ReviewPhysiological and biochemical perspectives of non-salt tolerant plants during bacterial interaction against soil salinity
Introduction
Glycophytes are plants that can grow optimally in soil containing low sodium concentrations and their survival is adversely affected by the accumulation of salt in soil (Horie et al., 2012). Several crop plants are glycophytes and their growth and yields are considerably reduced by global climatic changes, including low precipitation, high rate of evaporation, and irrigation using hard water (Shrivastava and Kumar, 2015). The rate of salinized arable land is increasing annually by 10% and it has been assessed that ∼50% of agricultural land would be salinized by 2050 (Jamil et al., 2011). Crop productivity is declining yearly owing to the adverse effects of soil salinity. To prevent food scarcity for the increasing human population, several studies from different perspectives are being conducted to enhance the stress tolerance of crop plants grown in saline soils using diverse strategies. Although traditional crop breeding has been practiced to develop tolerance to salt stress, only limited success has been achieved owing to the complex genetic nature of this trait (Flowers, 2004). Further, transgenic plant technology and molecular breeding applications to develop salt-tolerant agricultural plants have also achieved limited success (Bhatnagar-Mathur et al., 2008, James et al., 2008, Wang et al., 2003). Alternately, substances that mitigate salt stress and promote plant growth, such as phytohormones (Khadri et al., 2006), triacontanol (Radhakrishnan and Ranjitha-Kumari, 2008), and polyamines (Radhakrishnan and Lee, 2013) have been considered beneficial in increasing the salt stress tolerance in crop plants. Some of the physical factors (gamma irradiation and magnetic field) pre-treatment could mitigate the toxic effects of salt stress in crop plants (Baek et al., 2005, Radhakrishnan et al., 2012).
There is some evidence that some microorganisms have the potential to help alleviate salinity stress. Generally, plants are anchored in soil to absorb water and nutrients and for physical support. Soil contains nutrients as well as biologically important macro and microorganisms (Barber, 1995, Edwards and Fletcher, 1988). The beneficial effects of microorganisms (such as bacteria and fungi) on plant growth are well documented (Kang et al., 2014a, Kang et al., 2014b, Radhakrishnan and Lee, 2015). The chloroplast and mitochondria in the plant cell are evolutionarily considered as endophytic symbionts that have evolved from free-living bacteria (Margulis, 1970). This understanding has strongly indicated that soil microbes and plants have mutually interacted for their growth and survival. Microorganisms beneficial to plants secrete metabolites that solubilize the complex organic substances into simpler forms making them easily available to plants, enhance plant growth, and protect plants from diseases and other abiotic stresses (Bianco and Defez, 2009, Karlidag et al., 2013, Lopez-Gomez et al., 2014a, Lopez-Gomez et al., 2014b, Kang et al., 2015a). In particular, bacterial synthesis of aminocyclopropane-1-carboxylate (ACC) deaminase, exopolysaccharides, indole-3-acetic acid (IAA), gibberellins (GAs), hydrogen cyanide (HCN), proline, nodulation factors, 5-aminolevulinic acid, and siderophores, as well as the ability for phosphate solubilization, potassium solubilization, nitrogen fixation, and ammonia production in bacteria can increase the salt stress tolerance in plants (Qurashi and Sabri, 2011, Mohamed and Gomaa, 2012, Kang et al., 2014b, Nunkaew et al., 2014, Munoz et al., 2014, Palaniyandi et al., 2014). The identification of salt-tolerant and plant growth-promoting bacteria could be beneficial in increasing crop yields under conditions of soil salinity (Zahir et al., 2009, Ahmad et al., 2012, Martinez et al., 2015a). Bacterial isolates of Bacillus and Pseudomonas have been widely reported as plant growth-promoting bacteria under salt stress conditions (Table 1). In addition, other bacterial isolates of Achromobacter, Acinetobacter, Aeromonas, Alcaligenes, Arthrobacter, Azospirillum, Azotobacter, Brachybacterium, Brevibacterium, Burkholderia, Clostridium, Curtobacterium, Ensifer, Enterobacter, Exiguobacterium, Geobacillus, Haererohalobacter, Halobacillus, Halomonas, Klebsiella, Kocuria, Methylobacterium, Micrococcus, Nitrinicola, Oceanobacillus, Ochrobactrum, Paenibacillus, Planococcus, Promicromonospora, Raoultella, Rhizobium, Rhodopseudomonas, Serratia, Sinorhizobium, Sphingomonas, Staphylococcus, Streptomyces, and Variovorax genera have been identified and documented as having the capacity to mitigate the toxic effects of salinity stress in plants (Table 1).
Bacteria can survive in unfavorable environmental conditions, including drought, increased salinity, and extreme temperatures by synthesizing specific metabolites to adapt to the harsh environments (Sandhya and Ali, 2015). The inoculation and enrichment of salt-tolerant bacteria populations in salt-affected agricultural lands would be beneficial in enhancing the yields of crop plants. Although, several studies have reported that salt-tolerant bacteria enhance plant growth and yield, only a few studies have focused on the bacteria-induced functional changes in plant physiology and metabolism against salt stress. To understand the mechanism by which bacterial fertilizers mitigate the adverse effects of salinity stress in plants, this review assesses the biochemical and physiological changes induced in salt-stressed plants on interaction with beneficial soil bacteria.
