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. 2024 Oct 14;24:960. doi: 10.1186/s12870-024-05638-9

Inoculation with arbuscular mycorrhizal fungi improves plant biomass and nitrogen and phosphorus nutrients: a meta-analysis

Yingjie Wu 1, Chongjuan Chen 2,✉, Guoan Wang 3
PMCID: PMC11472555  PMID: 39396962

Abstract

Arbuscular mycorrhizal fungi (AMF) have profound effects on plant growth and nitrogen (N) and phosphorus (P) nutrition. However, a comprehensive evaluation of how plant N and P respond to AMF inoculation is still unavailable. Here, we complied data from 187 original researches and carried out a meta-analysis to assess the effects of AMF inoculation on plant growth and N and P nutrition. We observe overall positive effects of AMF inoculation on plant performance. The mean increases of plant biomass, N concentration, P concentration, N and P uptake of whole plant are 47%, 16%, 27%, 67%, and 105%, respectively. AMF inoculation induces more increases in plant concentrations and storage of P than N. Plant responses to AMF inoculation are substantially higher with single AMF species than with mixed AMF species, in laboratory experiments than in field experiments, and in legumes than in non-legumes. The response ratios of plant N and P nutrition are positively correlated with AMF colonization rate, N addition, P addition, and water condition, while unvaried with experiment duration. The biggest and smallest effect sizes of AMF inoculation on plant performance are observed in the application of nitrate and ammonium, respectively. Accordingly, this meta-analysis study clearly suggests that AMF inoculation improves both plant N and P nutrients and systematically clarifies the variation patterns in AMF effects with various biotic and abiotic factors. These findings highlight the important role of AMF inoculation in enhancing plant N and P resource acquisitions and provide useful references for evaluating the AMF functions under the future global changes.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12870-024-05638-9.

Keywords: Arbuscular mycorrhizal fungi, Plant nutrient uptake, Nitrogen, Phosphorus, Plant biomass, Meta-analysis

Introduction

Nitrogen (N) and phosphorus (P) are the two most limiting mineral nutrients for plant growth although both of them are essential components of proteins, nucleic acids, and enzymes etc., and are included in many metabolic processes in plants [1–3]. Given that the carbon, N and P cycles are tightly coupled [4, 5], improving plant N and P nutrients has important implications for enhancement in plant growth and thereby the carbon sequestration of terrestrial vegetation. Also, increases in crop N and P nutrition will greatly benefit the sustainable global food security. As we all know, the production and use of artificial fertilizers indeed dramatically improve plant nutrition and yield in agro-ecosystems, but have been causing many serious environmental issues, including degradation of soil quality, water eutrophication, biodiversity loss, soil acidification, etc [6, 7]. Moreover, despite N deposition in natural ecosystems alleviates the vegetation N limitation to some extent, it may aggravate vegetation P limitation and result in stoichiometry imbalance in ecosystems [8]. Accordingly, it is necessary to find an appropriate method to not only improve both plant N and P nutrition and growth but also avoid environment problems.

Arbuscular mycorrhizal fungi (AMF) are the most common mycorrhiza and form symbiosis with over 80% of terrestrial plant species [9]. AMF have an important role in improving plant nutritional status (especially for the acquisition of nutrients with poor mobility in soils) because they can acquire additional nutrients beyond rhizospheric zone with their abundant and superlong extraradical mycelium [9–12]. Phosphorus is relatively immobile in soils compared to N. Usually, only a small percentage of soil P is available to plants, while up to 90% of P are unavailable because of the strong precipitation reactions in the soil or sorption to mineral soil particles [10, 13]. As reported, P uptake rate by hyphae was six times higher than that by root hairs, and the P transfer rate was ten times faster in mycorrhizal hyphae than in root hairs [14]. Thus, the beneficial effects of AMF inoculation on plant P acquisition have been well documented [15, 16].

