Abstract
A large number of studies have indicated that salinity stress and saline soils are cruel environmental limiting factors that retard the growth of crop plants. Present scenario of climate change will further increase the border of the area affected by saline soils, and therefore this phenomenon will threaten the productivity of crops leading to depletion of food sources of human societies. Various strategies including soil quality management policies, improving crop resistance against salinity stress, detoxification of noxious ions, improving the quality of irrigation water, and many other effects need to be examined to decrease the detrimental consequences associated with saline soils. In this context, the use of microorganisms especially plant growth-promoting rhizobacteria (PGPR) has been proposed as a sustainable way to fortify the quality of soils to help crop plants grow under salinity stress. Recent advances in molecular soil biology studies suggested that PGPR are involved in the important physiological process associated with plant growth and development. Among the other mechanisms, improvement in water and nutrient uptake, decrease in the toxicity of hazardous ions, amelioration of photosynthesis, improvement in nitrogen fixation, regulation/modulation of physiological signaling networks are the common features exhibited by PGPR to enhance the growth of plants in saline soils. Thus, it should be noted that these miracle bacterial species are legendary soil guards to protect both soil texture and crop plants from salinity stress in the light of present and upcoming global climate changes.
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2.1 Introduction
The upcoming global climate changes have drastically affected the productivity of crop plants. The increased weather temperature, an imbalance in CO2 concentration, the delayed winter rainfall pattern, the drought stress, the modified micro- and macro-ecosystems, and more importantly soil salinity are the key issues associated with global climate changes. The constant erosion of the earth’s crust causes the worldwide geological changes. The main, and perhaps most important, consequent associated with earth erosion is the exchange of soil ion contents. An enormous number of chemical compounds including sodium, calcium, chloride sulfate, carbonate, manganese, and other mineral and non-mineral elements are deformed or widely spread throughout the soil texture.
The presence of these elements in the soil will change the quality of soils (especially those are currently used to cultivate crop plants), and therefore they will lose their potential to provide water and nutritional elements for plants to grow (Amozadeh and Fazeli-Nasab 2012). In addition to the earth’s crust erosion, the quality of irrigation water is another important factor to change the portion of toxic ions in soils. Many studies have reported that the excessive irrigation and poor/inadequate drainage are two factors that increase the salinity of soils (Ilangumaran and Smith 2017). Though the amount of stored salts in the soil structure is directly dependent on soil type, nonetheless the quality and quantity of water for irrigation can enhance the soil salinity by changing the total amount of ions present in each layer of soils (Phogat et al. 2018).
Normally, irrigation water contains 0.1–4 kg m−2 salt, and this amount of water is used annually in 1–1.5 m. So, an annual amount of 1–160 tons per hectare of salt is added to agricultural land. Irrigation water evaporates and its salts remain in the soil. For saltiness, these salts should be removed from the root area of the plants by leaching and drainage techniques. There is also evidence that farmers traditionally replaced resistant plants with susceptible plants, in dealing with the salinity problem. However, use of substitute plants to deal with salinity is likely to be used as a method for a long time before the leaching technique. Substitution of saline-resistant plants is used instead of susceptible plants in saline soils in the world. Some plants, such as sugar beet, barley, cotton, sugarcane, asparagus, and dates, have a high resistance to salinity (Kafi and Mahdavi-Damghani 2005).
The increasing demand for food production (especially for cereal plants) with a significant reduction in the use of chemical agents including herbicides, fungicides, pesticides, and synthetic fertilizers is a huge global concern to affect the future of agricultural systems. A huge number of scientific studies have reported that PGPR are environmental friendly microorganisms to increase the productivity of crop plants in modern agriculture epoch. In addition to their roles in the preparation of mineral and other chemical compounds for plant root system, they also exhibit their biological activities through direct and/or indirect interaction with other soil microorganisms to provide specific environment to fortify the growth of plants (Vejan et al. 2016). PGPR can protect plants from the harmful effects of pertaining to the environmental stresses including flooding, drought, salinity, heavy metals, and phytopathogens (Mayak et al. 2004; Yildirim et al. 2006) and also manage some of these operates through specific enzymes, which stimulate physiological changes in plants at the molecular level. Among these enzymes, ACC deaminase regulates plant hormones such as ethylene (Glick 2005; Arshad and Frankenberger 2012); on the other hand, PGPR stimulate plant growth through the activity of the enzyme ACC deaminase, which causes lower plant ethylene levels resulting in longer roots (Shah et al. 1998).
