Plant developmental stage drives the differentiation in ecological role of the maize microbiome

Abstract

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.

Plant Growth Stage Drives the Temporal and Spatial Dynamics of the Bacterial Microbiome in the Rhizosphere of Vigna subterranea

“…Furthermore, plant rhizobacterial communities respond differently to plant developmental stages than bulk soil bacterial communities based on multiple microbial attributes implemented in this study, such as alpha and beta diversities, community structure, biomarker analysis, and pattern network analysis. Our findings are consistent with previous results showing that plant developmental stages shape the assembly of plant microbiomes (Chaparro et al, 2014;Qiao et al, 2017;Cordovez et al, 2021;Ma et al, 2021;Xiong et al, 2021a). This was similar to the report by Shi et al (2015) who observed that the growth of plants drove the succession of rhizobacteria in the rhizosphere of Avena fatua.…”

Seasonal Dynamics and Persistency of Endophyte Communities in Kalidium schrenkianum Shifts Under Radiation Stress

“… Gao et al (2020) demonstrated that stochastic forces act on fungal community assembly in the leaves and roots of sorghum during the early stages of development. Similarly, Xiong et al (2021) reported that in maize, fungal communities are more strongly driven by stochastic processes during the early stages of plant development, while bacterial communities at the later stages of development. Compared to annual crops like sorghum and maize, the community assembly patterns of perennial halophyte K .…”

Selection and Characterization of Burkholderia spp. for Their Plant-Growth Promoting Effects and Influence on Maize Seed Germination

“…These microorganisms can form complex interactions with plants and have key roles in promoting plant productivity and health (3,4). The plantbacteria interaction has been the basis of bioproducts that promote increased productivity of agricultural crops, especially inoculants with mechanisms that promote plant-growth, nutrient acquisition and increases of plant tolerance and resistance to abiotic stresses and pests attack (5)(6)(7). Most of these interactions occur in the soil-plant interface using specific niches such as the rhizosphere, endosphere and rhizoplane (1,2,8).…”