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ARS Home » Midwest Area » Peoria, Illinois » National Center for Agricultural Utilization Research » Mycotoxin Prevention and Applied Microbiology Research » Research » Publications at this Location » Publication #278483

Title: Birth, death and horizontal transfer of the fumonisin biosynthetic gene cluster during the evolutionary diversification of Fusarium

item Proctor, Robert
item VAN HOVE, FRANCOIS - Catholic University Of Leuven
item SUSCA, ANTONIA - National Research Council - Italy
item STEA, GAETANO - National Research Council - Italy
item Busman, Mark
item VAN DER LEE, THEO - Plant Research International - Netherlands
item WAALWIJK, CEES - Plant Research International - Netherlands
item MORETTI, ANTONIO - National Research Council - Italy
item Ward, Todd

Submitted to: Molecular Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/8/2013
Publication Date: 10/1/2013
Citation: Proctor, R., Van Hove, F., Susca, A., Stea, G., Busman, M., van der Lee, T., Waalwijk, C., Moretti, A., Ward, T.J. 2013. Birth, death and horizontal transfer of the fumonisin biosynthetic gene cluster during the evolutionary diversification of Fusarium. Molecular Microbiology. 90(2):290–306.

Interpretive Summary: Mycotoxins are fungal metabolites that can contaminate crops and that pose health hazards to humans and domestic animals. Fumonisins are mycotoxins produced by multiple species of the agriculturally important fungus Fusarium. The ability to produce fumonisins is controlled by the fumonisin biosynthetic (FUM) gene cluster, 16 genes located adjacent to one another on a Fusarium chromosome. This study provides evidence that the FUM cluster has undergone complex changes during the evolution of Fusarium. The changes include multiple duplications of the cluster followed by loss of all or some of the resulting copies, movement of the cluster within a genome, and transfer of the cluster from one Fusarium species to another via a process involving cell fusion of the two species. Together, the results provide an explanation for the sporadic occurrence of the FUM cluster within Fusarium, and for differences in the type of fumonisins produced by different Fusarium species. The data also indicate that the ability to produce fumonisins may be transferable between species of Fusarium. The results of this study expand understanding of the mechanisms that shape the diversity and distribution of mycotoxin production and will be of interest to government, academic and industry scientists working to develop control strategies that limit mycotoxin contamination of cereals.

Technical Abstract: In fungi, genes required for synthesis of secondary metabolites are often clustered. The FUM gene cluster is required for synthesis of a family of toxic secondary metabolites, fumonisins, produced by species of Fusarium in the Gibberella fujikuroi species complex (GFSC). Fumonisins are a health and agricultural concern because their consumption is epidemiologically associated with human esophageal cancer and neural tube defects. Among GFSC species, the FUM cluster is discontinuously distributed but uniform in gene order and orientation. Here, analyses of phylogenetic relationships and synonymous site divergence provide evidence for amplification of the cluster within a GFSC ancestor and subsequent loss and sorting of paralogous clusters in a manner consistent with the birth-and-death model of multigene family evolution. The results also provide evidence that gene sequence variation responsible for structural variation of fumonisins arose independently in two cluster paralogs. In addition, the results indicate that the cluster relocated multiple times within the GFSC genome and has undergone horizontal gene transfer from GFSC to another Fusarium lineage. Thus, despite conservation of gene organization within the FUM cluster, the evolutionary history of the cluster in Fusarium has been complex.