Abstract
Whether arbuscular mycorrhizal fungi (AMF) inoculation promotes soil C sequestration is largely unknown. Here, meta-analysis and logistic regression were applied to study the ecological effects of AMF inoculation on soil organic C (SOC) turnover and plant growth under different inoculation manipulations, plant traits, and soil conditions. Results showed that AMF inoculation generally increased SOC stock and plant biomass accumulation. Soil sterilization, unsterilized inoculum wash (a filtrate of mycorrhizal inoculum excluding AMF) addition in non-mycorrhizal treatments, experimental type, and inoculated AMF species influenced soil microbial biomass C (MBC) but had no impact on SOC turnover. Plant root system, initial SOC content, and soil pH were the key factors that influenced the AMF-mediated SOC turnover. AMF inoculation in fertile or acidic soils might deplete SOC. The symbiosis between tap-rooted plants and AMF was more likely to sequestrate C into the soil compared to fibrous-rooted plants. Moreover, plant total dry biomass largely relied on its own photosynthetic pathway although AMF was introduced. Collectively, our results suggest that AMF inoculation is a promising approach for soil C sequestration.
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Introduction
Pedosphere is the most important reservoir of C in terrestrial ecosystems that links the biosphere and atmosphere (Wei et al. 2014; Parihar et al. 2020), which influences global C cycling and climate change (Schmidt et al. 2011; Wang et al. 2013; Zhang et al. 2018a). SOC stock mainly depends on the net primary productivity and the distribution of photosynthetic C between above- and below-ground biomass (Zhu and Miller 2003). AMF can influence primary productivity and global C cycling by forming symbiotic associations with more than 80% of the terrestrial plant species (Parniske 2008; Lee et al. 2013; Jia et al. 2023). Estimates show that approximately five Pg of C flows from the air into the soil by AMF symbionts every year (Bago et al. 2000; Soudzilovskaia et al. 2015). In addition, AMF is an important member of the root microbiome, which is widely used as a soil amendment to increase agricultural productivity and restore polluted soils (Hildebrandt et al. 2007; Kumar et al. 2015; Wang 2017). Meanwhile, AMF inoculation may be an effective biological tool for sequestrating C and improving plant health (Wu et al. 2023), especially under various stress conditions.
Hyphosphere, the active zone of soil surrounding extraradical fungal hyphae (Wang et al. 2022), plays an important role in soil C cycling (See et al. 2021). The hyphosphere microorganisms can enhance the mobilization of nutrients (Zhang et al. 2018b), which helps AMF acquire nutrients to meet their nutritional requirements, therefore stimulating mycelial growth (Frey-Klett et al. 2007). Studies have shown that the AMF extraradical hyphal networks account for 20–30% of the total soil microbial biomass (Miller and Kling 2000; Leake et al. 2004). The rapid turnover rate of extraradical mycorrhizal hyphae contributes directly to SOC formation and soil C cycling (Staddon et al. 2003). Meanwhile, hyphal cell walls are recalcitrant to microbial decomposition since they are mainly composed of chitin; therefore, the hyphal residues still accumulate in the soil under such high turnover rates (Zhu and Miller 2003; Leake et al. 2004). In addition, AMF also contribute indirectly to soil C sequestration by promoting soil aggregation (Zhu and Miller 2003; Leifheit et al. 2014). The exudates released by AMF extraradical hyphae bind soil particles and enhance soil aggregate stability (Wang et al. 2022). Moreover, AMF extraradical hyphae enmesh and entangle microaggregates into macroaggregates, which reinforces the physical protection of SOC (Miller and Kling 2000; Parihar et al. 2020). However, AMF inoculation may also stimulate the decomposition of fresh residues (e.g., litter) by regulating the activity and community composition of soil microorganisms (Wei et al. 2019).
Symbiotic relationships between plants and AMF depend on the benefits that host plants receive from the symbionts, which are largely affected by plant traits and AMF species. Plant root morphology (root architecture) and photosynthetic pathway (C3 or C4) reflect the nutrient uptake ability and energy supply condition of plants therefore influencing the reliance of plants on mycorrhizal symbiosis (Chandrasekaran et al. 2016, 2019; Li et al. 2023; Duan et al. 2023). Evidence shows that plants with tap-rooted system are more dependent on AMF and benefit more from mycorrhiza than the fibrous-rooted plants (Yang et al. 2015). However, the meta-analysis of Maherali (2014) indicates that the effect of AMF inoculation on plant growth is insensitive to the root to shoot ratio, root diameter, root hair length, and root hair density. In addition, C4 plants generally have higher photosynthetic efficiency and tolerance to adverse soil conditions compared to C3 plants (Nayyar and Gupta 2006; Taylor et al. 2010; Wang et al. 2012). However, the influence of AMF inoculation to host plants with different photosynthetic pathways remains unclear as contradictory results are reported in different studies (Hoeksema et al. 2010; Augé et al. 2015).
Plant-microbe-soil interactions determine the outcomes of mycorrhizal symbiosis in different soils, which are intimately associated with soil biota activities (Larimer et al. 2010; Jiang et al. 2020; Nerva et al. 2022). Synergism occurs when the symbionts of AMF and bacteria contribute differently to the host plant (Hoseinzade et al. 2016), while antagonism occurs when there is a competition for nutrients and energy between symbionts or when the function of symbionts overlaps with each other (Stanton 2003; Leigh et al. 2011). In addition, plants are less dependent on AMF in nutrient-rich environments (Schultz et al. 2001). Therefore, plants tend to invest less carbohydrates to AMF in managed ecosystems, which leads to a negative correlation between AMF colonization and soil nutrient availability (Miller et al. 1995; Kluber et al. 2012; Hou et al. 2019; Jerbi et al. 2021). The cost-benefit relationship between host plants and AMF shifts in nutrient-deficient soils, depending on soil N and P availability (Reynolds et al. 2005; Fellbaum et al. 2012). The symbiotic relationship between plants and AMF may even change from mutualism to parasitism under C limitation (Johnson et al. 2015). Moreover, soil pH affects soil nutrient availability, which regulates the relationships between host plants and AMF but there is no agreement on the relationship between AMF abundance and soil pH (Rozek et al. 2020; Jerbi et al. 2021).
