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Chapter 6 : and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle

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Abstract:

This chapter focuses on two filamentous ascomycetes: , which has been used extensively as a model to address questions of mating-type structure and evolution of reproductive lifestyle, and , which is the most rigorously studied filamentous ascomycete, in terms of structure and function of proteins. Molecular comparisons of alternate sequences at show that they are nonallelic. Sexual reproduction in filamentous ascomycetes is a complex developmental process requiring self/nonself recognition between cells and between nuclei. has been developed as a model for the genus; deletion strains have proven to be very useful to address questions of function. Heterothallic is a member of one group, which contains all known pathogens of cereals, while heterothallic represents the other. Homothallic is also in the first group but does not have a known close heterothallic relative. Homothallic and are in the second group, but neither is the closest relative of heterothallic . is a self-incompatible sordariomycete which contains two allelic idiomorphs denominated and + and corresponding to and in the standard terminology.

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
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Image of Figure 6.1
Figure 6.1

Cell-cell recognition and nucleus-nucleus recognition are necessary for mating. In the case of heterothallic matings (left), self-nonself recognition is required between mating partners. The male partner is a microconidium, macroconidium, or hyphal cell. A second recognition step occurs between nuclei; unlike nuclei must recognize each other and pair. For homothallic strains (right), the cell-cell recognition step is likely not required: it is known, for example, that homothallic and do not require external cells for fertilization. Current hypotheses suggest that homothallic species must have a mechanism that alters some nuclei so they are different from parental nuclei and that these now unlike nuclei can then pair to form the transient diploid. The process by which this is achieved is unknown at present (but see “Mating-Type Structure and Function in ”). The process of ascospore formation, once the diploid is formed, has been described in detail ( ).

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
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Image of Figure 6.2
Figure 6.2

Reproductive biology of in vitro. (Left panels) Mating of heterothallic ; (right panels) selfing of homothallic . (Top row) Mating plates; agar plugs bearing mycelium of each mating type (left) or the same mating type (right) are placed on opposite sides of a senescent corn leaf substrate. Fruiting bodies (pseudothecia) form in 4 to 7 days; color reflects the strain that acted as the female in the case of heterothallic matings. In block A, an albino and a pigmented strain were mated. (Middle row) Left, close-up of pseudothecia (note beaks); right, crushed pseudothecium and contents (asci). (Bottom row) Asci and ascospores. ascospores are multicellular, multinucleate, and filamentous. Note asci from selfs (right) usually contain complete tetrads.

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
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Image of Figure 6.3
Figure 6.3

Organization of the and loci. Lines represent sequences common to - and - or − and +. Boxes represent -specific sequences. (Top) Arrows indicate ORFs and direction of transcription. , GTPase-activating protein; , conserved ORF of unknown function; , β-glucosidase. (Bottom) . Arrowed boxes represent mating-type genes. . nomenclature for mating-type genes is shown above the corresponding box. Standard nomenclature for mating-type genes is shown under the corresponding box. Protein domains encoded by mating-type genes are indicated in the corresponding box.

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
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Image of Figure 6.4
Figure 6.4

Organization of loci in homothallic , , and species. (A) organization. (B through D) Proposed recombination events responsible for converting heterothallic ancestors to extant homothallic species, as described in the text (“The Direction of Evolution”) and references , and .

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
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Image of Figure 6.5
Figure 6.5

Experiments to convert heterothallic to homothallism. (A) A -deletion strain of carrying the gene from homothallic can self and is fertile. It can also outcross to strains of either mating type. Only a cross to a mating type 1 strain is fertile, however, perhaps reflecting the requirement that both 3′ untranslated regions be present for fertility (see “”) ( ). In contrast, a − deletion strain of carrying the gene from homothallic can self but is not fertile. It can also outcross to strains of either mating type. Only a cross to a mating type 2 strain is fertile, however, perhaps for reasons described above. (B) determines reproductive style. A − deletion strain of is sterile. If either or is introduced at the native site, transgenic strains are sterile but can cross to a strain of opposite mating type. If, however, the or genes are introduced, the strains are able to self, as described for panel A. Since the genetic background of the original strain is held constant, it is the gene alone that determines mating style.

