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

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. 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. 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. Video Abstract.

Xiong C ，Singh BK ，He JZ ，Han YL ，Li PP ，Wan LH ，Meng GZ ，Liu SY ，Wang JT ，Wu CF ，Ge AH ，Zhang LM ... -  《Microbiome》

Plant domestication shapes rhizosphere microbiome assembly and metabolic functions.

The rhizosphere microbiome, which is shaped by host genotypes, root exudates, and plant domestication, is crucial for sustaining agricultural plant growth. Despite its importance, how plant domestication builds up specific rhizosphere microbiomes and metabolic functions, as well as the importance of these affected rhizobiomes and relevant root exudates in maintaining plant growth, is not well understood. Here, we firstly investigated the rhizosphere bacterial and fungal communities of domestication and wild accessions of tetraploid wheat using amplicon sequencing (16S and ITS) after 9 years of domestication process at the main production sites in China. We then explored the ecological roles of root exudation in shaping rhizosphere microbiome functions by integrating metagenomics and metabolic genomics approaches. Furthermore, we established evident linkages between root morphology traits and keystone taxa based on microbial culture and plant inoculation experiments. Our results suggested that plant rhizosphere microbiomes were co-shaped by both host genotypes and domestication status. The wheat genomes contributed more variation in the microbial diversity and composition of rhizosphere bacterial communities than fungal communities, whereas plant domestication status exerted much stronger influences on the fungal communities. In terms of microbial interkingdom association networks, domestication destabilized microbial network and depleted the abundance of keystone fungal taxa. Moreover, we found that domestication shifted the rhizosphere microbiome from slow growing and fungi dominated to fast growing and bacteria dominated, thereby resulting in a shift from fungi-dominated membership with enrichment of carbon fixation genes to bacteria-dominated membership with enrichment of carbon degradation genes. Metagenomics analyses further indicated that wild cultivars of wheat possess higher microbial function diversity than domesticated cultivars. Notably, we found that wild cultivar is able to harness rhizosphere microorganism carrying N transformation (i.e., nitrification, denitrification) and P mineralization pathway, whereas rhizobiomes carrying inorganic N fixation, organic N ammonification, and inorganic P solubilization genes are recruited by the releasing of root exudates from domesticated wheat. More importantly, our metabolite-wide association study indicated that the contrasting functional roles of root exudates and the harnessed keystone microbial taxa with different nutrient acquisition strategies jointly determined the aboveground plant phenotypes. Furthermore, we observed that although domesticated and wild wheats recruited distinct microbial taxa and relevant functions, domestication-induced recruitment of keystone taxa led to a consistent growth regulation of root regardless of wheat domestication status. Our results indicate that plant domestication profoundly influences rhizosphere microbiome assembly and metabolic functions and provide evidence that host plants are able to harness a differentiated ecological role of root-associated keystone microbiomes through the release of root exudates to sustain belowground multi-nutrient cycles and plant growth. These findings provide valuable insights into the mechanisms underlying plant-microbiome interactions and how to harness the rhizosphere microbiome for crop improvement in sustainable agriculture. Video Abstract.

Yue H ，Yue W ，Jiao S ，Kim H ，Lee YH ，Wei G ，Song W ，Shu D ... -  《Microbiome》

Ecological Processes of Bacterial and Fungal Communities Associated with Typha orientalis Roots in Wetlands Were Distinct during Plant Development.

Wang L ，Liu J ，Zhang M ，Wu T ，Chai B ... -  《Microbiology Spectrum》

Microbial species pool-mediated diazotrophic community assembly in crop microbiomes during plant development.

Xiong C ，K Singh B ，Zhu Y-G ，Hu H-W ，Li P-P ，Han Y-L ，Han L-L ，Zhang Q-B ，Wang J-T ，Liu S-Y ，Wu C-F ，Ge A-H ，Zhang L-M ，He J-Z ... -  《mSystems》

Host selection shapes crop microbiome assembly and network complexity.

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.

Xiong C ，Zhu YG ，Wang JT ，Singh B ，Han LL ，Shen JP ，Li PP ，Wang GB ，Wu CF ，Ge AH ，Zhang LM ，He JZ ... -  《-》