Contents

1. Introduction ............................................... 1

2. Soil salinity: a global issue ............................................... 2

2.1. The magnitude of the problem ............................................... 2

2.2. Soil Salinization: The process ............................................... 3

3. Impact of soil-salinity on plant growth and development ............................................... 4

4. Impact of soil salinity on rhizospheric microbial diversity ............................................... 4

5. Mechanisms of osmotolerance in rhizobacteria ............................................... 6

6. Mitigation of salt stress in crops by PGPRs. ............................................... 6

6.1. PGPRs as effective candidates in salt stress amelioration in plants ............................................... 6

6.2. PGPR mediated plant root proliferation and plant vigor ............................................... 8

6.3. Bacterial production of phytohormones ............................................... 8

6.4. PGPR act as sink for ACC ............................................... 9

6.5. PGPR mediated ion homeostasis ............................................... 9

6.6. Accumulation of osmolytes ............................................... 10

6.7. Antioxidative Enzymes ............................................... 10

6.8. Bacterial Extracellular Polymeric Substance in plant stress alleviation ............................................... 10

6.9. Enhancement of plant nutrient uptake ............................................... 10

6.10. PGPR mediated disease suppression ............................................... 11

7. Conclusion ............................................... 11

8. References ............................................... 12

1 Introduction

Soil salinity in agriculture soils refers to the presence of high concentration of soluble salts in the soil moisture of the root zone. These concentrations of soluble salts through their high osmotic pressures affect plant growth by restricting the uptake of water and balanced absorption of essential nutritional ions by the roots (Tester and Davenport 2003). Salinity is one of the most serious factors limiting the productivity of agricultural crops, with adverse effects on germination, plant vigour and crop yield (Munns and Tester 2008). In a majority of cultivated plants, yields start declining even at relatively low salinity in soil (electrical conductivity, ECse > 1 dS/m) (Chinnusamy et al. 2005). Some of the most produced and widely used crops such as rice is relatively susceptible to excessive concentration of salts (Howell 2001), and currently, 30 % of worldwide paddy fields are affected by excess salinity (Rowell 1994).

Developing salt-tolerant crops has been a much desired scientific goal but with little success (Munns and Tester 2008). Successful remediation of salt degraded areas for crop production, based on sustainable management practices evolving efficient, low cost, easily adaptable methods, is the challenge. In addition, sustainable management practices in agriculture is essentially important as it offers the potential to meet our future agricultural needs, something that conventional agriculture will not be able to do. Recently, there has been a great interest in eco-friendly and sustainable agriculture with emphasis on the use of beneficial microorganisms. Indeed, several recent studies have demonstrated that local adaptation of plants to their environment is driven by genetic differentiation in closely associated microbes (Rodriguez and Redman 2008). Rhizosphere microorganisms have been shown to enhance the growth of many different crops grown in a wide range of root-zone salinities, and this approach is believed succeed where it has proved difficult to develop salt-tolerant germplasm.

Microorganisms that live in close association with the plant roots play a significant role in stress alleviation in crops grown in saline soils due to their unique properties of tolerance to extremities, their interaction with crop plants and potential deployment methods. About 2–5 % of rhizobacteria, when reintroduced by plant inoculation in a soil containing competitive microflora, exert a beneficial effect on plant growth and are termed as plant-growth-promoting rhizobacteria (PGPR). PGPR were first defined by Kloepper and Schroth (1978) to describe soil bacteria that colonise the roots of plants following inoculation onto seed, and they enhance plant growth. They are involved in various biotic activities of the soil ecosystem to make it dynamic for nutrient turn over and sustainable for crop production (Chandler et al. 1986; Diby et al. 2005a, b). They stimulate plant growth through mobilising nutrients in soils, producing numerous plant growth regulators, protecting plants from phytopathogens by controlling or inhibiting them, improving soil structure and bioremediating the polluted soils by sequestering toxic heavy metal species and degrading xenobiotic compounds (Braud et al. 2009; Hayat et al. 2010).

Use of these microorganisms in stressed soils can alleviate stresses in crop plants, thus opening a potential and promising strategy in sustainable agriculture. Several studies are now proving the hypothesis that PGPRs enable agricultural plants to maintain productivity under stressed conditions by various means, and the results are promising. These microbes also provide excellent models for understanding the stress tolerance, adaptation and response mechanisms that can be subsequently engineered into crop plants to cope with climate change induced stresses (Grover et al. 2011). Improvement in agricultural sustainability in saline soils inevitably requires management practices that enhance soil biological activity and thereby build-up long-term soil productivity and crop health.

2 Soil salinity: a global issue

2.1 The magnitude of the problem

Salinity is a significant problem affecting agriculture worldwide and is predicted to become a larger problem in the coming decades. Soil salinisation is reducing the area that can be used for agriculture by 1–2 % every year, hitting hardest in the arid and semi-arid regions (The Food and Agriculture Organization of the United Nations (FAO) 2002). As salt levels that are harmful to plant growth affect large terrestrial areas of the world, agricultural productivity is severely affected by soil salinity. It has been estimated that on a world-wide scale, the production by approximately 400 million hectares of arable land is being severely restricted by salinity (Bot et al. 2000). According to the Food and Agriculture Organization of the United Nations, Land and Plant Nutrition Management Service, over 6 % of the world’s land is salt-affected (Table 1). The Food and Agriculture Organization of the United Nations (FAO, 1988) estimates that, of the 250 million hectares of irrigated land in the world, approximately 50 % already show salinisation and soil saturation problems, and 10 million hectares are abandoned annually due to these problems. The United Nations Environment Program estimates that approximately 20 % of agricultural land and 50 % of cropland in the world is salt-stressed (Flowers and Yeo 1995).

