Indigenous microorganisms offset the benefits of growth and nutrition regulated by inoculated arbuscular mycorrhizal fungi for four pioneer herbs in karst soil

Yan Sun; Muhammud Umer; Pan Wu; Yun Guo; Wenda Ren; Xu Han; Qing Li; Bangli Wu; Kaiping Shen; Tingting Xia; Lipeng Zang; Shixiong Wang; Yuejun He

doi:10.1371/journal.pone.0266526

Abstract

Arbuscular mycorrhizal (AM) fungi, as beneficial soil microorganisms, inevitably interact with indigenous microorganisms, regulating plant growth and nutrient utilization in natural habitats. However, how indigenous microorganisms affect the benefits of growth and nutrition regulated by inoculated AM fungi for plants in karst ecosystem habitats remains unclear today. In this experiment, the Gramineae species Setaria viridis vs. Arthraxon hispidus and the Compositae species Bidens pilosa vs. Bidens tripartita exist in the initial succession stage of the karst ecosystem. These plant species were planted into different soil microbial conditions, including AM fungi soil (AMF), AM fungi interacting with indigenous microorganisms soil (AMI), and a control soil without AM fungi and indigenous microorganisms (CK). The plant biomass, nitrogen (N), and phosphorus (P) were measured; the effect size of different treatments on these variables of plant biomass and N and P were simultaneously calculated to assess plant responses. The results showed that AMF treatment differently enhanced plant biomass accumulation, N, and P absorption in all species but reduced the N/P ratio. The AMI treatment also significantly increased plant biomass, N and P, except for the S. viridis seedlings. However, regarding the effect size, the AM fungi effect on plant growth and nutrition was greater than the interactive effect of AM fungi with indigenous microorganisms. It indicates that the indigenous microorganisms offset the AM benefits for the host plant. In conclusion, we suggest that the indigenous microorganisms offset the benefits of inoculated AM fungi in biomass and nutrient accumulation for pioneer plants in the karst habitat.

Citation: Sun Y, Umer M, Wu P, Guo Y, Ren W, Han X, et al. (2022) Indigenous microorganisms offset the benefits of growth and nutrition regulated by inoculated arbuscular mycorrhizal fungi for four pioneer herbs in karst soil. PLoS ONE 17(4): e0266526. https://doi.org/10.1371/journal.pone.0266526

Editor: Jian Liu, Shandong University, CHINA

Received: December 28, 2021; Accepted: March 22, 2022; Published: April 25, 2022

Copyright: © 2022 Sun et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript.

Funding: This research was funded by the National Natural Science Foundation of China (NSFC: 31660156; 31360106), the Science and Technology Project of Guizhou Province ([2021] General-455; [2016] Supporting-2805), the Guizhou Hundred-level Innovative Talents Project (Qian-ke-he platform talents [2020] 6004), the First-class Disciplines Program on Ecology of Guizhou Province (GNYL[2017]007), the Talent-platform Program of Guizhou Province ([2017]5788; [2018]5781), The Basic Research Program in Guizhou Province ([2019]1060). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: NO. The authors have declared that no competing interests exist.

Introduction

Karst ecosystem occupies approximately 7~12% of emerged land globally, mainly distributed in southwest China, and is characterized by high habitat heterogeneity and high vegetation fragmentation [1] with high soil erosion, rocky desertification, and barren vegetation nutrient deficiency [2–7]. However, the karst vegetation retains a robust natural resilience even in harsh habitats [8, 9]. Initially, the pioneer herbaceous plants, mainly from Gramineae and Compositae, have high resistance to drought and barrenness, grow fast, and improve soil structure [10] in the primary succession stage ecosystem restoration [11, 12]. In addition, soil microorganisms play an essential role in recovering degraded karst systems [13] through promoting the growth and nutrient uptake by plants [14, 15] as well as increasing soil nutrient bioavailability [16]. Thus, soil microorganisms in karst vegetation restoration cannot be ignored.

AM fungi, a soil functional microorganism, can play critical roles in recovering degraded terrestrial ecosystems [17]. AM fungi formed a symbiotic relationship with 80% of terrestrial plants [18, 19], improve plant growth, nutrient accumulation [20, 21], enhance drought stress tolerance [22] and maintain soil structure [23], e.g. Guo et al. (2021) [24] proposed that AM fungi differently affected the competitive ability of Broussonetia papyrifera and Carpinus pubescens; Xia et al. (2020) [25] also showed that AM fungi increased nutrients of host plants by regulating the morphological development of karst plant roots. In addition, Shi et al. (2015) [26] illustrated that AM fungi increased the biomass, N, and P content in shoots and roots of plants. Furthermore, AM fungi mycelium can transfer the photosynthetic carbohydrates from the host plants to the soil, which recruits soil microorganisms [27]. However, we know relatively little about how regulation of plant growth and nutrient by AM fungi is affected by interaction with indigenous microorganisms.

AM fungi via extensive extraradical hyphae interacting with indigenous microbial communities play crucial roles in plant growth in natural habitats [28, 29]. AM fungi and bacteria are ubiquitous in natural soil [30]. Specifically, AM fungi regulate plant growth, and they are positively affected by cooperating with indigenous microorganisms [31, 32] or negatively affected by competing with indigenous microorganisms [33, 34]. Ortiz et al. (2015) [31] suggested that the combination of AM fungi and specific bacteria could promote plant growth by minimizing drought-related stress effects. Artursson et al. (2006) [35] also proposed that the co-inoculation of AM fungi and phosphorus-solubilizing bacteria positively promotes plant nutrient absorption. In addition, plant growth-promoting rhizobacteria could promote mycorrhizal fungal activity and establishment [36–38], which are called mycorrhiza helper bacteria [39]. In contrast, the competition phenomenon between AM fungi and bacteria was also widely reported [40]. Azcón-Aguilar et al. (1997) [41] presented evidence of direct competition between AM fungi and indigenous microorganisms for photosynthetic products of the host plant. Indirectly, Doumbou et al. (2005) [42] proposed that many Streptomyces sp. could exude antifungal compounds, which indicated that they are fungal competitors under the appropriate environmental conditions. Thus, the cooperation and competition between AM fungi and indigenous microorganisms are ineluctability in karst soil.

In summary, AM fungi play important roles in improving plant growth and nutrient absorption. However, AM fungi inevitably interact with indigenous microorganisms in the vegetation restoration of the karst-degraded ecosystem. It remains unclear how indigenous microorganisms affect the benefits of growth and nutrition regulated by AM fungi for plants in karst soils. Because of the complexity and uncertainty of the interaction between AM fungi with indigenous microorganisms, it is necessary to assess the effect size of AM fungi and indigenous microorganisms, and their interaction, on plant growth and nutrition. The aim is to clarify how indigenous microorganisms affect the benefits of growth and nutrition regulated by AM fungi for plants in karst soils. We hypothesize that: (1) AM fungi can promote the growth and nutrients of karst plants (H1), according to that AM fungi increased plant biomass and nutrition accumulation [20, 26]. (2) Indigenous microorganisms can offset the benefits from AM fungi on plant growth and nutrient accumulation (H2), according to that indigenous microorganisms may negatively affect the AM benefits for the host plant through competition [33, 34, 41–43].

Materials and methods

Experiment treatments

A potting experiment was conducted by using four herb species: Setaria viridis, Arthraxon hispidus, Bidens pilosa, and Bidens tripartita in polypropylene plastic pots in a greenhouse of Guizhou University in Guiyang, China (E: 106°22′ E; N: 29°49′ N; 1,120 m above the sea level). Three different microbial conditions soil was created to explore the interaction of AM fungi with indigenous microorganisms in the regulation of plant growth and nutrient utilization. It included AM fungi inoculating into sterilized soil (AMF treatment), AM fungi inoculating into natural conditions soil containing indigenous microorganisms (AMI treatment), and the control soil by removing microorganisms with sterilization (CK treatment). In the beginning, limestone soil (Calcaric regosols, FAO) [44] was collected from a typical karst habitat, from which approximately two-thirds of the soil was used for sterilization at 126°C, 0.14 Mpa for one hour to eliminate microbes, and one-third of the soil was retained for further experiments. Subsequently, a 2.5 kg soil subsample of the sterilized or unsterilized soil was put into each polypropylene plastic pot (180 mm × 160 mm, diameter × height). Five seeds of Setaria viridis, Arthraxon hispidus, Bidens pilosa, and Bidens tripartita were disinfected with a 10% H₂O₂ solution for 10 minutes and repeatedly washed with sterile water, and sown in each pot. After sowing seeds in each pot, seeds were covered with 200 g of the respective soil for promoting seed germination. In addition, the sterilized soil was inoculated with 10 g Glomus mosseae inoculum as the AMF treatment, and the original soil from field habitat was inoculated with 10 g Glomus mosseae inoculum as the AMI treatment, indicating the AM fungi interacting with the indigenous microorganisms in this experiment. Especially, CK treatment received an additional 10ml of the filtrate by weighing 10g of Glomus mosseae inoculum with sterile water using a double-layer filter paper, along with a 10 g of sterilized inoculum of Glomus mosseae was added in order to maintain the consistency of microflora except for the targeted fungus Glomus mosseae corresponding to AMF treatment. The inoculum propagated for four months with Trifolium repens, including approximately 100 spores per gram soil, hyphae, and colonized root pieces. There is mutual control between two of three treatments: the AM fungi effect through comparing AMF with CK treatment; the interactive effect of AM fungi with indigenous microorganisms through comparing AMI and CK treatment; and the indigenous microorganisms effect related to AM fungi through comparing AMI with AMF treatment. Of course, we had to admit that the unsterilized soil probably had native AM fungi under AMI treatment, even the targeted species Glomus mosseae. However, it was sure that the Glomus mosseae inoculum interacted with native AMF species and indigenous microorganisms; further, they jointly affected plants and soil for growth and nutrition when comparing AMI with AMF. All treatments were replicated five times, and four plant species contained 60 pots.

The physicochemical properties of limestone soil (per kg) were measured by the methods from Tan (2005) [45], the PH 8.2, total nitrogen (TN) 0.622 g, alkaline hydrolysis nitrogen (AN) 0.315 g, total phosphorus (TP) 1.274 g, available phosphorus (AP) 0.163 g, total potassium (TK) 37.79 g, and available potassium (AK) 0.532 g. All plant seeds were also collected from the same karst habitat used to collect soil. According to the primary field survey, these plants are successive pioneer species of karst communities as the herbaceous stage, which generally coexist in the same habitat as the main Gramineae and Compositae. Three weeks after seeds germination, only two seedlings were retained in the pot and cultured for five months. All growing seedlings were watered one time per day for maintaining field capacity, then harvested to determine the biomass, N, and P concentrations. The Glomus mosseae inoculum was initially purchased from the Institute of Nutrition Resources, Beijing Academy of Agricultural and Forestry Sciences (NO.BGA0046).

