Mitigation of Salinity Stress in Plants by Arbuscular Mycorrhizal Symbiosis: Current Understanding and New Challenges

Abstract

Modern agriculture is facing twin challenge of ensuring global food security and executing it in a sustainable manner. However, the rapidly expanding salinity stress in cultivable areas poses a major peril to crop yield. Among various biotechnological techniques being used to reduce the negative effects of salinity, the use of arbuscular mycorrhizal fungi (AMF) is considered to be an efficient approach for bio-amelioration of salinity stress. AMF deploy an array of biochemical and physiological mechanisms that act in a concerted manner to provide more salinity tolerance to the host plant. Some of the well-known mechanisms include improved nutrient uptake and maintenance of ionic homeostasis, superior water use efficiency and osmoprotection, enhanced photosynthetic efficiency, preservation of cell ultrastructure, and reinforced antioxidant metabolism. Molecular studies in past one decade have further elucidated the processes involved in amelioration of salt stress in mycorrhizal plants. The participating AMF induce expression of genes involved in Na⁺ extrusion to the soil solution, K⁺ acquisition (by phloem loading and unloading) and release into the xylem, therefore maintaining favorable Na⁺:K⁺ ratio. Colonization by AMF differentially affects expression of plasma membrane and tonoplast aquaporins (PIPs and TIPs), which consequently improves water status of the plant. Formation of AM (arbuscular mycorrhiza) surges the capacity of plant to mend photosystem-II (PSII) and boosts quantum efficiency of PSII under salt stress conditions by mounting the transcript levels of chloroplast genes encoding antenna proteins involved in transfer of excitation energy. Furthermore, AM-induced interplay of phytohormones, including strigolactones, abscisic acid, gibberellic acid, salicylic acid, and jasmonic acid have also been associated with the salt tolerance mechanism. This review comprehensively covers major research advances on physiological, biochemical, and molecular mechanisms implicated in AM-induced salt stress tolerance in plants. The review identifies the challenges involved in the application of AM in alleviation of salt stress in plants in order to improve crop productivity.

Keywords: antioxidants; aquaporins; arbuscular mycorrhizal fungi; ionic homeostasis; osmotic balance; photosynthetic efficiency; salinity.

FIGURE 1

Differential response of non-mycorrhizal and mycorrhizal plants under salt stress. Accumulation of salt in soil creates competition for nutrient uptake and transport. This leads to imbalance of the ionic composition of plant, thereby affecting plant’s physiological traits. AMF increase the volume of soil explored by plant roots, upregulate several cation transporters, leading to improved nutrient uptake, and also maintains ionic homeostasis. Salinity lowers soil water potential causing cellular dehydration due to decrease in water uptake. AM negates this effect by mediating accumulation of osmolytes and also improves plant’s water status by improving root hydraulic conductivity. Salinity induces oxidative stress due to imbalance in ROS (reactive oxygen species) generation and the quenching activities of antioxidants. AMF are known to improve both enzymatic and non-enzymatic antioxidant systems of plants. Photosynthesis is also negatively affected by salinity. AM has a positive effect on photosynthesis under salt stress. Overall, AMF improve the performance of plant under salt stress.

FIGURE 2

Role of transporter proteins in maintaining favorable K⁺:Na⁺ ratio in salt stressed plants. Salinity renders more concentration of Na⁺ and Cl^- in the soil. This results in imbalance in the ion uptake by plants. Na⁺ and K⁺ have similar physico-chemical nature and hence compete at their transport sites for entry into root symplast. Salt stress results in higher Na⁺ uptake and thus its cellular composition increases, leading to disruption of enzyme activity, protein synthesis, turgor maintenance, and so on. Plants counteract such negative effects by maintaining lower cellular Na⁺ content by activating certain cation transporters such as NHXs (sodium/hydrogen exchanger), SOS (salt overly sensitive), SKOR (outward rectifying K⁺ channel), HKT (high affinity potassium transporters), and AKT (inward rectifying K⁺ channel). NHXs are vacuolar Na⁺/H⁺antiporters. They help in maintaining lower cellular Na⁺ content by sequestering Na⁺ inside the vacuole. SOS1 is a plasma membrane Na⁺/H⁺ antiporter that extrude Na⁺ from the cytosol. It helps in reallocation of Na⁺ in roots and shoots. HKTs are Na⁺/K⁺ transporters that act in removing Na⁺ from the xylem stream and translocating it into the xylem parenchyma. SKOR mediates translocation of K⁺ toward shoot through xylem. AKT is a K⁺ channel present in phloem and mediate influx of K⁺ to shoots.

FIGURE 3

Salinity stress induced osmotic stress tolerance mechanism in plants. Salinity leads to build up of Na⁺ and Cl^- in soil, consequently lowering the soil water potential as compared to water potential of plant cells. This leads to reduced water uptake by plants and eventually causes cellular dehydration. Plants, in order to avoid such consequences, accumulate osmolytes, such as proline, trehalose, polyamines, and sucrose in higher concentration. Osmolytes accumulation results in lowering of cellular water potential and thereby maintains a favorable gradient for water uptake from soil to root. Thus, it prevents cellular dehydration and subside osmotic stress caused by salinity. AM symbiosis alleviates osmotic stress by influencing the expression of specific genes (P5CS, pyrroline-5-carboxylate synthase; TPS, trehalose-6-phosphate synthase; SPS, sucrose phosphate synthase; SS, sucrose synthase) involved in the biosynthesis of osmolytes.

FIGURE 4

Salinity stress induced oxidative stress tolerance mechanism in plants. Salinity causes oxidative stress in plants due to redox imbalance resulting from disturbance in equilibrium between ROS (reactive oxygen species) and antioxidants. Increased ROS concentration in the cell results in protein denaturation, membrane peroxidation, and nucleic acid denaturation. This consequently disturbs the normal functioning of the cell. To counteract the adverse consequences, plants induce antioxidative pathways (enzymatic and non-enzymatic). Enzymatic antioxidants include superoxide dismutase (SOD), peroxidase (POX), catalase (CAT), ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), and glutathione reductase (GR). Non-enzymatic antioxidants include ascorbate (AsA), glutathione (GSH), carotenoids, and α-tocopherol. An efficient antioxidative system abates the oxidative damage in plants. AM symbiosis reinforces the tolerance mechanism of plants to salinity induced oxidative stress.