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Article

Responses of Legumes to Rhizobia and Arbuscular Mycorrhizal Fungi Under Abiotic Stresses: A Global Meta-Analysis

by
Hai-Xia Duan
1,
Chong-Liang Luo
2,*,
Xia Wang
3,
Ye-Sen Cheng
3,*,
Muhammad Abrar
4 and
Asfa Batool
5
1
State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining 810016, China
2
Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810008, China
3
Forestry and Grassland Pest Control and Quarantine Station of Alxa League, Alxa League 750306, China
4
State Key Laboratory of Herbage Improvement and Grassland Agro-Ecosystems, College of Ecology, Lanzhou University, Lanzhou 730000, China
5
College of Biology and Agricultural Resources, Huanggang Normal University, Huanggang 438000, China
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(11), 2597; https://doi.org/10.3390/agronomy14112597
Submission received: 8 October 2024 / Revised: 30 October 2024 / Accepted: 1 November 2024 / Published: 4 November 2024
(This article belongs to the Section Farming Sustainability)
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Abstract

:
Arbuscular mycorrhizal fungi (AMF) and rhizobia play a pivotal role in enhancing crop productivity, shaping microbial community structure, and improving soil quality, making them key components for sustainable ecosystem development. The symbiotic relationship between AMF and rhizobia is crucial for facilitating efficient biological nitrogen fixation and nutrient absorption, thereby reducing the dependence on chemical fertilizers and promoting sustainable agricultural practices. The findings of various studies, however, indicate that soil environment can impede the symbiotic relationship between AMF and rhizobia. We conducted a comprehensive meta-analysis of 158 articles from 1980 to 2022 to explore the synergistic interactions in legume–AMF–rhizobium systems and the potential mechanisms underlying this synergism. Our findings revealed that the inoculation with AMF and/or rhizobia significantly (p < 0.001) increased legume plant nitrogen content, phosphorus content, shoot biomass, yield, AMF colonization rate, and the number and weight of nodules compared to uninoculated controls (effect size d > 0). Moreover, there was a substantial synergistic effect between AMF and rhizobia (p < 0.001). Nevertheless, soil salinity stress, drought stress, and pH stress could hinder the positive effects of inoculation treatments, possibly due to the plant trade-off strategies under abiotic stress conditions. This research may potentially lead to new solutions for sustainable agricultural systems amidst the challenges posed by global climate change.

1. Introduction

In recent years, the combination of intensified anthropogenic activities and the compounding effects of climate change have resulted in elevated global temperatures, further leading to higher evapotranspiration and persistent water scarcity [1]. Consequently, this can induce plant drought, agricultural habitat destruction, diminish availability of water resources, increase soil salinization, and other associated challenges that severely impede plant growth [2,3]. Ecosystems often experience simultaneous impacts from multiple global change factors [4], each with the potential to exert profound effects on the ecosystem [5].
Drought and salinization are among the most severe climate change factors impacting ecosystems today. The stress caused by drought and salinization can significantly restrict the uptake of soil nutrients by plant roots, thereby severely constraining plant growth [6,7]. According to a recent study, drought adversely affects normal physiological activities, growth, and biomass accumulation, and in extreme cases, it can even result in plant mortality [8]. Furthermore, soil salinization directly or indirectly influences vegetation-associated soil microbial communities, subsequently affecting ecosystem structure and productivity [9,10].
Soil microorganisms play a pivotal role in regulating plant stress resistance and promoting sustainable development [11]. Numerous studies have demonstrated that beneficial soil microorganisms can mitigate the adverse impacts of abiotic stresses on plants [12,13,14]. Arbuscular mycorrhizal fungi (AMF), as ubiquitous symbiotic fungi, establish mutualistic associations with over 80% of terrestrial flowering plant roots, forming arbuscular mycorrhizal structures that augment the host plant’s capacity to assimilate soil moisture and nutrients [15,16]. AMF can improve nutrient acquisition in host plants, modulate plant metabolism, increase crop yield, enhance stress tolerance, and delay senescence [17]. Additionally, AMF influences the antioxidant system of plants by mitigating the excessive accumulation of reactive oxygen species and safeguarding plant metabolism [17]. Moreover, AMF triggers plant defense responses to bolster resistance against environmental stressors while maintaining redox balance and photosynthetic activity [18,19].
AMF and rhizobia are common symbiotic microorganisms abundantly present in the rhizosphere microbiota of leguminous plants, establishing a long-term symbiosis and evolution with leguminous plants. Through their interaction, AMF and rhizobia play crucial roles in providing essential nutrients to host plants, enhancing phosphorus and nitrogen absorption, promoting plant growth, and improving stress resistance [14,20,21]. A previous study has shown that dual inoculation of AMF and rhizobia exhibits greater benefits for host plant growth compared to single inoculation or no inoculation due to the synergistic effects they exert on promoting plant development [15]. Upon infection by AMF, root nodules become enriched and expand further, thereby enhancing the host’s ability for nitrogen fixation [22]. Conversely, through biological nitrogen fixation processes, rhizobia provide additional nitrogen to support efficient colonization rates of AMF. The effects of AMF or rhizobia on host plants depend on the concentration of soil phosphorus and nitrogen [23]. The combined effect of dual inoculation with AMF and rhizobia primarily manifests in promoting nitrogen and phosphorus element uptake/utilization by plants, while increasing biomass production as well as stress resistance capabilities [24].
Maximizing the utilization of AMF rhizobia’s nutritional absorption and stress resistance enhancement, in conjunction with plant symbiosis, hold paramount importance for promoting sustainable agricultural development. However, relevant experiments have also revealed the negative effects, suggesting that initial inoculation with rhizobia or AMF can impede subsequent colonization by other symbionts [25,26,27]. The interplay between AMF and rhizobia exhibits mutual constraints [25], which may be influenced by host plant species and environmental conditions. A comprehensive analysis of plant–microorganism interactions under drought and salt–alkali abiotic stresses could aid researchers in predicting and addressing the impacts of climate change and environmental factors on plants. In addition, analyzing the plant growth, productivity, and microbial responses of each symbiotic organism (number and weight of nodules/arbuscular mycorrhizal colonization) under different soil water content, salinity levels, and pH values will help determine whether the synergistic results are associated with soil nutrient levels. This provides theoretical references for improving crop productivity and stress resistance while offering new insights for sustainable agricultural development.
To investigate the contextual dependence of synergistic outcomes in AMF–rhizobia–legume systems and elucidate potential underlying mechanisms, we conducted a comprehensive meta-analysis. Specifically, our study aimed to address the following questions: (1) Does the productivity of host plants differ in the benefits they derive from AMF and/or rhizobia under conditions of soil salinity, drought, and pH stress? (2) Does the response of host plant tissues’ nitrogen and phosphorus content to the synergistic effects of AMF and rhizobia vary under different levels of soil salinity, drought, and pH stress? (3) Does co-inoculation enhance infection or nodulation in AMF or rhizobia, and does this vary under different levels of soil salinity, drought, and pH stress?

