ARS | Publication request: Evidence for birth-and-death evolution and horizontal transfer of the fumonisin mycotoxin biosynthetic gene cluster in Fusarium

Submitted to: Fungal Genetics Conference/Asilomar
Publication Type: Abstract Only
Publication Acceptance Date: March 17, 2012
Publication Date: N/A

Technical Abstract: In fungi, genes required for synthesis of secondary metabolites are often clustered. The FUM gene cluster is required for synthesis of fumonisins, a family of toxic secondary metabolites produced predominantly by species in the Fusarium (Gibberella) fujikuroi species complex (FFSC). Fumonisins are a health and agricultural concern because their consumption is epidemiologically associated with multiple diseases in humans and other animals. Among FFSC species, the FUM cluster is discontinuously distributed but uniform in gene order and orientation. In this study, we demonstrate that the FUM cluster exists in at least four different genomic contexts within the FFSC and that phylogenetic relationships derived from analyses of FUM cluster genes are correlated with genomic context, but are inconsistent with species relationships inferred from analyses of primary-metabolism genes. In addition, analyses of synonymous site divergence suggested that FUM cluster divergence predated divergence of the FFSC. These results are not consistent with trans-species evolution of ancestral cluster alleles or with interspecies hybridization, but suggest duplication of the cluster within an FFSC ancestor and subsequent loss and sorting of paralogous clusters in a manner consistent with the birth-and-death model of evolution previously described for multigene families. A model based on horizontal gene transfer (HGT) could also explain these observations, but seems unlikely because it requires independent transfer events from multiple unknown donors to multiple FFSC recipients. However, analyses of phylogenetic relationships and synonymous site divergence provided strong evidence that F. oxysporum strain FRC O-1890 acquired the FUM cluster via a relatively recent HGT event from F. bulbicola or a closely related species within the FFSC. These results indicate that, as with other secondary metabolite clusters, species phylogenies do not provide an adequate picture of the complex evolutionary history of the FUM cluster within Fusarium.