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Review

Salt Stress Tolerance-Promoting Proteins and Metabolites under Plant-Bacteria-Salt Stress Tripartite Interactions

by
Ramasamy Krishnamoorthy
1,
Aritra Roy Choudhury
2,
Denver I. Walitang
3,4,
Rangasamy Anandham
5,
Murugaiyan Senthilkumar
6 and
Tongmin Sa
3,7,*
1
Department of Crop Management, Vanavarayar Institute of Agriculture, Pollachi 642103, Tamil Nadu, India
2
Bio-Evaluation Center, Korea Research Institute of Bioscience and Biotechnology, Cheongju 28116, Korea
3
Department of Environmental and Biological Chemistry, Chungbuk National University, Cheongju 28644, Korea
4
College of Agriculture, Fisheries and Forestry, Romblon State University, Romblon 5505, Philippines
5
Department of Agricultural Microbiology, Tamil Nadu Agricultural University, Coimbatore 641003, Tamil Nadu, India
6
Department of Crop Management, Agricultural College and Research Institute, Thanjavur 614902, Tamil Nadu, India
7
The Korean Academy of Science and Technology, Seongnam 13630, Korea
*
Author to whom correspondence should be addressed.
Appl. Sci. 2022, 12(6), 3126; https://0-doi-org.brum.beds.ac.uk/10.3390/app12063126
Submission received: 11 February 2022 / Revised: 11 March 2022 / Accepted: 15 March 2022 / Published: 18 March 2022
(This article belongs to the Special Issue Plant–Microorganism Interactions in Response to Salinized Soils)
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Abstract

:
The rapid increase in soil salinization has impacted agricultural output and poses a threat to food security. There is an urgent need to focus on improving soil fertility and agricultural yield, both of which are severely influenced by abiotic variables such as soil salinity and sodicity. Abiotic forces have rendered one-third of the overall land unproductive. Microbes are the primary answer to the majority of agricultural production’s above- and below-ground problems. In stressful conditions, proper communication between plants and beneficial microbes is critical for avoiding plant cell damage. Many chemical substances such as proteins and metabolites synthesized by bacteria and plants mediate communication and stress reduction. Metabolites such as amino acids, fatty acids, carbohydrates, vitamins, and lipids as well as proteins such as aquaporins and antioxidant enzymes play important roles in plant stress tolerance. Plant beneficial bacteria have an important role in stress reduction through protein and metabolite synthesis under salt stress. Proper genomic, proteomic and metabolomics characterization of proteins and metabolites’ roles in salt stress mitigation aids scientists in discovering a profitable avenue for increasing crop output. This review critically examines recent findings on proteins and metabolites produced during plant-bacteria interaction essential for the development of plant salt stress tolerance.

1. Introduction

One of the biggest abiotic factors impacting global agricultural productivity is salinity stress. Salt-induced conditions such as osmotic imbalance and ion toxicity when plants are exposed or grown in salt affected environments are referred to as salinity stress (syn: salt stress). By 2050, salt-affected regions are predicted to encompass about half of the total agricultural land [1]. Soil salinization refers to the excessive presence of soluble salt ions such as sodium, bicarbonate, magnesium, sulphate, potassium, chloride, calcium, and carbonate. Salinization is measured via the electrical conductivity (dS/m) of the soil [2]. When the electrical conductivity of the saturation extract (ECse) of the soil is 0–2, 2–4, 4–8, 8–16, and >16 dS/m, it is categorized as non, slightly, moderately, very, and extremely saline soil, respectively (USDA). One dS/m is approximately equal to 10mM of sodium chloride. The majority of cultivated plant species, particularly widely established horticultural and cereal crops, are glycophytes, which means they are sensitive to high concentrations of dissolved ions in the rhizosphere solution (e.g., >30 mM or >3.0 dSm−1). Soil salinization has a number of negative consequences to glycophytes including induced physiological and biochemical malfunctions, nutritional and different secondary (e.g., oxidative) disorders [3], as well as a reduced crop productivity, depending on salt concentration, exposure time, crop developmental stage, and environmental conditions (e.g., temperature, humidity, soil moisture, etc.). Soil salinization results in a combination of salt-induced multiple stresses cumulatively affecting plants. The reduced nutrient mobilization, hormonal instability, generation of reactive oxygen species (ROS), ionic toxicity, and osmotic stress all contribute to reduced plant development under salinity stress (Figure 1).
To solve the issue of excessive salinity, strategies such as conventional breeding, genetic engineering to create halotolerant transgenic plants, and chemical treatments are applied [4,5]. Such solutions, however, are not always viable, and some may even have further negative effects on the soil ecology. As a result, researching and implementing environmentally acceptable solutions to manage excessive salinity is critical for agricultural systems. Since salt stress mitigation is conferred by many complex pathways, altering a gene or a set of genes may not serve the purpose of stress alleviation. The use of plant growth-promoting bacteria (PGPB) to elicit mechanisms increasing plant tolerance to salt stress has emerged as a viable strategy for improving plant adaptability and resource-use efficiency in hostile settings [1,6,7]. Plants’ rhizospheres are home to a variety of microorganisms, some of which are capable of coping with salt stress. These halotolerant PGPB help plants to withstand saline environments through protein and metabolite production. The word “metabolites” refers to the low-molecular-weight (1000 Da) chemicals that play an important role in microbes and plant growth. PGPB produce a variety of proteins and metabolites such as ACC deaminase (ACCD), indole-3-acetic acid (IAA), antioxidants, extracellular polymeric substance (EPS), and volatile organic compounds (VOC) to mitigate salinity stress in plants. Several recent investigations have indicated that PGPB work as elicitors of salt tolerance and boost plant development [8,9]. This review focuses on recent findings on proteins and metabolites produced by bacteria and plants during plant-microbe interactions for salt stress mitigation.