Table 1 Salt-affected soils occur in all continents and under almost all climatic conditions
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Salt stress as one of the most widespread abiotic constraints in food production may also result in the negative ecological, social and/or economic outcomes. For instance, recent deposition of toxic salt sediments and sea intrusion in tsunami-affected areas of Maldives damaged >70 % of agriculture land, destroyed >370,000 fruit trees and affected around 15,000 farmers (The Food and Agriculture Organization of the United Nations (FAO) 2005). Postel (1998) estimates that soil salinisation costs the world’s farmers $11 billion a year in reduced income and warns that the figure is growing.

Coastal wet lands and coastal agricultural zones too are seriously affected by the salinity issue. Coastal wetlands comprise various habitat types, including salt marshes, mangroves, seagrasses, salt swamps, and sand dunes, because of their transitional situation between sea and terrestrial ecosystems, affected by salinity (Armstrong et al. 1985; Bharathkumar et al. 2008). Out of about 8.1 million hectares of salinised land in India, 3.1 million are reported to be in coastal regions (Tripathi et al. 2000).

2.2 Soil salinisation: the process

Salinisation consists of an accumulation of water soluble salts in the soil that include the ions potassium (K+), magnesium (Mg2+), calcium (Ca2+), chloride (Cl−), sulfate (SO4 2−), carbonate (CO3 2−), bicarbonate (HCO3−) and sodium (Na+). Depending on soils, the extracted solutions differ in the content of dissolved salts; if total salt concentration, i.e. electrical conductivity (ECse), exceeds 20 mM (~2 dS/m), they can be categorised as salt-affected (Abrol et al. 1988). The salinisation processes may be primary (natural) and secondary (anthropogenic) (Ghassemi et al. 1995). The major causes of naturally induced salinity are salt water intrusion and wind-born salt deposition in land. Mediterranean regions are currently experiencing increasing salt stress problems resulting from seawater intrusion into aquifers and irrigation with brackish water (Rana and Katerji 2000). Another major cause for soil salinity is the deposition of oceanic salt carried in wind and rain. Salts originate also from mineral weathering. The anthropogenic factors include crop irrigation with salt waters wherein soil salinisation is dramatically exacerbated and accelerated. The other factors may be inorganic fertilisers, soil amendments (e.g. gypsum, composts and manures) (Kotuby-Amacher et al. 2000).

Although Earth abounds in water, an almost negligible portion (~2.5 % or 35 million km3) is fresh or with low salt concentration (<1 dS/m) (Ondrasek et al. 2010; Shiklomanov and Rodda 2003), i.e. water that may be conditionally used for irrigation in crop production, whereas the rest is salty and therefore unsuitable for irrigation. However, it has been estimated that irrigated agriculture consumes ~70 % (and >90 % in many developing countries) of total water withdrawal to produce ~36 % of global food (Howell 2001). As a consequence, there is a continuous degradation of land resources (e.g. salt-affected soils), representing a large burden to natural ecosystems. When salt accumulates in the soil, excessive sodium (Na+) from salt destroys soil structure, deteriorates soil hydraulic properties, raises soil pH and reduces water infiltration and soil aeration, leading to soil compaction, increasing erosion and water run-off. Furthermore, sodium is the most pronounced destructor of secondary clay minerals by dispersion. Dispersion occurs because of Na+ replacement of calcium (Ca2+) and other coagulators like Mg2+ adsorbed on the surface and/or inter-layers of soil aggregates (Ondrasek et al. 2010). Dispersed clay particles undergo leaching through the soil and may accumulate and block pores, especially in fine-textured soil horizons (Burrow et al. 2002). The soil becomes unsuitable for proper root growth and plant development.

3 Impact of soil salinity on plant growth and development

Salinity affects plant growth and yield in many of crops in varying degrees (Table 2). Crops such as cereals (rice and maize), forages (clover) or horticultural crops (potatoes and tomatoes) are relatively susceptible to excessive concentration of salts, either dissolved in irrigation water or present in soil (rhizosphere) solution. Soil salinity has been reported to reduce yields, nodulation and the total nitrogen content in legume plants (Singleton and Bohlool 1984). El-Fouly et al. (2001) found that the dry weight of different plant organs of tomato was reduced in response to the increase of NaCl level in the root growth medium.

Table 2 Excess soil salinity causes poor and spotty stands of crops, uneven and stunted growth and poor yields, the extent depending on the degree of salinity
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During the onset and development of salt stress within a plant, all the major processes such as photosynthesis, protein synthesis and energy and lipid metabolism are affected (Parida and Das 2005). Photosynthetic capacity is reduced, due to the osmotic stress and partial closure of stomata (Meloni et al. 2003). Plants can also suffer from membrane destabilisation and a general nutrient imbalance (Hasegawa et al. 2000). Further plant responses to osmotic stress are decrease in cell growth and development, reduced leaf area and chlorophyll content, accelerated defoliation and senescence (Shannon and Grieve 1999). Figure 1 shows saline patch of soil in a wheat field (Uttar Pradesh, India) that clearly hinders plant growth.

