Prachi Sharma* and Ratul Baishya

Phosphate Solubilizing Bacteria-Assisted Salinity Tolerance in Plants: A Review

Department of Botany, University of Delhi-110007Email: prachisharma.du@gmail.com

Soil salinization is a major threat to crop yields especially in countries where irrigation is an essential aid in agriculture. Land degradation due to salinity is increasing day by day and hence becomes the greatest threat to agricultural sustainability. Salinity stress reduces the crop productivity as the plant suffers from high osmotic stress, nutritional imbalance, and toxicities. A wide range of mitigation strategies is required to cope with this problem. Efficient breeding programs, interspecific hybridization, and transgenic plants have met with very limited success, moreover, these strategies are long drawn and cost intensive. Therefore, there is a need to find low- cost biological methods for salinity stress management which could be exploited without hampering the sustainability issues and environmental ethics. In this respect, phosphate solubilizing bacteria seems to be a promising tool in the alleviation of salinity stress in plants. This review focuses mainly on various mechanisms like phosphate solubilization, siderophore production, production of ACC deaminase etc. by which the phosphate solubilizing bacteria enhances the overall performance of plants under salinity stress.

There are two ways in which the salt stress affects the plant growth. Firstly it becomes difficult for the plant roots to extract water from salt-affected soils and therefore, high salt concentration is toxic to the plant in many ways. Secondly, the growth and metabolism of the root cells which are in direct contact with toxic levels of salt are highly affected (Munns and Tester 2008). It affects irrigated land in areas with scarce water, high temperature, high evapotranspiration, or when farmers practice poor irrigation management. Salinity stress reduces the photosynthetic ability of the plants, causes

Soil salinity is a major environmental stress that limits agricultural productivity by adversely affecting the plant growth and development. As the world population is increasing day by day, there is an immense need to increase the area under cultivation to feed the growing population. But the degradation of land by soil salinization is the major threat which is posing a problem in increasing land under cultivation. Over 800 million hectares of land throughout the world are salt-affected, either by salinity or the associated conditions of sodicity. The increasing population and soil salinity are together going to affect the availability of water resources for agriculture purposes, hence, going to increase constraints to plant growth and survival and therefore, reducing the crop yield potential (Chaves et al. 2002, 2003). It has been estimated that worldwide 20% of total cultivated and 33% of irrigated agricultural lands are afflicted by high salinity. Furthermore, the salinized areas are increasing at a rate of 10% annually for various reasons, including low precipitation, high surface evaporation, weathering of native rocks, irrigation with saline water, and poor cultural practices. It has been estimated that more than 50% of the arable land would be salinized by the year 2050 (Srivastava and Kumar 2015).

destabilization of the membrane and nutrient imbalance in plants. The plants are adversely affected by the salt stress as they suffer from the reduction in the osmotic potential of the soil solution, nutritional imbalance, ion imbalance or a combination of these factors. The major physiological phenomenon like photosynthesis, protein content, energy and lipid metabolisms are highly affected in the plants which are suffering from salinity stress. A large amount of reduction in the rate of leaf surface expansion can be seen as an early response of the plant towards salinity, followed by cessation of the expansion as the stress increases but when the stress is reduced, the growth of the plant resumes (Parida and Das 2005). A saline soil is generally defined as one in which the electrical conductivity of the saturation extract (ECe) in the root zone exceeds 4 dS m-1 (approximately 40 mM NaCl) at 25°C and has an exchangeable sodium of 15%. The yield of most crop plants is reduced at this level of electrical conductivity, though many crops exhibit yield reduction at lower ECe (Munns 2005; Jamil et al. 2011). It has been estimated that more than 50% of the arable land would be salinized by the year 2050 (Munns and Tester 2008). Therefore, salinity is a serious environmental problem that causes osmotic stress and reduction in plant growth and crop productivity worldwide. Specific ion effects may cause direct toxicity or alternatively, the insolubility or competitive absorption of ions may affect the nutritional balance in

+plants. Salinity has shown to increase the uptake of Na 2+ +

or decrease the uptake of Ca and K . Accumulation of +excess Na may cause metabolic disturbances in

+ + 2+processes where low Na and high K or Ca are required for optimum function. The nitrate reductase activity in the stressed plant can be disrupted by the uptake and

