Polyploidy and Microbiome Associations Mediate Distinct Plant Responses to Pathogens

It has become increasingly clear that the microbiome plays a critical role in shaping the host organism’s response to disease. There also exists mounting evidence that an organism’s ploidy level is important in their response to pathogens and parasites. However, no study has determined if or how these two factors influence one another. We investigate the effect of whole-genome duplication in Arabidopsis thaliana on the above-ground (phyllosphere) microbiome, and determine the interacting impacts of ploidy and microbiome on disease outcome. Using seven independently derived synthetic autotetraploid Arabidopsis accessions, a synthetic leaf-associated bacterial community, and the model pathogen Pseudomonas syringae pv. Tomato DC3000, we confirm that polyploids are generally more resistant to pathogens, but illustrate that this resistance may be due in part to a decrease in the reliance on beneficial bacteria. Polyploids fare better against the pathogen than diploids regardless of microbial inoculation, while diploids harboring an intact microbiome have lower pathogen densities than those without. In addition, diploids have elevated numbers of differentially expressed defense-related genes in the presence of their phyllosphere microbiota, while polyploids exhibit constitutively activated defenses regardless of colonization by the synthetic community. These results imply that whole-genome duplication can disrupt host-microbiome associations, and suggest that the consequences of this disruption is an important difference between how diploids and polyploids utilize the microbiome.