Next Article in Journal
Controlled Release of Volatile Antimicrobial Compounds from Mesoporous Silica Nanocarriers for Active Food Packaging Applications
Next Article in Special Issue
Salinity-Induced Cytosolic Alkaline Shifts in Arabidopsis Roots Require the SOS Pathway
Previous Article in Journal
Protein–Protein Interaction Prediction for Targeted Protein Degradation
Previous Article in Special Issue
Characterization of the Wheat Heat Shock Factor TaHsfA2e-5D Conferring Heat and Drought Tolerance in Arabidopsis
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 23
Issue 13
10.3390/ijms23137036
ijms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Progress and Applications of Plant Growth-Promoting Bacteria in Salt Tolerance of Crops

by
Yaru Gao
†,
Hong Zou
†,
Baoshan Wang
* and
Fang Yuan
*
Shandong Provincial Key Laboratory of Plant Stress, College of Life Sciences, Shandong Normal University, Ji’nan 250014, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2022, 23(13), 7036; https://doi.org/10.3390/ijms23137036
Submission received: 30 May 2022 / Revised: 21 June 2022 / Accepted: 22 June 2022 / Published: 24 June 2022
(This article belongs to the Special Issue Study on the Molecular Adaptation Mechanisms to Environmental Stresses in Plants)
Browse Figures
Versions Notes

Abstract

:
Saline soils are a major challenge in agriculture, and salinization is increasing worldwide due to climate change and destructive agricultural practices. Excessive amounts of salt in soils cause imbalances in ion distribution, physiological dehydration, and oxidative stress in plants. Breeding and genetic engineering methods to improve plant salt tolerance and the better use of saline soils are being explored; however, these approaches can take decades to accomplish. A shorter-term approach to improve plant salt tolerance is to be inoculated with bacteria with high salt tolerance or adjusting the balance of bacteria in the rhizosphere, including endosymbiotic bacteria (living in roots or forming a symbiont) and exosymbiotic bacteria (living on roots). Rhizosphere bacteria promote plant growth and alleviate salt stress by providing minerals (such as nitrogen, phosphate, and potassium) and hormones (including auxin, cytokinin, and abscisic acid) or by reducing ethylene production. Plant growth-promoting rhizosphere bacteria are a promising tool to restore agricultural lands and improve plant growth in saline soils. In this review, we summarize the mechanisms of plant growth-promoting bacteria under salt stress and their applications for improving plant salt tolerance to provide a theoretical basis for further use in agricultural systems.

1. Introduction

Soil salinization is a growing challenge for agriculture. Poor soil stewardship and irrigation practices, as well as the large-scale use of chemical fertilizer, have exacerbated soil salinity problems worldwide, steadily reducing the amount of arable land [1]. Currently, there are more than 800 million hectares of saline soil worldwide, and 20% of irrigated soil is affected by salinity [2,3]. In China, approximately 3.6107 ha of land is considered saline soil, accounting for approximately 4.88% of the total farmland [4]. Excessive levels of salt in the soil inhibit crop growth and reduce yield; therefore, strategies for improving plant salt tolerance to better use saline soils are urgently needed.
High salt concentrations within plant tissue disrupt the cellular ion balance, leading to reactive oxygen species (ROS) production and Na+ and Cl− ion accumulation [5]. Excessive levels of ROS (oxygen radicals, superoxide, and hydrogen peroxide) destroy cellular structures and biomolecules. For example, ROS degrade chlorophyll and peroxidize lipids, which reduces photosynthetic activity, damages cell membranes, and eventually induces cell death [6]. Na+ and Cl− ions interfere with enzyme function and physiological processes. For instance, Na+ and Cl− ions interfere with stomatal opening and closing, resulting in osmotic stress and reduced photosynthesis [7,8]. Furthermore, high concentrations of Cl− ions inhibit nitrate reductase activity, which leads to nutrient imbalances [9]. Salt stress elevates ethylene levels in plants, which causes premature senescence and defoliation [10].
Several strategies for improving saline soils have been tested, including chemical and physical methods and the structural engineering of land for ecological restoration [11]. Examples include the improved surface runoff on the saline soils of the Yellow River Delta in China based on the auxiliary infiltration model of saline drainage engineering [12]. Using a network of natural sedimentation and evaporation terrace drainage ditches established the centralized transfer of excess salt, so as to achieve the discharge of soil salts [13]. However, these structural engineering measures treat the symptoms but not the root cause. Some unreasonable measures such as excessive drainage and freshwater pressure can also cause secondary soil salinization [14]. Biological and organic products offer an environmentally friendly approach to soil restoration. Amendments such as biochar can be used to improve the physicochemical properties of soil. Amendments such as biochar can be used to improve soil physicochemical properties. Biochar application has been used to repair depleted and saline–alkali soils [15]. Wu [16] reported that biochar increases the organic matter content and soil microbial activity, and thereby the nutritional status of saline soil.
Another biological restoration approach is to introduce genes into crops from naturally salt-tolerant plants such as halophytes. However, this is a time-consuming and costly process. Halophytes accumulate and discharge salt through their roots and/or leaves [17]. Therefore, halophytes are excellent models for studying crop salt tolerance and are a rich source of salt tolerance genes [18]. How to make crops not only thrive but also improve yield in saline environments is a hot research topic.
Soil microorganisms offer yet another approach for soil restoration and improving plant salt tolerance. Symbiotic bacteria promote plant growth and alleviate salt stress by providing minerals (such as nitrogen, phosphate, and potassium) and hormones (including auxin, cytokinin, and abscisic acid) or by reducing ethylene production. There are two types of plant growth-promoting bacteria: exosymbiotic bacteria and endosymbiotic bacteria. The former are associated with the outside of roots in the rhizosphere, also known as plant growth-promoting rhizobacteria (PGPR) [19]. The latter reside within roots or form a symbiont and are called plant growth-promoting endophytic bacteria (PGPEB). Salt-tolerant plants and bacteria co-evolved survival strategies to adapt to high-salt environments [20,21,22,23].
The current review summarizes the mechanism of plant growth-promoting bacteria under salt stress and its application in improving plant salt tolerance in order to provide a theoretical basis for the further application of plant growth-promoting bacteria in agricultural systems.

2. Summary of Plant Growth-Promoting Bacteria Isolation Procedures

At present, the use of fertilizer is causing great pressure on the environment in terms of environmental pollution and economic cost. Researchers have started to isolate and screen candidate promoting strains from some crops (such as wheat (Triticum aestivum) and rice (Oryza sativa)). There are many characteristics and commonalities of the separation method in PGPR and PGPEB as described below. To isolate PGPR, the rhizosphere soil is washed from the roots. Different specialized media for bacterial isolation, culture, and purification are prepared (Figure 1). NaCl is added to the medium to screen for salt-tolerant bacteria. To characterize the bacteria, vernier calipers are used to measure the colony diameter, and the salt tolerance threshold and pH tolerance are determined. The strains are then identified by sequence analysis. The gene sequences of related species are selected in the NCBI database to determine the taxonomy of the strains.
As for PGPEB, the roots are rinsed, surface disinfected, cut into small sections, and homogenized. The homogenate is then spread on agar media to isolate the PGPEB under saline conditions. After the dilution and further culture of the supernatant, colonies are purified and sequences are compared for species identification.

3. Growth-Promoting Bacteria Related to Salt Stress Currently Found in Plants

Salt affects the physicochemical and chemical properties and biological characteristics of the soil [24], which adversely affects plant growth, development, and reproduction. Plant symbionts alleviate the effects of salt stress by promoting seed germination, organ differentiation, biomass accumulation, and nutrient absorption; regulating plant hormone homeostasis [25,26]; inducing the antioxidant system; and maintaining ion homeostasis. Different plant growth-promoting bacteria have different regulatory mechanisms and different protective effects in monocots and dicots.
Table 1 illustrates the different mechanisms of action of different plant growth-promoting bacteria on monocots and dicots. Five monocotyledons and twenty-two dicotyledons related to PGPR were introduced. Many dicot crops have been reported to have enhanced salt tolerance after inoculation with plant growth-promoting bacteria, such as Arabidopsis thaliana (Arabidopsis), common bean (Phaseolus vulgaris), and radish (Raphanus sativus). Five monocot crops were reported to have better salt tolerance after being treated with plant growth-promoting bacteria via enhanced 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase activity, increased antioxidant enzyme activity, and improved osmotic regulation. Among the twenty-two dicotyledons, five plants enhanced their salt tolerance by increasing the IAA content through PGPR. Eight crops enhanced their salt tolerance through PGPR by enhancing ACC deaminase synthesis.
Table
Table 1. Interaction of plant growth-promoting bacteria (PGPR) under stress and their beneficial effects.
Table 1. Interaction of plant growth-promoting bacteria (PGPR) under stress and their beneficial effects.
Plant SpeciesPGPR SpeciesEffect or MechanismReference
Avena sativaKlebsiella sp.Regulating ion contents and proline levels[27]
Barley
(Hordeum vulgare)		Curtobacterium sp.Regulating proline content[28]
Hartmannibacter diazotrophicusEnhancing ACC deaminase activity[29]
Maize (Zea mays)Bacillus atrophaeusRelieving salt stress[30]
Azotobacter sp.Promoting nutrient absorption in plants[31]
Bacillus amyloliquefaciens SQR9Enhancing antioxidant enzyme activity and increasing the expression of salt-stress-response genes[32]
Bacillus sp.Increasing enzyme activities and proline and soluble sugar contents under salt stress; regulating ACC deaminase activity[33,34]
Enterobacter cloacae PM23Modulating plant physiology, antioxidant defense, compatible solute accumulation, and bio-surfactant-producing genes[35]
Geobacillus sp.Regulating proline content[36]
Pseudomonas sp.Enhancing proline and IAA content and EPS production[37]
Rhizobium sp.Regulating pigment biosynthesis[38]
Rice
(Oryza sativa)		Bacillus aryabhattai, Achromobacter denitrificans, and Ochrobactrum intermediumRelieving salt stress[39,40]
Bacillus pumilus and Pseudomonas pseudoalcaligenesIncreasing the absorption of nutrients[41]
Enterobacter sp.Reducing ethylene production[42]
Glutamicibacter sp. YD01Adjusting ethylene contents[43]
Micrococcus sp.Increasing IAA levels[44]
Rhizobacteria pseudomonasRegulating ACC deaminase activity[40]
Wheat
(Triticum aestivum)		Aeromonas sp.Regulating ethylene content and alleviating salt stress[45]
Arthrobacter sp.Maintaining plant nutrient absorption[46]
Bacillus sp. Regulating ACC deaminase activity[47,48]
Enterobacter sp.Reducing ethylene production[49]
Microbacterium sp.Regulating K+ content[45]
Planococcus rifietoensisRegulating phosphate production and ACC deaminase activity[50]
Pseudomonas fluorescence, Bacillus pumilus, and Exiguobacterium aurantiacumAdjusting osmotic substances[51]
Klebsiella sp.Regulating ion contents, proline levels, and antioxidant enzyme activity[52,53,54]
Serratia sp.Production of exopolysaccharides[49,55]
Serratia marcescens CDP-13Enhancing ACC deaminase activity and reducing salt-induced oxidative damage[55]
Arabidopsis thalianaAcillus atropheusRelieving salt stress[30]
Bacillus sp.Adjusting ACC deaminase activity[56]
Enterobacter sp.Reducing ethylene production by promoting ACC deaminase activity[37,57]
Enterobacter sp. SA187Enhancing sulfur metabolism[58]
Micrococcus sp.Increasing IAA levels[44]
Arachis hypogaea L.Brachybacterium sp.Regulating K+ content[59]
Brevibacterium sp.Regulating K+ content[59]
Haererohalobacter sp.Regulating K+ content[59]
Ochrobactrum sp.Regulating IAA levels and ACC deaminase activity[60]
Stenotrophomonas maltophilia BJ01Modulating physiology and biochemical activities[61]
Casuarina obesa (Miq.)Pantoea agglomerans and Bacillus sp.Increasing total chlorophyll production and proline accumulation[62]
Codonopsis pilosulaBacillus sp. Adjusting ACC deaminase activity[63]
Common bean
(Phaseolus vulgaris)		Aneurinibacillus Aneurinilyticus and Paenibacillus sp.Adjusting ACC deaminase activity[64]
Cucumber (Cucumis sativus)Bacillus sp.Adjusting ACC deaminase activity[65]
Burkholdera sp.Maintaining the water balance and regulating photosynthetic pigment content[8]
Strawberry (Fragaria ananassa)Kocuria sp.Maintaining phosphate[66]
Cotton (Gossypium hirsutum)Pseudomonas sp.Enhancing proline, IAA, and EPS content production[67]
Helianthus Annuus L.Azospirillum sp.Regulating chlorophyll content and improving photosynthesis[68]
Lens esculentaOceanobacillus sp.Production of exopolysaccharides[69]
Lettuce
(Lactuca sativa)		Pseudomonas mendocina Palleroni, arbuscular mycorrhizal (AM) fungusImproving antioxidase activity[70]
Limonium sinenseStreptomyces sp.Enhancing proline production[71]
Medicago cilitarisSinorhizobium sp.Promoting proline production[72]
Mentha arvensisExiguobacterium sp.Production of exopolysaccharides[73]
Pistacia vera L.Arthrobacter endophyticus,Zobellella denitrificans and Staphylococcus sciuriImproving photosynthesis[74]
Pea (Pisum sativum)Arthrobacter sp.Increasing nutrient uptake[75]
Rhizobium sp.Regulating pigment synthesis[75]
Variovorax sp.Enhancing ACC deaminase activity[76]
Radish (Raphanus
sativus)		Lactobacillus sp., P. putida, and Azotobacter
chroococcum		Mitigating salinity stress at the time of germination[77]
Sesuvium portulacastrumHalobacillus sp.Production of ammonia and cyanide (HCN)[78]
Silybum marianumPseudomonas sp.Enhancing proline and IAA content and EPS production[79]
Soybean
(Glycine max)		Arthrobacter woluwensis, Microbacterium oxydans, Arthrobacter aurescens, Bacillus megaterium, and Bacillus aryabhattaiMaintaining osmotic balance and regulating salt tolerance[80]
Tomato
(Solanum lycopersicum)		Achromobacter sp.Adjusting ethylene content[81]
Enterobacter sp.Reducing ethylene production[57]
Growth-promoting rhizobacteriaRelieving water stress and increasing K+ absorption[82]
Leclercia adecarboxylata MO1Promoting the production of IAA and ACC[83]
Sphingomonas sp.Exopolysaccharides and proline production[84,85]
Vigna radiata L.Enterococcus sp.Reducing sodium uptake[86]
Pantoea sp.Improving ACC deaminase activity[86]
Rhizobium sp.Increasing chlorophyll and photosynthesis[87]

