Comparative analyses of saprotrophy in Salisapilia sapeloensis and diverse plant pathogenic oomycetes reveal lifestyle-specific gene expression

Abstract

Oomycetes include many well-studied, devastating plant pathogens. Across oomycete diversity, plant-infecting lineages are interspersed by non-pathogenic ones. Unfortunately, our understanding of the evolution of lifestyle switches is hampered by a scarcity of data on the molecular biology of saprotrophic oomycetes, ecologically important primary colonizers of dead tissue that can serve as informative reference points for understanding the evolution of pathogens. Here, we established Salisapilia sapeloensis growing on axenic litter as a tractable system for the study of saprotrophic oomycetes. We generated multiple transcriptomes from S. sapeloensis and compared them to (a) 22 oomycete genomes and (b) the transcriptomes of eight pathogenic oomycetes grown under 13 conditions (three pathogenic lifestyles, six hosts/substrates, and four tissues). From these analyses we obtained a global perspective on the gene expression signatures of oomycete lifestyles. Our data reveal that oomycete saprotrophs and pathogens use generally similar molecular mechanisms for colonization, but exhibit distinct expression patterns. We identify S. sapeloensis specific array and expression of carbohydrate-active enzymes and regulatory differences in pathogenicity-associated factors, including the virulence factor EpiC2B. Further, S. sapeloensis was found to express only a small repertoire of effector genes. In conclusion, our analyses reveal lifestyle-specific gene regulatory signatures and suggest that, in addition to variation in gene content, shifts in gene regulatory networks might underpin the evolution of oomycete lifestyles.