Academic journal article Genetics

Ancient Trans-Specific Polymorphism at Pheromone Receptor Genes in Basidiomycetes

Academic journal article Genetics

Ancient Trans-Specific Polymorphism at Pheromone Receptor Genes in Basidiomycetes

Article excerpt

ABSTRACT

In the majority of sexual organisms, reproduction occurs almost exclusively through the combination of distinct and alternate forms, called sexes or mating types. In some fungi, there can be dozens to hundreds of alternate alleles that determine compatible mating types. Such extensive polymorphism is expected to be maintained by balancing selection, and in extreme cases may give rise to trans-specific polymorphism. Here, we analyzed sequences of two pheromone receptors in the Microbotryum fungal species complex (Basidiomycota), which has only two alternate mating types. Several lines of evidence strongly suggest that the pheromone receptors are two allelic sequences acting to determine the alternate A1 and A2 mating types required for mating in Microbotryum. Phylogenetic trees of pheromone receptors in the Microbotryum species complex indicated a trans-specific polymorphism: the Microbotryum sequences from a given mating type were all more similar to the pheromone receptors of distantly related classes of fungi than to the alternate pheromone receptor in the Microbotryum species. A phylogenetic tree built using other known pheromone receptors from basidiomycetes showed that trans-specific polymorphism is widespread. The pheromone receptor alleles from Microbotryum appeared as the oldest, being at least 370 million years old. This represents the oldest known trans-specific polymorphism known in any organism so far, which may be due to the existence of sex chromosomes, obligate sexuality, mitochondrial inheritance linked to the mating type, and a highly selfing mating system in Microbotryum.

IN sexual organisms, reproduction occurs almost exclusively through the combination of distinct and alternate forms, called sexes or mating types. Dimorphic sex chromosomes define mating compatibility in most mammals, while more polymorphic systems, involving dozens to hundreds of alleles, determinemating types in some plants and fungi (Richman 2000). Such extensive polymorphism at mating types is maintained by negative frequency-dependent selection, the most common form of balancing selection (Richman 2000): when a matingtype allele becomes rare, it has a selective advantage because the individuals carrying it can mate with a larger proportion of other individuals. Balanced polymorphism ofmultiple alleles is therefore frequent atmating-typeloci in a wide range of organisms, such as plants, insects, and fungi (May et al. 1999; Richman 2000), and it is also pervasive in various somatic self/nonself recognition systems, such as the vertebrate major histocompatibility complex (MHC) (Hughes and Yeager 1998) and the vegetative incompatibility system in fungi (Powell et al. 2007). Consistent with rare allele advantage, nonsynonymous mutations have been found to be positively selected in several mating-type and nonself recognition systems (Richman 2000; Cho et al. 2006), including in fungi (Wu et al. 1998; Karlsson et al. 2008).

In addition to potentially maintaining large numbers of alleles, genes under balancing selection also maintain alleles far longer than neutral genetic variation because the selective advantage of an allele when it becomes rare can counteract the effects of loss due to genetic drift. In extreme cases, trans-specific polymorphism can be observed, i.e., the maintenance of multiple allelic classes that transcend species boundaries by virtue of being more ancient than the species themselves (Richman 2000). When this occurs, an allele sampled from a particular species can be more related to members of the same functional allelic class in other species than to members of different allelic classes in the same species.

Fungi are highly interesting models for studying the origin and diversity of alleles by balancing and positive selection, in particular at their mating-type genes. In heterothallic fungi, mating-type loci determine sexual compatibility: only gametes differing at these loci can mate, and basidiomycetes often have high numbers of mating types. …

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