Determinations of the root mycorrhizal colonization, biomass, and the accumulation of nitrogen and phosphorus

The grid line-intersect method determined the root mycorrhizal colonization rate [46]. The biomass of S. viridis, A. hispidus, B. pilosa, and B. tripartita were respectively determined by weighing tissue of root, stem, and leaves after drying at 80°C to constant weight. The nitrogen and phosphorus concentrations in plant tissue were determined by the traditional Kjeldahl method and the Molybdenum-antimony anti-colorimetric method, respectively [47]. Additionally, the accumulations of nitrogen and phosphorus were calculated through nutrient concentration multiplying by biomass, respectively. Then the nutrient accumulation of plant individuals was accumulated by root, stem, and leaf.

Calculation of effect size

The effect size was calculated using the response ratio (lnR) of treatment groups to the control groups plant biomass referred from the proposition of [48] regarding the plant response mycorrhizal fungi. The AM fungi effect (AME) by AMF vs. CK, the interactive effect of AM fungi with indigenous microorganisms (AIE) by AMI vs. CK, and the indigenous microorganisms effect related to AM fungi (IME) by AMI vs. AMF were calculated respectively, due to the mutual control between two of three treatments in this experiment. Therefore, the modified method was adopted according to Hoeksema et al. (2010) [48] and Hedges et al. (1999) [49] as follows: Where Xt and Xc represent the biomass or nutrient accumulation of the plant in the values of the treatment group and control group, respectively, values> 0 indicate positive effects promoting plant growth or nutrient accumulation, values < 0 indicate negative effects suppressing plant growth or nutrient accumulation.

Statistical analyses

All of the statistical analyses were performed through SPSS 25.0 software. All of the data were tested for normality and homogeneity of variance before analysis. Two-way ANOVA was applied for assessing the effects of plant species (Ps; Setaria viridis vs. Arthraxon hispidus vs. Bidens pilosa vs. Bidens tripartita), soil microbial treatments (Ms; AMI vs. AMF vs. CK), and their interactions (Ms×Ps) on plant biomass, nitrogen accumulation, and phosphorus accumulation, N/P ratio and effect size by the lnR. The least significant difference (LSD) test was applied to compare significant differences in root mycorrhizal colonization, biomass, nitrogen, and phosphorus accumulations, and N/P ratio with effect size by the lnR among the three different conditions of soil microbial treatments with AMI, AMF, and CK or four plant species of Setaria viridis and Arthraxon hispidus and Bidens pilosa and Bidens tripartita at P≤0.05. All graphs were drawn on Origin 2018.

Results

Root mycorrhizal colonization of four plant species under different microbial treatments

A non-significant AMI > AMF of root mycorrhizal colonization was observed in the four species. However, the root mycorrhizal colonization of CK treatment was zero; meanwhile, the AM fungus spore and mycelium were not discovered under CK soil substrate via microscopic detection (Table 1). The root mycorrhizal colonization of B. pilosa and B. tripartita were significantly greater than that of A. hispidus and S. viridis, respectively, while for A. hispidus, it was also greater than S. viridis. Besides, there was no significant difference in root mycorrhizal colonization of B. pilosa and B. tripartita under AMI and AMF treatments (Table 1). These results indicate root mycorrhizal colonization is species differences, and it provides evidence for host preferences of AM fungal.

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Table 1. The mycorrhizal colonization rates of Setaria viridis, Arthraxon hispidus, Bidens pilosa, and Bidens tripartite.

https://doi.org/10.1371/journal.pone.0266526.t001

Biomass and its response ratio of four plant species under different microbial treatments

The soil microbial condition treatments (Ms) significantly affected biomass (Table 2). Significantly AMF > AMI > CK of biomass were observed in A. hispidus, B. pilosa, and B. tripartita seedlings except for S. viridis. Plant biomass was increased by AM fungus when comparing AMF with CK and AMI with CK, respectively. However, the plant biomass under AMI was significantly lower than under AMF (Fig 1A). The plant species (Ps) also significantly affected individual biomass (Table 2). Under AMF and CK treatments, the biomass of A. hispidus was significantly greater than the other three species. The biomass of S. viridis was significantly lower than the other three species under AMF and AMI treatments. In addition, there was a non-significant difference in biomass observed between B. pilosa and B. tripartita seedlings under any soil microbial condition treatments (Fig 1A). Meanwhile, the interaction of Ms×Ps significantly affected the individual biomass for the four species (Table 2). The results revealed that AMF and AMI treatments significantly increased the biomass accumulation of four karst pioneer species. Meanwhile, the biomass was significantly different between A. hispidus and S.viridis of Gramineae, except for B. pilosa and B. tripartita under AMF.

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Fig 1.

The biomass (A) and its response ratio lnR_Biomass (B) of four plant species through the different microbial treatments. Abbreviations: S. v = Setaria viridis; A. h = Arthraxon hispidus; B. p = Bidens pilosa; B. t = Bidens tripartita; AMF = the mycorrhizal fungi soil by AM fungi inoculation; AMI = the combining soil by AM fungi with indigenous microorganism; CK = the sterilized soil as the control by removing microorganism; AME = AM fungi effect; AIE = interactive effect related to AM fungi interacting with indigenous microbes; IME = indigenous microbial effect related to AM fungi. The different lowercase letters (a, b, c, d) indicate significant differences between species under AMF, AMI, and CK treatments, respectively. The different lowercase letters (x, y, z) indicate significant differences between AMF, AMI, and CK treatments for the same species (P < 0.05).

https://doi.org/10.1371/journal.pone.0266526.g001

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Table 2. Two-way ANOVAs for the effects of plant species (S. viridis vs. A. hispidus vs. B. pilosa vs. B. tripartita) and soil microbial condition (AMF vs. AMI vs. CK) on the biomass, the N accumulation, and their response ratio (lnR).

https://doi.org/10.1371/journal.pone.0266526.t002

Similarly, the soil microbial condition treatments (Ms), the plant species (Ps), and their interaction significantly affected the response ratio of biomass (lnR_Biomass) (Table 2). On the one hand, a positive effect (lnR_Biomass > 0) of biomass was observed in the four species under AME and AIE conditions except for S. viridis in AIE (Fig 1B). However, a significant AME > AIE was observed in lnR_Biomass, indicating that AM fungus was beneficial for plant biomass, but the positive effect was decreased when AM fungi interacted with indigenous microorganisms. On the other hand, a negative effect (lnR_Biomass < 0) was shown in the IME condition (Fig 1B), indicating that indigenous microorganisms offset the AM fungi promotion in plant growth. Precisely, the results indicated that AM fungi significantly increased the biomass accumulation of four karst pioneer species; however, the lnR_Biomass reduction by comparing AIE to AME specified that the indigenous microorganisms offset the benefits of inoculated AM fungi in promoting plant biomass.

Nitrogen accumulation and its response ratio of four plant species under different microbial treatments

The soil microbial condition treatments (Ms) significantly affected N accumulation (Table 2). Significantly AMF > AMI > CK of N accumulation were shown in A. hispidus, B. pilosa, and B. tripartita seedlings, except for S. viridis. Specifically, the N accumulation was enhanced by AM fungus when comparing AMF with CK and AMI with CK, respectively. At the same time, N accumulation under AMI was significantly lower than under AMF (Fig 2A). The plant species (Ps) also significantly affected N accumulation (Table 2). Under AMF and AMI treatments, N accumulation in S. viridis was significantly lower than other three species. For CK treatment, N accumulation in A. hispidus was significantly greater than the other three species. Moreover, there was a non-significant difference in N accumulation between B. pilosa and B. tripartita seedlings under any soil microbial condition treatments (Fig 2A). Furthermore, the interaction of Ms×Ps significantly affected the N accumulation for the four species (Table 2). These results showed that AMF and AMI treatments significantly increased the N accumulation of four karst pioneer species. Meanwhile, N accumulation was significantly different between A. hispidus and S. viridis, but not for B. pilosa and B. tripartita under AMF.

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Fig 2.

N accumulation (A) and response ratio lnR_N (B) of four plant species through the different microbial treatments. The meanings of abbreviations (S. v, A. h, B. p and B. t; AMF, AMI, and CK; AME, AIE and IME) and the lowercase letters (a, b, c, d; x, y, z) are the same as in Fig 1.

https://doi.org/10.1371/journal.pone.0266526.g002

Similarly, the soil microbial condition treatments (Ms), the plant species (Ps), and their interaction significantly affected the response ratio of N (lnR_N) (Table 2). One side has a positive effect (lnR_N > 0) of N was observed in four species under AME and AIE conditions except for S. viridis in AIE (Fig 2B). However, a significant AME > AIE was observed in lnR_N, indicating that AM fungus was beneficial for plant N accumulation, but the positive effect was decreased when AM fungi interacted with indigenous microorganisms. Another side has a negative effect (lnR_N < 0) obtainable in the IME condition (Fig 2B), indicating that indigenous microorganisms offset the AM fungi promotion in N accumulation. Overall, the results indicated that AM fungi significantly increased the N accumulation of four karst pioneer species; however, the lnR_N reduction by comparing AIE to AME specified that the indigenous microorganisms offset the benefits of inoculated AM fungi in promoting N accumulation.

Phosphorous accumulation and its response ratio of four plant species under different microbial treatments

The soil microbial condition treatments (Ms) significantly affected P accumulation (Table 3). Significantly AMF > AMI > CK of P accumulation was admissible in four species. Unambiguously, AM fungus enhanced P accumulation when comparing AMF with CK and AMI with CK; but the P accumulation under AMI was significantly lower than under AMF (Fig 3A). The plant species (Ps) also significantly affected P accumulation (Table 3). Under AMF and AMI treatments, the P accumulation in S. viridis was significantly lower than other three species. For CK treatments, the P accumulation of A. hispidus was significantly greater than the other three species. In addition, there was no significant difference in P accumulation between B. pilosa and B. tripartita seedlings under any microbial condition soil treatments (Fig 3A). Meanwhile, the interaction of Ms×Ps significantly affected the P accumulation for four species (Table 3). It shows that AMF and AMI treatments significantly increased the P accumulation of four karst pioneer species. Meanwhile, P accumulation was significantly different between A. hispidus and S. viridis of Gramineae, except for B. pilosa and B. tripartita of Compositae under AMF.

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Fig 3.

P accumulation (A) and response ratio lnR_P (B) of four plant species through the different microbial treatments. The meanings of abbreviations (S. v, A. h, B. p and B. t; AMF, AMI, and CK; AME, AIE and IME) and the lowercase letters (a, b, c, d; x, y, z) are the same as in Fig 1.

https://doi.org/10.1371/journal.pone.0266526.g003

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Table 3. Two-way ANOVAs for the effects of plant species (S. viridis vs. A. hispidus vs. B. pilosa vs. B. tripartita) and soil microbial condition (AMF vs. AMI vs. CK) on the P accumulation, the N/P ratio, and their response ratio (lnR).

https://doi.org/10.1371/journal.pone.0266526.t003

Likewise, the soil microbial condition treatments (Ms), the plant species (Ps), and their interaction significantly affected the response ratio of P (lnR_P) (Table 3). Alternatively, it has a positive effect (lnR_P > 0) of P on four species under AME and AIE conditions. However, a significant AME > AIE was observed in lnR_P, indicating that AM fungus was beneficial for plant P accumulation, but the positive effect was decreased when AM fungi interacted with indigenous microorganisms (Fig 3B). It also has a negative effect (lnR_P < 0) in the IME condition and depicts that the indigenous microorganisms offset the AM fungi promotion in P accumulation. Therefore, the results consolidated that AM fungi significantly increased P accumulation of four karst pioneer species, then the lnR_P reduction by comparing AIE to AME designated that the indigenous microorganisms offset the benefits of inoculated AM fungi in promoting P accumulation.

