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

Abstract

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 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 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.

Characterization of Host-Specific Genes from Pine- and Grass-Associated Species of the <em>Fusarium Fujikuroi </em>Species Complex

“…In fungi, the emerging evidence suggests that genes located in subtelomeres play adaptive roles, such as contributing to niche-or host-specificity and virulence in pathogens [65][66][67][68]. For example, the fungus Pneumocystis jiroveci have large and highly variable gene families located in its subtelomeric regions that encode for surface proteins with tightly regulated, yet switchable, expression patterns [69].…”

Characterization of Host-Specific Genes from Pine- and Grass-Associated Species of the Fusarium fujikuroi Species Complex

“…The subtelomeric regions are also thought to have higher genomic instability than elsewhere on the chromosome, which possibly allows for the tight regulation, and occasional switching of expression between different gene copies, allowing for organisms to evade the immune system of their respective hosts [67,68]. In addition, the literature suggests that genes located in subtelomeres play important evolutionary roles towards adaptation, such as contributing to niche-or host-specificity and virulence in pathogens [69][70][71][72]. For example, the fungus Pneumocystis jiroveci has large and highly variable gene families located in its subtelomeric regions that encode for surface proteins with tightly regulated, yet switchable, expression patterns [73].…”

Complementary Theory of Evolutionary Genetics

“…We previously found that in isolates Fol race 3 D11, Forc Forc016, Fom Fom001 and Focb race 1 160527, core and supernumerary chromosomes were flanked on both sides by inverted copies of a host-or population-specific subtelomeric element (Huang 2019). That is, the 5' copy in forward orientation was highly similar to the 3' copy in reverse orientation, with both copies located within 10-to 15-kb ends of the chromosome, respectively.…”