-1accumulation of Cl ions which will further go to affect

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the photosynthetic ability of the plants (Patel et al. 2011). The salt tolerance trait is complex both genetically and physiologically and hence, several approaches like conventional breeding programs, interspecific hybridization and use of transgenic plants to improve the salt tolerance of the plants were of limited success (Flowers 2004). One approach to solving the salt stress problem is the use of plant growth-promoting bacteria (PGPB). Many Gram-positive and -negative Phosphate solubilizing bacteria have been reported to colonize the plant rhizosphere and confer beneficial effects by various direct and indirect mechanisms like the production of exopolysaccharide, indole-3-acetic acids (IAA) and aminocyclopropane-1-carboxylate (ACC) deaminase (Nakbanpote et al. 2013). Therefore, in addition to the use of traditional breeding and transgenic plants, the exploitation of phosphate solubilizing bacteria has been proven to be a useful and cost-effective strategy to facilitate plant growth in saline soils (Tank and Saraf 2010).

PHOSPHORUS AS AN ESSENTIAL MACRO-NUTRIENT

Phosphorus (P) is one of the major essential macronutrients for plant growth and development. It is present at levels of 400–1,200 mg per kg of soil (Hayat et al. 2010). Phosphorus exists in two forms in soil, as organic and inorganic phosphates. Plants require an optimum amount of available phosphorus to support their growth and development. Phosphorus is known to have a significant role in root subdivision, vitality and disease resistance of plants. Phosphorus is an essential macronutrient in soil but presents in a very low concentration in available form. Iron, calcium, and aluminum rapidly immobilize inorganic available phosphorus and convert it into the unavailable form of tricalcium phosphate, iron phosphate, and aluminum phosphate. About 20% of soil phosphorus occurs in organic form and the general concentration of available phosphorus exists about 2 mM and rarely exceeds 10 mM. A minimum of the 5-20mM concentration of available phosphorus is required by the plants for the healthy growth and development. So, to provide sufficient amount of phosphorus and to combat phosphorus deficiency in plants, certain chemical fertilizers are added but this approach adversely affects the soil quality. Numerous microbes, especially bacteria, are potential solubilizers of phosphorus and used as biofertilizers in agricultural lands (Shrivastava et al. 2017). In addition, it has a very limited bioavailability to growing plants due to the high reactivity of phosphate ions in soils. To circumvent this deficiency, phosphatic fertilizers are applied in soils. But most of the applied Phosphorus in the forms of fertilizers is precipitated and therefore, a very small fraction is available for absorption by plants. Although phosphorus is abundant in soils in both organic and inorganic forms, it is frequently a major or even the prime limiting factor for

plant growth. There are three factors which affect the availability of soil inorganic phosphorus in the rhizosphere, which is: plant species, nutritional status of the soil and ambient soil conditions. To combat the phosphorus deficiency condition in plants, phosphate-solubilizing bacteria could play an important role in supplying phosphate to plants in a more environmental-friendly and sustainable manner (Khan et al. 2007).

PHOSPHATE SOLUBILIZING BACTERIA

A group of soil microorganisms capable of transforming insoluble Phosphorus into soluble and plant accessible forms across different genera, co l l ec t ive ly ca l l ed phospha te - so lub i l i z ing microorganisms, which have been found as a best eco-friendly option for providing inexpensive phosphorus to the plants. Plant yields can be improved to a large extent by exploiting the property of certain phosphate solubilizing bacteria, of converting insoluble forms of phosphorus into available form for increasing plant yields. The use of phosphate solubilizing bacteria as inoculants increases the Phosphorus uptake by plants. The concentration of soluble Phosphorus in soil is usually very low, normally at levels of 1 ppm or less (Goldstein 1994, 1995). The plant takes up several Phosphorus forms but the major part is absorbed in the forms of orthophosphates. There are several benefits to plants from phosphate solubilizing bacteria which include an increase in seed germination rate, root growth, yield, leaf area, chlorophyll content, nutrient uptake, protein content, hydraulic activity, tolerance to abiotic stress, shoot and root weights, bio control, and delayed senescence (Adesemoye and Kloepper 2009). Other beneficial effects of phosphate solubilizing bacteria include enhancing phosphorus availability, sequestering iron for plants by production of siderophores, producing plant hormones such as gibberellins, cytokinins, and auxins; and synthesizing the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase, which lowers plant levels of ethylene, thereby reducing environmental stress on plants (Glick et al. 2007; Adesemoye and Kloepper 2009). Salt stress suppresses the phosphorus uptake by plant roots and reduces the available phosphorus by sorption processes and low solubility of Ca-P minerals. Since phosphorus is one of the major macronutrients which is reducing plant growth and development. Numerous heterotrophic bacteria have the ability of solubilizing insoluble phosphate and thus, provide sufficient amount of phosphorus to the plants. In fact, the ability of heterotrophic bacteria to solubilize insoluble phosphate is well documented (New et al. 2013). Phosphate solubilizing bacteria can protect plants from deleterious effects of environmental stress like flooding, drought, salinity, heavy metals, and so on, by enhancing the growth of the plant through the production of organic acids which will solubilize the inorganic