N/P ratio and its response ratio of four plant species under different microbial treatments

The soil microbial condition treatments (Ms) significantly affected the N/P ratio (Table 3), significantly greater N/P ratio between plant species ranked as the CK > AMF ≈ AMI for S. viridis, the AMI > CK ≈ AMF for A. hispidus, the AMI > AMF > CK for B. Pilosa, and CK ≈AMI > AMF for B. tripartita (Fig 4A). The plant species (Ps) also significantly affected the N/P ratio (Table 3), and the N/P ratio for four plants showed species differences under different soil microbial treatments. Explicitly, there was a non-significant difference in the N/P ratio of the four species under AMF treatments. Under AMI treatments, the N/P ratio of A. hispidus and B. tripartita were significantly greater than S. viridis and B. pilosa, respectively. In the interim, the N/P ratio of the B. pilosa was greater than S. viridis seedlings. Under CK treatment, the N/P ratio of B. tripartita was significantly greater than the other three species, while the N/P ratio of B. pilosa was significantly lower than the other three species (Fig 4A). Likewise, the interaction of Ms×Ps significantly affected the N/P ratio for four species (Table 3). Therefore, AM fungi significantly reduced the N/P ratio of four species. Equally, the soil microbial condition treatments (Ms), the plant species (Ps), and their interaction significantly affected the response ratio of N/P (lnR_N/P) (Table 3, Fig 4B). Overall, AM fungi significantly reduced the N/P ratio for the four-karst pioneer species, portraying that the AM fungi alleviate P limitation and promote plant growth in karst areas with low P.

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Fig 4.

N/P ratio (A) and response ratio lnR_N/P (B) of four plant species through the different microbial treatments. The meanings of abbreviations (S. v, A. h, B. p and B. t; AMF, AMI, and CK; AME, AIE and IME) and the lowercase letters (a, b, c, d; x, y, z) are the same as in Fig 1.

https://doi.org/10.1371/journal.pone.0266526.g004

Discussion

AM fungi differently regulated the plant growth and nutrient accumulation

AM fungi significantly increased biomass and N and P accumulation for the four karst pioneer species (Figs 1A, 2A and 3A). Consistently, the positive influence of AM fungi inoculation on host plant growth and nutrient accumulation was also observed in some previous studies [50, 51]. For instance, He et al. (2017) [20] showed that AM fungi enhanced plant growth and nutrient absorption of B. papyrifera and B. pilosa in karst soil, which is consistent with our results that AM fungi significantly increased biomass and accumulation of N and P for the four plants. There are two main mechanisms that AM fungi promote plant growth and nutrient accumulation. One side is that AM fungi can extend the absorbing network beyond the rhizosphere nutrient depletion region and absorb a larger amount of soil mineral nutrients, thereby improving the ability of plants to obtain nutrients [52] and ultimately benefit plant growth [53–55]. Another is that AM fungi can secrete organic acids and soil enzymes to dissolve the insoluble nutrients and mineralize the organic nutrient [56–58], thereby promoting the availability of soil nutrients [59]. Elbon and Whalen (2014) [60] illustrated that AM fungi could increase the plant-available P concentration by secreting organic acids and phosphatase enzymes. Therefore, AM fungi facilitated the growth and nutrient accumulation of four karst pioneer plants, which can verify the hypothesis of H1. However, the specific mechanism of AM fungi affecting nutrient accumulation of karst pioneer species needs to be explored further.

The N/P ratio can predict plant nutrient restrictions [61]. A low N/P ratio (< 14) indicates N limitation, whereas a high N/P ratio (> 16) indicates P limitation, and both N and P limit plant growth when the N/P ratio is between 14 and 16 [62]. In our experiment, the N/P ratio of all species was greater than 16 under AMI and CK treatments, except for S. viridis under AMI and B. pilosa under CK, showing that plant growth was mainly limited by phosphorus in karst soil. However, the N/P ratio of the four species significantly decreased under AMF treatments compared with AMI and CK treatments for a whole (Fig 4A). AM fungi reduced the N/P ratio of seedlings, representing that AM fungus is more effective in assisting plants in obtaining P than N by alleviating P limitation. These results were similar to those of Shen et al. (2020) [63], who suggested that AM fungi alleviated the P limitation of plants via the mycorrhizal network in low-P karst soils. Consequently, the AM fungi play a vital role in alleviating the nutritional restriction of nutrient-deficient karst soils.

AM fungi enhanced four plants’ biomass, N, and P accumulation differently. Meanwhile, the A. hispidus, B. pilosa, and B. tripartita obtained greater benefits than the S. viridis (Figs 1A, 2A and 3A), demonstrating that the promotion effect of AM fungi on plants was different by host type. Besides, the mycorrhizal colonization of A. hispidus, B. pilosa, and B. tripartita was significantly higher than S. viridis (Table 1). It was well proof of the different roles of AM fungi on different species, and these differences reflected that AM fungi had the selectivity for host plants. AM fungi showed host-specific growth response [64] and induced differential growth responses in host plant species [65]. It was similar to the research conducted by Liu et al. (2003) [66], who proposed that Nicotiana tabacum was a more favorable host plant for Glomus constrictum and Glomus multicaule to the other hosts. Therefore, AM fungi are crucial for plant growth and nutrient utilization. However, the mutual selection between AM fungi and host plants cannot be ignored, and thus the specific mechanism of selective plant-AMF combinations of karst pioneer species needs to be explored in further study.

Indigenous microorganisms affected the benefits of AM fungi on plant growth and nutrient accumulation

In this experiment, the positive AM fungi effect on plant growth and nutrition was greater than the interactive effect related to AM fungi interacting with indigenous microorganisms for a whole (Figs 1B, 2B and 3B). It seems to imply that the indigenous microorganisms offset the benefits of AM fungi on plant growth and nutrient accumulation, signifying a negative relationship between AM fungi and indigenous microorganisms. Previous studies have demonstrated that AM fungi interact with a wide variety of indigenous microorganisms [67, 68]. Meanwhile, AM fungi regulated plant growth positively affected by cooperating with indigenous microorganisms [32] or negatively affected by competing with indigenous microorganisms [34], which depended on the species of indigenous microorganisms that interact with AM fungi [69–71]. Positively, Mortimer et al. (2012) [72] presented a synergistic relationship between AM fungi and nitrogen-fixing bacteria showing additive benefits for the growth and nutrient accumulation in the Acacia cyclops. Artursson et al. (2006) [35] illustrated that the plant growth-promoting rhizobacteria (PGPR) could enhance the activity of AM during a symbiotic relationship with the host plant. It is because of the stimulatory effects of PGPR on AM growth [73]. Negatively, AM fungi can compete with indigenous microorganisms to produce different effects on plant growth [74]. Some bacteria in the rhizosphere would compete for resources with AM fungi or inhibit the activity of AM fungi, thereby affecting plant growth [75]. It is because indigenous microorganisms have great advantages in colonizing plant roots due to their priority in resources and allocating root space of the host plants compared with colonizers [76, 77]. In addition, Dąbrowska et al. (2014) [78] presented that inoculation AM fungi promoted the growth of plants, but interactive effects of AM fungi with indigenous microorganisms inhibited plant growth. It was similar to our study that AM fungi positively affected plant growth and nutrient accumulation; however, indigenous microorganisms reduced this effect, indicating a negative relationship between AM fungi and indigenous microorganisms. It is possibly caused by the competition between AM fungi and indigenous microorganisms, mainly two sides. One side is interference competition, meaning that some microbes directly inhibit the function of AM fungi via exuding allelochemical substances [79] and bacterial antibiotics [80, 81]. For example, Doumbou et al. (2005) [42] proposed that numerous Streptomyces sp. could exude antifungal compounds, thereby inhibiting the function of AM fungi under certain environmental conditions. The other side is resources, and ecological niches competition, which was proposed by Leigh et al. (2011) [43] who suggested that resource competition for decomposition products between AM fungi and bacteria, resulting in an antagonistic relationship between them. Niwa et al. (2018) [76] suggested that the fungus inoculum mainly competed with the indigenous fungi, probably because their life-history strategy was identical to the inoculum fungus. All the above-mentioned can explain why the indigenous microorganisms relieved the benefits of AM fungi on plant growth and nutrient accumulation. It was consistent with Biró et al. (2000) [82], who found the indigenous microflora greatly reduced the functioning of the functioning of the mycorrhizal inoculum. Collectively, indigenous microorganisms offset the benefits of AM fungi in this study, which illustrated the interactions between AM fungi and indigenous microorganisms in karst areas should be mainly a negative relationship, it verified the hypothesis of H2 that indigenous microorganisms offset the benefits of AM fungi on plant growth and nutrient accumulation. However, the specific mechanisms of the negative relationship between specific microorganisms and AM fungi in karst soil remain to be further studied.

Conclusions

In this experiment, AM fungi significantly enhanced the biomass, N, and P accumulation for the four species but reduced the N/P ratio partly. AM fungi interacting with indigenous microorganisms increased plant biomass, N, and P accumulation, except for S. viridis seedlings. However, the benefits from interaction were lower than benefits from AM, indicating that the indigenous microorganisms offset the benefits of AM fungi for host plants. In conclusion, we suggest that the indigenous microorganisms offset the benefits of growth and nutrition regulated by inoculated AM fungi for pioneer plants in karst soil. Finally, it is necessary to understand the interactions of AM fungi with indigenous microbial communities to better apply mycorrhizal technology to the degraded ecosystem in karst areas.

Acknowledgments

We thank Xinyang Xu, Lu Gao, Li Wang, Xiaorun Hu and Jingting Li for helping in this experiment. We are grateful to the Institute of Nutrition Resources, Beijing Academy of Agricultural and Forestry Sciences for providing Glomus mosseae (NO. BGA0046) for use in our experiments.

