Fragmentation of an aflatoxin‐like gene cluster in a forest pathogen

Abstract

SummaryPlant pathogens use a complex arsenal of weapons, such as toxic secondary metabolites, to invade and destroy their hosts. Knowledge of how secondary metabolite pathways evolved is central to understanding the evolution of host specificity. The secondary metabolite dothistromin is structurally similar to aflatoxins and is produced by the fungal pine pathogen Dothistroma septosporum. Our study focused on dothistromin genes, which are widely dispersed across one chromosome, to determine whether this unusual distributed arrangement evolved from an ancestral cluster.We combined comparative genomics and population genetics approaches to elucidate the origins of the dispersed arrangement of dothistromin genes over a broad evolutionary timescale at the phylum, class and species levels.Orthologs of dothistromin genes were found in two major classes of fungi. Their organization is consistent with clustering of core pathway genes in a common ancestor, but with intermediate cluster fragmentation states in the Dothideomycetes fungi. Recombination hotspots in a D. septosporum population matched sites of gene acquisition and cluster fragmentation at higher evolutionary levels.The results suggest that fragmentation of a larger ancestral cluster gave rise to the arrangement seen in D. septosporum. We propose that cluster fragmentation may facilitate metabolic retooling and subsequent host adaptation of plant pathogens.

Evolution of Chemical Diversity in Echinocandin Lipopeptide Antifungal Metabolites

“…Under either of these hypotheses, we might have expected to encounter evidence of cluster degradation or to find at least a few cluster fragments or pseudogenes interspersed across the genomes of major secondary-metabolite-producing sister lineages of the Sordariomycetes, Dothideomycetes, and Lecanoromycetes or in other orders of the Leotiomycetes and Eurotiomycetes beyond the Helotiales and Eurotiales. However, in contrast to what has been observed in some fungal secondary-metabolite pathways (2,(56)(57)(58), ec.asm.org 705 Eukaryotic Cell this was not the case. BLAST searches using each of the shared pathway genes always retrieved the corresponding genes of other echinocandin-producing species as the most likely hits.…”

Elucidation of cladofulvin biosynthesis reveals a cytochrome P450 monooxygenase required for anthraquinone dimerization

“…Genes that encode these enzymes are arranged in a cluster, which is conserved across a number of other fungal species, although with different sets of tailoring genes. Such changes have been shown to drive the production of different anthraquinones, such as sterigmatocystin in A. nidulans and dothistromin in Dothistroma septosporum (11). A large gene cluster is also involved in the production of monodictyphenone in A. nidulans, which consists of the core PKS gene mdpG and at least seven tailoring genes (7,8).…”

Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases

“…However, within Aspergillus, homologous clusters are variable in their presence and composition. Rapid rearrangement and degeneration of these clusters resulted in a diversity of producers and nonproducers of aflatoxins among Aspergillus species and the virulence factor dothistromin in the pine pathogen Dothistroma septosporum (129). Secondary metabolism gene clusters in fungi will continue to be an important topic of evolutionary, ecological, and pharmacological studies in the coming years.…”