2. Materials and Methods

2.1. Literature Survey and Data Compilation

We conducted a comprehensive search for articles in English using Web of Science (http://apps.webofknowledge.com; accessed on 18–20 June 2022) and in Chinese using China National Knowledge Infrastructure (https://www.cnki.net; accessed on 15–17 June 2022). The search terms included ‘rhiz* AND mycorr* AND nitrogen fix*’ or ‘arbuscular mycorrhizal fung* AND rhiz* AND nitrogen fix*’ in the title, abstract, and keywords. The use of the wildcard character ‘*’ ensured inclusion of variations such as mycorrhizae, mycorrhizas, mycorrhizal, rhizobium, and rhizobia. We selected peer-reviewed literature published between 1980 and 2022 that investigated the effects of AMF and rhizobia inoculation integration on shoot biomass, yield, plant nitrogen and phosphorus content, nodulation (i.e., number of nodules and nodule weight), as well as the level of mycorrhizal colonization (i.e., % AMF colonization) in plants. Additionally, we reviewed the references cited in these articles to include any relevant studies missed during the initial search. Our inclusion criteria for meta-analysis required that each study (1) involved a legume plant along with both an AMF and a rhizobium; (2) encompassed an experiment that employed a full-factorial design, incorporating a non-inoculated control group, individual inoculation with rhizobia and AMF, as well as a combined treatment of AMF + rhizobia; and (3) presented the average biomass values and/or phosphorus and nitrogen tissue concentrations along with sample sizes of plants cultivated under each experimental treatment level. The search was completed on 20 June 2022, resulting in the identification of 158 studies that met our inclusion criteria in the meta-analysis.
Plant response was assessed by the mean dry shoot biomass, grain yield, plant nitrogen, phosphorus content, nodulation, and mycorrhizal colonization rate. The sample size, mean effect, and standard deviation (SD)/error data were also recorded. We converted the reported standard error to SD for analysis. For each data point in each study, we recorded the plant species examined and the site of the experiment. The dataset encompassed various AMF and rhizobia species (Supplementary Materials Table S1). We extracted data on mean values, sample sizes and SD/SE from the text, tables and/or figures from each study for the treatment with inoculation (i.e., inoculated with AMF and/or rhizobia) or without inoculation (CK) of legume nitrogen and phosphorus content, shoot biomass, grain yield, nodulation condition, and mycorrhizal colonization rate. In cases where the data were only available in the figures, digitization was performed using Getdata Graph Digitizer software 2.26 (Moscow, Russia; https://getdata-graph-digitizer.findmysoft.com; accessed on 22 June 2023) to obtain means and variances.

