefore uptake in saline soils, can greatly diminish the uptake of N and sulphur (S) by plants [70]. The ability of HT-PGPR to increase essential soil nutrient bioavailability is possible through a wide range of action mechanisms. N is abundant in the air, but plants can only absorb it in the form of nitrate (NO3−) or ammonium (NH4+) [76]. N-fixing bacteria, such as Pseudozyma rugulosa, Cryptococcus flavus, and Pseudozyma antarctica can convert atmospheric N into plant-available NO3− or NH4+, especially under saline conditions, through a loose symbiosis mechanism also known as biological nitrogen fixation [77,78,79]. Typically limited to bacteria, it has also been shown that a soil-isolated yeast strain, Candida tropicalis, possesses an intriguing and remarkable ability to fix N [80], as well as the NH4+-producing yeast Meyerozyma [81,82]. These N-fixing bacteria, known as rhizobacteria, live as free-living ectorhizospheric or endophytic symbiotics on plant roots [83]. These rhizobacteria are able to fix atmospheric N into ammonia due to the presence of FixABX genes, which are necessary for free-living bacteria, and Nif genes, which encode the production of nitrogenase enzymes that reduce atmospheric N into ammonia [84]. Under saline stress, the host plants are then able to directly absorb the fixed plant-available N, relieving some of the stress on the plant caused by salinity-induced N deficiencies [85].
P is essential in many biochemical processes and a component of nucleic acids, nucleotide coenzymes, and metabolic intermediates [86]. Plants under severe salt stress often have a deficiency in P [87], owing to competition with Na+ ions for membrane-transporter binding sites. When applied to soil, HT-PGPR with phosphate-solubilising capabilities, known as phosphate-solubilising bacteria (PSB), can significantly aid in raising soil P availabilities. PSBs have been shown to increase yields up to 50% without increasing the need for P fertilisers [88]. To meet the needs of plants, PSBs dissolve and absorb insoluble phosphate (Pi) to make it available for plant uptake. Two distinct types of PSBs can be identified by examining their P-dissolving patterns, (i) those that secrete organic acid to dissolve Pi compounds, and (ii) those that secrete phosphatase to enzymatically mineralise Pi compounds. By lowering soil pH and creating a P-offering micro-area around the plant rhizosphere, applications of both types of PSBs increase the plant’s access to P, and boost the efficiency of other beneficial microorganisms such as Rhizobium and Trichoderma [89]. The PSBs secretes low-molecular-weight organic acids, such as gluconic acid, citric acid, succinic acid, propionic acid, and lactic acid, as by-products of sugar metabolism in root exudates, which aid in the digestion and assimilation of nutritionally important ionic compounds [90].
HT-PGPR are also able to solubilise organic K and Zn in the soil, using organic acid secretions and a resulting change in soil pH [46,79]. Rhizobacteria can also increase soil Fe bioavailability by synthesising siderophores, which are low-molecular-weight (0.5–1 kDa) compounds with functional groups of hydroximates and catechol’s, which have a high affinity for ferric ions and a reversible binding mechanism [91,92]. Plants can then easily access the bacterial siderophore–Fe complexes that have formed, absorbing them via chelate destruction, direct uptake, or even hypothesised ligand exchanges [93]. Plant-made siderophores (phytosiderophores) may initiate the ligand exchange reaction between the bacterial siderophores and the Fe-containing complex, allowing the plants to take up the transferred Fe [94].

4.2. HT-PGPR Mediation Increase Availability of Indole-3-Acetic Acid

Indole-3-acetic acid (IAA) is a key plant hormone, important for seed germination, improved root and leaf growth, and reduction in adverse effects of salinity to plant production [95]. Exogenous production of phytohormones is not limited to only plants, in fact, many HT-PGPR have the ability to produce IAA, making them perfect bioinoculants to increase symbiotic plant IAA levels, which would improve plant growth under salinity stress [68,71,96]. HT-PGPR are able to use L-tryptophan, found in root exudates, as a precursor in the production of exogenous bacterial IAA [97], with the amount of IAA produced being altered by environmental conditions such as pH, temperature, osmotic stress, and carbon limitation [98]. The hydrolysis of IAA conjugates has also been hypothesised to result in IAA formation. Inducible adenylate cyclase is produced by Pseudomonas, Bacillus, Klebsiella, Azospirillum, Enterobacter, and Serratia [99]. Root-associated bacteria that produce IAA may also aid in nodule formation and stimulate the expansion of root system by means of the development of lateral roots [100]. The exogenous IAA synthesised by HT-PGPR helps maintain a healthy ratio of endogenous IAA in the roots, promoting root growth and development, increasing root mass and size, encouraging root exudations, and forming lateral roots, allowing the plant to make greater soil contact. In high salt environments, plant root systems can therefore be improved with symbiotic HT-PGPR relationships, increasing capacity for nutrient exchanges, water uptake, and growth [101,102,103]. This, in turn, can help plant leaves continue to grow, keeping photosynthetic rates and yields relatively unchanged. Table 2 gives examples of isolated IAA-producing microbes that have significantly increased shoot length and weight (fresh and dry), root length and weight (fresh and dry), and germination rates of salt-sensitive crop seeds grown under saline conditions. In addition, control plants showed either slight improvements or no effects from the selected microbes [93,104,105].

4.3. HT-PGPR Modulations of Ethylene

A key phytohormone that acts as a stress signal is ethylene, and at low concentrations triggers a number of defence mechanisms that help plants manage biotic and abiotic stresses [116]. The second peak of ethylene synthesis, also called stress ethylene, occurs only under conditions of prolonged and extreme stress. Roots are negatively impacted by stress ethylene as their development is stunted, which in turn affects root function, vegetative growth, and, ultimately, productivity and yield [87,117,118]. Plants produce ethylene from its precursor, 1-aminocyclopropane-1-carboxylic acid (ACC), which is oxidised by the enzyme ACC oxidase. Through the production of the enzyme ACC deaminase (ACC-D), some HT-PGPR with the AcdS genes can convert ACC found in root exudates into ammonia and ketobutyrate. As a result, the by-products are used by the rhizobacteria as their sole source of C and N [119]. In stressed plants, HT-PGPR and ACC-D activity of at least 20 nmol mg−1 h−1 can dramatically reduce the total pool level of ethylene precursors, and may diminish the second peak of ethylene production by as much as 90% [120]. The subsequent drop in ethylene concentration improves plant resistance to stress, restoring root function and allowing it to flourish despite adverse conditions [121]. Ethylene also interacts with other phytohormones either by manipulating gene expression or by affecting transcription factors [122], therefore the fine-tuning of ethylene levels may be a pathway to increased salt tolerance.

4.4. HT-PGPR Improves Osmoprotectants, Compatible Solutes, and Ion Homeostasis

The optimal operation of a plant’s physiological and metabolic functions depends on water homeostasis. Excessive salt accumulation in soil disrupts a plant cell’s ability to absorb water, and causes ionic toxicity and osmotic stress (Cl− and Na+ accumulation), which in turn prevents plant growth and development [123]. Numerous vital physiological processes, such as stem and root growth, photosynthesis and transpiration, cell structure maturation, hormonal status, nutrient uptake, and enzyme activity are therefore disrupted by the abundance of ions and hypertonic conditions [124,125]. To adapt to saline conditions, HT-PGPR mutually partnered with plants, will produce metabolites with low molecular weights that are recognised as relevant solutes, or osmoprotectant substances, which then aid in plant stress reduction, maintain high turgor pressure, and equalise ion efflux across the plasma membrane (Figure 3) [126]. To help plants with their water shortage, these substances also regulate stomatal opening, transpiration rate, and hydraulic conductivity [127,128]. Among the many suitable solutes produced by HT-PGPR, glycine betaine, carnitine, and especially proline, a reactive oxygen species (ROS) scavenger, are vital to plants [129,130]. Through processes like those shown in Figure 2, rhizobacteria help plants recover from abiotic stress by either acquiring these molecules from the surroundings or de novo production, depending on the stress level. Proline synthesis in particular is upregulated by plants during osmotic stress [131], as well as in response to HT-PGPR [17], enhancing control of cytosolic pH and maintain cell protein structures [132]. Most bacteria require the combined enzyme activity of glutamyl phosphate reductase, glutamyl kinase, and 1-1-pyrroline-5-carboxylate reductase to synthesise proline, with genes ProB, ProA, and ProC inducing this catalytic reaction [129,133]. Proline dehydrogenase enzyme activity has been shown to increase under salinity stress, leading to N-fixing bacteria showing higher proline metabolism [134,135]. Under saline circumstances, an HT-PGPR (Bacillus fortis strain SSB21) was involved in improved growth, increased chlorophyll and protein levels, and water use efficiency, due to increased proline synthesis [136]. Inoculation of Mentha arvensis with HT-PGPR from the genera Exiguobacterium, Bacillus, and Halomonas, also had a greater foliar proline concentration, compared to control plants [2].
Inoculating salt-sensitive plants with HT-PGPR can help to maintain ion homeostasis (K+/Na+), promote osmolyte accumulation, and increase nutrient (P, N, K, Mg, and Ca) bioavailability, which confers resistance against the negative consequences of salinity. Under 300 mM salt stress, the injection of salt-resistant Paenibacillus yonginensis DCY84T onto ginseng seeds resulted in increased levels of proline, polyamine, and total soluble sugars. Additionally, the treatment improved the nutritional availability of salt-stressed plants, ABA production, chlorophyll content, and the stimulation of stress-responsive genes [137]. Another suitable solute, glycine betaine (GB), accumulates in the cytosol of plants to counteract the effects of salt stress by reducing osmotic stress and preserving plant cell integrity as a whole [138,139]. When administered exogenously, GB improved salt tolerance in soybean, as evidenced by lower Na+ concentrations and increased catalase (CAT) and superoxide dismutase (SOD) activity in treated plants [140]. In Bacillus subtilis, GB production is initiated by the activity of two enzymes, (i) a precursor molecule, choline, an intermediary chemical GB aldehyde, is oxidised by type III alcohol dehydrogenase, and (ii) an end product called GB aldehyde dehydrogenase [129,141,142]. The generation of GB in transgenic plants often involves the choline oxidase enzyme from Arthrobacter globiformis, which turns choline into GB [143]. Increased concentrations of GB were seen in maize after being injected with HT-PGPR Bacillus subtilis HL3RS14, with plants under salt stress growing quicker [144]. Similarly, Acacia gerrardii infected with Bacillus subtilis BERA71 produced more GB and osmolyte under saline conditions [145].
On exposure to salt stress, ectoine (1,4,5,6-tetrahydro2-methyl-4-pyrimidinecarboxylic acid), another osmolyte, accumulates in the cytoplasm of plants [146]. Three enzymes, L-ectoine synthase, L-2,4-diaminobutyric acid aminotransferase, and L-2,4-diaminobutyric acid acetyltransferase, are involved in the synthesis of ectoine in bacteria, activated by EctB, EctA, and EctC genes [147]. In HT-PGPR, ectoine production quantity is inversely correlated with the rise in intracellular osmotic strain caused by various factors, such as salt stress [148]. In an experiment, it was discovered that ectoine, which was isolated from the halophilic Chromohalobacter salexigens KT989776, improved flax seed germination and decreased salt accumulation, phenoloxidase, and peroxidase activities in crops [149]. Trehalose, nonreducing disaccharides with two glucose moieties linked by α-1,1-glycosidic linkages, is another osmoprotectant used by HT-PGPR [150]. Trehalose cannot be produced by plants; however, HTPGPR play a significant role in supporting plants under salt stress by forming this osmoprotectant. Trehalose synthase, Alpha-trehalose-phosphate synthase, and Trehalose-6-phosphate phosphatase are a few of the enzymes that are included in trehalose production in HT-PGPR and are encoded by the OtsAB genes [151]. Most bacteria use the TreS and TreY/TreZ pathways to synthesise trehalose and tolerate the effects of salt stress, with trehalose levels increased during salinity and drought stress, similar to many other osmoprotectants [152,153]. Azospirillum brasilence, with the trehalose biosynthesis gene overexpressed, was used to inoculate maize, which then had increased root and leaf biomass, and increased ability to withstand osmotic stress. Similarly, when Rhizobium etli with trehalose-6-phosphate synthase overexpression, was inoculated into Phaseolus vulagris, plants showed osmotic stress resistance, higher number of nodules, and increased plant biomass [154]. Osmolyte accumulation and synthesis by HT-PGPR is therefore one of the critical processes that contribute to the reduction in multiple stress components caused by salinity. To decrease agricultural losses, salt-resistant transgenic crops may be created by genetically manipulating the genes from HT-PGPR that produce secondary metabolites [152].