Section snippets
Bacterial metabolites promoting salt tolerance in plants
Bacteria synthesize and secrete various substances that are helpful in conferring tolerance against salt stress in plants. Several salt-tolerant bacteria and their metabolites (listed in Table 1) can mitigate the adverse effects of salinity stress in plants by regulating plant cell physiological conditions. The predominant metabolite, ACC deaminase, is synthesized by Achromobacter, Aeromonas, Alcaligenes, Arthrobacter, Bacillus, Burkholderia, Enterobacter, Klebsiella, Ochrobactrum, Planococcus,
Beneficial effects of bacteria on seed germination and plant growth during salt stress
Under salt stress, the initial stage of plant growth (i.e., seed germination) is the most susceptible stage in the plant life cycle. Soil salinity decreases the rate of seed germination and inhibits plant growth by creating osmotic stress and causing an imbalance in the nutrient uptake (Almansouri et al., 2001, Upadhyay and Singh, 2015). Seed germination is regulated by sugars, nitrate, and phytohormones, such as auxin, cytokinins, ethylene, abscisic acid (ABA), GAs, brassinosteroid (BR) and
Bacterial regulation of plant nutrition and water transport in saline soil
Salt deposition in soil decreases the osmotic potential of the growth medium for plants and reduces the water availability (Mayak et al., 2004). Plants respond to salt-induced osmotic stress by closing their stomata, thus limiting the loss of cellular water content and gas exchange, which reduces the photosynthetic rate (Jones, 1993). Elevated level of Na+ in soil drives exit the water from the plant cell, reducing the cell turgor, photosynthesis, and carbon fixation (Yeo, 1998).
Bacteria-induced photosynthesis in salt-affected plants
Photosynthesis occurs in plant chloroplast and is a major metabolic process for plant survival. The photosynthetic machinery is located in the thylakoid membranes. Salinity-induced oxidative stress damages the thylakoid membranes resulting in the reduction of photosynthetic efficiency (Radhakrishnan and Lee, 2014). In addition, it causes the depletion of the photosynthetic electron chain and redirects the photon energy for reactive oxygen species (ROS) formation (Hichem et al., 2009), which
Role of bacteria as plant growth regulators in salt-stressed plants
GA (a plant growth promoting hormone) regulates the development of plants in both, normal and challenging environments. Salt stress decreases GA synthesis; however, bacterial association with plant roots triggers the endogenous GA production and activates several stress mitigating mechanisms to prevent salt stress-induced damage (Kang et al., 2014b). Bacteria producing phytohormones (IAA and GA) transport their metabolites to roots and enhance plant growth. Radish seeds pretreated with Bacillus
Effect of bacterial applications on antioxidants in plants under salt stress
Singlet oxygen, hydrogen peroxidase, superoxide radical, and hydroxyl radical are ROS generated by chloroplasts, mitochondria, peroxisomes, plasma membranes, endoplasmic reticulum, and cell wall during salinity stress (Choudhury et al., 2013, Das and Roychoudhury, 2014). ROS is an unwanted byproduct that damages lipids, proteins and nucleic acids (Yokoi and Rengel, 2002). The adverse effects of salinity affect lipids and increase lipid peroxidation rate and decrease ROS scavenging enzymes such
Changes in compatible solutes in salt-affected and bacterial co-inoculated plants
Osmotic adjustments in cells also participate in conferring stress tolerance. Compatible solutes such as proline and sugar are well-known osmoprotectants that maintain cell turgor (Weinberg et al., 1982, Mundree et al., 2002) to prevent oxidative stress. Proline content is enhanced in plants during salt stress to stabilize proteins and cell membranes and to scavenge ROS (Claussen, 2005). Some of the compatible solutes, glycine betaine (GB)-like quaternary ammonium compounds (QAC) are not
Genes and proteins expression in bacteria treated plants against salt stress
Salt stress-induced upregulation of SERK1 (somatic embryogenesis receptor-like kinase) and suppression of ethylene responsive element binding proteins (EREBP) is regulated by Bacillus amyloliquefaciens NBRISN13 in rice plants. In addition, salt stress in rice reduces the expression of salt-responsive genes (sodium proton antiporter (NHX1), salt-overly-sensitive 1 (SOS1), gigantea (GIG), betaine aldehyde dehydrogenase (BADH), serine-threonine protein kinase (SAPK4), and sucrose
Conclusions
Although, the symbiotic relationship between bacteria and glycophytic plant species is well-documented in literature, few studies have reported functional changes in plant physiology and metabolism associated with plant-bacterial interaction in saline soil. Bacterial attachment and their metabolites in soil and/or roots balance the nutrient transport and water movement in plants, and also regulate seed germination and plant growth during salt stress. The abnormal physiological functions of
Conflict of interest
The authors declare no conflict of interest.
Author contributions
RR and KHB designed the work, and RR collected the articles and wrote the manuscript. KHB edited the manuscript and both authors approved the final version of this manuscript.
Funding
Systems and Synthetic Agro-biotech Center through the Next-Generation BioGreen 21 Program (PJ011117), Rural Development Administration, South Korea.
Acknowledgments
This work was supported by a grant from the Systems and Synthetic Agro-biotech Center through the Next-Generation BioGreen 21 Program (PJ011117), Rural Development Administration, South Korea.
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