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
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Image of Figure 6.6
Figure 6.6

Diagrammatic representation of the MAT1-1-1 and MAT1-2-1 proteins, showing conserved motifs. These motifs are found in all Dothideomycete taxa examined including (), (), (), , and A signature motif within the HMG box (stippled rectangle) of MAT1-2-1 is also found in the MAT1-1-1 protein (Motif 1, white box). A motif found in the α1 box (light gray stippled) is found at the C-terminal end of both MAT proteins (Motif 2, gray box). A third common stretch is RK rich (checked box) (Lu and Turgeon, unpublished). To date, functional analyses of these motifs have not been done.

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
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Image of Figure 6.7
Figure 6.7

mating scheme. Selfs and crosses both yield progeny that are 50% homothallic and 50% heterothallic. The latter are all

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
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Image of Figure 6.8
Figure 6.8

Organization of the mating-type loci in homothallic and heterothallic strains. Heterothallic strains all carry the three-gene complement typical of Pyrenomycete strains. Homothallic strains carry two types of locus, as described in “Clues to Reproductive Lifestyle Conversion from Fungi with Nonstandard Mechanisms.” Arrows on the top line indicates repeated sequences in the version of the locus that carries both and One hypothesis is that these repeated sequences may promote an intramolecular recombination that would eliminate , leaving all three genes.

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
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Image of Figure 6.9
Figure 6.9

Control of fertilization by mating-type genes in . Gene actions are symbolized as follows: arrows connote positive regulation, and lines ending in bars connote repression. Proteins are displayed in association as established by yeast two-hybrid assays (Coppin and Debuchy, unpublished).

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
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Image of Figure 6.10
Figure 6.10

Internuclear recognition model. Gene actions are symbolized as in Fig. 6.9 . The + and − nuclei recognize each other inside plurinucleate cells based on their nuclear identity. The mat− nuclear identity is determined by the FMR1/SMR2 heterodimer that returns specifically to − nuclei. The mat+ nuclear identity is determined by the FPR1 homodimer that returns specifically to + nuclei. Internuclear recognition results from the superimposition of the nuclear identity of − and + nuclei, which triggers nuclear migration and expression of the genes required for ascogenous hyphae formation. The developmental arrest is overcome by the action of . Uniparental − asci result from the loss of the repressive action of the FMR1/SMR2 heterodimer, which allows basal expression of the target genes for mat+ nuclear identity. Expression of mat− and mat+ nuclear identity in the same nucleus triggers self-recognition, migration of the mutant nucleus and development of uninucleate ascogenous hypha. A similar rationale is applied to + mutations that yield a uniparental + progeny (see “The Internuclear Recognition Model” for more details).

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
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Image of Figure 6.11
Figure 6.11

Random segregation model. Gene actions are symbolized as in Fig. 6.9 . During their mitoses in the plurinucleate cells, the FMR1/SMR2 heterodimer and FPR1 homodimer repress the expression of target genes involved in ascogenous hyphae formation. Random pairing of nuclei yield −/− and +/+ pairs which do not undergo further development, while +/− pairs produce a regulatory product specified by cooperation of the + and − idiomorphs. This product is symbolized by MAT+/MAT−. It activates the expression of the genes required for ascogenous hyphae formation. Uniparental − asci result from the loss of repressive action of the FMR1/SMR2 on the target genes for ascogenous hyphae. Expression of these genes allows the mutant nucleus to trigger the development of ascogenous hyphae and to yield a − uniparental progeny. A similar rationale is applied to + mutations that yield uniparental + progeny (see “The Random Segregation Model” for more details).

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
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Tables

Generic image for table
Table 6.1

Function of heterologous genes

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
Generic image for table
Table 6.2

Genes adjacent to in Dothideomycetes

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
Generic image for table
Table 6.3

Percent nucleotide and amino acid identities of and genes and encoded proteins

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
Generic image for table
Table 6.4

Intergenic distance is conserved in the species

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
Generic image for table
Table 6.5

Functional analysis of genes from asexual species

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
Generic image for table
Table 6.6

Fungi that produce both self-fertile and self-sterile progeny

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6
Generic image for table
Table 6.7

Phenotype of mating-type gene mutations in

Citation: Turgeon B, Debuchy R. 2007. and : Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle, p 93-121. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch6

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