Plant Salinity Tolerance Conferred by Arbuscular Mycorrhizal Fungi and Associated Mechanisms: A Meta-Analysis.
ABSTRACT: Soil salinity often hinders plant productivity in both natural and agricultural settings. Arbuscular mycorrhizal fungal (AMF) symbionts can mediate plant stress responses by enhancing salinity tolerance, but less attention has been devoted to measuring these effects across plant-AMF studies. We performed a meta-analysis of published studies to determine how AMF symbionts influence plant responses under non-stressed vs. salt-stressed conditions. Compared to non-AMF plants, AMF plants had significantly higher shoot and root biomass (p < 0.0001) both under non-stressed conditions and in the presence of varying levels of NaCl salinity in soil, and the differences became more prominent as the salinity stress increased. Categorical analyses revealed that the accumulation of plant shoot and root biomass was influenced by various factors, such as the host life cycle and lifestyle, the fungal group, and the duration of the AMF and salinity treatments. More specifically, the effect of Funneliformis on plant shoot biomass was more prominent as the salinity level increased. Additionally, under stress, AMF increased shoot biomass more on plants that are dicots, plants that have nodulation capacity and plants that use the C3 plant photosynthetic pathway. When plants experienced short-term stress (<2 weeks), the effect of AMF was not apparent, but under longer-term stress (>4 weeks), AMF had a distinct effect on the plant response. For the first time, we observed significant phylogenetic signals in plants and mycorrhizal species in terms of their shoot biomass response to moderate levels of salinity stress, i.e., closely related plants had more similar responses, and closely related mycorrhizal species had similar effects than distantly related species. In contrast, the root biomass accumulation trait was related to fungal phylogeny only under non-stressed conditions and not under stressed conditions. Additionally, the influence of AMF on plant biomass was found to be unrelated to plant phylogeny. In line with the greater biomass accumulation in AMF plants, AMF improved the water status, photosynthetic efficiency and uptake of Ca and K in plants irrespective of salinity stress. The uptake of N and P was higher in AMF plants, and as the salinity increased, the trend showed a decline but had a clear upturn as the salinity stress increased to a high level. The activities of malondialdehyde (MDA), peroxidase (POD), and superoxide dismutase (SOD) as well as the proline content changed due to AMF treatment under salinity stress. The accumulation of proline and catalase (CAT) was observed only when plants experienced moderate salinity stress, but peroxidase (POD) and superoxide dismutase (SOD) were significantly increased in AMF plants irrespective of salinity stress. Taken together, arbuscular mycorrhizal fungi influenced plant growth and physiology, and their effects were more notable when their host plants experienced salinity stress and were influenced by plant and fungal traits.
Project description:A wide range of C3 and C4 plant species could acclimatize and grow under the impact of salinity stress. Symbiotic relationship between plant roots and arbuscular mycorrhizal fungi (AMF) are widespread and are well known to ameliorate the influence of salinity stress on agro-ecosystem. In the present study, we sought to understand the phenomenon of variability on AMF symbiotic relationship on saline stress amelioration in C3 and C4 plants. Thus, the objective was to compare varied mycorrhizal symbiotic relationship between C3 and C4 plants in saline conditions. To accomplish the above mentioned objective, we conducted a random effects models meta-analysis across 60 published studies. An effect size was calculated as the difference in mycorrhizal responses between the AMF inoculated plants and its corresponding control under saline conditions. Responses were compared between (i) identity of AMF species and AMF inoculation, (ii) identity of host plants (C3 vs. C4) and plant functional groups, (iii) soil texture and level of salinity and (iv) experimental condition (greenhouse vs. field). Results indicate that both C3 and C4 plants under saline condition responded positively to AMF inoculation, thereby overcoming the predicted effects of symbiotic efficiency. Although C3 and C4 plants showed positive effects under low (EC < 4 ds/m) and high (>8 ds/m) saline conditions, C3 plants showed significant effects for mycorrhizal inoculation over C4 plants. Among the plant types, C4 annual and perennial plants, C4 herbs and C4 dicot had a significant effect over other counterparts. Between single and mixed AMF inoculants, single inoculants Rhizophagus irregularis had a positive effect on C3 plants whereas Funneliformis mosseae had a positive effect on C4 plants than other species. In all of the observed studies, mycorrhizal inoculation showed positive effects on shoot, root and total biomass, and in nitrogen, phosphorous and potassium (K) uptake. However, it showed negative effects in sodium (Na) uptake in both C3 and C4 plants. This influence, owing to mycorrhizal inoculation, was significantly higher in K uptake in C4 plants. For our analysis, we concluded that AMF-inoculated C4 plants showed more competitive K(+) ions uptake than C3 plants. Therefore, maintenance of high cytosolic K(+)/Na(+) ratio is a key feature of plant salt tolerance. Studies on the detailed mechanism for the selective transport of K in C3 and C4 mycorrhizal plants under salt stress is lacking, and this needs to be explored.
