Background: Endophytic fungi are essential members of the plant microbial community, which play a vital role in promoting plant growth and development, and inducing disease resistance. However, little is known about the ecological mechanisms of endophytic fungi impacting the root microbiota community to improve crop health.
Results: An endophytic fungus Acrocalymma vagum (Code A21) isolated from wild rice enhanced rice yield by 5.73% and induced resistance against rice blast with 83.24% control efficiency in the field. The root microbiota community variations were discovered through 16S and ITS metabarcoding methods. A. vagum simplified the complexity of the rice microbiome community, reducing the proportion of the dominant pathogens Burkholderia and Ralstonia, and driving rice to recruit beneficial bacteria (Aquabacterium, Flavobacterium, and Lactobacillus) and fungi (Rhizophagus, Sarocladium, and Nigrospora). The recruited microbes were enriched in nutrient synthesis and stress resistance, especially biosynthesis of lactate, vitamin B12, and thiazole. We further isolated and identified 279 bacteria and 82 fungi from the A. vagum-fertilized rice roots to confirm the probiotic's functions. Among them, 5 Lactobacillus strains and 2 Nigrospora strains possessed significantly inhibitive activity on rice blast pathogen Magnaporthe oryzae. Additionally, 3 fungal strains in Sarocladium and Nigrospora genera promoted rice growth. Mutualistic mechanisms of A. vagum-rice were uncovered by the LC-MS/MS-based label-free quantitative assay. 13 secretory proteins of A. vagum cooperated to evade the host immune response and stimulate the symbiont resistance, such as alkaline phosphatases (ALP) as specific marker enzymes to symbiosis with the host and glycoside hydrolases (GHs) as effectors to colonize the host. Correspondingly, 206 rice proteins were induced to up-regulate, especially families of peroxidase (OsPRX), copper transporter (OsCOPT), and glutathione S-transferase (OsGSTU) related to growth and stress resistance.
Conclusion: Our study verified that endophytic fungi isolated from wild rice had great practical value on cultivated rice. A. vagum reshaped the microbiota community of cultivated rice by enhancing host traits, as the first report of simplification and optimization effect of endophytic fungi on plant recruiting microbes, which offers novel perspectives on using endophytic fungi to increase agricultural productivity.