Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/11/2007
Publication Date: 10/3/2007
Citation: Carbone, I., Jakobek, J.L., Ramirez-Prado, J.H., Horn, B.W. 2007. RECOMBINATION, BALANCING SELECTION AND ADAPTIVE EVOLUTION IN THE AFLATOXIN GENE CLUSTER OF ASPERGILLUS PARASITICUS. Molecular Ecology. 16(20):4401-4417. Interpretive Summary: Aspergillus parasiticus is a fungus that commonly infects peanut seeds and contaminates them with aflatoxins, carcinogenic compounds that pose a significant health hazard to animals, including humans. The fungus resides in soil where it is in contact with developing peanut pods. Little is known about the population genetics of A. parasiticus in agricultural fields and the evolution of the species over time. This study showed evidence that the genes responsible for aflatoxin formation have been repeatedly rearranged over the past million years while still maintaining the ability of the species to produce aflatoxin. This information allows for more precise targeting of aflatoxin genes in the development of novel biological control strategies to prevent aflatoxin contamination of crops.
Technical Abstract: Aflatoxins are toxic and carcinogenic polyketides produced by several Aspergillus species that are known to contaminate agricultural commodities, posing a serious threat to animal and human health. Aflatoxin (AF) biosynthesis has been studied extensively and involves over 20 genes clustered in a 70-kb DNA region. Aspergillus parasiticus is economically important and is a common agent of AF contamination. Naturally occurring nonaflatoxigenic strains of A. parasiticus are rarely found and generally produce O-methylsterigmatocystin (OMST), the immediate presursor of AF. To elucidate the evolutionary forces acting to retain AF and OMST pathway extrolites (chemotypes), we sequenced 21 intergenic regions spanning the entire cluster in 24 A. parasiticus isolates chosen to represent the genetic diversity within a single Georgia field population. Linkage disequilibrium analyses revealed five distinct recombination blocks in the A. parasiticus cluster. Phylogenetic network analyses showed a history of recombination between chemotype-specific haplotypes, as well as evidence of contemporary recombination. We performed coalescent simulations of variation in recombination blocks and found an approximately twofold deeper coalescence for cluster genealogies compared to non-cluster genealogies, our internal standard of neutral evolution. Significantly deeper cluster genealogies are indicative of balancing selection in the AF cluster of A. parasiticus and are further corroborated by the existence of trans-species polymorphisms and common haplotypes in the cluster for several closely related species. Estimates of Ka/Ks for representative cluster genes provide evidence of selection for OMST and AF chemotypes, and indicate a possible role of chemotypes in ecological adaptation and speciation.