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phosphates, cell wall degrading enzymes like chitinase, antibiotics, hydrogen cyanide and siderophores. All these factors have led to an increase in seedling emergence, vigor, and yield in many plant species (Patel et al. 2011). The elaborate picture of all the mechanisms influencing plant growth by phosphate solubilizing bacteria is shown in Fig. 1.

Phosphate solubilization by the production of organic acids – Generally, phosphate solubilizing bacteria releases low molecular weight organic acids, which is accepted as a major mechanism of phosphate solubilization (Goldstein 1995) in which they chelate the cations bound to phosphate through their hydroxyl and carboxyl groups, thereby converting it into soluble forms. Nutritional status, physiological and growth conditions of the culture influence greatly the complex phenomenon of phosphate solubilization. The main

VARIOUS MECHANISMS ADAPTED BY PHOSPHATE SOLUBILIZING BACTERIA FOR MITIGATING SALT STRESS

mechanism for the solubilization capacity of these bacteria is the production of organic acids (Chen et al. 2006). Gluconic acid is the principal organic acid produced by many organisms, but other acids which are involved in phosphate solubilization include 2-keto-gluconic, acetic, citric, glycolic, isobutyric, lactic, malonic, oxalic, propionic, and succinic acids (Rodriguez and Fraga 1999; Chen et al. 2006). There is experimental evidence to support the role of organic acids in mineral phosphate solubilization (Halder et al. 1990). Insoluble inorganic phosphate compounds such as tricalcium phosphate, dicalcium phosphate, hydroxylapatite and rock phosphate can be solubilized by certain bacterial strains belonging to genera Pseudomonas, Bacillus, Rhizobium, Burkholderia, Achromobacter, Agrobacterium, Microccocus, Aerobacter, Flavobacterium and Erwinia (Rodriguez and Fraga 1999). Strains from genera Pseudomonas, Bacillus, and Rhizobium are among the most powerful phosphate solubilizers and in case of substrates, tricalcium phosphate and hydroxylapatite are the one which can be easily degraded by these bacteria as compared to rock phosphate (Rodriguez and Fraga

Fig. 1: Showing plant growth promotion through various mechanisms of phosphate solubilizing bacteria.

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Soil also contains a wide range of organic substrates, which can be a source of Phosphorus for plant growth. To make this form of P available for plant nutrition, it must be hydrolyzed to inorganic Phosphorus. Mineralization of most organic phosphorous compounds is carried out by means of enzymes like phosphatase, phytase, phosphonoacetate hydrolase, and D-α-glycerophosphate. Chen et al. (2006) had reported four s t r a ins namely Ar throbac te r urea fac iens , Phyllobacterium myrsinacearum, Rhodococcus erythropolis and Delftia sp. for the first time as phosphate-solubilizing bacteria (PSB) after confirming their capacity to solubilize considerable amounts of tricalcium phosphate in the medium by secreting organic acids. The phosphate-solubilizing activity of Rhizobium was associated with the production of 2-keto-gluconic acid which was abolished by the addition of NaOH, indicating that the phosphate-solubilizing activity of this organism was entirely due to its ability to reduce pH of the medium (Halder and Chakrabarty 1993). Solubilization of phosphate-rich compounds is also carried out by the action of phosphatase enzymes called acid phosphatases. Acid phosphatases are a ubiquitous class of enzymes that catalyze the hydrolysis of phosphomonoesters at an acidic pH. These enzymes catalyze the hydrolysis of a wide variety of phosphomonoesters and catalyze transphosphorylation reactions by transferring a phosphoryl group to alcohol in the presence of certain phosphate acceptors. Acid phosphatase enzymes are generally located in the bacterial cell wall and in the extracellular polymeric

