Loss of Self‐Incompatibility by Mating‐Type Switching

Abstract

Sexual reproduction requires the fusion of compatible gametes. In many organisms without sexes, compatibility is described by the genes located at the mating‐types locus, and mating is restricted to haploid individuals carrying different alleles at this locus. To assure mating when no partners are around, a variety of mechanisms evolved that render two clonally derived cells compatible with each other, known as homothallism. This occurs mostly by incorporation of the two mating‐type alleles into the same haploid genome; however, this comes at a cost. Mating‐type switching reduces these costs by suppressing one of the mating‐type alleles. Clonal compatibility is maintained by structurally modifying the gene content or mating‐type conformation that defines the mating‐type identity of the cell. The presumed evolutionary steps from a self‐incompatibility to switching require incorporation of both mating‐type genes, silencing of one type, evolving a switching mechanism and optimising this mechanism.

Key Concepts

  • Mating types define compatibility between haploid individuals and are generally described by a single locus.
  • In most species, only two mating types exist that strongly reduce the availability of compatible mates.
  • Incorporation of the genes of both mating types (the mating‐type cassettes) into the same haploid genome can lead to self‐compatibility but comes at a large cost.
  • Under low densities, the benefit of self‐compatibility can overcome the cost of carrying both mating‐type cassettes.
  • Selection for suppression of one of the cassettes can restore a mostly outcrossing (heterothallic) phenotype, while probably retaining occasional selfing.
  • After the evolution of silencing, switching during asexual growth is an efficient way of locally generating compatible genotypes.
  • Suppression by dominance of mating type is likely to lead to switching by disruption or deletion.
  • Suppression is determined by the location of a locus and likely selects for evolution of positional switching.

Keywords: mating type; self‐incompatibility; self‐compatibility; fungi; mate finding; asexual reproduction; density dependence; yeast

Figure 1. Extracellular communication between cells benefits from asymmetry between signalling pheromones and perception of those pheromones. (a) When all cells secrete the same pheromone, distinction between self‐ and foreign‐produced pheromones is not possible. The gradient will always be locally declining because a cell will mainly perceive self‐produced pheromones. (b) Mating types can introduce variation by regulating expression of a pheromone and receptor that are not self‐compatible but respond to the pheromone of the opposite mating type. The pheromone gradient (for central individual indicated by the arrow) can thus be used to locate a conspecific individual.
Figure 2. Different mating‐type switching mechanisms. (a) Mating‐type switching in the flip‐flop system occurs by inversion of a region that contains the two mating‐type cassettes at the terminal end. The location of one of the cassettes close to a telomeric or centromeric region suppresses expression due to extension of the heterochromatic region (indicated by the circles). A repetitive region (dark squared) is used to induce switching. (b) In the three‐cassette system, two silent cassettes are present, which each can be used to introduce information into the active locus. (c) Unidirectional switching occurs if the active mating‐type cassette is lost, thereby releasing suppression of the other cassette.
Figure 3. Assumed evolutionary transitions from heterothallism to mating‐type switching through (proto‐)homothallism. Homologous recombination between the mating‐type idiomorphs into a haploid genome leads to a self‐compatible strain (proto‐homothallic) that carries a cost for expressing both mating types. Selection against this cost can lead to evolution of homothallism or silencing of one of the two mating‐type cassettes. Silencing can occur through interaction between the mating types (one dominant cassette) or through positional silencing. Silencing renders the genotype functionally heterothallic again, but incomplete suppression can occasionally result in homothallic self‐fertilisation. Incorporation of a switching mechanism maintains heterothallisms but increases the efficiency for self‐compatibility. Selection will continue to reduce costs of carrying both mating types. Black arrows indicate expected transitions towards switching. Grey arrows show less likely changes. Border colours indicate (mixes of) reproductive mode as described in the legend.
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Further Reading

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Pannell JR and Voillemot M (2001) Evolution and ecology of plant mating systems. In: eLS. Chichester: John Wiley & Sons, Ltd.

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Nieuwenhuis, Bart PS(Aug 2017) Loss of Self‐Incompatibility by Mating‐Type Switching. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0027279]