Host-specific subtelomere: structural variation and horizontal transfer in asexual filamentous fungal pathogens

Several asexual filamentous fungal pathogens contain supernumerary chromosomes carrying secondary metabolite (SM) or pathogenicity genes as well as transposons. 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 extent of horizontal transfer of supernumerary chromosomes within and between asexual pathogenic populations in adaptation 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 populations 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 supernumerary 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 specific to the host. We detected instances of recent horizontal transfer of regions of a supernumerary chromosome between distant populations in the F. oxysporum species complex, and we also found field isolates with two structurally different copies of a supernumerary chromosome in a young asexual population, raising the possibility that those copies originated from different lineages by intrastrain anastomosis. A large number of HET domain genes were located in SM/pathogenicity gene clusters, with a potential role in marking these gene clusters during vegetative reproduction. The emergence of novel asexual pathogenic populations by horizontal transfer of transposon-rich supernumerary chromosomes within and between populations poses challenges to the control and management of these pathogens.