Fig. 1
figure 1

A saline patch of soil in a wheat field clearly hinders plant growth. The photos were taken in Varanasi, Uttar Pradesh, India. Salt causes yellowing and death of wheat leaves. Salt-affected soil often exhibits a white or grey salt crust on the ground and the salt interferes with the growth of most plants

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Fig. 2
figure 2

Plant-growth-promoting rhizobacteria colonise the rhizosphere of plants and promote growth of plants through various means and help mitigate salt stress. Interaction of plant-growth-promoting rhizobacteria with several crops in saline conditions reduced the extent of poor growth and thus helps plants survive and improve performance in adverse conditions. Beneficial attributes of plant-growth-promoting rhizobacteria (PGPR) towards stress tolerance in crops grown in saline soils are described in the figure

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An increase in the uptake of Na+ or decrease in the uptake of Ca2+ and K+ in leaves lead to nutritional imbalances. Accumulation of excess Na+ may cause metabolic disturbances in processes where low Na+ and high K+ or Ca2+ are required for optimum function. Excess sodium and more importantly chloride has the potential to affect plant enzymes and cause cell swelling, resulting in reduced energy production and other physiological changes (Larcher 1980). Uptake and accumulation of Cl− disrupt photosynthetic function through the inhibition of nitrate reductase activity (Xu et al. 2000). Under excessive Na+ and Cl− rhizosphere concentration, there are competitive interactions with other nutrient ions (K+, NO3− and H2PO4 −) for binding sites and transport proteins in root cells, and thereafter for translocation, deposition and partitioning within the plant (Tester and Davenport 2003). Once the capacity of cells to store salts is exhausted, salts build up in the intercellular space leading to cell dehydration and death (White and Broadley 2001).

Under saline conditions, osmotic pressure in the rhizosphere solution exceeds that in root cells, influencing water and nutrient uptake. Almost all micro- and macronutrient contents decrease in the roots and shoots with increasing NaCl concentration in the growth medium. Salama et al. 1996 reported limited uptake of nutrients in different organs of wheat plants when there was high salt concentration in the root growth medium. The plants with perturbed nutrients relations are more susceptible to invasion of different pathogenic microorganisms and physiological dysfunctions, whereas their edible parts have markedly less economic and nutritional value due to reduced fruit size and shelf life, non-uniform fruit shape, decreased vitamin content, etc. (Romic et al. 2008).

The primary salinity effects give rise to numerous secondary ones such as oxidative stress, characterised by accumulation of reactive oxygen species potentially harmful to biomembranes, proteins, nucleic acids and enzymes (Porcel et al. 2012). To protect against oxidative stress, plant cells produce both antioxidant enzymes and non-enzymatic antioxidants (Hasegawa et al. 2000), and the modulation of antioxidant enzyme activity and concentrations are frequently used as indicators of oxidative stress in plants (Mayak et al. 2004).

4 Impact of soil salinity on rhizospheric microbial diversity

The microbial biomass is an important labile fraction of the soil organic matter, functioning both as an agent of transformation and recycling of the organic matter and soil nutrients, as also of a source of nutrients for the plants. It is well known that the environments of plant rhizospheres are more favourable microhabitats for microorganisms compared to surrounding bulk soils (Bais et al. 2006), and these microbes directly or indirectly influence plant growth and development. In addition, as the availability of nutrients for plants is regulated by the rhizospheric microbial activity, any factor affecting this community and its functions influences the availability of nutrients and growth of the plants. Enhanced microbial biomass and activities by rhizosphere effects are important to ecosystem functioning and pollutant degradation in natural ecosystems, plant health as well as in contaminated environments (Nie et al. 2009; Wenzel 2009).

Since the soil organic matter, and consequently the biomass and microbial activity, are generally more relevant in the first few centimetres at the surface of the soil, salinisation close to the surface can significantly affect a series of microbiologically mediated processes. The detrimental influence of salinity on the microbial soil communities and their activities reported in naturally saline soils (Rietz and Haynes 2003; Sardinha et al. 2003). Salinity has a negative impact on microbial abundance, diversity, composition and functions (Borneman et al. 1996). Omar et al. (1994) showed that, with an increase in the salinity level to above 5 %, the total count of bacteria and actinobacteria was drastically reduced. Salinity stress was shown to reduce the attachment of Azospirillum brasilense to maize and wheat roots (Jofre et al. 1998). In addition, increase in salinity inhibited nitrogen fixation at the level of nifH expression and nitrogenase activity in Azospirillum sp. (Tripathi et al. 2002). Increased salinity in the rhizosphere affects root exudation and decomposition of organic matter by microorganisms (Ondrasek et al. 2010). Similar observation were reported by Li et al. (2006), who noticed significant negative correlations between soil electrical conductivity and total CO2 emission or microbial biomass C, suggesting that salinity had an adverse effect on microbial biomass and activity. Therefore, naturally occurring soil organic matter decomposers may be sensitive to salt-induced stress. This effect is always more pronounced in the rhizosphere pursuant to increased water uptake by the plants due to transpiration.

Nelson and Mele (2007) reported that sodium chloride is more likely to affect rhizosphere microbial community structure indirectly through root exudates quantity and/or quality than directly through microbial toxicity and that plant health is a major determinant in rhizosphere microbial community structure. For microbes, life in high salt concentrations is bioenergetically taxing because they must maintain an osmotic balance between their cytoplasm and the surrounding medium while excluding sodium ions from the cell interior, and as a result, sufficient energy is required for osmoadaptation (Jiang et al. 2007). Depletion of potassium ions by plants reduces the ability of rhizobacteria to use potassium ions as a primary osmoregulator (Jofre et al. 1998). Plant use of osmolytes under salt stress deprives rhizobacteria of osmolytes, which finally limits the bacterial growth. Alteration of proteins, exopolysaccharide and lipopolysaccharide composition of the bacterial cell surface, impairment of molecular signal exchange between bacteria and their plant host due to the alteration of membrane glucan contents, and inhibition of bacterial mobility and chemotaxis towards plant roots significantly affect microbial diversity in the rhizosphere, under saline conditions. Ibekwe et al. (2010) suggested that changes in microbial diversity may be the first indicator of stress in salinity-affected soils. Therefore, if stress can be detected early enough in salinity affected soils, then some remedial action may be possible to improve soil quality and crop performance.