2. Soil Salinity in Agricultural Systems, a Global Scenario

A major difficulty for global agriculture is meeting the food demands of an expanding worldwide population, which is now growing at a speed of 1.1% per year, according to world population projections 2021. By 2050, the population is predicted to reach 9.7 billion, representing a nearly 24% increase over 2020 [10]. At the moment, the world’s total agricultural land area is estimated to be 47.0 million square kilometers; 20% of this land is currently afflicted by salinity, and this figure is forecasted to rise to 50% by 2050 [1]. Around 20% of total farmed land is impacted by salinity, of which 85% is affected by high salt concentrations and 15% is suffering from severe to acute crop production constraints. According to an estimate, roughly 52 million hectares of land are affected by salt in South Asia [11]. The countries where major salinity problems exist include, but are not limited, to Australia, China, Egypt, India, Iran, Iraq, Mexico, Pakistan, Russia, Syria, Turkey, and the United States [12]. We are going to face major issues in food production in the near future. Regardless, by 2050, we will have a depreciating fertile land area to feed an exponentially growing population. This is a concerning situation in which scientists must focus more on preventing soil salinization and improving soil fertility for sustainable food production.

3. Soil Salinity in Changing Plant Metabolites and Proteins

Plant development can be hampered by salinity in the rhizosphere because roots cannot draw water from salt-accumulated soil. The other big issue is the high quantity of salt ions in the water, which has a negative impact on plant cells. The high osmotic potential of the soil solution and limitations in nutrient absorption are caused by the abundance of Na+ and Cl− ions in the soil [13]. The presence of large concentrations of Na+ and Cl− ions in the soil influences the availability of other key elements in the soil and can decrease the plant’s capacity to access and absorb necessary nutrients and minerals [14].
Plants develop a variety of salt tolerance mechanisms (Figure 1). Some examples include: (1) antioxidant enzyme production, (2) ion homeostasis, (3) polyamine formation, (4) biosynthesis of solutes and osmoprotectants, (5) nitric oxide generation, (6) ion uptake and transport, and (7) hormone regulation [15]. The plant’s natural salinity stress tolerance mechanisms are elaborately described by Gupta and Huang, [16] and Behera and Hembram [17] in their reviews. Plants, in general, have their own mechanisms for dealing with salt stress. However, many plants, especially agricultural crops, are salt sensitive and do not have highly effective salt tolerance mechanisms. Therefore, plants recruit helpful PGPB in their rhizosphere area and form beneficial plant-bacteria associations, producing metabolites in response to salt stress.

4. Plant-Bacteria Interaction Regulates Plant Protein and Metabolites Production

PGPB such as Achromobacter, Arthrobacter, Azotobacter, Azospirillum, Bacillus, Burkholderia, Enterobacter, Klebsiella, Microbacterium, Paenibacillus, Pantoea, Pseudomonas, Serratia, and Streptomyces occupy the rhizosphere region of many plants. Plant beneficial bacteria may promote plant development through a variety of ways, including increased root and shoot growth via the synthesis of various phytohormones such as auxins and cytokinins, improvement of nutrient uptake, and protection from harmful pathogens [18]. To counteract salt stress, plants create primary and secondary metabolites; in addition, the participation of bacteria in enhancing plant metabolite synthesis is equally important. The bacterial-mediated pathways involved in plant salt stress mitigation are described in detail below. We divided salt stress mitigating features into two categories: direct mechanisms or bacterial metabolites (ACC deaminase, EPS, and phytohormone production) involvement in protecting the plants and indirect mechanisms or bacterial mediated metabolites modifications in plants.