4.5. Production of Exopolysaccharides and Volatile Organic Compounds by HT-PGPR

Exopolysaccharides (EPS) are often generated by HT-PGPR metabolites. Under salinity conditions, EPS production alone accounts for 40–90% of the weight of the bacterial extracellular matrix [108,155]. EPS facilitate microbial adhesion to plant roots, aid in biofilm formation to prevent cells from drying out due to salt stress, and increases the movement of bacteria that are connected to plant roots [156,157,158]. The phase of bacterial development, the composition of the medium, and exposure to environmental stresses, such as salt and dehydration, all affect EPS production [159,160]. Additionally, it has been shown that EPS have strong antioxidant properties and give bacteria resistance to ROS-dependent cell death. For example, the endophytic bacteria Gluconacetobacter diazotrophicus was shown in vitro and during rice plant colonisation, to be protected against oxidative destruction by EPS [161]. Similarly, the multilayer antioxidant activity of EPS generated by the halotolerant endophyte Glutamicibacter halophytocola KLBMP 5180 was studied to mitigate the destruction caused by salt stress on crops [162]. Another activity of EPS is soil aggregation and enhancing root-adhering soil through the formation of a sheath around roots, which increases water availability and nutrient (P, N, Fe, and K) accumulation from the soil [69,163]. Exopolysaccharides EX01 enhanced rice growth and improved osmotic stress tolerance through the increased expression of the HKT1/K+ transporter, minimising Na+ inflow and therefore reducing ionic toxicity in plants [23].
By regulating important plant metabolic processes and maintaining soil physicochemical properties, EPS-producing bacteria may also help increase crop production under saline conditions [43,164]. In addition to these well-recognised functions, bacterial EPS are also associated with cellular sensing and rhizosphere recognition, the protection of plants from phytopathogens, and act as a carbon source under nutrient-deficient settings [165,166]. In a severely salinized field (EC > 10 dS/m), Tiwari et al. [166] reported that inoculation with EPS-producing Pseudomonas sp. increased the yield of sunflower. Analysis also showed a decrease in the prevalence of charcoal rot virus in Macrophomina phaseolina under salinity soil after HT-PGPR inoculation. Salt-tolerant bacteria such as Bacillus insolitus, Bacillus amyloliquefaciens, Pseudomonas syringae, and Microbacterium spp. may improve wheat growth by preventing Na+ input into the stele of plants under salinity stress [167]. Mung beans treated with EPS-producing Bacillus drentensis and Enterobacter cloacae, under salt stress, showed increased availability of nutrients and water absorption in plants due to biofilm formation in the root zone [168]. Similarly, Pantoea alhagi NX-11, an EPS-producing endophyte, inoculation increased the salt resistance of rice plantlets by enhancing antioxidant activity, leading to greater development when compared to those plantings inoculated with EPS mutant NX-11eps [169]. In salty environments, maize treated with EPS-producing Azotobacter chrococcum strains C5 and C9 had reduced salt stress through increased K+/Na+ ratio, chlorophyll content, ion absorption (K, Na, Mg, Ca), and accumulation of polyphenols and proline [170], while an EPS-based Alcaligenes sp. bioformulation was especially effective in decreasing osmotic stress in rice [171]. In general, studies indicate that EPS generated by HT-PGPR play significant roles in assisting plants minimise salt stress effects and may be utilised as bioinoculants to enhance soil quality, rhizosphere colonisation, and nutrient uptake under saline conditions. EPS could also be used as a bioinoculant amendment to help protect the HT-PGPR microbes from the initial stress encountered when first introduced into saline soils.
When exposed to salinity or other environmental stresses, HT-PGPR produce volatile organic compounds (VOCs) less than 300 Da molecular weight, with lipophilic natures and a low boiling points [172,173]. Numerous microbial volatiles have been documented, and most have the potential to enhance the overall growth of crops [174]. VOCs are often employed as markers to identify individual bacterial species in ecosystems, and to determine how these communities interact [175]. Plant hormones expansin, gibberellin, auxin, ethylene, and cytokinin were affected by the 1,3-propanediol and VOC albuterol generated by Bacillus subtilis SYST2, demonstrating the impact these compounds can have on plant regulation [176]. The most researched bacterial VOCs include dimethyl disulfide, geosmin, acetoin, and 2,3-butanediol, which aid in composting, auxin homeostasis, sulphur nutrition, cell growth, inducing systemic and drought resistance in crops, and soil formation processes [177,178,179,180]. Alcohols, aldehydes, and ketones were found to be the most common VOCs released by six different Bacillus strains [181]. In Arabidopsis, most VOCs promote lateral root development and primary root growth, with shoot and root biomass increases seen due to VOCs generated by root-associated Microbacterium spp. Just a short interaction with bacterial VOCs can promote plant development, indicating that these compounds may be used to prepare crops without subjecting them to direct or prolonged bacterial exposure. Additionally, it was shown that the VOC-mediated crop development proliferation was tissue-dependent and only caused a biomass increase in crops that were exposed to VOCs through their roots [182]. Under 150 mM salt stress, quinoline and 4-nitroguaiacol, two bacterial VOCs generated by salt-resistant Pseudomonas simiae, and a VOC-producing HT-PGPR Paraburkholderia phytofirmans PsJN, not only alleviated salt stress, but also stimulated Arabidopsis development in an extreme salinity environment [183].
The control of the HKT1/K+ transporter, which prevents Na+ inflow under salt stress, has been demonstrated to be related to the synthesis of VOCs [23], with VOC-generating Bacillus subtilis increasing the salt-resistance of Arabidopsis by suppressing the HKT1 gene expression. Alcaligenes faecalis JBCS1294 produces a combination of three bacterial VOCs (propionic acid, benzoic acid, and butyric acid) [184], which in Arabidopsis stimulated plant development and promoted salt-resistance by regulating ionic transporters and hormonal pathways. Systematic investigation of microbial VOCs suggests that these substances could have previously unknown biological activities and ecological implications [174]. Though VOCs have significant contributions to plant stress tolerance pathways, including ion acquisition and controlling growth hormones, there is still much to learn about these metabolites, their direct functions, and their ability to help plants under stress. More research on microbial VOCs that help crops manage adverse environmental effects could lead to the creation of new agricultural bioinoculants.

5. Future Prospects

Increasing soil salinity significantly impacts agricultural productivity and presents a risk to food security. The use of HT-PGPR has shown preliminary effectiveness in increasing the salinity tolerance of crops through a range of mechanisms (Figure 4). Further studies are needed to understand how different HT-PGPR interact with plants, both in physiologically stressful and unstressed settings [185]. An emerging mapping approach known as “interactomics” is using bioinformatics tools to examine the interactions between biomolecules, including enzymes and proteins from rhizobacteria, and plant cells, to identify the communication channels between both partners under saline conditions [186]. As demonstrated in this review, it is possible to alter the phytomicrobiome surrounding plants via the decoding of feedback signals and interactions between microbes and plants. The in-depth study of the relationships between plant stress responses, microbiome assemblages, and signalling molecules is crucial for the future development of salt stress “smart agriculture” [187]. It will also be necessary to overcome the disadvantages of bioformulations, such as their short shelf life and inability to function in an abiotic stress environment. To enhance the quality of bioformulations for stressed agroecosystems, it may be possible to provide elements that reduce stress by using additives or metabolites to draw in microbes. In new formulations, HT-PGPR may be combined with osmoprotectants or cell-protectants to assist the microbes to progress beyond the initial stress and adapt to the environment. Fluorescent pseudomonads were more tolerant of salt after the exogenous addition of proline and glycine betaine to the growth media [188]. As a result, this may also be used to produce bioinoculants for saline soils. Therefore, by employing various HT-PGPR or their metabolites, novel bioformulations may be created to enhance crop production and increase the quality of saline soils (Figure 4 and Figure 5). In addition to helping prepare microbes and plants against stress such as salinity, altering gene elicitors that induce salt-stress responses and promote the creation of biofilms may also serve to save the newly added bacterium from the initial shock, as HT-PGPR that develop biofilms can protect plants and stimulate their development in salinity conditions [189]. Utilising HT-PGPR to increase saline soil productivity and quality may also have a significant impact on microbial diversity, nutrient availability, water activity, soil organic matter, pH, and EC. These cutting-edge formulas have the potential to not only protect and boost crop yields, but also help restore stressed and damaged agroecosystems.

