Abstract
Fungal genomes encode highly organized gene clusters that underlie the production of specialized (or secondary) metabolites. Gene clusters encode key functions to exploit plant hosts or environmental niches. Promiscuous exchange among species and frequent reconfigurations make gene clusters some of the most dynamic elements of fungal genomes. Despite evidence for high diversity in gene cluster content among closely related strains, the microevolutionary processes driving gene cluster gain, loss, and neofunctionalization are largely unknown. We analyzed the Fusarium graminearum species complex (FGSC) composed of plant pathogens producing potent mycotoxins and causing Fusarium head blight on cereals. We de novo assembled genomes of previously uncharacterized FGSC members (two strains of F. austroamericanum, F. cortaderiae, and F. meridionale). Our analyses of 8 species of the FGSC in addition to 15 other Fusarium species identified a pangenome of 54 gene clusters within FGSC. We found that multiple independent losses were a key factor generating extant cluster diversity within the FGSC and the Fusarium genus. We identified a modular gene cluster conserved among distantly related fungi, which was likely reconfigured to encode different functions. We also found strong evidence that a rare cluster in FGSC was gained through an ancient horizontal transfer between bacteria and fungi. Chromosomal rearrangements underlying cluster loss were often complex and were likely facilitated by an enrichment in specific transposable elements. Our findings identify important transitory stages in the birth and death process of specialized metabolism gene clusters among very closely related species.
Highlights
Fungal genomes encode highly organized structures that underlie the capacity to produce specialized metabolites
The N50 of previously sequenced genomes of the Fusarium graminearum species complex (FGSC) ranged from 149-9395 kb including the fully finished assembly of the reference genome F. graminearum PH-1 (FgramR)
By analyzing the completeness of all assemblies, we found the percentage of recovered BUSCO orthologues to be above 99.3% for all FGSC members
Summary
Fungal genomes encode highly organized structures that underlie the capacity to produce specialized ( called secondary) metabolites. The structures are composed of a tightly clustered group of non-homologous genes that in conjunction confer the enzymatic pathway to produce a specific metabolite (Osbourn, 2010). Specialized metabolites (SM) are not essential for the organism's survival but confer crucial benefits for niche adaptation and host exploitation. Specialized metabolites can promote defense (e.g penicillin), virulence (e.g trichothecenes) or resistance functions (e.g melanin) The backbone gene encodes for the enzyme defining the class of the produced metabolite and the enzyme is most often a polyketide synthase (PKS), nonribosomal peptides synthetase (NRPS), terpenes cyclase (TC) or a dimethylallyl tryptophan synthetase (DMATS). Additional genes in clusters encode functions to modify the main metabolite structure
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