Although complex interactions between hosts and microbial associates are increasingly well documented, we still know little about how and why hosts shape microbial communities in nature. In addition, host genetic effects on microbial communities vary widely depending on the environment, obscuring conclusions about which microbes are impacted and which plant functions are important. We characterized the leaf microbiota of 200 Arabidopsis thaliana genotypes in eight field experiments and detected consistent host effects on specific, broadly distributed microbial species (operational taxonomic unit [OTUs]). Host genetic effects disproportionately influenced central ecological hubs, with heritability of particular OTUs declining with their distance from the nearest hub within the microbial network. These host effects could reflect either OTUs preferentially associating with specific genotypes or differential microbial success within them. Host genetics associated with microbial hubs explained over 10% of the variation in lifetime seed production among host genotypes across sites and years. We successfully cultured one of these microbial hubs and demonstrated its growth-promoting effects on plants in sterile conditions. Finally, genome-wide association mapping identified many putatively causal genes with small effects on the relative abundance of microbial hubs across sites and years, and these genes were enriched for those involved in the synthesis of specialized metabolites, auxins, and the immune system. Using untargeted metabolomics, we corroborate the consistent association between variation in specialized metabolites and microbial hubs across field sites. Together, our results reveal that host genetic variation impacts the microbial communities in consistent ways across environments and that these effects contribute to fitness variation among host genotypes.

Although the complex interactions between hosts and microbial associates are increasingly well documented, we still know little about how and why hosts shape microbial communities in nature. We characterized the leaf microbiota within 200 clonal accessions in eight field experiments and detected effects of both local environment and host genotype on community structure. Within environments, hosts’ genetics preferentially associate with a core of ubiquitous microbial hubs that, in turn, structure the community. These microbial hubs correlate with host performance, and a GWAS revealed strong candidate genes for the host factors impacting heritable hubs. Our results reveal how selection may act to enhance fitness through microbial associations and bolster the possibility of enhancing crop performance through these host factors.TextHosts harbor complex microbial communities that are thought to impact health and development1. This is best studied in human hosts for which the microbiota has been implicated in a variety of diseases including obesity and cancer 2. Efforts are thus underway to determine the host factors shaping these resident populations 3,4 and to use next-generation probiotics to inhibit colonization by pathogens 5. Similarly, in agriculture, there is great hope of shaping the composition of the microbiota in order to mitigate disease and increase crop yield in a sustainable fashion. Indeed, the Food and Agriculture Organization of the United Nations has made the use of biological control and growth promoting microbial associations a clear priority for improving food production 6.Plant associated microbes can be beneficial in many ways including improving access to nutrients, activating or priming the immune system, and competing with pathogens. For example, seeds inoculated with a combination of naturally occurring microbes were recently found to be protected from a sudden-wilt disease that emerged after continuous cropping 7. Thus, it would be advantageous to breed crops that promote the growth of beneficial microbes under a variety of field conditions, a prospect that is made more likely by the demonstration of host genotypic effects on their microbiota 8–10. That said, microbial communities are complex entities that are influenced by the combined impact of host factors, environment and microbe-microbe interactions 11. As a consequence, the extent to which host plants can control microbial communities to their advantage, especially in a natural context, is unclear.Here, we combine large scale field experiments of plant genotypes grown in their natural environments, extensive microbial community analysis, and genome-wide association mapping to (i) disentangle how the influence of the host is distributed among microbial community members, and thus how host variation shapes the microbiota, (ii) propose plant genes and functions that correlate with variation in the microbiota across environmental conditions, and (iii) examine how key microbial associates impact plant fitness. Our motivation is to further the goal of generating plants with an enhanced ability to host beneficial microbial communities.