Foliar application of indole-3-acetic acid drives changes of soil fungal communities in endosphere and rhizosphere of Eucommia ulmoides

doi:10.21203/rs.3.rs-4948411/v1

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Foliar application of indole-3-acetic acid drives changes of soil fungal communities in endosphere and rhizosphere of Eucommia ulmoides

https://doi.org/10.21203/rs.3.rs-4948411/v1

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Aims: Eucommia ulmoides is a valuable tree species endemic to China. However, the limited scale and low prevalence of quality seed resources, coupled with their slow growth and low utilization rate, continue to result in a scenario where supply falls short of demand. Growth hormone plays an important role in the growth and development of plants, notably enhancing the rooting rate of E. ulmoides.

Methods: In this study, based on high-throughput sequencing technology and controlled pot experiments, to assess the influence on the endosphere and rhizosphere fungal communities, the impact of varying concentrations of indole-3-acetic acid (IAA) on the foliar application of E. ulmoides were explored.

Results: The results revealed that the application of IAA significantly altered the composition, diversity and functionality of the fungal communities within the endosphereand rhizosphere of E. ulmoides. The most pronounced effects were observed at an IAA concentration of 1000 µM, with a more substantial impact on the rhizosphere fungi compared to those in the endosphere fungi. Futhermore, the application of IAA significantly increased the abundance of beneficial fungi in the endosphere, which are crucial for the growth and health of E. ulmoides.

Conclusions: This study revealed that the foliar spray of IAA could significantly drived the change of fungal community composition in the rhizosphere and endosphere of E. ulmoides, and increased the beneficial functional microbiota. This study offers novel insights into efficient and sustainable agricultural practices from a microbiological perspective.

Plant hormone

plant fungi

fungal community

fungal abundance

IAA

The rhizosphere constitutes a multifaceted physicochemical microdomain at the interface of plant roots and soil, serving as the primary ecological niche for plant-microbe and microbe-microbe interactions. It is profoundly influenced by the architecture and activities of the root system (Wang et al. 2021). The rhizosphere microbiota refers to a distinctive community closely associated with plant roots. Through the secretion of organic compounds, plants selectively attract and recruit microorganisms from the surrounding soil aggregates. The endosphere denotes the internal tissues, organs, and intercellular spaces of plant roots housing microorganisms that are wholly or partly viable and non-pathogenic (endophytes) ༈Liu et al. 2022༉, endophytes play a crucial role in plant microecology, significantly influencing the metabolism of host plants. They promote plant growth, enhance stress resistance, and ultimately improve crop yields ༈Lundberg et al. 2012; Chen et al. 2021༉. After enriching the soil microorganisms, they inhabit the rhizosphere and endosphere of plants in parasitic, symbiotic, and epiphytic forms. They actively contribute to plant growth and development by releasing plant hormones and volatile substances. These substances can influence plant immunity, regulate plant development and morphology, aid in nutrient absorption, and protect plants from pathogenic bacteria. Moreover, they play a vital role in helping plants withstand various stresses and adversities ༈Berendsen et al. 2012; Ge et al. 2019༉. Although rhizosphere and endosphere microorganisms have numerous effects on plants, their artificial regulation remains challenging. This study aims to offer insights into regulating plant rhizosphere and endosphere microorganisms through the perspective of hormones, providing a valuable reference for future research.

Indole-3-acetic acid (IAA) is one of the most extensively studied mobile auxins, primarily synthesized from tryptophan through indole-3-pyruvic acid derivatization (Mashiguchi et al. 2011). In addition to its role in regulating host signaling molecules and controlling various physiological responses, IAA also serves as a crucial microbial signal in microbe-host interactions. For instance, IAA acts as a signaling molecule that modulates the expression of genes in plant pathogens, directly influencing pathogen virulence and thereby enhancing plant health ༈Cheng et al. 2006; Cheng et al. 2007; Davies 2010; Kunkel and Johnson 2021༉. Arabidopsis thaliana mutants with defective auxin signaling pathways are more susceptible to necrotrophic fungi such as Plectosphaerella cucumerina and Botrytis cinerea ༈Han and Kahmann 2019༉. IAA is primarily synthesized in young bud tissues. Under gravity induction, it is transported over long distances from the upper end of morphology to underground tissues or other functional sites through active transporter proteins in the vascular system, facilitating information signal transmission to ensure the spatial and temporal coordination of organ growth and development ༈Boursiac et al. 2013; Lacombe and Achard 2016; Park et al. 2017; Vandenbrink and Kiss 2019༉.

