Genetic and environmental factors collectively determine plant growth and yield. In the past 20 years, genome-wide association studies (GWAS) have been conducted on crops to decipher genetic loci that contribute to growth and yield, however, plant genotype appears to be insufficient to explain the trait variations. Here, we unravel the associations between genotypic, phenotypic, and rhizoplane microbiota variables of 827 foxtail millet cultivars by an integrated GWAS, microbiome-wide association studies (MWAS) and microbiome genome-wide association studies (mGWAS) method. We identify 257 rhizoplane microbial biomarkers associated with six key agronomic traits and validated the microbial-mediated growth effects on foxtail millet using marker strains isolated from the field. The rhizoplane microbiota composition is mainly driven by variations in plant genes related to immunity, metabolites, hormone signaling and nutrient uptake. Among these, the host immune gene FLS2 and transcription factor bHLH35 are widely associated with the microbial taxa of the rhizoplane. We further uncover a plant genotype-microbiota interaction network that contributes to phenotype plasticity. The microbial-mediated growth effects on foxtail millet are dependent on the host genotype, suggesting that precision microbiome management could be used to engineer high-yielding cultivars in agriculture systems.

Background The medicinal material quality of Citrus reticulata ‘Chachi’ differs depending on the bioactive components influenced by the planting area. Environmental factors, such as soil nutrients, the plant-associated microbiome and climatic conditions, play important roles in the accumulation of bioactive components in citrus. However, how these environmental factors mediate the production of bioactive components of medicinal plants remains understudied. Results Here, a multi-omics approach was used to clarify the role of environmental factors such as soil nutrients and the root-associated microbiome on the accumulation of monoterpenes in the peel of C. reticulata ‘Chachi’ procured from core (geo-authentic product region) and non-core (non-geo-authentic product region) geographical regions. The soil environment (high salinity, Mg, Mn and K) enhanced the monoterpene content by promoting the expression of salt stress-responsive genes and terpene backbone synthase in the host plants from the core region. The microbial effects on the monoterpene accumulation of citrus from the core region were further verified by synthetic community (SynCom) experiments. Rhizosphere microorganisms activated terpene synthesis and promoted monoterpene accumulation through interactions with the host immune system. Endophyte microorganisms derived from soil with the potential for terpene synthesis might enhance monoterpene accumulation in citrus by providing precursors of monoterpenes. Conclusions Overall, this study demonstrated that both soil properties and the soil microbiome impacted monoterpene production in citrus peel, thus providing an essential basis for increasing fruit quality via reasonable fertilization and precision microbiota management.

The quality of Chinese medicinal materials depends on the content of bioactive components, which are affected by the environmental factors of different planting regions. In this research, integrated analysis of the transcriptome and metabolome of C. reticulata ‘Chachi’ was performed in two regions, and three orchards were included in the analysis. In total, only 192 compounds were found in fresh peels, and among 18 differentially accumulated flavonoid metabolites, 15 flavonoids were enriched in peels from the Xinhui planting region. In total, 1228 genes were up-regulated in peels from Xinhui, including the CHS and GST genes, which are involved in the salt stress response. Overall, based on the correlation analysis of flavonoid content and gene expression in peels of C. reticulata ‘Chachi’, we concluded that the authenticity of the GCRP from Xinhui may be closely related to the higher content of naringin and narirutin, and the increase in the content of these may be due to the highly saline environment of the Xinhui region.

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