6. Conclusions

In addition to acting as a potential probiotic for plants impacted by salt, HT-PGPR can also help saline soils regain their natural balance. These bacteria are a useful tool for achieving the goals of sustainable farming due to their capacity to grow and encourage symbiotic plant growth in challenging environments. The beneficial effects on improving crop productivity from HT-PGPR includes the production of organic acids, osmoprotectants, EPS and VOCs, and balancing ion homeostasis, as illustrated in Figure 5. There is still much research to be conducted on halotolerant microbiota composition, structure, and metabolites. Nevertheless, as described in this review, HT-PGPR offer a new and exciting avenue in sustainable agriculture and food security. Further research will yield additional insights for developing future bioformulations that will contribute to the remediation of challenging growing environments.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Myo, E.M.; Ge, B.; Ma, J.; Cui, H.; Liu, B.; Shi, L.; Jiang, M.; Zhang, K. Indole-3-Acetic Acid Production by Streptomyces Fradiae NKZ-259 and Its Formulation to Enhance Plant Growth. BMC Microbiol. 2019, 19, 155. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Bharti, N.; Barnawal, D.; Awasthi, A.; Yadav, A.; Kalra, A. Plant Growth Promoting Rhizobacteria Alleviate Salinity Induced Negative Effects on Growth, Oil Content and Physiological Status in Mentha Arvensis. Acta Physiol. Plant 2014, 36, 45–60. [Google Scholar] [CrossRef]
  3. Morris, J.; González, J.E. The Novel Genes EmmABC Are Associated with Exopolysaccharide Production, Motility, Stress Adaptation, and Symbiosis in Sinorhizobium Meliloti. J. Bacteriol. 2009, 191, 5890–5900. [Google Scholar] [CrossRef] [Green Version]
  4. Ladeiro, B. Saline Agriculture in the 21st Century: Using Salt Contaminated Resources to Cope Food Requirements. J. Bot. 2012, 2012, 310705. [Google Scholar] [CrossRef]
  5. Shahid, S.A.; Zaman, M.; Heng, L. Soil Salinity: Historical Perspectives and a World Overview of the Problem. In Guideline for Salinity Assessment, Mitigation and Adaptation Using Nuclear and Related Techniques; Zaman, M., Shahid, S.A., Heng, L., Eds.; Springer International Publishing: Cham, Switzerland, 2018; pp. 43–53. ISBN 978-3-319-96190-3. [Google Scholar]
  6. Hernandez Fernandez, M.T.; Mataix-Solera, J.; Lichner, L.; Štekaurová, V.; Zaujec, A.; Garcia Izquierdo, C. Assessing the Microbiological, Biochemical, Soil-Physical and Hydrological Effects of Amelioration of Degraded Soils in Semiarid Spain. Biologia 2007, 62, 542–546. [Google Scholar] [CrossRef]
  7. Upadhyay, S.K.; Singh, J.S.; Saxena, A.K.; Singh, D.P. Impact of PGPR Inoculation on Growth and Antioxidant Status of Wheat under Saline Conditions. Plant Biol. 2012, 14, 605–611. [Google Scholar] [CrossRef]
  8. Orhan, F. Alleviation of Salt Stress by Halotolerant and Halophilic Plant Growth-Promoting Bacteria in Wheat (Triticum aestivum). Braz. J. Microbiol. 2016, 47, 621. [Google Scholar] [CrossRef] [Green Version]
  9. Al-Yassin, A. Adverse Effects of Salinity on Citrus. A review paper. J. Cent Eur. Agric. 2004, 4, 263–272. [Google Scholar]
  10. Egamberdieva, D.; Wirth, S.; Bellingrath-Kimura, S.D.; Mishra, J.; Arora, N.K. Salt-Tolerant Plant Growth Promoting Rhizobacteria for Enhancing Crop Productivity of Saline Soils. Front. Microbiol. 2019, 10, 2791. [Google Scholar] [CrossRef] [Green Version]
  11. Mishra, A.; Tanna, B. Halophytes: Potential Resources for Salt Stress Tolerance Genes and Promoters. Front. Plant Sci. 2017, 8, 829. [Google Scholar] [CrossRef]
  12. Rahman, M.M.; Mostofa, M.G.; Keya, S.S.; Siddiqui, M.N.; Ansary, M.M.U.; Das, A.K.; Rahman, M.A.; Tran, L.S.-P. Adaptive Mechanisms of Halophytes and Their Potential in Improving Salinity Tolerance in Plants. Int. J. Mol. Sci. 2021, 22, 10733. [Google Scholar] [CrossRef] [PubMed]
  13. Nguyen, H.M.; Sako, K.; Matsui, A.; Suzuki, Y.; Mostofa, M.G.; Ha, C.V.; Tanaka, M.; Tran, L.-S.P.; Habu, Y.; Seki, M. Ethanol Enhances High-Salinity Stress Tolerance by Detoxifying Reactive Oxygen Species in Arabidopsis thaliana and Rice. Front. Plant Sci. 2017, 8, 1001. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Dong, O.X.; Ronald, P.C. Genetic Engineering for Disease Resistance in Plants: Recent Progress and Future Perspectives. Plant Physiol. 2019, 180, 26–38. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Singh, R.; Singh, P.; Sharma, R. Microorganism as a Tool of Bioremediation Technology for Cleaning Environment: A Review. Proc. Int. Acad. Ecol. Environ. Sci. 2014, 4, 1–6. [Google Scholar]
  16. Gopalakrishnan, S.; Sathya, A.; Vijayabharathi, R.; Varshney, R.K.; Gowda, C.L.L.; Krishnamurthy, L. Plant Growth Promoting Rhizobia: Challenges and Opportunities. 3 Biotech 2015, 5, 355–377. [Google Scholar] [CrossRef] [Green Version]
  17. Abbas, R.; Rasul, S.; Aslam, K.; Baber, M.; Shahid, M.; Mubeen, F.; Naqqash, T. Halotolerant PGPR: A Hope for Cultivation of Saline Soils. J. King Saud Univ. Sci. 2019, 31, 1195–1201. [Google Scholar] [CrossRef]
  18. Sharma, K.; Sharma, S.; Vaishnav, A.; Jain, R.; Singh, D.; Singh, H.B.; Goel, A.; Singh, S. Salt-Tolerant PGPR Strain Priestia Endophytica SK1 Promotes Fenugreek Growth under Salt Stress by Inducing Nitrogen Assimilation and Secondary Metabolites. J. Appl. Microbiol. 2022, 133, 2802–2813. [Google Scholar] [CrossRef]
  19. Egamberdieva, D.; Wirth, S.J.; Alqarawi, A.A.; Abd_Allah, E.F.; Hashem, A. Phytohormones and Beneficial Microbes: Essential Components for Plants to Balance Stress and Fitness. Front. Microbiol. 2017, 8, 2104. [Google Scholar] [CrossRef]
  20. Sunita, K.; Mishra, I.; Mishra, J.; Prakash, J.; Arora, N.K. Secondary Metabolites From Halotolerant Plant Growth Promoting Rhizobacteria for Ameliorating Salinity Stress in Plants. Front. Microbiol. 2020, 11, 567768. [Google Scholar] [CrossRef]
  21. Hernández-Canseco, J.; Bautista-Cruz, A.; Sánchez-Mendoza, S.; Aquino-Bolaños, T.; Sánchez-Medina, P.S. Plant Growth-Promoting Halobacteria and Their Ability to Protect Crops from Abiotic Stress: An Eco-Friendly Alternative for Saline Soils. Agronomy 2022, 12, 804. [Google Scholar] [CrossRef]
  22. Ruginescu, R.; Gomoiu, I.; Popescu, O.; Cojoc, R.; Neagu, S.; Lucaci, I.; Batrinescu-Moteau, C.; Enache, M. Bioprospecting for Novel Halophilic and Halotolerant Sources of Hydrolytic Enzymes in Brackish, Saline and Hypersaline Lakes of Romania. Microorganisms 2020, 8, 1903. [Google Scholar] [CrossRef] [PubMed]
  23. Zhang, H.; Kim, M.-S.; Sun, Y.; Dowd, S.E.; Shi, H.; Paré, P.W. Soil Bacteria Confer Plant Salt Tolerance by Tissue-Specific Regulation of the Sodium Transporter HKT1. Mol. Plant Microbe Interact. 2008, 21, 737–744. [Google Scholar] [CrossRef] [PubMed]
  24. Assaha, D.V.M.; Ueda, A.; Saneoka, H.; Al-Yahyai, R.; Yaish, M.W. The Role of Na+ and K+ Transporters in Salt Stress Adaptation in Glycophytes. Front. Physiol. 2017, 8, 509. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Pan, J.; Peng, F.; Xue, X.; You, Q.; Zhang, W.; Wang, T.; Huang, C. The Growth Promotion of Two Salt-Tolerant Plant Groups with PGPR Inoculation: A Meta-Analysis. Sustainability 2019, 11, 378. [Google Scholar] [CrossRef] [Green Version]
  26. Huang, X.-F.; Chaparro, J.M.; Reardon, K.F.; Zhang, R.; Shen, Q.; Vivanco, J.M. Rhizosphere Interactions: Root Exudates, Microbes, and Microbial Communities. Botany 2014, 92, 267–275. [Google Scholar] [CrossRef]
  27. Nadeem, S.M.; Zahir, Z.A.; Naveed, M.; Nawaz, S. Mitigation of Salinity-Induced Negative Impact on the Growth and Yield of Wheat by Plant Growth-Promoting Rhizobacteria in Naturally Saline Conditions. Ann. Microbiol. 2013, 63, 225–232. [Google Scholar] [CrossRef]
  28. Phour, M.; Sindhu, S.S. Amelioration of Salinity Stress and Growth Stimulation of Mustard (Brassica juncea L.) by Salt-Tolerant Pseudomonas Species. Appl. Soil Ecol. 2020, 149, 103518. [Google Scholar] [CrossRef]
  29. Aslam, F.; Ali, B. Halotolerant Bacterial Diversity Associated with Suaeda fruticosa (L.) Forssk. Improved Growth of Maize under Salinity Stress. Agronomy 2018, 8, 131. [Google Scholar] [CrossRef] [Green Version]
  30. Zahir, Z.A.; Ghani, U.; Naveed, M.; Nadeem, S.M.; Asghar, H.N. Comparative Effectiveness of Pseudomonas and Serratia Sp. Containing ACC-Deaminase for Improving Growth and Yield of Wheat (Triticum aestivum L.) under Salt-Stressed Conditions. Arch. Microbiol. 2009, 191, 415–424. [Google Scholar] [CrossRef]
  31. Kasotia, A.; Varma, A.; Tuteja, N.; Choudhary, D.K. Amelioration of Soybean Plant from Saline-Induced Condition by Exopolysaccharide Producing Pseudomonas-Mediated Expression of High Affinity K + -Transporter (HKT1) Gene. Curr. Sci. 2016, 111, 1961–1967. [Google Scholar] [CrossRef]
  32. Kwon, S.-W.; Park, J.-Y.; Kim, J.-S.; Kang, J.-W.; Cho, Y.-H.; Lim, C.-K.; Parker, M.A.; Lee, G.-B. Phylogenetic Analysis of the Genera Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium on the Basis of 16S RRNA Gene and Internally Transcribed Spacer Region Sequences. Int. J. Syst. Evol. Microbiol. 2005, 55, 263–270. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Kwon, Y.S.; Ryu, C.-M.; Lee, S.; Park, H.B.; Han, K.S.; Lee, J.H.; Lee, K.; Chung, W.S.; Jeong, M.-J.; Kim, H.K.; et al. Proteome Analysis of Arabidopsis Seedlings Exposed to Bacterial Volatiles. Planta 2010, 232, 1355–1370. [Google Scholar] [CrossRef] [PubMed]
  34. Baek, D.; Rokibuzzaman, M.; Khan, A.; Kim, M.C.; Park, H.J.; Yun, D.; Chung, Y.R. Plant-Growth Promoting Bacillus Oryzicola YC7007 Modulates Stress-Response Gene Expression and Provides Protection From Salt Stress. Front. Plant Sci. 2020, 10, 1646. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Chu, T.N.; Tran, B.T.H.; Van Bui, L.; Hoang, M.T.T. Plant Growth-Promoting Rhizobacterium Pseudomonas PS01 Induces Salt Tolerance in Arabidopsis thaliana. BMC Res. Notes 2019, 12, 11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Rabhi, N.E.H.; Silini, A.; Cherif-Silini, H.; Yahiaoui, B.; Lekired, A.; Robineau, M.; Esmaeel, Q.; Jacquard, C.; Vaillant-Gaveau, N.; Clément, C.; et al. Pseudomonas Knackmussii MLR6, a Rhizospheric Strain Isolated from Halophyte, Enhances Salt Tolerance in Arabidopsis thaliana. J. Appl. Microbiol. 2018, 125, 1836–1851. [Google Scholar] [CrossRef] [PubMed]