5 Mechanisms of osmotolerance in rhizobacteria

Exposure of microorganisms to high-osmolality environments triggers rapid fluxes of cell water along the osmotic gradient out of the cell, thus causing a reduction in turgor and dehydration of the cytoplasm. Microbes have developed various adaptations to counteract the outflow of water. The cytoplasm is exposed to high ionic strength to achieve osmotic equilibrium by maintaining a cytoplasmic salt concentration similar to that of the surrounding media. The first response to osmotic up shifts and the resulting efflux of cellular water is uptake of K+ and also cells start to accumulate compatible solutes (Whatmore et al. 1990). The organic osmolytes include sugars and derivatives, amino acids and their derivatives, polyols and derivatives, betaines and ectoines (Lamosa et al. 1998). Compatible solutes could be synthesised de novo or, if present in the medium, can be taken up by the organisms. Paul and Nair (2008) reported that Pseudomonas fluorescens MSP-393, a PGPR strain, as a means of salt tolerance, de novo-synthesised, the osmolytes, alanine, glycine, glutamic acid, serine, thronine and aspartic acid in their cytosol. In addition to their well-studied function as osmoprotectants, compatible solutes also have protein-stabilising properties that support the correct folding of polypeptides under denaturing conditions both in vitro and in vivo (Street et al. 2006).

Yet, another mechanism is by altering the cell envelope composition resulting in changes in proteins, periplasmic glucans and capsular, exo and lipopolysaccharides. Pseudomonas survive under stress conditions due to the production of exopolysaccharides, which protects them from hydric stress and fluctuations in water potential by enhancing water retention and regulating the diffusion of carbon sources in microbial environment (Sandhya et al. 2009). Klein et al. (1999) reported changes in the fatty acid composition of the bacterial membrane under osmotic stress, by varying the length of acyl chains, number of double bonds or branching of acyl chains by methyl groups. Salt stress induced higher levels of cyclopropane fatty acid (DC19:0) and lower levels of oleic acid (C18:1) in the lipid membrane of Lactococcus lactis (Guillot et al. 2000). A cross-linking of the peptidoglycan has also been shown to respond to variations in the salinity stress; NaCl stressed cells had shorter peptidoglycan inter-peptide bridges than the unstressed cells (Piuri et al. 2005). Francius et al. (2011) showed that the presence of loose, flexible surface appendage around the bacteria under low electrolyte concentration condition acts as a protective barrier, thereby attenuating the impact of changes in extracellular ionic strength and lowering the osmotic pressure constraint.

Bacteria initiate a program of gene expression in response to osmotic stress by high NaCl concentrations, which are manifested as a set of proteins produced in increased amounts in response to the stress (Volker et al. 1994). Diby et al. (2005a) demonstrated differentially expressed salt responsive genes in the salt-tolerant PGPR, Pseudomonas pseudoalcaligenes. Peptide mass fingerprinting analysis of P. fluorescens under salt shock conditions revealed several over-expressed/repressed stress related proteins (Paul et al. 2006). Majority of proteins identified were homologous to stress proteins in prokaryotes. These stress alleviation proteins is believed to play a major role in helping the bacteria to maintain its metabolism unaltered considerably, thus delivering the plant-growth-promoting and biocontrol properties in saline soils (Paul et al. 2006). A transcriptional profiling of a salt-stressed soil bacterium Bacillus subtilis in the presence of 1.2 M NaCl has been shown to trigger the induction of 123 genes and led to the repression of 101 genes (Steil et al. 2003). Use of macro-array technique in Escherichia coli revealed that NaCl stress altered the expression of 152 genes, out which 45 were up regulated, whereas the rest 107 were down-regulated (Weber and Jung 2002). Several of the up-regulated genes have been shown to be involved in the cellular processes of adaptation and protection and in the biosynthesis, metabolism and transport of amino acids. The transcriptome analysis in Shewanella oneidensis MR-1 revealed that high salinity caused up-regulation of genes involved in Na+ eZux, K+ accumulation, glutamate biosynthesis and in aerobic as well as anaerobic respiration (Liu et al. 2005). Among genes potentially mediating K+ transport across bacterial membranes, the most dramatic changes in response to NaCl stress were observed in the level of expression of the K+ uptake protein kup/trkD (Shabala 2009). Very recently, it has been reported that the non-coding RNA named Yfr1 might be involved in salt sensing (Georg et al. 2009). The mechanisms of salt-tress adaptions in rhizobacteria have been recently reviewed by Paul (2013).

6 Mitigation of salt stress in crops by PGPRs

6.1 PGPRs as effective candidates in salt stress amelioration in plants

Salinity adversely affects the growth and yield of several crop plants, and soil aggregate stability is one of the most important properties controlling the growth of plants in semi-arid environments. Therefore, the improvement of soil structural stability is of great importance. The contribution of microbial populations, either as free-living organisms or associated with plant roots, and their activities to soil aggregate stability are proved to be highly beneficial (Jastrow and Miller 1991) in terms of rendering saline soils suitable for agriculture. Extensive research has been carried out on occurrence and functional diversity of agriculturally important microbes in stressed environments and their role in soil remediation, as reviewed by several authors (Graham 1992; Zahran 1999; Paul 2013). The occurrence of several of beneficial rhizobacteria like Rhizobium, Bradyrhizobium, Azotobacter, Azospirillum, Pseudomonas, Bacillus, etc. have been reported from stressed environments like desert ecosystems, acid soils, saline and alkaline areas and highly eroded hill slopes (Selvakumar et al. 2009; Upadhyay et al. 2009), and these are assumed to be involved in natural reclamation process of the soil.