2.2. Data Analysis

For our analysis, we selected Hedges’ d as the effect size measure for assessing the effects of AMF and/or rhizobia inoculation under salt, drought, and pH stress treatments. This choice was based on its reduced bias towards small sample sizes [28] and its widespread usage in ecological meta-analyses [29,30,31]. The random-effects model was employed for this meta-analysis to estimate the effect size along with their corresponding 95% confidence intervals (CIs) per category as well as overall. In this study, a significant effect of the inoculation treatment on the variable was determined if the 95% CI values of the effect size did not overlap zero; otherwise, it indicated an insignificant effect. A positive effect of inoculation treatment on plant index was inferred with an effect size > 0, while a negative effect was indicated by an effect size < 0.
In studies employing the severing, the treatment involving inoculation (i.e., inoculated with AMF and/or rhizobia) was used as the ‘treated’ group, while the treatment without inoculation was the ‘control’ group. We used Hedges’ d as the effect size, which was calculated as follows:
d = x t ¯ − x c ¯ S × J
The means of the treated and control groups are denoted as x t ¯ and x c ¯ , respectively. Negative Hedges’ d values indicate a reduction in response variables due to inoculation treatment, and vice versa. J is a weighting factor based on the replicates and was calculated as follows:
J = 1 − 3 4   ×   ( n t   +   n c   −   2 )   − 1
and S is the pooled standard deviation based on the standard deviations, calculated as follows:
S   = ( n t   −   1 )   ×   s d t 2   +   ( n c   −   2 )   ×   s d c 2   n t   +   n c   −   2
where n and sd are the sample size and standard deviation of the treated or control group, respectively. The effect sizes were weighted by the inverse of the sampling variance to account for inequalities in study variance. Therefore, the calculation of each effect size (Vd) was performed as described by Koricheva et al. [29]:
V d = n t   +   n c n t   ×   n c + d 2 2   ×   ( n t   ×   n c )
We employed the Q statistic to assess the heterogeneity of effect sizes both within and between groups. A significance level of <0.05 was considered for between-group heterogeneity (QM) when calculating the p-value for moderators in the random-effects model. The meta-analysis was conducted utilizing the Metan module (1.85) for Stata/MP 17.0 (Stata Corp., Lakeway Dr, TX, USA). All the figures were prepared using OriginPro 2021 (OriginLab Corp., Northampton, MA, USA).

3. Results

3.1. Plant Nitrogen and Phosphorus Content Responses to Symbionts

In this study, it was observed that, irrespective of soil abiotic stress conditions, inoculation with AMF and/or rhizobia significantly enhanced the nitrogen and phosphorus content of the plants (d > 0, p < 0.001) under varying levels of soil salinity, water availability, and pH (Table 1 and Figure 1). Furthermore, the co-inoculation with AMF and rhizobia treatment showed a synergistic effect (p < 0.001; Table 1 and Figure 1) between AMF and rhizobia, highlighting their combined benefits. In contrast, the presence of salt stress, drought conditions, and extreme pH levels (acidic or alkaline) inhibited the promoting effect of inoculation treatments on crop nitrogen and phosphorus content, particularly in the case of co-inoculation with AMF and rhizobia treatment (Table 2 and Figure 2).
Compared to the treatment of non-salt stress, the rhizobia, AMF, and co-inoculation treatments significantly inhibited the accumulation of nitrogen and phosphorus content in leguminous plants under salt stress. Specifically, in non-salt stress treatments, the rhizobia, AMF, and co-inoculation treatments showed higher d values of 2.57, 2.35, and 4.83 (QM = 33.3, p < 0.05; Table 2 and Figure 2a) in plant nitrogen content, respectively, compared to the salt stress treatment with d values of 1.61, 0.90, and 3.30 (QM = 23.6, p < 0.001; Table 2 and Figure 2a). Similarly, drought stress significantly suppressed the effect size of all inoculation treatments on plant nitrogen and phosphorus content (Table 2 and Figure 2b,e). In well-watered treatments, the rhizobia, AMF, and co-inoculation treatments exhibited higher effect sizes with d values of 2.84, 2.44, and 4.35 (QM = 38.7, p < 0.001; Table 2 and Figure 2b), respectively, in terms of plant nitrogen content compared to the drought stress treatment where d values were observed as 1.07, 1.37, and 2.23 (QM = 37.0, p < 0.001; Table 2 and Figure 2b), respectively. On the other hand, either high (alkaline soil) or low (acidic soil) soil pH stress inhibited plant nitrogen and phosphorus accumulation but the effect was not significant (p > 0.05, Figure 2c,f).

3.2. Plant Yield and Shoot Biomass Responses to Symbionts

The results presented in Figure 3 show that inoculation with AMF and/or rhizobia significantly increased legume yield and shoot biomass compared to uninoculated controls (d > 0, p < 0.001). However, when both symbionts were present, the combined effects on plant growth were not strictly additive; instead, a synergistic effect between AMF and rhizobia was observed (p < 0.001; Table 1 and Figure 3). The promoting effect of inoculation on legume yield and shoot biomass was as follows: co-inoculation of AMF and rhizobia, rhizobia inoculation, and AMF inoculation (yield QM = 1010, p < 0.001; shoot biomass QM = 1479, p < 0.001; Table 1), where the mean d values of plant yield were 3.97, 2.26, and 1.70 in co-inoculation of AMF and rhizobia, rhizobia inoculation, and AMF inoculation treatment, respectively (Figure 3a–c).
The promoting effect of inoculation treatments on plant yield and shoot biomass was inhibited by soil stress caused by salt, drought, and pH (acidic and alkaline), especially in co-inoculation with AMF and rhizobia treatment compared to non-stress treatment (Table 2 and Figure 4). For example, under well-watered conditions, the d values of plant yield in the rhizobia, AMF, and co-inoculation treatments were 2.05, 1.66, and 3.41 (QM = 246, p < 0.001; Table 2 and Figure 4b), respectively, which were higher than those in the drought stress treatment (the d values were 1.20, 0.77, and 1.83, respectively; QM = 195, p < 0.001; Table 2 and Figure 4b). Compared to the non-stress treatments, consistent changes in plant shoot biomass and yield were observed for all inoculation treatments under soil stress conditions.

