Résumé
The rhizosheath, a cohesive soil layer firmly adhering to plant roots, plays a vital role in facilitating water and mineral uptake. Using genome wide association (GWAS) combined with bulk segregant analysis and gene expression studies in pearl millet, rhizosheath formation was shown to be under complex genetic control in pearl millet and suggests that it is mainly regulated by root exudation. We investigated the impact of root exudates on the microbiota composition, interactions, and assembly processes, and rhizosheath structure in pearl millet using four distinct lines with contrasting soil aggregation abilities. Utilizing 16S rRNA gene and ITS metabarcoding for microbiota profiling, coupled with FTICR-MS metabonomic analysis of metabolite composition in distinct plant compartments and root exudates, we revealed substantial disparities in microbial diversity and interaction networks. The ß-NTI analysis highlighted bacterial rhizosphere turnover driven primarily by deterministic processes, showcasing prevalent homogeneous selection in root tissue (RT) and root-adhering soil (RAS). Conversely, fungal communities were more influenced by stochastic processes. In bulk soil assembly, a combination of deterministic and stochastic mechanisms shapes composition, with deterministic factors exerting a more pronounced role. Metabolic profiles across shoots, RT, and RAS in different pearl millet lines mirrored their soil aggregation levels, emphasizing the impact of inherent plant traits on microbiota composition and unique metabolic profiles in RT and exudates. Notably, exclusive presence of antimicrobial compounds, including DIMBOA and H-DIMBOA, emerged in root exudates and RT of low aggregation lines. Moreover, using a conceptual model and data from the two carbon isotopes’ measurements, we evidenced a priming effect for all pearl millet lines. Importantly, the priming effect amplitude (Clost =Cnew ratio) was higher for the low-aggregating lines than for the high-aggregating ones, indicating a better C sequestration potential of the latter.These findings underscore the interconnectedness of root exudates and microbiota, which jointly shape rhizosheath structure, deepening insights into soil-plant-microbe interactions and ecological processes shaping rhizosphere microbial communities. Deciphering plant-microbe interactions and their contribution to soil aggregation and microbiota dynamics holds promise for carbon storage in soils.