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Title: Sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale

item Moore, Geromy
item ELLIOTT, JACALYN - North Carolina State University
item SINGH, RAKHI - North Carolina State University
item Horn, Bruce
item Dorner, Joe
item STONE, ERIC - North Carolina State University
item CHULZE, SOFIA - Universidad Nacional De Cordoba
item BARROS, GERMAN - Universidad Nacional De Cordoba
item NAIK, MANJUNATH - College Of Agriculture
item WRIGHT, GRAEME - Queensland Department Of Primary Industries & Fisheries
item HELL, KERSTIN - International Institute Of Tropical Agriculture (IITA)
item CARBONE, IGNAZIO - North Carolina State University

Submitted to: PLoS Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/9/2013
Publication Date: 8/29/2013
Citation: Moore, G.G., Elliott, J.L., Singh, R., Horn, B.W., Dorner, J.W., Stone, E.A., Chulze, S.N., Barros, G.G., Naik, M.K., Wright, G.C., Hell, K., Carbone, I. 2013. Sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale. PLoS Pathogens. 9(8):e1003574. doi:10.1371/journal.ppat.1003574.

Interpretive Summary: Recent population studies have uncovered evidence of extensive recombination among field isolates of Aspergillus flavus and A. parasiticus sampled in Georgia, USA. Also determined for these Georgia populations was the distribution of mating type alleles. What has yet to be determined is whether or not evidence of recombination is detectable in geographically-isolated populations of A. flavus and A. parasiticus from around the world. As well, whether or not the distribution of mating type alleles for these distantly related populations influences chemotype diversity exhibited in a species population. Observing evidence that recombination is a global occurrence will allow researchers to better understand the risks with applying potentially unstable biocontrol strains in fields where recombination is occurring. The goals of this project are (1) to analyze genomic regions within the aflatoxin gene cluster for A. flavus and A. parasiticus populations representing four continents and use comparative analyses to infer recombination, then to compare findings with previously analyzed populations from Georgia, USA; and (2) to identify and sequence the mating type idiomorphs for global populations of A. flavus and A. parasiticus, and perform statistical analyses that may offer insights into species diversity, or lack thereof, in a sample field population.

Technical Abstract: The worldwide costs associated with aflatoxin monitoring and crop losses are in the hundreds of millions of dollars. Aflatoxins also account for considerable health risks, even in countries where food contamination is regulated. Aspergillus flavus and A. parasiticus are the most common agents of aflatoxin contamination of oil-rich seed and grain crops. Sexual reproduction in these species occurs between individuals belonging to different vegetative compatibility groups (VCGs), and suggests that the vegetative compatibility system is not a barrier to gene flow and that recombination could result in progeny differing in toxicity from the parents. To study this we examined natural genetic variation in A. flavus and A. parasiticus sampled from single peanut fields across five continents. Analysis of molecular sequence variation across multiple intergenic regions in the aflatoxin gene clusters of A. flavus and A. parasiticus revealed significant linkage disequilibrium organized into distinct blocks that are conserved across different localities, which indicates that genetic recombination is a global occurrence. We also found that differences in the proportions of MAT1-1 and MAT1-2 were correlated with the amount of asexual (i.e. clonal amplification of VCGs) and sexual reproduction in populations. Also, comparing frequency distribution plots for population aflatoxin concentrations with distribution of MAT1-1 and MAT1-2 shows a correlation, with a more continuous distribution of toxicity exhibited among populations with a higher component of sexual reproduction. Current biological control through competitive exclusion by atoxigenic A. flavus may eventually cause more harm than good as its efficacy will be determined by a population’s recombination potential, which is related to the distribution of mating types in that population. The existence of sympatric species should also be taken into consideration when devising biocontrol strategies. Aspergillus flavus S strains appear to have isolates with toxin profiles similar to A. flavus, A. parasiticus or both. The ability to detect recombination, along with understanding the factors that contribute to recombination in populations may help us better control aflatoxin contamination throughout our world.