4. The Mechanism of PGPR in Improving Stress Tolerance

Salinity stress adversely affects plant morphology, physiology, and biochemical functions. Some plants (especially halophytes) accumulate salt in the xylem and extrude it through the leaves, while others have evolved special structures (salt glands) to excrete the salt, which is removed by external forces such as wind or water. Yuan [88] found that the unique root microbiota of Suaeda salsa not only improve its adaptability to saline soils, but also improve other non-halophytes such as cucumber and rice. Endophytes in plant tissues help plants resist drought stress through various chemical substances (abscisic acid, indole-3-acetic acid, ACC deaminase, and various volatile compounds) released by themselves [89]. Although both exogenous PGPR and endogenous PGPR can improve the stress response of plants, the living environment of endophytes is not affected by soil pH and other bacteria [90] and their mechanisms are different.
A model describing how PGPR enhances plant salt tolerance is shown in Figure 2. PGPR improves the salt tolerance of plants through the following mechanisms: (1) inducing the antioxidant system; (2) maintaining the water balance within the plant, releasing bound phosphorus and potassium from the soil, chelating iron, and fixing atmospheric nitrogen [90]; (3) selectively absorbing K+ and excluding Na+ to maintain a high K+/Na+ ratio [91]; (4) using PGPR release of exopolysaccharides (EPSs) [92] as the formation of protective biofilms reduces the toxicity of Na+; (5) maintaining plant hormone levels [93,94]; and (6) increasing osmotic regulatory substances.

4.1. Inducing the Antioxidant System

Salt stress induces ROS production (including superoxide radical (O2−), hydroxyl radical (OH−), and hydrogen peroxide (H2O2)), which damages DNA, alters the redox status, perturbs protein formation, degrades membrane proteins, peroxidizes lipids, reduces membrane fluidity, and interferes with enzyme activity, resulting in cell damage and potentially cell death. Under these conditions, enzymatic antioxidant systems (such as superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase (APX)) and non-enzymatic antioxidants (such as glutathione (GSH) and ascorbate) play important roles in neutralizing ROS to protect plant cells from oxidative stress. PGPR induce the plant’s antioxidant system to protect plants from oxidative stress. Salt stress induces the adaptive response mechanisms, including the accumulation of compatible substances (including organic matter and inorganic substances, such as proline and soluble sugars) and reducing membrane hydraulic potential to reduce osmotic stress [95,96]. PGPR inoculation in potato grown under salt stress conditions enhanced APX, SOD, CAT, and glutathione reductase activities [97]. Azospirillum lipoferum FK1 inoculation enhanced nutrient absorption and the levels of antioxidant enzymes [98]. Trichoderma, Pseudomonas, and their combination inoculation increased peroxidase (POD), APX, SOD, and CAT activities to alleviate salt stress [99]. These results indicate that PGPR help protect plants from oxidative stress.

4.2. Maintaining the Water Balance and Access to Nutrients

Cell hydration is critical for plant physiological and metabolic processes and for plant growth. The potential water gradient in the xylem guides evapotranspiration from root to leaf, preventing an imbalance between transpiration rates in aboveground organs and soil water absorption. Under osmotic stress, photosynthesis decreases and plant growth slows. The inoculation of beneficial bacteria into pepper roots enhances root systems, thereby increasing the plant’s ability to absorb water from the surrounding environment [100]. The proportion of intracellular aquaporins determines the hydraulic conductivity on the root surface, thus determining the plant absorption of saline soil water [101]. Plasma membrane intrinsic proteins (PIPs) are important aquaporins in plants and enable adaptation to changing environmental conditions [102]. The gene expression analysis of maize (Zea mays) roots inoculated with Bacillus megaterium and Pantoea agglomerans revealed that the upregulation of ZmPIP2 and ZmPIP1-1 resulted in increased water uptake under salt stress conditions [103]. These studies suggest that PGPR promote plant tolerance to osmotic stress.
Bacteria residing on the root surface help plants absorb water and nutrients through nitrogen fixation, phosphate dissolution, and siderophore production [104,105]. Nitrogen is an essential nutrient and is often exogenously applied in large quantities. However, inorganic fertilizers often alter soil structure and, thus, the soil microbiota composition [106]. The relationship between nitrogen-fixing rhizobia and legume roots is well studied. In this symbiotic relationship, the rhizobia provide nitrogen to legumes, yielding reduced carbon and creating a suitable environment for nitrogenase activity [107]. All stages of nitrogen fixation in legumes are sensitive to salinity, and improving salt tolerance in diazotrophs, such as Azospira, increases the yield of various cereal crops [108,109].
Under salt conditions, PGPR can promote plant growth and its absorption and utilization of mineral nutrients. Phosphorus is an essential nutrient but primarily exists in an insoluble form in soil, making phosphorus deficiency a common problem in crop production. Phosphate-solubilizing microorganisms (PSMs) convert phosphate into an easily accessible, soluble form for use by plants [107]. When plants are exposed to salt stress, Phosphate-solubilizing bacteria (PSB) include strains of Arthrobacter Pseudomonas, Bacillus and Rhizobium which secrete acidic substances [110,111] to acidify the soil and improve phosphorus utilization through ion chelation and ion exchange [112]. Furthermore, the soluble phosphorus produced by PSB were combined with heavy metals to become insoluble substances, thereby reducing the content of heavy metals in the soil [113]. Several salt-tolerant PGPR have been identified. Zhu [114] isolated Kushneria sp. YCWA18 from Copper East Coast Bridge salt, which has a high phosphate solubilization capacity and grows normally on a solid medium containing 20% NaCl. Iron is a trace element in plants but is critical for many biochemical processes including photosynthesis [115]. Although the iron content in the soil is generally higher than the plant’s iron requirement, plants growing in calcareous soils are more prone to iron deficiency due to the lack of natural iron sources [105,116]. Siderophores are metal chelators produced by PGPR that bind and transport various metals to improve uptake and protect plants from pathogenic bacteria [117,118]. The respiration, photosynthesis and nitrogen fixation in plants are all related to siderophore production. Several siderophore-producing PGPR have been found to be associated with halophytes [119,120,121].

4.3. Maintaining Ion Homeostasis

Under salt stress, Na+ flows into the roots through the xylem and eventually accumulates on the leaf surface [122]. Na+ efflux from plants is difficult because only a small fraction of Na+ moves through the phloem to the root, where excessive Na+ is toxic to the plant. Excessive aboveground Na+ concentrations disturb the activities of respiration and photosynthesis enzymes, increase the Na+/K+ ratio, and inhibit cytosolic enzymes [123,124]. Salt stress activates Ca2+ channels to initiate Ca2+ signaling. The Ca2+ signal is sensed by calmodulin (CBL4; also called SOS3). Calmodulin forms a complex with CBL-interacting protein kinases (CIPK24; also called SOS2) to phosphorylate SOS1, which is important for maintaining the Na+/K+ ratio [125,126,127]. PGPR maintains ion homeostasis by increasing the affinity of K+ transporters [128] and by restricting the Na+ uptake in the root to reduce Na+ accumulation in aerial organs [129].

4.4. Production of Exopolysaccharides

Exopolysaccharides are homo- or heteropolysaccharides produced by rhizosphere bacteria that improve bacterial survival under adverse conditions. The composition of polysaccharides varies, but all include the monomers glucose, galactose, and mannose and bind to other components such as aminoglycans and urinary sugars to form a capsule-like protective biofilm on the root surface [130]. This biofilm traps excess Na+ and inhibits its uptake into the roots [131]. Wheat (Triticum aestivum) plants inoculated with Aeromonas hydrophila and Bacillus accumulated EPS on the roots, which capture Na+ and restrict its uptake [45]. Inoculation of Bacillus subtilis GB03 into Arabidopsis roots downregulated the genes associated with the ion homeostasis (HKT1) of the K ion transporters and reduced the Na+ uptake [101,132]. Under salt stress, the inoculation of Halomonas variabilis (HT1) and Planococcus rifietoensis (RT4) on chickpea (Cicer arietinum) stabilized the soil structure and soil aggregates, which improved the chickpea growth [133]. The inoculation of plants with B. subtilis improves salt stress tolerance and downregulates the expression of HKT1 transporter genes [132]. Quinoa (Chenopodium quinoa) seed inoculated with Enterobacter sp. MN17 and Bacillus exhibited improved water uptake when grown in high salt (2.34% NaCl) concentrations [134]. The inoculation of B. subtilis ssp. and B. lipois SM19 significantly reduced the adverse effects of salt stress in wheat [135].