References

1. Nie YP, Chen HS, Wang KL, and Ding YL. Rooting characteristics of two widely distributed woody plant species growing in different karst habitats of southwest China. Plant Ecol. 2014;215(10):1099–1109. https://doi.org/10.1007/s11258-014-0369-0.
- View Article
- Google Scholar
2. Liu Y, Liu C, Rubinato M, Guo K, Zhou J, and Cui M. An Assessment of Soil’s Nutrient Deficiencies and Their Influence on the Restoration of Degraded Karst Vegetation in Southwest China. Forests. 2020;11(8):797. https://doi.org/10.3390/f11080797.
- View Article
- Google Scholar
3. Peng T and Wang SJ. Effects of land use, land cover and rainfall regimes on the surface runoff and soil loss on karst slopes in southwest China. Catena. 2012;90(1):53–62. https://doi.org/10.1016/j.catena.2011.11.001.
- View Article
- Google Scholar
4. Jiang Z, Lian Y, and Qin X. Rocky desertification in Southwest China: Impacts, causes, and restoration. Earth-Sci. Rev. 2014;132:1–12. https://doi.org/10.1016/j.earscirev.2014.01.005.
- View Article
- Google Scholar
5. Green SM, Dungait JAJ, Tu C, Buss HL, Sanderson N, Hawkes SJ, et al. Soil functions and ecosystem services research in the Chinese karst Critical Zone. Chem. Geol. 2019;527. https://doi.org/10.1016/j.chemgeo.2019.03.018.
- View Article
- Google Scholar
6. Yang H, Zang Y, Yuan Y, Tang J, and Chen X. Selectivity by host plants affects the distribution of arbuscular mycorrhizal fungi: evidence from ITS rDNA sequence metadata. BMC Evol. Biol. 2012;12(1):1–13. https://doi.org/10.1186/1471-2148-12-50 pmid:22498355
- View Article
- PubMed/NCBI
- Google Scholar
7. Hartmann A, Goldscheider N, Wagener T, Lange J, and Weiler M. Karst water resources in a changing world: Review of hydrological modeling approaches. Rev. Geophys. 2014;52(3):218–242. https://doi.org/10.1002/2013rg000443.
- View Article
- Google Scholar
8. Zeng F, Peng W, Song T, Wang K, Wu H, Song X, et al. Changes in vegetation after 22 years’ natural restoration in the Karst disturbed area in northwestern Guangxi, China. Acta Ecol. Sin. 2007;27(12):5110–5119. https://doi.org/10.1016/s1872-2032(08)60016-5.
- View Article
- Google Scholar
9. Pang D, Cao J, Dan X, Guan Y, Peng X, Cui M, et al. Recovery approach affects soil quality in fragile karst ecosystems of southwest China: Implications for vegetation restoration. Ecol. Eng. 2018;123:151–160. https://doi.org/10.1016/j.ecoleng.2018.09.001.
- View Article
- Google Scholar
10. Long ZF, Tang CB, and Yang YC. Discussion on the effect of herbage in the comprehensive administration and the sustainable development in the karst area. Guizhou Agricultural Sciences. 2005;33(Z1):69–71.
- View Article
- Google Scholar
11. Cao J, Yuan D, Tong L, Azim M, Yang H, and Huang F. An overview of karst ecosystem in Southwest China: current state and future management. J. Res. Ecol. 2015;6(4):247–256. https://doi.org/10.5814/j.issn.1674-764x.2015.04.008.
- View Article
- Google Scholar
12. Anding L. The Composition and Structural Feature of Plant Community in Different Karst Stony Desertification Areas. Appl. Ecol. Environ. Res. 2017;15(4):1167–1183. https://doi.org/10.15666/aeer/1504_11671183.
- View Article
- Google Scholar
13. Chen X, Su Y, He X, Wei Y, Wei W, and Wu J. Soil bacterial community composition and diversity respond to cultivation in Karst ecosystems. World J. Microbiol. Biotechnol. 2012;28(1):205–13. https://doi.org/10.1007/s11274-011-0809-0 pmid:22806796
- View Article
- PubMed/NCBI
- Google Scholar
14. Richardson AE and Simpson RJ. Soil Microorganisms Mediating Phosphorus Availability. Plant Physiol. 2011;156(3):989–996. https://doi.org/10.2307/41435012 pmid:21606316
- View Article
- PubMed/NCBI
- Google Scholar
15. Wang X, Yan B, Fan B, Shi L, and Liu G. Temperature and soil microorganisms interact to affect Dodonaea viscosa growth on mountainsides. Plant Ecol. 2018;219(7):759–774. https://doi.org/10.1007/s11258-018-0832-4.
- View Article
- Google Scholar
16. Liu WX, Xu WH, Han Y, Wang CH, and Wan SQ. Responses of microbial biomass and respiration of soil to topography, burning, and nitrogen fertilization in a temperate steppe. Biol. Fert. Soils. 2007;44(2):259–268. https://doi.org/10.1007/s00374-007-0198-6.
- View Article
- Google Scholar
17. Johnson NC, Wilson GW, Bowker MA, Wilson JA, and Miller RM. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. P. Natl. Acad. Sci. USA. 2010;107(5):2093–8. https://doi.org/10.1073/pnas.0906710107 pmid:20133855
- View Article
- PubMed/NCBI
- Google Scholar
18. Smith SE and Read DJ. Mycorrhizal Symbiosis. Q. Rev. Biol. 2008;3(3):273–281. https://doi.org/10.1097/00010694-198403000-00011.
- View Article
- Google Scholar
19. Kardol P and Wardle DA. How understanding aboveground-belowground linkages can assist restoration ecology. Trends Ecol. Evol. 2010;25(11):670–9. https://doi.org/10.1016/j.tree.2010.09.001 pmid:20888063
- View Article
- PubMed/NCBI
- Google Scholar
20. He YJ, Jiang CH, Yang H, Wang YJ, and Zhong ZC. Arbuscular mycorrhizal fungal composition affects the growth and nutrient acquisition of two plants from a karst area. Sains Malays. 2017;46(10):1701–1708. https://doi.org/10.17576/jsm-2017-4610-05.
- View Article
- Google Scholar
21. Ferrol N, Azcon-Aguilar C, and Perez-Tienda J. Review: Arbuscular mycorrhizas as key players in sustainable plant phosphorus acquisition: An overview on the mechanisms involved. Plant Sci. 2019;280:441–447. https://doi.org/10.1016/j.plantsci.2018.11.011 pmid:30824024
- View Article
- PubMed/NCBI
- Google Scholar
22. Auge RM, Toler HD, and Saxton AM. Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza. 2015;25(1):13–24. https://doi.org/10.1007/s00572-014-0585-4 pmid:24831020
- View Article
- PubMed/NCBI
- Google Scholar
23. Rillig MC and Mummey DL. Mycorrhizas and soil structure. New Phytol. 2006;171(1):41–53. https://doi.org/10.1111/j.1469-8137.2006.01750.x pmid:16771981
- View Article
- PubMed/NCBI
- Google Scholar
24. Guo Y, He YJ, Wu BL, Lin Y, He MH, Han X, et al. The interspecific competition presents greater nutrient facilitation compared to intraspecific competition through AM fungi interacting with litter for two host plants in karst soil. J. Plant Ecol. 2021. https://doi.org/10.1093/jpe/rtab110.
- View Article
- Google Scholar
25. Xia T, Wang Y, He Y, Wu C, Shen K, Tan Q, et al. An invasive plant experiences greater benefits of root morphology from enhancing nutrient competition associated with arbuscular mycorrhizae in karst soil than a native plant. PLoS One. 2020;15(6):e0234410. https://doi.org/10.1371/journal.pone.0234410 pmid:32516341
- View Article
- PubMed/NCBI
- Google Scholar
26. Shi Z, Mickan B, Feng G, and Chen Y. Arbuscular mycorrhizal fungi improved plant growth and nutrient acquisition of desert ephemeral Plantago minuta under variable soil water conditions. J. Arid Land. 2015;7(3):414–420. https://doi.org/10.1007/s40333-014-0046-0
- View Article
- Google Scholar
27. Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, et al. Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol. 2015;205(4):1537–1551. https://doi.org/doi.org/10.1111/nph.13138 pmid:25382456
- View Article
- PubMed/NCBI
- Google Scholar
28. Micallef SA, Shiaris MP, and Colón-Carmona A. Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J. Exp. Bot. 2009;60(6):1729–1742. https://doi.org/10.1093/jxb/erp053 pmid:19342429
- View Article
- PubMed/NCBI
- Google Scholar
29. Gahan J and Schmalenberger A. Arbuscular mycorrhizal hyphae in grassland select for a diverse and abundant hyphospheric bacterial community involved in sulfonate desulfurization. Appl. Soil Ecol. 2015;89:113–121. https://doi.org/10.1016/j.apsoil.2014.12.008.
- View Article
- Google Scholar
30. Marulanda A, Barea JM, and Azcon R. An indigenous drought-tolerant strain of Glomus intraradices associated with a native bacterium improves water transport and root development in Retama sphaerocarpa. Microb. Ecol. 2006;52(4):670–678. https://doi.org/10.1007/s00248-006-9078-0 pmid:17075734
- View Article
- PubMed/NCBI
- Google Scholar
31. Ortiz N, Armada E, Duque E, Roldán A, and Azcón R. Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing plant drought tolerance under natural soil conditions: effectiveness of autochthonous or allochthonous strains. J. Plant Physiol. 2015;174:87–96. https://doi.org/10.1016/j.jplph.2014.08.019 pmid:25462971
- View Article
- PubMed/NCBI
- Google Scholar
32. Frey-Klett P and Garbaye J. Mycorrhiza helper bacteria: a promising model for the genomic analysis of fungal-bacterial interactions. New Phytol. 2005;168(1):4–8. https://doi.org/10.1111/j.1469-8137.2005.01553.x pmid:16159316
- View Article
- PubMed/NCBI
- Google Scholar
33. Vigo C, Norman J, and Hooker J. Biocontrol of the pathogen Phytophthora parasitica by arbuscular mycorrhizal fungi is a consequence of effects on infection loci. Plant Pathol. 2000;49(4):509–514. https://doi.org/10.1046/j.1365-3059.2000.00473.x.
- View Article
- Google Scholar
34. Xiao Y, Zhao Z, Chen L, and Li Y. Arbuscular mycorrhizal fungi and organic manure have synergistic effects on Trifolium repens in Cd-contaminated sterilized soil but not in natural soil. Appl. Soil Ecol. 2020;149:103485. https://doi.org/10.1016/j.apsoil.2019.103485.
- View Article
- Google Scholar
35. Artursson V, Finlay RD, and Jansson JK. Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ. Microbiol. 2006;8(1):1–10. https://doi.org/10.1111/j.1462-2920.2005.00942.x pmid:16343316
- View Article
- PubMed/NCBI
- Google Scholar
36. Fester T, Maier W, and Strack D. Accumulation of secondary compounds in barley and wheat roots in response to inoculation with an arbuscular mycorrhizal fungus and co-inoculation with rhizosphere bacteria. Mycorrhiza. 1999;8(5):241–246. https://doi.org/10.1007/s005720050240
- View Article
- Google Scholar
37. Battini F, Cristani C, Giovannetti M, and Agnolucci M. Multifunctionality and diversity of culturable bacterial communities strictly associated with spores of the plant beneficial symbiont Rhizophagus intraradices. Microbiol. Res. 2016;183:68–79. https://doi.org/10.1016/j.micres.2015.11.012 pmid:26805620
- View Article
- PubMed/NCBI
- Google Scholar
38. Garbaye J. Tansley review no. 76 helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol. 1994;128(2):197–210. https://doi.org/10.1111/j.1469-8137.1994.tb04003.x pmid:33874371
- View Article
- PubMed/NCBI
- Google Scholar
39. Frey-Klett P, Garbaye J, and Tarkka M. The mycorrhiza helper bacteria revisited. New Phytol. 2007;176(1):22–36. https://doi.org/10.1111/j.1469-8137.2007.02191.x pmid:17803639
- View Article
- PubMed/NCBI
- Google Scholar
40. Srivastava R, Khalid A, Singh US, and Sharma AK. Evaluation of arbuscular mycorrhizal fungus, fluorescent Pseudomonas and Trichoderma harzianum formulation against Fusarium oxysporum f. sp. lycopersici for the management of tomato wilt. Biol. Control. 2010;53(1):24–31. https://doi.org/10.1016/j.biocontrol.2009.11.012.
- View Article
- Google Scholar