4.1. Bacterial Proteins and Metabolites in Plant Stress Mitigation (Direct Mechanism)

4.1.1. ACC Deaminase

Ethylene is a gaseous hormone that is produced by plants and, in certain cases, microorganisms. At lower concentrations, ethylene promotes seed germination, root elongation, and flowering [19]. However, under stress conditions, ethylene synthesis in plants increases, which has a negative impact on plant growth. S-adenosyl-methionine (SAM), derived from the methionine amino acid, is the main substrate in the ethylene biosynthesis pathway. The ACC synthase enzyme catalyzes the synthesis of 1-aminocyclopropane-1-carboxylic acid (ACC) from SAM, and the ACC oxidase enzyme catalyzes the conversion of ACC to ethylene [20]. The production of ACC deaminase by bacteria aids in the reduction of stress ethylene by cleaving ACC into ammonia and alpha keto butyrate [21,22] (Figure 2A). Another benefit of this ACC deaminase is that it eliminates IAA feedback inhibition produced by increased ethylene synthesis in plants. Glick and colleagues investigated this enzyme and discovered that ACC deaminase is an inducible enzyme whose synthesis is encouraged by its substrate, ACC. This enzyme is found in the bacterial cytoplasm (it is not secreted), importantly, ACC deaminase-producing bacteria (rhizospheric, endophytic, or epiphytic) can modulate ACC concentrations in the rhizosphere and phyllosphere by consuming plant exuded ACC, or within plant tissues (e.g., the endosphere and root nodules), thereby directly limiting the actions of ACC and, as a result, limiting ethylene production [23]. Glick et al. [24] developed a scenario for the operation of bacterial ACC deaminase in which a considerable amount of ACC is secreted from plant roots or seeds, taken up by soil microorganisms, and hydrolyzed to ammonia and alpha-ketobutyrate. ACC absorption and hydrolysis reduce the quantity of ACC found outside the plant roots. Furthermore, by exuding more ACC into the rhizosphere, the balance between the internal and external ACC levels is maintained (Figure 2A).
In one of our studies, we have isolated halotolerant ACC-deaminase producing bacteria from the rhizosphere of halophytic plants near the Yellow Sea in saline media (850 mM NaCl) [25]. Brevibacterium linens RS16, a promising isolate, alleviated salt stress in rice and red pepper plants [26,27,28]. Using Pseudomonas sp. with ACC deaminase generating ability, we were also able to reduce salt stress ethylene in red pepper [29,30]. Liu et al. [31] demonstrated the role of ACC deaminase in lowering stress ethylene production in tomato plants by developing a Pseudomonas azotoformans CHB 1107 ACC deaminase gene (acdS) positive mutant. The ACC deaminase producing halotolerant Glutamicibacter sp. YD01 reduced stress ethylene production in rice seedlings grown up to 200 mM of salt stress [32]. Another evidence showed that ACC deaminase enzyme producing Streptomyces sp. GMKU 336 down-regulated the ACC oxidase (ACO1) and the ethylene responsive element binding protein (EREBP1) genes in rice plants grown at 150 mM of salt stress [33].

4.1.2. Extracellular Polymeric Substance (EPS)

EPS are polymers that microorganisms biosynthesize. It is composed of polysaccharides, proteins, and DNA, and its synthesis is predominantly prompted by environmental signals [34]. Since the carboxyl and hydroxyl functional groups predominate in varying amounts depending on EPS composition, the majority of the examined EPS are negatively charged [35]. The key elements influencing biosorption of other ions are connected to the binding sites or their chemical nature, such as pH, metal content, ionic strength, surface characteristics, EPS molecular weight, and branching degree [36]. EPS binds with sodium ions, minimizing the consequences of high soil salinity, while EPS produced by bacteria reduces salt stress by maintaining a Na+/K+ equilibrium, allowing plants to thrive under unfavorable soil conditions (Figure 2B) [37].
A rise in salt concentration also drives an increase in bacterial EPS synthesis, which leads to the formation of biofilms and the strengthening of Na+ chelation [38]. In line with this, Kasotia et al. [39] revealed that in salt-tolerant Pseudomonas spp., EPS increased with increasing NaCl concentration (up to 500 mM). In comparison to sodium ion absorption by root, potassium ion uptake was increased (up to 65%) in soybean plants grown under salt stress conditions. Inoculation with EPS producing Bacillus aryabhattai ALT29 and Arthrobacter woluwensis ALT43, on the other hand, increased K+ ion absorption up to 67% as compared to the control plant [40]. Planococcus rifietoensis RT4 produced EPS and biofilm which alleviated salinity stress in Cicer arietinum plants cultivated in 200mM salt stress [41].

