Plant microbiomes are essential to host health and productivity but the ecological processes that govern crop microbiome assembly are not fully known. Here we examined bacterial communities across 684 samples from soils (rhizosphere and bulk soil) and multiple compartment niches (rhizoplane, root endosphere, phylloplane, and leaf endosphere) in maize (Zea mays)-wheat (Triticum aestivum)/barley (Hordeum vulgare) rotation system under different fertilization practices at two contrasting sites. Our results demonstrate that microbiome assembly along the soil-plant continuum is shaped predominantly by compartment niche and host species rather than by site or fertilization practice. From soils to epiphytes to endophytes, host selection pressure sequentially increased and bacterial diversity and network complexity consequently reduced, with the strongest host effect in leaf endosphere. Source tracking indicates that crop microbiome is mainly derived from soils and gradually enriched and filtered at different plant compartment niches. Moreover, crop microbiomes were dominated by a few dominant taxa (c. 0.5% of bacterial phylotypes), with bacilli identified as the important biomarker taxa for wheat and barley and Methylobacteriaceae for maize. Our work provides comprehensive empirical evidence on host selection, potential sources and enrichment processes for crop microbiome assembly, and has important implications for future crop management and manipulation of crop microbiome for sustainable agriculture.

Background Plants 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. Results Our 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. Conclusions Our 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.