Heterothallism

Heterothallic species have sexes that reside in different individuals. The term is applied particularly to distinguish heterothallic fungi, which require two compatible partners to produce sexual spores, from homothallic ones, which are capable of sexual reproduction from a single organism.

In heterothallic fungi, two different individuals contribute nuclei to form a zygote. Examples of heterothallism are included for ''Saccharomyces cerevisiae, Aspergillus fumigatus, Aspergillus flavus'', ''Penicillium marneffei'' and ''Neurospora crassa''. The heterothallic life cycle of ''N. crassa'' is given in some detail, since similar life cycles are present in other heterothallic fungi.

Life cycle of ''Saccharomyces cerevisiae''

The yeast ''Saccharomyces cerevisiae'' is heterothallic. This means that each yeast cell is of a certain mating type and can only mate with a cell of the other mating type. During vegetative growth that ordinarily occurs when nutrients are abundant, ''S. cerevisiae'' reproduces by mitosis as either haploid or diploid cells. However, when starved, diploid cells undergo meiosis to form haploid spores. Mating occurs when haploid cells of opposite mating type, MATa and MATα, come into contact. Ruderfer et al. pointed out that such contacts are frequent between closely related yeast cells for two reasons. The first is that cells of opposite mating type are present together in the same ascus, the sac that contains the tetrad of cells directly produced by a single meiosis, and these cells can mate with each other. The second reason is that haploid cells of one mating type, upon cell division, often produce cells of the opposite mating type with which they may mate.

Katz Ezov et al. presented evidence that in natural ''S. cerevisiae'' populations clonal reproduction and a type of “self-fertilization” (in the form of intratetrad mating) predominate. Ruderfer et al. analyzed the ancestry of natural ''S. cerevisiae'' strains and concluded that outcrossing occurs only about once every 50,000 cell divisions. Thus, although ''S. cerevisiae'' is heterothallic, it appears that, in nature, mating is most often between closely related yeast cells. The relative rarity in nature of meiotic events that result from outcrossing suggests that the possible long-term benefits of outcrossing (e.g. generation of genetic diversity) are unlikely to be sufficient for generally maintaining sex from one generation to the next. Rather, a short-term benefit, such as meiotic recombinational repair of DNA damages caused by stressful conditions such as starvation may be the key to the maintenance of sex in ''S. cerevisiae''.Birdsell JA, Wills C (2003). The evolutionary origin and maintenance of sexual recombination: A review of contemporary models. Evolutionary Biology Series >> Evolutionary Biology, Vol. 33 pp. 27-137. MacIntyre, Ross J.; Clegg, Michael, T (Eds.), Springer.

Life cycle of ''Aspergillus fumigatus''

''Aspergillus fumigatus'', is a heterothallic fungus. It is one of the most common ''Aspergillus'' species to cause disease in humans with an immunodeficiency. ''A. fumigatus'', is widespread in nature, and is typically found in soil and decaying organic matter, such as compost heaps, where it plays an essential role in carbon and nitrogen recycling. Colonies of the fungus produce from conidiophores thousands of minute grey-green conidia (2–3 μm) that readily become airborne. A. fumigatus possesses a fully functional sexual reproductive cycle that leads to the production of cleistothecia and ascospores.

Although ''A. fumigatus'' occurs in areas with widely different climates and environments, it displays low genetic variation and lack of population genetic differentiation on a global scale. Thus the capability for heterothallic sex is maintained even though little genetic diversity is produced. As in the case of ''S. cereviae'', above, a short-term benefit of meiosis may be the key to the adaptive maintenance of sex in this species.

Life cycle of ''Aspergillus flavus''

''A. flavus'' is the major producer of carcinogenic aflatoxins in crops worldwide. It is also an opportunistic human and animal pathogen, causing aspergillosis in immunocompromised individuals. In 2009, a sexual state of this heterothallic fungus was found to arise when strains of opposite mating type were cultured together under appropriate conditions.

Sexuality generates diversity in the aflatoxin gene cluster in ''A. flavus'', suggesting that production of genetic variation may contribute to the maintenance of heterothallism in this species.

Life cycle of ''Talaromyces marneffei''

Henk et al. showed that the genes required for meiosis are present in T. marneffei, and that mating and genetic recombination occur in this species.

Henk et al. concluded that ''T. marneffei'' is sexually reproducing, but recombination in natural populations is most likely to occur across spatially and genetically limited distances resulting in a highly clonal population structure. Sex is maintained in this species even though very little genetic variability is produced. Sex may be maintained in ''T. marneffei'' by a short-term benefit of meiosis, as in ''S. cerevisiae'' and ''A. fumigatus'', discussed above.

Life cycle of ''Neurospora crassa''

The sexual cycle of '' N. crassa'' is heterothallic. Sexual fruiting bodies (perithecia) can only be formed when two mycelia of different mating type come together. Like other ascomycetes, ''N. crassa'' has two mating types that, in this case, are symbolized by ‘A’ and ‘a’. There is no evident morphological difference between the ‘A’ and 'a' mating type strains. Both can form abundant protoperithecia, the female reproductive structure (see figure, top of §). Protoperithecia are formed most readily in the laboratory when growth occurs on solid (agar) synthetic medium with a relatively low source of nitrogen. Nitrogen starvation appears to be necessary for expression of genes involved in sexual development. The protoperithecium consists of an ascogonium, a coiled multicellular hypha that is enclosed in a knot-like aggregation of hyphae. A branched system of slender hyphae, called the trichogyne, extends from the tip of the ascogonium projecting beyond the sheathing hyphae into the air. The sexual cycle is initiated (i.e. fertilization occurs) when a cell (usually a conidium) of opposite mating type contacts a part of the trichogyne (see figure, top of §). Such contact can be followed by cell fusion leading to one or more nuclei from the fertilizing cell migrating down the trichogyne into the ascogonium. Since both ‘A’ and ‘a’ strains have the same sexual structures, neither strain can be regarded as exclusively male or female. However, as a recipient, the protoperithecium of both the ‘A’ and ‘a’ strains can be thought of as the female structure, and the fertilizing conidium can be thought of as the male participant.

The subsequent steps following fusion of ‘A’ and ‘a’ haploid cells, have been outlined by Fincham and Day, and by Wagner and Mitchell. After fusion of the cells, the further fusion of their nuclei is delayed. Instead, a nucleus from the fertilizing cell and a nucleus from the ascogonium become associated and begin to divide synchronously. The products of these nuclear divisions (still in pairs of unlike mating type, i.e. ‘A’ / ‘a’) migrate into numerous ascogenous hyphae, which then begin to grow out of the ascogonium. Each of these ascogenous hypha bends to form a hook (or crozier) at its tip and the ‘A’ and ‘a’ pair of haploid nuclei within the crozier divide synchronously. Next, septa form to divide the crozier into three cells. The central cell in the curve of the hook contains one ‘A’ and one ‘a’ nucleus (see figure, top of §). This binuclear cell initiates ascus formation and is called an “ascus-initial” cell. Next the two uninucleate