  37. Chen, L.; Liu, Y.; Wu, G.; Veronican Njeri, K.; Shen, Q.; Zhang, N.; Zhang, R. Induced Maize Salt Tolerance by Rhizosphere Inoculation of Bacillus Amyloliquefaciens SQR9. Physiol. Plant 2016, 158, 34–44. [Google Scholar] [CrossRef]
  38. Pinedo, I.; Ledger, T.; Greve, M.; Poupin, M.J. Burkholderia Phytofirmans PsJN Induces Long-Term Metabolic and Transcriptional Changes Involved in Arabidopsis thaliana Salt Tolerance. Front. Plant Sci. 2015, 6, 466. [Google Scholar] [CrossRef] [Green Version]
  39. Sukweenadhi, J.; Kim, Y.-J.; Choi, E.-S.; Koh, S.-C.; Lee, S.-W.; Kim, Y.-J.; Yang, D.C. Paenibacillus Yonginensis DCY84T Induces Changes in Arabidopsis thaliana Gene Expression against Aluminum, Drought, and Salt Stress. Microbiol. Res. 2015, 172, 7–15. [Google Scholar] [CrossRef]
  40. Kim, Y.-J.; Sukweenadhi, J.; Seok, J.W.; Kang, C.H.; Choi, E.-S.; Subramaniyam, S.; Yang, D.C. Complete Genome Sequence of Paenibacillus Yonginensis DCY84T, a Novel Plant Symbiont That Promotes Growth via Induced Systemic Resistance. Stand. Genom. Sci. 2017, 12, 63. [Google Scholar] [CrossRef] [Green Version]
  41. Kim, K.; Jang, Y.-J.; Lee, S.-M.; Oh, B.-T.; Chae, J.-C.; Lee, K.-J. Alleviation of Salt Stress by Enterobacter Sp. EJ01 in Tomato and Arabidopsis Is Accompanied by Up-Regulation of Conserved Salinity Responsive Factors in Plants. Mol. Cells 2014, 37, 109–117. [Google Scholar] [CrossRef]
  42. Qurashi, A.W.; Sabri, A.N. Bacterial Exopolysaccharide and Biofilm Formation Stimulate Chickpea Growth and Soil Aggregation under Salt Stress. Braz. J. Microbiol. 2012, 43, 1183–1191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  43. Khan, M.A.; Asaf, S.; Khan, A.L.; Jan, R.; Kang, S.-M.; Kim, K.-M.; Lee, I.-J. Rhizobacteria AK1 Remediates the Toxic Effects of Salinity Stress via Regulation of Endogenous Phytohormones and Gene Expression in Soybean. Biochem. J. 2019, 476, 2393–2409. [Google Scholar] [CrossRef]
  44. Khan, M.A.; Asaf, S.; Khan, A.L.; Adhikari, A.; Jan, R.; Ali, S.; Imran, M.; Kim, K.-M.; Lee, I.-J. Halotolerant Rhizobacterial Strains Mitigate the Adverse Effects of NaCl Stress in Soybean Seedlings. Biomed. Res. Int. 2019, 2019, 9530963. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Vaishnav, A.; Kumari, S.; Jain, S.; Varma, A.; Tuteja, N.; Choudhary, D.K. PGPR-Mediated Expression of Salt Tolerance Gene in Soybean through Volatiles under Sodium Nitroprusside: PGPR-Mediated Amelioration of Soybean under Salt Stress. J. Basic Microbiol. 2016, 56, 1274–1288. [Google Scholar] [CrossRef] [PubMed]
  46. Vaishnav, A.; Kumari, S.; Jain, S.; Varma, A.; Choudhary, D.K. Putative Bacterial Volatile-Mediated Growth in Soybean (Glycine max L. Merrill) and Expression of Induced Proteins under Salt Stress. J. Appl. Microbiol. 2015, 119, 539–551. [Google Scholar] [CrossRef]
  47. Ma, Y.; Rajkumar, M.; Oliveira, R.S.; Zhang, C.; Freitas, H. Potential of Plant Beneficial Bacteria and Arbuscular Mycorrhizal Fungi in Phytoremediation of Metal-Contaminated Saline Soils. J. Hazard. Mater. 2019, 379, 120813. [Google Scholar] [CrossRef]
  48. Kiani, M.Z.; Ali, A.; Sultan, T.; Ahmad, R.; Hydar, S.I. Plant Growth Promoting Rhizobacteria Having 1-Aminocyclopropane-1-Carboxylic Acid Deaminase to Induce Salt Tolerance in Sunflower (Helianthus annus L.). Nat. Resour. 2015, 6, 391–397. [Google Scholar] [CrossRef] [Green Version]
  49. Mahmoud, M.B.; Hidri, R.; Talbi-Zribi, O.; Taamalli, W.; Abdelly, C.; Djébali, N. Auxin and Proline Producing Rhizobacteria Mitigate Salt-Induced Growth Inhibition of Barley Plants by Enhancing Water and Nutrient Status. S. Afr. J. Bot. 2020, 128, 209–217. [Google Scholar] [CrossRef]
  50. Sultana, S.; Paul, S.C.; Parveen, S.; Alam, S.; Rahman, N.; Jannat, B.; Hoque, S.; Rahman, M.T.; Karim, M.M. Isolation and Identification of Salt-Tolerant Plant-Growth-Promoting Rhizobacteria and Their Application for Rice Cultivation under Salt Stress. Can. J. Microbiol. 2020, 66, 144–160. [Google Scholar] [CrossRef]
  51. Chauhan, P.S.; Lata, C.; Tiwari, S.; Chauhan, A.S.; Mishra, S.K.; Agrawal, L.; Chakrabarty, D.; Nautiyal, C.S. Transcriptional Alterations Reveal Bacillus Amyloliquefaciens-Rice Cooperation under Salt Stress. Sci. Rep. 2019, 9, 11912. [Google Scholar] [CrossRef] [Green Version]
  52. Nghia, N.K.; Tien, T.T.M.; Oanh, N.T.K.; Nuong, N.H.K. Isolation and Characterization of Indole Acetic Acid Producing Halophilic Bacteria from Salt Affected Soil of Rice–Shrimp Farming System in the Mekong Delta, Vietnam. Agric. For. Fish. 2017, 6, 69. [Google Scholar] [CrossRef] [Green Version]
  53. Jha, Y.; Subramanian, R.B.; Patel, S. Combination of Endophytic and Rhizospheric Plant Growth Promoting Rhizobacteria in Oryza Sativa Shows Higher Accumulation of Osmoprotectant against Saline Stress. Acta Physiol. Plant 2011, 33, 797–802. [Google Scholar] [CrossRef]
  54. Niu, S.-Q.; Li, H.-R.; Paré, P.W.; Aziz, M.; Wang, S.-M.; Shi, H.; Li, J.; Han, Q.-Q.; Guo, S.-Q.; Li, J.; et al. Induced Growth Promotion and Higher Salt Tolerance in the Halophyte Grass Puccinellia Tenuiflora by Beneficial Rhizobacteria. Plant Soil 2016, 407, 217–230. [Google Scholar] [CrossRef]
  55. Kang, S.-M.; Shahzad, R.; Bilal, S.; Khan, A.L.; Park, Y.-G.; Lee, K.-E.; Asaf, S.; Khan, M.A.; Lee, I.-J. Indole-3-Acetic-Acid and ACC Deaminase Producing Leclercia Adecarboxylata MO1 Improves Solanum lycopersicum L. Growth and Salinity Stress Tolerance by Endogenous Secondary Metabolites Regulation. BMC Microbiol. 2019, 19, 80. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Vaishnav, A.; Singh, J.; Singh, P.; Rajput, R.S.; Singh, H.B.; Sarma, B.K. Sphingobacterium Sp. BHU-AV3 Induces Salt Tolerance in Tomato by Enhancing Antioxidant Activities and Energy Metabolism. Front. Microbiol. 2020, 11, 443. [Google Scholar] [CrossRef]
  57. Yan, J.; Smith, M.D.; Glick, B.R.; Liang, Y. Effects of ACC Deaminase Containing Rhizobacteria on Plant Growth and Expression of Toc GTPases in Tomato (Solanum lycopersicum) under Salt Stress. Botany 2014, 92, 775–781. [Google Scholar] [CrossRef]
  58. Han, Q.-Q.; Lü, X.-P.; Bai, J.-P.; Qiao, Y.; Paré, P.W.; Wang, S.-M.; Zhang, J.-L.; Wu, Y.-N.; Pang, X.-P.; Xu, W.-B.; et al. Beneficial Soil Bacterium Bacillus Subtilis (GB03) Augments Salt Tolerance of White Clover. Front. Plant Sci. 2014, 5, 525. [Google Scholar] [CrossRef]
  59. Shah, D.; Khan, M.S.; Aziz, S.; Ali, H.; Pecoraro, L. Molecular and Biochemical Characterization, Antimicrobial Activity, Stress Tolerance, and Plant Growth-Promoting Effect of Endophytic Bacteria Isolated from Wheat Varieties. Microorganisms 2021, 10, 21. [Google Scholar] [CrossRef]
  60. Vaishnav, A.; Kumar, R.; Singh, H.B.; Sarma, B.K. Extending the Benefits of PGPR to Bioremediation of Nitrile Pollution in Crop Lands for Enhancing Crop Productivity. Sci. Total Environ. 2022, 826, 154170. [Google Scholar] [CrossRef] [PubMed]
  61. Safdarian, M.; Askari, H.; Shariati, J.V.; Nematzadeh, G. Transcriptional Responses of Wheat Roots Inoculated with Arthrobacter Nitroguajacolicus to Salt Stress. Sci. Rep. 2019, 9, 1792. [Google Scholar] [CrossRef]
  62. Singh, R.P.; Jha, P.N. The Multifarious PGPR Serratia Marcescens CDP-13 Augments Induced Systemic Resistance and Enhanced Salinity Tolerance of Wheat (Triticum aestivum L.). PLoS ONE 2016, 11, e0155026. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Pirhadi, M.; Enayatizamir, N.; Motamedi, H.; Sorkheh, K. Screening of Salt Tolerant Sugarcane Endophytic Bacteria with Potassium and Zinc for Their Solubilizing and Antifungal Activity. Biosci. Biotech. Res. Comm. 2016, 9, 530–538. [Google Scholar] [CrossRef]
  64. Ramadoss, D.; Lakkineni, V.K.; Bose, P.; Ali, S.; Annapurna, K. Mitigation of Salt Stress in Wheat Seedlings by Halotolerant Bacteria Isolated from Saline Habitats. Springerplus 2013, 2, 6. [Google Scholar] [CrossRef] [Green Version]
  65. El-Esawi, M.A.; Alaraidh, I.A.; Alsahli, A.A.; Alzahrani, S.M.; Ali, H.M.; Alayafi, A.A.; Ahmad, M. Serratia Liquefaciens KM4 Improves Salt Stress Tolerance in Maize by Regulating Redox Potential, Ion Homeostasis, Leaf Gas Exchange and Stress-Related Gene Expression. Int. J. Mol. Sci. 2018, 19, 3310. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  66. Alla, M.M.N.; Hassan, N.M. A Possible Role for C4 Photosynthetic Enzymes in Tolerance of Zea mays to NaCl. Protoplasma 2012, 249, 1109–1117. [Google Scholar] [CrossRef] [PubMed]
  67. Habib, S.H.; Kausar, H.; Saud, H.M. Plant Growth-Promoting Rhizobacteria Enhance Salinity Stress Tolerance in Okra through ROS-Scavenging Enzymes. Biomed. Res. Int. 2016, 2016, 6284547. [Google Scholar] [CrossRef] [Green Version]
  68. Etesami, H.; Beattie, G.A. Mining Halophytes for Plant Growth-Promoting Halotolerant Bacteria to Enhance the Salinity Tolerance of Non-Halophytic Crops. Front. Microbiol. 2018, 9, 148. [Google Scholar] [CrossRef] [Green Version]
  69. Xin, C.-S.; Dong, H.-Z.; Luo, Z.; Tang, W.; Zhang, D.-M.; Li, W.-J.; Kong, X.-Q. Effects of N, P, and K Fertilizer Application on Cotton Growing in Saline Soil in Yellow River Delta. Acta Agron. Sin. 2010, 36, 1698–1706. [Google Scholar] [CrossRef]
  70. Thomine, S.; Lanquar, V. Iron Transport and Signaling in Plants. In Transporters and Pumps in Plant Signaling; Geisler, M., Venema, K., Eds.; Signaling and Communication in Plants; Springer: Berlin/Heidelberg, Germany, 2011; pp. 99–131. ISBN 978-3-642-14369-4. [Google Scholar]
  71. Fageria, N.; Gheyi, H.; Moreira, A. Nutrient Bioavailability in Salt Affected Soils. J. Plant Nutr. 2011, 34, 945–962. [Google Scholar] [CrossRef]
  72. Sharma, S.; Kulkarni, J.; Jha, B. Halotolerant Rhizobacteria Promote Growth and Enhance Salinity Tolerance in Peanut. Front. Microbiol. 2016, 7, 1600. [Google Scholar] [CrossRef] [Green Version]
  73. Teo, H.M.; Bhubalan, K.; Ci, M.S.; Ng, L.C. Setting a Plausible Route for Saline Soil-Based Crop Cultivations by Application of Beneficial Halophyte-Associated Bacteria: A Review. Microorganisms 2022, 10, 657. [Google Scholar] [CrossRef] [PubMed]
  74. Raymond, J.; Siefert, J.L.; Staples, C.R.; Blankenship, R.E. The Natural History of Nitrogen Fixation. Mol. Biol. Evol. 2004, 21, 541–554. [Google Scholar] [CrossRef] [PubMed]
  75. Hachiya, T.; Sakakibara, H. Interactions between Nitrate and Ammonium in Their Uptake, Allocation, Assimilation, and Signaling in Plants. J. Exp. Bot. 2017, 68, 2501–2512. [Google Scholar] [CrossRef] [PubMed]
