Although many fungi are currently classified as asexual, it is possible that laboratory conditions conducive to mating remain to be defined, or compatible mating partners have not as yet been isolated from natural environments for these species. An example is the recent discovery of the sexual cycle of the fungal pathogen Aspergillus fumigatus, which requires six months incubation under specialized conditions in the dark [13]. It is also possible that the same fungus can engage in different modes of reproduction (sexual and asexual) in different locations (for example, when free-living or in a multicellular host) or at different times (for example, sexual reproduction of some plant pathogens is coincident with specific developmental stages of their hosts). To fully understand the mating behavior of a fungus requires extensive environmental sampling and laboratory mating assays.
Detailed genomic and genetic studies can also provide clues as to whether species may be sexual. Whole genome analyses of many putatively asexual fungi have often revealed the presence of MAT loci and suites of apparently intact mating and meiotic genes. In their survey of the red yeast Sporidiobolales, for example, Coelho et al. [3] found retention of apparently functional copies of the genes encoding the homeodomain mating-type transcriptional regulators and the pheromone receptors in several of the 16 asexual species investigated. If sexuality has been lost in these species, the loss must have been very recent to avoid the erosive signature of gene loss and decay. Population genetic studies have often revealed that presumptive asexual fungi exist in a 1:1 ratio of opposite mating types and with evidence of recent recombination, possibly reflecting cryptic sexuality.
One question facing the approach of interpreting the reproductive mode through genome analysis is: what would the genome of an asexual fungus look like? Coelho et al. [3] found several asexual species of red yeasts in which the mating-type genes encoding the homeodomain transcription factors are disabled by mutations, and infer that these mutations are a cause, or a consequence, of asexuality. Yet Lodderomyces elongisporus, which is classified as a self-fertile sexual fungus (it makes an ascus with a single lone spore), has no discernible MAT locus (it lacks the a1, a2, α1, and α2 genes), and is also missing the a factor pheromone, the a pheromone receptor, and the a pheromone transporter genes required for signaling in mating [1]. Is it truly sexual, or does it produce one-spored asci asexually? Candida parapsilosis is an a/a diploid for which no mating has been observed; it has also lost the a1 HD transcription factor and lacks a key region of the α-factor receptor involved in response of Candida albicans white cells to pheromone; additionally, no isolate of the α mating type has yet been isolated from nature or patients [1, 7]. Thus, C. parapsilosis could be asexual or it may undergo cryptic unisexual mating like C. albicans and Cryptococcus neoformans [14, 15]. Or rare α isolates may remain to be discovered. Candida glabrata is a haploid yeast related to S. cerevisiae, and natural populations contain both a and α isolates; however, no mating has yet been detected in the lab despite prodigious efforts [5]. C. glabrata could be asexual, or it may simply be that its mating rituals will require further wile on our part to discern patterns of cryptic sexuality. Finally, a note of caution. Candida lusitaniae has lost the α2 HD gene at MAT, and Candida guilliermondii has lost both the a1 and α2 genes, yet both have maintained complete sexual cycles [1, 2]. Thus, loss of MAT genes is not synonymous with asexuality.
Given the flexible reproduction modes and enormous diversities of phenotypic traits and environmental niches of fungi, as well as their complicated population dynamics, studies of their reproductive and mating systems are surely going to provide us with more surprises.