2.2 Salinity
Salinity is one of the major limiting factors that cause osmotic stress and decrease plant growth and crop productivity in arid and semiarid regions. In salinity process, increase in concentration of soluble salts in the root zone is one of the major complications, and also the rhizospheric populations affect the plant productivity (Cicek and Cakirlar 2002; Tank and Saraf 2010; Fazeli-Nasab 2018).
2.3 Adverse Effects of Salinity
2.3.1 Physiological and Morphological Disturbances
Salt stress reduces many aspects of plant metabolism like growth and yield. Salinity stress increases Na+, which eventually decreases Ca2+ and K+ (Yildirim et al. 2006). Accumulation of Na+ can cause metabolic disturbances in some processes where Na+ (low) and K+ or Ca+2 (high) are required for optimal functioning and growth (Marschner 1995; Xu et al. 1999). The ability of cells to save salts is exhausted; salts build up in the intercellular space and then kill cells and organs (Sheldon et al. 2004). At higher status of available salt, the leaf area, size, and leaf production are reduced leading to the death of the plant (Suárez and Medina 2005).
2.3.2 Disturbances in Photosynthesis
Increasing salinity in the soil decreased some plant mechanisms like photosynthesis, chlorophyll content, and stomatal conductance, and all of these mechanisms will decrease photosynthetic capacity due to the osmotic stress and partial closure of stomata (Drew et al. 1990; Han and Lee 2005; Azad et al. 2017). Accumulation of Cl− disrupts photosynthetic cycle.
2.3.3 Effects on Plant Growth and Crop Yield
Soil salinity limits plant growth and crop production in many parts of the world, particularly in arid and semiarid areas. However plants can suffer from membrane destabilization and general nutrient imbalance (Hasegawa et al. 2000; Parida and Das 2005). Plants after exposure by salt accumulate different molecules in their organics like proline, glucose, and glycine betaine.
Salinity tolerance can be defined by maintaining plant growth in an environment containing NaCl or a mixture of salts. Bray (1997) defined salt tolerance as having a negative effect on the growth of plants that store salt in their tissues, and also Maas and Hoffman classified crops into four groups on the basis of their tolerance to salinity: (i) relatively tolerant plants, (ii) resistant plants, (iii) semi-sensitive plants, and (iv) sensitive plants (Table 2.1).
2.3.4 Mechanisms to Combat Salinity Stress
Most of the salinity problems in higher plants are due to an increase in sodium chloride, which has spread to soils in the dry and coastal areas and their water resources. The high salinity of sodium chloride causes at least three types of problems in higher plants: (1) The osmotic pressure of the external solution results in an increase in the osmotic pressure of the plant cells, which requires osmotic regulation of the plant cells in order to avoid waste. (2) Removal and transfer of nutrients such as potassium and calcium ions are interrupted by excess sodium. (3) High levels of sodium and chlorine produce direct toxic effects on membrane and enzyme systems. Osmotic stress is induced in plants under drought stress conditions, and since about 100 years ago, the term salinity stress is a form of physiological drought (Rengel 1992; Ding et al. 2018).
Some of the mechanisms for avoiding salinity are presence of small leaves to reduce transpiration, fewer stomata per leaf area, the presence of thick cuticle, and an increase in root-to-crown ratio. In the atmosphere, by regulating the osmotic content of sugars, the Na+ and Cl− levels are limited to the limb (Reich et al. 2017).