4.5. Induction of Plant Hormones

Most PGPR produce IAA, which enhances plant growth under salt stress [25]. Tryptophan in root exudates is converted to IAA by rhizosphere bacteria, which is then absorbed by plant roots [136,137]. Inoculation with P. stutzeri, P. putida, and Stenotrophomonas maltophilia to Coleus plants was found to increase IAA, cytokinin (CK), and gibberellic acid (GA) production [26]. PGPR may respond to salt stress by synthesizing CK or altering hormone homeostasis in plants. In addition to promoting growth under salt stress conditions, inoculation with Pseudomonas sp. (P. aurantiaca and P. extremorientalis TSAU6 and TSAU20) also relieves salt-induced seed dormancy [138]. The ability of PGPR to synthesize CK highlights their importance in stimulating plant growth.
GA regulates cell division, elongation, and root and leaf meristem activities. It also plays an important role in plant development and physiological processes. The PGPR Azospira sp. helps produce GA [139]. Abscisic acid (ABA) is a stress-responsive hormone that plays a role in leaf shedding and plant growth. Under water deficit, ABA regulates plant adaptation to stress by activating stress resistance genes. ABA is transferred from root to leaf to control stomatal closure to reduce transpiration on the leaf surface and limit water loss. ABA-producing PGPR may also play an important role in plant–PGPR interactions [25]. PGPR improve plant tolerance to osmotic stress by regulating ABA biosynthesis or translocation [140].
Ethylene, another stress-responsive hormone, increases salt tolerance by negatively regulating root growth and downregulating nitrogen fixation [141]. ACC deaminase is an intracellular enzyme that inhibits ethylene biosynthesis, and can degrade the ethylene precursor ACC, thereby reducing ethylene levels during plant growth and helping to alleviate salt stress. PGPR hinder ethylene biosynthesis by secreting ACC deaminase [142]. ACC deaminase breaks down ACC (an ethylene precursor) into beta-ketone glutaric acid and ammonia, which alters the expression of the ACC oxidase gene involved in ACC synthetase. ACC deaminase-producing strains of P. fluorescens and Enterobacter spp. significantly improved maize growth under salt stress [143].
Of course, in the process of the plant relief of salt stress, it is often not a single hormone alone, but the result of multiple hormone interactions. There is a synergistic effect between plant hormones, and low concentrations of IAA and GA can promote plant growth to alleviate salt stress; IAA promotes the division of the nucleus, while CK promotes the division of the cytoplasm [144], and the two together complete the division of the nucleus and plastid, thereby promoting plant growth. In addition, ABA adjusts the opening and closing of stomata, thereby adjusting photosynthesis to relieve salt stress [25]; however, high concentrations of IAA can promote the synthesis of ethylene to improve plant salt resistance.

4.6. Increasing Osmotic Substances

Increased Na+ absorption by plants under salt stress causes osmotic and oxidative stress [145]. Malondialdehyde (MDA) is generated by the lipid peroxidation of the plasma membrane by ROS [146]. PGPR reduced the MDA content under salt stress in several plants: in wheat inoculated with B. giganossus [147], maize inoculated with Kocuria rhizophila Y1 [148], and canola (Brassica napus) inoculated with E. cloacae HSNJ4. [147] Furthermore, inoculation with Azotobacter sp. increased the free radical scavenging activity in the pennyroyal (Mentha pulegium L.) under salt stress [146].
Rhizobia may trigger specific chemical changes in plants—such as changes in total protein, IAA, total sugar, and ethylene content—to improve abiotic stress tolerance, a process known as inducible systemic tolerance [149]. Soluble solutes (sugar and protein) mitigate the lethal effects of salt stress and maintain ion balance in cells [150]. A salt-tolerant Bacillus strain that promotes bacterial growth in the rhizosphere improved maize growth and development under drought and saline conditions [151]. Proline has multiple functional roles in response to many abiotic stresses, such as an osmoprotectant and for stabilizing cellular structures and ROS clearance [152]. Pritsh et al. [153] observed that the bacteria belonging to Bacillus, Microbacterium, Enterobacter, Narnitrophomonas, Microbacterium, and Acrobacter increase the proline content in rice (Oryza sativa).

5. The Role of PGPEB in Alleviating Salt Stress

Endophytic bacteria are detected in almost all land plants [154]. The endophytic bacteria community structure depends on soil biotic and abiotic factors, host colonization factors, and the ability to survive and compete within host plant tissues. Endophytes interact with plant tissues and participate in various physiological activities. Plants without endophytes have less ability to cope with pathogens and are more susceptible to environmental stresses. Table 2 describes six monocotyledons and nine dicotyledons associated with PGPEB. Seven of the six monocotyledons improved stress resistance by enhancing ACC deaminase synthesis through PGPRB, and seven crops improved stress resistance by increasing the IAA content through PGPEB. Among the nine dicotyledons, seven plants improved stress resistance by enhancing ACC deaminase synthesis through PGPRB, and seven crops improved the stress resistance by increasing the IAA content through PGPEB. PGPEB inoculation increases plant salt tolerance via nitrogen fixation, the modulation of plant hormone levels (auxin, cytokinin, ethylene, and gibberellin), phosphate, iron and potassium solubilization, secondary metabolite synthesis, antibiosis activities against plant pathogens [155], and enhancing photosynthesis (Figure 3).
Table
Table 2. Interaction of plant growth-promoting rhizobacteria (PGPEB) under stress and their beneficial effects.
Table 2. Interaction of plant growth-promoting rhizobacteria (PGPEB) under stress and their beneficial effects.
Plant SpeciesPGPEB SpeciesEffect or MechanismReference
Cape (Aloe ferox Mill)Achromobacter xylosoxidansEnhancing ACC deaminase activity[156]
Millet (Pennisetum glaucum)Bacillus subtilis, Bacillus cereus, and Bacillus amyloliquefaciensParticipating in ACC deaminase synthesis and enhancing IAA content[157]
Onion
(Allium cepa)		Bacillus subtilis, Bacillus megaterium, and Burkholderia phytofirmansParticipating in ACC deaminase synthesis and enhancing IAA content[158,159]
Rice
(Oryza sativa)		Pantoea ananatisEnhancing IAA content and siderophore production[160]
Sugarcane (Saccharum officinarum)Gluconacetobacter diazotrophicusEnhancing IAA content and nitrogen fixation[161,162]
Wheat
(Triticum aestivum)		Paraburkholderia, phytofirmans, and Bacillus cabrialessiRecovery of nitrogen, phosphorus, and potassium[163,164]
Arabidopsis thalianaSerratia proteamaculans Para and burkholderia phytofirmansEnhancing IAA content and enhancing ACC deaminase activity[165,166]
Arachis hypogaeaChryseobacterium indologenes, Enterobacter cloacae, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Enterobacter ludwigiiNitrogen fixation, enhancing IAA content and ACC deaminase production, siderophore production, and phosphate solubilization[167]
Cotton (Gossypium hirsutum)Pantoea spp., Empedobacter spp., Enterobacter spp., Rhizobium spp., and Klebsiella spp.Adjusting ACC deaminase activity[168,169]
Dodonaea viscosaStreptomyces alboniger, Bacillus idriensis, Pseudomonas taiwanensis, and Pseudomonas geniculateSiderophore production, phosphate solubilization, enhancing IAA content and ACC deaminase production[170]
Helianthus Annuus L. Stentotrophomonas indicatrixEnhancing IAA content, phosphate solubilization, siderophore and secondary metabolite synthesis[171]
Poplar (Populus)Stenotrophomonas maltophilia, and Pseudomonas putidaEnhancing IAA content and ACC deaminase synthesis[172]
Potato
(Solanum tuberosum)		Klebsiella oxytoca, Pseudomonas marginalis, Pseudomonas Viridilivida, Bacillus endophyticu, and Bacillus atrophaeusNitrogen fixation and phosphatase production[173,174]
Soybean
(Glycine max)		Bradyrhizobium japonicumEnhancing IAA content and ACC deaminase production, nitrogen fixation[172,175]
Tomato
(Solanum lycopersicum)		Pseudomonas fluorescens and Pseudomonas migulaeEnhancing IAA content and ACC deaminase synthesis[176,177]
ROS are produced under various stresses, and two systems are involved in ROS scavenging: the enzymatic system and the non-enzymatic system. The endophytic fungus Piriformospora improves the antioxidant enzyme activity and salt tolerance of barley (Hordeum vulgare) under salt stress [178]. Similarly to PGPR, PGPEB significantly reduce MDA production, as observed with Streptomyces inoculation [179]. Endophytic actinomycetes also promote host plant salt tolerance by regulating stomatal aperture. Endophytes also produce biologically active substances and regulate host hormone levels to allow the host to quickly respond to water deficit.
Endophytes promote salt tolerance by reducing the Na+ and Cl− content and increasing the aboveground part K+ content in the roots. Furthermore, the Na+ absorbed by plants mainly accumulates in the roots but is restricted from entering the shoots [180]. Thus, under salinity stress, endophytes change the ion balance of host plants to reduce ion toxicity and alleviate cellular damage. Similar to PGPR, PGPEB enhance plant salt tolerance by increasing IAA levels. For example, some endophytes regulate the auxin content in halophytes and use the antagonism between auxin and ethylene to improve salt tolerance. These halophytic endophytes could be applied to improve salt tolerance in other crops. Tiwari and colleagues [181] demonstrated that wheat plants growing in saline soil had increased fitness when inoculated with IAA-producing rhizosphere bacteria [80]. The ABA is associated with the stomata opening and closing. An endophytic fungus isolated from soybean (Glycine max) produces GA, which reduces the plant ABA content [182], thereby more rapidly responding to water loss and accelerating stomatal closure through a range of signaling and hormonal regulatory processes [183].
PGPR and PGPEB play an important role in plant salt tolerance, and most PGPR and PGPEB can both enhance plants’ ability to cope with stresses by increasing plant IAA content, inducing peroxidation systems, maintaining ionic homeostasis, and synthesizing ACC deaminase or enhancing ACC deaminase activity. PGPR can also reduce plant Na+ uptake by releasing extracellular polysaccharides to restrict the free flow of soil Na+, so as to alleviate the damage of salt stress to plants. In conclusion, PGPR and PGPEB play important roles in plant salt tolerance and can be used with halophytes and non-halophytes to improve saline soils.

6. Future Perspectives

6.1. Halophytes Can Be Used to Identify Rhizosphere Bacteria

Symbiotic bacteria are beneficial bacteria associated with the rhizosphere and plant roots, and they improve plant salt tolerance. However, the long-term effectiveness and stability of inoculating rhizobia from halophytes onto non-halophyte plants is not well known. Extracting plant growth-promoting bacteria from halophytes and utilizing them in crop production is challenging [184]. Synthesized biopolymer esters have been used to improve bacterial survival and persistence in inoculated crops by slowly releasing the bacteria into the soil. The activity of some halophyte-associated PGPB was maintained and enhanced with biopolymer esters. Meanwhile, the type of iron-friendly complexes can also increase PGPB salt tolerance by the production of iron-chelating substances [185], enabling PGPB to utilize the ferrophilins synthesized by other soil microorganisms. The extraction of plant growth-promoting bacteria from halophytes improves the salt resistance of some non-halophytes. Studies have shown that the isolation and screening of rhizosphere bacteria and root endophytes with two strains (Halomonas, Bacillus) in the presence of 1% NaCl can promote alfalfa growth, and Bacillus has a stronger effect on stem and root biomass [184].

6.2. Methods to Improve Symbiont Bacteria Utilization

Enzymes that hydrolyze fungal cell walls are important for plant disease resistance. Studies have shown that in the process of plant pathogen fungus infection host, plant endophyte chitinella (Chitinophagaceae) and yellow bacterium (Flavobacteriaceae) family members were enriched in plants, and showed enhanced enzyme activity related to fungal cell wall degradation, as well as NRPSs and PKSs encoding secondary metabolites biosynthesis, so as to provide disease protection to plants [186]. Based on the disease resistance mechanisms of endophytes, we can speculate that these enzymes may also improve salt tolerance in plants. Since many enzymes that hydrolyze fungal cell walls are encoded by single genes, these genes can be isolated and transferred into PGPB to create versatile salt-tolerant PGPB. ACC deaminase-related genes were transferred into salt-tolerant PGPB strains to regulate ethylene levels in halophytes and non-halophytes and improve salt tolerance [101]. Many bacterial endophytes can be cultured and can be directly applied to crops either by spraying, seed, or root inoculation [187]. A method for applying salt tolerant bacteria to agricultural production is to use bacterial capsules [188]. Bacterial capsules are polymer-coated outside of the bacteria, and the coating is positively charged and combines with a negatively charged cell wall to form a mixed capsule. It can be used to improve the survival and persistence of pathogenic bacteria on inoculated crops [188]. Bacterial capsules are non-toxic, durable, convenient, easy to store, and easy to apply. Rainfall or irrigation dissolves the capsule to slowly release the bacteria. Additionally, capsules can include a variety of beneficial bacteria with complementary activities to improve plant salt tolerance and reduce application costs [188].