3.3. Microbial Responses to Symbionts

Inoculation with AMF and/or rhizobia significantly (p < 0.001) increased legume nodule number, nodule weight, and AMF colonization rate compared to uninoculated controls (Table 1 and Figure 5). In most cases, the effects were further enhanced when plants were co-cultivated with both symbionts, regardless of soil stress treatment (Table 3 and Figure 5 and Figure 6). These results demonstrated a significant synergistic effect between AMF and rhizobia (Table 3 and Figure 5 and Figure 6).
The promotion of co-inoculation with AMF and rhizobia on the nodulation level of rhizobia was suppressed by both salt stress and drought stress, as evidenced by a decrease in nodule weight and number of rhizobia compared to non-stress treatment (Figure 6a,b,d–e). In the non-salt stress treatment, the d values of nodule number in the rhizobia, AMF, and co-inoculation treatments were 4.82, 0.86, and 5.76 (QM = 48.7, p < 0.001; Table 3 and Figure 6a), respectively, which were higher than those observed under salt stress conditions of 3.85, 1.18, and 4.12 (Figure 6a), respectively. Additionally, acidic and alkaline soil inhibited the nodule weight and number of rhizobia in AMF and/or rhizobia treatments, which reducing the synergistic effect between AMF and rhizobia (Figure 6c,f).
The colonization rate of AMF was suppressed by soil salt stress, drought stress, and pH stress, thereby inhibiting the promoting effect of co-inoculation with AMF and rhizobia treatment on AMF colonization level compared to non-stress treatment (Figure 6g–i). In the non-water stress treatment, the d values of AMF colonization rate in the rhizobia, AMF, and co-inoculation treatments were 0.80, 2.54, and 3.88, respectively (QM = 101, p < 0.001; Table 3 and Figure 6h), which were higher than those observed under drought stress treatments of 0.727, 1.970, and 2.674, respectively (Figure 6h).
In addition, in terms of rhizobia nodulation, the inoculation effect of rhizobia surpasses that of AMF, with the mean d values for nodule number being 2.66 and 0.95, respectively (QM = 420, p < 0.001; Table 1 and Figure 5a–c). In contrast, regarding AMF colonization level, the inoculation effect of AMF exceeds that of rhizobia, as indicated by mean d values for AMF colonization rate being 0.51 and 1.04, respectively (QM = 677, p < 0.001; Table 1 and Figure 5g–i).

