Differential Expression of Fungal Genes Determines the Lifestyle of <i>Plectosphaerella</i> Strains During <i>Arabidopsis thaliana</i> Colonization

Abstract

The fungal genus <i>Plectosphaerella</i> comprises species and strains with different lifestyles on plants, such as <i>P. cucumerina</i>, which has served as model for the characterization of <i>Arabidopsis thaliana</i> basal and nonhost resistance to necrotrophic fungi. We have sequenced, annotated, and compared the genomes and transcriptomes of three <i>Plectosphaerella</i> strains with different lifestyles on <i>A. thaliana</i>, namely, PcBMM, a natural pathogen of wild-type plants (Col-0), Pc2127, a nonpathogenic strain on Col-0 but pathogenic on the immunocompromised <i>cyp79B2 cyp79B3</i> mutant, and P0831, which was isolated from a natural population of <i>A. thaliana</i> and is shown here to be nonpathogenic and to grow epiphytically on Col-0 and <i>cyp79B2 cyp79B3</i> plants. The genomes of these <i>Plectosphaerella</i> strains are very similar and do not differ in the number of genes with pathogenesis-related functions, with the exception of secreted carbohydrate-active enzymes (CAZymes), which are up to five times more abundant in the pathogenic strain PcBMM. Analysis of the fungal transcriptomes in inoculated Col-0 and <i>cyp79B2 cyp79B3</i> plants at initial colonization stages confirm the key role of secreted CAZymes in the necrotrophic interaction, since PcBMM expresses more genes encoding secreted CAZymes than Pc2127 and P0831. We also show that P0831 epiphytic growth on <i>A. thaliana</i> involves the transcription of specific repertoires of fungal genes, which might be necessary for epiphytic growth adaptation. Overall, these results suggest that in-planta expression of specific sets of fungal genes at early stages of colonization determine the diverse lifestyles and pathogenicity of <i>Plectosphaerella</i> strains.