6.3. Challenges in Applying Symbiotic Bacteria

The unique root microbiota of Glycine soja improve its adaptability to saline soil, but also benefit other non-halophytes such as Sorghum dochna and Sesbania cannabina [189]. Salt-tolerant bacteria isolated from the roots of the halophyte, Arthrocnemum indicum, enhanced the salt tolerance of peanut (Arachis hypogaea) seedlings [109], demonstrating that halophyte microbiota can be used on non-halophytes to improve salt tolerance. Can all halophyte microbiota promote salt tolerance? Are halophyte microbiota harmful to non-halophytes? Which PGPR and PGPEB species isolated from halophytes are most effective for improving salt tolerance? Which may play the greatest roles in promoting plant salt tolerance? What is the best application method for rhizobia: soaking, inoculation, or direct watering? All of these questions need to be investigated. Moreover, the vast majority of halophyte symbiotic bacteria have not been studied, and this information could help improve the salt tolerance of non-halophytes.
With increasing emphasis on environmental protection and agricultural sustainability, it is imperative to address the adverse effects of salt stress on plants in a cost-effective manner. Plant growth-promoting bacteria promote abiotic stress tolerance in crops, and studying their mechanisms will help improve crop growth under stress conditions. It is important to optimize bacterial strain combinations to address the abiotic stresses frequently encountered in crop production and to establish inoculation programs.
Moreover, clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 (Cas9) genome editing could be used to modify the stress response genes to improve plant stress tolerance. It is difficult to maintain bacterial populations after field inoculation, possibly due to the incompatibility between plants and bacteria, poor inoculation methods, or soil conditions, for example, saline areas are not suitable for bacterial proliferation, and pesticides may reduce bacterial survival. However, it is unclear whether the rapid and stable isolation of the halophytic symbiont and its application to non-halophytes will adversely affect some non-halophytes, or which side has more advantages and disadvantages. Moreover, plant growth-promoting bacteria function differently in different plants. In addition, current research on plant growth-promoting bacteria has mainly focused on the screening and chemical analysis of physiologically active substances, while their application in agricultural crops is not well studied.
Our understanding of the bacteria that promote plant growth has gradually improved. Environmentally friendly crop production practices have been established to reduce agricultural pollution from pesticides and fertilizers. These alternatives to traditional agricultural practices help reduce pollution and improve human health.