4. Discussion

The interaction between plants and soil microorganisms is pivotal for the functioning of terrestrial ecosystems and their response to environmental and climate change [32]. Plants contribute carbon to the soil through their litter, roots, and root exudates, serving as the primary energy source for the soil food web. Soil microorganisms can establish symbiotic relationships by colonizing roots (e.g., forming mycorrhizae and root nodules), modulating plant hormone production to enhance plant growth or mitigate the plant stress signals, thereby engaging in direct interactions with plants [33,34]. The significance of rhizosphere microbial interactions for sustainable agricultural development has emerged as a major focus in soil microbial research [35], wherein AMF and rhizobia are extensively utilized in agricultural production due to their crucial ecological roles. AMF directly supply nutrients such as nitrogen, phosphorus, zinc, copper, and water to plants in exchange for fatty acids derived from host plants’ resources [36,37]. Rhizobia can convert atmospheric nitrogen gas into an accessible form essential for plant growth [19]. In our meta-analyses, inoculations exhibited significant positive effects on plant nitrogen and phosphorus content. Furthermore, the co-inoculation of AMF and rhizobia demonstrated a synergistic effect, consistent with the studies reported by [38]. Consistent with previous findings conducted by Bai et al. [39] and Leite et al. [40], our study revealed that both AMF inoculation and co-inoculation of AMF and rhizobia significantly enhanced the phosphorus content in host plants under soil stress conditions. However, rhizobia inoculation alone did not exert a significant influence on plant phosphorus content. These results indicate that AMF plays a crucial role in facilitating host plants’ acquisition of phosphorus.
Both AMF and rhizobia demonstrated a positive impact on shoot biomass and yield of leguminous plants, with an even more pronounced effect observed when AMF and rhizobia were co-inoculated. These findings highlight the synergistic relationship between AMF and rhizobia in promoting host plant biomass increase and yield accumulation, consistent with previous studies reporting enhanced growth, elevated nitrogen and phosphorus content, as well as improved biomass production and yield of host plants during co-inoculation of AMF and rhizobia [39,40,41].
In the process of long-term evolution, a harmonious and mutually advantageous symbiotic relationship gradually emerges between AMF and rhizobia, which can be attributed to the following factors: Firstly, AMF infection provides plants and rhizobia with essential phosphorus and other nutrients, thereby enhancing their nitrogen fixation ability [42]. Secondly, by forming hyphal bridges and networks in the root system through extracellular hyphae, AMF enhances nodulation and increases the rate of nitrogen fixation in host plants. Thirdly, AMF infection of host plants stimulates higher rates of photosynthesis and respiration, resulting in increased production of photosynthetic products and enhanced transport of carbon to the roots. Ultimately, this improves the nitrogen fixation efficiency of rhizobia [43]. Fourthly, AMF infection promotes crop growth and development by augmenting root biomass and length while creating larger areas for rhizobial colonization [44]. Fifthly, AMF infection induces expression of nodule-related genes in host plants (such as Nod factor), leading to an increase in both the number and nitrogen fixation ability of rhizobia [45]. Sixthly, root nodules provide sufficient nitrogen sources for AMF growth through nitrogen fixation. This benefits spore germination and hyphal growth while increasing mycorrhizal infection rates in plant roots [46]. Last but not least, rhizobia promote flavonoid excretion from host plant roots to induce colonization by AMF [47].
Recently conducted studies have provided confirmation that the infection of plants by AMF can enhance the growth and enrichment of root nodules, thereby leading to an improvement in the host’s ability for nitrogen fixation [22,38,40]. In reciprocation, rhizobia are capable of supplying sufficient nitrogen to AMF through biological nitrogen fixation, consequently increasing the rate of AMF colonization. The combined inoculation with AMF and/or rhizobia has been found to significantly augment legume colonization rates by AMF, as well as increase nodule number and weight when compared to uninoculated controls. Furthermore, a significant synergistic effect between AMF and rhizobia was observed. This synergism is likely attributed to the fact that rhizobia and AMF both assist plants in acquiring complementary resources: nitrogen for rhizobia and phosphorus for AMF [38].
However, the effects of co-inoculation are contingent upon various factors, including host plant species, strain type, and soil environment [19]. The interaction between AMF and rhizobia does not consistently exhibit a synergistic promoting effect; in fact, dual inoculation of AMF and rhizobia may have no effect or even result in mutual restraint [25]. Furthermore, related experiments have also revealed negative effects, suggesting that prior inoculation of either rhizobia or AMF can inhibit subsequent colonization by other symbiotes [26,48,49]. For instance, Larimer et al. [50] revealed that upon infection of Amorpha fruticosa by rhizobia, there was a reduction in AMF hyphal abundance, indicating an antagonistic relationship between AMF and rhizobia. However, the combined effect of these symbiotic associations ultimately resulted in enhanced host growth and development. Kaschuk et al. [51] conducted a meta-analysis and determined that the single inoculation of AMF and rhizobia had a positive impact on host plant growth, while the dual inoculation did not exhibit a significant synergistic effect on the host. In a pot experiment conducted by Tsimilli-Michael et al. [49], it was observed that the single inoculation of AMF with Glomus fasciculatum enhanced photosystem II (PSII) activity in alfalfa, whereas dual inoculation with both AMF and Rhizobium meliloti actually inhibited PSII activity. This inhibition can be attributed to competition between AMF and rhizobia, which hinders photosynthesis in the host plant and reduces carbon allocation to both symbionts. Additionally, a previous study has shown that high-density rhizobial inoculation in peas leads to reduced colonization of AMF hyphae in plant roots [25]. This finding suggests a negative correlation between rhizobial nodulation and AMF colonization under highly nodulated conditions.
In case of limited soil nutrients, the mutualistic relationship between AMF and plants gradually transitions to parasitism, while a competitive relationship exists between AMF and rhizobia [51]. The symbiotic effect of dual inoculation with AMF and rhizobia is intricate, involving a “trade-off” of photosynthetic carbon among AMF, rhizobia, and plants. Depending on the accumulation, distribution, and competition for photosynthetic carbon resources, synergistic promotion effects, no effects, or antagonistic effects can be observed. The interaction between AMF and rhizobia is influenced by various comprehensive factors. Therefore, when applying microorganisms to improve ecosystem environments or remediate polluted soils in agricultural applications, it is crucial to comprehensively consider the interactions among microorganisms in their natural environment as well as clarify the influencing factors.
The dual inoculation enhanced the growth and development of alfalfa under drought stress while also improving their drought tolerance by increasing the activity of antioxidant enzymes in hosts [52]. Erman et al. [53] found that dual inoculation with AMF and Mesorhizobium ciceri had the most significant promoting effect on chickpeas under irrigation conditions due to sufficient soil moisture facilitating rhizobia nodulation, which requires an ample supply of phosphorus elements. Consequently, rhizobia promote further infection by AMF, ultimately leading to increased yield accumulation in chickpeas [53]. Interestingly, our study revealed that under soil salt, drought, and pH stress conditions compared to non-stress treatment, the promotion effects of inoculation on plant shoot biomass, yield, nitrogen and phosphorus content in plants, as well as AMF colonization level and rhizobial nodulation, were inhibited. This may be attributed to legume plants allocating resources towards adversity resistance when exposed to stressful soil environments, resulting in reduced investment in mycorrhizal symbiosis and rhizobial nodulation, thereby diminishing microbial synergy possibilities [19,50]. Similarly, a recent study has shown that although dual inoculation with AMF (a 1:1 mixture of Fusarium graminearum and Fusarium oxysporum) along with Mesorhizobium tianshanense has a more pronounced promoting effect on host plants compared to single inoculations under normal water supply conditions, during drought stress periods this synergistic effect weakens significantly such that it is not as effective as single inoculations alone [13]. This phenomenon can potentially be attributed to co-parasitism.
Liu et al. [54] discovered that soil salinity concentration partially inhibits the colonization of AMF and rhizobia in alfalfa, thereby suppressing their interaction. However, dual inoculation of AMF and rhizobia significantly enhances the stress resistance of alfalfa, mitigating the damage caused by saline–alkali stress on host plants and providing a theoretical foundation for the rational utilization of saline–alkali land. Consistent with previous findings, our meta-analysis revealed that soil salt stress significantly reduced the effect size of inoculations on host nutrient absorption, yield accumulation, and microbial symbiosis. Ashrafi et al. [55] observed a decrease in nodule number and AMF infection rate in alfalfa with increasing salt concentration. Salt stress hampers both AMF colonization and rhizobial nodulation due to increased energy allocation towards stress resistance rather than towards supporting AMF and rhizobia interactions. Additionally, high salt ion concentrations damage the cell structure of rhizobia while reducing their activity, thus inhibiting AMF and rhizobial colonization. Shafer et al. [56] found that although dual inoculation of AMF and Rhizobium leguminosarum promotes clover growth under low pH conditions, overall low pH impedes the interaction between AMF and rhizobia, possibly because it does not affect AMF infection but instead stimulates soil nutrient release, promoting host plant growth without enriching harmful ions in soil. Therefore, low pH does not influence the effectiveness of AMF infection as suggested by recent research indicating that decreased soil pH directly suppresses AMF biomass leading to reduced community diversity [57]. Soil pH affects mineral elements cycling through acidification pathways among others.
The symbiotic effect of co-inoculation between AMF and rhizobia is complex, involving a trade-off among AMF, rhizobia, and plants in terms of photosynthetic carbon assimilation. Depending on the accumulation, distribution, and competition for photosynthetic carbon resources, synergistic promotion, no effect, or antagonistic effects can be observed. Various agronomic management practices such as aboveground litter input, cultivation techniques, soil type selection, and increased planting density can all influence the colonization of AMF [19,58,59]. These factors have the potential to regulate the interaction between AMF and rhizobia by influencing their infection process efficiency. Therefore, extensive hypothetical analyses and validation experiments are required in future research to establish a reliable foundation for the practical application of dual inoculation with AMF and rhizobia. Furthermore, most current studies primarily focus on single-factor effects while neglecting the multi-factorial impacts and their interactions on AMF–rhizobium diversity as well as ecosystem functioning, especially within the context of global climate change. Urgent attention is required for future research endeavors in this important area.

