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Chapter 6 : Mating and Parasexual Genetics in

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Abstract:

This chapter outlines the discovery that can be coaxed to mate in the laboratory and the recognition that a phenotypic switching system—white-opaque switching—is intimately involved in this process. Many features of mating in relate to prior knowledge of the mating machinery of the model organism . Of particular interest are the departures from the “paradigm” which serve to underscore the unique features of the mating apparatus. For these reasons, the chapter begins by briefly comparing the two organisms and reviewing the mating cycle in . Mating in is dependent on signaling between cells of opposite mating types. This chapter addresses how the mating-type loci regulate gene expression to give rise to three distinctive cell types, a, α, and a/α. It talks about the identities of the genes that make up the different classes of cell-type-specific genes in C. albicans: a1-α2-repressed, a-specific, and α-specific genes. It discusses the apparent paradox that, although has a robust parasexual cycle that can be readily observed in the laboratory, population studies indicate that the population is largely clonal. The critical role of white-opaque switching in mating seems unique to and may reflect a long evolutionary relationship between mating and life inside a mammalian host. Chromosome loss, a general propensity of , provides a means of completing a parasexual cycle that in principle can be used to generate diversity.

Citation: Miller M, Johnson A. 2006. Mating and Parasexual Genetics in , p 71-88. In Heitman J, Filler S, Edwards, Jr. J, Mitchell A (ed), Molecular Principles of Fungal Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555815776.ch6

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Figures

Image of Figure 1.
Figure 1.

Mating in Cell type is specified by the configuration of the locus, which encodes regulators of mating gene expression. cells express -specific genes (asg), including the -factor pheromone (circles) and the α-factor receptor. α cells encode α2, which represses the -specific genes, and α1, which activates the α-specific genes (αsg), including α-factor mating pheromone (squares) and the -factor pheromone receptor. /α cells contain both 1 and α2, which heterodimerize and together repress the haploid-specific genes (hsg) that are required for mating in both cell types. The 1-α2 heterodimer also represses α1, thereby repressing the α-specific genes.

Citation: Miller M, Johnson A. 2006. Mating and Parasexual Genetics in , p 71-88. In Heitman J, Filler S, Edwards, Jr. J, Mitchell A (ed), Molecular Principles of Fungal Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555815776.ch6
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Image of Figure 2.
Figure 2.

A comparison of the locus and the locus. (A) The locus contains genes for three transcriptional regulatory genes: 1, α1, and α2. DNA sequence inside of the dashed lines is nonidentical between homologs. (B) The homologous locus contains three transcriptional regulatory genes (outlined): 1, α1, α2, and an additional regulator, 2. In addition, the locus contains two alleles each of genes homologous to a poly(A) polymerase (), an oxysterol binding protein (), and a phosphatidylinositol kinase () with no apparent function in mating. These genes are omitted in subsequent figures for clarity.

Citation: Miller M, Johnson A. 2006. Mating and Parasexual Genetics in , p 71-88. In Heitman J, Filler S, Edwards, Jr. J, Mitchell A (ed), Molecular Principles of Fungal Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555815776.ch6
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Image of Figure 3.
Figure 3.

Constructed mating strains of . Mating strains have been constructed from /α diploids by two methods. (A) Targeted deletion of both regulatory proteins in one allele of the locus results in and α mating strains. (B) When grown on sorbose, diploids are induced to lose one homolog of chromosome 5 (on which the locus resides), resulting in a hemizygous strain. When cultured on rich medium (YEPD), the single remaining homolog of chromosome 5 duplicates, producing a homozygous / or α/α strain.

Citation: Miller M, Johnson A. 2006. Mating and Parasexual Genetics in , p 71-88. In Heitman J, Filler S, Edwards, Jr. J, Mitchell A (ed), Molecular Principles of Fungal Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555815776.ch6
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Image of Figure 4.
Figure 4.

White-opaque switching. (A, B) White colonies with opaque sectors. When grown on medium containing the dye phloxine B, opaque sectors are darkly stained. (C) White cells of are ellipsoidal when grown under rich conditions. Here, they are visualized by scanning electron microscopy. Preparation and visualization were done with the assistance of the Electron Microscopy Laboratory, University of California, Berkeley. (D) Opaque cells of are larger and more elongated than white cells. In addition, their surface is covered with “pimple” structures of unknown function. (E) White cells are visualized by DIC microscopy. (F) Opaque cells are visualized by DIC microscopy. (G) The 1 and α2 transcriptional regulators together repress white-opaque switching in cells. Reprinted from ( ) and ( ) with permission of the publishers.

Citation: Miller M, Johnson A. 2006. Mating and Parasexual Genetics in , p 71-88. In Heitman J, Filler S, Edwards, Jr. J, Mitchell A (ed), Molecular Principles of Fungal Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555815776.ch6
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Image of Figure 5.
Figure 5.

