Maize root-associated microbes likely under adaptive selection by the host to enhance phenotypic performance

The root-associated microbiome (rhizobiome) plays a non-negligible role in determining plant health, stress tolerance, and nutrient use efficiency. However, it remains unclear to what extent the composition of the rhizobiome is governed by intraspecific variation in host plant genetics in the field and the degree to which host plant selection can reshape the composition of the rhizobiome. Here we quantify the rhizosphere microbial communities associated with a replicated diversity panel of 230 maize (Zea mays L.) genotypes grown in agronomically relevant conditions under high N (+N) and low N (-N) treatments. We show that the abundance of many root-associated microbes within a functional core microbial community of 150 abundant and consistently reproducible microbial groups is explainable by natural genetic variation in the host plant, with a greater proportion of microbial variance attributable to plant genetic variation in low N conditions. Population genetic approaches identify signatures of purifying selection in the maize genome associated with the abundance of several groups of microbes in the maize rhizobiome. Genome-wide association studies conducted using rhizobiome phenotypes identified n = 467 microbe-associated plant loci (MAPLs) in the maize genome linked to variation in the abundance of n = 115 microbial groups in the maize rhizosphere. In 62/115 cases, which is more than expected by chance, the abundance of these same microbial groups was correlated with variation in plant vigor indicators derived from high throughput phenotyping of the same field experiment. This study provides insights into harnessing the full potential of root-associated microbial symbionts in maize production.