4.1.3. Bacteria-Derived Phytohormones

Plant hormones are classified into several types, including indole acetic acid (IAA), gibberellins (GA), cytokinins (CK), abscisic acid (ABA), ethylene, and the cofactor pyrroloquinoline quinone (PQQ) [42]. It is widely established that the use of PGPB promotes plant development and makes plants more resistant to salt stress by enhancing physiological response through the involvement of various growth promoting metabolites. Under salt stress, IAA generated by halotolerant and halophilic plant growth promoting rhizobacteria (PGPR) boosted root and branch length and total fresh weight of wheat plants [43]. Microorganism-produced phytohormones promote root biomass and root surface development, allowing plants to absorb more nutrients from saline soil (Figure 2C). The endophytic bacteria Curtobacterium sp. SAK1 increased soybean salinity stress resistance by producing IAA and ABA under 300 mM salt stress [44]. Recently, it was discovered that the IAA producing Bacillus velezensis FMH2 increased plant root length and lateral root production that improved tomato salinity tolerance [45]. To alleviate salt stress (100 mM), a halotolerant IAA generating Nocardioides sp. NIMMe6 was employed as a seed priming agent for the wheat crop. The researchers utilized Nocardioides sp. NIMMe6 and a phytohormone-rich bacterial culture filtrate extract that was discovered to boost wheat plant salinity tolerance [46]. Phytohormones such as IAA and ABA produced by Arthrobacter woluwensis AK1 increased the expression of stress-resistance genes (GmST1 and GmLAX3) in soybean plants cultivated under 300 mM NaCl [47]. In addition to the direct methods, some microbial osmolytes are directly engaged in the reduction of salt stress. A study using Pseudomonas sp. UW4 trehalose gene overexpressing mutant, improved salt stress tolerance in tomato plants cultivated in 800 mM NaCl [48].

4.2. Bacteria-Mediated Plant Metabolite Biosynthesis for Salt Stress Mitigation (Indirect Mechanism)

4.2.1. Osmolyte Synthesis in Plant

Osmolytes are osmoprotectant solutes that improve the cell’s ability to retain water without interfering with regular metabolism. The primary function of these organic metabolites is to control osmotic adjustment. These osmotic solutes or osmoprotectants aid plants in withstanding extreme osmotic stress throughout the plant’s life cycle [49].
These substances help to maintain the osmotic differences that exist between the cell’s surroundings and the cytoplasm. Osmolytes are neutral substances that protect proteins and other cell membranes from different stress events that affect cellular metabolism. Proline, sucrose, polyols, trehalose, glycine betaine (GB), and alanine betaine are among the metabolites. Bacillus fortis SSB21 inoculation altered proline levels and increased the expression of stress-related genes such as CAPIP2, CaKR1, CaOSM1, and CAChi2 in plants [50]. Salt stress-induced proline buildup was observed to be considerably higher in salt challenged (300 mM) Sulla carnosa plants that were inoculated with either Acinetobacter sp. B3, Pseudomonas putida Br18, or Curtobacterium sp. Br20 bioinoculants compared to uninoculated plants [51]. Inoculation of salt-stressed soybean plants with Bacillus firmus SW5 increased proline levels by up to 23.1% [52]. Notably, the proline synthesis gene (P5CS1) expression was dramatically up-regulated in Enterobacter sp. EJ01-infected plants under stressful conditions [53]. Details about bacterial mediated modification of plant stress related genes and their impact on plants are given in Table 1.
Trehalose, a non-reducing disaccharide, is a key osmoprotectant for osmotic adjustment in stressed plants. It is not only a source of energy during desiccation, but also an effective stabilizer for dehydrated enzymes, proteins, and lipid membranes, as well as other biological structures. The use of trehalose was found to increase the antioxidant enzyme activity in Arabidopsis sp. seedlings grown in 250 mM salt stress [54]. One of our elite strains, Brevibacterium linens RS16, alleviated salt stress (150 mM) by mediating the accumulation of osmolytes such as proline and glycine betaine in rice plant cells [55].

