Host-specific subtelomere: Genomic architecture of pathogen emergence in asexual filamentous fungi

Several asexual species of filamentous fungal pathogens contain supernumerary chromosomes carrying secondary metabolite (SM) or pathogenicity genes. Supernumerary chromosomes have been shown in in vitro experiments to transfer from pathogenic isolates to non-pathogenic ones and between isolates whose fusion can result in vegetative or heterokaryon incompatibility (HET). However, much is still unknown about the acquisition and maintenance of SM/pathogenicity gene clusters in the adaptation of these asexual pathogens to their hosts. We investigated several asexual fungal pathogens for genomic elements involved in maintaining telomeres for supernumerary and core chromosomes during vegetative reproduction. We found that in vegetative species or lineages with a nearly complete telomere-to-telomere genome assembly (e.g. Fusarium equiseti and five formae speciales of the F. oxysporum species complex), core and super-numerary chromosomes were flanked by highly similar subtelomeric sequences on the 3’ side and by their reverse complements on the 5’ side. This subtelomere sequence structure was preserved in isolates from the same species or from polyphyletic lineages in the same forma specialis (f.sp.) of the F. oxysporum species complex. Moreover, between some isolates within F. oxysporum f.sp. lycopersici , the mean rate of single nucleotide polymorphisms (SNPs) in a supernumerary chromosome was at least 300 times lower than those in core chromosomes. And a large number of HET domain genes were located in SM/pathogenicity gene clusters, with a potential role in maintaining these gene clusters during vegetative reproduction.