Eucommia ulmoides Oliver is a perennial deciduous tree belonging to the family Eucommiaceae and genus Eucommia. It is a relict plant from the Tertiary period of China and has been listed in the second-class protected plant list of China due to its national significance (Gao et al. 2021; Xiang et al. 2024). E. ulmoides is a unique and valuable medicinal and oil-bearing tree species native to China. Its bark, seeds, flowers and other parts contain a variety of active ingredients, with a variety of effective components with pharmacological effects such as lowering blood lipids, preventing osteoporosis, and anti-tumor properties. Extracted gutta-percha is widely used in the rubber industry, contributing significantly to pharmaceuticals, health products, food, and various industrial applications, thereby holding substantial economic value ༈Duan et al. 2024; Suzuki et al. 2012; Wang et al. 2017; Liu et al. 2020; Xiang et al. 2024༉. However, due to the fact that it takes 15 ~ 20 years for E. ulmoides to mature and be harvested for medicinal purposes, demand has outstripped supply in recent years, and long-term overexploitation has led to a growing scarcity of E. ulmoides resources in China ༈Yao et al. 2012; Wang et al. 2017༉. Currently, foliar spraying is predominantly used in agriculture. Given that E. ulmoides is a species that thrives in strong sunlight and is not suitable for dense afforestation, foliar application from E. ulmoides is chosen to reduce costs and enhance efficiency ༈Ghani et al. 2022; Yadav et al. 2022; Tavan et al. 2024༉.

In this study, various concentrations of the exogenous hormone IAA were applied to the foliar surface of E. ulmoides to investigate their effects on fungal communities in the rhizosphere and endosphere niches of the plant. The aim was to explore the potential for promoting the growth of E. ulmoides through microbial perspectives and to provide a theoretical basis for effective tree fertilization and sustainable agricultural development.

Potting soil collection

Soil samples were collected from Guizhou University in Guiyang City, Guizhou Province, China (N 26°44', E 106°67'). Guiyang City is situated at the watershed between the Pearl River and Yangtze River, characterized by a subtropical humid and moderate climate with no severe summer heat or winter cold, which is conducive to plant growth. The soil was sourced from the yellow-brown soil layer beneath a Pinus massoniana forest. Prior to potting, the soil was thoroughly mixed after removing surface impurities such as plant litter, small stones and plant roots.

Plant pot experiments

In this study, a pot experiment was conducted to investigate the impact of different concentrations of indole-3-acetic acid (IAA) on the rhizosphere and endosphere fungal communities associated with E. ulmoides. The experiment included three concentration levels of IAA: 10 µM, 100 µM, and 1000 µM, alongside a blank control group, with three replicates per treatment. In April 2023, 2 kg of pre-mixed soil was placed in plastic pots, and each pot was sown with 5 surface-sterilized seeds of E. ulmoides (Huazhong 8), which had undergone a germination promotion treatment following a 2-minute soak in 75% alcohol. A total of 48 pots were sown to ensure there were enough seedlings with consistent growth for hormone spraying. Once the E. ulmoides seedlings developed cotyledons, 3 healthy and well-growing seedlings were retained per pot, while 2 seedlings with poorer growth were removed. To protect the seedlings from rainwater, white plastic sheds were erected over them in an open field setting. Soil moisture levels were maintained by adjusting with sterile water to ensure optimal growth conditions for each pot of seedlings. Natural ambient temperature was maintained throughout the experiment, and no external carbon sources were introduced. By May 2023, when the E. ulmoides seedlings reached four weeks of age, 36 pots showing uniform growth were randomly assigned to four groups: a blank control (CK) and three treatment groups (10 µM IAA, 100 µM IAA, and 1000 µM IAA). Each group consisted of 3 pots for subsequent analysis. Referring to the described method (Gupta et al. 2022) for preparing the required hormone aqueous solution, first dissolve the plant hormone in a small amount of NaOH solution, and then dilute it to the desired concentration with water, and add Tween 20 (100 µl L^− 1). The blank control plants were treated with a NaOH solution containing Tween 20. Using a sprayer, 15 mL of hormone solution was evenly sprayed onto the leaves of 3 E. ulmoides seedlings in each pot once a week for 8 weeks. At the conclusion of the experiment, rhizosphere and endosphere soil samples from each treatment replicate were collected, thoroughly mixed, and stored at -80°C for total DNA extraction.