  76. Parmar, P.; Sindhu, S.S. Potassium Solubilization by Rhizosphere Bacteria: Influence of Nutritional and Environmental Conditions. J. Microbiol. Res. 2013, 3, 25–31. [Google Scholar] [CrossRef]
  77. Yan, N.; Marschner, P.; Cao, W.; Zuo, C.; Qin, W. Influence of Salinity and Water Content on Soil Microorganisms. Int. Soil Water Conserv. Res. 2015, 3, 316–323. [Google Scholar] [CrossRef] [Green Version]
  78. Richardson, A.E.; Hocking, P.J.; Simpson, R.J.; George, T.S.; Richardson, A.E.; Hocking, P.J.; Simpson, R.J.; George, T.S. Plant Mechanisms to Optimise Access to Soil Phosphorus. Crop Pasture Sci. 2009, 60, 124–143. [Google Scholar] [CrossRef]
  79. Mukherjee, S.; Sen, S.K. Exploration of Novel Rhizospheric Yeast Isolate as Fertilizing Soil Inoculant for Improvement of Maize Cultivation. J. Sci. Food Agric. 2015, 95, 1491–1499. [Google Scholar] [CrossRef]
  80. Nutaratat, P.; Srisuk, N.; Arunrattiyakorn, P.; Limtong, S. Plant Growth-Promoting Traits of Epiphytic and Endophytic Yeasts Isolated from Rice and Sugar Cane Leaves in Thailand. Fungal Biol. 2014, 118, 683–694. [Google Scholar] [CrossRef]
  81. Fernandez-San Millan, A.; Farran, I.; Larraya, L.; Ancin, M.; Arregui, L.M.; Veramendi, J. Plant Growth-Promoting Traits of Yeasts Isolated from Spanish Vineyards: Benefits for Seedling Development. Microbiol. Res. 2020, 237, 126480. [Google Scholar] [CrossRef]
  82. Riggs, P.J.; Chelius, M.K.; Iniguez, A.L.; Kaeppler, S.M.; Triplett, E.W. Enhanced Maize Productivity by Inoculation with Diazotrophic Bacteria. Funct. Plant Biol. 2001, 28, 829–836. [Google Scholar] [CrossRef]
  83. Tairo, E.V.; Ndakidemi, P.A. Possible Benefits of Rhizobial Inoculation and Phosphorus Supplementation on Nutrition, Growth and Economic Sustainability in Grain Legumes. Am. J. Res. Commun. 2013, 1, 532–556. [Google Scholar]
  84. Oberson, A.; Frossard, E.; Bühlmann, C.; Mayer, J.; Mäder, P.; Lüscher, A. Nitrogen Fixation and Transfer in Grass-Clover Leys under Organic and Conventional Cropping Systems. Plant Soil 2013, 371, 237–255. [Google Scholar] [CrossRef] [Green Version]
  85. Kolodiazhnyi, O.I. Phosphorus Compounds of Natural Origin: Prebiotic, Stereochemistry, Application. Symmetry 2021, 13, 889. [Google Scholar] [CrossRef]
  86. Etesami, H.; Maheshwari, D.K. Use of Plant Growth Promoting Rhizobacteria (PGPRs) with Multiple Plant Growth Promoting Traits in Stress Agriculture: Action Mechanisms and Future Prospects. Ecotoxicol. Environ. Saf. 2018, 156, 225–246. [Google Scholar] [CrossRef] [PubMed]
  87. Etesami, H. Enhanced Phosphorus Fertilizer Use Efficiency with Microorganisms. In Nutrient Dynamics for Sustainable Crop Production; Meena, R.S., Ed.; Springer: Singapore, 2020; pp. 215–245. ISBN 9789811386602. [Google Scholar]
  88. Timofeeva, A.; Galyamova, M.; Sedykh, S. Prospects for Using Phosphate-Solubilizing Microorganisms as Natural Fertilizers in Agriculture. Plants 2022, 11, 2119. [Google Scholar] [CrossRef] [PubMed]
  89. Goswami, D.; Pithwa, S.; Dhandhukia, P.; Thakker, J.N. Delineating Kocuria Turfanensis 2M4 as a Credible PGPR: A Novel IAA-Producing Bacteria Isolated from Saline Desert. J. Plant Interact. 2014, 9, 566–576. [Google Scholar] [CrossRef]
  90. Haas, D.; Défago, G. Biological Control of Soil-Borne Pathogens by Fluorescent Pseudomonads. Nat. Rev. Microbiol. 2005, 3, 307–319. [Google Scholar] [CrossRef]
  91. Saha, M.; Sarkar, S.; Sarkar, B.; Sharma, B.K.; Bhattacharjee, S.; Tribedi, P. Microbial Siderophores and Their Potential Applications: A Review. Environ. Sci. Pollut. Res. Int. 2016, 23, 3984–3999. [Google Scholar] [CrossRef]
  92. Rajkumar, M.; Ae, N.; Prasad, M.N.V.; Freitas, H. Potential of Siderophore-Producing Bacteria for Improving Heavy Metal Phytoextraction. Trends Biotechnol. 2010, 28, 142–149. [Google Scholar] [CrossRef]
  93. Latour, X.; Delorme, S.; Mirleau, P.; Lemanceau, P. Identification of Traits Implicated in the Rhizosphere Competence of Fluorescent Pseudomonads: Description of a Strategy Based on Population and Model Strain Studies. Agronomie 2003, 23, 397–405. [Google Scholar] [CrossRef]
  94. Gong, Q.; Li, Z.; Wang, L.; Dai, T.; Kang, Q.; Niu, D. Exogenous of Indole-3-Acetic Acid Application Alleviates Copper Toxicity in Spinach Seedlings by Enhancing Antioxidant Systems and Nitrogen Metabolism. Toxics 2019, 8, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  95. Gao, Y.; Zou, H.; Wang, B.; Yuan, F. Progress and Applications of Plant Growth-Promoting Bacteria in Salt Tolerance of Crops. Int. J. Mol. Sci. 2022, 23, 7036. [Google Scholar] [CrossRef] [PubMed]
  96. Jha, C.K.; Saraf, M. Plant Growth Promoting Rhizobacteria (PGPR): A Review. J. Agric. Res. Dev. 2015, 5, 108–119. [Google Scholar] [CrossRef]
  97. Ahmad, F.; Ahmad, I.; Khan, M. Indole Acetic Acid Production by the Indigenous Isolates of Azotobacter and Fluorescent Pseudomonas in the Presence and Absence of Tryptophan. Turk. J. Biol. 2005, 29, 29–34. [Google Scholar]
  98. Spaepen, S.; Vanderleyden, J.; Remans, R. Indole-3-Acetic Acid in Microbial and Microorganism-Plant Signaling. FEMS Microbiol. Rev. 2007, 31, 425–448. [Google Scholar] [CrossRef] [Green Version]
  99. Mohite, B. Isolation and Characterization of Indole Acetic Acid (IAA) Producing Bacteria from Rhizospheric Soil and Its Effect on Plant Growth. J. Soil Sci. Plant Nutr. 2013, 13, 638–649. [Google Scholar] [CrossRef]
  100. Defez, R.; Andreozzi, A.; Romano, S.; Pocsfalvi, G.; Fiume, I.; Esposito, R.; Angelini, C.; Bianco, C. Bacterial IAA-Delivery into Medicago Root Nodules Triggers a Balanced Stimulation of C and N Metabolism Leading to a Biomass Increase. Microorganisms 2019, 7, 403. [Google Scholar] [CrossRef] [Green Version]
  101. Albacete, A.; Ghanem, M.E.; Martínez-Andújar, C.; Acosta, M.; Sánchez-Bravo, J.; Martínez, V.; Lutts, S.; Dodd, I.C.; Pérez-Alfocea, F. Hormonal Changes in Relation to Biomass Partitioning and Shoot Growth Impairment in Salinized Tomato (Solanum lycopersicum L.) Plants. J. Exp. Bot. 2008, 59, 4119–4131. [Google Scholar] [CrossRef]
  102. Ramos Solano, B.; Barriuso, J.; Gutiérrez Mañero, F.J. Physiological and Molecular Mechanisms of Plant Growth Promoting Rhizobacteria (PGPR). In Plant-Bacteria Interactions; John Wiley & Sons, Ltd.: New York, NY, USA, 2008; pp. 41–54. ISBN 978-3-527-62198-9. [Google Scholar]
  103. Etesami, H.; Alikhani, H.A. Co-Inoculation with Endophytic and Rhizosphere Bacteria Allows Reduced Application Rates of N-Fertilizer for Rice Plant. Rhizosphere 2016, 2, 5–12. [Google Scholar] [CrossRef]
  104. Kerbab, S.; Silini, A.; Chenari Bouket, A.; Cherif-Silini, H.; Eshelli, M.; El Houda Rabhi, N.; Belbahri, L. Mitigation of NaCl Stress in Wheat by Rhizosphere Engineering Using Salt Habitat Adapted PGPR Halotolerant Bacteria. Appl. Sci. 2021, 11, 1034. [Google Scholar] [CrossRef]
  105. Amini Hajiabadi, A.; Mosleh Arani, A.; Ghasemi, S.; Rad, M.H.; Etesami, H.; Shabazi Manshadi, S.; Dolati, A. Mining the Rhizosphere of Halophytic Rangeland Plants for Halotolerant Bacteria to Improve Growth and Yield of Salinity-Stressed Wheat. Plant Physiol. Biochem. 2021, 163, 139–153. [Google Scholar] [CrossRef]
  106. Pliego, C.; Cazorla, F.M.; González-Sánchez, M.A.; Pérez-Jiménez, R.M.; de Vicente, A.; Ramos, C. Selection for Biocontrol Bacteria Antagonistic toward Rosellinia Necatrix by Enrichment of Competitive Avocado Root Tip Colonizers. Res. Microbiol. 2007, 158, 463–470. [Google Scholar] [CrossRef] [PubMed]
  107. Fatima, T.; Arora, N.K. Pseudomonas Entomophila PE3 and Its Exopolysaccharides as Biostimulants for Enhancing Growth, Yield and Tolerance Responses of Sunflower under Saline Conditions. Microbiol. Res. 2021, 244, 126671. [Google Scholar] [CrossRef]
  108. Li, M.; Guo, R.; Yu, F.; Chen, X.; Zhao, H.; Li, H.; Wu, J. Indole-3-Acetic Acid Biosynthesis Pathways in the Plant-Beneficial Bacterium Arthrobacter Pascens ZZ21. Int. J. Mol. Sci. 2018, 19, 443. [Google Scholar] [CrossRef] [PubMed]
  109. Ahemad, M.; Khan, M.S. Comparative Toxicity of Selected Insecticides to Pea Plants and Growth Promotion in Response to Insecticide-Tolerant and Plant Growth Promoting Rhizobium Leguminosarum. Crop Prot. 2010, 29, 325–329. [Google Scholar] [CrossRef]
  110. Yaish, M.W.; Antony, I.; Glick, B.R. Isolation and Characterization of Endophytic Plant Growth-Promoting Bacteria from Date Palm Tree (Phoenix dactylifera L.) and Their Potential Role in Salinity Tolerance. Antonie Leeuwenhoek Int. J. Gen. Mol. Microbiol. 2015, 107, 1519–1532. [Google Scholar] [CrossRef] [PubMed]
  111. Hernández-Rodríguez, A.; Heydrich-Pérez, M.; Acebo-Guerrero, Y.; Velazquez-del Valle, M.G.; Hernández-Lauzardo, A.N. Antagonistic Activity of Cuban Native Rhizobacteria against Fusarium verticillioides (Sacc.) Nirenb. in Maize (Zea mays L.). Appl. Soil Ecol. 2008, 39, 180–186. [Google Scholar] [CrossRef]
  112. Shaharoona, B.; Naveed, M.; Arshad, M.; Zahir, Z.A. Fertilizer-Dependent Efficiency of Pseudomonads for Improving Growth, Yield, and Nutrient Use Efficiency of Wheat (Triticum aestivum L.). Appl. Microbiol. Biotechnol. 2008, 79, 147–155. [Google Scholar] [CrossRef]
  113. Barbaccia, P.; Gaglio, R.; Dazzi, C.; Miceli, C.; Bella, P.; Lo Papa, G.; Settanni, L. Plant Growth-Promoting Activities of Bacteria Isolated from an Anthropogenic Soil Located in Agrigento Province. Microorganisms 2022, 10, 2167. [Google Scholar] [CrossRef]
  114. Wani, P.A.; Khan, M.S. Bacillus Species Enhance Growth Parameters of Chickpea (Cicer arietinum L.) in Chromium Stressed Soils. Food Chem. Toxicol. 2010, 48, 3262–3267. [Google Scholar] [CrossRef]
  115. Jin, T.; Ren, J.; Li, Y.; Bai, B.; Liu, R.; Wang, Y. Plant Growth-Promoting Effect and Genomic Analysis of the P. Putida LWPZF Isolated from C. Japonicum Rhizosphere. AMB Express 2022, 12, 101. [Google Scholar] [CrossRef] [PubMed]
  116. Bhattacharyya, P.N.; Jha, D.K. Plant Growth-Promoting Rhizobacteria (PGPR): Emergence in Agriculture. World J. Microbiol. Biotechnol. 2012, 28, 1327–1350. [Google Scholar] [CrossRef] [PubMed]
  117. Seleiman, M.F.; Al-Suhaibani, N.; Ali, N.; Akmal, M.; Alotaibi, M.; Refay, Y.; Dindaroglu, T.; Abdul-Wajid, H.H.; Battaglia, M.L. Drought Stress Impacts on Plants and Different Approaches to Alleviate Its Adverse Effects. Plants 2021, 10, 259. [Google Scholar] [CrossRef] [PubMed]