41. Azcón-Aguilar C and Barea JM. Arbuscular mycorrhizas and biological control of soil-borne plant pathogens–an overview of the mechanisms involved. Mycorrhiza. 1997;6(6):457–464. https://doi.org/10.1007/s005720050147
- View Article
- Google Scholar
42. Doumbou CL, Hamby Salove MK, Crawford DL, and Beaulieu C. Actinomycetes, promising tools to control plant diseases and to promote plant growth. Phytoprotection. 2005;82(3):85–102. https://doi.org/10.7202/706219ar.
- View Article
- Google Scholar
43. Leigh J, Fitter AH, and Hodge A. Growth and symbiotic effectiveness of an arbuscular mycorrhizal fungus in organic matter in competition with soil bacteria. FEMS Microbiol. Ecol. 2011;76(3):428–438. https://doi.org/10.1111/j.1574-6941.2011.01066.x pmid:21303398
- View Article
- PubMed/NCBI
- Google Scholar
44. He YJ, Cornelissen JHC, Wang P, Dong M, and Ou J. Nitrogen transfer from one plant to another depends on plant biomass production between conspecific and heterospecific species via a common arbuscular mycorrhizal network. Environmental Science and Pollution Research. 2019;26(9):8828–8837. https://doi.org/10.1007/s11356-019-04385-x pmid:30712202
- View Article
- PubMed/NCBI
- Google Scholar
45. Tan KH. Soil sampling, preparation, and analysis. CRC press; 2005.
46. Giovannetti M and Mosse B. An evaluation of techniques for measuring vesicular-arbuscular infection in roots. New Phytol. 1980;84(3):489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x.
- View Article
- Google Scholar
47. Bao SD. Soil and agricultural chemistry analysis. China agriculture press, Beijing; 2000.
48. Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, et al. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 2010;13(3):394–407. https://doi.org/10.1111/j.1461-0248.2009.01430.x pmid:20100237
- View Article
- PubMed/NCBI
- Google Scholar
49. Hedges LV, Gurevitch J, and Curtis PS. The Meta-Analysis of Response Ratios in Experimental Ecology. Ecology. 1999;80(4):1150–1156. https://doi.org/10.2307/177062
- View Article
- Google Scholar
50. Bona E, Cantamessa S, Massa N, Manassero P, Marsano F, Copetta A, et al. Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads improve yield, quality and nutritional value of tomato: a field study. Mycorrhiza. 2017;27(1):1–11. https://doi.org/10.1007/s00572-016-0727-y pmid:27539491
- View Article
- PubMed/NCBI
- Google Scholar
51. Zhang F, Li Q, Yerger EH, Chen X, Shi Q, and Wan F. AM fungi facilitate the competitive growth of two invasive plant species, Ambrosia artemisiifolia and Bidens pilosa. Mycorrhiza. 2018;28(8):703–715. https://doi.org/10.1007/s00572-018-0866-4 pmid:30220052
- View Article
- PubMed/NCBI
- Google Scholar
52. Allen MF. Linking water and nutrients through the vadose zone: a fungal interface between the soil and plant systems. J. Arid Land. 2011;3(3):155–163. https://doi.org/10.3724/sp.J.1227.2011.00155.
- View Article
- Google Scholar
53. Smith SE and Smith FA. Roles of Arbuscular Mycorrhizas in Plant Nutrition and Growth: New Paradigms from Cellular to Ecosystem Scales. Annu. Rev. Plant Biol. 2011;62(1):227–250. https://doi.org/10.1146/annurev-arplant-042110-103846 pmid:21391813
- View Article
- PubMed/NCBI
- Google Scholar
54. Lugtenberg BJJ, Malfanova N, Kamilova F, and Berg G. Plant Growth Promotion by Microbes. Molecular Microbial Ecology of the Rhizosphere 2013;2:559–573. https://doi.org/10.1002/9781118297674.ch53
- View Article
- Google Scholar
55. Leff JW, Jones SE, Prober SM, Barberan A, Borer ET, Firn JL, et al. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proceedling of the National Academy of Science. 2015;112(35):10967–10972. https://doi.org/10.1073/pnas.1508382112 pmid:26283343
- View Article
- PubMed/NCBI
- Google Scholar
56. Tawaraya K, Naito M, and Wagatsuma T. Solubilization of Insoluble Inorganic Phosphate by Hyphal Exudates of Arbuscular Mycorrhizal Fungi. J. Plant Nutr. 2006;29(4):657–665. https://doi.org/10.1080/01904160600564428.
- View Article
- Google Scholar
57. Wu F, Li Z, Lin Y, and Zhang L. Effects of Funneliformis mosseae on the utilization of organic phosphorus in Camellia oleifera Abel. Can. J. Microbiol. 2021;67(5):349–357. https://doi.org/10.1139/cjm-2020-0227 pmid:33769090
- View Article
- PubMed/NCBI
- Google Scholar
58. Cappellazzo G, Lanfranco L, Fitz M, Wipf D, and Bonfante P. Characterization of an amino acid permease from the endomycorrhizal fungus Glomus mosseae. Plant Physiol. 2008;147(1):429–37. https://doi.org/10.1104/pp.108.117820 pmid:18344417
- View Article
- PubMed/NCBI
- Google Scholar
59. Hodge A, Campbell CD, and Fitter AH. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature. 2001;413:297–299. https://doi.org/10.1038/35095041 pmid:11565029
- View Article
- PubMed/NCBI
- Google Scholar
60. Elbon A and Whalen JK. Phosphorus supply to vegetable crops from arbuscular mycorrhizal fungi: a review. Biol. Agric. Hortic. 2014;31(2):73–90. https://doi.org/10.1080/01448765.2014.966147.
- View Article
- Google Scholar
61. Zhang LX, Bai YF, and Han XG. Differential Responses of N:P Stoichiometry of Leymus chinensis and Carex korshinskyi to N Additions in a Steppe Ecosystem in Nei Mongol. Acta Bot. Sin. 2004;46:259–270. https://doi.org/10.1300/J079v30n03_01.
- View Article
- Google Scholar
62. Koerselman Willem, and Meuleman AFM. The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J. App. Ecol. 1996;33(6):1441–1450. https://doi.org/10.2307/2404783
- View Article
- Google Scholar
63. Shen K, Cornelissen JHC, Wang Y, Wu C, He Y, Ou J, et al. AM fungi alleviate phosphorus limitation and enhance nutrient competitiveness of invasive plants via mycorrhizal networks in karst areas. Front. Ecol. Evol. 2020;8. https://doi.org/10.3389/fevo.2020.00125.
- View Article
- Google Scholar
64. Bever JD. Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol. 2003;157(3):465–473. https://doi.org/10.2307/1514052 pmid:33873396
- View Article
- PubMed/NCBI
- Google Scholar
65. Van der Heijden MG, Boller T, Wiemken A, and Sanders IR. Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology. 1998;79(6):2082–2091.
- View Article
- Google Scholar
66. Liu R and Wang F. Selection of appropriate host plants used in trap culture of arbuscular mycorrhizal fungi. Mycorrhiza. 2003;13(3):123–127. https://doi.org/10.1007/s00572-002-0207-4 pmid:12687445
- View Article
- PubMed/NCBI
- Google Scholar
67. Wilson GW, Rice CW, Rillig MC, Springer A, and Hartnett DC. Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol. Lett. 2009;12(5):452–61. https://doi.org/10.1111/j.1461-0248.2009.01303.x pmid:19320689
- View Article
- PubMed/NCBI
- Google Scholar
68. Giovannini L, Palla M, Agnolucci M, Avio L, Sbrana C, Turrini A, et al. Arbuscular mycorrhizal fungi and associated microbiota as plant biostimulants: research strategies for the selection of the best performing inocula. Agronomy-Basel. 2020;10(1):106. https://doi.org/10.3390/agronomy10010106.
- View Article
- Google Scholar
69. Vázquez MM, César S, Azcón R, and Barea JM. Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Applied Soil Ecology. 2000;15(3):261–272. https://doi.org/10.1016/s0929-1393(00)00075-5
- View Article
- Google Scholar
70. Larimer AL, Clay K, and Bever JD. Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. Ecological. 2014;95(4):1045–1054. https://doi.org/10.1890/13-0025.1 pmid:24933822
- View Article
- PubMed/NCBI
- Google Scholar
71. Diagne N, Baudoin E, Svistoonoff S, Ouattara C, Diouf D, Kane A, et al. Effect of native and allochthonous arbuscular mycorrhizal fungi on Casuarina equisetifolia growth and its root bacterial community. Arid Land Res. Manage. 2017;32(2):212–228. https://doi.org/10.1080/15324982.2017.1406413.
- View Article
- Google Scholar
72. Mortimer PE, Le Roux MR, Pérez-Fernández MA, Benedito VA, Kleinert A, Xu J, et al. The dual symbiosis between arbuscular mycorrhiza and nitrogen fixing bacteria benefits the growth and nutrition of the woody invasive legume Acacia cyclops under nutrient limiting conditions. Plant Soil. 2012;366(1–2):229–241. https://doi.org/10.1007/s11104-012-1421-2.
- View Article
- Google Scholar
73. Linderman RG. Vesicular-arbuscular mycorrhizal (VAM) fungi. In Plant Relationships Part B. Springer, Berlin, Heidelberg; 1997: 117–128.
74. Bender SF, Schlaeppi K, Held A, and Van der Heijden MGA. Establishment success and crop growth effects of an arbuscular mycorrhizal fungus inoculated into Swiss corn fields. Agriculture Ecosystems & Environment. 2019;273:13–24. https://doi.org/10.1016/j.agee.2018.12.003.
- View Article
- Google Scholar
75. Miransari M. Interactions between arbuscular mycorrhizal fungi and soil bacteria. Appl. Microbiol. Biotechnol. 2011;89(4):917–930. https://doi.org/10.1007/s00253-010-3004-6 pmid:21104242
- View Article
- PubMed/NCBI
- Google Scholar
76. Niwa R, Koyama T, Sato T, Adachi K, Tawaraya K, Sato S, et al. Dissection of niche competition between introduced and indigenous arbuscular mycorrhizal fungi with respect to soybean yield responses. Sci. Rep-UK. 2018;8(1):7419. https://doi.org/10.1038/s41598-018-25701-4 pmid:29743529
- View Article
- PubMed/NCBI
- Google Scholar
77. Hausmann NT and Hawkes CV. Order of plant host establishment alters the composition of arbuscular mycorrhizal communities. Ecology. 2010;91(8):2333–2343. https://doi.org/10.1890/09-0924.1 pmid:20836455
- View Article
- PubMed/NCBI
- Google Scholar
78. Dąbrowska G, Baum C, Trejgell A, and Hrynkiewicz K. Impact of arbuscular mycorrhizal fungi on the growth and expression of gene encoding stress protein–metallothionein BnMT2 in the non‐host crop Brassica napus L. J. Plant Nutr. Soil Sci. 2014;177(3):459–467. https://doi.org/10.1002/jpln.201300115.
- View Article
- Google Scholar
79. Rousk J, Demoling LA, Bahr A, and Baath E. Examining the fungal and bacterial niche overlap using selective inhibitors in soil. FEMS Microbiol. Ecol. 2008;63(3):350–358. https://doi.org/10.1111/j.1574-6941.2008.00440.x pmid:18205814
- View Article
- PubMed/NCBI
- Google Scholar
80. de Boer W, Verheggen P, Klein Gunnewiek PJ, Kowalchuk GA, and van Veen JA. Microbial community composition affects soil fungistasis. Appl. Environ. Microbiol. 2003;69(2):835–44. https://doi.org/10.1128/AEM.69.2.835-844.2003 pmid:12571002
- View Article
- PubMed/NCBI
- Google Scholar
81. Li X, Garbeva P, Liu X, Klein Gunnewiek PJA, Clocchiatti A, Hundscheid MPJ, et al. Volatile-mediated antagonism of soil bacterial communities against fungi. Environ. Microbiol. 2020;22(3):1025–1035. https://doi.org/10.1111/1462-2920.14808 pmid:31580006
- View Article
- PubMed/NCBI
- Google Scholar
82. Biró B, Köves-Péchy K, Takács IVT, Eggenberger P, and Strasser. RJ. Interrelations between Azospirillum and Rhizobium nitrogen-fixers and arbuscular mycorrhizal fungi in the rhizosphere of alfalfa in sterile, AMF-free or normal soil conditions. Appl. Soil Ecol. 2000;15(2):159–168. https://doi.org/10.1016/s0929-1393(00)00092-5.
- View Article
- Google Scholar