However, how AMF inoculation affects plant N acquisition is still being controversially discussed [17–26]. Some studies found that AMF can take up and deliver substantial N to host plants [17, 27, 28]. For instance, Wang et al. [29] found that more than 40% of rice N was acquired by mycorrhizal pathway. Tanaka and Yano [30] showed that even 74% of maize shoot N derived from its fungal partner. Whereas, some studies concluded that AMF has no effects [19, 24] or even negative effects [20, 22, 31] on plant N acquisition. For example, shoot N concentration did not differ between inoculated and uninoculated Parkinsonia aculeata [24]. Even AMF inoculation was found to decrease stem, leaf and pod N and 15N concentrations of soybean [31], as well as reduce N acquisition and grain yield of maize in N deficient soils [22]. Accordingly, although a lot of individual studies have been conducted to investigate how plant N acquisition respond to AMF inoculation, a general conclusion of the effects of AMF inoculation on plant N nutrition is still unavailable. And, it is even more unclear whether magnitudes of the effects of AMF inoculation on plant N and P nutrition are similar.

The direction and magnitude of the effects of AMF inoculation on plant growth and N and P acquisitions are related with various factors [11, 12]. On the one hand, this may be because that AMF have additional non-nutritional functions on host plants, such as improving plant’s resistances against environment stresses [9]. On the other hand, this should be related to that those factors may influence the growth and development of AMF [32, 33]. As reported from previous studies, those factors include AMF type [26, 34–36], AMF colonization rate [16], plant type [37], experiment type [19], experiment duration [38, 39], N form [17, 30, 40], N addition rate [23, 41], P addition rate [42], and water addition [32]. However, there are still lacking a comprehensive study exploring the influences of these factor on the effects of AMF inoculation on plant growth and N and P acquisitions.

Based on the above, here we compiled data from 187 original studies and conducted a meta-analysis to identify the general pattern of AMF inoculation effects on plant growth and N and P nutrition (especially for N) in different plant parts (belowground, aboveground and the whole plant); to compare the effects of AMF inoculation on N nutrition with those on P nutrition; to clarify whether and how the effects of AMF inoculation on plant performance vary with AMF type, plant type, AMF colonization rate, experiment duration, N addition, P addition, water addition, experiment type, and N form. This study will enhance our knowledges about the roles of AMF inoculation in plant N and P nutrients.

Materials and methods

Data compilation

The records of AMF inoculation effects on plant biomass, N and P nutrients were collected by searching from Web of Science, China National Knowledge Infrastructure and Google Scholar with the keywords of ‘arbuscular mycorrhizal fungi or AMF’, ‘mycorrhiza’, ‘nitrogen or N’. The keywords of ‘phosphorus or P’ and ‘biomass or weight’ were not included in the search keywords because of two reasons. On the one hand, a lot of researches regarding to the AMF inoculation effects on plant P nutrition and biomass were conducted and the conclusions were clearer than those of N nutrition. On the other hand, after reading a great amount publications and pre-checking the collected publications, we found that almost all studies focusing on AMF inoculation effects on plant N nutrition also reported plant biomass and P simultaneously. By October 2021, a total of 187 publications covering the period from 1976 to 2021 were selected from 9910 papers (Table S1, Fig. S1). Among these publications, there were only 26 papers that just reported N-related data while not having P-related data, which allowing us to compare the differences of AMF inoculation effects on N and P nutrition. The compiled database consisted of 15 variables that are related to plant biomass and N and P nutrition, including biomass, N concentration, P concentration, N uptake, and P uptake of plant aboveground, plant belowground, and the whole plant, respectively (Table S2). The following six criteria were used to select appropriate studies: (1) articles must be original research, if it was not the original paper, the corresponding original paper was found; (2) studies conducted both in laboratory and field were included; (3) at least one of the selected variables were measured, and the reported variables were measured both in control and AMF treatment; (4) for multifactorial studies, only control and AMF treatment data were collected and the interacting effects were excluded; (5) plant biomass and N and P concentrations were recorded based on dry weight; (6) the mean values, standard deviations or standard errors and sample sizes of the target variables were given or could be calculated from the selected studies.