Project description:Arbuscular mycorrhizal fungi (AMF) are often considered bioameliorators. AMF can promote plant growth under various stressful conditions; however, differences between male and female clones in mycorrhizal strategies that protect plants from the detrimental effects of salinity are not well studied. In this study, we aimed to examine the interactive effects of salinity and AMF on the growth, photosynthetic traits, nutrient uptake, and biochemical responses of <i>Morus alba</i> males and females. In a factorial setup, male and female <i>M. alba</i> clones were subjected to three salinity regimes (0, 50, and 200 mM NaCl) and planted in soil with or without <i>Funneliformis mosseae</i> inoculation. The results showed that NaCl alone conferred negative effects on the growth, salinity tolerance, photosynthetic performance, and shoot and root ionic ratios (K<sup>+</sup>/Na<sup>+</sup>, Ca<sup>2+</sup>/Na<sup>+</sup>, and Mg<sup>2+</sup>/Na<sup>+</sup>) in both sexes; in contrast, mycorrhizal inoculation mitigated the detrimental effects of salinity. Furthermore, the mycorrhizal effects were closely correlated with Mn<sup>2+</sup>, proline, and N concentrations. Females benefited more from AMF inoculation as shown by the enhancements in their biomass accumulation, and N, proline, K<sup>+</sup>, Mg<sup>2+</sup>, Fe<sup>2+</sup>, Zn<sup>2+</sup>, and Mn<sup>2+</sup> concentrations than males with mycorrhizal inoculation under saline conditions. In comparison, male plants inoculated with AMF showed improvements in biomass allocated to the roots, P, and peroxidase concentrations under saline conditions. These sex-specific differences suggest that male and female mulberry clones adopted different mycorrhizal strategies when growing under saline conditions. Overall, our results provide insight into the sex-specific difference in the performance of AMF-associated mulberry clones, suggesting that female mulberry could be more suitable for vegetation remediation than the male one, due to its higher salinity tolerance.
Project description:BACKGROUND:The interaction between arbuscular mycorrhizal fungi (AMF) and AMF spore associated bacteria (SAB) were previously found to improve mycorrhizal symbiotic efficiency under saline stress, however, the information about the molecular basis of this interaction remain unknown. Therefore, the present study aimed to investigate the response of maize plants to co-inoculation of AMF and SAB under salinity stress. RESULTS:The co-inoculation of AMF and SAB significantly improved plant dry weight, nutrient content of shoot and root tissues under 25 or 50 mM NaCl. Importantly, co-inoculation significantly reduced the accumulation of proline in shoots and Na+ in roots. Co-inoculated maize plants also exhibited high K+/Na+ ratios in roots at 25 mM NaCl concentration. Mycorrhizal colonization significantly positively altered the expression of ZmAKT2, ZmSOS1, and ZmSKOR genes, to maintain K+ and Na+ ion homeostasis. Confocal laser scanning microscope (CLSM) view showed that SAB were able to move and localize into inter- and intracellular spaces of maize roots and were closely associated with the spore outer hyaline layer. CONCLUSION:These new findings indicate that co-inoculation of AMF and SAB effectively alleviates the detrimental effects of salinity through regulation of SOS pathway gene expression and K+/Na+ homeostasis to improve maize plant growth.