Apart from developing mechanisms for own stress tolerance, PGPRs can also impart some degree of tolerance to plants, towards abiotic stresses like salinity. Interaction of PGPR with several crops in saline conditions reduced the extent of poor growth and thus helps plants survive and improve performance in adverse conditions (Dimkpa et al. 2009). Many studies have been published on beneficial effects of bacterial inoculation on plant physiology and growth under salt stress conditions and examples are summarised in Table Error! Reference source not found.. Some PGPR may exert a direct stimulation on plant growth and development by providing plants with fixed nitrogen, phytohormones, iron that has been sequestered by bacterial siderophores, and soluble phosphate (Hayat et al. 2010; Rodriguez and Fraga 1999). Others do this indirectly by protecting the plant against soil-borne diseases, most of which are caused by pathogenic fungi (Lugtenberg and Kamilova 2009). Soil-borne pseudomonads have received particular attention because of their catabolic versatility, excellent root-colonising ability and capacity to produce a wide range of enzymes and metabolites that help the plant withstand varied biotic and abiotic stress conditions (Vessey 2003). Various attributes of PGPRs in amelioration of salt stress in crops are summarised in Fig. 2.

Table 3 Rhizobacteria impart some degree of tolerance to plants, towards salinity stress
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6.2 PGPR-mediated plant root proliferation and plant vigour

PGPRs colonise the rhizosphere of plants and promote growth of the plants through various means. Paul and Sarma (2006) demonstrated using GS Root® software (PP systems, Winterstreet, USA) that the PGPR strain, P. fluorescens IISR-6, significantly enhanced the root biomass of black pepper vines. Rhizobacteria-mediated root proliferation has been well proved and it also works in stressed soils (Diby et al. 2005a). Hence, a fruitful strategy to alleviate negative effects of salt stress in plants might be the co-inoculation of seeds with different PGPR species. Inoculation of various plant species with PGPRs has also reported to lead to enhanced formation of lateral roots and root hairs that can result in enhanced tolerance to abiotic stress. Paul and Nair (2008) reported the root colonisation potential of the salt tolerant Pseudomonas strain was not hampered with higher salinity in soil. Promotion of root growth results in a larger root surface and can, therefore, have positive effects on water acquisition and nutrient uptake (Diby et al. 2005b; Paul and Sarma, 2006) that is expected to alleviate the stress effects in the plant. In addition, Kohler et al. (2009) observed in lettuce that the plants inoculated with PGPRs were more hydrated than the control plants under saline conditions. Greater hydration induced by the PGPR strain might be attributable to increased water use efficiency (Saravanakumar and Samiyappan 2007).

Mayak et al. (2004) observed that, when tomato plants were root bacterised with a suspension of beneficial bacteria, the extent of growth suppression due to salt stress was decreased and the bacterial treated plants accumulated more fresh and dry weights than un-treated plants. Fu et al. (2010) reported that, with increasing salt concentration, growth of eggplant was progressively inhibited, but when the plants were inoculated with the PGPR Pseudomonas sp. DW1, the extent of growth suppression was decreased and these treated plants had greater dry weights than untreated plants, indicating the beneficial role of rhizobacteria in alleviating the debilitating effects of salt stress. Furthermore, PGPRs have been reported to help seed germination in stressed soils and Barassi et al. (2006) reported the same in Azospirillum-inoculated lettuce seeds under salt stress. Applications of bio-priming of radish with PGPR strains significantly improved the percentage of seed germination under saline conditions (Kaymak et al. (2009).

Rojas-Tapias et al. (2012) observed enhanced chlorophyll content in maize upon inoculation with Azotobacter strains, revealing a positive effect on growth and plant development. Also in maize and canola, the rhizobacterial treatment increased the total chlorophyll contents (a, b and carotenoids) (Glick et al. 1998; Nadeem et al. 2007). The increase in chlorophyll content may also be the result of an increased photosynthetic leaf area of the plant (Nadeem et al. 2007) by rhizobacteria inoculation, compared with the un-inoculated control where the leaf area was reduced owing to stress (Marcelis et al. 1999). However, it has been reported that, when pepper plants were co-inoculated with A. brasilense and Pantoea dispersa, there were higher plant dry matter accumulation under salinity, and it was related to a higher source activity due to higher stomatal conductance and photosynthesis than non-inoculated plants, but without affecting chlorophyll concentration or photosystem II photochemical efficiency (del Amor and Cuadra-Crespo 2012).

6.3 Bacterial production of phytohormones

It is most likely that the plant growth hormones of microbial origin in the vicinity of plant roots could evoke a physiological response in the host plant. Production of indole acetic acid, gibberellins and other growth regulators produced by PGPR is believed to support increase root length, root surface area and number of root tips, leading to enhanced uptake of nutrients thereby improving plant health under stress conditions (Egamberdieva and Kucharova 2009). Indole acetic acid production is a relatively common trait of PGPR, and such bacteria is believed to counteract salinity stress in plants. Morphological plant root changes have been observed repeatedly upon Azospirillum inoculation and have been attributed to the production of plant-growth-promoting substances: auxins, cytokinins, and gibberellins, with auxin production being quantitatively the most important (Spaepen et al. 2008). Sadeghi et al. (2012) demonstrated that a Streptomyces isolate increased plant growth in wheat and produced indole acetic acid and auxin in presence of salt. Stimulation of shoot biomass of lettuce plants grown in drying soil by the cytokinin-producing PGPR B. subtilis (Arkhipova et al. 2007) implied considerable root-to-shoot cytokinin signalling. Yao et al. (2010) showed that inoculation of P. putida Rs-198 in seeds resulted in increased production of indole acetic acid and inhibited production of abscisic acid, increasing growth parameters in cotton seedlings. Indole acetic acid is a plant growth hormone, while abscisic acid is a well-known stress-inducible plant hormone and growth inhibitor. As phytohormone production seems a relatively common trait of PGPR, it is suggested to pay more attention in selecting microbial inoculants with high phytohormone production to potentially ameliorate salt stress.