The data on biomass of whole plant was acquired directly from papers or by summing aboveground and belowground biomass. The plant N or P uptake of aboveground and belowground were obtained directly from selected studies or calculated using the corresponding biomass and N or P concentrations. The plant N or P uptake of whole plant could be calculated by multiplying biomass and N or P concentrations of the whole plant, or by adding N or P uptake of aboveground and belowground. The N or P concentrations of aboveground, belowground, and whole plant were estimated by dividing the corresponding biomass into N or P uptake if they were available in the original articles. The shoot, leaf, fruit, and grain parts were all regarded as plant aboveground, they were summed to calculate the data of aboveground and further of whole plant when data of these plant parts were all reported or at least when data of shoot or leaf were showed. In addition to the 15 main variables mentioned above, other information related to plants, AMF, and experiment conditions, including AMF type, plant type, AMF colonization rate, experiment duration, N addition, P addition, water addition, experiment type and N type were also collected. If the required data were not available in the original publications, they are extracted using GetData Graph Digitizer software (version 2.24, http://www.getadata-graph-digtizer.com) when the data were presented as figures or obtained from supplementary materials.

Considering that AMF type, plant type, experiment type and N type may influence the responses of the main variables to AMF inoculation, we classified these factors and examined whether there are differences of AMF inoculation effects on the plant biomass and N and P nutrients between or among different classifications of these factors. AMF inoculum was classified into single and mixed AMF species. Single inoculation indicated that only one kind of AMF species was used in the experiment, while mixed inoculation indicated more than one AMF species was applied. Plant types were divided into leguminous and non-leguminous plants because AMF that interacted with rhizobia could affect the nutrient absorption of plants. Experiment type was categorized into laboratory and field experiment. Because mycorrhizal fungi showed differential N preference and different N forms applied in the substrates might have different influences on AMF inoculation effects on plant N and P absorptions, thereby N type was divided into four categories: urea, ammonium (NH4+), nitrate (NO3–), ammonium and nitrate (NH4+ and NO3–). Also, we analyzed the changes in AMF inoculation effects with continuous factors including AMF colonization rate, experiment duration, N addition, P addition, and water condition to explore their effects on the responses of plant biomass and N and P nutrients to AMF inoculation. Considering that some control treatments showed low colonization rate because of having not sterilization or incomplete sterilization, AMF colonization rates used in this study were the colonization rate in AMF treatment group. Experiment duration was converted to days if it was reported as other units in studies. The units of N or P addition rates were unified as per unit substrate, and the records were excluded if the units could not be converted.

Statistical analyses

The effect size, as a metric for the responses of plant biomass and N and P nutrients to AMF inoculation, was defined as the natural log response ratio (RR) [43]. For a given response variable, RR was the ratio of the value in AMF treatment (XT) to that in corresponding control treatment (XC) (Eq. 1).

graphic file with name M1.gif 1

The 95% confidence intervals (CIs) of the effect sizes across all study variables were generated using bootstrapping techniques. The number of iterations used for bootstrapping was 10,000. The effect of AMF on a specific response variable was considered significant if the 95% CI did not overlap with 0. In order to better explain the changes in variables, the mean effect size was transformed back to the percentage change as follows:

graphic file with name M2.gif 2

Differences in the overall effects of AMF inoculation on plant biomass, N and P concentrations and uptake among plant aboveground, belowground, and whole plant, as well as the influences of AMF type, plant type, experiment type and N type on the effects of AMF inoculation on all response variables were tested using one-way analysis of variance (one-way ANOVA). Besides, the correlations between the response ratios (lnRR) of plant biomass and N and P nutrients and AMF colonization rate, experiment duration, N addition, P addition, and water condition, and between plant aboveground N/P values (and N/P differences between control and AMF treatment) and N and P addition were analyzed. The one-way ANOVA and correlation analyses were performed using SPSS software (SPSS for Windows, Version 20.0, Chicago, IL, USA). Statistical significance was set at P < 0.05.