Recent studies emphasized the importance of AMF in soil C sequestration (Frey 2019; Verbruggen et al. 2021; Wu et al. 2023); however, most of these studies only conceptually discuss and conclude the pathways that AMF may have on SOC turnover. Here, we analyzed the role of AMF in SOC turnover combining the factors of inoculation manipulations, plant traits, and soil conditions using meta-analysis and logistic regression model. We hypothesized that AMF inoculation might increase the biomass of mycorrhizal symbionts, which subsequently led to soil C sequestration.
Materials and methods
Data collection
An extensive literature search was performed with the following bibliographic databases: Web of Science, ScienceDirect, and China National Knowledge Infrastructure (CNKI), covering all the research papers that were published before September 2022. The following search terms were used: (Arbuscular mycorrhiz* OR AM fungi OR AMF) AND soil AND (C or organic matter). From this search, 5360, 456, and 281 peer-reviewed publications were retrieved from Web of Science, Science Direct, and CNKI, respectively. After deleting duplicate papers, a total of 6014 articles were found. The publications were selected based on the following criteria to reduce bias: (1) mycorrhizal inoculation treatment and a corresponding non-mycorrhizal treatment (control) must be conducted in parallel under the same environmental conditions in each experiment; (2) the species of the host plant in each experiment must be mentioned; (3) the inoculation procedure of AMF must be explained explicitly, including the species of AMF (multiple or single) and the pre-treatment of the soil (sterilized or non- sterilized); (4) at least three replicates were included in each experimental treatment; (5) treatments with both AMF inoculation and soil organic amendments (such as biochar) were excluded to improve comparability; and (6) treatments with both AMF and non-mycorrhizal microorganisms (such as plant growth promoting rhizobacteria) were excluded. In the end, 132 peer-reviewed publications were included in our dataset (Supplementary Data 1).
Only the data from the top layer at the final sampling time were extracted when there were multiple soil layers or sampling times within one study. Each pair of host plant and AMF species was considered an independent observation when there were different combinations of plants and AMF within one study. For each study, the following data were collected: experimental duration, experimental type (field or pot), plant species, AMF species, AMF inoculum type (single-species or multi-species), extraradical hyphal density, root mycorrhizal colonization rate, soil sterilization before inoculation, unsterilized inoculum wash addition in non-mycorrhizal treatments, fertilization, and initial soil properties, including soil pH, SOC, and total N (TN). The mean, standard error (SE) or standard deviation (SD), and sample size (n) of the SOC, MBC, total N and P content of plant root and shoot, and total dry weight biomass of the host plant (TDB) in both mycorrhizal and non-mycorrhizal treatments were either collected from tables and texts or extracted from figures using Web Plot Digitizer (version 4.6). Each variable was unified to its most commonly used unit before meta-analysis. Soil organic matter (SOM) was calculated to SOC by dividing the empirical factor of 1.724 when no explanatory information was available in the publication. SE was converted to SD by multiplying the square root of the respective sample size (Eq. 1). When SD and SE were both missing, we estimated the respective SD according to the method provided by Yang et al. (2015). Briefly, the coefficient of variations (\({\text{CV}}=\frac{{\text{SD}}}{{\text{mean}}}\)) of the observations that had both mean and SD were calculated and then averaged to get an average CV of the dataset. The missing SD was approximated by multiplying the respective mean value with the average CV. The soil pH of the CaCl2 solution extract was converted to the soil pH of deionized water extract using Eq. 2 (Augusto et al. 2008). If the extraction method was not reported in the publication, deionized water extraction was assumed to be the default method.
Variable interpretation
-
(1)
Inoculation type was categorized into two main classes: “single” and “mixed” inoculum by the number of AMF species in the inoculum. Most of the studies involved only one species of AMF within the following ten genera: Acaulospora, Claroideoglomus, Corymbiglomus, Diversispora, Funneliformis, Gigaspora, Glomus, Paraglomus, Rhizophagus, and Septoglomus (AMF classification based on Schüßler and Walker 2010). The most frequently-used AMF genera (100 studies) were Funneliformis and Rhizophagus; therefore, they were separated as two individual subgroups and the remaining eight genera were classified together as “others.” As for the mixed group, the AMF inocula were either commercial inoculum or the natural AM fungi present in field plots and contained more than one mycorrhizal species. Therefore, there were four subgroups of inoculation type in the meta-analysis: “Funneliformis,” “Rhizophagus,” “others,” and “mixed.”
-
(2)
Previous studies have shown that the morphology of plant roots may affect the colonization of AMF; thus, plant root systems were classified as “tap” and “fibrous” roots according to the method of Yang et al. (2015). In addition, the host plant was categorized as “C3” and “C4” plant based on its photosynthetic pathway. The plant types were obtained either directly from the manuscript or from other peer-reviewed papers involving the same plant species.
-
(3)
Fertilization indicated whether inorganic fertilizers were applied during the experiment. There were two major subgroups: fertilized (F) and non-fertilized (nF). The fertilized subgroup was further divided into N fertilizer addition (N) and N and P fertilizer addition (NP). However, the application amount of the fertilizer was not analyzed due to the limited sample size.
-
(4)
Soil sterilization before AMF inoculation determined whether the growth of the newly added AMF was influenced by the native microorganisms. Consequently, the incubation conditions were divided into two categories: experiments with non-sterilized soils were marked as “non-sterilized,” while those with sterilized soils were marked as “sterilized.”
-
(5)
Experimental type had two levels: pot studies/experiments and field experiments.
-
(6)
Experimental duration was divided into three levels: short-term (≤ 60 days), medium-term (60–180 days), and long-term (> 180 days).
-
(7)
Whether the AMF inoculum wash was added to non-mycorrhizal treatments was marked by: no Wash addition and Wash addition. The addition of AMF inoculum filtrates equalized the background microflora between AMF inoculated treatment and the control.