Project description:Microbes living symbiotically in plant tissues mutually cooperate with each other by providing nutrients for proliferation of the partner organism and have a beneficial effect on plant growth. However, few studies thus far have examined the interactive effect of endophytic bacteria and arbuscular mycorrhizal fungi (AMF) in hostile conditions and their potential to improve plant stress tolerance. In this study, we investigated how the synergistic interactions of endophytic bacteria and AMF affect plant growth, nodulation, nutrient acquisition and stress tolerance of Acacia gerrardii under salt stress. Plant growth varied between the treatments with both single inoculants and was higher in plants inoculated with the endophytic B. subtilis strain than with AMF. Co-inoculated A. gerrardii had a significantly greater shoot and root dry weight, nodule number, and leghemoglobin content than those inoculated with AMF or B. subtilis alone under salt stress. The endophytic B. subtilis could alleviate the adverse effect of salt on AMF colonization. The differences in nitrate and nitrite reductase and nitrogenase activities between uninoculated plants and those inoculated with AMF and B. subtilis together under stress were significant. Both inoculation treatments, either B. subtilis alone or combined with AMF, enhanced the N, P, K, Mg, and Ca contents and phosphatase activities in salt-stressed A. gerrardii tissues and reduced Na and Cl concentration, thereby protecting salt-stressed plants from ionic and osmotic stress-induced changes. In conclusion, our results indicate that endophytic bacteria and AMF contribute to a tripartite mutualistic symbiosis in A. gerrardii and are coordinately involved in the plant adaptation to salt stress tolerance.
Project description:Arbuscular mycorrhizal (AM) fungi (AMF) are widely known to form a symbiosis with most higher plants and enhance plant adaptation to a series of environmental stresses. Sweet sorghum (<i>Sorghum bicolor</i> (L.) Moench) is considered a promising alternative feedstock for bioalcohol production because of its sugar-rich stalk and high biomass. However, little is known of AMF benefit for biomass production and salt tolerance of sweet sorghum. Here, we investigated the effects of <i>Acaulospora</i> <i>mellea</i> ZZ on growth and salt tolerance in two sweet sorghum cultivars (Liaotian5 and Yajin2) under different NaCl addition levels (0, 0.5, 1, 2, and 3 g NaCl/kg soil). Results showed AMF colonized the two cultivars well under all NaCl addition levels. NaCl addition increased mycorrhizal colonization rates in Yajin2, but the effects on Liaotian5 ranged from stimulatory at 0.5 and 1 g/kg to insignificant at 2 g/kg, and even inhibitory at 3 g/kg. High NaCl addition levels produced negative effects on both AM and non-AM plants, leading to lower biomass production, poorer mineral nutrition (N, P, K), higher Na<sup>+</sup> uptake, and lower soluble sugar content in leaves. Compared with non-AM plants, AM plants of both cultivars had improved plant biomass and mineral uptake, as well as higher K<sup>+</sup>/Na<sup>+</sup> ratio, but only Yajin2 plants had a low shoot/root Na ratio. AM inoculation increased the activities of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT), and soluble sugar content in leaves. Overall, both cultivars benefited from mycorrhization, and Yajin2 with less salt tolerance showed higher mycorrhizal response. In conclusion, AMF could help to alleviate the negative effects caused by salinity, and thus showed potential in biomass production of sweet sorghum in saline soil.
