Abstract

BackgroundPlants live with diverse microbial communities which profoundly affect multiple facets of host performance, but if and how host development impacts the assembly, functions and microbial interactions of crop microbiomes are poorly understood. Here we examined both bacterial and fungal communities across soils, epiphytic and endophytic niches of leaf and root, and plastic leaf of fake plant (representing environment-originating microbes) at three developmental stages of maize at two contrasting sites, and further explored the potential function of phylloplane microbiomes based on metagenomics.ResultsOur results suggested that plant developmental stage had a much stronger influence on the microbial diversity, composition and interkingdom networks in plant compartments than in soils, with the strongest effect in the phylloplane. Phylloplane microbiomes were co-shaped by both plant growth and seasonal environmental factors, with the air (represented by fake plants) as its important source. Further, we found that bacterial communities in plant compartments were more strongly driven by deterministic processes at the early stage but a similar pattern was for fungal communities at the late stage. Moreover, bacterial taxa played a more important role in microbial interkingdom network and crop yield prediction at the early stage, while fungal taxa did so at the late stage. Metagenomic analyses further indicated that phylloplane microbiomes possessed higher functional diversity at the early stage than the late stage, with functional genes related to nutrient provision enriched at the early stage and N assimilation and C degradation enriched at the late stage. Coincidently, more abundant beneficial bacterial taxa like Actinobacteria, Burkholderiaceae and Rhizobiaceae in plant microbiomes were observed at the early stage, but more saprophytic fungi at the late stage.ConclusionsOur results suggest that host developmental stage profoundly influences plant microbiome assembly and functions, and the bacterial and fungal microbiomes take a differentiated ecological role at different stages of plant development. This study provides empirical evidence for host exerting strong effect on plant microbiomes by deterministic selection during plant growth and development. These findings have implications for the development of future tools to manipulate microbiome for sustainable increase in primary productivity.2NpR2QgL41qVHhBsXo3pXwVideo

Highlights

  • Plants live with diverse microbial communities which profoundly affect multiple facets of host perfor‐ mance, but if and how host development impacts the assembly, functions and microbial interactions of crop micro‐ biomes are poorly understood

  • Regression analysis based on beta-diversity partitioning further showed that species turnover drove the temporal changes in community composition, and plant developmental stage had the strongest effect on microbial communities in the phylloplane (Fig. S3)

  • By examining the temporal dynamics of bacterial and fungal communities across soils, multiple plant compartments and fake plant phylloplane at two geographically distant sites, this study provides a systematic understanding on the succession of microbiome composition and their potential functions during plant development

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Summary

Introduction

Plants live with diverse microbial communities which profoundly affect multiple facets of host perfor‐ mance, but if and how host development impacts the assembly, functions and microbial interactions of crop micro‐ biomes are poorly understood. We examined both bacterial and fungal communities across soils, epiphytic and endophytic niches of leaf and root, and plastic leaf of fake plant (representing environment-originating microbes) at three developmental stages of maize at two contrasting sites, and further explored the potential function of phyllo‐ plane microbiomes based on metagenomics. We still lack a comprehensive understanding on the mechanisms of microbiome assembly along with plant developmental stage in field, across the soil– plant continuum in which microbiomes are interactively influenced by multiple host and environmental factors like climate, edaphic factors and fertilization regimes

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