Sex, drugs and recombination: the wild life of Aspergillus

Abstract

Throughout the eukaryotes, sexual reproduction is an almost universal phenomenon. However, within the Kingdom Fungi, this relationship is not so clear-cut. Fungi exhibit a spectrum of reproductive modes and life-cycles; amongst the better known species, sexual reproduction is often facultative, can be rare, and in over half of the known Ascomycota (the moulds) is unknown (Taylor etal. 1999). However, over the last decade, it has become apparent that many of these asexual mitosporic taxa undergo cryptic recombination via unobserved mechanisms and that wholly asexual fungi are, in fact, a rarity (Taylor etal. 1999, 2001; Heitman 2010). This revolution in our understanding of fungal sexuality has come about in two ways: Firstly, sexual reproduction leaves an imprint on fungal genomes by maintaining genes required for mating and by generating patterns of mutation and recombination restricted to meiotic processes. Secondly, scientists have become better at catching fungi in flagrante delicto. The genus Aspergillus is one such fungus where a combination of population genetics, genomics and taxonomy has been able to intuit the existence of sex, then to catch the fungus in the act and formally describe their sexual stages. So, why are sexy moulds exciting? One species in particular, Aspergillus flavus, is notorious for its ability to produce a diverse array of secondary metabolites, of which the polyketide aflatoxins (AF) are carcinogenic and others (such as cyclopiazonic acid) are toxigenic. Because of the predilection of A.flavus to grow on crops, such as peanuts, corn and cotton, biocontrol is widely used to mitigate infection by pre-applying nonaflatoxigenic (AF-) strains to competitively exclude the wild-type AF+ strains. However, the eventual fate in nature of these biocontrol strains is not known. In this issue of Molecular Ecology, Olarte etal. (2012) make an important contribution by using laboratory crosses of A.flavus to show that not only is AF highly heritable, but AF- strains can become AF+ via crossing over during meiosis. This observation has raised the spectre of cross-breeding and non-mendelian inheritance of AF between native and biocontrol strains of the fungus, leading to an increase in the natural diversity of the fungus with perhaps unanticipated consequences.