Resistance to salinity can be elevated through five major strategies:
- 1.
Resistance to salinity in plants by improving traditional breeding and selection.
- 2.
In the development of plants, along with their ancestors, they may acquire the trait of salinity resistance.
- 3.
Farming of species that have salt tolerance (halophytes) can be identified, cloned, and inoculated by modification and selection for the development of their agronomic characteristics.
- 4.
Salinity resistance genes.
- 5.
Salinity-resistant plant growth-promoting rhizobacteria (Carter et al. 2012).
Plant growth responds to salinity in two stages: (1) a rapid stage (osmotic phase that inhibits growth of young leaves) and (2) a slower stage (ionic stage that accelerates senescence of mature leaves) (Munns and Tester 2008). The ability of plantsagainst salt condition is determined by several biochemical pathways that make easy retention and/or acquisition of water, protect chloroplast functions, and maintain ion homeostasis (Parida and Das 2005).
2.3.5 Production of Phytohormones
Studies have shown that indoleacetic acid and cytokinin are produced from amino acids such as tryptophan and adenine which secreted from the roots. Ethylene precursor is hydrolyzed to 1- amino cyclopropane, 2-carboxylic acid (1-aminocyclopropane-1-caboxylic, ACC) by enzyme ACC deaminase (Zahir et al. 2004). Activities of PGPR cause physiological changes in the morphology of the plant, and the set of these changes have a positive effect on growth, nutrition, and plant health.
2.3.6 Plant Hormones
2.3.6.1 Ethylene
The evolution of roots approximately 400 million years ago opened up the biological colonization of the land (Jackson 2017). Ethylene is a gaseous plant growth hormone produced endogenously by almost all plants and even in soil that plays a key role in inducing several physiological functions (Saleem et al. 2007).
The hormone ethylene also known as a stress hormone is released as a physiological response to different stresses such as edaphic and adaphic. Salinity can increase biosynthesis rate of ethylene via elevated levels of ACC, which may lead to physiological changes in plant tissues. Any check on this accelerated ethylene production in plants can improve growth of plants under salt stress (Hontzeas et al. 2004).
2.3.6.2 The Effect of Ethylene in Root Growth and Development
Ethylene was known as a stress hormone that is released by the plant as a physiological response when exposed to a different kind of stresses. It has been observed that plants inoculated with PGPR having ACC deaminase activity are more resistant to the deleterious effect of stress ethylene synthesized as a consequence of stress conditions (Penrose and Glick 2003; Zahir et al. 2004). Ethylene is of great importance in plant growth and development and also in some functions like inhibition of seed germination and root growth (Nordström and Eliasson 1984). As after germination, high level of ethylene would inhibit root elongation. Inhibition of the root elongation has been prevented due to inoculation of PGPR capable of containing ACC deaminase even in the presence of high (6%) concentration of salts, NaCl (Tank and Saraf 2010). PGPR inoculation helped in seed germination followed by lowering the plant’s ethylene concentration, thereby decreasing the ethylene inhibition of seedling root length, while in many plants a burst of ethylene is required to break seed dormancy (Nascimento 2003).
2.3.6.3 Stress/Wound Ethylene
The term stress is used for an external factor capable of inducing a potentially injurious strain in living organisms. Stress ethylene is one of the general phenomena observed in plant tissues subjected to various unfavorable conditions (Hyodo 2017). Several kinds of stress are related to ACC such as effects of phytopathogenic bacteria and resistance to stress from polyaromatic hydrocarbons and from heavy metals (Glick et al. 2007). Plant seed inoculated with biocontrol bacteria strongly decreases plant diseases level and may help to protect fieldworkers from exposure to pathogens (Egamberdieva et al. 2008).
Bacterial strains containing ACC deaminase can, in part, at least alleviate the stress-induced ethylene-mediated negative impact on plants (Glick et al. 1998; Glick 2005; Safronova et al. 2006). It reported that ACC deaminase bacteria conferred salt tolerance onto plants by lowering the synthesis of salt-induced stress ethylene and promoted the growth of canola in the saline environment, and also it is related that in plants Cd is the strongest heavy element inductor of ethylene biosynthesis (Cheng et al. 2007).