6.4 PGPR act as sink for ACC

In plants grown under salt stress soils, 1-aminocyclopropane-1-carboxylate (ACC) levels increase, resulting in high ethylene concentration that ultimately increases plant damage (Botella et al. 2000). Chemical inhibitors of ethylene synthesis, such as cobalt ions and aminoethoxyvinyle glycine, are often used to overcome the problems associated with salt stress. However, these chemicals are not only expensive, but they have harmful effects on the environment (Dodd 2009). Rhizobacteria have been reported to act as a sink for 1-aminocyclopropane-1-carboxylate (Saleem et al. 2007), hydrolysing it to ammonia and a-ketobutyrate and thereby lowering the level of ethylene in stressed plants. In the presence of 1-aminocyclopropane-1-carboxylate deaminase producing bacteria, plant 1-aminocyclopropane-1-carboxylate is sequestered and degraded by bacterial cells to supply nitrogen and energy (Mayak et al. 2004), facilitating plant growth under the salinity stress condition (Nadeem et al. 2010; Siddikee et al. 2010). Furthermore, by removing 1-aminocyclopropane-1-carboxylate, the bacteria reduce the deleterious effect of ethylene, ameliorating plant stress and promoting plant growth (Glick et al. 2007). The effectiveness of 1-aminocyclopropane-1-carboxylate deaminase containing rhizobacteria for enhancing salt tolerance and consequently improving the growth of tomato, rice and various other crops under salt-stress conditions have been well proved (Bal et al. 2013 and Mayak et al. 2004). Siddikee et al. (2010) reported that halotolerant strains of bacteria that belong to different bacterial genera, i.e. Bacillus, Brevibacterium, Planococcus, Zhihengliuella, Halomonas, Exiguobacterium, Oceanimonas, Corynebacterium, Arthrobacter and Micrococcus that were originally isolated from coastal soils, have a real potential to enhance plant growth under saline stress via 1-aminocyclopropane-1-carboxylate deaminase activity. The enzyme 1-aminocyclopropane-1-carboxylate deaminase has been found in a wide range of other rhizobacteria as well, such as the genera Achromobacter, Acidovorax, Alcaligenes, Enterobacter, Klebsiella, Methylobacterium, Pseudomonas, Rhizobium and Variovorax (Esquivel-Cote et al. 2010).

6.5 PGPR-mediated ion homeostasis

Microbes can alter root uptake of toxic ions and nutrients by altering host physiology or by directly reducing foliar accumulation of toxic ions (Na+ and Cl−) while improving the nutritional status of both macro- (N, P and K) and micronutrients (Zn, Fe, Cu and Mn), mostly via unknown mechanisms. Potassium plays a key role in plant water stress tolerance and has been found to be the cationic solute responsible for stomatal movements in response to changes in bulk leaf water status (Caravaca et al. 2004). Zhang et al. (2008) reported that inoculation with B. subtilis GB03 could mediate the level of salt tolerance in Arabidopsis thaliana through regulation of the potassium transporter HKT1. Certain volatiles emitted by PGPR have been shown to down regulate HKT1 expression in roots but up-regulates it in shoots, orchestring lower Na+ levels and recirculation of Na+ in the whole plant under salt conditions (Zhang et al. 2008). These results supported the idea that bacteria can mediate the expression of an ion high-affinity K+ transporter (AtHKT1) in Arabidopsis under saline condition. PGPR-inoculated plants have been demonstrated to have increased K+ concentration, which in turn resulted in a high K+/Na+ ratio leading to their effectiveness in salinity tolerance (Kohler et al. 2009; Nadeem et al. 2013; Rojas-Tapias et al. 2012). Ashraf et al. (2004) found that Azospirillum could restrict Na+ influx into roots. In addition, high K+/Na+ ratios were found in salt-stressed maize in which selectivity for Na+, K+, and Ca2+ was altered in favour of the plant, upon inoculation with Azospirillum (Hamdia et al. 2004).

Salinity not only reduces Ca2+ and K+ availability in plants but also reduces Ca2+ and K+ mobility and transport to the growing parts of plants. However, Fu et al. (2010) reported significantly increased Ca2+ in shoots of eggplants inoculated with Pseudomonas when compared to the non-inoculated eggplant under saline conditions. Yao et al. (2010) demonstrated that PGPRs are involved in significantly increasing the cotton’s absorbability of Mg2+ and Ca2+ and decreasing the absorption of the Na+. It has also been shown that Ca2+ plays a major role as an early signalling molecule at the onset of salinity.

Salt stress leads to damage to the plant cell membrane and hence increase its permeability resulting in electrolyte leakage and accumulation of it in the surrounding tissues. Inoculation with Rhizobium and Pseudomonas in Zea mays have been reported to lower the electrolyte leakage (Bano and Fatima 2009 and Sandhya et al. 2010). Similar observations were made by Shukla et al. (2012) in Arachis hypogaea, suggesting that PGPR protect the integrity of the plant cell membrane from the detrimental effect of salt.