Meta-analysis
The natural logarithm transformed response ratio (lnRR) was used to calculate the effect size using the following equation:
where Xe and Xc were the mean values of a certain variable in the AMF-inoculated treatment and the respective control. Weighed effect sizes were calculated using the inverse variance method. The random effects model was applied to pool the mean effect size of each subgroup, and the 95% confidence interval (CI) of the mean effect size was estimated on the basis of the standard normal distribution. The effect of AMF inoculation on a certain variable was significantly positive (or negative) when the lower and upper limits of the 95% CI were both larger (or smaller) than zero; otherwise, the effect of AMF inoculation was not significant since the 95% CI overlapped with zero.
The relationship between the weighted effect sizes and the initial SOC, TN, soil C to N ratio, and pH were tested separately by meta-regression using a linear regression approach (if the sample size is sufficient: n ≥ 10).
Logistic regression
Logistic regression was performed to access the importance of different predictor variables (plant type, root system, fertilization, inoculation type, growth condition, inoculum wash addition, and initial soil properties) on the change of SOC, MBC, and TDB after AMF inoculation. C3 plant, tap root, mixed inoculum, no soil sterilization, no fertilization, and no wash addition were set as the baselines of the respective categorical predictor variables. Effects of AMF inoculation on the response variables (SOC, MBC, and TDB) were transformed into binary outcomes of positive (increasing) and negative (decreasing). Only the two main classes of the AMF inoculation type (“single” and “mixed”) and fertilization type (fertilized and non-fertilized) were chosen in the model. The weight of each observation was calculated with Eq. 4 and rounded afterwards, where ne and nc were the sample sizes of the AMF-inoculated treatment and the respective control.
A full model of the logistic regression was simulated using all the predictor variables with the Eq. 5, where P was the probability that AMF inoculation had a positive effect on the response variable (e.g., increasing SOC content); the ratio of P to 1-P was commonly referred as the odds; xi, n, α, and βi were predictor variables, the total amount of the predictor variables, intercept, and coefficients.
Continuous predictor variables were standardized before simulation for better comparison. Observations with the Cook’s distance over 0.5 were considered to be outliers and removed from the dataset. The stepwise algorithm from both directions (forward and backward) was applied to select variables from the full model. McFadden’s, Cox and Snell’s, and Tjur’s pseudo-R2 were calculated to compare different models. The Hosmer-Lemeshow test was performed to examine the goodness of fit of a logistic regression model. The significance of the variables included in the final model was tested using the likelihood ratio chi-square test.
Results
Inoculation manipulations
The inoculation of AMF positively affected SOC, MBC, plant total dry biomass (TDB), and the P content of plant shoots (Fig. 1). However, no significant difference was found between the non-sterilized and sterilized subgroups except for the MBC (Fig. 1a). Soil sterilization led to an average increase of 110.97% in MBC, which was 5.79 times higher than that of the non-sterilized subgroup (Fig. 1a). In contrast to the significant increase in P uptake by plant shoots, the uptakes of N in plant roots and shoots were not sensitive to AMF inoculation except for the shoot N uptake in the non-sterilized subgroup (increased by 2.58–38.62%).
AMF inoculum wash addition to non-mycorrhizal treatments significantly influenced soil MBC but had no effects on SOC, TDB, root N, root P, Shoot N, and shoot P (Fig. 1b). Wash addition retarded the effect size (lnRR) of MBC by 57.94% compared to those without wash additions, despite that the sample size of the wash addition subgroup was 7.83 times smaller than the no wash addition subgroup. Moreover, wash addition was likely to reduce plant shoot N content with an average lnRR of − 0.05 since the 95% confidence interval overlapped with zero.
There was no significant difference between AMF inoculation types in terms of TDB (Fig. 2a). Inoculation of Funneliformis significantly increased SOC by 234.52% compared to the mixed subgroup (inoculation of multiple AMF species), while the effect of Rhizophagus and other single AMF species on SOC was not significantly different from the Funneliformis and the mixed subgroup. The average increase of MBC in the mixed subgroup was 1.93, 5.19, and 3.66 times higher than that of the single inoculation subgroups of Funneliformis, Rhizophagus, and other AMF genera, respectively. Only the MBC of the latter two subgroups was significantly lower than the mixed subgroup.
Fertilization and experimental conditions
Fertilization significantly influenced the effect of AMF inoculation on SOC and MBC but had no effect on TDB (Fig. 2b). In detail, AMF inoculation greatly promoted the accumulation of SOC in non-fertilized soils, which was 2.46 times higher than that in the fertilized soils. In contrast, the increase of MBC in the non-fertilized subgroup only accounted for 29.33% of the increase in the fertilized subgroup averagely. However, AMF inoculation may reduce SOC and MBC in soils added with N fertilizer, leading to an average decrease of 0.74% and 5.82%, respectively. Moreover, the increase of TDB in soils added with N fertilizer was significantly lower than the others.
Experimental types and duration only affected soil MBC after AMF inoculation (Fig. S1). Soil MBC increased considerably in pot experiments, which was 4.29 times higher than the field experiments (Fig. S1a). In addition, the effect of AMF inoculation on MBC was greater in long-term experiments (> 180 days) than in medium-term experiments (60–180 days). However, both medium-term and long-term experiments were not significantly different from the short-term experiments (≤ 60 days) in terms of MBC (Fig. S1b).
Plant type and root system
Plant photosynthetic pathway (C3/C4) and plant root system (tap/fibrous) alone had no obvious effect on SOC stock; whereas AMF inoculation in tap-rooted C4 plant treatments (C4-T) increased SOC by 326.88% compared to the fibrous-rooted C4 plants (C4-F) (Fig. 3a). The increases of TDB due to AMF inoculation in tap-rooted plants were 1.87 times higher compared to fibrous-rooted plants. This phenomenon was more pronounced among C3 plants, although plant photosynthetic pathway generally had no effect on TDB (Fig. 3c). Moreover, the average increase of MBC in fibrous-rooted plants was 5.45 times higher than that of the tap-rooted plants among C3 plants (Fig. 3b). AMF inoculation significantly promoted plant P uptake in both shoots and roots except for fibrous-rooted C3 plants (Fig. S2c, d), but had no effect on plant N uptake (Fig. S2a, b).
