Polyploidy and microbiome associations mediate similar responses to pathogens in Arabidopsis

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 whether 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 and a synthetic leaf-associated bacterial community, we confirm that polyploids are generally more resistant to the model pathogen Pseudomonas syringae pv. Tomato DC3000. Polyploids fare better against the pathogen than diploids do, regardless of microbial inoculation, whereas diploids harboring an intact microbiome have lower pathogen densities than those without. In addition, diploids have elevated numbers of defense-related genes that are differentially expressed in the presence of their phyllosphere microbiota, whereas polyploids exhibit some constitutively activated defenses, regardless of colonization by the synthetic community. These results imply that whole-genome duplication can enhance immunity, resulting in a decreased dependence on the microbiome for protection against pathogens.