  118. Wang, X.; Komatsu, S. The Role of Phytohormones in Plant Response to Flooding. Int. J. Mol. Sci. 2022, 23, 6383. [Google Scholar] [CrossRef]
  119. Glick, B.R. Bacteria with ACC Deaminase Can Promote Plant Growth and Help to Feed the World. Microbiol. Res. 2014, 169, 30–39. [Google Scholar] [CrossRef]
  120. Glick, B.R.; Cheng, Z.; Czarny, J.; Duan, J. Promotion of Plant Growth by ACC Deaminase-Producing Soil Bacteria. Eur. J. Plant Pathol. 2007, 119, 329–339. [Google Scholar] [CrossRef]
  121. Iqbal, N.; Khan, N.A.; Ferrante, A.; Trivellini, A.; Francini, A.; Khan, M.I.R. Ethylene Role in Plant Growth, Development and Senescence: Interaction with Other Phytohormones. Front. Plant Sci. 2017, 8, 475. [Google Scholar] [CrossRef] [Green Version]
  122. Riyazuddin, R.; Verma, R.; Singh, K.; Nisha, N.; Keisham, M.; Bhati, K.K.; Kim, S.T.; Gupta, R. Ethylene: A Master Regulator of Salinity Stress Tolerance in Plants. Biomolecules 2020, 10, 959. [Google Scholar] [CrossRef]
  123. Carmen, B.; Roberto, D. Soil Bacteria Support and Protect Plants Against Abiotic Stresses; IntechOpen: Rijeka, Croatia, 2011; ISBN 978-953-307-394-1. [Google Scholar]
  124. Pérez-López, U.; Robredo, A.; Lacuesta, M.; Mena-Petite, A.; Muñoz-Rueda, A. Elevated CO2 Reduces Stomatal and Metabolic Limitations on Photosynthesis Caused by Salinity in Hordeum Vulgare. Photosynth. Res. 2012, 111, 269–283. [Google Scholar] [CrossRef]
  125. Munns, R. Comparative Physiology of Salt and Water Stress. Plant Cell Environ. 2002, 25, 239–250. [Google Scholar] [CrossRef] [Green Version]
  126. Dodd, I.C.; Pérez-Alfocea, F. Microbial Amelioration of Crop Salinity Stress. J. Exp. Bot. 2012, 63, 3415–3428. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  127. Paul, D.; Lade, H. Plant-Growth-Promoting Rhizobacteria to Improve Crop Growth in Saline Soils: A Review. Agron. Sustain. Dev. 2014, 34, 737–752. [Google Scholar] [CrossRef]
  128. Morillon, R.; Chrispeels, M.J. The Role of ABA and the Transpiration Stream in the Regulation of the Osmotic Water Permeability of Leaf Cells. Proc. Natl. Acad. Sci. USA 2001, 98, 14138–14143. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  129. Sleator, R.D.; Hill, C. Bacterial Osmoadaptation: The Role of Osmolytes in Bacterial Stress and Virulence. FEMS Microbiol. Rev. 2002, 26, 49–71. [Google Scholar] [CrossRef] [PubMed]
  130. Nawaz, A.; Shahbaz, M.; Asadullah; Imran, A.; Marghoob, M.U.; Imtiaz, M.; Mubeen, F. Potential of Salt Tolerant PGPR in Growth and Yield Augmentation of Wheat (Triticum aestivum L.) Under Saline Conditions. Front. Microbiol. 2020, 11, 2019. [Google Scholar] [CrossRef] [PubMed]
  131. Kaur, G.; Asthir, B. Proline: A Key Player in Plant Abiotic Stress Tolerance. Biol. Plant 2015, 59, 609–619. [Google Scholar] [CrossRef]
  132. Krasensky, J.; Jonak, C. Drought, Salt, and Temperature Stress-Induced Metabolic Rearrangements and Regulatory Networks. J. Exp. Bot. 2012, 63, 1593–1608. [Google Scholar] [CrossRef] [Green Version]
  133. Kunst, F.; Ogasawara, N.; Moszer, I.; Albertini, A.M.; Alloni, G.; Azevedo, V.; Bertero, M.G.; Bessières, P.; Bolotin, A.; Borchert, S.; et al. The Complete Genome Sequence of the Gram-Positive Bacterium Bacillus Subtilis. Nature 1997, 390, 249–256. [Google Scholar] [CrossRef] [Green Version]
  134. Meena, M.; Divyanshu, K.; Kumar, S.; Swapnil, P.; Zehra, A.; Shukla, V.; Yadav, M.; Upadhyay, R.S. Regulation of L-Proline Biosynthesis, Signal Transduction, Transport, Accumulation and Its Vital Role in Plants during Variable Environmental Conditions. Heliyon 2019, 5, e02952. [Google Scholar] [CrossRef] [Green Version]
  135. Kohl, D.H.; Straub, P.F.; Shearer, G. Does Proline Play a Special Role in Bacteroid Metabolism? Plant Cell Environ. 1994, 17, 1257–1262. [Google Scholar] [CrossRef]
  136. Yasin, N.A.; Akram, W.; Khan, W.U.; Ahmad, S.R.; Ahmad, A.; Ali, A. Halotolerant Plant-Growth Promoting Rhizobacteria Modulate Gene Expression and Osmolyte Production to Improve Salinity Tolerance and Growth in Capsicum annum L. Environ. Sci. Pollut. Res. Int. 2018, 25, 23236–23250. [Google Scholar] [CrossRef] [PubMed]
  137. Sukweenadhi, J.; Balusamy, S.R.; Kim, Y.-J.; Lee, C.H.; Kim, Y.-J.; Koh, S.C.; Yang, D.C. A Growth-Promoting Bacteria, Paenibacillus Yonginensis DCY84T Enhanced Salt Stress Tolerance by Activating Defense-Related Systems in Panax Ginseng. Front. Plant Sci. 2018, 9, 813. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  138. Wutipraditkul, N.; Wongwean, P.; Buaboocha, T. Alleviation of Salt-Induced Oxidative Stress in Rice Seedlings by Proline and/or Glycinebetaine. Biol. Plant 2015, 59, 547–553. [Google Scholar] [CrossRef]
  139. Hoque, M.A.; Banu, M.N.A.; Okuma, E.; Amako, K.; Nakamura, Y.; Shimoishi, Y.; Murata, Y. Exogenous Proline and Glycinebetaine Increase NaCl-Induced Ascorbate-Glutathione Cycle Enzyme Activities, and Proline Improves Salt Tolerance More than Glycinebetaine in Tobacco Bright Yellow-2 Suspension-Cultured Cells. J. Plant Physiol. 2007, 164, 1457–1468. [Google Scholar] [CrossRef] [PubMed]
  140. Malekzadeh, P. Influence of Exogenous Application of Glycinebetaine on Antioxidative System and Growth of Salt-Stressed Soybean Seedlings (Glycine max L.). Physiol. Mol. Biol. Plants 2015, 21, 225–232. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  141. Kappes, R.M.; Kempf, B.; Kneip, S.; Boch, J.; Gade, J.; Meier-Wagner, J.; Bremer, E. Two Evolutionarily Closely Related ABC Transporters Mediate the Uptake of Choline for Synthesis of the Osmoprotectant Glycine Betaine in Bacillus Subtilis. Mol. Microbiol. 1999, 32, 203–216. [Google Scholar] [CrossRef]
  142. Salazar, B.; Ortiz, A.; Keswani, C.; Minkina, T.; Mandzhieva, S.; Pratap Singh, S.; Rekadwad, B.; Borriss, R.; Jain, A.; Singh, H.B.; et al. Bacillus spp. as Bio-Factories for Antifungal Secondary Metabolites: Innovation Beyond Whole Organism Formulations. Microb. Ecol. 2022. [Google Scholar] [CrossRef]
  143. Giri, J. Glycinebetaine and Abiotic Stress Tolerance in Plants. Plant Signal. Behav. 2011, 6, 1746–1751. [Google Scholar] [CrossRef]
  144. Mukhtar, S.; Zareen, M.; Khaliq, Z.; Mehnaz, S.; Malik, K.A. Phylogenetic Analysis of Halophyte-Associated Rhizobacteria and Effect of Halotolerant and Halophilic Phosphate-Solubilizing Biofertilizers on Maize Growth under Salinity Stress Conditions. J. Appl. Microbiol. 2020, 128, 556–573. [Google Scholar] [CrossRef]
  145. Hashem, A.; Abd_Allah, E.F.; Alqarawi, A.A.; Al-Huqail, A.A.; Shah, M.A. Induction of Osmoregulation and Modulation of Salt Stress in Acacia Gerrardii Benth. by Arbuscular Mycorrhizal Fungi and Bacillus Subtilis (BERA 71). Biomed. Res. Int. 2016, 2016, 6294098. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  146. Masouleh, S.S.S.; Aldine, N.J.; Sassine, Y.N. The Role of Organic Solutes in the Osmotic Adjustment of Chilling-Stressed Plants (Vegetable, Ornamental and Crop Plants). Ornam. Hortic. 2020, 25, 434–442. [Google Scholar] [CrossRef]
  147. Moghaieb, R.E.A.; Tanaka, N.; Saneoka, H.; Murooka, Y.; Ono, H.; Morikawa, H.; Nakamura, A.; Nguyen, N.T.; Suwa, R.; Fujita, K. Characterization of Salt Tolerance in Ectoine-Transformed Tobacco Plants (Nicotiana tabaccum): Photosynthesis, Osmotic Adjustment, and Nitrogen Partitioning. Plant Cell Environ. 2006, 29, 173–182. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  148. Grammann, K.; Volke, A.; Kunte, H.J. New Type of Osmoregulated Solute Transporter Identified in Halophilic Members of the Bacteria Domain: TRAP Transporter TeaABC Mediates Uptake of Ectoine and Hydroxyectoine in Halomonas Elongata DSM 2581T. J. Bacteriol. 2002, 184, 3078–3085. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  149. Elsakhawy, T.A.; Nashwa, A.H.F.; Ghazi, A.A. The Potential Use of Ectoine Produced by a Moderately Halophilic Bacteria Chromohalobacter Salexigens KT989776 for Enhancing Germination and Primary Seedling of Flax “Linum usitatissimum L.” under Salinity Conditions. Biotechnol. J. Int. 2019, 23, 1–12. [Google Scholar] [CrossRef]
  150. Chandra, G.; Chater, K.F.; Bornemann, S. Unexpected and Widespread Connections between Bacterial Glycogen and Trehalose Metabolism. Microbiology 2011, 157, 1565–1572. [Google Scholar] [CrossRef] [Green Version]
  151. Vílchez, J.I.; García-Fontana, C.; Román-Naranjo, D.; González-López, J.; Manzanera, M. Plant Drought Tolerance Enhancement by Trehalose Production of Desiccation-Tolerant Microorganisms. Front. Microbiol. 2016, 7, 1577. [Google Scholar] [CrossRef] [Green Version]
  152. Rodríguez-Salazar, J.; Suárez, R.; Caballero-Mellado, J.; Iturriaga, G. Trehalose Accumulation in Azospirillum Brasilense Improves Drought Tolerance and Biomass in Maize Plants. FEMS Microbiol. Lett. 2009, 296, 52–59. [Google Scholar] [CrossRef] [Green Version]
  153. Duan, J.; Müller, K.M.; Charles, T.C.; Vesely, S.; Glick, B.R. 1-Aminocyclopropane-1-Carboxylate (ACC) Deaminase Genes in Rhizobia from Southern Saskatchewan. Microb. Ecol. 2009, 57, 423–436. [Google Scholar] [CrossRef]
  154. Suárez, R.; Wong, A.; Ramírez, M.; Barraza, A.; Orozco, M.D.C.; Cevallos, M.A.; Lara, M.; Hernández, G.; Iturriaga, G. Improvement of Drought Tolerance and Grain Yield in Common Bean by Overexpressing Trehalose-6-Phosphate Synthase in Rhizobia. Mol. Plant Microbe Interact. 2008, 21, 958–966. [Google Scholar] [CrossRef] [Green Version]
  155. Flemming, H.C.; Wingender, J. Relevance of Microbial Extracellular Polymeric Substances (EPSs)--Part I: Structural and Ecological Aspects. Water Sci. Technol. 2001, 43, 1–8. [Google Scholar] [CrossRef]
  156. Liu, X.; Luo, Y.; Li, Z.; Wang, J.; Wei, G. Role of Exopolysaccharide in Salt Stress Resistance and Cell Motility of Mesorhizobium Alhagi CCNWXJ12-2T. Appl. Microbiol. Biotechnol. 2017, 101, 2967–2978. [Google Scholar] [CrossRef]
  157. Qin, Y.; Druzhinina, I.S.; Pan, X.; Yuan, Z. Microbially Mediated Plant Salt Tolerance and Microbiome-Based Solutions for Saline Agriculture. Biotechnol. Adv. 2016, 34, 1245–1259. [Google Scholar] [CrossRef] [PubMed]
  158. Ruppel, S.; Franken, P.; Witzel, K. Properties of the Halophyte Microbiome and Their Implications for Plant Salt Tolerance. Funct. Plant Biol. 2013, 40, 940–951. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  159. De Vuyst, L.; Degeest, B. Heteropolysaccharides from Lactic Acid Bacteria. FEMS Microbiol. Rev. 1999, 23, 153–177. [Google Scholar] [CrossRef] [PubMed]