Soil conditions and AMF colonization rates
The effect size (lnRR) of AMF inoculation on SOC was negatively correlated with the initial SOC content (Fig. 4a). According to the linear regression formula, AMF inoculation reduced SOC stock when the initial SOC content was higher than 18.81 g kg–1. In addition, AMF inoculation increased soil MBC only when the root mycorrhizal colonization rate exceeded 22.9%, despite that the effect size of MBC was positively correlated with the colonization rate (Fig. 4b). Increasing external mycorrhizal hyphal density and AMF colonization rate of roots led to larger accumulations of P in plant shoots and roots (Fig. 4c, d, e, f).
Contribution of environmental factors to SOC, MBC, and TDB
Root type, initial SOC content, and soil pH significantly influenced the SOC turnover in soils inoculated with AMF (Fig. 5). While the effect of AMF inoculation on SOC turnover was not sensitive to plant type, fertilization, and soil C to N ratio since they were excluded from the full model of the logistic regression for SOC by the stepwise algorithm. In detail, the odds of increasing SOC for fibrous-rooted plants were reduced by 96.0% compared to tap-rooted plants, indicating that the symbiosis association between AMF and tap-rooted plants was more likely to sequestrate C into the soil. In addition, AMF inoculation in soils with higher initial SOC content was less likely to increase SOC stock, while increasing soil pH level (ranging from 4.5 to 9.1) was more likely to cause SOC sequestration.
Plant type (C3/C4) was the key factor that influenced the total dry biomass (TDB) of plants under AMF inoculation, where C4 plants were more likely to produce higher TDB than C3 plants (Table S1). Specifically, the odds of increasing TDB for C4 plants was 14.65 times higher compared to C3 plants. Fibrous-rooted plants had a relatively lower odds (0.26) of increasing TDB compared to tap-rooted plants, although the influence of plant root system was less important compared to plant type. In addition, soil sterilization was the only factor that had a significantly effect on soil MBC, which increased the odds of increasing soil MBC by 11.89 times compared to non-sterilized soils. However, the effect of AMF inoculation on TDB and MBC was not influenced by inoculation types, indicating that most of the AMF species were highly adaptive to different ecosystems. Unfortunately, we could not include the inoculum wash addition in the logistic model for MBC due to lack of data.
Discussion
Soil sterilization before AMF inoculation substantially decreases the population of the living microbes in the soil, avoiding competitions by soil microbes for nutrients and C (Tiunov and Scheu 2005; Sghir et al. 2014). In addition, soil sterilization generates a large amount of microbial necromass that provides extra labile C and energy for the living soil microbes (Zhang et al. 2023). Thus, the MBC of sterilized soils observed in this study may be significantly higher than that of the non-sterilized soils. Meanwhile, the input of microbial necromass triggers soil C priming effects that reduces SOC stock (Shahbaz et al. 2016), which counteracts the accumulating effect of the increased soil MBC on SOC stock. Moreover, the nutrient supply from mycorrhizal symbionts to host plants may be reduced in sterilized soils because AMF lack saprotrophic capability (Hodge et al. 2010) and most of the living microbes, including saprophytic microorganisms, are exterminated during sterilization. This explains why plant growth and nutrient uptake in sterilized soils are similar to those in non-sterilized soils, even if the MBC of the former is significantly higher than the latter. In addition, AMF inoculum wash addition directly increases the MBC of the non-mycorrhizal treatments; therefore, the increasing effect of AMF inoculation on MBC is weakened in the wash addition subgroup. This phenomenon may be amplified because of the proliferation of the microorganisms in the newly added wash during the experiment. Moreover, a large proportion of the included studies failed to equalize non-AM microorganisms during AMF inoculation. Therefore, the positive effect of AMF inoculation on soil MBC may be exaggerated in these studies because the effects reported for AMF treatments are not solely due to the inoculated fungi but to the combination of AMF and its associated microflora. However, the intervention of imbalanced background soil microflora on SOC (even MBC) is minor compared to soil sterilization.
Some studies show that the responses of plant growth and SOC turnover to AMF species and diversity varied significantly (Giri et al. 2003; Jin et al. 2013; Al-Karaki and Williams 2021; Frew 2021). However, according to the logistic regression in this study, the effect of AMF inoculation on SOC and TDB is insensitive to neither the species of AMF nor the diversity of the AMF species of the inoculum (inoculation type). One possible reason for the different results is the high functional redundancy among AMF species (Hahn et al. 2018). Consequently, inoculations of single AMF species lead to similar results, while the effectiveness of mixed inoculation is reduced because of the intense competition between AMF with similar functions (Maherali and Klironomos 2007; Yang et al. 2017), especially those within the same family (Crossay et al. 2019). Despite all these differences due to inoculation manipulations, AMF inoculation, as a soil ameliorating method, universally promotes plant growth and SOC accumulation.
The meta-analysis of Maherali (2014) indicated that there was no clear relationship between root architecture and plant growth response to AMF colonization. Similarly, the result of our meta-analysis failed to distinguish the role of root types in promoting plant growth and SOC accumulation, although the mean effect sizes of SOC and TDB for tap-rooted plants are higher than those for fibrous-rooted plants. However, combining the results of our logistic regression, it can be concluded that tap-rooted plants generally benefit more from the mycorrhizal symbiosis compared to fibrous-rooted plants, which further leads to more pronounced increases of TDB and SOC. This is in line with the results of Yang et al. (2015), who found that fibrous-rooted plants might be less dependent on mycorrhiza than tap-rooted plants. The main reason for this phenomenon is that fibrous-rooted plants already have well-developed fine roots and active root hairs, while tap-rooted plants rely on mycorrhizal symbiosis absorbing nutrients (Sullivan et al. 2000; Bates and Lynch 2001; Yang et al. 2015). Therefore, the increase of plant TDB is more pronounced in tap-rooted plants than in fibrous-rooted plants under AMF inoculation, which sequestrates more C into the soil (SOC) because mycorrhizal symbionts enhance the reallocation of photosynthetic C into below-ground biomass (Heinonsalo et al. 2010).