6.6 Accumulation of osmolytes

Maintaining water homeostasis and the functioning of photosynthetic structures are essential for alleviating the impact of salinity on plant growth and crop yield. One of the most common stress responses in plants is overproduction of different types of compatible organic solutes such as proline and glycine betaine (Serraj and Sinclair 2002). Proline accumulation is a sensitive physiological index of the response of plants to salt and other stresses (Peng et al. 2008) to maintain higher leaf water potential during stress and to keep plants protected against oxidative stress. PGPRs have been demonstrated to enhance plant stress tolerance by contributing to osmolyte accumulation in plants. Increased accumulation of proline has been reported in soybean plants grown under saline conditions upon inoculation with PGPR strains that alleviated salinity stress and improved growth (Han and Lee 2005). Zarea et al. (2012) also reported increased the proline accumulation in wheat upon root colonisation with PGPRs. Azospirillum could also accumulate proline (Bashan 1999; Casanovas et al. 2003) in plants as an osmoprotectant. It is reported that proline protects higher plants against salt/osmotic stresses, not only by adjusting osmotic pressure but also by stabilising many functional units such as complex II electron transport and enzymes such as ribulose bisphosphate carboxylase/oxygenase (RUBISCO) (Makela et al. 2000). Proline also helps the plant cell by stabilising subcellular structures such as membranes and proteins, scavenging free radicals and buffering cellular redox potential under salt stress to alleviate salt stress (Ashraf and Foolad 2007 and Kohler et al. 2009). Increased total soluble sugar (TSS) content of plants under salinity stress is another important defence strategy to cope with salinity stress, and Upadhyay et al. (2012) showed that an increased proline and total soluble sugar in the PGPR-treated wheat plants significantly contributed to their osmotolerance. Similarly, trehalose metabolism in rhizobia also seems important for improving plant growth, yield and adaptation to abiotic stress of leguminous plants (Suarez et al. 2008).

6.7 Antioxidative enzymes

Formation of reactive oxygen species upon salt shock in plants brings about damage to lipids, protein and nucleic acids. Reactive oxygen species production is favoured due to over-reduction of photosynthetic electron chain by the limiting of photosynthesis under salinity (Johnson et al. 2003; Hichem et al. 2009). Antioxidants have been reported to have greater resistance to this oxidative damage (Spychalla and Desborough 1990). The activities of the antioxidative enzymes such as catalase, guaicol peroxidase and superoxide dismutase increase under salt stress in plants and a correlation of these enzyme levels and salt tolerance exists (Mittova et al. 2002, 2003). Researches with application of PGPRs have shown significant increase in plants of several of plant-defence-related enzymes, superoxide dismutase, peroxidase, catalase, polyphenol oxidase, phenylalanine ammonia-lyase, lipoxygenase and phenolics (Liang et al. 2011; Nautiyal et al. 2008; Chakraborty et al. 2013). These PGPR-induced antioxidative enzymes are believed to be contributing to the salt stress tolerance in plants also by eliminating hydrogen peroxide from salt-stressed roots (Kim et al. 2005). However, few data are available about the mechanisms involved in bacterial-mediated plant antioxidative protection.

6.8 Bacterial extracellular polymeric substance in plant stress alleviation

Extracellular polymeric substance-producing PGPR have been reported to significantly enhance the volume of soil macropores and the rhizosphere soil aggregation, resulting in increased water and fertiliser availability to inoculated plants, which in turn is believed to help plants to better manage the salt shock. The influence of extracellular polymeric substance-producing PGPR on the aggregation of root-adhering soils has been well described (Upadhyay et al. 2011; Alami et al. 2000). PGPR strains that produce bacterial extracellular polymeric substance bind cations including Na+, and it may be envisaged that increasing the population density of extracellular polymeric substance-producing bacteria in the root zone would decrease the content of Na+ available for plant uptake, thus help alleviating salt stress in plants growing in saline environments (Geddie et al. 1993). Roberson and Firestone (1992) demonstrated that the extracellular polymeric substance of bacteria possess unique water holding and cementing properties, thus play a vital role in the formation and stabilisation of soil aggregates and regulation of nutrients and water flow across plant roots through biofilm formation.

6.9 Enhancement of plant nutrient uptake

Mineral nutritional status of plants greatly affects their ability to adapt to adverse environmental conditions and in particular to abiotic stress factors, impairment of which exacerbates the adverse effects of abiotic stresses. Nutritional imbalance hampers plant growth, development and also the yield. Imbalances may result from the effect of salinity on nutrient availability, competitive uptake, transport or partitioning within the plant or may be caused by physiological inactivation of a given nutrient resulting in an increase in the plant’s internal requirement for that essential element (Grattan and Grieve 1994). Crop performance may be adversely affected by salinity-induced nutritional disorders. Nitrogen, in one form or another, accounts for about 80 % of the total mineral nutrients absorbed by plants, and inadequate nitrogen is often a growth-limiting nutritional stress (Marschner 1995). Studies indicate that salinity reduces N uptake/accumulation (Feigin 1985). In addition, it is known that salt stress causes reduction in P accumulation in plants, which develop P-deficiency symptoms. Salinity reduces phosphate uptake/accumulation in crops grown in soils primarily by reducing phosphate availability (Sharpley et al. 1992). Besides, maintenance of adequate levels of K+ is essential for plant survival in saline habitats, and sodium-induced K+ deficiency has been implicated in various crops (Botella et al. 1997).

PGPRs have been proved to be vital for circulation of plant nutrients in many ways, thereby reducing the need for chemical fertilisers. Apart from fixing N2, many strains of PGPR can affect plant growth directly by solubilising inorganic phosphate, improving nutrient uptake and mineralising organic phosphate (Dobbelaere et al. 2003; Ogut et al. 2010). Solubilisation of phosphorus in rhizosphere is the most common mode of action implicated in PGPR that increase the nutrient availability to the host plant (Rashid et al. 2004). These rhizobacteria are critical for the transfer of P from poorly available forms and are important for maintaining P in readily available pools. Diby et al. (2005b) reported enhanced nutrient mobilisation in the rhizosphere of black pepper and significant uptake of nitrogen (N) and phosphorus (P) in the PGPR-treated black pepper vines that resulted in root proliferation and enhanced plant growth. Strains of rhizobacteria that have efficient phosphorus-solubilising ability even under high saline (60 g L−1 NaCl) conditions have been reported (Son et al. 2006; Upadhyay et al. 2011). The damaging effects of NaCl on wheat seedlings were demonstrated to be reduced by inoculation with A. brasilense (Creus et al. 1997). Azospirillum inoculated lettuce seeds had better germination and vegetative growth than non-inoculated controls after being exposed to NaCl (Barassi et al. 2006). Dardanelli et al. (2008) reported as salt stress affect nodulation during Phaseolus–Rhizobium interaction, a secondary inoculation of the salt-stressed plants with Azospirillum caused an extended exudation of plant flavonoids compared to Rhizobium alone. This co-inoculation of plants with different bacterial strains contributed to relieving of the abiotic stress.