DNA extraction, general amplification, and high-throughput sequencing

Total DNA was extracted from 0.5 g rhizosphere soil samples and root samples using the FastDNA® SPIN Kit for Soil, following standard manufacturer's procedures. The concentration and purity of DNA were assessed using a Nanodrop 2000 UV-Vis spectrophotometer (Thermo Fisher Scientific) and by electrophoresis in a 1% (w/v) agarose gel. DNA samples were then used to amplify the fungal internal transcribed spacer (ITS) region using primers ITS1F (Shao et al. 2024): 5'-CTTGGTCATTTAGAGGAAGTAA-3′ and ITS2: 5'-GCTGCGTTCTTCATCGATGC-3′. The PCR reaction conditions for amplifying the ITS region were as follows ༈Dong et al. 2024༉: initial denaturation at 95°C for 3 minutes, followed by denaturation at 95°C for 30 seconds, annealing at 55°C for 30 seconds, extension at 72°C for 30 seconds, single extension at 72°C for 10 minutes, and storage at 4°C. The PCR products obtained were sent to Biomarker Technologies Co., Beijing, China for high-throughput amplicon sequencing using the Illumina NovaSeq 6000 platform (Illumina, Santiago CA, USA).

Data Analysis

Raw data processing

With the assistance of DADA2 in Qiime2 (2020.6) software, all original sequences obtained through high-throughput sequencing underwent quality control, denoising, splicing, and removal of chimeric sequences. Subsequently, amplicon sequence variants (ASVs) were generated, representing 0.005% of the total sequenced sequences (Callahan et al. 2016). The sequence data has been deposited into the NCBI Sequence Read Archive (SRA) database under the BioProject accession number PRJNA1129317. Using UNITE (Release 8.0) as the reference database, fungal ASVs were classified and annotated with a confidence threshold of 70%.

Community composition and function analysis

A total of 12 samples were analyzed at the genus classification level, encompassing both a control group and a group treated with three concentrations of IAA (10 µM, 100 µM, and 1000 µM). Samples were categorized into two groups: endosphere and rhizosphere soil. Each group included the control (CK) and the aforementioned IAA treatments. Subsequently, Origin 2021 software was utilized to create histograms depicting community composition, enabling the analysis of fungal community structure and functional differences within the rhizosphere and endosphere niches of E. ulmoides across the three concentrations. The fungal community abundance data for each sample group represent the mean values derived from both the control group and the three IAA concentrations.

In this study, fungal communities from 12 samples were analyzed across various ecological guilds using the FUNGuild database (https://github.com/UMNFuN/FUNGuild). A histogram depicting the ecological function composition of these fungal communities was generated based on the relative abundance of each guild, using OmicStudio tools (https://www.omicstudio.cn/tool). Additionally, Origin 2021 and the Tutu Cloud Platform (cloudtutu.com.cn) were employed to create a total functional column chart and Principal Coordinates Analysis (PCoA) plot, respectively.

Linear discriminant analysis

Linear discriminant analysis (LEfSe) was conducted using the Galaxy platform (https://huttenhower.sph.harvard.edu/galaxy/) to identify differential fungal taxa that characterized the fungal communities within the endosphere and rhizosphere niches of E. ulmoides across different treatment groups. The analysis utilized the nonparametric Kruskal-Wallis rank-sum test to detect species with significant abundance differences between these groups. Subsequently, the Wilcoxon rank-sum test was employed to assess the consistency of these differentially abundant species within each subgroup. Finally, LEfSe was used to estimate the impact of these differential species, with a filter value (LDA score) set to 2.5 in this study.

Results and Analysis

Effects of IAA foliar sprays on fungal community diversity in the underground niche of E. ulmoides

Through ITS gene deep sequencing, a total of 6451 ASVs were identified across 12 rhizosphere soil samples of E. ulmoides, representing taxa from 13 phyla, 36 classes, 73 orders, 137 families, 210 genera, and 262 species. Similarly, 26280 ASVs were detected in 12 endosphere samples, encompassing taxa from 16 phyla, 47 classes, 106 orders, 217 families, 421 genera, and 582 species. The impact of foliar IAA spray on fungal community diversity in both rhizosphere and endosphere niches of E. ulmoides was analyzed using the ACE richness index (Fig. 1).

