A novel phyllosphere resident Protomyces species that interacts with the Arabidopsis immune system.

We describe the genome contents of six Protomyces spp. that are pathogenic within the typical host range of the genus and a novel Protomyces strain (SC29) that was previously isolated from the phylloplane of wild Arabidopsis thaliana (Arabidopsis), an atypical or possible alternate host. Genome-wide phylogenetic analysis defined SC29 as a distinct Protomyces sp. Analysis of gene family expansions, gene retention, and gene loss patterns among these Protomyces spp. lead us to hypothesize that SC29 may have undergone a host jump. The role of phyllosphere residency in the lifecycle of Protomyces spp. was previously unknown. Genomic changes in SC29 and all other Protomyces spp. were consistent with adaptations to the plant phylloplane. As predicted by our analysis of its mating locus, SC29 did not cause disease on Arabidopsis as a single strain, but could persist in its phylloplane, while the closely related P. inouyei does not. SC29 treated Arabidopsis exhibited enhanced immunity against Botrytis cinerea infection, associated with activation of MAPK3/6, camalexin, and SA-signalling pathways. We conclude that SC29 is a novel Protomyces sp. able to survive in the Arabidopsis phylloplane and that phylloplane residency is an important element in the lifecycle of Protomyces spp.