Submitted to: Journal of Evolutionary Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/29/2007
Publication Date: 7/9/2007
Citation: Carbone, I., Ramirez-Prado, J.H., Jakobek, J.L., Horn, B.W. 2007. Gene duplication, modularity and adaptation in the evolution of the aflatoxin gene cluster. Journal of Evolutionary Biology 7:111. Interpretive Summary: Molds belonging to the genus Aspergillus produce various toxins that contaminate agricultural commodities. A detailed examination of the toxin-producing genes suggests that production of carcinogenic aflatoxins and related toxins is in some manner beneficial to the molds. This information provides important information necessary for the development of novel biological control strategies to prevent aflatoxin contamination of crops.
Technical Abstract: The biosynthesis of aflatoxin (AF) involves over 20 enzymatic reactions in a complex polyketide pathway that converts acetate and malonate to the intermediates sterigmatocystin (ST) and O-methylsterigmatocysin (OMST), the respective penultimate and ultimate precursors of AF. Although these precursors are chemically and structurally very similar, their accumulation differs at the species level for Aspergilli. Notable examples are A. nidulans, which synthesizes only ST, A. flavus that makes predominantly AF, and A. parasiticus that generally produces either AF or OMST. Whether these differences are important in the evolutionary/ecological processes of species adaptation and diversification is unknown. To elucidate the mechanisms that have driven formation of these clusters, we performed systematic searches of aflatoxin cluster homologs across five Aspergillus genomes. We found a high level of gene duplication and identified seven modules consisting of highly correlated gene pairs (aflA/aflB, aflR/aflS, aflX/aflY, aflF/aflE, aflT/aflQ, aflC/aflW, and aflG/aflL). Gene modules may have arisen from duplications of a single gene, whereby the copy retained the function of the pre-duplication gene (aflF/aflE); subfunctionalization in which copies partition the ancestral function (aflA/aflB); and possibly neofunctionalization, an adaptive process in which a completely new function has evolved for the duplicated copy (aflT/aflQ and aflC/aflW). Other gene modules comprise genes that augment a specific pathway function (aflR/aflS and aflX/aflY). Overall estimates of mean Ka/Ks values were significantly higher in section Flavi than non-section Flavi species, indicating increased positive selection acting in the evolution of genes in OMST and AF clusters relative to the ST cluster in A. nidulans.