The functional structure of foxtail millet rhizoplane microbiome and its association with yield

Abstract

ABSTRACT Root-associated microbial communities profoundly influence plant growth and productivity. Although the rhizosphere microbiome has been extensively studied, the functional distinctiveness and host-specific role of the closely adhering rhizoplane microbiota remain unclear. In this study, we performed deep metagenomic sequencing of both the rhizosphere and rhizoplane microbiomes in foxtail millet (Setaria italica). We constructed a comprehensive non-redundant gene catalog, reconstructed 595 metagenome-assembled genomes (MAGs), and analyzed the co-occurrence networks. Our results revealed that the rhizoplane sustains a core microbial network with greater complexity and connectivity than rhizospheres. Metabolically, the rhizoplane microbiome is enriched in the functions underlying host adaptation, including ammonium production and polysaccharide decomposition. Our results showed that the associations between microbial features (taxonomic and functional) and yield were significantly stronger in the rhizoplane than in the rhizosphere. We identified 22 yield-positive MAGs, primarily from Bacillales, harboring genes for plant growth-promoting traits, such as nutrient solubilization and phytohormone synthesis. Collectively, our findings illustrate that the rhizoplane is not only a subset of the rhizosphere but also a critical host-microbe interface and functional hotspot where specialized microbial processes are directly coordinated to enhance plant performance and yield. IMPORTANCE Plant roots selectively recruit diverse and beneficial microorganisms from the surrounding soil, assembling a distinctive rhizosphere microbiome. Substantial research, primarily utilizing amplicon sequencing, has elucidated the taxonomic composition of these rhizosphere communities across a wide range of plant species. The functional architecture, assembly processes, and coexistence mechanisms of the rhizoplane microbiome remain poorly understood, and their link to host plant traits is unclear. We elucidate the taxonomic and functional structural disparities between the rhizosphere and rhizoplane microbiomes, thereby clarifying the composition and functional roles of the rhizoplane microbiome, and further examine the association between the rhizoplane microbiome and millet yield. A deeper understanding of root-associated microbial communities may inform the development of effective agricultural probiotics, thereby enhancing sustainable farming practices. Additionally, the candidate biomarkers identified in this work offer potential targets for improving cultivation practices and supporting the long-term agricultural sustainability of foxtail millet. Plant roots selectively recruit diverse and beneficial microorganisms from the surrounding soil, assembling a distinctive rhizosphere microbiome. Substantial research, primarily utilizing amplicon sequencing, has elucidated the taxonomic composition of these rhizosphere communities across a wide range of plant species. The functional architecture, assembly processes, and coexistence mechanisms of the rhizoplane microbiome remain poorly understood, and their link to host plant traits is unclear. We elucidate the taxonomic and functional structural disparities between the rhizosphere and rhizoplane microbiomes, thereby clarifying the composition and functional roles of the rhizoplane microbiome, and further examine the association between the rhizoplane microbiome and millet yield. A deeper understanding of root-associated microbial communities may inform the development of effective agricultural probiotics, thereby enhancing sustainable farming practices. Additionally, the candidate biomarkers identified in this work offer potential targets for improving cultivation practices and supporting the long-term agricultural sustainability of foxtail millet.