Results

Overall effects of AMF inoculation on plant biomass and N and P nutrients

The mean effect sizes of AMF inoculation on aboveground, belowground, and whole plant are 0.39, 0.47, and 0.38 for biomass; are 0.13, 0.17, and 0.15 for N concentration; are 0.29, 0.26, and 0.24 for P concentration; are 0.50, 0.64, and 0.51 for N uptake; and are 0.67, 0.80, and 0.72 for P uptake (Fig. 1). The 95% CIs of these response variables do not overlap with zero, displaying positive effects of AMF inoculation on plant biomass, N concentration, P concentration, N and P uptake in all plant parts (Fig. 1). The influences of AMF inoculation on these variables show great variations. Inoculation with AMF averagely increases 47–59% in plant biomass, 13–19% in plant N concentration, 27–34% in plant P concentration, 64–90% in plant N uptake, and 95–122% in plant P uptake for different plant parts (Fig. 1).

Fig. 1.

Fig. 1

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The effects of AMF inoculation on biomass, N concentration, P concentration, N uptake, and P uptake of plant aboveground (▲), plant belowground (▼), and whole plant (●). The mean effect size is displayed as the mean ± 95% CIs. The effects of AMF inoculation on variables are considered significant if the 95% CIs do not overlap with 0. If the mean effect size > 0, AMF inoculation increases plant biomass and N and P uptake. If the mean effect size < 0, AMF inoculation decreases plant biomass and N and P uptake. The values on the right y-axis represent the mean percentage change of the corresponding variables. The sample size of each variable is indicated next to the 95% CI

Influences of AMF type and plant type on AMF inoculation effects on plant biomass and N and P nutrients

Plant biomass, N concentration, P concentration, N and P uptake are improved markedly by AMF inoculation both with single and mixed AMF species and both in leguminous and non-leguminous plants (Fig. 2). Responses in plant biomass, P concentration, N and P uptake to AMF inoculation are much higher in conditions in which single AMF species rather than mixed AMF species were inoculated (Fig. 2a). AMF inoculation has greater effects on biomass, N concentration and N uptake in legumes than in non-legumes (Fig. 2b).

Fig. 2.

Fig. 2

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The influences of (a) AMF type (single AMF and mixed AMF) and (b) plant type (leguminous plants and non-leguminous plants) on AMF inoculation effects on biomass, N concentration, P concentration, N uptake, and P uptake of plant aboveground (▲), plant belowground (▼), and whole plant (●). The effect size is displayed as the mean ± 95% CIs. The dashed line is drawn at mean effect size = 0. The effects of AMF inoculation on variables are considered significant if the 95% CIs do not overlap with 0. If the mean effect size > 0, AMF inoculation increases plant biomass and N and P uptake. If the mean effect size < 0, AMF inoculation decreases plant biomass and N and P uptake. The sample size of each variable is indicated next to the 95% CI. The influences of AMF type and plant type on AMF inoculation effects on the variables are significant when P < 0.05

Influences of AMF colonization rate, experiment duration, N addition, P addition, and water addition on AMF inoculation effects on plant biomass and N and P nutrients

The effects of AMF inoculation on biomass, P concentration, N and P uptake in whole plant, those on biomass and P uptake in plant aboveground, and those on N concentration in plant belowground increase with AMF colonization rate (Fig. 3A & S2A & S3A).

Fig. 3.

Fig. 3

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Relationships between the response ratios (lnRR) of biomass, N concentration, P concentration, N uptake, and P uptake of whole plant with (A) AMF colonization rate, (B) experiment duration, (C) N addition, (D) P addition, and (E) water condition. Dark lines represent the regression results as P < 0.05, and purple shaded areas represent the 95% CIs. The n indicates the sample size and r values are the corresponding correlation coefficients

The effects of AMF inoculation on plant biomass and N and P nutrients are invariant with experiment duration except that those on biomass and N uptake of plant belowground show increasing trends with experiment duration (Fig. 3B & S2B & S3B).

