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Title: Sexual reproduction in Aspergillus flavus sclerotia: acquisition of novel alleles from soil populations and uniparental mitochondrial inheritance

Author
item Horn, Bruce
item GELL, RICHARD - North Carolina State University
item SINGH, RAKHI - North Carolina State University
item Sorensen, Ronald - Ron
item CARBONE, IGNAZIO - North Carolina State University

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/14/2015
Publication Date: 1/5/2016
Publication URL: http://dx.doi.org/10.5061/dryad.sk35h
Citation: Horn, B.W., Gell, R.M., Singh, R., Sorensen, R.B., Carbone, I. 2016. Sexual reproduction in Aspergillus flavus sclerotia: acquisition of novel alleles from soil populations and uniparental mitochondrial inheritance. PLoS One. 11(1): e0146169.

Interpretive Summary: The fungus Aspergillus flavus colonizes agricultural commodities worldwide and contaminates them with carcinogenic aflatoxin. Sexual reproduction was recently discovered in A. flavus and is responsible for much of the genetic variation observed in nature, including the ability of the fungus to produce aflatoxin. However, the frequency of sexual reproduction in the field is not known, nor is it understood how and when fertilization occurs in relation to crop infection. In this study, laboratory and field experiments showed that fertilization occurs during crop infection as well as on the soil surface after crop harvest. When fertilized on soil, A. flavus can obtain novel genes from soil populations of the fungus. Furthermore, A. flavus strains can function as either female or male during sexual reproduction. This research increases our understanding of the life cycle of A. flavus and is critical for devising new strategies for controlling aflatoxin in crops.

Technical Abstract: Aspergillus flavus colonizes agricultural commodities worldwide and contaminates them with carcinogenic aflatoxins. The high genetic diversity of A. flavus populations is largely due to sexual reproduction characterized by the formation of ascospore-bearing ascocarps embedded within sclerotia. A. flavus is heterothallic and laboratory crosses between strains of the opposite mating type produce progeny showing genetic recombination. Sclerotia formed in crops are dispersed onto the soil surface at harvest and are predominantly produced by single strains of one mating type. Less commonly, sclerotia may be fertilized during co-infection of crops with sexually compatible strains. In this study, laboratory and field experiments were performed to examine sexual reproduction in single-strain and fertilized sclerotia following exposure of sclerotia to natural fungal populations in soil. Female and male roles and mitochondrial inheritance in A. flavus were also examined through reciprocal crosses between sclerotia and conidia. Single-strain sclerotia produced ascospores on soil and progeny showed biparental inheritance that included novel alleles originating from fertilization by native soil strains. Sclerotia fertilized in the laboratory and applied to soil before ascocarp formation also produced ascospores with evidence of recombination in progeny, but only known parental alleles were detected. In reciprocal crosses, sclerotia and conidia from both strains functioned as female and male, respectively, indicating A. flavus is hermaphroditic, although the degree of fertility depended upon the parental sources of sclerotia and conidia. All progeny showed maternal inheritance of mitochondria from the sclerotia. Compared to A. flavus populations in crops, soil populations would provide a higher likelihood of exposure of sclerotia to sexually compatible strains and a more diverse source of genetic material for outcrossing.