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.

Keywords: AMF; antioxidant; effect size; photosynthesis; phylogenetic signal; plant biomass; plant physiology; standardized mean difference.

Figure 1

The total number of publications about mycorrhizal effects on plant salinity stress physiology available in the “SCOPUS” and “Web of Science” databases from 1980 to 2019. The inlets in the main plots show the total number of publications found in the search, while the main plots show the number of articles by year.

Figure 2

Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) Flow Chart describing the search protocol utilized to identify and select published research for this analysis.

Figure 3

Growth responses of AMF-inoculated plants compared with those of non-inoculated plants under non-stressed conditions and at various levels of salinity. Error bars are effect size (SMD) means ±95% CIs. Where the CIs do not overlap the vertical dashed lines, the effect size for a parameter is significant, i.e., the growth responses of AMF plants were significantly different from those of non-AMF plants. n, number of studies included in the meta-analysis; p, significance level of SMD.

Figure 4

Effects of mycorrhizae on plant shoot biomass under non-saline, low salinity, and moderate salinity conditions for various categorical variables such as (A) Fungal genera, (B) Plant Family, (C) Plant clade, (D) Plant lifestyle, (E) Plant Photosynthetic pathway, (F) Plant Life forms, (G) Plant lifecycle, (H) Plant nodulation, and (I) Salinity duration. Error bars are the effect size means ±95% CIs. Where the CIs do not overlap the vertical dashed lines, the effect size for a parameter is significant, i.e., the growth responses of AMF plants were significantly different from those of non-AMF plants. n, number of studies included in the meta-analysis; p, significance level of SMD.

Figure 5

Effect of mycorrhizae on plant root dry biomass under non-saline, low salinity, and moderate salinity conditions for various categorical variables such as (A) Fungal genera, (B) Plant Family, (C) Plant clade, (D) Plant lifestyle, (E) Plant Photosynthetic pathway, (F) Plant Life forms, (G) Plant lifecycle, (H) Plant nodulation, and (I) Salinity duration. Error bars are effect size means ±95% CIs. Where the CIs do not overlap the vertical dashed lines, the effect size for a parameter is significant, i.e., the growth responses of AMF plants were significantly different from those of non-AMF plants. n, number of studies included in the meta-analysis; p, significance level of SMD.

Figure 6

Phylogenetic signals of plant families (A,B) and fungi (C,D) for the effects of AMF on plant shoot (A,C) and root (B,D) biomass under non-saline and salinity stress conditions. C mean, I, K, K-star, and lambda are as described in the section Materials and Methods. The red bar indicates that the signals are positive. *, **indicates that the signals are significant at p < 0.05 and p <0.01, respectively.

Figure 7

Effects of mycorrhizae on plant photosynthetic parameters under different levels of salinity stress. Error bars are the effect size means ±95% CIs. Where the CIs do not overlap the vertical dashed lines, the effect size for a parameter is significant. n, number of studies included in the meta-analysis. Chla, Chlorophyll a; Chlb, Chlorophyll b; Fv/Fm, maximal photochemical efficiency; Gs, Stomatal conductance; Pn, rate of photosynthesis; and RWC, Relative water content; n, number of studies included in the meta-analysis; p, significance level of SMD.

Figure 8

Effects of mycorrhizae on plant nutrient uptake under non-stress, low salinity stress, and moderate salinity stress. Error bars are effect size means ±95% CIs. Where the CIs do not overlap the vertical dashed lines, the effect size for a parameter is significant. n, number of studies included in the meta-analysis. Ca, Calcium; K, potassium; Na, sodium; N, Nitrogen and P, phosphorus. n, number of studies included in the meta-analysis; p, significance level of SMD.

Figure 9

Effects of mycorrhizae on plant enzymatic activity under non-stressed, low salinity, and moderate salinity stress. Error bars are means ±95% CIs. Where the CIs do not overlap the vertical dashed lines, the effect size for a parameter is significant. n, number of studies included in the meta-analysis. CAT, catalase; Car, Carotenoids; EL, electrical leakage; H2O2, hydrogen peroxide; MDA, malondialdehyde; POD, peroxidase and SOD, superoxide dismutase and SS, soluble sugars. n, number of studies included in the meta-analysis, p, significance level of SMD.