5. Conclusions

Microbial symbionts can exert a profound effect on plant growth and fitness; however, the outcomes of plant–microbial interactions are highly contingent upon specific circumstances. Our meta-analysis revealed that inoculation with AMF and/or rhizobia significantly enhanced AMF colonization rate, nodule number, nodule weight, plant nitrogen content, plant phosphorus content, shoot biomass, and yield in legumes compared to uninoculated controls. Furthermore, a synergistic effect was observed between AMF and rhizobia. The effects of AMF and/or rhizobia inoculation on plants were found to be contingent upon soil salt levels, soil moisture conditions, and soil pH values. Specifically, high levels of soil salt concentration as well as drought stress and acidic or alkaline pH hindered the symbiotic relationship between plants and beneficial microorganisms. Consequently, these abiotic stresses suppressed the promoting effects of inoculation treatments on host yield and nutrient absorption, particularly when co-inoculating with both AMF and rhizobia compared to non-stress conditions.
By integrating variations in the nitrogen content, phosphorus content, biomass, yield, root nodulation, and AMF colonization levels of host plants, we propose that the enhanced productivity of legumes facilitated by AMF can be attributed to their promotion of host nitrogen and phosphorus uptake. This enables plants to acquire sufficient nutrients for sustaining growth and ultimately increasing productivity. Simultaneously, rhizobia contribute to this process by providing adequate nitrogen through biological nitrogen fixation for both the host plant and AMF symbionts, ensuring shoot biomass accumulation and promoting overall plant productivity.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14112597/s1, Table S1: Species of arbuscular mycorrhizal fungi and rhizobium included in the meta-analysis.

Author Contributions

Conceptualization, A.B.; Methodology, H.-X.D., C.-L.L., X.W., M.A. and A.B.; Software, H.-X.D., C.-L.L. and M.A.; Validation, Y.-S.C. and A.B.; Formal analysis, X.W.; Investigation, X.W., Y.-S.C. and M.A.; Resources, Y.-S.C.; Data curation, X.W., Y.-S.C., M.A. and A.B.; Writing—original draft, H.-X.D.; Writing—review & editing, H.-X.D. and C.-L.L.; Visualization, Y.-S.C.; Supervision, H.-X.D.; Funding acquisition, C.-L.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Natural Science Foundation of Qinghai Province of China (no. 2022-ZJ-970Q) and the National Natural Science Foundation of China (no. 32360328).

Data Availability Statement

All data contained in this article can be shared, and if detailed data and analyses are required, we can provide all of these during the review process.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the research reported in this paper.

