Heterosis in root microbiota inhibits growth of soil-borne fungal pathogens in hybrid rice

In nature, plants are colonized by various microbes that play essential roles in their growth and health. Heterosis is a natural genetic phenomenon whereby first-generation hybrids exhibit superior phenotypic performance relative to their parents. It remains unclear whether this concept can be extended to the "hybridization" of microbiota from two parents in their descendants and what benefits the hybrid microbiota might convey. Here, we investigated the structure and function of the root microbiota from three hybrid rice varieties and their parents through amplicon sequencing analysis of bacterial 16S ribosomal DNA (rDNA) and fungal internal transcribed spacer (ITS) regions. We show that the bacterial and fungal root microbiota of the varieties are distinct from those of their parental lines and exhibit potential heterosis features in diversity and composition. Moreover, the root bacterial microbiota of hybrid variety LYP9 protects rice against soil-borne fungal pathogens. Systematic analysis of the protective capabilities of individual strains from a 30-member bacterial synthetic community derived from LYP9 roots indicated that community members have additive protective roles. Global transcription profiling analyses suggested that LYP9 root bacterial microbiota activate rice reactive oxygen species production and cell wall biogenesis, contributing to heterosis for protection. In addition, we demonstrate that the protection conferred by the LYP9 root microbiota is transferable to neighboring plants, potentially explaining the observed hybrid-mediated superior effects of mixed planting. Our findings suggest that some hybrids exhibit heterosis in their microbiota composition that promotes plant health, highlighting the potential for microbiota heterosis in breeding hybrid crops.