  160. Kaushal, M.; Wani, S.P. Rhizobacterial-Plant Interactions: Strategies Ensuring Plant Growth Promotion under Drought and Salinity Stress. Agric. Ecosyst. Environ. 2016, 231, 68–78. [Google Scholar] [CrossRef]
  161. Meneses, C.; Gonçalves, T.; Alquéres, S.; Rouws, L.; Serrato, R.; Vidal, M.; Baldani, J.I. Gluconacetobacter Diazotrophicus Exopolysaccharide Protects Bacterial Cells against Oxidative Stress in Vitro and during Rice Plant Colonization. Plant Soil 2017, 416, 133–147. [Google Scholar] [CrossRef]
  162. Xiong, Y.-W.; Ju, X.-Y.; Li, X.-W.; Gong, Y.; Xu, M.-J.; Zhang, C.-M.; Yuan, B.; Lv, Z.-P.; Qin, S. Fermentation Conditions Optimization, Purification, and Antioxidant Activity of Exopolysaccharides Obtained from the Plant Growth-Promoting Endophytic Actinobacterium Glutamicibacter Halophytocola KLBMP 5180. Int. J. Biol. Macromol. 2020, 153, 1176–1185. [Google Scholar] [CrossRef]
  163. Gupta, G.; Parihar, S.; Ahirwar, N.; Snehi, S.K.; Singh, V. Plant Growth Promoting Rhizobacteria (PGPR): Current and Future Prospects for Development of Sustainable Agriculture. Microb. Biochem. Technol. 2015, 7, 096–102. [Google Scholar]
  164. Xiong, Y.-W.; Gong, Y.; Li, X.-W.; Chen, P.; Ju, X.-Y.; Zhang, C.-M.; Yuan, B.; Lv, Z.-P.; Xing, K.; Qin, S. Enhancement of Growth and Salt Tolerance of Tomato Seedlings by a Natural Halotolerant Actinobacterium Glutamicibacter Halophytocola KLBMP 5180 Isolated from a Coastal Halophyte. Plant Soil 2019, 445, 307–322. [Google Scholar] [CrossRef]
  165. Mishra, J.; Arora, N.K. Secondary Metabolites of Fluorescent Pseudomonads in Biocontrol of Phytopathogens for Sustainable Agriculture. Appl. Soil Ecol. 2018, 125, 35–45. [Google Scholar] [CrossRef]
  166. Tewari, S.; Arora, N.K. Role of Salicylic Acid from Pseudomonas Aeruginosa PF23EPS+ in Growth Promotion of Sunflower in Saline Soils Infested with Phytopathogen Macrophomina Phaseolina. Environ. Sustain. 2018, 1, 49–59. [Google Scholar] [CrossRef]
  167. Ashraf, M.; Hasnain, S.; Berge, O.; Mahmood, T. Inoculating Wheat Seedlings with Exopolysaccharide-Producing Bacteria Restricts Sodium Uptake and Stimulates Plant Growth under Salt Stress. Biol. Fertil. Soils 2004, 40, 157–162. [Google Scholar] [CrossRef]
  168. Mahmood, S.; Daur, I.; Al-Solaimani, S.G.; Ahmad, S.; Madkour, M.H.; Yasir, M.; Hirt, H.; Ali, S.; Ali, Z. Plant Growth Promoting Rhizobacteria and Silicon Synergistically Enhance Salinity Tolerance of Mung Bean. Front. Plant Sci. 2016, 7, 876. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  169. Sun, L.; Lei, P.; Wang, Q.; Ma, J.; Zhan, Y.; Jiang, K.; Xu, Z.; Xu, H. The Endophyte Pantoea Alhagi NX-11 Alleviates Salt Stress Damage to Rice Seedlings by Secreting Exopolysaccharides. Front. Microbiol. 2020, 10, 3112. [Google Scholar] [CrossRef] [PubMed]
  170. Rojas-Tapias, D.; Moreno-Galván, A.; Pardo-Díaz, S.; Obando, M.; Rivera, D.; Bonilla, R. Effect of Inoculation with Plant Growth-Promoting Bacteria (PGPB) on Amelioration of Saline Stress in Maize (Zea mays). Appl. Soil Ecol. 2012, 61, 264–272. [Google Scholar] [CrossRef]
  171. Fatima, T.; Mishra, I.; Verma, R.; Arora, N.K. Mechanisms of Halotolerant Plant Growth Promoting Alcaligenes Sp. Involved in Salt Tolerance and Enhancement of the Growth of Rice under Salinity Stress. 3 Biotech 2020, 10, 361. [Google Scholar] [CrossRef] [PubMed]
  172. Mhlongo, M.I.; Piater, L.A.; Dubery, I.A. Profiling of Volatile Organic Compounds from Four Plant Growth-Promoting Rhizobacteria by SPME–GC–MS: A Metabolomics Study. Metabolites 2022, 12, 763. [Google Scholar] [CrossRef]
  173. Vespermann, A.; Kai, M.; Piechulla, B. Rhizobacterial Volatiles Affect the Growth of Fungi and Arabidopsis thaliana. Appl. Environ. Microbiol. 2007, 73, 5639–5641. [Google Scholar] [CrossRef] [Green Version]
  174. Kanchiswamy, C.N.; Malnoy, M.; Maffei, M.E. Chemical Diversity of Microbial Volatiles and Their Potential for Plant Growth and Productivity. Front. Plant Sci. 2015, 6, 151. [Google Scholar] [CrossRef] [Green Version]
  175. Tirranen, L.S.; Gitelson, I.I. The Role of Volatile Metabolites in Microbial Communities of the LSS Higher Plant Link. Adv. Space Res. 2006, 38, 1227–1232. [Google Scholar] [CrossRef]
  176. Tahir, H.A.S.; Gu, Q.; Wu, H.; Raza, W.; Hanif, A.; Wu, L.; Colman, M.V.; Gao, X. Plant Growth Promotion by Volatile Organic Compounds Produced by Bacillus Subtilis SYST2. Front. Microbiol. 2017, 8, 171. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  177. Meldau, D.G.; Meldau, S.; Hoang, L.H.; Underberg, S.; Wünsche, H.; Baldwin, I.T. Dimethyl Disulfide Produced by the Naturally Associated Bacterium Bacillus Sp B55 Promotes Nicotiana Attenuata Growth by Enhancing Sulfur Nutrition. Plant Cell 2013, 25, 2731–2747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  178. Cho, S.M.; Kang, B.R.; Han, S.H.; Anderson, A.J.; Park, J.-Y.; Lee, Y.-H.; Cho, B.H.; Yang, K.-Y.; Ryu, C.-M.; Kim, Y.C. 2R,3R-Butanediol, a Bacterial Volatile Produced by Pseudomonas Chlororaphis O6, Is Involved in Induction of Systemic Tolerance to Drought in Arabidopsis thaliana. Mol. Plant Microbe Interact. 2008, 21, 1067–1075. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  179. Zhang, H.; Kim, M.-S.; Krishnamachari, V.; Payton, P.; Sun, Y.; Grimson, M.; Farag, M.A.; Ryu, C.-M.; Allen, R.; Melo, I.S.; et al. Rhizobacterial Volatile Emissions Regulate Auxin Homeostasis and Cell Expansion in Arabidopsis. Planta 2007, 226, 839–851. [Google Scholar] [CrossRef] [PubMed]
  180. Li, H.F.; Imai, T.; Ukita, M.; Sekine, M.; Higuchi, T. Compost Stability Assessment Using a Secondary Metabolite: Geosmin. Environ. Technol. 2004, 25, 1305–1312. [Google Scholar] [CrossRef] [PubMed]
  181. Gutiérrez-Luna, F.M.; López-Bucio, J.; Altamirano-Hernández, J.; Valencia-Cantero, E.; de la Cruz, H.R.; Macías-Rodríguez, L. Plant Growth-Promoting Rhizobacteria Modulate Root-System Architecture in Arabidopsis thaliana through Volatile Organic Compound Emission. Symbiosis 2010, 51, 75–83. [Google Scholar] [CrossRef]
  182. Cordovez, V.; Schop, S.; Hordijk, K.; Dupré de Boulois, H.; Coppens, F.; Hanssen, I.; Raaijmakers, J.M.; Carrión, V.J. Priming of Plant Growth Promotion by Volatiles of Root-Associated Microbacterium spp. Appl. Environ. Microbiol. 2018, 84, e01865-18. [Google Scholar] [CrossRef] [Green Version]
  183. Ledger, T.; Rojas, S.; Timmermann, T.; Pinedo, I.; Poupin, M.J.; Garrido, T.; Richter, P.; Tamayo, J.; Donoso, R. Volatile-Mediated Effects Predominate in Paraburkholderia Phytofirmans Growth Promotion and Salt Stress Tolerance of Arabidopsis thaliana. Front. Microbiol. 2016, 7, 1838. [Google Scholar] [CrossRef] [Green Version]
  184. Bhattacharyya, D.; Lee, Y.H. A Cocktail of Volatile Compounds Emitted from Alcaligenes Faecalis JBCS1294 Induces Salt Tolerance in Arabidopsis thaliana by Modulating Hormonal Pathways and Ion Transporters. J. Plant Physiol. 2017, 214, 64–73. [Google Scholar] [CrossRef] [PubMed]
  185. Meena, K.K.; Sorty, A.M.; Bitla, U.M.; Choudhary, K.; Gupta, P.; Pareek, A.; Singh, D.P.; Prabha, R.; Sahu, P.K.; Gupta, V.K.; et al. Abiotic Stress Responses and Microbe-Mediated Mitigation in Plants: The Omics Strategies. Front. Plant Sci. 2017, 8, 172. [Google Scholar] [CrossRef] [Green Version]
  186. Siebers, N.; Kruse, J. Short-Term Impacts of Forest Clear-Cut on Soil Structure and Consequences for Organic Matter Composition and Nutrient Speciation: A Case Study. PLoS ONE 2019, 14, e0220476. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  187. Rodriguez, P.A.; Rothballer, M.; Chowdhury, S.P.; Nussbaumer, T.; Gutjahr, C.; Falter-Braun, P. Systems Biology of Plant-Microbiome Interactions. Mol. Plant 2019, 12, 804–821. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  188. Arif, F.; Ghoul, M. Halotolerance of Indigenous Fluorescent Pseudomonads in the Presence of Natural Osmoprotectants. Annu. Res. Rev. Biol. 2018, 24, 1–11. [Google Scholar] [CrossRef]
  189. Ansari, F.A.; Ahmad, I.; Pichtel, J. Growth stimulation and alleviation of salinity stress to wheat by the biofilm forming Bacillus pumilus strain FAB10. Appl. Soil Ecol. 2019, 143, 45–54. [Google Scholar] [CrossRef]
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Figure 1. Effects of salinity stress and associated tolerance mechanisms induced by halotolerant plant growth-promoting rhizobacteria (HT-PGPR) in both plant roots and shoots.
Figure 1. Effects of salinity stress and associated tolerance mechanisms induced by halotolerant plant growth-promoting rhizobacteria (HT-PGPR) in both plant roots and shoots.
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Figure 2. Effect of HT-PGPR on plant growth and salinity tolerance in glycophytic plants. The plate shown includes potential HT-PGPR isolated from native halophytes and consists of rhizobacteria and endophytes. Beneficial effects are shown in blue boxes, the underlying processes in orange boxes, and benefits plants in the last column.
Figure 2. Effect of HT-PGPR on plant growth and salinity tolerance in glycophytic plants. The plate shown includes potential HT-PGPR isolated from native halophytes and consists of rhizobacteria and endophytes. Beneficial effects are shown in blue boxes, the underlying processes in orange boxes, and benefits plants in the last column.
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Figure 3. Model of osmoprotectants and compatible solutes produced by halotolerant plant growth-promoting rhizobacteria (HT-PGPR), their cellular locations, and functions.
Figure 3. Model of osmoprotectants and compatible solutes produced by halotolerant plant growth-promoting rhizobacteria (HT-PGPR), their cellular locations, and functions.
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Figure 4. Advantages of biofilm production by HT-PGPR in making saline soil suitable for crop production.
Figure 4. Advantages of biofilm production by HT-PGPR in making saline soil suitable for crop production.
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Figure 5. Benefits of HT-PGPR to alleviate salinity stress. The HT-PGPR improve crop productivity by improving organic acids; producing osmoprotectants, exopolysaccharides (EPS), and volatile organic compounds (VOCs); and remediating saline soils.