Results indicated that the influence of IAA treatment on fungal community diversity in both rhizosphere and endosphere niches was not statistically significant, although there was an increasing trend in fungal diversity with higher hormone concentrations (Fig. 1A). For instance, the ACE index for rhizosphere fungal communities of E. ulmoides in the 10 µM, 100 µM, and 1000 µM IAA treatment groups were 427.77, 502.26, and 560.70, respectively. In the endosphere samples of E. ulmoides, the ACE index in these treatment groups were 1969.04, 1913.90, and 2100.18, respectively, indicating a dose-dependent effect of IAA on fungal diversity.

Furthermore, the study revealed that fungal community diversity in the endosphere of E. ulmoides was significantly higher than that in the rhizosphere fungal communities across both control and IAA treatment groups (Fig. 1B).

Effect of IAA foliar sprays on fungal community composition in the underground niche of E. ulmoides

In the rhizosphere niche of E. ulmoides (Fig. 2A), the dominant fungal community in the control group was Galactomyces (15.60%). Foliar application of IAA would affect the composition of the rhizosphere fungal community of E. ulmoides, with greater changes observed at higher hormone concentrations. Specifically, in the 10 µM IAA treatment group, Galactomyces remains the dominant genus in the rhizosphere fungal community, but its relative abundance shifts to 18.26%. In the 100 µM IAA treatment group, the dominant genus in the rhizosphere fungal community shifts to an unclassified genus of Fungi, with a relative abundance of 26.58%. Similarly, in the 1000 µM IAA treatment group, the rhizosphere fungal community is dominated by unclassified of Fungi (15.35%), all of which were low-abundance genera in the control group.

In the endosphere niche (Fig. 2B), foliar application of IAA had minimal effect on fungal community composition. For instance, Fusarium exhibited a relative abundance of 3.28% in the control group, and with 10 µM IAA, 100 µM IAA, and 1000 µM IAA treatments, it showed relative abundances of 4.31%, 2.74%, and 3.47% respectively, with no significant changes observed. Overall, the foliar application of IAA had little impact on the fungal community composition in the endosphere niche.

Effects of IAA foliar sprays on fungal community function in the underground niche of E. ulmoides

Based on the FUNGuild platform, 67 and 77 ecological functional groups were identified by annotating fungal communities in the rhizosphere and endosphere niches of E. ulmoides, respectively. Both niches shared several functional groups, such as Arbuscular Mycorrhizal, Soil Saprotroph, Animal Pathogen, and Dung Saprotroph-Plant Saprotroph. Additionally, each niche harbored unique functional groups. Specifically, the rhizosphere niche had seven exclusive functional types, including Lichenized-Undefined Saprotroph, Endophyte-Plant Pathogen-Undefined Saprotroph, and Endophyte-Plant Pathogen. The endosphere niche similarly featured seven unique functional types, such as Dung Saprotroph-Endophyte, Dung Saprotroph-Endophyte-Undefined Saprotroph, and Ectomycorrhizal-Undefined Saprotroph (Fig. 3A).

Regardless of the rhizosphere or endosphere niche, the dominant functional type among fungal communities in the control treatment was Undefined Saprotroph. Results indicated that foliar application of IAA influenced fungal community functions in both rhizosphere and endosphere niches of E. ulmoides, with specific functional groups enriched across different IAA concentration treatments. For instance, under 100 µM IAA treatment, the rhizosphere niche showed enrichment in Animal Pathogen-Undefined Saprotroph (26.17%) and Soil Saprotroph (11.51%), while the endosphere niche was enriched in Arbuscular Mycorrhizal (18.81%) and Plant Pathogen (10.43%). Notably, under 1000 µM IAA treatment, differences in dominant functional groups like Plant Pathogen (7.69%) and Dung Saprotroph (5.55%) in the rhizosphere niche versus Arbuscular Mycorrhizal (28.98%) and Plant Pathogen (9.95%) in the endosphere niche were observed (Fig. 3B). The PCoA plot (Fig. 3C) illustrated distinctions in fungal community characteristics between rhizosphere and endosphere niches under 100 µM IAA treatment, while showing similar β diversity characteristics, suggesting functional similarity in fungal communities across both niches.