[ref1] 1. Nie YP, Chen HS, Wang KL, and Ding YL. Rooting characteristics of two widely distributed woody plant species growing in different karst habitats of southwest China. Plant Ecol. 2014;215(10):1099–1109. https://doi.org/10.1007/s11258-014-0369-0.
View Article
Google Scholar

[2] View Article

[3] Google Scholar

[ref2] 2. Liu Y, Liu C, Rubinato M, Guo K, Zhou J, and Cui M. An Assessment of Soil’s Nutrient Deficiencies and Their Influence on the Restoration of Degraded Karst Vegetation in Southwest China. Forests. 2020;11(8):797. https://doi.org/10.3390/f11080797.
View Article
Google Scholar

[5] View Article

[6] Google Scholar

[ref3] 3. Peng T and Wang SJ. Effects of land use, land cover and rainfall regimes on the surface runoff and soil loss on karst slopes in southwest China. Catena. 2012;90(1):53–62. https://doi.org/10.1016/j.catena.2011.11.001.
View Article
Google Scholar

[8] View Article

[9] Google Scholar

[ref4] 4. Jiang Z, Lian Y, and Qin X. Rocky desertification in Southwest China: Impacts, causes, and restoration. Earth-Sci. Rev. 2014;132:1–12. https://doi.org/10.1016/j.earscirev.2014.01.005.
View Article
Google Scholar

[11] View Article

[12] Google Scholar

[ref5] 5. Green SM, Dungait JAJ, Tu C, Buss HL, Sanderson N, Hawkes SJ, et al. Soil functions and ecosystem services research in the Chinese karst Critical Zone. Chem. Geol. 2019;527. https://doi.org/10.1016/j.chemgeo.2019.03.018.
View Article
Google Scholar

[14] View Article

[15] Google Scholar

[ref6] 6. Yang H, Zang Y, Yuan Y, Tang J, and Chen X. Selectivity by host plants affects the distribution of arbuscular mycorrhizal fungi: evidence from ITS rDNA sequence metadata. BMC Evol. Biol. 2012;12(1):1–13. https://doi.org/10.1186/1471-2148-12-50 pmid:22498355
View Article
PubMed/NCBI
Google Scholar

[17] View Article

[18] PubMed/NCBI

[19] Google Scholar

[ref7] 7. Hartmann A, Goldscheider N, Wagener T, Lange J, and Weiler M. Karst water resources in a changing world: Review of hydrological modeling approaches. Rev. Geophys. 2014;52(3):218–242. https://doi.org/10.1002/2013rg000443.
View Article
Google Scholar

[21] View Article

[22] Google Scholar

[ref8] 8. Zeng F, Peng W, Song T, Wang K, Wu H, Song X, et al. Changes in vegetation after 22 years’ natural restoration in the Karst disturbed area in northwestern Guangxi, China. Acta Ecol. Sin. 2007;27(12):5110–5119. https://doi.org/10.1016/s1872-2032(08)60016-5.
View Article
Google Scholar

[24] View Article

[25] Google Scholar

[ref9] 9. Pang D, Cao J, Dan X, Guan Y, Peng X, Cui M, et al. Recovery approach affects soil quality in fragile karst ecosystems of southwest China: Implications for vegetation restoration. Ecol. Eng. 2018;123:151–160. https://doi.org/10.1016/j.ecoleng.2018.09.001.
View Article
Google Scholar

[27] View Article

[28] Google Scholar

[ref10] 10. Long ZF, Tang CB, and Yang YC. Discussion on the effect of herbage in the comprehensive administration and the sustainable development in the karst area. Guizhou Agricultural Sciences. 2005;33(Z1):69–71.
View Article
Google Scholar

[30] View Article

[31] Google Scholar

[ref11] 11. Cao J, Yuan D, Tong L, Azim M, Yang H, and Huang F. An overview of karst ecosystem in Southwest China: current state and future management. J. Res. Ecol. 2015;6(4):247–256. https://doi.org/10.5814/j.issn.1674-764x.2015.04.008.
View Article
Google Scholar

[33] View Article

[34] Google Scholar

[ref12] 12. Anding L. The Composition and Structural Feature of Plant Community in Different Karst Stony Desertification Areas. Appl. Ecol. Environ. Res. 2017;15(4):1167–1183. https://doi.org/10.15666/aeer/1504_11671183.
View Article
Google Scholar

[36] View Article

[37] Google Scholar

[ref13] 13. Chen X, Su Y, He X, Wei Y, Wei W, and Wu J. Soil bacterial community composition and diversity respond to cultivation in Karst ecosystems. World J. Microbiol. Biotechnol. 2012;28(1):205–13. https://doi.org/10.1007/s11274-011-0809-0 pmid:22806796
View Article
PubMed/NCBI
Google Scholar

[39] View Article

[40] PubMed/NCBI

[41] Google Scholar

[ref14] 14. Richardson AE and Simpson RJ. Soil Microorganisms Mediating Phosphorus Availability. Plant Physiol. 2011;156(3):989–996. https://doi.org/10.2307/41435012 pmid:21606316
View Article
PubMed/NCBI
Google Scholar

[43] View Article

[44] PubMed/NCBI

[45] Google Scholar

[ref15] 15. Wang X, Yan B, Fan B, Shi L, and Liu G. Temperature and soil microorganisms interact to affect Dodonaea viscosa growth on mountainsides. Plant Ecol. 2018;219(7):759–774. https://doi.org/10.1007/s11258-018-0832-4.
View Article
Google Scholar

[47] View Article

[48] Google Scholar

[ref16] 16. Liu WX, Xu WH, Han Y, Wang CH, and Wan SQ. Responses of microbial biomass and respiration of soil to topography, burning, and nitrogen fertilization in a temperate steppe. Biol. Fert. Soils. 2007;44(2):259–268. https://doi.org/10.1007/s00374-007-0198-6.
View Article
Google Scholar

[50] View Article

[51] Google Scholar

[ref17] 17. Johnson NC, Wilson GW, Bowker MA, Wilson JA, and Miller RM. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. P. Natl. Acad. Sci. USA. 2010;107(5):2093–8. https://doi.org/10.1073/pnas.0906710107 pmid:20133855
View Article
PubMed/NCBI
Google Scholar

[53] View Article

[54] PubMed/NCBI

[55] Google Scholar

[ref18] 18. Smith SE and Read DJ. Mycorrhizal Symbiosis. Q. Rev. Biol. 2008;3(3):273–281. https://doi.org/10.1097/00010694-198403000-00011.
View Article
Google Scholar

[57] View Article

[58] Google Scholar

[ref19] 19. Kardol P and Wardle DA. How understanding aboveground-belowground linkages can assist restoration ecology. Trends Ecol. Evol. 2010;25(11):670–9. https://doi.org/10.1016/j.tree.2010.09.001 pmid:20888063
View Article
PubMed/NCBI
Google Scholar

[60] View Article

[61] PubMed/NCBI

[62] Google Scholar

[ref20] 20. He YJ, Jiang CH, Yang H, Wang YJ, and Zhong ZC. Arbuscular mycorrhizal fungal composition affects the growth and nutrient acquisition of two plants from a karst area. Sains Malays. 2017;46(10):1701–1708. https://doi.org/10.17576/jsm-2017-4610-05.
View Article
Google Scholar

[64] View Article

[65] Google Scholar

[ref21] 21. Ferrol N, Azcon-Aguilar C, and Perez-Tienda J. Review: Arbuscular mycorrhizas as key players in sustainable plant phosphorus acquisition: An overview on the mechanisms involved. Plant Sci. 2019;280:441–447. https://doi.org/10.1016/j.plantsci.2018.11.011 pmid:30824024
View Article
PubMed/NCBI
Google Scholar

[67] View Article

[68] PubMed/NCBI

[69] Google Scholar

[ref22] 22. Auge RM, Toler HD, and Saxton AM. Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza. 2015;25(1):13–24. https://doi.org/10.1007/s00572-014-0585-4 pmid:24831020
View Article
PubMed/NCBI
Google Scholar

[71] View Article

[72] PubMed/NCBI

[73] Google Scholar

[ref23] 23. Rillig MC and Mummey DL. Mycorrhizas and soil structure. New Phytol. 2006;171(1):41–53. https://doi.org/10.1111/j.1469-8137.2006.01750.x pmid:16771981
View Article
PubMed/NCBI
Google Scholar

[75] View Article

[76] PubMed/NCBI

[77] Google Scholar

[ref24] 24. Guo Y, He YJ, Wu BL, Lin Y, He MH, Han X, et al. The interspecific competition presents greater nutrient facilitation compared to intraspecific competition through AM fungi interacting with litter for two host plants in karst soil. J. Plant Ecol. 2021. https://doi.org/10.1093/jpe/rtab110.
View Article
Google Scholar

