Establishing Alliances: Plant and Microbial Drivers of Microbiome Assembly across Community Complexity and Timescale

Aboveground and belowground plant tissues harbor microbial communities that confer several benefits to the plant host including nutrient acquisition, immune system development, pathogen protection, and stress tolerance. Despite the tremendous potential of harnessing plant microbiomes for inducing desired outcomes in plants, their promise remains elusive as we do not understand many of the critical underpinnings of microbiome assembly. In this dissertation, I examine two of the understudied facets of plant microbiome assembly, influences of host produced salicylic acid (SA) and microbial interactions, with a focus on internal root microbial communities, the endosphere. Using serial passaging of endosphere microbiomes, I demonstrate host SA impacts specific taxa that assemble inside root tissue. Furthermore, I uncovered endosphere microbiota span lifestyles as bacteria isolated from final passage communities displayed both plant growth promoting and pathogenic phenotypes. I then transitioned to using a series of bacterial synthetic communities (SynComs) to investigate specific microbial interactions and the influence of SA in both fully assembled endosphere communities and early colonization of plant tissue. I found evidence that the genus Streptomyces contributes to a variety of SA-influenced and non-SA influenced interactions with diverse microbiota following several weeks of microbiome assembly. Finally, I zoom in on the interactions taking place within hours of inoculation. While SA does not mediate colonization at these early timepoints, I identify specific SynCom members that consistently establish as primary colonizers of plant tissue. Among primary colonizers, differences in internal and external colonization trajectories, motility phenotypes, and potential competitive interactions were revealed during early plant colonization. Altogether, this dissertation elaborates on the role of salicylic acid and microbial interactions as well as the intersection of the two in mediating the alliance between plant hosts and their microbiota. These findings demonstrate both mechanisms and approaches that work to untangle assembly processes for harnessing the full potential of plant microbiomes.