Plant photosynthetic pathway may be more important to TDB than root type under AMF inoculation according to the results of our logistic regression model. Generally, C4 plants can accumulate more biomass compared to C3 plants because C4 plants have higher photosynthesis efficiency and adaptability to adverse conditions (Wang et al. 2012; Pinto et al. 2014). Consequently, C4 plants are more responsive to mycorrhizal inoculation than C3 plants since the nutrient demand of C4 plants is generally higher than C3 plants (Frew 2019; Hoeksema et al. 2010). The formation of mycorrhizal symbiosis can activate soil microorganisms and improve soil nutrient availability in the rhizosphere, which enlarges the difference in TDB between C4 and C3 plants. In addition, C3 plants inoculated with AMF reduce aboveground respiration to offset the increased belowground C demand, but C4 plants increase photosynthetic rates to cover the C demand for AMF (Rezácová et al. 2018). This tactical advantage allows C4 plants to accumulate more C under AMF inoculation compared to C3 plants. However, the absorptive roots of C4 plants are usually thinner than C3 plants (Edwards et al. 2010; Ma et al. 2019), which may limit the external hyphal length density and colonization rate (Sun et al. 2022). Therefore, C4 plants may depend less on AMF symbiosis compared to C3 plants.
The effect of AMF inoculation is influenced by soil environmental conditions, such as soil pH and nutrient limitations (Yang et al. 2015). Previous studies have shown that root mycorrhizal colonization is positively correlated with soil pH within the range of 5.5 to 7.5, and AMF has a higher colonization rate in near neutral or slightly alkaline soils (Soti et al. 2014; Carrino-Kyker et al. 2016). Similar results were also found in this study but with a wider range of soil pH ranging from 4.5 to 9.1, meaning that mycorrhizal symbiosis is more resilient to extreme soil pH conditions than previously expected. In addition, our results indicate that AMF inoculation depletes SOC in soils with high initial SOC contents. This may be attributed to the enhanced soil priming effects since considerable amounts of fresh plant C are transferred to the soil through the mycorrhizal hyphal network (Kaiser et al. 2015; Frey 2019). Moreover, the C loss via soil priming effects is greater in more fertile soils (Huang et al. 2021), which explains why the increase of SOC in fertilized soils is significantly lower than that in non-fertilized soils. Additionally, balanced fertilization (N and P) increases soil microbial biomass and microbial Cuse efficiency, which leads to more respiratory C loss and less C sequestration compared to non-fertilization soils (Lin et al. 2012). In contrast, AMF inoculation is likely to deplete SOC under the sole application of N fertilizers probably because extra N supply may trigger P limitation that stimulates soil microbes to mine for P from the SOM (Xiao et al. 2019).
Conclusion
This study investigated the effects of AMF inoculation on soil C turnover and plant growth under different inoculation manipulations, plant traits, and soil conditions by meta-analysis and logistic regression. Our study reveals that AMF inoculation generally enhances plant biomass accumulation and sequestrates more C into SOC, but the increasing effects are insensitive to the species of inoculated AMF. Root type, initial SOC content, and soil pH are the most important factors that influence SOC turnover under AMF inoculation. AMF inoculation is likely to deplete SOC stock in soils with high initial SOC contents. Plant photosynthetic pathways and soil sterilization are the determinant factors for TDB and MBC, respectively. This study confirms that AMF inoculation is a promising way to sequestrate C in soils with low SOC contents. However, the plant-microbe-soil interactions triggered by AMF inoculation are still unclear and need further investigation.
Data Availability
The data will be available on request.
References
Al-Karaki GN, Williams M (2021) Mycorrhizal mixtures affect the growth, nutrition, and physiological responses of soybean to water deficit. Acta Physiol Plant 43:75. https://doi.org/10.1007/s11738-021-03250-0
Augé RM, Toler HD, Saxton AM (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24. https://doi.org/10.1007/s00572-014-0585-4
Augusto L, Bakker MR, Meredieu C (2008) Wood ash applications to temperate forest ecosystems - potential benefits and drawbacks. Plant Soil 306:181–198. https://doi.org/10.1007/s11104-008-9570-z
Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–957. https://doi.org/10.1104/pp.124.3.949
Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236:243–250. https://doi.org/10.1023/A:1012791706800
Carrino-Kyker SR, Kluber LA, Petersen SM, Coyle KP, Hewins CR, DeForest JL, Smemo KA, Burke DJ (2016) Mycorrhizal fungal communities respond to experimental elevation of soil pH and P availability in temperate hardwood forests. Fems Microbiol Ecol 92:fiw024. https://doi.org/10.1093/femsec/fiw024
Chandrasekaran M, Kim K, Krishnamoorthy R, Walitang D, Sundaram S, Joe MM, Selvakumar G, Hu SJ, Oh SH, Sa T (2016) Mycorrhizal symbiotic efficiency on C3 and C4 plants under salinity stress - a meta-analysis. Front Microbiol 7:1246. https://doi.org/10.3389/fmicb.2016.01246
Chandrasekaran M, Chanratana M, Kim K, Seshadri S, Sa T (2019) Impact of arbuscular mycorrhizal fungi on photosynthesis, water status, and gas exchange of plants under salt stress-a meta-analysis. Front Plant Sci 10:457. https://doi.org/10.3389/fpls.2019.00457