Comparison of the effects of IAA foliar sprays on the fungal communities in the rhizosphere and endosphere of E. ulmoides

Linear discriminant analysis (LDA) was employed to analyze the impact of different concentrations of IAA on fungal communities within the rhizosphere and endosphere of E. ulmoides. The study revealed higher specificity of fungal communities in the rhizosphere compared to the endosphere. Specifically, at the genus level, 13 fungal genera such as Aspergillus、Hemileucoglossum、unclassified of Helotiaceae、unclassified of Pseudeurotiaceae、Pseudaleuria、Teunomyces、Galactomyces、Pleiocarpon、Conlarium、Clavulina、Solicoccozyma、unclassified of Chytridiomycota、Entrophospora 13 fungal genera were significantly associated with the rhizosphere niche of E. ulmoides (Fig. 4A, C), whereas only Neofusicoccum, Tausonia, and one undefined genus correlated significantly with the endosphere niche (Fig. 4B, D). These findings indicate that foliar application of IAA had a more pronounced effect on rhizosphere fungal communities than on endosphere communities. The higher the LDA value, the greater the contribution to the differences between groups, indicating that this microbial group is a more important biomarker than other microorganisms. Under the control group and three different concentrations of IAA, the taxonomic compositions of fungal communities in the rhizosphere and endosphere niches of E. ulmoides showed significant differences. However, the number of taxa showing significant abundance differences was highest in the 1000 µM IAA concentration treatment group, regardless of whether in the rhizosphere or endosphere niches. Specifically, in the rhizosphere niche fungal community of the treatment group, there were 14 taxa with significant differences in abundance, includin 1 class (Pezizomycetes), 2 orders (Pezizales, Ohygenales), 3 families (Aspergillaceae, Mycosphaerellaceae, Piskurozymaceae), 4 genera (Aspergillus, Pseudaleuria, Solicoccozyma, unclassified of Helotiaceae) and three species (Aspergillus-versicolor, Candida-metapsilosis, unclassified of Helotiaceae, unidentified) (Fig. 4A, C). In the endosphere niche, the number of taxa with significant abundance differences in the fungal community was 8, including 1 class (Pucciniomycetes), 2 orders (Capnodiales, Septobasidiales), 1 family (Septobasidiaceae), 1 genus (Neofusicoccum) and 3 species (Setophoma-vemoniae, Neofusicoccum-italicum, Neosetophma-rosigene) (Fig. 4B, D).

The microbiome of medicinal plants is an important factor affecting plant health and productivity, making it a focal point in agricultural management practices and biotechnological advancements. Plant hormones, which regulate numerous physiological processes, significantly impact plant growth, development, and yield (Luo et al. 2016). Different concentrations of IAA exert varying effects on plants; for instance, increased IAA levels stimulate epinastic leaf growth in Arabidopsis, while deficiencies can lead to hyponastic leaves ༈Li et al. 2007༉. Similarly, our study observed shifts in fungal community compositions within the rhizosphere and endosphere niches of E. ulmoides under different IAA concentrations, revealing distinct variations with increasing concentrations across these niches. Stefano et al.༈2021༉ demonstrated significant alterations in the microbial composition of Solanum lycopersicum L. rhizosphere through exogenous hormone applications on the foliar surface. In our study, foliar IAA application exerted a greater influence on the fungal community composition in the rhizosphere compared to the endosphere niche of E. ulmoides. This effect is likely due to the direct entry of hormone residues from foliar sprays into the soil, influencing rhizosphere fungal taxa through osmosis. In contrast, the impact on endosphere microorganisms primarily occurs through plant-mediated IAA transport from leaves to roots. Furthermore, fungal community diversity was found to be higher in the endosphere of E. ulmoides than in the rhizosphere. This disparity may be attributed to the rhizosphere effect, where root exudates such as organic acids and sugars attract and promote the growth of certain fungi while inhibiting others, potentially reducing overall fungal diversity in the rhizosphere. Conversely, the endosphere provides a more stable environment less susceptible to external environmental fluctuations, thereby supporting a broader range of fungal species.

Rhizosphere and endosphere microorganisms have a variety of different functions and potential effects on plants. In this study, we observed that applying IAA to the foliar surface of E. ulmoides influenced the functional groups of microorganisms in both its rhizosphere and endosphere. Specifically, there was an increase in Undefined Saprophytes, Plant Pathogens, Arbuscular Mycorrhizal Fungi, Animal Pathogens, Ectomycorrhizal Fungi, and Soil Saprophytes. These findings are consistent with prior research on the effects of IAA application in similar contexts (Zhang et al. 2023; Dong et al. 2024; Shao et al. 2024). In this study, the abundance of beneficial microorganisms in the endosphere niche of E. ulmoides increased with higher concentrations of IAA. Specifically, Arbuscular Mycorrhizal Fungi were most prevalent at 1000 µM IAA. Mycorrhizal Fungi are well-known for forming symbiotic relationships with most terrestrial plants, aiding in water and nutrient uptake from soil, improving soil fertility, and enhancing plant growth ༈Sun et al. 2023༉. The research demonstrated that foliar application of IAA significantly boosted the population of beneficial microorganisms within the endosphere. This application also enhanced plant stress resistance and nutrient absorption to a certain extent, offering valuable insights for utilizing biological agents to stimulate tree growth in subsequent applications.

IAA is a crucial bioactive molecule in living organisms, exerting effects not only on plants themselves but also influencing plant-associated microorganisms. Recent studies have identified IAA as a pivotal plant hormone affecting the phytopathogenic fungi of E. ulmoides (Shao et al. 2024). The impact of exogenous auxins on plants is concentration-dependent; for instance, concentrations of 10 µM stimulate hypocotyl fragment elongation in Arabidopsis ༈Adamowski et al. 2019༉, whereas 5 nM inhibits root growth ༈Fendrych et al. 2018༉. During plant growth, roots secrete exudates comprising amino acids, vitamins, auxins, and organic acids (such as acetic acid), which recruit beneficial microorganisms to colonize and enhance plant development. Furthermore, aside from soil nutrient availability, root exudates also alter soil pH, influencing pathogenic bacteria and beneficial fungi ༈Vicente et al. 2020༉. This phenomenon elucidates why this study observed the highest number of enriched fungal differential groups when the applied exogenous auxin concentration was 1000 µM. Moreover, the transportation of IAA from the foliar surface to the root system via the vascular system increased auxin secretion in the roots, thereby altering the composition of the soil microbiome. Consequently, the impact of foliar application of IAA on the rhizosphere niche exceeded that on the endosphere niche.

This study revealed that the foliar spray of IAA could significantly drived the change of fungal community composition in the rhizosphere and endosphere of E. ulmoides, and increased the beneficial functional microbiota. The results provide a reference for the large-scale cultivation of E. ulmoides and the promotion of IAA production and utilization in agriculture field.

PCoA principal coordinate analysis

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

Funding

This work was supported by “Hundred” Talent Projects of Guizhou Province [Qian Ke He [2020]6005]; the National Natural Science Foundation of China [No. 32260003, 32360029, 32160007]; Construction Program of Biology First-class Discipline in Guizhou [GNYL[2017]009].

Author contributions

Keyun Song, Shenglv Lu and Qingsong Ran performed material preparation, data collection and analysis. Chunbo Dong, Yanwei Zhang and Yanfeng Han conceived the conception and design. Zhaoying He and Qiuyu Shao wrote and edited the paper. All authors read and approved the final manuscript.

Data Availability

The datasets generated during and/or analyzed during the current study are available in the NCBI Sequence Read Archive (SRA) database (BioProject: PRJNA1129317, https://www.ncbi.nlm.nih.gov/bioproject/PRJNA1129317)

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Foliar application of indole-3-acetic acid drives changes of soil fungal communities in endosphere and rhizosphere of Eucommia ulmoides

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Abstract

Figures

Introduction

Materials and methods

Potting soil collection

Plant pot experiments

DNA extraction, general amplification, and high-throughput sequencing

Data Analysis

Raw data processing

Community composition and function analysis

Linear discriminant analysis

Results and Analysis

Disscussion

Conclusions

Abbreviations

Declarations

Competing Interests

Funding

Author contributions

Data Availability

References

Status:

Version 1