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Chapter 4 : Mating-Type Locus Control of Cell Identity

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Abstract:

This chapter addresses how loci is identified from budding ascomycetes to filamentous ascomycetes to basidiomycetes function to specify cell identity. The chapter begins with an introduction to the cell identity determination paradigm established in the budding yeast . It explores how cell identity determination affects sexual reproduction in basidiomycetes. Through these examples, we see how cell identity determination lays the foundation for effective sexual reproduction and survival across diverse fungi. In , a single-celled ascomycete, growth can take place either clonally through haploid cell budding, or sexually through mating followed by meiosis. For most ascomycetes, the precise mechanisms by which these transcriptional regulators specify cell identity is not known; however, MAT control in is explored in more detail. An ascomycete in which cell identity determination has been studied in detail is the human fungal pathogen . A detailed expression analysis determined the transcriptional profiles of cells with targeted deletions of the regulator components in every possible combination in both the white and opaque phases. Control of cell identity by the locus in basidiomycetes expands the simple transcription factor-encoding locus seen in ascomycetes to a more complex structure. The fate of fused hyphae is determined by the interactions of the homeodomain proteins after cell fusion: if different alleles of an homeodomain (HD1) and HD2 protein from the same gene pair interact, this complex will form a heterodimeric transcriptional regulator that stimulates dikaryotic growth.

Citation: Stanton B, Hull C. 2007. Mating-Type Locus Control of Cell Identity, p 59-73. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch4
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Image of Figure 4.1
Figure 4.1

control of cell identity in . (A) In , in cells encodes the homeodomain transcription factor 1. α in α cells encodes the α-domain protein α1 and the homeodomain transcription factor α2. In diploid cells, both and α alleles are present. (B) In cells, the 1 protein is present but has no known function. The -specific genes (sg) are constitutively expressed, whereas the α-specific genes (αsg) are not expressed. In α cells, α2 represses -specific genes while α1 activates α-specific genes to specify the α cell type. In an /α diploid, α2 maintains repression of -specific genes, but it also heterodimerizes with 1 to form a transcriptional regulatory complex that represses haploid-specific genes (including α). This repression establishes the diploid cell type, allowing continued sexual development.

Citation: Stanton B, Hull C. 2007. Mating-Type Locus Control of Cell Identity, p 59-73. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch4
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Image of Figure 4.2
Figure 4.2

control of cell identity in (A) The locus of contains two alleles that specify the P or M cell type. Haploid P cells contain the allele that encodes mat1-P (homeodomain) and mat1-P (α domain) proteins. The allele is contained within M cells and encodes the mat1-M (HMG domain) and mat1-M (unknown domain) proteins. All of the proteins are required for sexual development. (B) In haploid cells, P or M is expressed constitutively to specify the P or M cell identity, respectively. In diploid P/M cells, all four proteins are expressed. M and P are thought to bind to the promoter to activate its expression (the product of which is a direct inducer of meiosis).

Citation: Stanton B, Hull C. 2007. Mating-Type Locus Control of Cell Identity, p 59-73. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch4
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Image of Figure 4.3
Figure 4.3

control of cell identity in . (A) The mating-type-like () locus of has two alleles, each housing transcription factors and three other kinds of genes. contains the homeodomain transcription factor 1 and the HMG-domain protein 2. α encodes the α-domain protein α1 and the homeodomain transcription factor α2. In addition to these proteins, both and α encode diverged alleles of a poly(A) polymerase (), an oxysterol binding protein (), and a phosphatidyl inositol kinase (). The roles of , , and in cell type determination are unknown. (B) Cells that contain only information (/ or /Δ at the locus) mate as cells because the putative transcription factor 2 activates genes involved in establishing the -type mating. Cells that contain only α information (α/α or α/Δ at the locus) mate as α cells because the predicted transcription factor α1 activates genes involved in α-type mating. Cells containing both and α information (/α at the locus) do not mate with other cells because 1 and α2 work together to repress genes that are necessary for mating and white-opaque switching. Cells that are unable to switch from white to opaque cannot undergo mating, and 1 and α2 repress this switch.

Citation: Stanton B, Hull C. 2007. Mating-Type Locus Control of Cell Identity, p 59-73. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch4
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Figure 4.4

configurations in filamentous ascomycetes. (A) The mating-type () locus of has two alleles: encodes the α-domain protein MAT1-1-1, and encodes the HMG-domain protein MAT1-2-1. (B) The + allele of encodes the HMG-domain protein FPR1. The − allele encodes the HMG-domain protein SMR2, a protein of unknown class, SMR1, and the α-domain protein FMR1. (C) The allele of encodes the HMG-domain protein MAT a-1 and a protein of unknown class, MAT a-2. The allele encodes the HMG-domain protein MAT A-3, a protein of unknown class, MAT A-2, and the α-domain protein MAT A-1.

