Heritable maize microbiomes contribute to local adaptation and host stress resilience

Beneficial interactions with microorganisms are pivotal for plant adaptation and fitness. Yet, the adaptive trajectories and genetic mechanisms underlying plant-microbiome interactions remain elusive. Here, we surveyed the root and rhizosphere microbiome of 129 accessions of Zea mays, sourced from diverse habitats and grown under control and different stress conditions. We demonstrate the impact of domestication and local adaptation on heritable variation in microbiome assembly. Plant genotype and native environment were predictive of the microbiome composition, and the microbiome itself was correlated with plant fitness. Combining microbiome and environmental properties identified host genetic variants linked to rhizosphere microbiome variation with respect to their native habitats. We functionally characterized a gene that controls lateral root formation and mediates association with a keystone microbe, linked to growth promotion and biomass heterosis. We conclude that genetic variation in traditional crop varieties contributes to optimizing the adaptation of the microbiome to local constraints, which bears implications for breeding resilient cultivars.