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Chapter 16 : Cloning the Mating-Type Genes of : A Historical Perspective

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Abstract:

This chapter describes the life cycle of and ascribes function to the principal genetic determinants, the mating-type genes, that govern it, and presents the strategies that were devised for the successful isolation of these genes. In the world wide population of , a large number of A and B mating specificities are conferred by the extensive series of alleles of the genes residing at these loci. In and other Basidiomycetes, the genetic variability ensured by mating is further enhanced by the multiallelic mating-type system. Extraordinarily exact and regular in its supervision of mycelial interactions, the mating-type system of is not influenced by external factors such as nutrition and environmental conditions. Genomic DNA was isolated from a strain carrying the Aα4 allele to make the library used in the chromosomal walk from PAB1. The library was constructed in a cosmid vector in which the TRP1 gene would be the selectable marker in transformation. The mating genes are similar to other genes (and many fungal genes in general) in that there are no obvious promoter sequences such as a TATA box or CAAT box. Information from several previous studies was incorporated to create a successful strategy to isolate active fragments from the Bα and Bβ loci of .

Citation: Stankis M, Specht C. 2007. Cloning the Mating-Type Genes of : A Historical Perspective, p 267-282. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch16
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Figure 16.1

(A) Life cycle of in diagrammatic representation. See the text for details. (B) Nuclear migration (shown for one mate). In a compatible interaction, a reciprocal exchange of nuclei takes place: in the fusion cell, the nucleus of each mate divides, and the daughter nuclei migrate into the cells of the other mating type. The donor nuclei rapidly divide, as they migrate throughout the existing mycelium of the other mate. Eventually they reach the apical cells. The nuclei move at a speed exceeding the rate of radial growth of the mycelia, i.e., at velocities of 1 to 6 mm per h, depending on the temperature ( ). At these velocities, a migrating nucleus can traverse one cell, which is typically 100 µm in length, in 1 min. Microtubules and microfibrils are associated with the migrating nuclei ( ). Nuclear migration requires the rapid dissolution of the septa between cells, a process that has been correlated with the production of a specific hydrolytic enzyme, R-glucanase ( ). Nuclear migration is regulated by the mating-type genes. (C) Conjugate nuclear division. The migrating nuclei arrive at the growing hyphal tips, where they pair, but do not fuse, with the resident nucleus. A mechanism for segregating paired nuclei, common to many Basidiomycetes, ensures that each newly formed cell has two nuclei, one from each parent. This is accomplished through the formation of a unique structure called a hook cell or clamp connection. Prior to nuclear division, a short branch arises on the side of the apical cell, into which one of the nuclei moves. Both nuclei then divide in synchrony and new cell walls form perpendicular to the spindles to generate three cells. One of each of the daughter nuclei is retained in the new apical cell, one in the hook cell and one in the subterminal cell. The hook or clamp cell then fuses with the subterminal cell, providing a bridge for the previously entrapped daughter nucleus to move into the subapical cell, where it pairs with its partner. This restores the dikaryotic condition to the penultimate cell. The presence of fused hook cells (clamp connections) can be used to identify dikaryotic mycelia. The formation of the hook cell and synchronized nuclear division are regulated by the genes, and the fusion of the hook cell with the subterminal cell is regulated by the genes. (D) Processes controlled by the and mating-type genes of . Adapted from Stankis et al. ( ).

Citation: Stankis M, Specht C. 2007. Cloning the Mating-Type Genes of : A Historical Perspective, p 267-282. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch16
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Image of Figure 16.2
Figure 16.2

(A) Selection strategy for the isolation of the mating-type gene. Following the isolation of the linked gene ( ), a chromosomal “walk” to 4 was accomplished by DNA-DNA hybridization of overlapping clones from a cosmid library ( ). Hypothesizing that the addition of 4 DNA to the genome of the recipient 1 strain, to create transformants merodiploid for , would activate -regulated developmental events, transformants at each step of the walk were screened by light microscopy for unfused hook cells. (B) Selection strategy for the isolation of the and mating-type genes. A mixture of protoplasts prepared from two strains having compatible mating types ( and ) and the same mating type (2 2) were transformed with a genomic library constructed with DNA from a b1 strain. Full sexual development, i.e., the formation of fruiting bodies, could occur if a transformant, merodiploid for either the or mating-type genes, mated with an -compatible regenerate, or fused with one during protoplast manipulation. Two fruiting transformants yielded haploid basidiospores which revealed the -activated phenotype ( ). The transforming and DNA was recovered using plasmid rescue techniques ( ).

Citation: Stankis M, Specht C. 2007. Cloning the Mating-Type Genes of : A Historical Perspective, p 267-282. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch16
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Image of Figure 16.3
Figure 16.3

(A) A generalized map of the mating-type region of Sequences demonstrating mating activity in , 3, 4, 5, and specificities average about 50% similarity, although they are embedded in a region of DNA common to all strains examined, as denoted by the shaded line. The transition from common sequence, encoding ( mitochondrial intermediate peptidase), at the left end, to the heterogeneous region is gradual in all mating types, except , where the transition (not shown) is extremely abrupt due to a natural deletion of the Z gene. The right boundary of the common sequence is approximately 7 to 8.5 kb from that of the left, except in , where heterogeneous DNA extends only 4.5 kb ( ). The and mating-type genes are a dyad of divergently transcribed homeodomain (HD1 and HD2) genes whose products regulate sexual development. Gene has no apparent function in mating. The coding region of each gene is boxed, and introns conserved among the alleles of each gene are shown as vertical black lines. The starred intron in HD2 is inserted between the codons for the highly conserved amino acid residues W and F. The direction of transcription is depicted by an arrow. GenBank accession numbers of DNA sequences used to generate map: , U13942 and M97179; , L43072, U13943, and M97180; , U13944 and M97181; 5, U22049; 6, AF274566. (B) A generalized map of the α Y and Z proteins and the β V6 protein. Each protein is depicted as a solid line with NH-and COOH-termini as denoted for α Y. The Y proteins all contain an HD2 homeodomain, a predicted coiled coil that overlaps a 28-residue bipartite nuclear localization sequence (NLS) that is embedded within a basic region ( ), and a serine-rich region (not shown). These characteristics have been observed for each Y protein studied to date, and the position of each feature is approximately the same in each Y allele. The Z proteins also contain features bearing on their presumptive function as transcriptional regulators, which reside in the same relative position in each allele: an atypical homeodomain sequence (HD1), two highly acidic 30-amino-acid regions rich in glutamate and aspartate (ARs), and two predicted coiled-coil regions (white ovals). The C-terminal regions of Z which are predicted to form a coiled coil display extremely high identity among the alleles ( ). The interacton of coiled coils is the mechanism by which both homo- and heterodimerizations of regulatory transcription factors occur in many organisms. Discussions and graphic presentations of the Y and Z regions which are involved in mating interactions, specificity, and binding are available ( ). The V6 protein, encoded by , displays an HD2 homeodomain motif. (C) The active regulatory complex encoded by and . Activation of development follows mating via the interaction of Y and Z proteins from compatible mates. An active complex is formed from the HD1 protein from one mate in combination with the HD2 protein from the other mate, that is, Yi in combination with Zj or Yj in combination with Zi. The heteromultimer is postulated to be a transcription factor that directs development down a new pathway by binding upstream of specific target genes ( ). The V protein, encoded at the locus, may be the HD2 partner of an HD1-HD2 pair, similar to the composition of the active products.

Citation: Stankis M, Specht C. 2007. Cloning the Mating-Type Genes of : A Historical Perspective, p 267-282. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch16
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