Crossay T, Majorel C, Redecker D, Gensous S, Medevielle V, Durrieu G, Cavaloc Y, Amir H (2019) Is a mixture of arbuscular mycorrhizal fungi better for plant growth than single-species inoculants? Mycorrhiza 29:325–339. https://doi.org/10.1007/s00572-019-00898-y
Duan DD, Feng XX, Wu NN, Tian Z, Dong X, Liu HN, Nan ZB, Chen T (2023) Drought eliminates the difference in root trait plasticity and mycorrhizal responsiveness of two semiarid grassland species with contrasting root system. Int J Mol Sci 24:10262. https://doi.org/10.3390/ijms241210262
Edwards EJ, Osborne CP, Strömberg CAE, Smith SA, Consortium CG (2010) The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:587–591. https://doi.org/10.1126/science.1177216
Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Bucking H (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. P Natl A Sci USA 109:2666–2671. https://doi.org/10.1073/pnas.1118650109
Frew A (2019) Arbuscular mycorrhizal fungal diversity increases growth and phosphorus uptake in C3 and C4 crop plants. Soil Biol Biochem 135:248–250. https://doi.org/10.1016/j.soilbio.2019.05.015
Frew A (2021) Contrasting effects of commercial and native arbuscular mycorrhizal fungal inoculants on plant biomass allocation, nutrients, and phenolics. Plants People Planet 3:536–540. https://doi.org/10.1002/ppp3.10128
Frey SD (2019) Mycorrhizal fungi as mediators of soil organic matter dynamics. Annu Rev Ecol Evol S 50:237–259. https://doi.org/10.1146/annurev-ecolsys-110617-062331
Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36. https://doi.org/10.1111/j.1469-8137.2007.02191.x
Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of Acacia auriculiformis. Biol Fert Soils 38:170–175. https://doi.org/10.1007/s00374-003-0636-z
Hahn PG, Bullington L, Larkin B, LaFlamme K, Maron JL, Lekberg Y (2018) Effects of short- and long-term variation in resource conditions on soil fungal communities and plant responses to soil biota. Front Plant Sci 9:1605. https://doi.org/10.3389/fpls.2018.01605
Heinonsalo J, Pumpanen J, Rasilo T, Hurme KR, Ilvesniemi H (2010) Carbon partitioning in ectomycorrhizal Scots pine seedlings. Soil Biol Biochem 42:1614–1623. https://doi.org/10.1016/j.soilbio.2010.06.003
Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146. https://doi.org/10.1016/j.phytochem.2006.09.023
Hodge A, Helgason T, Fitter AH (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3:267–273. https://doi.org/10.1016/j.funeco.2010.02.002
Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407
Hoseinzade H, Ardakani MR, Shahdi A, Rahmani HA, Noormohammadi G, Miransari M (2016) Rice (Oryza sativa L.) nutrient management using mycorrhizal fungi and endophytic Herbaspirillum seropedicae. J Integr Agr 15:1385–1394. https://doi.org/10.1016/S2095-3119(15)61241-2
Hou LF, He XL, Li X, Wang SJ, Zhao LL (2019) Species composition and colonization of dark septate endophytes are affected by host plant species and soil depth in the Mu Us sandland, northwest China. Fungal Ecol 39:276–284. https://doi.org/10.1016/j.funeco.2019.01.001
Huang JS, Liu WX, Yang S, Yang L, Peng ZY, Deng MF, Xu S, Zhang BB, Ahirwal J, Liu LL (2021) Plant carbon inputs through shoot, root, and mycorrhizal pathways affect soil organic carbon turnover differently. Soil Biol Biochem 160:108322. https://doi.org/10.1016/j.soilbio.2021.108322
Jerbi M, Labidi S, Bahri BA, Laruelle F, Tisserant B, Ben Jeddi F, Sahraoui ALH (2021) Soil properties and climate affect arbuscular mycorrhizal fungi and soil microbial communities in Mediterranean rainfed cereal cropping systems. Pedobiologia-J Soil Ecol 87–88:150748. https://doi.org/10.1016/j.pedobi.2021.150748
Jia YY, Qin WH, Zhang T, Feng G (2023) Progress on mechanisms underlying arbuscular mycorrhizal fungi maintaining desert ecosystem stability under climate change. Chin Sci Bull 68:3172–3184. https://doi.org/10.1360/TB-2023-005
Jiang YJ, Luan L, Hu KJ, Liu MQ, Chen ZY, Geisen S, Chen XY, Li HX, Xu QS, Bonkowski M, Sun B (2020) Trophic interactions as determinants of the arbuscular mycorrhizal fungal community updates with cascading plant-promoting consequences. Microbiome 8:142. https://doi.org/10.1186/s40168-020-00918-6
Jin HY, Germida JJ, Walley FL (2013) Impact of arbuscular mycorrhizal fungal inoculants on subsequent arbuscular mycorrhizal fungi colonization in pot-cultured field pea (Pisum sativum L.). Mycorrhiza 23:45–59. https://doi.org/10.1007/s00572-012-0448-9
Johnson NC, Wilson GWT, Wilson JA, Miller RM, Bowker MA (2015) Mycorrhizal phenotypes and the Law of the Minimum. New Phytol 205:1473–1484. https://doi.org/10.1111/nph.13172
Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, Solaiman ZM, Murphy DV (2015) Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol 205:1537–1551. https://doi.org/10.1111/nph.13138
Kluber LA, Carrino-Kyker SR, Coyle KP, DeForest JL, Hewins CR, Shaw AN, Smemo KA, Burke DJ (2012) Mycorrhizal response to experimental pH and P manipulation in acidic hardwood forests. PLoS ONE 7:e48946. https://doi.org/10.1371/journal.pone.0048946
Kumar A, Dames JF, Gupta A, Sharma S, Gilbert JA, Ahmad P (2015) Current developments in arbuscular mycorrhizal fungi research and its role in salinity stress alleviation: a biotechnological perspective. Crit Rev Biotechnol 35:461–474. https://doi.org/10.3109/07388551.2014.899964
Larimer AL, Bever JD, Clay K (2010) The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51:139–148. https://doi.org/10.1007/s13199-010-0083-1
Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 82:1016–1045. https://doi.org/10.1139/B04-060
Lee EH, Eo JK, Ka KH, Eom AH (2013) Diversity of arbuscular mycorrhizal fungi and their roles in ecosystems. Microbiology 41:121–125. https://doi.org/10.5941/MYCO.2013.41.3.121
Leifheit EF, Veresoglou SD, Lehmann A, Morris EK, Rillig MC (2014) Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation – a meta-analysis. Plant Soil 374:523–537. https://doi.org/10.1007/s11104-013-1899-2
Leigh J, Fitter AH, Hodge A (2011) Growth and symbiotic effectiveness of an arbuscular mycorrhizal fungus in organic matter in competition with soil bacteria. FEMS Microbiol Ecol 76:428–438. https://doi.org/10.1111/j.1574-6941.2011.01066.x
Li ZY, Wang SY, Wang WN, Gu JC, Ding YY, Wang Y (2023) Contrasting responses of new pioneer and fibrous roots exposed to nitrogen deposition: a field study using three woody species. Plant Soil. https://doi.org/10.1007/s11104-023-06241
Lin XG, Feng YZ, Zhang HY, Chen RR, Wang JH, Zhang JB, Chu HY (2012) Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in North China Revealed by 454 Pyrosequencing. Environ Sci Technol 46:5764–5771. https://doi.org/10.1021/es3001695
Ma ZQ, Guo DL, Xu XL, Lu MZ, Bardgett RD, Eissenstat DM, McCormack ML, Hedin LO (2019) Evolutionary history resolves global organization of root functional trait. Nature 570:E25–E25. https://doi.org/10.1038/nature25783
Maherali H (2014) Is there an association between root architecture and mycorrhizal growth response? New Phytol 204:192–200. https://doi.org/10.1111/nph.12927
Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748. https://doi.org/10.1126/science.1143082
Miller RM, Kling M (2000) The importance of integration and scale in the arbuscular mycorrhizal symbiosis. Plant Soil 226:295–309. https://doi.org/10.1023/A:1026554608366
Miller M, McGonigle T, Addy H (1995) Functional ecology of vesicular arbuscular mycorrhizas as influenced by phosphate fertilization and tillage in an agricultural ecosystem. Crit Rev Biotechnol 15:241–255. https://doi.org/10.3109/07388559509147411
Nayyar H, Gupta D (2006) Differential sensitivity of C3 and C4 plants to water defificit stress: association with oxidative stress and antioxidants. Environ Exp Bot 58:106–113. https://doi.org/10.1016/j.envexpbot.2005.06.021
Nerva L, Giudice G, Quiroga G, Belfiore N, Lovat L, Perria R, Volpe MG, Moffa L, Sandrini M, Gaiotti F, Balestrini R, Chitarra W (2022) Mycorrhizal symbiosis balances rootstock-mediated growth-defence tradeoffs. Biol Fert Soils 58:17–34. https://doi.org/10.1007/s00374-021-01607-8
Parihar M, Rakshit A, Meena VS, Gupta VK, Rana K, Choudhary M, Tiwari G, Mishra PK, Pattanayak A, Bisht JK, Jatav SS, Khati P, Jatav HS (2020) The potential of arbuscular mycorrhizal fungi in C cycling: a review. Arch Microbiol 202:1581–1596. https://doi.org/10.1007/s00203-020-01915-x
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775. https://doi.org/10.1038/nrmicro1987
Pinto H, Sharwood RE, Tissue DT, Ghannoum O (2014) Photosynthesis of C3, C3–C4, and C4 grasses at glacial CO2. J Exp Bot 65:3669–3681. https://doi.org/10.1093/jxb/eru155
Reynolds HL, Hartley AE, Vogelsang KM, Bever JD, Schultz PA (2005) Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture. New Phytol 167:869–880
Rezácová V, Slavíková R, Zemková L, Konvalinková T, Procházková V, St’vícek V, Hrselová H, Beskid O, Hujslová M, Gryndlerová H, Gryndler M, Püschel D, Jansa J (2018) Mycorrhizal symbiosis induces plant carbon reallocation differently in C3 and C4 Panicum grasses. Plant Soil 425:441–456. https://doi.org/10.1007/s11104-018-3606-9
Rozek K, Rola K, Blaszkowski J, Leski T, Zubek S (2020) How do monocultures of fourteen forest tree species affect arbuscular mycorrhizal fungi abundance and species richness and composition in soil? Forest Ecol Manag 465:118091. https://doi.org/10.1016/j.foreco.2020.118091
Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kogel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56. https://doi.org/10.1038/nature10386
Schultz PA, Miller RM, Jastrow JD, Rivetta CV, Bever JD (2001) Evidence of a mycorrhizal mechanism for the adaptation of Andropogon gerardii (Poaceae) to high- and low-nutrient prairies. Am J Bot 88:1650–1656. https://doi.org/10.2307/3558410
Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and new genera. The Royal Botanic Garden Edinburgh, The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University, Gloucester, UK, pp. 56. Electronic version freely available online at: www.amf-phylogeny.com
See CR, Keller AB, Hobbie SE, Kennedy PG, Weber PK, Pett-Ridge J (2021) Hyphae move matter and microbes to mineral microsites: Integrating the hyphosphere into conceptual models of soil organic matter stabilization. Global Change Biol 28:2527–2540. https://doi.org/10.1111/gcb.16073
Sghir F, Chliyeh M, Touati J, Mouria B, Touhami AO, Filali-Maltouf A, El Modafar C, Moukhli A, Benkirane A, Douira A (2014) Effect of a dual inoculation with endomycorrhizae and Trichoderma harzianum on the growth of date palm seedlings. Int J Pure App Biosci 2:12–26
Shahbaz M, Sanaullah M, Kuzyakov Y, Heitkamp F, Blagodatskaya E (2016) Microbial residues accelerate decomposition of soil organic matter: new mechanism, actors and thresholds. Workshop “SOMmic – Microbial Contribution and Impact on Soil Organic Matter, Structure and Genesis“. Leipzig, Germany, November 9–11, 2016