6.10 PGPR-mediated disease suppression

In general, competition for nutrients, niche exclusion, induced systemic resistance (ISR) and antifungal metabolites production are the chief modes of biocontrol activity in PGPR (Lugtenberg and Kamilova 2009). Many rhizobacteria have been reported to produce antifungal metabolites like HCN, phenazines, pyrrolnitrin, 2,4-diacetylphloroglucinol, pyoluteorin, viscosinamide and tensin (Bhattacharyya and Jha 2011). Several strains of PGPRs have been demonstrated to exhibit biological control of plant pathogens even in saline soils. Diby et al. (2005a) reported that the population of the biocontrol agent, P. fluorescens in the saline rhizospheric soil did not change considerably with increasing salinity in the soil, indicating that the colonisation efficiency of the strain was not affected by the salinity factor. Paul and Nair (2008) ascertained that the osmotolerance mechanisms of the salt-tolerant PGPRs effectively nullified the detrimental effects of high osmolarity and fully serve as biocontrol agents in crops grown in saline soils. Egamberdieva (2012) reported the repression of cucumber and tomato root rot caused by F. solani in salinated soil when the plants were treated with salt tolerant P. chlororaphis strain. PGPR-mediated biocontrol of several plant diseases against an array of pathogens have been reported even under saline conditions (Elmer 2003; Paul and Nair 2008; Rangarajan et al. 2003; Triky-Dotan et al. 2005).

Induced systemic resistance is the enhanced defensive capacity that a plant develops against a broad spectrum of plant pathogens after colonisation of the roots by certain strains of microorganisms (van Loon et al. 1998). Research on these lines has led to the identification of several species of microorganisms with strong activity and microbial components such as lipopolysacharides, flagella, siderophores, cyclic lipopeptides, 2,4-diacetylphloroglucinol, homoserine lactones and certain volatiles (Lugtenberg and Kamilova 2009) as elicitors of induced systemic resistance. Induced systemic resistance in plants by rhizobacteria has been proved against several bacterial, fungal and viral plant diseases (Leeman et al. 1995; Park et al. 2009). Induced systemic resistance involves jasmonate and ethylene signalling within the plant, and these hormones stimulate the host plant’s defence responses against a variety of plant pathogens (Glick, 2012). The term induced systemic tolerance (IST) has been proposed for PGPR-induced physical and chemical changes that result in enhanced tolerance to abiotic stress (Sarma et al. 2012). Induced systemic tolerance to salt stress was also noted in a study with Arabidopsis (Zhang et al. 2008) using B. subtilis GB03, a commercial biological control agent. Some of the volatiles organic compounds emitted from Bacillus (Ryu et al. 2004) are believed to be bacterial determinants involved in induced systemic tolerance.

7 Conclusion

The costs associated with soil salinity are potentially enormous, and the effects of salinity may impact heavily on agriculture, biodiversity and the environment. As the saline areas under agriculture are increasing every year across the globe, it is of much public concern. Salt-stressed soils are known to suppress the growth of plants. Salinity also disturbs the sustainability of beneficial microorganisms associated with the plant rhizosphere. There is a growing worldwide demand for sound, ecologically compatible and environmentally friendly techniques in saline soil agriculture. Application of certain beneficial microorganisms, PGPRs, is an important alternative to some of the traditional agricultural techniques, and it is now widely in practice. PGPRs that live in association with plant–roots offer enhanced plant growth and stress alleviation by various means. Salt-tolerant PGPRs have own mechanisms for osmotolerance and could provide a significant benefit to the plants grown in saline soils, in terms of osmotolerance, better growth, vigour and yield. PGPRs enhance plant growth by several different mechanisms such as asymbiotic N2 fixation, solubilisation of mineral phosphate and other essential nutrients, production of plant hormones and other. Bacterial production of 1-aminocyclopropane-1-carboxylate deaminase, induced systemic resistance, IST and control of phytopathogenic microorganisms in the rhizosphere are also modes of support to the plant. PGPRs mitigate salt stress in crops by enhancing osmolyte accumulation in plants, increasing K+ concentration and maintaining a high K+/Na+ ratio and scavenging ROS generated by plants with bacterial antioxidative enzymes, etc. PGPR-mediated saline stress alleviation in plants have been reported in many of crops grown in various geographical locations.

Commercial application of microbial inoculants to improve crop growth and yield in saline environments is a potential strategy for saline soil agriculture. There are several PGPR inoculants currently commercialised that promote growth or control pathogens or induce systemic resistance against pathogens or bring about mitigation of stress tolerance through at least one mechanism. The potential PGPR isolates are formulated using different organic and inorganic carriers either through solid or liquid fermentation technologies. Use of PGPR consortium with known functions that could act synergistically is of interest as they offer multiple modes of action, and temporal or spatial variability. Understanding the interaction between consortium of microbial inoculants and plant systems will pave way to harness more benefits from microbial inoculants for improving plant growth and enhancing tolerance to stress.