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Figure 1. Mean effect sizes (Hedges’ d) of different inoculations on plant nitrogen (N) content (a–c) and plant phosphorus (P) content (d–f) under different soil treatments. The red, blue, and yellow circles represent rhizobium, AMF, and dual inoculation treatment, respectively. Error bars represent bias-corrected 95% bootstrap confidence intervals (CIs). Abbreviations: Rh, rhizobium; AMF, arbuscular mycorrhizal fungi.
Figure 1. Mean effect sizes (Hedges’ d) of different inoculations on plant nitrogen (N) content (a–c) and plant phosphorus (P) content (d–f) under different soil treatments. The red, blue, and yellow circles represent rhizobium, AMF, and dual inoculation treatment, respectively. Error bars represent bias-corrected 95% bootstrap confidence intervals (CIs). Abbreviations: Rh, rhizobium; AMF, arbuscular mycorrhizal fungi.
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Figure 2. Mean effect sizes (Hedges’ d) of different inoculations on plant nitrogen (N) content (a–c) and plant phosphorus (P) content (d–f) under different soil salt, water, and pH levels. The red, blue, and yellow circles represent rhizobium, AMF, and dual inoculation treatment, respectively. Error bars represent bias-corrected 95% bootstrap confidence intervals (CIs). If the CIs do not overlap the vertical dashed lines of 0, the effect size for a parameter is statistically significant at p < 0.001. Abbreviations: Rh, rhizobium; AMF, arbuscular mycorrhizal fungi.
Figure 2. Mean effect sizes (Hedges’ d) of different inoculations on plant nitrogen (N) content (a–c) and plant phosphorus (P) content (d–f) under different soil salt, water, and pH levels. The red, blue, and yellow circles represent rhizobium, AMF, and dual inoculation treatment, respectively. Error bars represent bias-corrected 95% bootstrap confidence intervals (CIs). If the CIs do not overlap the vertical dashed lines of 0, the effect size for a parameter is statistically significant at p < 0.001. Abbreviations: Rh, rhizobium; AMF, arbuscular mycorrhizal fungi.
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Figure 3. Mean effect sizes (Hedges’ d) of different inoculations on plant yield (a–c) and shoot biomass (d–f) under different soil treatments. The red, blue, and yellow circles represent rhizobium, AMF, and dual inoculation treatment, respectively. Error bars represent bias-corrected 95% bootstrap confidence intervals (CIs). Abbreviations: Rh, rhizobium; AMF, arbuscular mycorrhizal fungi.
Figure 3. Mean effect sizes (Hedges’ d) of different inoculations on plant yield (a–c) and shoot biomass (d–f) under different soil treatments. The red, blue, and yellow circles represent rhizobium, AMF, and dual inoculation treatment, respectively. Error bars represent bias-corrected 95% bootstrap confidence intervals (CIs). Abbreviations: Rh, rhizobium; AMF, arbuscular mycorrhizal fungi.
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Figure 4. Mean effect sizes (Hedges’ d) of different inoculations on plant yield (a–c), and shoot biomass (d–f) under different soil salt, water, and pH levels. The red, blue, and yellow circles represent rhizobium, AMF, and dual inoculation treatment, respectively. Error bars represent bias-corrected 95% bootstrap confidence intervals (CIs). If the CIs do not overlap the vertical dashed lines of 0, the effect size for a parameter is statistically significant at p < 0.001. Abbreviations: Rh, rhizobium; AMF, arbuscular mycorrhizal fungi.
Figure 4. Mean effect sizes (Hedges’ d) of different inoculations on plant yield (a–c), and shoot biomass (d–f) under different soil salt, water, and pH levels. The red, blue, and yellow circles represent rhizobium, AMF, and dual inoculation treatment, respectively. Error bars represent bias-corrected 95% bootstrap confidence intervals (CIs). If the CIs do not overlap the vertical dashed lines of 0, the effect size for a parameter is statistically significant at p < 0.001. Abbreviations: Rh, rhizobium; AMF, arbuscular mycorrhizal fungi.
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Figure 5. Mean effect sizes (Hedges’ d) of different inoculations on nodule number (a–c) and nodule weight (d–f) of rhizobia and AMF colonization rates (g–i) of plant roots under different soil treatments. The red, blue, and yellow circles represent rhizobium, AMF, and dual inoculation treatment, respectively. Error bars represent bias-corrected 95% bootstrap confidence intervals (CIs). Abbreviations: Rh, rhizobium; AMF, arbuscular mycorrhizal fungi.
Figure 5. Mean effect sizes (Hedges’ d) of different inoculations on nodule number (a–c) and nodule weight (d–f) of rhizobia and AMF colonization rates (g–i) of plant roots under different soil treatments. The red, blue, and yellow circles represent rhizobium, AMF, and dual inoculation treatment, respectively. Error bars represent bias-corrected 95% bootstrap confidence intervals (CIs). Abbreviations: Rh, rhizobium; AMF, arbuscular mycorrhizal fungi.
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Figure 6. Mean effect sizes (Hedges’ d) of different inoculations on nodule number (a–c) and nodule weight (d–f) of rhizobia and AMF colonization rates (g–i) of plant root under different soil salt, water, and pH levels. The red, blue, and yellow circles represent rhizobium, AMF, and dual inoculation treatment, respectively. Error bars represent bias-corrected 95% bootstrap confidence intervals (CIs). If the CIs do not overlap by the vertical dashed lines of 0, the effect size for a parameter is statistically significant at p < 0.001. Abbreviations: Rh, rhizobium; AMF, arbuscular mycorrhizal fungi.