Ethylene production in plants is induced by various environmental factors such as wounding, physical load, disease, drought, waterlogging, chilling temperature, and exposure to various chemicals (Hyodo 2017). There is evidence that treatment with aminoethoxy vinyl glycine (AVG) prevents ethylene inhibition of root elongation (Hall et al. 1996) and also ethylene inhibitors can decrease the negative effect and the expression of stress symptoms induced by ethylene in plants (Rost et al. 1986; Elad 1990).
2.3.6.4 ACC Deaminase and Its Biochemistry
Inoculation of PGPR in pepper, bean, canola, and lettuce under salt stress has been used for mitigating the effects of salinity. Reports also showed an improvement of squash plant when applied directly or as a transplant under salinity stress (Yildirim et al. 2006).
The enzyme ACC deaminase cleaves ethylene, and also for many plants a burst of ethylene is required to break seed dormancy and germination; however, higher levels of ethylene inhibits the root elongation (Ali-Soufi et al. 2017; Soni et al. 2018). Plants that are treated with ACC deaminase-producing PGPR have been shown to exhibit more resistant to the deleterious effects of stress ethylene synthesized as a consequence of stressful conditions such as flooding (Grichko and Glick 2001), heavy metals (Grichko et al. 2000), the presence of phytopathogens (Wang et al. 2000), drought, and high salt conditions (Penrose and Glick 2003).
The activity of ACC deaminase has been widely reported in different species of Gram-negative bacteria (Wang et al. 2000; Babalola et al. 2003), Gram-positive bacteria (Belimov et al. 2001; Ghosh et al. 2003)), rhizobia (Ma et al. 2003), endophytes (Pandey et al. 2005), and fungi (Jia et al. 1999). ACC deaminase is prevalent in different kinds of bacteria, viz., Agrobacterium and Azospirillum (Blaha et al. 2006), Alcaligenes and Bacillus (Belimov et al. 2001), Burkholderia (Blaha et al. 2006), Enterobacter (Penrose and Glick 2001), Methylobacterium (Madhaiyan et al. 2006), Pseudomonas (Belimov et al. 2001), Ralstonia solanacearum (Arshad and Frankenberger Jr 2012), Rhizobium (Ma et al. 2003), Rhodococcus (Stiens et al. 2006), Sinorhizobium meliloti (Belimov et al. 2001), and Variovorax paradoxus (Glick 2005). Owing to ACCD activity, these bacteria are known to help plant grow under biotic and abiotic stresses condition by decreasing the level of “stress ethylene” which is inhibitory to plant growth (Singh et al. 2015). The ACC deaminase enzyme produced by several rhizobacteria catalyzes and reduces the deleterious ethylene level (Soni et al. 2018) that acts as a sink for ACC and protects stressed plants from deleterious effects of stress ethylene (Glick 2005). Reports also showed that inoculation of plant with ACC deaminase containing PGPR has also resulted in enhanced chlorophyll contents of maize and lettuce (Han and Lee 2005; Tank and Saraf 2010).
The ability of a newly isolated ACC-utilizing bacterium, Kluyvera ascorbata SUD165, to improve the growth of canola, tomato, and Indian mustard seedlings treated with toxic concentrations of nickel, lead, and zinc has recently been demonstrated (Shah et al. 1998; Burd et al. 2000; Safronova et al. 2006).
2.4 Mechanisms of Salt Tolerance
2.4.1 Cytoplasmic Osmotic Regulation
Halophilic bacteria accumulate more salt in the protoplasm than those that are present in the external solvent medium through active ion harvesting; therefore, the intracellular water pressure remains negative in comparison with the external solution and its enzymatic systems evolved in a manner that is carried out under conditions of high salt levels in the protoplasm. Marine algae also use their own special organic solutions for osmotic regulation to keep their sodium cytoplasm concentration low (Ashraf and Wu 1994; Cao et al. 2017). One of the problems of salt stress is the reduction of the osmotic potential of the soil solution, so that the plant can absorb water from the soil. It should reduce the osmotic potential to less than the osmotic potential of the soil.
