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Chapter 21 : History of the Mating Types in

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Abstract:

This chapter presents some general features of and a synopsis of its life cycle. The life cycle of is characterized by three cell types: a cigar-shaped haploid, unicellular form that divides by budding and is nonpathogenic; a dikaryotic, filamentous form that grows at the tip cell and is pathogenic; and a diploid spore, the teliospore, formed within the tumors induced by the fungus, that is not capable of vegetative growth but germinates and undergoes meiosis to produce the haploid yeast-like form. Heterothallism and Sex Factors Stakman and Christensen demonstrated for the first time that is heterothallic. Six mutants designated (three , two , and one ) were obtained, all of which induced tumors and produced teliospores when inoculated with their progenitors, with themselves and with each other, and thus behave as “universal” alleles. The locus of was the first multiallelic mating-type locus cloned and understood at the molecular level and provided a framework in which to understand the more complex A multiallelic mating-type locus of other basidiomycetes. Strains with an inactive gene for the pheromone precursor can respond to the pheromone produced by cells of opposite mating type but they cannot induce a response in cells of opposite mating type, and strains with an inactive receptor gene can induce a response in cells of opposite mating type but cannot respond to cells of opposite mating type.

Citation: Banuett F. 2007. History of the Mating Types in , p 351-375. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch21
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Figure 21.1

Morphological transitions in the life cycle of . exhibits three forms (cell types) during its life cycle: a haploid unicellular form; a filamentous dikaryon; and a diploid spore, the teliospore (reviewed in references , and ). The transition from one form to the other entails conjugation, karyogamy, and meiosis. These processes are accompanied by changes in ploidy, growth habit, and pathogenicity (see references , and for details). These morphological transitions are governed by two unlinked mating-type loci, and , by environment, by nutrients, and possibly by plant signals (reviewed in references , and ). (From reference , with permission.)

Citation: Banuett F. 2007. History of the Mating Types in , p 351-375. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch21
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Image of Figure 21.2
Figure 21.2

Teliospore germination and meiosis. The teliospore is a diploid spore, resistant to adverse environmental conditions. It is formed within the tumors following a discrete developmental program during which changes in morphology take place and karyogamy occurs ( ). Upon germination, a short filament (the promycelium) emerges, into which the diploid nucleus migrates and undergoes meiosis to form a septate promycelium consisting of four haploid cells ( ) (A). Clones of these primary meiotic products arise by budding to produce yeast-like cells (panel A), which can be removed with the aid of a micromanipulator for single tetrad analysis (panel B). Alternatively, the teliospore is allowed to germinate and form a microcolony, which is then resuspended in water and spread on an agar surface (panel C).

Citation: Banuett F. 2007. History of the Mating Types in , p 351-375. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch21
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Image of Figure 21.3
Figure 21.3

The fuzz reaction of haploid and Fuz– diploid strains on charcoal agar. Haploid and diploid strains carrying different and alleles produce a white fuzziness due to the formation of filaments in combination with haploid tester strains ( ). Saturated cultures of tester strains (vertical lines) were cross-streaked versus haploid (top four horizontal lines) and Fuz– diploids (bottom four horizontal lines). The testers are, from left to right, (FB1), (FB2), (FB6b), and (FB6a). The horizontal lines represent, from top to bottom, strains , , , , and (class I; FB-D12-3); (class II; FB-D11-21); (class III; FB-D11-7); and (class IV; FB-D12-11) (see reference for further details). (From reference , with permission.)

Citation: Banuett F. 2007. History of the Mating Types in , p 351-375. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch21
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Image of Figure 21.4
Figure 21.4

The molecular structure and organization of the locus. The locus is the major determinant of filamentous growth and pathogencity (reviewed in references , and ) and is estimated to have 25 naturally occurring alleles ( ), each of which consists of two divergently transcribed genes, and , separated by an intergenic region of approximately 200 bp ( ). Each gene codes for a polypeptide containing a homeodomain-related motif ( ). The bW and bE polypeptides have the same structural organization, a variable region at the amino terminus and a constant region for the remainder of the polypeptide, but show no similarity except for the homeodomain region ( ). The active b protein is found only in the dikaryon and consists of a bW and a bE subunit encoded by different alleles, for example, bW1-bE2 or bW2-bE1 ( ). Each dikaryon has two different active heterodimers, but only one is necessary for activity ( ). The variable region is the specificity determinant and controls dimerization of these polypeptides ( ). The homeodomain of both bE and bW is required for activity ( ). (From reference with permission.)