4.2.2. Phytohormones Production in Plant

Plant hormones, commonly referred to as phytohormones, are a class of naturally occurring chemical compounds that regulate plant physiological processes at low concentrations. These hormones influence plant growth differentiation and development by regulating a variety of processes. ABA regulates water relations not only by decreasing transpiration via ABA-induced stomatal closure but also by promoting water flow via ABA-induced increase in activity of water channel aquaporins [67]. Salt stress reduces the availability of water, resulting in decreased bulk and relative water content in plants. Bacillus subtilis IB22 treatment was found to increase root ABA content and reduced shoot ABA accumulation by up regulating (HvNCED2) and down-regulating ABA catabolic genes (HvCYP707A1) in barley grown under 100mM salt concentration [56]. Volatile organic compounds (VOCs) released by B. subtilis GB03 can activate phytohormone signaling in Arabidopsis thaliana, producing auxin, cytokinins, salicylic acid, and gibberellins [68].

4.2.3. Antioxidant Property in Plant

Increased salinity causes the generation of reactive oxygen species (ROS) such as superoxide radical (O2-), hydroxyl radical (OH-), and hydrogen peroxide (H2O2) in plants [69]. The primary cause of ROS generation is the over-reduction of photosynthetic electrons caused by decreased photosynthetic activity [70]. Enzymatic antioxidants such as catalase (CAT), superoxide dismutase (SOD), ascorbate peroxidase (APX), glutathione reductase (GR) and non-enzymatic antioxidants such as flavonoids, carotenoids, glutathione, and tocopherols are involved in the detoxification of ROS compounds [71] (Figure 3). Most of the non-enzymatic antioxidants are produced in the secondary metabolic processes [72]. The CAT and APX enzymes detoxify hydrogen peroxide by converting hydrogen peroxide (H2O2) to H2O and O2, and they are essential for ROS detoxification. When compared to salt-stressed soybean plants, peroxidase (POD) and polyphenol oxidase (PPO) concentrations were considerably increased in Bacillus aryabhattai ALT29 and Arthrobacter woluwensis ALT43-inoculated soybean plants (21–68%) [40].
The antioxidant enzyme system was discovered to be increased in Paenibacillus yonginensis DCY84 treated Panax ginseng plant grown in 300 mM salt concentration compared to control plants [60]. Ascorbate peroxidase 2 is an enzyme that converts the reactive oxygen species H2O2 to H2O via ascorbate oxidation [73]. Inoculation of Burkholderia phytofirmans PsJN in Arabidopsis thaliana enhanced the accumulation of the ascorbate peroxidase 2 enzyme at 250mM of salt stress [64]. Similarly, inoculation of Enterobacter sp. EJ01 was found to increase the ascorbate peroxidase enzyme in tomato plants in order to mitigate salt stress [53]. Another study found that employing Bacillus firmus SW5 improved the activity of antioxidant enzymes (APX, CAT, SOD, and POD) in soybeans by up to 48% [52]. Their findings revealed that during salt stress, Bacillus firmus SW5 elevated the antioxidant synthesizing genes up to three times more than control plants. Koccuria rhizophila 14asp inoculated plants exposed to salinity have stronger antioxidant (SOD and CAT) activities that increased as the salt concentration increases compared to uninoculated plants [59]. Nocardioides sp. NIMMe6 and a phytohormone-rich bacterial culture filtrate extract in wheat plants up-regulated the genes involved in CAT, Mn-dependent superoxide dismutase (MnSOD), POD, and APX enzyme synthesis under salt stress condition [46]. According to El-Esawi et al. [61], the application of Serratia liquefaciens KM4 reduces maize salt stress by up-regulating genes involved in the synthesis of antioxidant enzymes. By inducing the accumulation of antioxidant enzymes (ascorbate peroxidase, superoxide dismutase, and catalase), our psychrotolerant Pseudomonas frederiksbergensis OS261 strain reduced salt stress in red pepper plants [74].

4.2.4. Plant Aquaporin

Aquaporin (AQP) proteins have been demonstrated to transport water and other tiny molecules across biological membranes, which is critical for plants dealing with salt stress (Figure 3). Higher plant aquaporins are members of a large gene family of major intrinsic proteins that are categorized into 5 subfamilies based on amino acid sequence similarity: plasma membrane intrinsic proteins (PIPs), tonoplast intrinsic proteins (TIPs), nodulin-26-like intrinsic proteins (NIPs), small basic intrinsic proteins (SIPs), and uncharacterized intrinsic proteins (XIPs). Aquaporin, also known as plasma membrane integral protein (PIP), is the principal channel that mediates water uptake into plant cells. In plants, PIPs are the most prevalent subfamily. PIP1 and PIP2 are the two primary categories of the PIP family. According to Marulanda et al. [66], salt stress impacted maize plant aquaporin genes (ZmPIP1s and ZmPIP2s) were up-regulated after Bacillus megaterium inoculation (Table 1). The PIP2s are all involved in fast water transfer. The ZmPIP2-1 gene was found to be strongly up-regulated in maize roots inoculated with Pantoea agglomerans in salt stress condition, followed by ZmPIP1-1 and ZmPIP2-5 [65].