Citation: Stanton B, Hull C. 2007. Mating-Type Locus Control of Cell Identity, p 59-73. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch4
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Figure 4.5

control of cell and nuclear identity in . (A) Fertilization occurs between opposite mating types when a male structure fuses with a female structure and the male nucleus is transferred. In these cells, mating type (either or ) is specified by the expression of mating-type-specific proteins: is expressed in cells, and is expressed in cells. (B) After fertilization and repeated mitotic divisions, a plurinucleate cell results. The nuclei from this cell must be paired and sequestered to a dikaryotic cell that contains one nucleus of each mating type. The nuclear identity is specified by the FPR1 protein, and the nuclear identity is specified by the FMR1 and SMR2 proteins.

Citation: Stanton B, Hull C. 2007. Mating-Type Locus Control of Cell Identity, p 59-73. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch4
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Image of Figure 4.6
Figure 4.6

control of cell identity in . (A) The allele houses the cell-type-specific pheromone gene and pheromone receptor gene . contains their counterparts, and , as well as and . The products of and do not belong to any known class of proteins and have no obvious role in sexual development but have been found to be involved in mitochondrial function ( ). The locus encodes two homeodomain transcription factors, bE and bW, with and housed in the allele and and housed in the allele (B) Haploid cell types (large, open circles) are specified by the expression of the pheromone (•) and pheromone receptor (forked receptor on the cell surface) or the pheromone (▪) and pheromone receptor (semicircular receptor on cell surface). Pheromones are sensed by their corresponding receptors on the opposite cell type. These signals activate cell fusion when two cells of opposite mating types encounter one another. After cell fusion, the proteins encoded by the locus (bE and bW) interact with one another in specific combinations to specify the dikaryotic state and prepare cells for further sexual development.

Citation: Stanton B, Hull C. 2007. Mating-Type Locus Control of Cell Identity, p 59-73. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch4
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Image of Figure 4.7
Figure 4.7

control of cell identity in (A) The locus contains four pairs of divergently transcribed genes that each encode two homeodomain transcription factors, HD1 and HD2. The pair is contained within the α sublocus, while the β sublocus contains the and pairs. (These pairs are not always complete and sometimes encode only one of the two genes.) Lettering within the gene name refers to the gene pair from which it originated, while the number indicates the type of homeodomain it represents ( for HD1 and for HD2). The locus contains three subfamilies of genes. Each subfamily has two genes encoding pheromones ( and one gene encoding a pheromone receptor (. The pheromone products of one subfamily are proposed to interact with the pheromone receptor of an allelic subfamily. (B) The products of both the and mating-type loci act to initiate and maintain the dikaryotic state. The filamentous dikaryon contains one nucleus from each mating type in each cell and characteristic clamp connections (domed structures between adjacent filament cells). The products of the locus (pheromones and pheromone receptors) control nuclear migration and clamp cell fusion, while the products of the locus (HD1 and HD2 homeodomain proteins) control the expression of genes required to drive dikaryon formation, specifically to coordinate nuclear division and initiate clamp cell formation.

Citation: Stanton B, Hull C. 2007. Mating-Type Locus Control of Cell Identity, p 59-73. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch4
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Image of Figure 4.8
Figure 4.8

control of cell identity in . (A) The mating-type () locus of contains pheromones, pheromone receptors, and homeodomain transcription factors as well as many genes with no apparent role in cell type determination. A schematic of the locus for var. is shown. encodes three copies of the MF pheromone, the putative pheromone receptor Ste3, and the homeodomain transcription factor Sxi2. α encodes three copies of the MFα pheromone, the putative pheromone receptor Ste3α, and the homeodomain transcription factor Sxi1α. The remaining genes have related but diverged alleles in both and α. Note: schematic diagram is not to scale. () The determinants of haploid cell identity are unknown; however, it is likely that pheromones and pheromone receptors play a role. The expression of could specify the mating type, and the expression of α could specify the α mating type. Pheromones would be sensed by surface receptors of opposite mating types to activate cell fusion when two cells of opposite mating types are in close proximity to one another. After cell fusion has taken place, the homeodomain transcription factors Sxi1α and Sxi2 are predicted to interact with one another to activate the expression of genes involved in the specification of the dikaryotic state. The dikaryon is then capable of undergoing further sexual development.

Citation: Stanton B, Hull C. 2007. Mating-Type Locus Control of Cell Identity, p 59-73. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch4
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