Author Contributions

Conceptualization, F.Y.; writing—original draft, Y.G. and H.Z.; writing—review and editing, F.Y. and B.W. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the National Natural Science Research Foundation of China (NSFC, project nos. 32170301 and 31600200), and the MOE Layout Foundation of Humanities and Social Sciences (21YJAZH108).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Shrivastava, P.; Kumar, R. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J. Biol. Sci. 2015, 22, 123–131. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. 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] [PubMed] [Green Version]
  3. 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]
  4. Li, J.G.; Pu, L.J.; Han, M.F.; Zhu, M.; Zhang, R.S.; Xiang, Y.Z. Soil salinization research in China: Advances and prospects. J. Geogr. Sci. 2014, 24, 943–960. [Google Scholar] [CrossRef]
  5. Grover, M.; Ali, S.Z.; Sandhya, V.; Rasul, A.; Venkateswarlu, B. Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J. Microbiol. Biotechnol. 2011, 27, 1231–1240. [Google Scholar] [CrossRef]
  6. Apel, K.; Hirt, H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004, 55, 373–399. [Google Scholar] [CrossRef] [Green Version]
  7. Munns, R. A Leaf Elongation Assay Detects an Unknown Growth Inhibitor in Xylem Sap from Wheat and Barley. Funct. Plant Biol. 1992, 19, 127–135. [Google Scholar] [CrossRef]
  8. Kang, S.-M.; Khan, A.L.; Waqas, M.; You, Y.-H.; Kim, J.-H.; Kim, J.-G.; Hamayun, M.; Lee, I.J. Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J. Plant Interact. 2014, 9, 673–682. [Google Scholar] [CrossRef] [Green Version]
  9. Nadeem, S.M.; Ahmad, M.; Zahir, Z.A.; Javaid, A.; Ashraf, M. The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol. Adv. 2014, 32, 429–448. [Google Scholar] [CrossRef]
  10. 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]
  11. Bird, P.R.; Jackson, T.T.; Kearney, G.A.; Saul, G.R.; Waller, R.A.; Whipp, G. The effect of improved pastures and grazing management on soil water storage on a basaltic plains site in south-west Victoria. Aust. J. Exp. Agric. 2004, 44, 559–569. [Google Scholar] [CrossRef]
  12. Liu, C.; Li, K.; Ma, D. Construction and Engineering Application of Salt-Discharging Model for Local Saline-Alkali Soil with Compact Structure in the Yellow River Delta. Appl. Environ. Soil Sci. 2020, 2020, 2906747. [Google Scholar] [CrossRef]
  13. Xue, B.X.; Zhao, Z.Q.; Wei, L.; Li, T.Y.; Kang, X.F. Study of the comprehensive landscaping treatment technique of saline-alkali land in Daqing based on the network of the grading of trapezoidal terrace ditches. Desalination Water Treat. 2014, 52, 1183–1192. [Google Scholar] [CrossRef]
  14. Banin, A.; Fish, A. Secondary desertification due to salinization of intensively irrigated lands: The Israeli experience. Environ. Monit. Assess. 1995, 37, 17–37. [Google Scholar] [CrossRef] [PubMed]
  15. Yuan, P.; Wang, J.; Pan, Y.; Shen, B.; Wu, C. Review of biochar for the management of contaminated soil: Preparation, application and prospect. Sci. Total Environ. 2019, 659, 473–490. [Google Scholar] [CrossRef]
  16. Wu, D.; Sun, P.; Lu, P.-Z.; Chen, Y.-Y.; Guo, J.-M.; Liu, M.; Wang, L.; Zhang, C.-J. Effect and Approach of Enteromorpha prolifera Biochar to Improve Coastal Saline Soil. Huan Jing Ke Xue 2020, 41, 1941–1949. [Google Scholar] [PubMed]
  17. Flowers, T.J.; Colmer, T.D. Salinity tolerance in halophytes. New Phytol. 2008, 179, 945–963. [Google Scholar] [CrossRef]
  18. Hasanuzzaman, M.; Nahar, K.; Alam, M.M.; Bhowmik, P.C.; Hossain, M.A.; Rahman, M.M.; Prasad, M.N.; Ozturk, M.; Fujita, M. Potential Use of Halophytes to Remediate Saline Soils. BioMed Res. Int. 2014, 2014, 589341. [Google Scholar] [CrossRef]
  19. Gerhardt, K.E.; Gerwing, P.D.; Greenberg, B.M. Opinion: Taking phytoremediation from proven technology to accepted practice. Plant Sci. 2017, 256, 170–185. [Google Scholar] [CrossRef]
  20. Príncipe, A.; Alvarez, F.; Castro, M.G.; Zachi, L.; Fischer, S.E.; Mori, G.B.; Jofré, E. Biocontrol and PGPR Features in Native Strains Isolated from Saline Soils of Argentina. Curr. Microbiol. 2007, 55, 314–322. [Google Scholar] [CrossRef]
  21. Zhao, S.; Zhou, N.; Zhao, Z.Y.; Zhang, K.; Wu, G.H.; Tian, C.Y. Isolation of Endophytic Plant Growth-Promoting Bacteria Associated with the Halophyte Salicornia europaea and Evaluation of their Promoting Activity Under Salt Stress. Curr. Microbiol. 2016, 73, 574–581. [Google Scholar] [CrossRef]
  22. Jha, B.; Gontia, I.; Hartmann, A. The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant Soil 2012, 356, 265–277. [Google Scholar] [CrossRef]
  23. 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]
  24. Chen, X.; Pan, Y.; Hao, C.; Tan, Y. Effect of Salt Solution on Characteristics of Soil Infiltration. Agric. Sci. Technol. 2012, 357–360, 438. [Google Scholar]
  25. Dodd, I.C.; Zinovkina, N.Y.; Safronova, V.I.; Belimov, A.A. Rhizobacterial mediation of plant hormone status. Ann. Appl. Biol. 2010, 157, 361–379. [Google Scholar] [CrossRef]
  26. Patel, T.; Saraf, M. Biosynthesis of phytohormones from novel rhizobacterial isolates and their in vitro plant growth-promoting efficacy. J. Plant Interact. 2017, 12, 480–487. [Google Scholar] [CrossRef] [Green Version]
  27. Sapre, S.; Gontia-Mishra, I.; Tiwari, S. Klebsiella sp. confers enhanced tolerance to salinity and plant growth promotion in oat seedlings (Avena sativa). Microbiol. Res. 2018, 206, 25–32. [Google Scholar] [CrossRef]
  28. Cardinale, M.; Ratering, S.; Suarez, C.; Montoya, A.M.Z.; Geissler-Plaum, R.; Schnell, S. Paradox of plant growth promotion potential of rhizobacteria and their actual promotion effect on growth of barley (Hordeum vulgare L.) under salt stress. Microbiol. Res. 2015, 181, 22–32. [Google Scholar] [CrossRef]
  29. Suarez, C.; Cardinale, M.; Ratering, S.; Steffens, D.; Jung, S.; Montoya, A.M.Z.; Geissler-Plaum, R.; Schnell, S. Plant growth-promoting effects of Hartmannibacter diazotrophicus on summer barley (Hordeum vulgare L.) under salt stress. Appl. Soil Ecol. 2015, 95, 23–30. [Google Scholar] [CrossRef]
  30. Kerbab, S.; Silini, A.; Bouket, A.C.; Cherif-Silini, H.; Eshelli, M.; Rabhi, N.E.H.; 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]
  31. Hamdia, A.B.E.; Shaddad, M.A.K.; Doaa, M.M. Mechanisms of salt tolerance and interactive effects of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regul. 2004, 44, 165–174. [Google Scholar] [CrossRef]
  32. Chen, L.; Liu, Y.; Wu, G.; Njeri, K.V.; 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] [PubMed]
  33. Misra, S.; Chauhan, P.S. ACC deaminase-producing rhizosphere competent Bacillus spp. mitigate salt stress and promote Zea mays growth by modulating ethylene metabolism. 3 Biotech 2020, 10, 119. [Google Scholar] [CrossRef]
  34. Li, H.Q.; Jiang, X.W. Inoculation with plant growth-promoting bacteria (PGPB) improves salt tolerance of maize seedling. Russ. J. Plant Physiol. 2017, 64, 235–241. [Google Scholar] [CrossRef]
  35. Ali, B.; Wang, X.; Saleem, M.H.; Sumaira; Hafeez, A.; Afridi, M.S.; Khan, S.; Zaib Un, N.; Ullah, I.; do Amaral Junior, A.T.; et al. PGPR-Mediated Salt Tolerance in Maize by Modulating Plant Physiology, Antioxidant Defense, Compatible Solutes Accumulation and Bio-Surfactant Producing Genes. Plants 2022, 11, 345. [Google Scholar] [CrossRef]
  36. Abdelkader, A.F.; Esawy, M.A. Case study of a biological control: Geobacillus caldoxylosilyticus (IRD) contributes to alleviate salt stress in maize (Zea mays L.) plants. Acta Physiol. Plant 2011, 33, 2289–2299. [Google Scholar] [CrossRef]
  37. Nadeem, S.M.; Zahir, Z.A.; Naveed, M.; Arshad, M. Rhizobacteria containing ACC-deaminase confer salt tolerance in maize grown on salt-affected fields. Can. J. Microbiol. 2009, 55, 1302–1309. [Google Scholar] [CrossRef]
  38. Bano, A.; Fatima, M. Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biol. Fert. Soils 2009, 45, 405–413. [Google Scholar] [CrossRef]
  39. Sultana, S.; Paul, S.C.; Parveen, S.; Alam, S.; Rahman, N.; Jannat, B.; Hoque, S.; Rahman, M.T.; Karim, 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]
  40. 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]
  41. Jha, Y.; Subramanian, R.B. Paddy plants inoculated with PGPR show better growth physiology and nutrient content under saline conditions. Chil. J. Agric. Res. 2013, 73, 213–219. [Google Scholar] [CrossRef] [Green Version]
  42. Sarkar, A.; Ghosh, P.K.; Pramanik, K.; Mitra, S.; Soren, T.; Pandey, S.; Mondal, M.H.; Maiti, T.K. A halotolerant Enterobacter sp. displaying ACC deaminase activity promotes rice seedling growth under salt stress. Res. Microbiol. 2018, 169, 20–32. [Google Scholar] [CrossRef] [PubMed]
  43. Ji, J.; Yuan, D.; Jin, C.; Wang, G.; Li, X.Z.; Guan, C.F. Enhancement of growth and salt tolerance of rice seedlings (Oryza sativa L.) by regulating ethylene production with a novel halotolerant PGPR strain Glutamicibacter sp. YD01 containing ACC deaminase activity. Acta Physiol. Plant 2020, 42, 42. [Google Scholar] [CrossRef]
  44. Sukweenadhi, J.; Kim, Y.J.; Choi, E.S.; Koh, S.C.; Lee, S.W.; Kim, Y.J.; Yang, D.C. Paenibacillus yonginensis DCY84(T) induces changes in Arabidopsis thaliana gene expression against aluminum, drought, and salt stress. Microbiol. Res. 2015, 172, 7–15. [Google Scholar] [CrossRef] [PubMed]
  45. 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. Fert. Soils 2004, 40, 157–162. [Google Scholar] [CrossRef]
  46. Tiwari, S.; Singh, P.; Tiwari, R.; Meena, K.K.; Yandigeri, M.; Singh, D.P.; Arora, D.K. Salt-tolerant rhizobacteria-mediated induced tolerance in wheat (Triticum aestivum) and chemical diversity in rhizosphere enhance plant growth. Biol. Fert. Soils 2011, 47, 907–916. [Google Scholar] [CrossRef]
  47. Pourbabaee, A.A.; Bahmani, E.; Alikhani, H.A.; Emami, S. Promotion of Wheat Growth under Salt Stress by Halotolerant Bacteria Containing ACC deaminase. J. Agric. Sci. Technol. 2016, 18, 855–864. [Google Scholar]
  48. 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]
  49. 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]
  50. Rajput, L.; Imran, A.; Mubeen, F.; Hafeez, F.Y. Salt-Tolerant Pgpr Strain Planococcus Rifietoensis Promotes the Growth and Yield of Wheat (Triticum Aestivum L.) Cultivated in Saline Soil. Pak. J. Bot. 2013, 45, 1955–1962. [Google Scholar]
  51. Nawaz, A.; Shahbaz, M.; Assadullah; 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. [Google Scholar] [CrossRef] [PubMed]
  52. Singh, R.P.; Jha, P.; Jha, P.N. The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress. J. Plant Physiol. 2015, 184, 57–67. [Google Scholar] [CrossRef]
  53. Singh, R.P.; Jha, P.N. The PGPR Stenotrophomonas maltophilia SBP-9 Augments Resistance against Biotic and Abiotic Stress in Wheat Plants. Front. Microbiol. 2017, 8, 01945. [Google Scholar] [CrossRef]
  54. Singh, R.P.; Jha, P.N. Analysis of fatty acid composition of PGPR Klebsiella sp SBP-8 and its role in ameliorating salt stress in wheat. Symbiosis 2017, 73, 213–222. [Google Scholar] [CrossRef]
  55. 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] [Green Version]
  56. Real, F.; Pouchelet, M.; Rabinovitch, M. Leishmania (L.) amazonensis: Fusion between parasitophorous vacuoles in infected bone-marrow derived mouse macrophages. Exp. Parasitol. 2008, 119, 15–23. [Google Scholar] [CrossRef] [PubMed]
  57. 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] [PubMed]
  58. Andres-Barrao, C.; Alzubaidy, H.; Jalal, R.; Mariappan, K.G.; de Zelicourt, A.; Bokhari, A.; Artyukh, O.; Alwutayd, K.; Rawat, A.; Shekhawat, K.; et al. Coordinated bacterial and plant sulfur metabolism in Enterobacter sp. SA187-induced plant salt stress tolerance. Proc. Natl. Acad. Sci. USA 2021, 118, e2107417118. [Google Scholar] [CrossRef]