The effects of AMF inoculation on biomass of whole plant decrease with increasing N addition while increase with increasing P addition (Fig. 3C & 3D). The effects of AMF inoculation on N concentration of whole plant increase with increasing N addition. AMF inoculation effects on P concentration of whole plant and plant aboveground positively correlated with both N and P additions (Fig. 3C & 3D). AMF inoculation effects on plant N and P uptake keep unchanged except that those on P uptake of whole plant and plant belowground increase with P addition (Fig. 3C & 3D & S2C & S2D & S3C & S3D).

The response ratios of N concentration, N and P uptake in whole plant increase while those of biomass and P concentration do not vary with increasing water level (Fig. 3E). There are no relationships between the response ratios of these variables and water condition in plant belowground (Fig. 3E & S2E & S3E).

Influences of experiment type and N type on AMF inoculation effects on plant biomass and N and P nutrients

AMF inoculation distinctly improve plant biomass, N concentration, P concentration, N and P uptake both in laboratory and filed conditions expect biomass, N and P uptake of belowground and P concentrations of whole plant in filed condition (Fig. 4a). The biomass of aboveground and whole plant, P concentration of whole plant, P uptake of aboveground and belowground are increased by AMF inoculation more in laboratory than in filed condition (P < 0.05) (Fig. 4a).

Fig. 4.

Fig. 4

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The influences of (a) experimental type (laboratory experiments and field experiments) and (b) N type (urea; NH4+; NO3–; NH4+ and NO3–) on AMF inoculation effects on biomass, N concentration, P concentration, N uptake, and P uptake of plant aboveground (▲), plant belowground (▼), and whole plant (●). The effect size is displayed as the mean ± 95% CIs. The dashed line is drawn at mean effect size = 0. The effects of AMF inoculation on variables are considered significant if the 95% CIs do not overlap with 0. If the mean effect size > 0, AMF inoculation increases plant biomass and N and P uptake. If the mean effect size < 0, AMF inoculation decreases plant biomass and N and P uptake. The sample size of each variable is indicated next to the 95% CI. The influences of experimental type and N type on AMF inoculation effects on the variables are significant when P < 0.05

N type affects the effects of AMF inoculation on plant biomass, P concentration, N and P uptake, but does not influence the AMF effects on plant N concentration (Fig. 4b). AMF inoculation has the greatest positive effects on plant biomass, P concentration, N and P uptake when NO3– is added (Fig. 4b). The least positive effects, no significant effect or even negative effects of AMF on plant biomass, P concentration, N and P uptake are observed when NH4+ is added (Fig. 4b).

Discussion

Overall effects of AMF inoculation on plant biomass and N and P uptake

Overall, from the syntheses of 187 peer-reviewed publications, this meta-analysis clearly indicates that inoculation with AMF has significantly positive effects on plant biomass and plant N and P nutrients (Fig. 1). This result evidences the generally beneficial roles of AMF inoculation in plant growth and nutrients, especially for plant N since this study systematically evaluates the AMF functions on plant N nutrient, although negative [20, 22, 31], positive [26, 44–46], and unobvious effects [19, 24] of AMF inoculation on plant N nutrition have been reported in existing studies. The extraradical mycelium of the AMF largely extends the root system and improves the soil nutrients accessibility to host plant [9, 10, 47], also AMF have been found to accelerate the mineralization and activation of organic nutrients [48–51], both of them are responsible for the beneficial influences of AMF inoculation on plant performance.

Specifically, inoculation with AMF increases plant biomass, N concentration, P concentration, N uptake, and P uptake in whole plant by 47%, 16%, 27%, 67% and 105%, respectively (Fig. 1). Although the responses of these variables to AMF inoculation vary greatly, AMF inoculation causes more increases in plant P concentration and uptake than in N concentration and uptake (Fig. 1). This finding is in accord with a meta-analysis study, which focused on the effects of AMF species and taxonomic groups on plant performance under stressful and unstressful conditions and observed stronger positive effects of AMF on P nutrition than on N nutrition [26]. This should be associated with the crucial role of AMF in enhancing the acquisition of immobile nutrients [16], and also may be related to the competition between AMF and host plants for N nutrition because AMF themselves have a substantial N demand to sustain their development and functions [18, 22, 52, 53].

