Aim: Cryptic species in the Neofusicoccum parvum–N. ribis species complex have only recently been described, invalidating previous interpretations on host and geographical distribution. This study aimed to characterize the diversity and distribution of these species and to understand the patterns of host association, likely origins and their patterns of spread.Location: Australia, Brazil, Cameroon, Chile, China, Colombia, Ethiopia, France, Greece, India, Indonesia, Iran, Italy, Japan, Kenya, Mexico, New Zealand, Panama, Portugal, Puerto Rico, South Africa, South Korea, Spain, Swaziland, Taiwan, Thailand, Uganda, United States of America, Uruguay, Zambia and Zimbabwe.Methods: Using the unique polymorphisms that separate species within the complex, we evaluated sequence search results available in public and in our own databases. In addition, the global distribution of diversity of N. parvum was analysed using seven microsatellite markers.Results: Neofusicoccum parvum is found in 90 hosts across six continents and 29 countries. Neofusicoccum kwambonambiense is found on four continents, six countries and on 14 hosts; N. occulatum is found on four continents, four countries and on 11 hosts; N. umdonicola is found on two continents, countries and hosts; N. cordaticola is found on three continents, countries and hosts; N. batangarum is found on two continents, three countries and three hosts; and N. ribis is found on one host in one country. Population genetic analysis of the global N. parvum population reflects admixture and repeat introductions.Main conclusions: This study illustrates the unfettered and frequent movement of latent pathogens across international borders. Amongst the species in the N. parvum–N. ribis complex, N. parvum is the most widespread and has been reported on the majority of the hosts studied. The current dispersal of N. parvum and its sister species is probably due to repeated introductions of plant material into new growing areas, with Eucalyptus and Vitis vinifera being two prominent candidates for material transfer.

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 to M. populorum is 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 in M. populorum growing on poplar wood-chip medium compared with M. 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 of M. populorum to infect, colonize, and cause mortality on poplar woody stems. Significance Some of the most damaging tree diseases are caused by pathogens that induce cankers, a stem deformation often lethal. To investigate the cause of this adaptation, we sequenced the genomes of poplar pathogens that do and do not cause cankers. We found a unique cluster of genes that produce secondary metabolites and are co-activated when the canker pathogen is grown on poplar wood and leaves. The gene genealogy is discordant with the species phylogeny, showing a signature of horizontal transfer from fungi associated with wood decay. Furthermore, genes encoding hemicellulose-degrading enzymes are up-regulated on poplar wood chips, with some having been acquired horizontally. We propose that adaptation to colonize poplar woody stems is the result of acquisition of these genes.