[79] View Article

[80] Google Scholar

[ref25] 25. Xia T, Wang Y, He Y, Wu C, Shen K, Tan Q, et al. An invasive plant experiences greater benefits of root morphology from enhancing nutrient competition associated with arbuscular mycorrhizae in karst soil than a native plant. PLoS One. 2020;15(6):e0234410. https://doi.org/10.1371/journal.pone.0234410 pmid:32516341
View Article
PubMed/NCBI
Google Scholar

[82] View Article

[83] PubMed/NCBI

[84] Google Scholar

[ref26] 26. Shi Z, Mickan B, Feng G, and Chen Y. Arbuscular mycorrhizal fungi improved plant growth and nutrient acquisition of desert ephemeral Plantago minuta under variable soil water conditions. J. Arid Land. 2015;7(3):414–420. https://doi.org/10.1007/s40333-014-0046-0
View Article
Google Scholar

[86] View Article

[87] Google Scholar

[ref27] 27. Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, et al. Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol. 2015;205(4):1537–1551. https://doi.org/doi.org/10.1111/nph.13138 pmid:25382456
View Article
PubMed/NCBI
Google Scholar

[89] View Article

[90] PubMed/NCBI

[91] Google Scholar

[ref28] 28. Micallef SA, Shiaris MP, and Colón-Carmona A. Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J. Exp. Bot. 2009;60(6):1729–1742. https://doi.org/10.1093/jxb/erp053 pmid:19342429
View Article
PubMed/NCBI
Google Scholar

[93] View Article

[94] PubMed/NCBI

[95] Google Scholar

[ref29] 29. Gahan J and Schmalenberger A. Arbuscular mycorrhizal hyphae in grassland select for a diverse and abundant hyphospheric bacterial community involved in sulfonate desulfurization. Appl. Soil Ecol. 2015;89:113–121. https://doi.org/10.1016/j.apsoil.2014.12.008.
View Article
Google Scholar

[97] View Article

[98] Google Scholar

[ref30] 30. Marulanda A, Barea JM, and Azcon R. An indigenous drought-tolerant strain of Glomus intraradices associated with a native bacterium improves water transport and root development in Retama sphaerocarpa. Microb. Ecol. 2006;52(4):670–678. https://doi.org/10.1007/s00248-006-9078-0 pmid:17075734
View Article
PubMed/NCBI
Google Scholar

[100] View Article

[101] PubMed/NCBI

[102] Google Scholar

[ref31] 31. Ortiz N, Armada E, Duque E, Roldán A, and Azcón R. Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing plant drought tolerance under natural soil conditions: effectiveness of autochthonous or allochthonous strains. J. Plant Physiol. 2015;174:87–96. https://doi.org/10.1016/j.jplph.2014.08.019 pmid:25462971
View Article
PubMed/NCBI
Google Scholar

[104] View Article

[105] PubMed/NCBI

[106] Google Scholar

[ref32] 32. Frey-Klett P and Garbaye J. Mycorrhiza helper bacteria: a promising model for the genomic analysis of fungal-bacterial interactions. New Phytol. 2005;168(1):4–8. https://doi.org/10.1111/j.1469-8137.2005.01553.x pmid:16159316
View Article
PubMed/NCBI
Google Scholar

[108] View Article

[109] PubMed/NCBI

[110] Google Scholar

[ref33] 33. Vigo C, Norman J, and Hooker J. Biocontrol of the pathogen Phytophthora parasitica by arbuscular mycorrhizal fungi is a consequence of effects on infection loci. Plant Pathol. 2000;49(4):509–514. https://doi.org/10.1046/j.1365-3059.2000.00473.x.
View Article
Google Scholar

[112] View Article

[113] Google Scholar

[ref34] 34. Xiao Y, Zhao Z, Chen L, and Li Y. Arbuscular mycorrhizal fungi and organic manure have synergistic effects on Trifolium repens in Cd-contaminated sterilized soil but not in natural soil. Appl. Soil Ecol. 2020;149:103485. https://doi.org/10.1016/j.apsoil.2019.103485.
View Article
Google Scholar

[115] View Article

[116] Google Scholar

[ref35] 35. Artursson V, Finlay RD, and Jansson JK. Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ. Microbiol. 2006;8(1):1–10. https://doi.org/10.1111/j.1462-2920.2005.00942.x pmid:16343316
View Article
PubMed/NCBI
Google Scholar

[118] View Article

[119] PubMed/NCBI

[120] Google Scholar

[ref36] 36. Fester T, Maier W, and Strack D. Accumulation of secondary compounds in barley and wheat roots in response to inoculation with an arbuscular mycorrhizal fungus and co-inoculation with rhizosphere bacteria. Mycorrhiza. 1999;8(5):241–246. https://doi.org/10.1007/s005720050240
View Article
Google Scholar

[122] View Article

[123] Google Scholar

[ref37] 37. Battini F, Cristani C, Giovannetti M, and Agnolucci M. Multifunctionality and diversity of culturable bacterial communities strictly associated with spores of the plant beneficial symbiont Rhizophagus intraradices. Microbiol. Res. 2016;183:68–79. https://doi.org/10.1016/j.micres.2015.11.012 pmid:26805620
View Article
PubMed/NCBI
Google Scholar

[125] View Article

[126] PubMed/NCBI

[127] Google Scholar

[ref38] 38. Garbaye J. Tansley review no. 76 helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol. 1994;128(2):197–210. https://doi.org/10.1111/j.1469-8137.1994.tb04003.x pmid:33874371
View Article
PubMed/NCBI
Google Scholar

[129] View Article

[130] PubMed/NCBI

[131] Google Scholar

[ref39] 39. Frey-Klett P, Garbaye J, and Tarkka M. The mycorrhiza helper bacteria revisited. New Phytol. 2007;176(1):22–36. https://doi.org/10.1111/j.1469-8137.2007.02191.x pmid:17803639
View Article
PubMed/NCBI
Google Scholar

[133] View Article

[134] PubMed/NCBI

[135] Google Scholar

[ref40] 40. Srivastava R, Khalid A, Singh US, and Sharma AK. Evaluation of arbuscular mycorrhizal fungus, fluorescent Pseudomonas and Trichoderma harzianum formulation against Fusarium oxysporum f. sp. lycopersici for the management of tomato wilt. Biol. Control. 2010;53(1):24–31. https://doi.org/10.1016/j.biocontrol.2009.11.012.
View Article
Google Scholar

[137] View Article

[138] Google Scholar

[ref41] 41. Azcón-Aguilar C and Barea JM. Arbuscular mycorrhizas and biological control of soil-borne plant pathogens–an overview of the mechanisms involved. Mycorrhiza. 1997;6(6):457–464. https://doi.org/10.1007/s005720050147
View Article
Google Scholar

[140] View Article

[141] Google Scholar

[ref42] 42. Doumbou CL, Hamby Salove MK, Crawford DL, and Beaulieu C. Actinomycetes, promising tools to control plant diseases and to promote plant growth. Phytoprotection. 2005;82(3):85–102. https://doi.org/10.7202/706219ar.
View Article
Google Scholar

[143] View Article

[144] Google Scholar

[ref43] 43. Leigh J, Fitter AH, and Hodge A. Growth and symbiotic effectiveness of an arbuscular mycorrhizal fungus in organic matter in competition with soil bacteria. FEMS Microbiol. Ecol. 2011;76(3):428–438. https://doi.org/10.1111/j.1574-6941.2011.01066.x pmid:21303398
View Article
PubMed/NCBI
Google Scholar

[146] View Article

[147] PubMed/NCBI

[148] Google Scholar

[ref44] 44. He YJ, Cornelissen JHC, Wang P, Dong M, and Ou J. Nitrogen transfer from one plant to another depends on plant biomass production between conspecific and heterospecific species via a common arbuscular mycorrhizal network. Environmental Science and Pollution Research. 2019;26(9):8828–8837. https://doi.org/10.1007/s11356-019-04385-x pmid:30712202
View Article
PubMed/NCBI
Google Scholar

[150] View Article

[151] PubMed/NCBI

[152] Google Scholar

[ref45] 45. Tan KH. Soil sampling, preparation, and analysis. CRC press; 2005.

[ref46] 46. Giovannetti M and Mosse B. An evaluation of techniques for measuring vesicular-arbuscular infection in roots. New Phytol. 1980;84(3):489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x.
View Article
Google Scholar

[155] View Article

[156] Google Scholar

[ref47] 47. Bao SD. Soil and agricultural chemistry analysis. China agriculture press, Beijing; 2000.

[ref48] 48. Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, et al. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 2010;13(3):394–407. https://doi.org/10.1111/j.1461-0248.2009.01430.x pmid:20100237
View Article
PubMed/NCBI
Google Scholar

[159] View Article

[160] PubMed/NCBI

[161] Google Scholar

[ref49] 49. Hedges LV, Gurevitch J, and Curtis PS. The Meta-Analysis of Response Ratios in Experimental Ecology. Ecology. 1999;80(4):1150–1156. https://doi.org/10.2307/177062
View Article
Google Scholar

[163] View Article

[164] Google Scholar

[ref50] 50. Bona E, Cantamessa S, Massa N, Manassero P, Marsano F, Copetta A, et al. Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads improve yield, quality and nutritional value of tomato: a field study. Mycorrhiza. 2017;27(1):1–11. https://doi.org/10.1007/s00572-016-0727-y pmid:27539491
View Article
PubMed/NCBI
Google Scholar

[166] View Article

[167] PubMed/NCBI

[168] Google Scholar

[ref51] 51. Zhang F, Li Q, Yerger EH, Chen X, Shi Q, and Wan F. AM fungi facilitate the competitive growth of two invasive plant species, Ambrosia artemisiifolia and Bidens pilosa. Mycorrhiza. 2018;28(8):703–715. https://doi.org/10.1007/s00572-018-0866-4 pmid:30220052
View Article
PubMed/NCBI
Google Scholar

[170] View Article

[171] PubMed/NCBI

[172] Google Scholar

[ref52] 52. Allen MF. Linking water and nutrients through the vadose zone: a fungal interface between the soil and plant systems. J. Arid Land. 2011;3(3):155–163. https://doi.org/10.3724/sp.J.1227.2011.00155.
View Article
Google Scholar

[174] View Article

[175] Google Scholar

[ref53] 53. Smith SE and Smith FA. Roles of Arbuscular Mycorrhizas in Plant Nutrition and Growth: New Paradigms from Cellular to Ecosystem Scales. Annu. Rev. Plant Biol. 2011;62(1):227–250. https://doi.org/10.1146/annurev-arplant-042110-103846 pmid:21391813
View Article
PubMed/NCBI
Google Scholar

[177] View Article

[178] PubMed/NCBI

[179] Google Scholar

[ref54] 54. Lugtenberg BJJ, Malfanova N, Kamilova F, and Berg G. Plant Growth Promotion by Microbes. Molecular Microbial Ecology of the Rhizosphere 2013;2:559–573. https://doi.org/10.1002/9781118297674.ch53
View Article
Google Scholar

[181] View Article

[182] Google Scholar

[ref55] 55. Leff JW, Jones SE, Prober SM, Barberan A, Borer ET, Firn JL, et al. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proceedling of the National Academy of Science. 2015;112(35):10967–10972. https://doi.org/10.1073/pnas.1508382112 pmid:26283343
View Article
PubMed/NCBI
Google Scholar