Influences of AMF type and plant type on AMF inoculation effects on plant biomass and N and P nutrients

The effects of AMF inoculation on plant biomass and N and P nutrients are significantly influenced by AMF type (Fig. 2a). Consistently, Treseder [35] found that AMF taxa showed large variations in their effects on plant biomass and P content. Also, Marro et al. [26] observed AMF inoculation effects on plant performance in terms of biomass and N and P nutrition varied greatly among different AMF species, from significantly positive effects to insignificant effects. Among them, Scutellospora calospora, Diversispora spurca, and Acaulospora laevis are the AMF species that exerted the highest positive effects on plant biomass, N nutrition, and P nutrition, respectively [26]. The differential effects of AMF species on plant performance may be mainly depended on the density of inoculated spores and whether the selected inoculants can form a good symbiotic relationship with the host plants, as plant nutrients and growth will be improved when both of which are appropriate. Specifically, we find that inoculation with single AMF is more beneficial than mixed AMF species for plant growth and N and P nutrients (Fig. 2a). In contrast, some studies considered that mixed inoculum could maintain higher fungal diversity, thus the complementarity among fungal species could provide more benefits for host plants than single inoculum [38]. For example, Hoeksema et al. [54] observed that the response of plant biomass to AMF inoculation was substantially higher when multiple AMF species rather than single AMF species was inoculated. In this study, Funneliformis sp. and Rhizophagus sp. were the most used single AMF species, and both species had been widely evidenced to form good symbiotic relationships with host plants and could enhance plant performance [33, 36]. Moreover, it was reported that Rhizophagus irregularis had a greater positive effect on C3 plant performance than mixed AMF inoculum, and Funneliformis mosseae improved much more on C4 plants than mixed AMF inoculants [36]. We guess that the major reason for the greater promoting effects on plant growth and nutrition of single AMF than mixed AMF in this study might be that the applied mixed AMF inoculum were usually just two AMF species and unable to form a good complementary relationship. Of course, more researches are needed to validate it in the future.

The AMF inoculation effects on plant biomass and N and P nutrients differs between leguminous and non-leguminous plants (Fig. 2b), indicating that the effects of AMF inoculation on plant biomass and N and P nutrients are depended on the functional characteristics of host plants. This is in accord with the results in Treseder [35] and Hoeksema et al. [54], in which the effects of AMF inoculation on biomass and P content differed between N-fixing woody and non-N-fixing woody and between N-fixing forb and non-N-fixing forb. Our results show that the improved effects of AMF inoculation on plant biomass and N nutrients are more obvious in legumes than in non-legumes (Fig. 2b). This indicates that the combined association of AMF species and Rhizobium exerted more benefits on the growth and N nutrients of host plants than infection alone [37]. It was also found that the increases in N levels of root and shoot tissues in Prosopis juliflora inoculated with the combination of Funneliformis fasciculatum and Rhizobium was more than those with single inoculation [37]. In contrast, AMF inoculation shows a little more benefit on plant P nutrients in non-legumes than in legumes (Fig. 2b). Similarly, the non-N-fixing woody was observed to show notable higher increase in P content than N-fixing woody with the presence of AMF [35]. This implies that Rhizobium may weaken the positive effects of AMF inoculation on plant P nutrients. The possible reason is that the N fixation ability of Rhizobium is easily constrained by P and thus will compete with associated fungi or plants for P [55].

Influences of AMF colonization rate, experiment duration, N addition, P addition, and water condition on AMF inoculation effects on plant biomass and N and P nutrients

AMF colonization rate is an important index concerning the relationship between AMF and host plants, which can reflect the extent of mycorrhizal infection and the effects of AMF on host plants to a large extent [56]. Usually, the effect sizes of AMF inoculation on plant biomass and nutrition, especially P, are expected to increase with increasing AMF colonization rate [10, 16, 35]. Consistently, the effect sizes of AMF inoculation on plant biomass and P concentration and P uptake increase with AMF colonization rate in this study (Fig. 3A), demonstrating that high AMF colonization rate is more conducive to plant P acquisition. Besides, the responses of N uptake in whole plant and N concentrations in plant belowground to AMF inoculation are positively correlated with AMF colonization rate (Fig. 3A & S3A). This result reveals a potential greater role of high AMF colonization rate in improving plant N nutrition than low AMF colonization rate. These results evidence the importance of improving infection rate to enhance AMF inoculation effects on plant performance.

