Decoding microbial diversity in roots of rice plants under flooded conditions: influence of the host genotype, root compartment, and mycorrhizal association

Rice is a vital staple for more than half of the world’s population, uniquely adapted to grow under flooded conditions. Our current understanding of root-associated microbiomes in rice plants under flooded conditions (anaerobic rice) is, however, limited. While rice plants are capable of establishing symbiotic associations with arbuscular mycorrhizal (AM) fungi, also under flooded conditions, little is known about the impact that mycorrhizal associations might have on the root microbiome. Here, we used metagenomic sequencing to characterize the root-associated microbiomes of cultivated rice grown under flooded conditions. The root endosphere and rhizosphere compartments were found to harbor distinct microbial communities, with bacterial taxa comprising approximately 95% of the total microbial community. At the phylum level, the root bacteriome was primarily composed of Pseudomonadota (Alphaproteobacteria, Betaproteobacteria, and Gammaproteobacteria), followed by Actinomycetota. The fungal microbiome was dominated by Ascomycota (Sordariomycetes, Eurotiomycetes, and Dothideomycetes) and Basidiomycota. Both root compartment and host genotype significantly influenced microbiome composition, with most genotype-specific recruitment occurring at the species level. These associations were further reshaped in plants pre-inoculated with the AM fungus Rhizophagus irregularis . Co-occurrence networks revealed a genotype-dependent effect in the complexity of microbial taxa in mycorrhizal rice plants. Key microbial species primarily involved in methane production and nutrient cycling (e.g., phosphate-solubilizing bacteria and nitrogen-cycling bacteria) residing in roots of flooded rice were identified. Functional analysis of gene abundance related to those microbial communities revealed compartmentalization, with nutrient-cycling bacteria being more prevalent at the endosphere. Overall, this study demonstrated that the rice genotype, root compartment, and mycorrhizal condition shape the root microbiome in rice plants, ultimately influencing holobiont dynamics in flooded rice fields.

IMPORTANCE

Plant roots harbor a large diversity of microorganisms that strongly influence plant health and improve stress tolerance. Among them, root colonization by arbuscular mycorrhizal (AM) fungi enhances mineral nutrition and mitigates environmental stress. Although most rice cultivated worldwide is grown under anaerobic conditions (flooded fields), investigation of microbial communities inhabiting root-associated compartments of flooded rice, including AM fungi, has received only little attention. Here, we demonstrated that the rice genotype, root compartment, and mycorrhizal condition markedly influence the microbiome in roots of rice plants in flooded conditions, thus illustrating the potential of the rice plant to shape its root-associated microbiome. Differential root-associated microbiomes of commercial rice varieties include microbes primarily associated with methane production and nutrient cycling. Elucidation of factors influencing root-associated microbiomes in flooded rice systems, including their association with AM fungi, offers practical guidance for exploiting root-associated microbial communities for sustainable rice cultivation while reducing reliance on agrochemicals.