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

Abstract

BackgroundPlants live with diverse microbial communities which profoundly affect multiple facets of host performance such as nutrition acquisition, disease suppression and productivity, 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 (rhizosphere and bulk soil), plant epiphytic and endophytic niches (phylloplane, rhizoplane, leaf and root endosphere), 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 compartment niches than in soils, with the strongest effect in the phylloplane. Air (represented by fake plants) was an important source of phylloplane microbiomes which were co-shaped by both plant development and seasonal environmental factors. Further, we demonstrated that bacterial and fungal communities in plant compartment niches exhibited contrasting response to host developmental stages, with higher alpha diversity and stronger deterministic assembly within bacterial microbiomes at the early stage but a similar pattern within mycobiomes at the late stage. Moreover, we found that 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 and functional genes involved in nutrient provision and disease resistance at the early stage than 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 plant development stages. This study provides empirical evidence for host exerting strong effect on plant microbiomes by deterministic selection to meet the physiological requirement of plant developmental stages. These findings have implications for the development of future tools to manipulate microbiome for sustainable increase in primary productivity.

Plant selection and ecological microhabitat drive domestications of shrub-associated microbiomes in a revegetated shrub ecosystem

“…In the results, the pattern of niche driving to microbial was supported by some studies on crops (Xiong et al, 2021a, b) and wild plants (Cregger et al, 2018; Zheng and Gong, 2019; Wang et al, 2022) from local to regional areas. However, recent studies have shown that fungal compositional variance is better predicted by sampled sites than by microhabitats in regional areas (Bernard et al, 2021; Thiergart et al, 2020).…”

“…S5), further indicating that the rhizosphere act as a hotspot of plant-microbe-soil interactions. However, another study found that plant bacterial communities are gradually filtered and enriched from bulk soils to plant niches (Xiong et al, 2021b). This could be primarily attributed to the harsher soil conditions (low nutrients and soil moisture) in the root zone and bulk soil than in the rhizosphere in the desert ecosystem.…”

“…SourceTracker, based on Bayesian approach, was performed to evaluate the source of the plant microbial communities in each habitat (Knights et al, 2011; Xiong et al, 2021b). To further support the microbial source analysis, nestedness analysis was performed.…”

The effects of ectomycorrhizal and saprotropic fungi on soil nitrogen mineralization differ from those of arbuscular and ericoid mycorrhizal fungi on the eastern Qinghai-Tibetan Plateau

“…DNA was extracted from 0.25 g of each soil sample by using the PowerSoil ® Kit(100) and the concentration of extracted DNA was then determined by a NanoDrop 1000 spectrophotometer. Soil fungi were amplified fungal ITS2region and selected primers pairs fITS7 (5’- GTGARTCATCGAATCTTTG-3’) and ITS4 (5’-AGCCTCCGCTTATTGATATGCTTAART-3’) ( Xiong et al., 2021 ). The 25 μL PCR reaction mixture contained 8.5 μL of sterile deionized water, 0.75 μL of each primer, 12.5 μL of KAPA Polymerase and 2.5 μL of diluted template DNA.…”

Water and Carbon Dynamics, Ecosystem Stability of Forest and Grassland in Response to Climate Change

“…DNA was extracted from 0.25 g of each soil sample by using the PowerSoil ® Kit(100) and the concentration of extracted DNA was then determined by a NanoDrop 1000 spectrophotometer. Soil fungi were amplified fungal ITS2region and selected primers pairs fITS7 (5'-GTGARTCATCGAATCTTTG-3') and ITS4 (5'-AGCCTCCGCTTATTGATATGCTTAART-3') (Xiong et al, 2021). The 25 mL PCR reaction mixture contained 8.5 mL of sterile deionized water, 0.75 mL of each primer, 12.5 mL of KAPA Polymerase and 2.5 mL of diluted template DNA.…”