It is theoretically expected that the inoculated AMF need time to establish the infection with host plants and develop their extraradical mycelium [38, 39]. Therefore, the increasing AMF functions and then AMF inoculation effects on plant performance with increasing experiment duration is expected. Unexpectedly, the response ratios of biomass, N and P nutrition are unchanged with increasing experiment duration (Fig. 3B). This pattern may be related to that, most of the experiments occurred in this study are conducted in laboratory using pots, in which the nutrient availabilities are high in the early period of the experiment and decrease with increasing experiment duration [33]. In view of this, AMF inoculation effects in the early stage of experiment are limited by fewer hyphae, while the comparable effects of AMF inoculation in the late stage may be constrained by the limited nutrient availabilities. However, it cannot be simply inferred from this result that experiment duration does not influence the effects of AMF inoculation on plant growth and nutrition. In the future, more field experiments are needed to verify, as the nutritional changes over experiment duration are relatively small in field experiments.

Nitrogen and P availabilities are regarded as the major factors controlling the AMF inoculation rate and functions [16, 41, 42, 57]. It has long been recognized that plant response to AMF inoculation usually decreases with increasing N and P addition because plants will tend to reduce carbon allocation to roots and mycorrhizas in such an environment [16, 41, 58, 59]. However, we unexpectedly find that AMF inoculation effects on N and P nutrition increase with N and P addition (Fig. 3C & 3D). This seems to contradict previous conclusions, in fact that is not the case. Although plant response to AMF inoculation under different N or P applications has been extensively studied, the N and P nutrition or limitation of host plants should be viewed together rather than separately to avoid contradictions [54, 60]. Generally, plant performance benefit most from AMF inoculation when plants are P limited rather than N limited because N limitation will reduce plant photosynthetic capacity and thus C supply for the fungi [9, 10, 16]. Differences in plant N/P between control and AMF treatment increase both with N and P addition, suggesting that plant P limitation is aggravated by AMF inoculation along with increasing N and P addition (Fig. S4). This may explain why AMF inoculation effects on plant N and P nutrition are positively correlated with N and P addition.

AMF have additional non-nutritional benefits for host plants, as they can improve the adaptabilities of host plants to diverse environment status, such as water condition [61, 62]. Therefore, water condition is also an important factor influencing AMF functions [32, 33, 61] in addition to N and P nutrients in growth medium. AMF inoculation effects on N and P nutrition of whole plant are positively correlated with water condition (Fig. 3E), suggesting greater functions of AMF infection under higher water regimes. Our previous experiment showed similar results that the inoculation of Funneliformis mosseae exerted greater benefits on regulating maize biomass and N uptake strategy under higher water availability [33]. The possible cause is that, well-watered conditions can support better growth and then larger functional effects of mycelium [63–65].

Influences of experiment type and N type on AMF inoculation effects on plant biomass and N and P nutrients

Despite the overall positive effects of AMF inoculation, this study displays that not all the effect sizes of AMF inoculation on plant performance in laboratory- and field-based trials distinctly higher than zero, though no negative effects are found (Fig. 4a). Importantly, we find markedly greater AMF inoculation effects on plant performance in laboratory experiments than in field experiments (Fig. 4a). These results are consistent with previous studies and indicate that the experiment type could influence the outcomes of AMF inoculation [16, 54]. Three reasons could be responsible for the more positive effects of AMF inoculation in laboratory experiments. First, higher AMF background in non-inoculated controls in field experiments should be the most important ones, which causes lower increases in AMF colonization rate by AMF inoculation (Fig. S5) and thus smaller AMF inoculation effects compared with those in laboratory experiments. Second, the inter- and intraspecific competition for light, water or nutrients among plants in most filed tests are often absent for laboratory studies [19], which could weaken the AMF inoculation effects in field experiments. Third, the significant difference in sample size between laboratory and field experiments (739 vs. 20 for whole plant biomass; 324 vs. 30 and 161 vs. 8 for N uptake in plant aboveground and belowground, respectively; 283 vs. 30 and 136 vs. 8 for P uptake in plant aboveground and belowground, respectively, Fig. 4a) is also a possible reason, and this also emphasizes the importance and necessity to carry out more in situ researches.