Pheromone response in and . (A) cells “shmoo” in response to α-factor pheromone. (Image courtesy of Emma McCullagh, University of California, San Francisco.) opaque cells undergo a similar polarized growth response in the presence of α-factor. (B) Pheromone signaling in requires many signaling components, including a pheromone receptor (Ste2), a heterotrimeric G-protein (Gpa1, Ste4, Ste18), a protein kinase signaling cascade (Ste20, Ste11, Ste7, Fus3), and a transcriptional regulator (Ste12). encodes homologs of several pheromone signaling components. signaling components that are required for mating are shaded in dark gray, and components that are only partially required are shaded in light gray. The Cek1 and Cek2 MAP kinases are partially redundant in mating. Unshaded components have not been tested.

Citation: Miller M, Johnson A. 2006. Mating and Parasexual Genetics in , p 71-88. In Heitman J, Filler S, Edwards, Jr. J, Mitchell A (ed), Molecular Principles of Fungal Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555815776.ch6
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Image of Figure 6.
Figure 6.

Cell-type determination in and . (A) In cells, the -specific genes (asg) and haploid-specific genes (hsg) are transcribed constitutively. Expression is indicated by an arrow or block next to each class of genes. In α cells, the -specific genes are repressed by the transcriptional regulator α2, and the α-specific genes (αsg) are activated by the α1 transcriptional regulator. As in cells, the haploid-specific genes are constitutively expressed. In /α cells, the 1-α2 heterodimer directly represses expression of haploid specific genes (hsg) and the α1 regulator required for α-specific gene expression. Additionally, 2 represses expression of the -specific genes. (B) In cells, expression of the -specific genes depends on the positive transcriptional regulator 2. The opaque state is also required for the expression of -specific genes. In α cells, the 2 regulator is absent, and the -specific genes are not expressed. Instead, α1 and the opaque state activate expression of the α-specific genes. In /α cells, the 1-α2 heterodimer represses the switch to opaque, thereby preventing expression of the - and α-specific genes. Additionally, the 1- α2 regulator represses genes that participate in mating in both cell types, the equivalents of “haploid-specific genes” in the diploid organism.

Citation: Miller M, Johnson A. 2006. Mating and Parasexual Genetics in , p 71-88. In Heitman J, Filler S, Edwards, Jr. J, Mitchell A (ed), Molecular Principles of Fungal Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555815776.ch6
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Image of Figure 7.
Figure 7.

Mating gene regulation in . A number of genes are controlled by 1-α2, α1, and possibly by 2, in the SC5314 background. Genes that are controlled by a particular regulator (top row) are entered into each column below the regulator. In the leftmost column, these target genes are classified according to their function in mating. Six genes are regulated by 1-α2 in white-phase cells. Genes that are upregulated in the opaque phase are indirectly controlled by 1-α2 and include members from all categories of genes on the left. While the α-specific genes (controlled by α1) have been identified, the -specific genes (depending on 2 for their expression) have not been rigorously identified. Three candidate -specific genes are induced upon exposure to α-factor and are likely to be -specific genes, based on their roles in mating. Genes induced in cells upon exposure to α-factor mating pheromone are also included above.

Citation: Miller M, Johnson A. 2006. Mating and Parasexual Genetics in , p 71-88. In Heitman J, Filler S, Edwards, Jr. J, Mitchell A (ed), Molecular Principles of Fungal Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555815776.ch6
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Image of Figure 8.
Figure 8.

A schematic for karyogamy in . (A) and α opaque cells respond to secreted pheromones by forming polarized growth projections. (B) Mating projections grow toward one another, and nuclei migrate into the projections. (C) Cell fusion between two cells forms a zygote and combines the two parent nuclei into the same cytoplasmic compartment. (D) The two nuclei undergo karyogamy (nuclear fusion). A nascent bud begins to emerge near the site of cell fusion. (E) The single remaining nucleus divides, and the daughter nucleus migrates into the daughter bud prior to septation. The daughter cell is tetraploid and contains information from both parental nuclei.

Citation: Miller M, Johnson A. 2006. Mating and Parasexual Genetics in , p 71-88. In Heitman J, Filler S, Edwards, Jr. J, Mitchell A (ed), Molecular Principles of Fungal Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555815776.ch6
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Image of Figure 9.
Figure 9.

A parasexual cycle for . diploid/ and α/α opaque cells must switch to the opaque phase in order to mate. The mating products are /α tetraploids, and they quickly revert to the white phase. Tetraploids are stable under standard laboratory conditions, but can be induced to undergo rapid, concerted chromosome loss on certain growth media. Chromosomes are lost randomly until a diploid state is reached (within the resolution of flow cytometry). Because chromosome loss is random, all three possible combinations of alleles are generated during chromosome loss: /α ,/, and α/α. The resulting diploid and α/α products are competent to switch to opaque and mate with cells of the opposite type, thereby completing a parasexual cycle.

Citation: Miller M, Johnson A. 2006. Mating and Parasexual Genetics in , p 71-88. In Heitman J, Filler S, Edwards, Jr. J, Mitchell A (ed), Molecular Principles of Fungal Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555815776.ch6
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