1999). Bacteria such as Pseudomonas sp., Erwinia herbicola, Pseudomonas cepacia and Burkholderia cepacia produces the organic acids especially the gluconic acid, which seems to be the major agent for phosphate solubilization (Rodriguez and Fraga 1999). 2-keto-gluconic acid is another important organic acid which is produced by strains which have the phosphate-solubilizing ability like Rhizobium leguminosarum, Rhizobium meliloti, Bacillus firmus, and other unidentified soil bacteria. Mixtures of lactic, isovaleric, isobutyric, and acetic acids were found to be produced by two strains of Bacillus licheniformis and B. amyloliquefaciens. Other organic acids, such as glycolic acid, oxalic acid, malonic acid, succinic acid, citric acid and propionic acid, have also been released by the phosphate solubilizers (Chen et al. 2006). Goldstein (1994, 1995) had proposed that the direct periplasmic oxidation of glucose to gluconic acid, and often 2-keto-gluconic acid forms the metabolic basis of the mineral phosphate solubilization phenotype in some Gram-negative bacteria. Alternative possibilities other than

+organic acids include the release of H to the outer surface in exchange for cation uptake or ATPase which

+can constitute alternative ways, with the help of H translocation, for solubilization of mineral phosphates (Rodriguez and Fraga 1999).

Production of ACC deaminase - Ethylene is an essential metabolite for the normal growth and development of plants. This plant growth hormone is produced endogenously by approximately all plants and is also produced by different biotic and abiotic processes in soils and is important in inducing multiple physiological changes in plants. Apart from being a plant growth regulator, ethylene has also been established as a stress hormone (Ahemad and Kibret 2014). Under stress conditions like those generated by salinity, drought, water logging, heavy metals and pathogenicity, the endogenous level of ethylene is significantly increased which negatively affects the overall plant growth. For instance, the high concentration of ethylene induces defoliation and other cellular processes that may lead to reduced crop performance (Bhattacharyya and Jha 2011). It has been proposed that many plant growth promoting bacteria may promote plant growth by lowering the levels of ethylene in plants. This is a t t r i b u t e d t o t h e a c t i v i t y o f e n z y m e 1 - aminocyclopropane-1-carboxylate (ACC) deaminase, which hydrolyzes ACC, the immediate biosynthesis precursor of ethylene in plants. Ammonia and α-ketobutyrate the products of ethylene hydrolysis can be used by the bacterium as a source of nitrogen and carbon for growth. In this way, the bacterium acts as a sink for ACC and thus lowers ethylene level in plants, preventing some of the potentially deleterious consequences of high ethylene concentrations. Phosphate solubilizing bacteria with ACC deaminase trait usually give very consistent results in improving plant growth and yield and thus are good candidates for bio-fertilizer formulation (Hayat et al. 2010). A check on the accelerated ethylene production in plants could be helpful in minimizing the negative effect of salt stress on plant growth and development. Soil salinity alters various physiological processes in plants, including the imbalance of nutrients taken up by roots and the production of additional ethylene. Typically, the presence of endophytic bacteria is important for plant growth and development, however, the importance of bacteria is greater when plants are exposed to environmental stress conditions. Under salt stress conditions, the availability of auxin, ACC deaminase and the nutrients produced by these bacteria is critical to minimize the consequences of physiological stress and to maintain adequate nutrition to support the

substance that surrounds it (Behera et al. 2017). However, detailed biochemical and molecular mechanisms of phosphate solubilization of symbiotic nodule bacteria need to be investigated. The beneficial effects of Phosphate solubilizing bacteria on plant growth varied significantly depending on environmental conditions, bacterial strain, host plant, and soil conditions. The most common mechanism used by microorganisms for solubilizing tri-calcium phosphates seems to be acidification of the medium via biosynthesis and release of a wide variety of organic acids (Rodriguez and Fraga 1999).

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Function as Biopesticides - Another major benefit of Phosphate solubilizing bacteria is to produce antibacterial compounds that are effective against certain plant pathogens and pests. The application of microorganisms to control diseases, which is a form of biological control, is an environment-friendly approach. The major indirect mechanism of plant growth promotion in rhizobacteria is through acting as biocontrol agents. In general, competition for nutrients, niche exclusion, induced systemic resistance and antifungal metabolites production are the chief modes of biocontrol activity in Phosphate solubilizing bacteria (Ahemad and kibret 2014). Moreover, these bacteria