Host plants as well as AMF species often show diverse N preference [30, 33, 66–68]. Furthermore, most studies considered that their N preferences are depended on environment N availability and composition thus show plasticity [69, 70]. The applied N forms therefore should influence the AMF inoculation effects on plant growth and nutrient acquisition, especially for N uptake [33]. The effect sizes of AMF inoculation on plant biomass, P concentration, N and P uptake show great variations among different N types (Fig. 4b), implying that N forms play an important role in regulating AMF inoculation effects on response variables. Specifically, the promoted effects of AMF inoculation on those variables are greatest as NO3– applied while lowest as NH4+ applied (Fig. 4b). This indicates that NO3– is the most conducive N form but NH4+ is the least conducive N form to the improvement of AMF inoculation on plant performance [33], which should be mainly related to the physiologically toxic of high NH4+ concentration on plants and highly accessibilities of NO3– for plants [71].

Conclusions

We conduct a meta-analysis on the effects of AMF inoculation on plant performance variables including biomass, N concentration, P concentration, N and P uptake. This study clearly reveals that AMF inoculation significantly improve plant growth and N and P nutrition, and the magnitudes of AMF inoculation effects on plant performance are influenced by AMF type, plant type, AMF colonization rate, experiment duration, N addition, P addition, water condition, experiment type, and N type (Fig. 5). Specifically, AMF inoculation benefits for plants are larger in single AMF inoculation compared to mixed AMF inoculation, leguminous plants compared to non-leguminous plants, laboratory experiments compared to field experiments. The response ratios of plant biomass and N and P nutrients to AMF inoculation increase with increasing AMF colonization rate and keep unchanged with increasing experiment duration. AMF inoculation effects on whole plant N and P concentrations are positively correlated with N addition, P addition, and water condition (Fig. 5). Additionally, the positive effects of AMF on the response variables are highest when NO3– is applied, followed by urea and the mixture of NO3– and NH4+, while lowest when NH4+ is used (Fig. 5). Results of this meta-analysis provide comprehensive knowledges of the responses of plant biomass and N and P nutrients to AMF inoculation, and will improve our understandings of the mechanisms for AMF inoculation effects on plant growth and nutritional status.

Fig. 5.

Fig. 5

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A conceptual framework for the plant responses to AMF inoculation and their changes with various biotic and abiotic factors. Biom, biomass; Nconcen, N concentration; Pconcen, P concentration; Nuptake, N uptake; Puptake, P uptake. The upward arrows and numbers indicate the increases in percentage change by AMF inoculation. The above right panel show how AMF colonization rate, experiment duration, N addition, P addition, and water condition (those factors are represented by different types of lines), and AMF type, plant type, experiment type and N type (those factors are indicated in arrows) affect the plant responses to AMF inoculation

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1 (31.6KB, xlsx)
Supplementary Material 2 (379.6KB, xlsx)
Supplementary Material 3 (1.7MB, docx)

Acknowledgements

Not applicable.

Abbreviations

AMF

Arbuscular mycorrhizal fungi

N

Nitrogen

P

Phosphorus

Author contributions

Yingjie Wu and Chongjuan Chen planned and designed the research. Yingjie Wu collected data, conducted analyses, and wrote original manuscript. All authors commented on the manuscript.

Funding

This research was supported by grants from the National Natural Science Foundation of China (No. 42003061, 42272213).

Data availability

Data is provided within the manuscript or supplementary information files.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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