Unraveling the interplay between root exudates, microbiota, and rhizosheath formation in pearl millet

Abstract

Background The rhizosheath, a cohesive soil layer firmly adhering to plant roots, plays a vital role in facilitating water and mineral uptake. In pearl millet, rhizosheath formation is genetically controlled and influenced by root exudates. Here, 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. Results 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. Conclusions This research underscores the pivotal influence of root exudates in shaping the root-associated microbiota composition across pearl millet lines, entwined with their soil aggregation capacities. 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 the advancement of sustainable agricultural strategies.

Insights into Bacterial Extracellular Vesicle Biogenesis, Functions, and Implications in Plant–Microbe Interactions

“…Root exudates play an important role in the interaction with soil microorganisms [ 6 ]. Notably, the communication between plants and microorganisms involves a complex web of interactions, with root exudates playing a crucial role in shaping the microbial community [ 7 , 8 ]. Alahmad et al [ 8 ] demonstrated a connection between root exudates, microbial community composition, assembly processes, and co-occurrence networks in the rhizosphere of pearl millet (PM) lines.…”

“…Notably, the communication between plants and microorganisms involves a complex web of interactions, with root exudates playing a crucial role in shaping the microbial community [ 7 , 8 ]. Alahmad et al [ 8 ] demonstrated a connection between root exudates, microbial community composition, assembly processes, and co-occurrence networks in the rhizosphere of pearl millet (PM) lines. They utilized an in situ untargeted metabonomic approach, offering comprehensive insights into the metabolic profiles associated with various compartments of pearl millet and their implications for plant–microbe interactions.…”