Rhizosheath inhabiting Massilia are linked to heterosis in roots of maize

Abstract

Heterosis, or hybrid vigor, describes the superior performance of F1 hybrids compared to parental inbreds. While soil microbiomes are proposed to influence heterosis, it remains unclear how heterotic plants shape their microbiomes and how interactions relate to stress responses. Here, we investigate the role of rhizosheath formation—the soil tightly adhering to roots—in maize heterosis under nitrogen deprivation. Across sterilization, inoculation, and transplantation experiments, hybrids develop larger rhizosheaths than inbreds, and rhizosheath size associates with biomass heterosis. Rhizosheath-enriched genus Massilia correlates with lateral root density, rhizosheath size, and growth. Untargeted metabolomics and flavone-deficient mutants reveal links between Massilia and flavonoid pathways, while growth promotion by Massilia can also occur independently of host flavones. Metagenomic analysis shows that larger rhizosheaths recruit microbial functions related to nutrient cycling and stress adaptation. These findings identify rhizosheath formation as an integrative trait associated with heterosis and a promising target for breeding resilient crops.