Project description:BACKGROUND:Halophytes are better than glycophytes at employing mechanisms to avoid salt injury, but both types of plants can undergo damage due to high soil salinity. Arbuscular mycorrhizal fungi (AMF) can mitigate the damage from salt stress in both halophytes and glycophytes by enhancing salt tolerance and improving energy efficiency. However, variations in mycorrhizal symbiotic efficiency between halophytes and glycophytes were still poorly understood. Therefore, we evaluated the magnitude of AMF effects on plant growth and determined the mechanisms that regulate the growth response of halophytes and glycophytes by performing a meta-analysis of 916 studies (from 182 publications). RESULTS:Arbuscular mycorrhizal fungi significantly enhance biomass accumulation, osmolytes synthesis (soluble sugar and soluble protein), nutrients acquisition (nitrogen, phosphorus, and potassium ion), antioxidant enzyme activities (superoxide dismutase and catalase), and photosynthetic capacity (chlorophyll and carotenoid contents, photosynthetic rate, stomatal conductance, and transpiration rate). AMF also substantially decreased sodium ion acquisition and malondialdehyde levels in both halophytes and glycophytes under salt stress conditions. Mycorrhizal halophytes deploy inorganic ions (potassium and calcium ions) and limited organic osmolytes (proline and soluble sugar) to achieve energy-efficient osmotic adjustment and further promote biomass accumulation. Mycorrhizal glycophytes depend on the combined actions of soluble sugar accumulation, nutrients acquisition, sodium ion exclusion, superoxide dismutase elevation, and chlorophyll synthesis to achieve biomass accumulation. CONCLUSIONS:Arbuscular mycorrhizal fungi inoculation is complementary to plant function under salt stress conditions, not only facilitating energy acquisition but also redistributing energy from stress defence to growth. Glycophytes are more dependent on AMF symbiosis than halophytes under salt stress conditions.
Project description:<h4>Background and aims</h4>Plant biomass-density relationships during self-thinning are determined mainly by allometry. Both allometry and biomass-density relationship have been shown to vary with abiotic conditions, but the effects of biotic interactions have not been investigated. Arbuscular mycorrhizal fungi (AMF) can promote plant growth and affect plant form. Here experiments were carried out to test whether AMF affect plant allometry and the self-thinning trajectory.<h4>Methods</h4>Two experiments were conducted on Medicago sativa L., a leguminous species known to be highly dependent on mycorrhiza. Two mycorrhizal levels were obtained by applying benomyl (low AMF) or not (high AMF). Experiment 1 investigated the effects of AMF on plant growth in the absence of competition. Experiment 2 was a factorial design with two mycorrhizal levels and two plant densities (6000 and 17 500 seeds m(-2)). Shoot biomass, root biomass and canopy radius were measured 30, 60, 90 and 120 d after sowing. The allometric relationships among these aspects of size were estimated by standardized major axis regression on log-transformed data.<h4>Key results</h4>Shoot biomass in the absence of competition was lower under low AMF treatment. In self-thinning populations, the slope of the log (mean shoot biomass) vs. log density relationship was significantly steeper for the high AMF treatment (slope = -1·480) than for the low AMF treatment (-1·133). The canopy radius-biomass allometric exponents were not significantly affected by AMF level, but the root-shoot allometric exponent was higher in the low AMF treatment. With a high level of AMF, the biomass-density exponent can be predicted from the above-ground allometric model of self-thinning, while this was not the case when AMF were reduced by fungicide.<h4>Conclusions</h4>AMF affected the importance of below-ground relative to above-ground interactions and changed root vs. shoot allocation. This changed allometric allocation of biomass and altered the self-thinning trajectory.
Project description:The Arbuscular mycorrhizal fungi (AMF) (Funneliformis mosseae), are the most widely distributed symbiont assisting plants to overcome counteractive environmental conditions. In order to improve the sustainability and the activity of AMF, the use of nanotechnology was important. The main objective of this study was to investigate the effect of titanium dioxide nanoparticles (TiO2NPs) on the activity of AMF in common bean roots as well as its activity under salinity stress using morphological and molecular methods. The activity of AMF colonization has increased in the presence of TiO2NPs especially for arbuscule activity (A%), which increased three times with the presence of TiO2NPs. The improvement rate of Funneliformis mosseae on plant growth increased from 180% to 224% of control at the lowest level of salinity and increased from 48% to 130% at higher salinity level, respectively. The AMF dependencies for plant dry biomass increased in the presence of TiO2NPs from 277% in the absence of salinity to 465 and 883% % at low and high salinity levels, respectively. The presence of AMF co-inoculated with TiO2NPs resulted in increasing the salinity tolerance of plants at all levels and reached 110% at salinity level of 100 mM NaCl. Quantitative colonization methods showed that the molecular intensity ratio and the relative density of paired inocula AMF Nest (NS) or chitin synthases gene (Chs) with TiO2NPs were higher significantly P.>0.05 than single inoculants of AMF gene in roots under the presence or the absence of salinity by about two folds and about 40%. Hence, the positive effect of TiO2NPs was confined to its effect on AMF not on bean plants itself.