4.2.5. Sodium and Potassium Transport in Plant Cell

Arabidopsis K+ Transporter 1 (AKT1) is a potassium plasma membrane transporter that participates in root K+ absorption at extracellular concentrations greater than 10 µM (Figure 3). The AKT1 gene was shown to be highly up-regulated in plants infected with Burkholderia phytofirmans PsJN and subjected to 250 mM salt stress [64]. Recently Kocuria rhizophila 14 asp inoculation decreased sodium uptake and increased potassium transport in roots of pea grown in 150mM salt concentration [59]. In line with this, another study utilizing Bacillus velezensis FMH2 demonstrated that it reduced sodium buildup in root and shoot and enhanced potassium uptake in tomato plants cultivated in 171 mM salt stress [45].
Under saline circumstances, the toxicity of Na+ might be reduced in plant cells by a variety of methods, including restricting Na+ absorption, translocating Na+ from the xylem stream to the root system, sequestering Na+ in vacuoles, and exporting it out of cells. Na+/H+ antiporters (NHX1 and NHX7) and ion balance regulators (H+-PPase and HKT1) regulate Na+ sequestration, export, and recirculation. El-Esawi et al. [61] discovered that Serratia liquefaciens KM4 inoculation significantly reduced plant Na+ and Cl− accumulation and increased the expression of NHX1, H+-PPase, and HKT1 genes in maize under control and saline conditions, implying that Serratia liquefaciens KM4 helps in reducing toxic ion accumulation by sequestering them in plant vacuoles (Figure 3).

4.2.6. Salt Overly Sensitive (SOS) Pathway in Plant

The SOS signalling system, which includes SOS3, SOS2, and SOS1, has been postulated to mediate cellular signalling under salt stress in order to maintain ion homeostasis. SOS1 is one of many plasma membrane Na+/H+ antiporters involved in salt tolerance, and it is essential for regulating long-distance Na+ transport from root to shoot. SOS3 encodes a pyridoxal kinase that is involved in the production of pyridoxal-5-phosphate, which is a cofactor for many cellular processes. SOS3 regulates Na+ and K+ homeostasis by altering ion transporter activity (Figure 3). It has also been proposed that SOS3 performs a specific role in Arabidopsis root hair development. A study conducted by Bharti et al. [63] showed an increase in SOS1 and SOS3 expression levels in roots of wheat grown under salt stress. Similarly, inoculation of Azotobacter chroococcum 76A up-regulated the SOS signaling pathway and mitigated salt stress in tomato plants [75].

4.2.7. Hopanoids: Recent Frontier in Bacteria-Mediated Stress Mitigation

Hopanoids are a class of sterol-like lipids found in bacteria, archaea, and plants that help to maintain membrane stiffness under a variety of stress circumstances [76,77]. Bacterial hopanoids have been investigated intensively over the last five decades, and they’ve lately been discovered to be a key role in bacteria-microbe interactions [76,77,78]. Environmental stressors, such as changes in the extracellular milieu’s osmolarity, can cause increased hopanoid production, which provides stiffness to the bacterial membrane [79]. In agro-ecosystems, the majority of research has found a link between hopanoid production and nitrogen fixation [77]. Bradyrhizobium sp. is an example of a rhizobial species. When higher hopanoids are generated, nodule-forming bacterial strains symbiotically associated with legumes have been observed to fix increased atmospheric nitrogen [80]. Bacterial strains that synthesize hopanoid include Anabaena sp. Azotobacter sp., Beijerinckia sp., Burkholderia sp., Frankia sp., and Nostoc sp. are among the bacteria that have been identified and are capable of fixing nitrogen from the atmosphere [80,81,82].
Recent omics-based research has linked particular hopanoids, such as hpnP and shc, to methanol use in bacterial strains [83]. A particular bacterial genus Methylobacterium spp. are well-known plant-associated bacteria that can colonize the plant endosphere and use methanol as their primary carbon source [84]. Methylobacterium sp. has been shown to improve plant growth and stress tolerance in a variety of plant species under a variety of environmental circumstances [85,86,87,88,89]. The genome sequencing data of Methylobacterium oryzae CBMB20, a well-known plant growth-promoting endophytic bacteria responsible for reducing salt stress in plants [22,89], identified two distinct gene sequences, HpnK (WP 003601714.1) and HpnJ (WP 012317976.1). The functions of these newly discovered hopanoid genes in plant-bacteria interactions or stress mitigation mechanisms have yet to be determined. As a result, more research is needed to fully comprehend the role of hopanoids in plant growth promotion and salt stress mitigation, which will open up a new frontier in plant-bacterial interaction.

