Deciphering how plant–microbiota interactions achieve beneficial outcomes for crops will provide innovative strategies for sustainable agriculture. Here, we dissected rice-microbiota dynamics using a tailored gnotobiotic cultivation system that models the semiaquatic environment in a paddy field. Inoculation with native soil microbiota resulted in root-growth-promotion (RGP) and root-growth-inhibition (RGI) phenomena in different cultivars. This preference persisted in a simplified synthetic community and individual bacterial strains, indicating that cultivar-specific growth promotion is an intrinsic property of microbial inocula. Though stochastic process dominated the assembly of root microbiome in gnotobiotic cultivation, absolute quantification revealed that imbalance of detrimental and beneficial bacterial loads in roots correlated with RGP or RGI outcomes in different rice cultivars. From the host perspective, genetic screening identified that receptor-like kinase mutants, including OsFLS2 (FLAGELLIN-SENSITIVE 2), inverted microbiota functionality, converting RGP to RGI. In particular, over 4534 rice genes responded to microbiota inoculation and 46.1% of them were reprogrammed in osfls2 mutants, demonstrating the prominent regulatory role of OsFLS2 in rice-microbiota signaling. On the basis of these results, we propose that the rice-microbiota relationships are gated by cultivar-specific preferences of the bacterial microbiota and host immune receptor kinase, which provides a useful framework for crop microbiome engineering in the future.
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