The Genomic Landscape Of Tree Rot In Phellinus noxius And Its Hymenochaetales Members

Background: The order Hymenochaetales of filamentous fungi contains some of the most aggressive wood decayers that have caused major forest incidents as early as 1971. It is also phylogenetically placed between the well-studied Agaricales and Ustillaginales orders, making Hymenochaetales species interesting for investigating the evolutionary transition between the orders of Basidiomycota. Results: We report four whole-genomes from this group including the tree rot pathogen Phellinus noxius, the wood decomposing fungus Phellinus lamaensis, the laminated root rot pathogen Phellinus sulphurascens, and the trunk rot pathogen Porodaedalea pini. While expansion of transposable elements constitutes the main difference between these genomes ranging from 31- to 53-megabases, their karyotype is conserved with distant fungi. We found many genes reflecting their ability as white-rot fungi, and transcriptome data from in planta colonization of P. noxius revealed members of carbohydrate active enzymes, P450s, and nucleotide-binding-oligomerization-domain like receptors that are upregulated at different infection phases. Population genomics analyses of 60 P. noxius isolates across the Asia Pacific region revealed extraordinary genetic diversity and mono-/heterokaryotic nature, and that the isolates can be divided into two genetically separated lineages with contrasting evolutionary scenarios. Conclusions: These genomes shed light on the basic biology and population genetics of fungal tree pathogens. The combined genome and transcriptome analysis of P. noxius can serve as a starting point for understanding the survival strategies of this devastating pathogen, from which new control methods could be developed.