  59. Shukla, P.S.; Agarwal, P.K.; Jha, B. Improved Salinity Tolerance of Arachis hypogaea (L.) by the Interaction of Halotolerant Plant-Growth-Promoting Rhizobacteria. J. Plant Growth Regul. 2012, 31, 195–206. [Google Scholar] [CrossRef]
  60. Paulucci, N.S.; Gallarato, L.A.; Reguera, Y.B.; Vicario, J.C.; Cesari, A.B.; de Lema, M.B.G.; Dardanelli, M.S. Arachis hypogaea PGPR isolated from Argentine soil modifies its lipids components in response to temperature and salinity. Microbiol. Res. 2015, 173, 1–9. [Google Scholar] [CrossRef]
  61. Alexander, A.; Singh, V.K.; Mishra, A. Halotolerant PGPR Stenotrophomonas maltophilia BJ01 Induces Salt Tolerance by Modulating Physiology and Biochemical Activities of Arachis hypogaea. Front. Microbiol. 2020, 11, 568289. [Google Scholar] [CrossRef] [PubMed]
  62. Diagne, N.; Ndour, M.; Djighaly, P.I.; Ngom, D.; Ngom, M.C.N.; Ndong, G.; Svistoonoff, S.; Cherif-Silini, H. Effect of Plant Growth Promoting Rhizobacteria (PGPR) and Arbuscular Mycorrhizal Fungi (AMF) on Salt Stress Tolerance of Casuarina obesa (Miq.). Front. Sustain. Food Syst. 2020, 4, 598–608. [Google Scholar] [CrossRef]
  63. Han, Q.Q.; Wu, Y.N.; Gao, H.J.; Xu, R.; Pare, P.W.; Shi, H.Z.; Zhao, Q.; Li, H.R.; Khan, S.A.; Wang, Y.Q.; et al. Improved salt tolerance of medicinal plant Codonopsis pilosula by Bacillus amyloliquefaciens GB. Acta Physiol. Plant 2017, 39, 35. [Google Scholar] [CrossRef]
  64. Gupta, S.; Pandey, S. ACC Deaminase Producing Bacteria With Multifarious Plant Growth Promoting Traits Alleviates Salinity Stress in French Bean (Phaseolus vulgaris) Plants. Front. Microbiol. 2019, 10, 1506. [Google Scholar] [CrossRef] [PubMed]
  65. Nadeem, S.M.; Ahmad, M.; Naveed, M.; Imran, M.; Zahir, Z.A.; Crowley, D.E. Relationship between in vitro characterization and comparative efficacy of plant growth-promoting rhizobacteria for improving cucumber salt tolerance. Arch. Microbiol. 2016, 198, 379–387. [Google Scholar] [CrossRef] [PubMed]
  66. Kore, T.; Lembisana, V.; Devi, H.; Kabir, J. Packaging, storage and value addition of aonla, an underutilized fruit, in India. Fruits 2013, 68, 255–266. [Google Scholar] [CrossRef] [Green Version]
  67. Yao, L.X.; Wu, Z.S.; Zheng, Y.Y.; Kaleem, I.; Li, C. Growth promotion and protection against salt stress by Pseudomonas putida Rs-198 on cotton. Eur. J. Soil Biol. 2010, 46, 49–54. [Google Scholar] [CrossRef]
  68. Naz, R.; Bano, A. Molecular and Physiological Responses of Sunflower (Helianthus Annuus L.) to Pgpr and Sa under Salt Stress. Pak. J. Bot. 2015, 47, 35–42. [Google Scholar]
  69. Aisha Waheed, Q. Osmoadaptation and plant growth promotion by salt tolerant bacteria under salt stress. Afr. J. Microbiol. Res. 2011, 5, 3546–3554. [Google Scholar] [CrossRef]
  70. Kohler, J.; Hernández, J.A.; Caravaca, F.; Roldán, A. Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ. Exp. Bot. 2009, 65, 245–252. [Google Scholar] [CrossRef]
  71. Qin, S.; Feng, W.W.; Wang, T.T.; Ding, P.; Xing, K.; Jiang, J.H. Plant growth-promoting effect and genomic analysis of the beneficial endophyte Streptomyces sp KLBMP 5084 isolated from halophyte Limonium sinense. Plant Soil 2017, 416, 117–132. [Google Scholar] [CrossRef]
  72. Salah, I.B.; Albacete, A.; Messedi, D.; Gandour, M.; Andujar, C.M.; Zribi, K.; Martinez, V.; Abdelly, C.; Perez-Alfocea, F. Hormonal responses of nodulated Medicago ciliaris lines differing in salt tolerance. Environ. Exp. Bot. 2013, 86, 35–43. [Google Scholar] [CrossRef]
  73. 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]
  74. Khalilpour, M.; Mozafari, V.; Abbaszadeh-Dahaji, P. Tolerance to salinity and drought stresses in pistachio (Pistacia vera L.) seedlings inoculated with indigenous stress-tolerant PGPR isolates. Sci. Hortic. 2021, 289. [Google Scholar] [CrossRef]
  75. Barnawal, D.; Bharti, N.; Maji, D.; Chanotiya, C.S.; Kalra, A. ACC deaminase-containing Arthrobacter protophormiae induces NaCl stress tolerance through reduced ACC oxidase activity and ethylene production resulting in improved nodulation and mycorrhization in Pisum sativum. J. Plant Physiol. 2014, 171, 884–894. [Google Scholar] [CrossRef]
  76. Wang, Q.; Dodd, I.C.; Belimov, A.A.; Jiang, F. Rhizosphere bacteria containing 1-aminocyclopropane-1- carboxylate deaminase increase growth and photosynthesis of pea plants under salt stress by limiting Na+ accumulation. Funct. Plant Biol. 2016, 43, 161–172. [Google Scholar] [CrossRef]
  77. Hussein, K.A.; Joo, J.H. Plant Growth-Promoting Rhizobacteria Improved Salinity Tolerance of Lactuca sativa and Raphanus sativus. J. Microbiol. Biotechnol. 2018, 28, 938–945. [Google Scholar] [CrossRef] [Green Version]
  78. Desale, P.; Patel, B.; Singh, S.; Malhotra, A.; Nawani, N. Plant growth promoting properties of Halobacillus sp. and Halomonas sp. in presence of salinity and heavy metals. J. Basic Microbiol. 2014, 54, 781–791. [Google Scholar] [CrossRef]
  79. Egamberdieva, D.; Berg, G.; Lindstrom, K.; Rasanen, L.A. Alleviation of salt stress of symbiotic Galega officinalis L. (goat’s rue) by co-inoculation of Rhizobium with root-colonizing Pseudomonas. Plant Soil 2013, 369, 453–465. [Google Scholar] [CrossRef]
  80. Khan, N.; Bano, A. Exopolysaccharide producing rhizobacteria and their impact on growth and drought tolerance of wheat grown under rainfed conditions. PLoS ONE 2019, 14, e0222302. [Google Scholar] [CrossRef] [Green Version]
  81. Mayak, S.; Tirosh, T.; Glick, B.R. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem. 2004, 42, 565–572. [Google Scholar] [CrossRef] [PubMed]
  82. Cordero, I.; Balaguer, L.; Rincon, A.; Pueyo, J.J. Inoculation of tomato plants with selected PGPR represents a feasible alternative to chemical fertilization under salt stress. J. Plant Nutr. Soil Sci. 2018, 181, 694–703. [Google Scholar] [CrossRef]
  83. 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] [Green Version]
  84. Halo, B.A.; Khan, A.L.; Waqas, M.; Al-Harrasi, A.; Hussain, J.; Ali, L.; Adnan, M.; Lee, I.J. Endophytic bacteria (Sphingomonas sp. LK11) and gibberellin can improve Solanum lycopersicum growth and oxidative stress under salinity. J. Plant Interact. 2015, 10, 117–125. [Google Scholar] [CrossRef] [Green Version]
  85. Palaniyandi, S.A.; Damodharan, K.; Yang, S.H.; Suh, J.W. Streptomyces sp. strain PGPA39 alleviates salt stress and promotes growth of ‘Micro Tom’ tomato plants. J. Appl. Microbiol. 2014, 117, 766–773. [Google Scholar] [CrossRef] [PubMed]
  86. Panwar, M.; Tewari, R.; Nayyar, H. Native halo-tolerant plant growth promoting rhizobacteria Enterococcus and Pantoea sp. improve seed yield of Mungbean (Vigna radiata L.) under soil salinity by reducing sodium uptake and stress injury. Physiol. Mol. Biol. Plants 2016, 22, 445–459. [Google Scholar] [CrossRef] [Green Version]
  87. Ahamd, M.; Zahir, Z.A.; Nadeem, S.M.; Nazli, F.; Jamil, M.; Jamshaid, M.U. Physiological Response of Mung Bean to Rhizobium and Pseudomonas Based Biofertilizers under Salinity Stress. Pak. J. Agric. Sci. 2014, 51, 557–564. [Google Scholar]
  88. Yuan, Z.; Druzhinina, I.S.; Labbé, J.; Redman, R.; Qin, Y.; Rodriguez, R.; Zhang, C.; Tuskan, G.; Lin, F. Specialized Microbiome of a Halophyte and its Role in Helping Non-Host Plants to Withstand Salinity. Sci. Rep. 2016, 6, 32467. [Google Scholar] [CrossRef]
  89. Ullah, A.; Nisar, M.; Ali, H.; Hazrat, A.; Hayat, K.; Keerio, A.A.; Ihsan, M.; Laiq, M.; Ullah, S.; Fahad, S.; et al. Drought tolerance improvement in plants: An endophytic bacterial approach. Appl. Microbiol. Biotechnol. 2019, 103, 7385–7397. [Google Scholar] [CrossRef]
  90. Santoyo, G.; Moreno-Hagelsieb, G.; del Carmen Orozco-Mosqueda, M.; Glick, B.R. Plant growth-promoting bacterial endophytes. Microbiol. Res. 2016, 183, 92–99. [Google Scholar] [CrossRef]
  91. Islam, F.; Yasmeen, T.; Arif, M.S.; Ali, S.; Ali, B.; Hameed, S.; Zhou, W. Plant growth promoting bacteria confer salt tolerance in Vigna radiata by up-regulating antioxidant defense and biological soil fertility. Plant Growth Regul. 2015, 80, 23–36. [Google Scholar] [CrossRef]
  92. Timmusk, S.; Abd El-Daim, I.A.; Copolovici, L.; Tanilas, T.; Kännaste, A.; Behers, L.; Nevo, E.; Seisenbaeva, G.; Stenström, E.; Niinemets, U. Drought-Tolerance of Wheat Improved by Rhizosphere Bacteria from Harsh Environments: Enhanced Biomass Production and Reduced Emissions of Stress Volatiles. PLoS ONE 2014, 9, e96086. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  93. Etesami, H.; Hosseini, H.M.; Alikhani, H.A.; Mohammadi, L. Bacterial Biosynthesis of 1-Aminocyclopropane-1-Carboxylate (ACC) Deaminase and Indole-3-Acetic Acid (IAA) as Endophytic Preferential Selection Traits by Rice Plant Seedlings. J. Plant Growth Regul. 2014, 33, 654–670. [Google Scholar] [CrossRef]
  94. Singh, R.P.; Shelke, G.M.; Kumar, A.; Jha, P.N. Biochemistry and genetics of ACC deaminase: A weapon to “stress ethylene” produced in plants. Front. Microbiol. 2015, 6, 937. [Google Scholar]
  95. Munns, R. Comparative physiology of salt and water stress. Plant Cell Environ. 2002, 25, 239–250. [Google Scholar] [CrossRef] [PubMed]
  96. Jaleel, C.A.; Manivannan, P.; Sankar, B.; Kishorekumar, A.; Gopi, R.; Somasundaram, R.; Panneerselvam, R. Water deficit stress mitigation by calcium chloride in Catharanthus roseus: Effects on oxidative stress, proline metabolism and indole alkaloid accumulation. Colloids Surf. B Biointerfaces 2007, 60, 110–116. [Google Scholar] [CrossRef] [PubMed]
  97. Gururani, M.A.; Upadhyaya, C.P.; Strasser, R.J.; Yu, J.W.; Park, S.W. Evaluation of abiotic stress tolerance in transgenic potato plants with reduced expression of PSII manganese stabilizing protein. Plant Sci. 2013, 198, 7–16. [Google Scholar] [CrossRef]
  98. El-Esawi, M.A.; Al-Ghamdi, A.A.; Ali, H.M.; Alayafi, A.A. Azospirillum lipoferum FK1 confers improved salt tolerance in chickpea (Cicer arietinum L.) by modulating osmolytes, antioxidant machinery and stress-related genes expression. Environ. Exp. Bot. 2019, 159, 55–65. [Google Scholar] [CrossRef]
  99. Singh, D.P.; Singh, V.; Gupta, V.K.; Shukla, R.; Prabha, R.; Sarma, B.; Patel, J.S. Microbial inoculation in rice regulates antioxidative reactions and defense related genes to mitigate drought stress. Sci. Rep. 2020, 10, 4818. [Google Scholar] [CrossRef]
  100. Marasco, R.; Rolli, E.; Vigani, G.; Borin, S.; Sorlini, C.; Ouzari, H.; Zocchi, G.; Daffonchio, D. Are drought-resistance promoting bacteria cross-compatible with different plant models? Plant Signal. Behav. 2013, 8, e26741. [Google Scholar] [CrossRef] [Green Version]
  101. 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]
  102. Moshelion, M.; Halperin, O.; Wallach, R.; Oren, R.; Way, D.A. Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: Crop water-use efficiency, growth and yield. Plant Cell Environ. 2014, 38, 1785–1793. [Google Scholar] [CrossRef] [PubMed]
  103. Gond, S.K.; Torres, M.S.; Bergen, M.S.; Helsel, Z.; White, J.F. Induction of salt tolerance and up-regulation of aquaporin genes in tropical corn by rhizobacterium Pantoea agglomerans. Lett. Appl. Microbiol. 2015, 60, 392–399. [Google Scholar] [CrossRef] [PubMed]
  104. Beattie, G.A. Microbiomes: Curating communities from plants. Nature 2015, 528, 340–341. [Google Scholar] [CrossRef] [Green Version]
  105. Pii, Y.; Penn, A.; Terzano, R.; Crecchio, C.; Mimmo, T.; Cesco, S. Plant-microorganism-soil interactions influence the Fe availability in the rhizosphere of cucumber plants. Plant Physiol. Biochem. 2015, 87, 45–52. [Google Scholar] [CrossRef]