Project description:<i>Eclipta prostrata</i> (L.) is an important and well-known medicinal plant due to its valuable bioactive compounds. Microorganisms, including arbuscular mycorrhizal fungi (AMF), and salinity could directly impact plant metabolome, thus influencing their secondary metabolites and the efficacy of herbal medicine. In this study, the role of different single AMF species (<i>Funneliformis mosseae</i>, <i>Septoglomus deserticola</i>, <i>Acaulospora lacunosa</i>) and a mixture of six AMF species in plant growth and physio-biochemical characteristics of <i>E. prostrata</i> under non-saline conditions was investigated. Next, the most suitable AM treatment was chosen to examine the impact of AMF on physio-biochemical features and polyphenol profiles of <i>E. prostrata</i> under saline conditions (100 and 200 mM NaCl). The findings indicated that AMF mixture application resulted in more effective promotion on the aboveground part of non-saline plants than single AMF species. AM mixture application improved growth and salt tolerance of <i>E. prostrata</i> through increasing the activity of catalase, peroxidase (at 4 weeks), proline, and total phenolic content (at 8 weeks). Such benefits were not observed under high salinity, except for a higher total phenolic concentration in mycorrhizal plants at 8 weeks. Through high-performance liquid chromatography, 14 individual phenolic compounds were analyzed, with wedelolactone and/or 4,5-dicaffeoylquinic acid abundant in all treatments. Salinity and mycorrhizal inoculation sharply altered the polyphenol profiles of <i>E. prostrata</i>. Moderate salinity boosted phenolic compound production in non-AM plants at 4 weeks, while at 8 weeks, the decline in the content of phenolic compounds occurred in uncolonized plants subjected to both saline conditions. Mycorrhization augmented polyphenol concentration and yield under non-saline and saline conditions, depending on the growth stages and salt stress severity. Plant age influenced polyphenol profiles with usually a higher content of phenolic compounds in older plants and changed the production of individual polyphenols of both non-AM and AM plants under non-stress and salt stress conditions. A better understanding of factors (involving mycorrhiza and salinity) affecting the phenolic compounds of <i>E. prostrata</i> facilitates the optimization of individual polyphenol production in this medicinal plant.
Project description:The positive effects of arbuscular mycorrhizal fungi (AMF) have been demonstrated for plant biomass, and zinc (Zn) and phosphorus (P) uptake, under soil nutrient deficiency. Additionally, a number of Zn and P transporter genes are affected by mycorrhizal colonisation or implicated in the mycorrhizal pathway of uptake. However, a comprehensive study of plant physiology and gene expression simultaneously, remains to be undertaken. Medicago truncatula was grown at different soil P and Zn availabilities, with or without inoculation of Rhizophagus irregularis. Measures of biomass, shoot elemental concentrations, mycorrhizal colonisation, and expression of Zn transporter (ZIP) and phosphate transporter (PT) genes in the roots, were taken. Mycorrhizal plants had a greater tolerance of both P and Zn soil deficiency; there was also evidence of AMF protecting plants against excessive Zn accumulation at high soil Zn. The expression of all PT genes was interactive with both P availability and mycorrhizal colonisation. MtZIP5 expression was induced both by AMF and soil Zn deficiency, while MtZIP2 was down-regulated in mycorrhizal plants, and up-regulated with increasing soil Zn concentration. These findings provide the first comprehensive physiological and molecular picture of plant-mycorrhizal fungal symbiosis with regard to soil P and Zn availability. Mycorrhizal fungi conferred tolerance to soil Zn and P deficiency and this could be linked to the induction of the ZIP transporter gene MtZIP5, and the PT gene MtPT4.