2.4.2 The Accumulation of Substances in Vacuole
Most of the high salinity plants accumulate sodium and potassium for osmotic regulation in vacuole. However, some grasses may also use organic solvents in vacuole (Srinivas et al. 2018). In this method, sodium transfer from cytoplasm to vacuole and also the return of potassium from vacuole to cytoplasm are performed by pumps. In this way, in addition to reducing the toxicity of sodium ion in the cytoplasm, the osmotic potential of the cell also decreases (due to the accumulation of salts in the vaccine), and this way the plant will be able to absorb water and salts from the soil. The mechanism of this problem is energy, that is, the transfer of sodium from the cytoplasm to the vaccine and the transfer of potassium from vaccine to cytoplasm with energy.
2.4.3 Absorption and Replacement of Ions
The first line of defense against the addition of excess sodium into the plant is the plasma membrane of the root cell, which has low sodium permeability in all studied species. Conversely, root cells have shown a high tendency to absorb potassium, which can accumulate unlike concentration slopes (Pitman et al. 1981; Mangalassery et al. 2017). Plants that tolerate low salinity under high concentration of sodium in the root environment show a significant reduction in potassium uptake and increase sodium uptake in the shoot (Rains 1969; Makhlouf et al. 2015).
2.4.4 Movement Paths Along the Root
Water and salts can enter the root through two paths of symplast and apoplasts. Symplast is through the cytoplasmic pathway of the root cells, which extends from the epidermis to the root of the brain and is related through the connections between the adjacent cells. Apoplasts transfer material through cell walls. Entering the symplast route is the most important control point for entering salt into the plant. The water entering the apoplastic pathway is more similar to that of the intracellular solution than with the solution outside the root, although the concentration of apoplastic salt can be corrected by absorbing into the cells along the path and by exchanging the ion walls of the cell (Tester and Davenport 2003; Reddy et al. 2017). If the only route for the transfer of salts to the xylem is apoplastic pathway, air organs should be full of salt, however, the existence of a casparian strip makes this necessary that salts and water should pass through endoderm via the entrance of the symplastic system. It has been determined that thoracic plants often have a thick layer of cork, or dendritic cellulose cells have endoderm, while mesophytes often have a thin layer of casparian strip (Esashi 2017; Zarayneh et al. 2018).
2.4.5 Recovery of Sodium from Transpiration
When the water and soluble substances reach the root from the symplast they will be transfered from xylem to the air organs. Xylem parenchyma not only prevents the entrance of salts into the transpiration system, but also can reduce salts concentration in Sap via reabsorption of salts from transmitance of root to air oragns in transpiration system. The sodium in xylem is transmited to the Phloem in the base of stem by active transport which significantly reduces the amount of sodium in the transpiration. This conclusion was achived based on the experiments that aerial parts of the stem were wounded in a circular manner so that the phloem were disconnected but xylem left in a natural state. Then, Na22 was applied to the environment and it was observed that the plants with injured stem transmitted higher radioactive sodium to the leaves (about 84%) compared to the uninjured stems. Probably, the readsorbed salts are returned to the tip of the root inside the phloem (Gleason et al. 2017; Keisham et al. 2018).
2.4.6 Control of Salinity Levels in Leaves
The amount of salt in the transpiration pathway is lower than that of the extra-root solution even from salt accumulation pools, for example, barley, grown in 150 mM of NaCl in its transpiration pathway, has about 5 mM of sodium chloride (Rains 1969; Makhlouf et al. 2015). Rice, wheat, and barley have two adaptation methods to tolerate salts that reach the air organs – (1) salting by growth and (2) distribution of salts to older leaves – after the accumulation of salt in older leaves, they disappear, and thus the amount of salt in the plant decreases (Munns 1993; Sarabi et al. 2017).
