Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen

Abstract

Some of the most damaging tree pathogens can attack woody stems, causing lesions (cankers) that may be lethal. To identify the genomic determinants of wood colonization leading to canker formation, we sequenced the genomes of the poplar canker pathogen,Mycosphaerella populorum, and the closely related poplar leaf pathogen,M. populicola. A secondary metabolite cluster unique toM. populorumis fully activated following induction by poplar wood and leaves. In addition, genes encoding hemicellulose-degrading enzymes, peptidases, and metabolite transporters were more abundant and were up-regulated inM. populorumgrowing on poplar wood-chip medium compared withM. populicola. The secondary gene cluster and several of the carbohydrate degradation genes have the signature of horizontal transfer from ascomycete fungi associated with wood decay and from prokaryotes. Acquisition and maintenance of the gene battery necessary for growth in woody tissues and gene dosage resulting in gene expression reconfiguration appear to be responsible for the adaptation ofM. populorumto infect, colonize, and cause mortality on poplar woody stems.