Citation: Banuett F. 2007. History of the Mating Types in , p 351-375. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch21
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Image of Figure 21.5
Figure 21.5

Amino acid sequence comparison of bE and bW polypeptides. The amino acid sequences of seven bE and four bW polypeptides are shown ( ). The variable region of bE and bW encompasses the first 110 and 140 amino acids, respectively. The remainder of the polypeptide is the constant region (not shown in its entirety) and contains the homeodomain. The three helices of the homeodomain are shaded. The homeodomain of bE belongs to the atypical class of homeodomains, whereas that of bW belongs to the typical class (see reference ).

Citation: Banuett F. 2007. History of the Mating Types in , p 351-375. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch21
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Image of Figure 21.6
Figure 21.6

Deletion analysis of the locus. The or or both genes were deleted in haploid strains ( ), and the resulting mutants were tested for b activity (filament formation [Fuz phenotype] and tumor induction [Tum phenotype]) by cospotting on charcoal agar and inoculation into corn plants, respectively. The strains listed under strain 1 are derivatives of , and those under strain 2 are derivatives of . Mixtures of wild-type and strains result in a Fuz Tum phenotype (row 1). Deletion of one gene or one gene in one of the partners does not affect activity (rows 2 and 3, respectively). On the other hand, activity is abolished by deletion of both and in one of the partners (row 4), both and genes in both partners (row 5), in both partners (row 6), or in both partners (row 7). In contrast, deletion of in one partner and in the other (row 8) or of in one partner and in the other (row 9) does not abolish activity and demonstrates that and from different alleles are necessary for activity ( ). The dikaryon contains two active heterodimers, but only one is necessary for function (rows 8 and 9).

Citation: Banuett F. 2007. History of the Mating Types in , p 351-375. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch21
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Image of Figure 21.7
Figure 21.7

chimeric alleles delimit the specificity region. Chimeras between and or between and were generated by homologous recombination at the locus ( ). Three classes of chimeras were generated by the crossover events indicated by the lines. Class I chimeras exhibit specificity, class II chimeras exhibit and specificity, and class III chimeras have switched from to specificity ( ). N2 and C2 refer to the borders of the specificity region; N1 and C1 refer to the borders of the specificity region. The class II chimeras have N1 C2 borders, that is, they share one border with and the other with . Because class II chimeras have both and specificity, it has been proposed that differences at only one border are sufficient for dimerization and generation of the active heterodimer ( ). The specificity region for encompasses a region of approximately 40 amino acids, and that of encompasses a region of approximately 70 amino acids ( ). Similar conclusions were reached by Kämper et al. ( ) from yeast two-hybrid interactions and analysis of alleles.

Citation: Banuett F. 2007. History of the Mating Types in , p 351-375. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch21
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Image of Figure 21.8
Figure 21.8

Molecular structure and organization of the locus. The locus has two alleles, and ( ), and codes for components of a pheromone response pathway ( ). Both and contain a pheromone precursor and a receptor gene. The pheromone precursor genes code for polypeptides of 40 and 38 amino acids for and , respectively, and the pheromone precursors contain a CAAX box at the C terminus ( ). This sequence is a substrate for prenylation and carboxymethylation, and the modification is necessary for full activity of the mature pheromones ( ). The modified pheromone precursors are processed further to yield lipopeptides of 13 and 9 amino acids for and , respectively. The allele contains additional genes: and , and a pseudopheromone gene, ( ), not present in the allele. (From reference with permission.)

Citation: Banuett F. 2007. History of the Mating Types in , p 351-375. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch21
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Tables

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Table 21.1

The locus is multiallelic

Citation: Banuett F. 2007. History of the Mating Types in , p 351-375. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch21
Generic image for table
Table 21.2

Compatibility reactions among progeny from cross 10A4 × 17D4 and from solopathogen 410qq

Citation: Banuett F. 2007. History of the Mating Types in , p 351-375. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch21

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