Sexuality Generates Diversity in the Aflatoxin Gene Cluster: Evidence on a global Scale.

MOORE, G.; ELLIOTT, J; SINGH, R.; HORN, B; DORNER, J.; STONE, E.; CHULZE, S.; BARROS, G.; NAIK, M.; WRIGHT, G; HELL, K.; CARBONE, I

PLOS PATHOGENS

PUBLIC LIBRARY SCIENCE

Lugar: San Francisco; Año: 2013 vol. 9 p. 1 - 12

1553-7366

Aflatoxins are produced by Aspergillus flavus and A. parasiticus in oil-rich seed and grain crops and are a serious problem in agriculture, with aflatoxin B1 being the most carcinogenic natural compound known. Sexual reproduction in these species occurs between individuals belonging to different vegetative compatibility groups (VCGs).  Because the vegetative compatibility system is not a barrier to genetic exchange, parents of different genotypes can mate and recombine to produce novel progeny that differ in aflatoxigenicity.  We examined natural genetic variation in 788 isolates of A. flavus and A. parasiticus sampled from single peanut fields in the United States (Georgia), Africa (Benin), Argentina (Córdoba), Australia (Queensland) and India (Karnataka).  Analysis of molecular sequence variation across multiple intergenic regions in the aflatoxin gene clusters of A. flavus and A. parasiticus revealed significant linkage disequilibrium (LD) organized into distinct blocks that are conserved across different localities, suggesting that genetic recombination is a global occurrence.  To assess the contributions of asexual and sexual reproduction to aflatoxigenicity in populations from each locality/species, we tested the null hypothesis of an equal number of MAT1-1 and MAT1-2 mating type individuals, which is indicative of a sexually recombining population.  All samples were clone-corrected using multi-locus sequence typing which associates closely with VCG.  For both A. flavus and A. parasiticus, when the proportions of MAT1-1 and MAT1-2 were significantly different, there was more extensive LD in the aflatoxin cluster and isolates grouped into specific toxin classes, either the non-aflatoxigenic class in A. flavus or the B1-dominant and G1-dominant classes in A. parasiticus; a mating type ratio close to 1:1 was associated with higher aflatoxin concentrations.  This work shows that the relative frequency of mating types in populations is a good predictor of aflatoxin production and that sexual reproduction is a major determinant of aflatoxigenicity in these agriculturally important fungi.