[184] View Article

[185] PubMed/NCBI

[186] Google Scholar

[ref56] 56. Tawaraya K, Naito M, and Wagatsuma T. Solubilization of Insoluble Inorganic Phosphate by Hyphal Exudates of Arbuscular Mycorrhizal Fungi. J. Plant Nutr. 2006;29(4):657–665. https://doi.org/10.1080/01904160600564428.
View Article
Google Scholar

[188] View Article

[189] Google Scholar

[ref57] 57. Wu F, Li Z, Lin Y, and Zhang L. Effects of Funneliformis mosseae on the utilization of organic phosphorus in Camellia oleifera Abel. Can. J. Microbiol. 2021;67(5):349–357. https://doi.org/10.1139/cjm-2020-0227 pmid:33769090
View Article
PubMed/NCBI
Google Scholar

[191] View Article

[192] PubMed/NCBI

[193] Google Scholar

[ref58] 58. Cappellazzo G, Lanfranco L, Fitz M, Wipf D, and Bonfante P. Characterization of an amino acid permease from the endomycorrhizal fungus Glomus mosseae. Plant Physiol. 2008;147(1):429–37. https://doi.org/10.1104/pp.108.117820 pmid:18344417
View Article
PubMed/NCBI
Google Scholar

[195] View Article

[196] PubMed/NCBI

[197] Google Scholar

[ref59] 59. Hodge A, Campbell CD, and Fitter AH. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature. 2001;413:297–299. https://doi.org/10.1038/35095041 pmid:11565029
View Article
PubMed/NCBI
Google Scholar

[199] View Article

[200] PubMed/NCBI

[201] Google Scholar

[ref60] 60. Elbon A and Whalen JK. Phosphorus supply to vegetable crops from arbuscular mycorrhizal fungi: a review. Biol. Agric. Hortic. 2014;31(2):73–90. https://doi.org/10.1080/01448765.2014.966147.
View Article
Google Scholar

[203] View Article

[204] Google Scholar

[ref61] 61. Zhang LX, Bai YF, and Han XG. Differential Responses of N:P Stoichiometry of Leymus chinensis and Carex korshinskyi to N Additions in a Steppe Ecosystem in Nei Mongol. Acta Bot. Sin. 2004;46:259–270. https://doi.org/10.1300/J079v30n03_01.
View Article
Google Scholar

[206] View Article

[207] Google Scholar

[ref62] 62. Koerselman Willem, and Meuleman AFM. The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J. App. Ecol. 1996;33(6):1441–1450. https://doi.org/10.2307/2404783
View Article
Google Scholar

[209] View Article

[210] Google Scholar

[ref63] 63. Shen K, Cornelissen JHC, Wang Y, Wu C, He Y, Ou J, et al. AM fungi alleviate phosphorus limitation and enhance nutrient competitiveness of invasive plants via mycorrhizal networks in karst areas. Front. Ecol. Evol. 2020;8. https://doi.org/10.3389/fevo.2020.00125.
View Article
Google Scholar

[212] View Article

[213] Google Scholar

[ref64] 64. Bever JD. Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol. 2003;157(3):465–473. https://doi.org/10.2307/1514052 pmid:33873396
View Article
PubMed/NCBI
Google Scholar

[215] View Article

[216] PubMed/NCBI

[217] Google Scholar

[ref65] 65. Van der Heijden MG, Boller T, Wiemken A, and Sanders IR. Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology. 1998;79(6):2082–2091.
View Article
Google Scholar

[219] View Article

[220] Google Scholar

[ref66] 66. Liu R and Wang F. Selection of appropriate host plants used in trap culture of arbuscular mycorrhizal fungi. Mycorrhiza. 2003;13(3):123–127. https://doi.org/10.1007/s00572-002-0207-4 pmid:12687445
View Article
PubMed/NCBI
Google Scholar

[222] View Article

[223] PubMed/NCBI

[224] Google Scholar

[ref67] 67. Wilson GW, Rice CW, Rillig MC, Springer A, and Hartnett DC. Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol. Lett. 2009;12(5):452–61. https://doi.org/10.1111/j.1461-0248.2009.01303.x pmid:19320689
View Article
PubMed/NCBI
Google Scholar

[226] View Article

[227] PubMed/NCBI

[228] Google Scholar

[ref68] 68. Giovannini L, Palla M, Agnolucci M, Avio L, Sbrana C, Turrini A, et al. Arbuscular mycorrhizal fungi and associated microbiota as plant biostimulants: research strategies for the selection of the best performing inocula. Agronomy-Basel. 2020;10(1):106. https://doi.org/10.3390/agronomy10010106.
View Article
Google Scholar

[230] View Article

[231] Google Scholar

[ref69] 69. Vázquez MM, César S, Azcón R, and Barea JM. Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Applied Soil Ecology. 2000;15(3):261–272. https://doi.org/10.1016/s0929-1393(00)00075-5
View Article
Google Scholar

[233] View Article

[234] Google Scholar

[ref70] 70. Larimer AL, Clay K, and Bever JD. Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. Ecological. 2014;95(4):1045–1054. https://doi.org/10.1890/13-0025.1 pmid:24933822
View Article
PubMed/NCBI
Google Scholar

[236] View Article

[237] PubMed/NCBI

[238] Google Scholar

[ref71] 71. Diagne N, Baudoin E, Svistoonoff S, Ouattara C, Diouf D, Kane A, et al. Effect of native and allochthonous arbuscular mycorrhizal fungi on Casuarina equisetifolia growth and its root bacterial community. Arid Land Res. Manage. 2017;32(2):212–228. https://doi.org/10.1080/15324982.2017.1406413.
View Article
Google Scholar

[240] View Article

[241] Google Scholar

[ref72] 72. Mortimer PE, Le Roux MR, Pérez-Fernández MA, Benedito VA, Kleinert A, Xu J, et al. The dual symbiosis between arbuscular mycorrhiza and nitrogen fixing bacteria benefits the growth and nutrition of the woody invasive legume Acacia cyclops under nutrient limiting conditions. Plant Soil. 2012;366(1–2):229–241. https://doi.org/10.1007/s11104-012-1421-2.
View Article
Google Scholar

[243] View Article

[244] Google Scholar

[ref73] 73. Linderman RG. Vesicular-arbuscular mycorrhizal (VAM) fungi. In Plant Relationships Part B. Springer, Berlin, Heidelberg; 1997: 117–128.

[ref74] 74. Bender SF, Schlaeppi K, Held A, and Van der Heijden MGA. Establishment success and crop growth effects of an arbuscular mycorrhizal fungus inoculated into Swiss corn fields. Agriculture Ecosystems & Environment. 2019;273:13–24. https://doi.org/10.1016/j.agee.2018.12.003.
View Article
Google Scholar

[247] View Article

[248] Google Scholar

[ref75] 75. Miransari M. Interactions between arbuscular mycorrhizal fungi and soil bacteria. Appl. Microbiol. Biotechnol. 2011;89(4):917–930. https://doi.org/10.1007/s00253-010-3004-6 pmid:21104242
View Article
PubMed/NCBI
Google Scholar

[250] View Article

[251] PubMed/NCBI

[252] Google Scholar

[ref76] 76. Niwa R, Koyama T, Sato T, Adachi K, Tawaraya K, Sato S, et al. Dissection of niche competition between introduced and indigenous arbuscular mycorrhizal fungi with respect to soybean yield responses. Sci. Rep-UK. 2018;8(1):7419. https://doi.org/10.1038/s41598-018-25701-4 pmid:29743529
View Article
PubMed/NCBI
Google Scholar

[254] View Article

[255] PubMed/NCBI

[256] Google Scholar

[ref77] 77. Hausmann NT and Hawkes CV. Order of plant host establishment alters the composition of arbuscular mycorrhizal communities. Ecology. 2010;91(8):2333–2343. https://doi.org/10.1890/09-0924.1 pmid:20836455
View Article
PubMed/NCBI
Google Scholar

[258] View Article

[259] PubMed/NCBI

[260] Google Scholar

[ref78] 78. Dąbrowska G, Baum C, Trejgell A, and Hrynkiewicz K. Impact of arbuscular mycorrhizal fungi on the growth and expression of gene encoding stress protein–metallothionein BnMT2 in the non‐host crop Brassica napus L. J. Plant Nutr. Soil Sci. 2014;177(3):459–467. https://doi.org/10.1002/jpln.201300115.
View Article
Google Scholar

[262] View Article

[263] Google Scholar

[ref79] 79. Rousk J, Demoling LA, Bahr A, and Baath E. Examining the fungal and bacterial niche overlap using selective inhibitors in soil. FEMS Microbiol. Ecol. 2008;63(3):350–358. https://doi.org/10.1111/j.1574-6941.2008.00440.x pmid:18205814
View Article
PubMed/NCBI
Google Scholar

[265] View Article

[266] PubMed/NCBI

[267] Google Scholar

[ref80] 80. de Boer W, Verheggen P, Klein Gunnewiek PJ, Kowalchuk GA, and van Veen JA. Microbial community composition affects soil fungistasis. Appl. Environ. Microbiol. 2003;69(2):835–44. https://doi.org/10.1128/AEM.69.2.835-844.2003 pmid:12571002
View Article
PubMed/NCBI
Google Scholar

[269] View Article

[270] PubMed/NCBI

[271] Google Scholar

[ref81] 81. Li X, Garbeva P, Liu X, Klein Gunnewiek PJA, Clocchiatti A, Hundscheid MPJ, et al. Volatile-mediated antagonism of soil bacterial communities against fungi. Environ. Microbiol. 2020;22(3):1025–1035. https://doi.org/10.1111/1462-2920.14808 pmid:31580006
View Article
PubMed/NCBI
Google Scholar

[273] View Article

[274] PubMed/NCBI

[275] Google Scholar

[ref82] 82. Biró B, Köves-Péchy K, Takács IVT, Eggenberger P, and Strasser. RJ. Interrelations between Azospirillum and Rhizobium nitrogen-fixers and arbuscular mycorrhizal fungi in the rhizosphere of alfalfa in sterile, AMF-free or normal soil conditions. Appl. Soil Ecol. 2000;15(2):159–168. https://doi.org/10.1016/s0929-1393(00)00092-5.
View Article
Google Scholar

[277] View Article

[278] Google Scholar

Figures

Abstract

Introduction

Materials and methods

Experiment treatments

Determinations of the root mycorrhizal colonization, biomass, and the accumulation of nitrogen and phosphorus

Calculation of effect size

Statistical analyses

Results

Root mycorrhizal colonization of four plant species under different microbial treatments

Biomass and its response ratio of four plant species under different microbial treatments

Nitrogen accumulation and its response ratio of four plant species under different microbial treatments

Phosphorous accumulation and its response ratio of four plant species under different microbial treatments

N/P ratio and its response ratio of four plant species under different microbial treatments

Discussion

AM fungi differently regulated the plant growth and nutrient accumulation

Indigenous microorganisms affected the benefits of AM fungi on plant growth and nutrient accumulation

Conclusions

Acknowledgments

References