Figure 5. Benefits of HT-PGPR to alleviate salinity stress. The HT-PGPR improve crop productivity by improving organic acids; producing osmoprotectants, exopolysaccharides (EPS), and volatile organic compounds (VOCs); and remediating saline soils.
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Table
Table 1. Effects of inoculating plant species with various halotolerant plant growth-promoting rhizobacteria (HT-PGPR) species. Table summarises genes involved, mechanisms to increase salt tolerance, and actual effects observed in different plants.
Table 1. Effects of inoculating plant species with various halotolerant plant growth-promoting rhizobacteria (HT-PGPR) species. Table summarises genes involved, mechanisms to increase salt tolerance, and actual effects observed in different plants.
Plant
Species		HT-PGPR
Species		Gene/s
Involved		Mechanism to Mitigate StressEffect ObservedReferences
Arabidopsis thaliana L.Bacillus oryzicola YC7007RD22, KIN1, RD29B, RD20, RD22, and ERD1Stem and the root of the seedlings released stress-related genesEnhanced plant tolerance to salt stress[35]
Pseudomonas
putida PS01		APX2 and GLYI7APX2 and GLYI7 genes were downregulatedABA signalling, jasmonic acid production route, ROS scavenging, detoxification[36]
Pseudomonas knackmussii MLR6NHX1, HKT1, SOS2, SOS3, SAG13, and PR1Enhanced stomatal conductance, transpiration rate, chlorophyll, and carotenoid levelsReduced electrolyte leakage and priming ROS accumulation increasing cell membrane stability[37]
Bacillus amyloliquefaciens SQR9NHX1 and NHX7Involved in reducing GSH biosynthesisReduced ion toxicity by sequestering Na+ into vacuoles and releasing Na+ from the cell[38]
Burkholderia phytofirmans PsJNUpregulation of RD29A and GLYI7, and downregulation of LOX2Enhancement of proline and transcription of genes related to abscisic acid signalling and downregulated gene Lipoxygenase 2Abscisic acid signalling, ROS reduction, detoxifying, jasmonate synthesis, and ion transport[39]
Paenibacillus yonginensis DCY84TAtRSA1, AtVQ9 and AtWRKY8Upregulated salt-stress genesPromoted more resistance to salinity, drought, and aluminium stresses[40,41]
Enterobacter sp. EJ01DREB2b, RD29A, RD29B, RAB18, P5CS1, P5CS2, MPK3, and MPK6Upregulated salt-stress genesPromoted more resistance to salinity and enhanced plant growth[42]
Bacillus subtilis GB03HKT1Down- and upregulates HKT1 in roots and shoots, respectivelyDecreased total plant Na+ accumulation[23]
Bacopa monneri L.Dietzia natronolimnaea STR1SOS1, SOS4, TaST, TaNHX1, TaHAK, and TaHKT1Reduction in ABA-signalling, upregulated TaABARE and TaOPR1Abscisic acid signalling, ROS scavenging, antioxidant enzyme activity, enhanced ion transporter expression, high K+/Na+ ratio[24]
Bacillus pumilus STR2, Exiguobacterium oxidotolerens
STR36		-Mixture of plant growth-promoting traits under primary and secondary saline conditionProduced higher yield, high proline/lipid content peroxidation[2]
Cicer arietinum L.Planococcus rifietoensis (RT4) and Halomonas variabilis (HT1)-Biofilm and exopolysaccharides productionImproved crop growth, soil aggregation, and soil fertility[43]
Glycine max L.Arthrobacter woluwensis AK1-Reduced endogenous ABA and controlled antioxidant activityMitigated salinity stress and increased plant growth[44]
Microbacterium
oxydans,
Arthrobacter
woluwensis,
Arthrobacter aurescens, Bacillus aryabhattai, and Bacillus
megaterium		-Increased production of IAA, GA, siderophores, and phosphate solubilisationIncreased antioxidant enzymes and K absorption; reduced Na+ in plant tissue; phytohormone[45]
Pseudomonas simiae AUP5CS, PPO and HKT1Downregulated HKT1, LOX, PPO, and P5CS genesIncreased chlorophyll, phosphate solubilisation, IAA, and siderophores; decreased root surface in saline[46]
Pseudomonas sp. strain AK-1HTK1Improve K+/Na+ ratio and Exopolysaccharide production binds free Na+ from soilIncreased shoot/root length and decreased Na+/K+ ratio[33]
Pseudomonas simiae AUVSP2Increase vegetative storage protein (VSP), gamma-glutamyl hydrolase (GGH), and RuBisCo proteinsReduced Na, increased K and P in soybean seedling roots, high proline and chlorophyll content[47]
Helianthus annuus L.Pseudomonas libanensis TR1-ACC-deaminase and exopolysaccharide productionNi and Na+ accumulation potential increased along with plant growth.[48]
Pseudomonas spp.-Upregulating of ACC deaminaseImproved P and K contents, and K+/Na+ ratio in shoot[49]
Hordeum vulgare L.Bacillus mojavensis, B. pumilus and Pseudomonas fluorescensS1 and S3ACC deaminase, IAA, and proline productionReduced plant Na concentration, stimulated root growth, improved water and nutrient absorption[50]
B. aryabhattai MS3BZ8, SOS1, GIG, and NHX1Increased salt stress resistance and accumulationAdaptation of plant under saline condition[51]
Bacillus amyloliquefaciens SN13DHNUpregulated salt stress-responsive genes and protein-related genesLipid peroxidation and electrolyte leakage reduced; increased rice biomass, water content, proline, and total soluble sugar[52]
Bacillus megaterium ST2-1-IAA productionStimulated the growth of rice roots and dry biomass[53]
Pseudomonas pseudoalcaligenes
ST1, Bacillus pumilus ST2		EU440977 and FJ840535Accumulation of proline decrease with inoculation, antioxidative activityEnhanced plant growth by ROS scavenging and higher accumulation of osmoprotectant[54]
Puccinellia tenuiflora L.Bacillus subtilis
(GB03)		-Upregulated PtHKT1;5 and PtSOS1 genes,
downregulated PtHKT2;1		Na homeostasis modulation, exclusive K+ absorption[55]
Solanum lycopersicum L.Leclercia adecarboxylata MO1-ACC deaminase and IAA productionIncreased soluble sugars: organic glucose, sucrose, fructose, malic, amino acid, and proline[56]
Sphingobacterium sp. BHU-AV3-Reduction in ROS concentration in plantEnhanced antioxidant activities and energy metabolism[57]
Enterobacter sp. EJ01DREB2b, RD29A, RD29B, and RAB18Downregulated P5CS1 and P5CS2, and upregulated MPK3 and MPK6Biosynthesis, defence pathway modulation,
salt response		[42]
Pseudomonas putida UW4Toc GTPaseToc GTPase genes were upregulated and reduction in ACC deaminaseIncreased shoot length and chlorophyll concentration[58]
Trifolium repens L.Bacillus subtilis (GB03)-Reduced shoot and root Na+, improving K+/Na+ ratioDecreased Na+, increased chlorophyll, leaf osmotic potential, cell membrane integrity[59]
Triticum aestivum L.Pseudomonas aeruginosa GI-1, and Burkholderia gladioli GI-6-P solubilisation, catalase activity, IAA production, N assimilation, and siderophores productionEncouraged growth and yield and improve soil fertility[60,61]
Arthrobacter nitroguajacolicus-Upregulated 152 genes whereas 5 genes were downregulatedAmplified ACC, IAA, siderophore, and phosphate solubility. ROS detoxification, Na+ homeostasis, abiotic stress[62]
Serratia marcescens CDP-13-Increased salt tolerance in plantACC deaminase, phosphate solubilisation, siderophore, indole acetic acid, N fixation, and ammonia synthesis[63]
Pseodomonas sp and Enterobacter cloacae (R-10)B-22 and S-49K and Zn solubilisation for identifying antifungal activityEnhanced K+ uptake, dry matter of wheat[64]
Hallobacillus sp. SL3
Bacillus halodenitrificans PU62		acdSIAA production and siderophore production, phosphate solubilising, and siderophore productionIncreased root elongation and dry weight[65]
Zea mays L.Serratia liquefaciens KM4Upregulation of stress-related genes (APX, CAT, SOD, RBCS, RBCL, H+-PPase, HKT1, and NHX1)Regulating redox potential and stress-related gene expressionHigher leaf gas exchange, osmoregulation, antioxidative defence mechanisms, and nutrient uptake boosted maize growth and biomass production[66]
Azospirillum lipoferum, Azospillum sp., Azotobacter chroococcum, Azotobacter sp., and Bacillus sp.-Exopolysaccharide inoculation in the soilIncreased root and shoot dry weights, chlorophyll and carotenoids, restricted Na and Cl uptake, and increased shoot N, P, and K[67]
Abelmoschus
esculentus L.		Enterobacter sp.
UPMR18		X55749ROS pathway upgradation and enhancement in antioxidant enzyme activitiesHigher germination, growth, and chlorophyll improved salt tolerance[68]
Table
Table 2. Indole-3-acetic acid producing halotolerant plant growth-promoting rhizobacteria (HT-PGPR) and their role in plants.
Table 2. Indole-3-acetic acid producing halotolerant plant growth-promoting rhizobacteria (HT-PGPR) and their role in plants.
HT-PGPRCropRole in PlantsReference
Streptomyces fradiae NKZ-259TomatoIncreases root and shoot length[1]
Stenotrophomonas maltophilia AVO63AvocadoProtection against white root rot[106]
Pseudomonas entomophila PE3SunflowerAntioxidant, hydroxyl-scavenging; reduction in Na+ accumulation[107]
Arthrobacter pascens ZZ21Forest soilEnhanced plant growth and remediate fluoranthene-contaminated soil[108]
Rhizobium sp. MRP1PeaProduce HCN, ammonia and EPS[109]
Paenibacillus xylanexedens (PD-R6) and Enterobacter cloacae (PD-P6)Date palmEnhances nutrient uptake in roots and improves plant growth[110]
Burkholderia cepacia 0057MaizeEnhancement of disease control[111]
Bradyrhizobium japonicumWheatImproved growth and yield[112]
Bacillus tequilensis SI 319, Pseudomonas lini SI 287, P. frederiksbergensis SI 307, and Brevibacterium frigoritolerans SI 433Soil sampleIncreased plant growth[113]
Bacillus sp. PSB10ChickpeaReduced uptake of chromium [114]
Pseudomonas putida LWPZFKatsuraImproved plant growth and contained anti-heavy-metal properties[115]
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Kumar, V.; Raghuvanshi, N.; Pandey, A.K.; Kumar, A.; Thoday-Kennedy, E.; Kant, S. Role of Halotolerant Plant Growth-Promoting Rhizobacteria in Mitigating Salinity Stress: Recent Advances and Possibilities. Agriculture 2023, 13, 168. https://doi.org/10.3390/agriculture13010168

AMA Style

Kumar V, Raghuvanshi N, Pandey AK, Kumar A, Thoday-Kennedy E, Kant S. Role of Halotolerant Plant Growth-Promoting Rhizobacteria in Mitigating Salinity Stress: Recent Advances and Possibilities. Agriculture. 2023; 13(1):168. https://doi.org/10.3390/agriculture13010168

Chicago/Turabian Style

Kumar, Vikash, Nikhil Raghuvanshi, Abhay K. Pandey, Abhishek Kumar, Emily Thoday-Kennedy, and Surya Kant. 2023. "Role of Halotolerant Plant Growth-Promoting Rhizobacteria in Mitigating Salinity Stress: Recent Advances and Possibilities" Agriculture 13, no. 1: 168. https://doi.org/10.3390/agriculture13010168

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