Figure 6. Mean effect sizes (Hedges’ d) of different inoculations on nodule number (a–c) and nodule weight (d–f) of rhizobia and AMF colonization rates (g–i) of plant root under different soil salt, water, and pH levels. The red, blue, and yellow circles represent rhizobium, AMF, and dual inoculation treatment, respectively. Error bars represent bias-corrected 95% bootstrap confidence intervals (CIs). If the CIs do not overlap by the vertical dashed lines of 0, the effect size for a parameter is statistically significant at p < 0.001. Abbreviations: Rh, rhizobium; AMF, arbuscular mycorrhizal fungi.
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Table 1. Between-group heterogeneity (QM) data for the effects of inoculations on plant nitrogen (N), phosphorus (P) content, yield, biomass, AMF colonization rate, nodule number, and nodule weight response variables.
Table 1. Between-group heterogeneity (QM) data for the effects of inoculations on plant nitrogen (N), phosphorus (P) content, yield, biomass, AMF colonization rate, nodule number, and nodule weight response variables.
Response VariablesTreatmentsdfQMp
Plant NInoculations13621125<0.001
Plant PInoculations1298527<0.001
YieldInoculations8661010<0.001
Shoot biomassInoculations14791231<0.001
Nodule numberInoculations1164420<0.001
Nodule weightInoculations1234581<0.001
AMF colonization rateInoculations1681677<0.001
Note: QM with p < 0.05 indicates significant differences between groups (bold). df: degrees of freedom, df = n − 1, where n is the number of samples. Abbreviations: AMF, arbuscular mycorrhizal fungi.
Table 2. Between-group heterogeneity (QM) results for the effects of different inoculations, soil salt, water, and pH levels on plant N content, plant P content, plant shoot biomass, and yield response variables.
Table 2. Between-group heterogeneity (QM) results for the effects of different inoculations, soil salt, water, and pH levels on plant N content, plant P content, plant shoot biomass, and yield response variables.
Response VariablesModeratorsInoculationsdfQMp
Plant NNon-salt stressInoculations3023.6<0.001
Salt stressInoculations3333.30.011
Well-wateredInoculations5438.7<0.001
DroughtInoculations6937.0<0.001
Acid soilInoculations42242.0<0.001
Neutral soilInoculations41469.4<0.001
Alkaline soilInoculations569616<0.001
Plant PNon-salt stressInoculations4568.2<0.001
Salt stressInoculations5137.8<0.001
Well-wateredInoculations4350.2<0.001
DroughtInoculations6942.90.018
Acid soilInoculations40936.2<0.001
Neutral soilInoculations411521<0.001
Alkaline soilInoculations579453<0.001
Shoot biomassNon-salt stressInoculations802334<0.001
Salt stressInoculations773568<0.001
Well-wateredInoculations691101<0.001
DroughtInoculations738104<0.001
Acid soilInoculations543440<0.001
Neutral soilInoculations644706<0.001
Alkaline soilInoculations688742<0.001
YieldNon-salt stressInoculations921239<0.001
Salt stressInoculations894217<0.001
Well-wateredInoculations799246<0.001
DroughtInoculations805195<0.001
Acid soilInoculations718207<0.001
Neutral soilInoculations698216<0.001
Alkaline soilInoculations787148<0.001
Note: QM with p < 0.05 indicates significant differences between groups (bold). df: degrees of freedom, df = n − 1, where n is the number of samples.
Table 3. Between-group heterogeneity (QM) results for the effects of different inoculations, soil salt, water, and pH levels on nodule number, nodule weight, and AMF colonization rate response variables.
Table 3. Between-group heterogeneity (QM) results for the effects of different inoculations, soil salt, water, and pH levels on nodule number, nodule weight, and AMF colonization rate response variables.
Response VariablesModeratorsInoculationsdfQMp
Nodule numberNon-salt stressInoculations2748.7<0.001
Salt stressInoculations2743.3<0.001
Well-wateredInoculations4438.7<0.001
DroughtInoculations5937.0<0.001
Acid soilInoculations16242.0<0.001
Neutral soilInoculations11469.4<0.001
Alkaline soilInoculations36961.6<0.001
Nodule weightNon-salt stressInoculations3568.2<0.001
Salt stressInoculations4137.8<0.001
Well-wateredInoculations5350.2<0.001
DroughtInoculations7942.9<0.001
Acid soilInoculations20962.8<0.001
Neutral soilInoculations11152.1<0.001
Alkaline soilInoculations17975.3<0.001
AMF colonization rateNon-salt stressInoculations62334<0.001
Salt stressInoculations73568<0.001
Well-wateredInoculations91101<0.001
DroughtInoculations78104<0.001
Acid soilInoculations87440<0.001
Neutral soilInoculations144706<0.001
Alkaline soilInoculations187148<0.001
Note: QM with p < 0.05 indicates significant differences between groups (bold). df: degrees of freedom, df = n − 1, where n is the number of samples. Abbreviations: AMF, arbuscular mycorrhizal fungi.
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Duan, H.-X.; Luo, C.-L.; Wang, X.; Cheng, Y.-S.; Abrar, M.; Batool, A. Responses of Legumes to Rhizobia and Arbuscular Mycorrhizal Fungi Under Abiotic Stresses: A Global Meta-Analysis. Agronomy 2024, 14, 2597. https://doi.org/10.3390/agronomy14112597

AMA Style

Duan H-X, Luo C-L, Wang X, Cheng Y-S, Abrar M, Batool A. Responses of Legumes to Rhizobia and Arbuscular Mycorrhizal Fungi Under Abiotic Stresses: A Global Meta-Analysis. Agronomy. 2024; 14(11):2597. https://doi.org/10.3390/agronomy14112597

Chicago/Turabian Style

Duan, Hai-Xia, Chong-Liang Luo, Xia Wang, Ye-Sen Cheng, Muhammad Abrar, and Asfa Batool. 2024. "Responses of Legumes to Rhizobia and Arbuscular Mycorrhizal Fungi Under Abiotic Stresses: A Global Meta-Analysis" Agronomy 14, no. 11: 2597. https://doi.org/10.3390/agronomy14112597

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