Microbiome eco-evolution of cultivated and wild rice species across the genus Oryza and its importance in supporting rice growth

BACKGROUND: Crop wild relatives and their microbiomes are essential for sustainable crop production. However, the co-evolution of wild rice species and their microbiomes remains poorly understood. Herein, we investigated microbiome assembly across 17 wild rice and one cultivated rice species under controlled conditions spanning ~15 million years of evolution. RESULTS: Our data reveal distinct eco-evolutionary patterns for bacteria and fungi. Host divergence time was the predominant driver of root microbiota structure, outweighing polyploidy and life cycle, and exerted a stronger effect on bacteria than fungi. Bacterial community exhibited a significant phylosymbiosis with its host, but fungi did not. Over evolutionary time, bacterial diversity decreased while phylogenetic clustering increased. Deterministic and stochastic processes co-drove bacteria assembly, whereas stochastic processes strongly drove fungi assembly. Potentially functional taxa, including nitrogen-fixing and methane-cycle bacteria, were differentially enriched across evolutionary time and polyploidization events. Notably, co-speciating bacteria better predicted grain weight than fungi, with core species making a major contribution. Using a synthetic community (SynCom) derived from the wild rice core microbiome and four nitrogen-fixing strains enriched in early- and medium-diverging Oryza species, we demonstrated that the SynCom strongly promoted rice growth, with the removal of key members markedly reducing its impact. CONCLUSIONS: These results reveal co-phylogenetic patterns between Oryza and root-associated bacteria, highlighting the closer functional linkage between rice traits and bacteria than fungi, likely due to their co-evolution. Our findings provide new insights into crop-microbiome symbiosis from an eco-evolutionary perspective and underscore the importance of co-speciating microbiomes from wild relatives in supporting crop growth. Video Abstract.