Phytohormone production – Salinity highly reduces the seed germination and it could be related to a decline in endogenous levels of plant growth hormones or phytohormones. It has been reported that salt stress reduces the supply of cytokinin from root to shoot and also the recovery of diffusible auxin from maize coleoptile tips. Indeed, the exogenous application of plant growth regulators (PGRs), e.g., gibberellins, auxins, cytokinins produced some benefit in alleviating the adverse effects of salt stress and they also improve germination, growth, fruit setting, fresh vegetable and seed yields and yield quality. Seeds of the plants, when inoculated with the phosphate solubilizing bacteria, produces phytohormones which will enhance the growth of the plants and further protect the plant from the adverse effects of various stress conditions (Egamberdieva 2009). The production of different phytohormones like IAA, gibberellic acid, and cytokinins by phosphate solubilizing bacteria can change the root architecture of the plant and promote the plant development. Several Phosphate solubilizing bacteria as well as some pathogenic, symbiotic and free-living rhizobacterial species are reported to produce IAA and gibberellic acid in the rhizospheric soil and thereby plays a significant role in increasing the root surface area and the number of root tips in many plants. Recent investigations on auxin synthesizing rhizobacteria as phytohormone producer demonstrated that the rhizobacteria can synthesize IAA from tryptophan by different pathways, although the general mechanism of auxin synthesis was basically concentrated on the tryptophan-independent pathways (Bhattacharyya and Jha 2011).

level of growth and development required to complete the lifecycle of the plants (Yaish et al. 2015).Under stress conditions, the plant hormone ethylene endogenously regulates plant homeostasis and results in reduced root and shoot growth. Plant ACC is sequestered and degraded by the bacterial cells to supply nitrogen and energy when the bacteria is producing its own ACC deaminase enzyme. And hence, by degrading plant ACC, the bacteria reduce the deleterious effects of ethylene and thus, alleviate the stress and enhances the plant growth (Glick 2007).

mediate biological control indirectly by eliciting induced systemic resistance against a number of plant diseases. Application of some phosphate solubilizing bacterial strains to seeds or seedlings has also been found to lead to a state of induced systemic resistance in the treated plant (Behera et al. 2014). Some bacteria produce a wide range of low-molecular-weight metabolites with antifungal potential. The best known is hydrogen cyanide (HCN), to which the producing bacterium, usually a pseudomonad is resistant. HCN produced by bacteria can inhibit the black root rot pathogens of tobacco (Hillel et al. 2005). Fungal cell wall-degrading enzymes e.g., chitinase and β-1, 3-glucanase produced by the phosphate solubilizing bacteria play a significant role in inhibiting the growth of phytopathogens in the soil, hence promoting plant growth (Hayat et al. 2010).

CONCLUSION

Salinization of soil is a serious problem and is increasing gradually in many parts of the world, particularly in arid and semiarid areas. For increasing the agricultural productivity, our dependence on chemical fertilizers and pesticides has encouraged the development of industries that are producing life-threatening chemicals and which are not only hazardous for human consumption but are also disturbing the ecological balance. Bio-fertilizers like phosphate solubilizing bacteria can help to solve the problem of feeding an increasing global population at a

Siderophore production - Iron is a vital nutrient for almost all forms of life. In the aerobic environment, iron

3+occurs principally as Fe and is likely to form insoluble hydroxides and oxyhydroxides, thus making it generally inaccessible to both plants and microorganisms. Commonly, bacteria acquire iron by the secretion of low-molecular-mass iron chelators referred to as siderophores which have high association constants for complexing iron. Not only iron, siderophores also form stable complexes with other heavy metals that are of environmental concern, such as Al, Cd, Cu, Ga, In, Pb and Zn, as well as with radionuclides including U and Np Binding of the siderophore to a metal increases the soluble metal concentration. Hence, bacterial siderophores help to alleviate the stresses imposed on plants by high soil levels of heavy metals (Ahemad and kibret 2014). Some plants can bind and release iron from bacterial iron-siderophore complexes, and use the iron for growth. Therefore, the plant is benefitted both by the suppression of the phytopathogens and simultaneously increasing the plant growth due to the enhanced iron nutrition. There are several examples in the literature, where the plant diseases are suppressed by the siderophore production. Overproduction of siderophores is induced in the certain mutant strain of P. putida which are more effective in controlling the pathogenic fungus Fusarium oxysporum in tomato plant than the wild-type strains. Biological control activity of the wild-type strains is lost when they lose their siderophore activity (Hillel et al. 2005).

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