INTRODUCTION: Endophytic fungi are essential microorganisms in promoting plant health. However, the mechanism of endophytic fungi regulating root microbiota to enhance crop production and resistance remains unclear. OBJECTIVES: We aimed i) to explore the microbial alteration driven by endophytic Acrocalymma vagum in developing crop yield and rice resistance
ii) to reveal the mechanism of root-released compound stimulated by A. vagum in recruiting benefit microbes. METHODS: The microbiome was applied in a culture-dependent and culture-independent method to study the microbial communities of the A. vagum-rice holobiont using 16S rRNA and ITS gene metabarcoding. Non-target metabolome identified distinct metabolites responsible for community variations. Label-free proteomic analyses investigated the association between primary genes related to the holobiont formation. CRISPR/Cas9 technique and homologous recombination replacement were used to characterize the functions of putative genes. RESULTS: A. vagum enhanced cultivated rice yield by 5.73 ± 1.76 % and induced 83.24 ± 9.86 % control efficiency against rice blast. We discovered that A. vagum simplified rice microbial structure based on co-occurrence networks, by lowering the proportion of potentially pathogenic predominant Burkholderia and driving rice to recruit beneficial Lactobacillus, Sarocladium and Nigrospora to promote rice growth with the increases of 44.41 ± 5.10 % shoot height and 70.21 ± 9.57 % shoot biomass. Moreover, the holobiont released coumaric and trans-ferulic acids to attract beneficial microbes. 206 rice proteins were notably up-regulated in the holobiont, particularly the OsPrxs. CRISPR/Cas9-edited mutants of OsPRX70 and OsPRX95 reduced the promotion effect of A. vagum on rice growth. Furthermore, the pathways of 39 overexpressed proteins in A. vagum were enriched in invading the host and inducing resistance. The knockouts of AvGH3, AvGH7, AvMFS1, and AvCBA transformed A. vagum role from endophyte to pathogen. CONCLUSIONS: The A. vagum-rice holobiont releases recruitment signals and improves the rice community structure. We provide ecological and molecular evidence to confirm the mutualism of endophyte-plant-promoting growth and disease resistance.