  106. Rueda-Puente, E.; Castellanos, T.; Troyo-Dieguez, E.; de Leon-Alvarez, J.L.D.; Murillo-Amador, B. Effects of a nitrogen-fixing indigenous bacterium (Klebsiella pneumoniae) on the growth and development of the halophyte Salicornia bigelovii as a new crop for saline environments. J. Agron. Crop Sci. 2003, 189, 323–332. [Google Scholar] [CrossRef]
  107. Backer, R.; Rokem, J.S.; Ilangumaran, G.; Lamont, J.; Praslickova, D.; Ricci, E.; Subramanian, S.; Smith, D.L. Plant Growth-Promoting Rhizobacteria: Context, Mechanisms of Action, and Roadmap to Commercialization of Biostimulants for Sustainable Agriculture. Front. Plant Sci. 2018, 9, 1473. [Google Scholar] [CrossRef] [Green Version]
  108. Vessey, J.K. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 2003, 255, 571–586. [Google Scholar] [CrossRef]
  109. 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]
  110. Rodriguez, H.; Fraga, R. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 1999, 17, 319–339. [Google Scholar] [CrossRef]
  111. Tchakounté, G.V.T.; Berger, B.; Patz, S.; Becker, M.; Fankem, H.; Taffouo, V.D.; Ruppel, S. Selected Rhizosphere Bacteria Help Tomato Plants Cope with Combined Phosphorus and Salt Stresses. Microorganisms 2020, 8, 1844. [Google Scholar] [CrossRef] [PubMed]
  112. Adnan, M.; Fahad, S.; Zamin, M.; Shah, S.; Mian, I.A.; Danish, S.; Zafar-Ul-Hye, M.; Battaglia, M.L.; Naz, R.M.M.; Saeed, B.; et al. Coupling Phosphate-Solubilizing Bacteria with Phosphorus Supplements Improve Maize Phosphorus Acquisition and Growth under Lime Induced Salinity Stress. Plants 2020, 9, 900. [Google Scholar] [CrossRef] [PubMed]
  113. Wan, W.; Qin, Y.; Wu, H.; Zuo, W.; He, H.; Tan, J.; Wang, Y.; He, D. Isolation and Characterization of Phosphorus Solubilizing Bacteria with Multiple Phosphorus Sources Utilizing Capability and Their Potential for Lead Immobilization in Soil. Front. Microbiol. 2020, 11, 752. [Google Scholar] [CrossRef] [Green Version]
  114. Zhu, F.; Qu, L.; Hong, X.; Sun, X. Isolation and Characterization of a Phosphate-Solubilizing Halophilic Bacterium Kushneria sp. YCWA18 from Daqiao Saltern on the Coast of Yellow Sea of China. Evid.-Based Complement. Altern. Med. 2011, 2011, 615032. [Google Scholar] [CrossRef] [Green Version]
  115. Alkhatib, R.; Alkhatib, B.; Abdo, N.; Al-Eitan, L.; Creamer, R. Physio-biochemical and ultrastructural impact of (Fe3O4) nanoparticles on tobacco. BMC Plant Biol. 2019, 19, 253. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  116. Jin, C.W.; Li, G.X.; Yu, X.H.; Zheng, S.J. Plant Fe status affects the composition of siderophore-secreting microbes in the rhizosphere. Ann. Bot. 2010, 105, 835–841. [Google Scholar] [CrossRef] [PubMed]
  117. Ji, S.H.; Gururani, M.A.; Chun, S.C. Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars. Microbiol. Res. 2014, 169, 83–98. [Google Scholar] [CrossRef]
  118. Kirankumar, R.; Jagadeesh, K.S.; Krishnaraj, P.U.; Patil, M.S. Enhanced growth promotion of tomato and nutrient uptake by plant growth promoting rhizobacterial isolates in presence of tobacco mosaic virus pathogen. Karnataka J. Agric. Sci. 2008, 21, 309–311. [Google Scholar]
  119. Sgroy, V.; Cassan, F.; Masciarelli, O.; Del Papa, M.F.; Lagares, A.; Luna, V. Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Appl. Microbiol. Biotechnol. 2009, 85, 371–381. [Google Scholar] [CrossRef]
  120. Teng, S.; Liu, Y.; Zhao, L. Isolation, identification and characterization of ACC deaminase-containing endophytic bacteria from halophyte Suaeda salsa. Wei Sheng Wu Xue Bao 2010, 50, 1503–1509. [Google Scholar]
  121. Kataoka, R.; Güneri, E.; Turgay, O.C.; Yaprak, A.E.; Sevilir, B.; Başköse, I. Sodium-resistant plant growth-promoting rhizobacteria isolated from a halophyte, Salsola grandis, in saline-alkaline soils of Turkey. Eurasian J. Soil Sci. 2017, 6, 216–225. [Google Scholar] [CrossRef] [Green Version]
  122. Tester, M.; Davenport, R. Na+ tolerance and Na+ transport in higher plants. Ann. Bot. 2003, 91, 503–527. [Google Scholar] [CrossRef] [PubMed]
  123. Baral, A.; Shruthi, K.S.; Mathew, M.K. Vesicular trafficking and salinity responses in plants. IUBMB Life 2015, 67, 677–686. [Google Scholar] [CrossRef]
  124. Jacoby, R.P.; Che-Othman, M.H.; Millar, A.H.; Taylor, N.L. Analysis of the sodium chloride-dependent respiratory kinetics of wheat mitochondria reveals differential effects on phosphorylating and non-phosphorylating electron transport pathways. Plant Cell Environ. 2016, 39, 823–833. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  125. Halfter, U.; Ishitani, M.; Zhu, J.K. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS. Proc. Natl. Acad. Sci. USA 2000, 97, 3735–3740. [Google Scholar] [CrossRef]
  126. Zhu, J.K. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 2002, 53, 247–273. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  127. Epstein, E. How calcium enhances plant salt tolerance. Science 1998, 280, 1906–1907. [Google Scholar] [CrossRef]
  128. Rodriguez-Navarro, A.; Rubio, F. High-affinity potassium and sodium transport systems in plants. J. Exp. Bot. 2006, 57, 1149–1160. [Google Scholar] [CrossRef] [Green Version]
  129. Bhat, M.A.; Kumar, V.; Bhat, M.A.; Wani, I.A.; Dar, F.L.; Farooq, I.; Bhatti, F.; Koser, R.; Rahman, S.; Jan, A.T. Mechanistic Insights of the Interaction of Plant Growth-Promoting Rhizobacteria (PGPR) with Plant Roots Toward Enhancing Plant Productivity by Alleviating Salinity Stress. Front. Microbiol. 2020, 11, 1952. [Google Scholar] [CrossRef]
  130. Upadhyay, S.K.; Singh, J.S.; Singh, D.P. Exopolysaccharide-Producing Plant Growth-Promoting Rhizobacteria Under Salinity Condition. Pedosphere 2011, 21, 214–222. [Google Scholar] [CrossRef]
  131. Dodd, I.C.; Perez-Alfocea, F. Microbial amelioration of crop salinity stress. J. Exp. Bot. 2012, 63, 3415–3428. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  132. Zhang, H.; Kim, M.S.; Sun, Y.; Dowd, S.E.; Shi, H.; Pare, P.W. Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT. Mol. Plant Microbe Interact. 2008, 21, 737–744. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  133. 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] [Green Version]
  134. Yang, A.; Akhtar, S.S.; Iqbal, S.; Amjad, M.; Naveed, M.; Zahir, Z.A.; Jacobsen, S.-E. Enhancing salt tolerance in quinoa by halotolerant bacterial inoculation. Funct. Plant Biol. 2016, 43, 632–642. [Google Scholar] [CrossRef] [PubMed]
  135. Atouei, M.T.; Pourbabaee, A.A.; Shorafa, M. Alleviation of Salinity Stress on Some Growth Parameters of Wheat by Exopolysaccharide-Producing Bacteria. Iran. J. Sci. Technol. Trans. A Sci. 2019, 43, 2725–2733. [Google Scholar] [CrossRef]
  136. Ilangumaran, G.; Smith, D.L. Plant Growth Promoting Rhizobacteria in Amelioration of Salinity Stress: A Systems Biology Perspective. Front. Plant Sci. 2017, 8, 1768. [Google Scholar] [CrossRef] [PubMed]
  137. Spaepen, S.; Vanderleyden, J. Auxin and Plant-Microbe Interactions. Cold Spring Harb. Perspect. Biol. 2010, 3, a001438. [Google Scholar] [CrossRef] [Green Version]
  138. Egamberdieva, D.; Kucharova, Z. Selection for root colonising bacteria stimulating wheat growth in saline soils. Biol. Fertil. Soils 2009, 45, 563–571. [Google Scholar] [CrossRef]
  139. Bottini, R.; Cassan, F.; Piccoli, P. Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl. Microbiol. Biotechnol. 2004, 65, 497–503. [Google Scholar] [CrossRef]
  140. Belimov, A.A.; Dodd, I.C.; Safronova, V.I.; Dumova, V.A.; Shaposhnikov, A.I.; Ladatko, A.G.; Davies, W.J. Abscisic acid metabolizing rhizobacteria decrease ABA concentrations in planta and alter plant growth. Plant Physiol. Biochem. 2014, 74, 84–91. [Google Scholar] [CrossRef]
  141. Mahajan, S.; Tuteja, N. Cold, salinity and drought stresses: An overview. Arch. Biochem. Biophys. 2005, 444, 139–158. [Google Scholar] [CrossRef] [PubMed]
  142. 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]
  143. Panwar, M.; Tewari, R.; Gulati, A.; Nayyar, H. Indigenous salt-tolerant rhizobacterium Pantoea dispersa (PSB3) reduces sodium uptake and mitigates the effects of salt stress on growth and yield of chickpea. Acta Physiol. Plant. 2016, 38, 278. [Google Scholar] [CrossRef]
  144. Yang, W.; Cortijo, S.; Korsbo, N.; Roszak, P.; Schiessl, K.; Gurzadyan, A.; Wightman, R.; Jönsson, H.; Meyerowitz, E. Molecular mechanism of cytokinin-activated cell division in Arabidopsis. Science 2021, 371, 1350–1355. [Google Scholar] [CrossRef] [PubMed]
  145. Prittesh, P.; Avnika, P.; Kinjal, P.; Jinal, H.N.; Sakthivel, K.; Amaresan, N. Amelioration effect of salt-tolerant plant growth-promoting bacteria on growth and physiological properties of rice (Oryza sativa) under salt-stressed conditions. Arch. Microbiol. 2020, 202, 2419–2428. [Google Scholar] [CrossRef]
  146. Li, H.; Lei, P.; Pang, X.; Li, S.; Xu, H.; Xu, Z.; Feng, X. Enhanced tolerance to salt stress in canola (Brassica napus L.) seedlings inoculated with the halotolerant Enterobacter cloacae HSNJ. Appl. Soil Ecol. 2017, 119, 26–34. [Google Scholar] [CrossRef]
  147. Li, X.Z.; Sun, P.; Zhang, Y.N.; Jin, C.; Guan, C.F. A novel PGPR strain Kocuria rhizophila Y1 enhances salt stress tolerance in maize by regulating phytohormone levels, nutrient acquisition, redox potential, ion homeostasis, photosynthetic capacity and stress-responsive genes expression. Environ. Exp. Bot. 2020, 174. [Google Scholar] [CrossRef]
  148. Rashid, U.; Yasmin, H.; Hassan, M.N.; Naz, R.; Nosheen, A.; Sajjad, M.; Ilyas, N.; Keyani, R.; Jabeen, Z.; Mumtaz, S.; et al. Drought-tolerant Bacillus megaterium isolated from semi-arid conditions induces systemic tolerance of wheat under drought conditions. Plant Cell Rep. 2022, 41, 549–569. [Google Scholar] [CrossRef]
  149. Gusain, Y.S.; Singh, U.S.; Sharma, A.K. Bacterial mediated amelioration of drought stress in drought tolerant and susceptible cultivars of rice (Oryza sativa L.). Afr. J. Biotechnol. 2015, 14, 764–773. [Google Scholar]
  150. Akram, N.A.; Shafiq, F.; Ashraf, M. Ascorbic Acid-A Potential Oxidant Scavenger and Its Role in Plant Development and Abiotic Stress Tolerance. Front. Plant Sci. 2017, 8, 613. [Google Scholar] [CrossRef]
  151. Morcillo, R.J.L.; Manzanera, M. The Effects of Plant-Associated Bacterial Exopolysaccharides on Plant Abiotic Stress Tolerance. Metabolites 2021, 11, 337. [Google Scholar] [CrossRef] [PubMed]
  152. Vardharajula, S.; Ali, S.Z.; Grover, M.; Reddy, G.; Bandi, V. Drought-tolerant plant growth promoting Bacillus spp.: Effect on growth, osmolytes, and antioxidant status of maize under drought stress. J. Plant Interact. 2011, 6, 1–14. [Google Scholar] [CrossRef]
  153. Abbasi, S.; Sadeghi, A.; Safaie, N. Streptomyces alleviate drought stress in tomato plants and modulate the expression of transcription factors ERF1 and WRKY70 genes. Sci. Hortic. 2020, 265, 109206. [Google Scholar] [CrossRef]
  154. Luo, S.; Xu, T.; Chen, L.; Chen, J.; Rao, C.; Xiao, X.; Wan, Y.; Zeng, G.; Long, F.; Liu, C.; et al. Endophyte-assisted promotion of biomass production and metal-uptake of energy crop sweet sorghum by plant-growth-promoting endophyte Bacillus sp. SLS18. Appl. Microbiol. Biotechnol. 2012, 93, 1745–1753. [Google Scholar] [CrossRef]
  155. Rajini, S.B.; Nandhini, M.; Udayashankar, A.C.; Niranjana, S.R.; Lund, O.S.; Prakash, H.S. Diversity, plant growth-promoting traits, and biocontrol potential of fungal endophytes of Sorghum bicolor. Plant Pathol. 2020, 69, 642–654. [Google Scholar] [CrossRef]
  156. Karthikeyan, B.; Joe, M.M.; Islam, M.R.; Sa, T. ACC deaminase containing diazotrophic endophytic bacteria ameliorate salt stress in Catharanthus roseus through reduced ethylene levels and induction of antioxidative defense systems. Symbiosis 2012, 56, 77–86. [Google Scholar] [CrossRef]