Soti PG, Jayachandran K, Purcell M, Volin JC, Kitajima K (2014) Mycorrhizal symbiosis and Lygodium microphyllum Invasion in South Florida-a biogeographic comparison. Symbiosis 62:81–90. https://doi.org/10.1007/s13199-014-0272-4
Soudzilovskaia NA, Douma JC, Akhmetzhanova AA, van Bodegom PM, Cornwell WK, Moens EJ, Treseder KK, Tibbett M, Wang YP, Cornelissen JHC (2015) Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry. Global Ecol Biogeogr 24:371–382. https://doi.org/10.1111/geb.12272
Staddon PL, Ramsey CB, Ostle N, Ineson P, Fitter AH (2003) Rapid turnover of hyphae of mycorrhizal fungi determined by AMS microanalysis of 14C. Science 300:1138–1140. https://doi.org/10.1126/science.1084269
Stanton ML (2003) Interacting guilds: moving beyond the pairwise perspective on mutualisms. Am Nat 162:S10–S23. https://doi.org/10.1086/378646
Sullivan WM, Jiang ZC, Hull RJ (2000) Root morphology and its relationship with nitrate uptake in Kentucky bluegrass. Crop Sci 40:765–772. https://doi.org/10.2135/cropsci2000.403765x
Sun YF, Li YW, Lu XM, Wang Y, Bai YF (2022) Contrasting effects of arbuscular mycorrhizal fungi on nitrogen uptake in Leymus chinensis and Cleistogenes squarrosa grasses, dominants of the Inner Mongolian steppe. Plant Soil 475:395–410. https://doi.org/10.1007/s11104-022-05375-8
Taylor SH, Hulme SP, Rees M, Ripley BS, Woodward FI, Osborne CP (2010) Ecophysiological traits in C-3 and C-4 grasses: a phylogenetically controlled screening experiment. New Phytol 185:780–791. https://doi.org/10.1111/j.1469-8137.2009.03102.x
Tiunov AV, Scheu S (2005) Arbuscular mycorrhiza and Collembola interact in affecting community composition of saprotrophic microfungi. Oecologia 142:636–642. https://doi.org/10.1007/s00442-004-1758-1
Verbruggen E, Struyf E, Vicca S (2021) Can arbuscular mycorrhizal fungi speed up carbon sequestration by enhanced weathering? Plants People Planet 3:445–453. https://doi.org/10.1002/ppp3.10179
Wang FY (2017) Occurrence of arbuscular mycorrhizal fungi in mining-impacted sites and their contribution to ecological restoration: mechanisms and applications. Crit Rev Env Sci Tec 47:1901–1957. https://doi.org/10.1080/10643389.2017.1400853
Wang CL, Guo LY, Li YX, Wang Z (2012) Systematic comparison of C3 and C4 plants based on metabolic network analysis. BMC Syst Biol 6:S9. https://doi.org/10.1186/1752-0509-6-S2-S9
Wang F, Jiang RF, Kertesz MA, Zhang FS, Feng G (2013) Arbuscular mycorrhizal fungal hyphae mediating acidification can promote phytate mineralization in the hyphosphere of maize (Zea mays L.). Soil Biol Biochem 65:69–74. https://doi.org/10.1016/j.soilbio.2013.05.010
Wang F, Zhang L, Zhou JC, Rengel Z, George TS, Feng G (2022) Exploring the secrets of hyphosphere of arbuscular mycorrhizal fungi: processes and ecological functions. Plant Soil 481:1–22. https://doi.org/10.1007/s11104-022-05621-z
Wei YW, Yu DP, Lewis BJ, Zhou L, Zhou WM, Fang XM, Zhao W, Wu SN, Dai LM (2014) Forest carbon storage and tree carbon pool dynamics under natural forest protection program in northeastern China. Chinese Geogr Sci 24:397–405. https://doi.org/10.1007/s11769-014-0703-4
Wei LL, Vosátka M, Cai BP, Ding J, Lu CY, Xu JH, Yan WF, Li YH, Liu CX (2019) The role of arbuscular mycorrhiza fungi in the decomposition of fresh residue and soil organic carbon: a mini-review. Soil Sci Soc Am J 83:511–517. https://doi.org/10.2136/sssaj2018.05.0205
Wu SL, Fu W, Rillig MC, Chen BDD, Zhu YG, Huang LB (2023) Soil organic matter dynamics mediated by arbuscular mycorrhizal fungi - an updated conceptual framework. New Phytol. https://doi.org/10.1111/nph.19178
Xiao D, Che RX, Liu X, Tan YJ, Yang R, Zhang W, He XY, Xu ZH, Wang KL (2019) Arbuscular mycorrhizal fungi abundance was sensitive to nitrogen addition but diversity was sensitive to phosphorus addition in karst ecosystems. Biol Fert Soils 55:457–469. https://doi.org/10.1007/s00374-019-01362-x
Yang HS, Zhang Q, Dai YJ, Liu Q, Tang JJ, Bian XM, Chen X (2015) Effects of arbuscular mycorrhizal fungi on plant growth depend on root system: a meta-analysis. Plant Soil 389:361–374. https://doi.org/10.1007/s11104-014-2370-8
Yang HS, Zhang Q, Koide RT, Hoeksema JD, Tang JJ, Bian XM, Hu SJ, Chen X (2017) Taxonomic resolution is a determinant of biodiversity effects in arbuscular mycorrhizal fungal communities. J Ecol 105:219–228. https://doi.org/10.1111/1365-2745.12655
Zhang SP, Wang L, Wei W, Hu JJ, Mei SH, Zhao QY, Tsang YF (2018a) Enhanced roles of biochar and organic fertilizer in microalgae for soil carbon sink. Biodegradation 29:313–321. https://doi.org/10.1007/s10532-017-9790-0
Zhang L, Shi N, Fan J, Wang F, George TS, Feng G (2018b) Arbuscular mycorrhizal fungi stimulate organic phosphate mobilization associated with changing bacterial community structure under field conditions. Environ Microbiol 20:2639–2651. https://doi.org/10.1111/1462-2920.14289
Zhang Q, Li XY, Liu JJ, Liu JY, Han L, Wang X, Liu HY, Xu MP, Yang GH, Ren CJ, Han XH (2023) The contribution of microbial necromass carbon to soil organic carbon in soil aggregates. Appl Soil Ecol 190:104985. https://doi.org/10.1016/j.apsoil.2023.104985
Zhu YG, Miller RM (2003) Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems. Trends in Plant Sci 8:407–409. https://doi.org/10.1016/S1360-1385(03)00184-5
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Tao, J., Liu, X. Does arbuscular mycorrhizal fungi inoculation influence soil carbon sequestration?. Biol Fertil Soils 60, 213–225 (2024). https://doi.org/10.1007/s00374-024-01793-1
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DOI: https://doi.org/10.1007/s00374-024-01793-1