2.4.7 Tubers and glandular trichomes
Susceptible plants often have specific methods for managing salt in the leaves. Examples of these mechanisms are the tubers and glandular trichomes for the removal of salts to the outer surfaces of the leaves. Salt glands are known in at least 11 plant families (10 dicotyledons and 1 cotyledon family, Gramminae). Salt tubers in gramminae contain two cells, one of which is base and the other is a warhead cell. Solar cells are collected by the base cell and driven out of the warhead cell. Both cells have dense cytoplasm with a large number of mitochondria and lack central vasculature. Anatomical sacks are distinguished from salt glands in the spinach family. Particularly in Atriplex, where all 200 species have salt bags that contain outburst cavities that include a long and narrow leg and a cell-like cell at the top of the epidermis, different species of Atriplex can be identified from the shape of their salt bags. The salt solution is transmited from mesophilic cells to glandular trichomes through stem cells agianst the gradient concentration. The salt accumulates in the central vacuolic glandular trichomes, which is eventually torn and is released at the surface of the leaf. Accumulated salts in the surface of the leaf may reduce transpiration and increase light reflection; more than 80% sodium chloride entering the Atriplex leaves may be removed through glandular trichomes (Akbar et al. 1972; Hairmansis et al. 2017).
2.4.8 Broiling to Regulate Osmotic Pressure in Leaves
All salt-tolerating plants are not able to excrete salts. Many salinity-resistant and nonsaline plants tolerate temporary increase of salt in apoplasts by increasing the amount of mesophilic cell water and therefore dilutes the salts and increases their capacity to absorb the salt from the apoplast solution (Kramer 1984; Joshi et al. 2015).
2.5 Conclusion
The salinity stress and saline soils are cruel factors that adversely affect the growth of crop plants leading to decrease in agriculture productivity and hence depletion of food sources of human societies. Salinity is one of the major limiting factors that cause osmotic stress and decrease plant growth and crop productivity in arid and semiarid regions. Salt stress reduces many aspects of plant metabolism like growth and yield. Most of the salinity problems in higher plants are due to an increase in sodium chloride which has spread to soils in the dry and coastal areas and their water resources. More importantly salinity in the soil decreases plant mechanisms like photosynthesis, chlorophyll content, stomatal conductance, membrane destabilization, and general nutrient imbalance. To mitigate the salinity, many strategies including soil quality management policies, use of saline resistance varieties, detoxification of noxious ions, improvement in the quality of irrigation water etc. have been in practice. However all these strategies pose limitations and are not sustainable; in this context, the use of microorganisms especially PGPR has been proposed as a sustainable and eco-friendly way to fortify the quality of soils to help crop plants grow under salinity stress. PGPR are involved in the important physiological process associated with plant growth and development under salinity. Among the various strategies adopted to elevate salinity use of halophilic, PGPR seems to be the best alternatives. PGPR elevate salinity or exhibit tolerance to salinity through the regulation of production of stress hormone ethylene under the influence of ACC deaminase, osmotic regulation, and accumulation of salts in their cytoplasm and absorption and replacement of ions. PGPR are responsible for increasing nutrient uptake, decreasing the toxicity of hazardous ions, amelioration of photosynthesis, improvement in nitrogen fixation, regulation/modulation of physiological signaling networks, etc. These miracle bacterial species are legendary soil guards to protect both soil texture and crop plants from salinity stress.
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Fazeli-Nasab, B., Sayyed, R.Z. (2019). Plant Growth-Promoting Rhizobacteria and Salinity Stress: A Journey into the Soil. In: Sayyed, R., Arora, N., Reddy, M. (eds) Plant Growth Promoting Rhizobacteria for Sustainable Stress Management . Microorganisms for Sustainability, vol 12. Springer, Singapore. https://doi.org/10.1007/978-981-13-6536-2_2
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