5. Conclusions and Future Prospects

The response of plants to salinity stress is highly complicated and occurs from the cellular to the whole plant level, including transcription, post-transcription, translation, and post-translation processes. Plants’ morphological and anatomical features adapt as a result of changes in metabolic processes in order to tolerate the stress environment. The study of intercellular and intracellular molecular interactions during salinity stress responses, as well as how plants can successfully adapt to salt stress, should be prioritized in the future. If a single candidate gene/candidate metabolite responsible for salt stress mitigation in plants is identified, it will be more valuable in future research. This can be achieved only when we have sufficient knowledge regarding signaling molecules involved in plant-bacterial interaction and cracking the genomic and metabolomics of plants grown in salt stress condition.

Author Contributions

Conceptualization, R.K. and T.S.; validation, R.A. and M.S.; resources, R.K., A.R.C. and M.S.; writing, original draft preparation, R.K., R.A.; and T.S.; writing, review and editing, A.R.C., D.I.W. and T.S.; supervision, T.S.; funding acquisition, T.S. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Basic Science Research Program, National Research Foundation of Korea (NRF), Ministry of Education, Science and Technology [2021R1A2C1006608], Republic of Korea.

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.

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Applsci 12 03126 g001 550
Figure 1. Effects of salt stress on plant characteristics and the plant’s innate stress-response system. ABA—Abscisic Acid; SOD—Superoxide Dismutase; CAT—Catalase; GPX—Glutathione Peroxidases; APX—Ascorbate Peroxidase.
Figure 1. Effects of salt stress on plant characteristics and the plant’s innate stress-response system. ABA—Abscisic Acid; SOD—Superoxide Dismutase; CAT—Catalase; GPX—Glutathione Peroxidases; APX—Ascorbate Peroxidase.
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Figure 2. Bacterial metabolite mediated mechanism for minimizing salt stress in order to boost plant growth and development. (A) The ACC deaminase enzyme, (B) EPS production, and (C) Phytohormones production. SAM (S-adenosyl-L-methionine); ACC (1-Aminocyclopropane-1-Carboxylic Acid); EPS (Extracellular Polymeric Substances). Top plane of (B,C) are without bacterial cell and bottom plane is with bacterial cells.
Figure 2. Bacterial metabolite mediated mechanism for minimizing salt stress in order to boost plant growth and development. (A) The ACC deaminase enzyme, (B) EPS production, and (C) Phytohormones production. SAM (S-adenosyl-L-methionine); ACC (1-Aminocyclopropane-1-Carboxylic Acid); EPS (Extracellular Polymeric Substances). Top plane of (B,C) are without bacterial cell and bottom plane is with bacterial cells.
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Figure 3. Bacterial mediated plant processes for reducing salt stress, thereby boosting plant growth and development. Rhizosphere and phyllosphere bacteria involved in stress mitigation. Compounds in bold and underlined (pink colored) are up-regulated during plant-bacteria interactions in salt stress mitigation. TCA cycle (tricarboxylic acid cycle); ETC (electron transport chain); IAA (indole acetic acid); ABA (abscisic acid); CAT (catalase); SOD (superoxide dismutase); APX (ascorbate peroxidase); POD (peroxidase); VOCs (volatile organic compounds); SOS (salt overly sensitive).
Figure 3. Bacterial mediated plant processes for reducing salt stress, thereby boosting plant growth and development. Rhizosphere and phyllosphere bacteria involved in stress mitigation. Compounds in bold and underlined (pink colored) are up-regulated during plant-bacteria interactions in salt stress mitigation. TCA cycle (tricarboxylic acid cycle); ETC (electron transport chain); IAA (indole acetic acid); ABA (abscisic acid); CAT (catalase); SOD (superoxide dismutase); APX (ascorbate peroxidase); POD (peroxidase); VOCs (volatile organic compounds); SOS (salt overly sensitive).