  157. Kushwaha, P.; Kashyap, P.L.; Srivastava, A.K.; Tiwari, R.K. Plant growth promoting and antifungal activity in endophytic Bacillus strains from pearl millet (Pennisetum glaucum). Braz. J. Microbiol. 2020, 51, 229–241. [Google Scholar] [CrossRef]
  158. Pan, D.; Mionetto, A.; Tiscornia, S.; Bettucci, L. Endophytic bacteria from wheat grain as biocontrol agents of Fusarium graminearum and deoxynivalenol production in wheat. Mycotoxin Res. 2015, 31, 137–143. [Google Scholar] [CrossRef]
  159. Weilharter, A.; Mitter, B.; Shin, M.V.; Chain, P.S.G.; Nowak, J.; Sessitsch, A. Complete Genome Sequence of the Plant Growth-Promoting Endophyte Burkholderia phytofirmans Strain PsJN. J. Bacteriol. 2011, 193, 3383–3384. [Google Scholar] [CrossRef] [Green Version]
  160. Megías, E.; Megías, M.; Ollero, F.J.; Hungria, M. Draft Genome Sequence of Pantoea ananatis Strain AMG521, a Rice Plant Growth-Promoting Bacterial Endophyte Isolated from the Guadalquivir Marshes in Southern Spain. Genome Announc. 2016, 4, e01681-15. [Google Scholar] [CrossRef] [Green Version]
  161. Beracochea, M.; Taule, C.; Battistoni, F. Draft Genome Sequence of Kosakonia radicincitans UYSO10, an Endophytic Plant Growth-Promoting Bacterium of Sugarcane (Saccharum officinarum). Microbiol. Resour. Announc. 2019, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  162. Bertalan, M.; Albano, R.; de Pádua, V.; Rouws, L.; Rojas, C.; Hemerly, A.; Teixeira, K.; Schwab, S.; Araujo, J.; Oliveira, A.; et al. Complete genome sequence of the sugarcane nitrogen-fixing endophyte Gluconacetobacter diazotrophicus Pal. BMC Genom. 2009, 10, 450. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  163. Aziz, M.Z.; Yaseen, M.; Naveed, M.; Wang, X.; Fatima, K.; Saeed, Q.; Mustafa, A. Polymer-Paraburkholderia phytofirmans PsJN Coated Diammonium Phosphate Enhanced Microbial Survival, Phosphorous Use Efficiency, and Production of Wheat. Agronomy 2020, 10, 1344. [Google Scholar] [CrossRef]
  164. de Los Santos Villalobos, S.; Robles, R.I.; Parra Cota, F.I.; Larsen, J.; Lozano, P.; Tiedje, J.M. Bacillus cabrialesii sp. nov., an endophytic plant growth promoting bacterium isolated from wheat (Triticum turgidum subsp. durum) in the Yaqui Valley, Mexico. Int. J. Syst. Evol. Microbiol. 2019, 69, 3939–3945. [Google Scholar] [CrossRef]
  165. 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]
  166. Zúñiga, A.; Poupin, M.J.; Donoso, R.; Ledger, T.; Guiliani, N.; Gutiérrez, R.A.; González, B. Quorum sensing and indole-3-acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Mol. Plant Microbe Interact. 2013, 26, 546–553. [Google Scholar] [CrossRef] [Green Version]
  167. Dhole, A.; Shelat, H.; Vyas, R.; Jhala, Y.; Bhange, M. Endophytic occupation of legume root nodules by nifH-positive non-rhizobial bacteria, and their efficacy in the groundnut (Arachis hypogaea). Ann. Microbiol. 2016, 66, 1397–1407. [Google Scholar] [CrossRef]
  168. Li, C.H.; Zhao, M.W.; Tang, C.M.; Li, S.P. Population dynamics and identification of endophytic bacteria antagonistic toward plant-pathogenic fungi in cotton root. Microb. Ecol. 2010, 59, 344–356. [Google Scholar] [CrossRef]
  169. Li, C.-H.; Shi, L.; Han, Q.; Hu, H.-L.; Zhao, M.-W.; Tang, C.-M.; Li, S.-P. Biocontrol of verticillium wilt and colonization of cotton plants by an endophytic bacterial isolate. J. Appl. Microbiol. 2012, 113, 641–651. [Google Scholar] [CrossRef]
  170. Afzal, I.; Iqrar, I.; Shinwari, Z.K.; Yasmin, A. Plant growth-promoting potential of endophytic bacteria isolated from roots of wild Dodonaea viscosa L. Plant Growth Regul. 2016, 81, 399–408. [Google Scholar] [CrossRef]
  171. Adeleke, B.S.; Babalola, O.O. Roles of Plant Endosphere Microbes in Agriculture-A Review. J. Plant Growth Regul. 2022, 41, 1411–1428. [Google Scholar] [CrossRef]
  172. Taghavi, S.; Garafola, C.; Monchy, S.; Newman, L.; Hoffman, A.; Weyens, N.; Barac, T.; Vangronsveld, J.; van der Lelie, D. Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl. Environ. Microbiol. 2009, 75, 748–757. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  173. Nawangsih, A.A.; Damayanti, I.K.A.; Wiyono, S.; Kartika, J.G. Selection and Characterization of Endophytic Bacteria as Biocontrol Agents of Tomato Bacterial Wilt Disease. HAYATI J. Biosci. 2011, 18, 66–70. [Google Scholar] [CrossRef] [Green Version]
  174. Shinjo, R.; Uesaka, K.; Ihara, K.; Sakazaki, S.; Yano, K.; Kondo, M.; Tanaka, A. Draft Genome Sequence of Burkholderia vietnamiensis Strain RS1, a Nitrogen-Fixing Endophyte Isolated from Sweet Potato. Microbiol. Resour. Announc. 2018, 7, e00820-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  175. Subramanian, P.; Kim, K.; Krishnamoorthy, R.; Sundaram, S.; Sa, T. Endophytic bacteria improve nodule function and plant nitrogen in soybean on co-inoculation with Bradyrhizobium japonicum MN110. Plant Growth Regul. 2014, 76, 327–332. [Google Scholar] [CrossRef]
  176. Ali, S.; Charles, T.C.; Glick, B.R. Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol. Biochem. 2014, 80, 160–167. [Google Scholar] [CrossRef]
  177. Issa, A.; Esmaeel, Q.; Sanchez, L.; Courteaux, B.; Guise, J.-F.; Gibon, Y.; Ballias, P.; Clément, C.; Jacquard, C.; Vaillant-Gaveau, N.; et al. Impacts of Paraburkholderia phytofirmans Strain PsJN on Tomato (Lycopersicon esculentum L.) Under High Temperature. Front. Plant Sci. 2018, 9, 1397. [Google Scholar] [CrossRef] [Green Version]
  178. Waller, F.; Achatz, B.; Baltruschat, H.; Fodor, J.; Becker, K.; Fischer, M.; Heier, T.; Hückelhoven, R.; Neumann, C.; von Wettstein, D.; et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. USA 2005, 102, 13386–13391. [Google Scholar] [CrossRef] [Green Version]
  179. Bu, N.; Li, X.M.; Li, Y.Y.; Ma, C.Y.; Ma, L.J.; Zhang, C. Effects of Na2CO3 stress on photosynthesis and antioxidative enzymes in endophyte infected and non-infected rice. Ecotox. Environ. Safe 2012, 78, 35–40. [Google Scholar] [CrossRef]
  180. Sabzalian, M.R.; Mirlohi, A. Neotyphodium endophytes trigger salt resistance in tall and meadow fescues. J. Plant Nutr. Soil. Sci. 2010, 173, 952–957. [Google Scholar] [CrossRef]
  181. Shukla, K.P.; Sharma, S.; Singh, N.K.; Singh, V.; Tiwari, K.; Singh, S. Nature and role of root exudates: Efficacy in bioremediation. Afr. J. Biotechnol. 2011, 10, 9717–9724. [Google Scholar]
  182. Ramesh, A.; Sharma, S.K.; Joshi, O.P.; Khan, I.R. Phytase, phosphatase activity and p-nutrition of soybean as influenced by inoculation of bacillus. Indian J. Microbiol. 2011, 51, 94–99. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  183. Malinowski, D.P.; Belesky, D.P. Adaptations of Endophyte-Infected Cool-Season Grasses to Environmental Stresses: Mechanisms of Drought and Mineral Stress Tolerance. Crop Sci. 2000, 40, 923–940. [Google Scholar] [CrossRef]
  184. Kearl, J.; McNary, C.; Lowman, J.S.; Mei, C.; Aanderud, Z.T.; Smith, S.T.; West, J.; Colton, E.; Hamson, M.; Nielsen, B.L. Salt-Tolerant Halophyte Rhizosphere Bacteria Stimulate Growth of Alfalfa in Salty Soil. Front. Microbiol. 2019, 10, 1849. [Google Scholar] [CrossRef] [Green Version]
  185. Dong, Z.; Hu, J.; Hu, B. Regulation of microbial siderophore transport and its application in environmental remediation. Sheng Wu Gong Cheng Xue Bao 2019, 35, 2189–2200. [Google Scholar]
  186. Carrion, V.J.; Perez-Jaramillo, J.; Cordovez, V.; Tracanna, V.; de Hollander, M.; Ruiz-Buck, D.; Mendes, L.W.; van Ijcken, W.F.J.; Gomez-Exposito, R.; Elsayed, S.S.; et al. Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science 2019, 366, 606–612. [Google Scholar] [CrossRef]
  187. Adeleke, B.S.; Babalola, O.O.; Glick, B.R. Plant growth-promoting root-colonizing bacterial endophytes. Rhizosphere 2021, 20, 100433. [Google Scholar] [CrossRef]
  188. Saad, M.M.; Abo-Koura, H.A.; Bishara, M.M.; Gomaa, I.M. Microencapsulation: Toward the Reduction of the Salinity Stress Effect on Wheat Plants Using NPK Rhizobacteria. Biotechnol. J. Int. 2020, 1–18. [Google Scholar] [CrossRef] [Green Version]
  189. Zheng, Y.; Xu, Z.; Liu, H.; Liu, Y.; Zhou, Y.; Meng, C.; Ma, S.; Xie, Z.; Li, Y.; Zhang, C.-S. Patterns in the Microbial Community of Salt-Tolerant Plants and the Functional Genes Associated with Salt Stress Alleviation. Microbiol. Spectr. 2021, 9. [Google Scholar] [CrossRef]
Ijms 23 07036 g001 550
Figure 1. Isolation summary of PGPR (A) and PGPEB (B).
Figure 1. Isolation summary of PGPR (A) and PGPEB (B).
Ijms 23 07036 g001
Ijms 23 07036 g002 550
Figure 2. Mechanism of PGPR in salt stress alleviation. Black circles surrounding the roots represent the PGPR. Under salt stress, plants reduce transpiration and water loss by increasing K+ absorption and reducing Na+ absorption, thus alleviating osmotic stress and ion stress; PGPR promote plant growth by increasing nutrient absorption; meanwhile, PGPR regulate hormone production (IAA, GAs, CK, and ABA) and ACC deaminase activity to alleviate salt stress. Exopolysaccharides (EPSs) are homologous or heteropolysaccharides produced by rhizosphere bacteria. EPSs bind soil particles into aggregates to form a closed substrate that increases root adhesion to the soil (RAS/RT) in each root tissue, giving protection from environmental fluctuations. Protective EPS capsules have a strong water retention capacity, protecting plants from desiccation under salt stress, as well as help plants to absorb nutrients.
Figure 2. Mechanism of PGPR in salt stress alleviation. Black circles surrounding the roots represent the PGPR. Under salt stress, plants reduce transpiration and water loss by increasing K+ absorption and reducing Na+ absorption, thus alleviating osmotic stress and ion stress; PGPR promote plant growth by increasing nutrient absorption; meanwhile, PGPR regulate hormone production (IAA, GAs, CK, and ABA) and ACC deaminase activity to alleviate salt stress. Exopolysaccharides (EPSs) are homologous or heteropolysaccharides produced by rhizosphere bacteria. EPSs bind soil particles into aggregates to form a closed substrate that increases root adhesion to the soil (RAS/RT) in each root tissue, giving protection from environmental fluctuations. Protective EPS capsules have a strong water retention capacity, protecting plants from desiccation under salt stress, as well as help plants to absorb nutrients.
Ijms 23 07036 g002
Ijms 23 07036 g003 550
Figure 3. Mechanisms of PGPEB in salt stress alleviation. White dots represent the PGPEB in the plant. Under salt stress, endophytes coregulate the hormone balance, including increasing IAA and ABA contents and activating the ASA-GSH cycle, alleviating osmotic stress by increasing K+ and Na+ absorption, and alleviating oxidative stress.
Figure 3. Mechanisms of PGPEB in salt stress alleviation. White dots represent the PGPEB in the plant. Under salt stress, endophytes coregulate the hormone balance, including increasing IAA and ABA contents and activating the ASA-GSH cycle, alleviating osmotic stress by increasing K+ and Na+ absorption, and alleviating oxidative stress.
Ijms 23 07036 g003
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

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. https://doi.org/10.3390/ijms23137036

AMA Style

Gao Y, Zou H, Wang B, Yuan F. Progress and Applications of Plant Growth-Promoting Bacteria in Salt Tolerance of Crops. International Journal of Molecular Sciences. 2022; 23(13):7036. https://doi.org/10.3390/ijms23137036

Chicago/Turabian Style

Gao, Yaru, Hong Zou, Baoshan Wang, and Fang Yuan. 2022. "Progress and Applications of Plant Growth-Promoting Bacteria in Salt Tolerance of Crops" International Journal of Molecular Sciences 23, no. 13: 7036. https://doi.org/10.3390/ijms23137036

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop