Rare taxa maintain the stability of crop mycobiomes and ecosystem functions

Abstract

Plants harbour highly diverse mycobiomes which sustain essential functions for host health and productivity. However, ecological processes that govern the plant-mycobiome assembly, interactions and their impact on ecosystem functions remain poorly known. Here we characterized the ecological role and community assembly of both abundant and rare fungal taxa along the soil-plant continuums (rhizosphere, phyllosphere and endosphere) in the maize-wheat/barley rotation system under different fertilization practices at two contrasting sites. Our results indicate that mycobiome assembly is shaped predominantly by compartment niche and host species rather than by environmental factors. Moreover, crop-associated fungal communities are dominated by few abundant taxa mainly belonging to Sordariomycetes and Dothideomycetes, while the majority of diversity within mycobiomes are represented by rare taxa. For plant compartments, the abundant sub-community is mainly determined by stochastic processes. In contrast, the rare subcommunity is more sensitive to host selection and mainly governed by deterministic processes. Furthermore, our results demonstrate that rare taxa play an important role in fungal co-occurrence network and ecosystem functioning like crop yield and soil enzyme activities. These results significantly advance our understanding of crop mycobiome assembly and highlight the key role of rare taxa in sustaining the stability of crop mycobiomes and ecosystem functions.

Plant Developmental Stage Drives the Differentiation in Ecological Role of Plant Bacterial and Fungal Microbiomes

“…These ndings are consistent with previous studies showing that plant compartment is a determining factor shaping the assembly of plant-associated microbiomes [26][27][28][29]42], and that plant seasonal status has signi cant effects on microbiomes in grasses phyllosphere and Arabidopsis rhizosphere [32,71]. Further, metagenomic analysis in our study revealed that the functional diversity and enriched functional traits in the maize phylloplane varied across three stages.…”

“…To assess the relative importance of determinism and stochasticity in microbiome assembly, we calculated the beta Nearest Taxon Index (βNTI) using null model (999 randomizations) [59], and de ned |βNTI| ≥ 2 as dominant deterministic processes and |βNTI| < 2 as dominant stochastic processes [60,61] Microbial interkingdom network analysis at bacterial and fungal genus level was performed using the CoNet [62] in Cytoscape (v3.5) [63] based on Spearman correlation scores (Spearman's r > 0.7 or r < −0.7; P < 0.01). Both bacterial and fungal genera present in at least 10 samples were retained for the network analysis [42]. The networks were visualized in Gephi [64].…”

“…Nonparametric statistical test (Kruskal-Wallis test or Wilcoxon test) was performed to evaluate the alpha-diversity difference and the taxonomical difference among different niches and stages. More information on the network analysis, random forest modeling analysis and source tracking analysis are detailed in our previous publication [29,42].…”

“…Sequencing was performed on the Illumina MiSeq platform with a Paired-End protocol. The raw sequences were quality-ltered using USEARCH (v10.0) [48] as previously described [29,42], and all correct biological reads (i.e. zero-radius operational taxonomic units, ZOTUs) were picked at 100% similarity using unoise3 command [49] with default parameters.…”

Disease-induced Changes in Plant Microbiome Assembly and Functional Adaptation

“…Total DNA was extracted from the aforementioned samples using the FastDNA SPIN Kit for Soil (MP Biomedicals, Solon, USA) following manufacturer's instructions. The V5-V6 region of bacterial 16S rRNA gene (799F-1115R) [14,51], and the ITS2 region (fITS7-ITS4) of fungal ITS [16,52,53] were ampli ed ( Table S1). The primers sequence and PCR ampli cations were shown in Table S1.…”