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Table
Table 1. Various metabolites produced by plant growth promoting bacteria in increasing the salt stress mitigation and growth of various plants/crops.
Table 1. Various metabolites produced by plant growth promoting bacteria in increasing the salt stress mitigation and growth of various plants/crops.
CropSalinity LevelMicroorganism UsedMetabolites/Process InvolvedGeneImpact on PlantReference
Solanum lycopersicum0–60 mMPseudomonas azotoformans CHB 1107Proline and ethyleneacdSReduced stress and increased nutrient uptake[31]
Hordeum vulgare0–100 mMBacillus subtilis
IB22		ABAHvNCED2Regulated stomata opening and increased plant growth[56]
Triticum aestivum0–100 mMNocardioides sp. NIMMe6Antioxidant geneCAT, APX, MnSOD
and POD		Seedling growth increased [46]
Solanum lycopersicum0–800 mMPseudomonas sp. UW4Trehalose over-expressingtreSIncreased trehalose accumulation and plant growth[48]
Arabidopsis thaliana0–250 mMArthrobacter
endophyticus SYSU 333322		Root cortical cell growth, Auxin transportAT5G44610
AT1G16510		Salinity tolerance[57]
Triticum aestivum0–200 mMArthrobacter
nitroguajacolicus		Ion homeostasisKT1, HKT1, NHX2, and SOS1Plant growth improvement and stress mitigation[58]
Glycine max0–300 mMArthrobacter woluwensis AK1IAA and ABAGmST1, GmLAX3Up-regulated stress responsive gene[59]
Panax ginseng0–300 mMPaenibacillus yonginensis DCY84Antioxidant enzymesPgAPX and PgCATIncreased carotenoid and
reduced ROS accumulation 		[60]
Glycine
max		0–80 mMBacillus firmus SW5Antioxidant enzyme-encoding genes up regulation APX, CAT, POD, Fe-SODosmolytes levels, total phenolic and flavonoid and
antioxidant enzymes activities		[52]
Zea mays0–160 mMSerratia liquefaciens KM4Stress-related genesAPX, CAT,
SOD, H+-PPase, HKT1, and NHX1		Increased Plant growth, potassium accumulation [61]
Capsicum annum0–50 mMBacillus fortis SSB21ProlineCAPIP2
CAOSM1		Alleviate oxidative stress[50]
Oryza sativa0–150 mMStreptomyces
sp. GMKU 336		ACC deaminase ACO1 and EREBP1 genesReduced ethylene accumulation in plant[33]
Arabidopsis thaliana0–100 mMBacillus
amyloliquefaciens FZB42		Glutathione-S-transferase
peroxidases
redox, proline		AT1G49570
P5CS1
Fresh and dry biomass increase[62]
Triticum aestivum0–150 mMDietzia natronolimnaeaSOS pathwaySOS1 and SOS3Improved stress tolerance[63]
Arabidopsis thaliana0–250 mMBurkholderia phytofirmans PsJN.Potassium transportAKT1Reduced sodium toxicity in cell[64]
Zea mays600–1000 mMPantoea agglomeransAquaporinZmPIP, PIP2-1Improved water uptake and seedling biomass[65]
Arabidopsis thaliana and Solanum lycopersicum0–200 mMEnterobacter sp. EJ01Proline biosynthesis P5CS1 and P5CS2Reduced stress and improved plant growth[53]
Zea mays0–150 mMBacillus megateriumAquaporinZmPIP1s ZmPIP2sImproved water uptake[66]
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Krishnamoorthy, R.; Roy Choudhury, A.; Walitang, D.I.; Anandham, R.; Senthilkumar, M.; Sa, T. Salt Stress Tolerance-Promoting Proteins and Metabolites under Plant-Bacteria-Salt Stress Tripartite Interactions. Appl. Sci. 2022, 12, 3126. https://0-doi-org.brum.beds.ac.uk/10.3390/app12063126

AMA Style

Krishnamoorthy R, Roy Choudhury A, Walitang DI, Anandham R, Senthilkumar M, Sa T. Salt Stress Tolerance-Promoting Proteins and Metabolites under Plant-Bacteria-Salt Stress Tripartite Interactions. Applied Sciences. 2022; 12(6):3126. https://0-doi-org.brum.beds.ac.uk/10.3390/app12063126

Chicago/Turabian Style

Krishnamoorthy, Ramasamy, Aritra Roy Choudhury, Denver I. Walitang, Rangasamy Anandham, Murugaiyan Senthilkumar, and Tongmin Sa. 2022. "Salt Stress Tolerance-Promoting Proteins and Metabolites under Plant-Bacteria-Salt Stress Tripartite Interactions" Applied Sciences 12, no. 6: 3126. https://0-doi-org.brum.beds.ac.uk/10.3390/app12063126

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