|OLARTE, RODRIGO - North Carolina State University
|WORTHINGTON, CAROLYN - North Carolina State University
|SINGH, RAKHI - North Carolina State University
|MONACELL, JAMES - North Carolina State University
|STONE, ERIC - North Carolina State University
|XIE, DE-YU - North Carolina State University
|CARBONE, IGNAZIO - North Carolina State University
Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/11/2015
Publication Date: 3/16/2015
Publication URL: http://doi:10.1111/mec.13153
Citation: Olarte, R.A., Worthington, C.J., Horn, B.W., Moore, G.G., Singh, R., Monacell, J.T., Dorner, J.W., Stone, E.A., Xie, D., Carbone, I. 2015. Enhanced diversity and aflatoxigenicity in interspecific hybrids of Aspergillus flavus and Aspergillus parasiticus. Molecular Ecology 24(8):1889-1909.
Interpretive Summary: Aspergillus flavus and A. parasiticus are fungal pathogens that produce aflatoxins, which are highly carcinogenic compounds that pose a serious health risk to humans and animals. These fungi infect agriculturally important commodities such as corn, cotton and peanut. Each species produces a different array of mycotoxins. A. flavus typically produces both B aflatoxin and cyclopiazonic acid whereas A. parasiticus produces B and G aflatoxins but not cyclopiazonic acid. In this study we crossed A. flavus with A. parasiticus and obtained viable hybrid progeny. Toxin analysis revealed significantly higher aflatoxin production in some progeny compared to the parents. Furthermore, sexual reproduction and genetic recombination resulted in several progeny that produced unique combinations of mycotoxins. These results suggest that hybridization has a dual role in creating new aflatoxin-producing species and in generating and maintaining a diversity of mycotoxin profiles.
Technical Abstract: Aspergillus flavus and A. parasiticus are two of the most important aflatoxin-producing species that contaminate agricultural commodities worldwide. Both species are heterothallic and undergo sexual reproduction in laboratory crosses. Here, we examine the possibility of interspecific matings between A. flavus and A. parasiticus. These species can be distinguished morphologically and genetically, as well as by their mycotoxin profiles. Aspergillus flavus produces both B aflatoxins and cyclopiazonic acid (CPA), B aflatoxins or CPA alone, or neither mycotoxin; A. parasiticus produces B and G aflatoxins or the aflatoxin precursor O-methylsterigmatocystin, but not CPA. Only four out of forty-five attempted interspecific crosses between compatible mating types of A. flavus and A. parasiticus were fertile and produced viable ascospores. Single ascospore strains from each cross were isolated and were shown to be recombinant hybrids using multilocus genotyping and array comparative genome hybridization. Conidia of parents and their hybrid progeny were haploid and predominantly monokaryons and dikaryons based on flow cytometry. Multilocus phylogenetic inference showed that experimental hybrid progeny were grouped with naturally occurring A. flavus L strain and A. parasiticus. Higher total aflatoxin concentrations in some F1 progeny strains compared to midpoint parent aflatoxin levels indicate synergism in aflatoxin production; moreover, three progeny strains synthesized G aflatoxins that were not produced by the parents, and there was evidence of putative allopolyploidization in one strain. These results suggest that hybridization is an important diversifying force resulting in the genesis of novel toxin profiles in these agriculturally important species.