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Chapter 33 : Mating Systems and Sexual Morphogenesis in Ascomycetes

Authors: Robert Debuchy1, Véronique Berteaux-Lecellier*2, Philippe Silar4
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Affiliations: 1: Univ Paris-Sud, Institut de Génétique et Microbiologie, UMR8621, F-9140 Orsay, France; CNRS, Institut de Génétique et Microbiologie, UMR8621, F-91405 Orsay, France; 2: Univ Paris-Sud, Institut de Génétique et Microbiologie, UMR8621, F-9140 Orsay, France; CNRS, Institut de Génétique et Microbiologie, UMR8621, F-91405 Orsay, France; 3: *Present address: Centre de Recherche Insulaire et Observatoire de l’Environnement, 4SR CNRS-EPHE, BP 1013, 98729 Papetoai Moorea, Polynésie Française; 4: UFR des Sciences du Vivant, Univ de Paris 7—Denis Diderot, F-75013 Paris, France; Univ Paris-Sud, Institut de Génétique et Microbiologie, UMR8621, F-9140 Orsay, France; CNRS, Institut de Génétique et Microbiologie, UMR8621, F-91405 Orsay, France
Content Type: Monograph
Publication Year: 2010

Category: Microbial Genetics and Molecular Biology; Fungi and Fungal Pathogenesis

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Abstract:

This chapter provides an up-to-date review of complex cellular transition steps in Pezizomycotina, from the differentiation of reproductive cells to the development of the fructification. Initiation of sexual reproduction in the sordariomycete , as it is for several ascomycetes, is clearly not dependent on a particular pH range. In many fungi, light is one of the prominent physical factors controlling sexual reproduction, either by stimulating or inhibiting the formation of reproductive structures. Although most Pezizomycotina can be classified as self-compatible or self-incompatible, some species present peculiar mating characteristics. There are several studies showing that pheromone and pheromone receptors are essential for the fusion of the trichogyne with the male cell in self-incompatible filamentous ascomycetes. Recent data have begun to shed light on the various molecular processes occurring during sexual reproduction in filamentous Ascomycetes. In addition to the well-known variety of body plan exhibited by Pezizomycotina fruiting bodies, sequencing has uncovered a large set of mating-type structures, all based on a common pattern. Indeed, it is now well established that MAT1-1-1 and MAT1-1-2 genes control fertilization by using pheromone/receptor genes in self-incompatible Pezizomycotina, but little is known about their roles after fertilization. The few indications that come from , , and indicate that they control the formation of biparental ascogenous hyphae and meiosis.

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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Mating Systems and Sexual Morphogenesis in Ascomycetes
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Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
/content/10.1128/9781555816636.ch33.ch33fig01
FIGURE 1
Fruiting body plan evolution in filamentous ascomycetes. (A) Representative fruiting bodies of major evolutionary lineages. Lineages in light gray do not produce multicellular fructifications; those underlined produce mostly apothecia or apothecia-like (e.g., truffles and others) fructifications. Laboulbeniomycetes and Sordariomycetes produce mostly perithecia, Dothideomycetes produce mostly pseudothecia, and Eurotiomycetes produce mostly cleistothecia and gymnothecia. Abbreviations: , ; , . , and photos are by P. Silar; images of and were kindly provided by J. L. Cheype, that of by B. G. Turgeon, and that of by Raymond Boyer. (B) Schematic representation of various Pezizomycotina fruiting bodies.
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FIGURE 1

Fruiting body plan evolution in filamentous ascomycetes. (A) Representative fruiting bodies of major evolutionary lineages. Lineages in light gray do not produce multicellular fructifications; those underlined produce mostly apothecia or apothecia-like (e.g., truffles and others) fructifications. Laboulbeniomycetes and Sordariomycetes produce mostly perithecia, Dothideomycetes produce mostly pseudothecia, and Eurotiomycetes produce mostly cleistothecia and gymnothecia. Abbreviations: , ; , . , and photos are by P. Silar; images of and were kindly provided by J. L. Cheype, that of by B. G. Turgeon, and that of by Raymond Boyer. (B) Schematic representation of various Pezizomycotina fruiting bodies.

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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FIGURE 2
Life cycle and fruiting body development in Pezizomycotina. (A) Schematic representation of the major stages of the sexual cycle of a heterothallic pezizomycotina. The germinating ascospore (a) gives rise to a mycelium on which both male and female gametes differentiate(b). Fertilization occurs only between male and female gametes of opposite mating types (c). The trichogyne catches a microconidium (c, arrow), and the ascogonium develops into a perithecium(d). Inside the perithecium, dikaryotic ascogenous hyphae emerge from the plurinucleate dikaryotic cells. After one or two rounds of mitosis, the ascogenous hypha gives rise to a crozier (e). Karyogamy takes place in the upper cell (indicated by an asterisk) and is immediately followed by meiosis, a mitosis, and ascospore formation (f and g). (B) Schematic representation of various croziers (adapted from a drawing by M. Chadefaud [ ]). All these structures derive from a dikaryotic hypha. The cell in which karyogamy takes place is indicated by an asterisk. (a through d) Tricellular crozier. (a and b) Simple crozier; (c) crozier with a lateral cell which does not fuse with the basal one; (d) prototypical crozier. The lateral cell will fuse with the basal one to give rise to another crozier cell; (e and f) bicellular crozier. The lateral cell does not exist any more.
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FIGURE 2

Life cycle and fruiting body development in Pezizomycotina. (A) Schematic representation of the major stages of the sexual cycle of a heterothallic pezizomycotina. The germinating ascospore (a) gives rise to a mycelium on which both male and female gametes differentiate(b). Fertilization occurs only between male and female gametes of opposite mating types (c). The trichogyne catches a microconidium (c, arrow), and the ascogonium develops into a perithecium(d). Inside the perithecium, dikaryotic ascogenous hyphae emerge from the plurinucleate dikaryotic cells. After one or two rounds of mitosis, the ascogenous hypha gives rise to a crozier (e). Karyogamy takes place in the upper cell (indicated by an asterisk) and is immediately followed by meiosis, a mitosis, and ascospore formation (f and g). (B) Schematic representation of various croziers (adapted from a drawing by M. Chadefaud [ ]). All these structures derive from a dikaryotic hypha. The cell in which karyogamy takes place is indicated by an asterisk. (a through d) Tricellular crozier. (a and b) Simple crozier; (c) crozier with a lateral cell which does not fuse with the basal one; (d) prototypical crozier. The lateral cell will fuse with the basal one to give rise to another crozier cell; (e and f) bicellular crozier. The lateral cell does not exist any more.

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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FIGURE 3
Mating-type structure in Fungi. α1, genes encoding transcription factors with an α1 domain; PPF, genes encoding proteins with a PPF domain; HMG1 and HMG2, genes encoding transcription factors with an HMG domain (phylogenetically related genes are boxed); HOM1, genes encoding transcription factor with a TALE homeodomain (reviewed by ); HOM2, genes encoding a transcription factor with a typical homeodomain; other, genes encoding proteins with uncharacterized features. Mating-type structures from . , and were compiled from works of Butler and others ( ). The mating-type structures of , and were obtained from studies by ), and , respectively.
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FIGURE 3

Mating-type structure in Fungi. α1, genes encoding transcription factors with an α1 domain; PPF, genes encoding proteins with a PPF domain; HMG1 and HMG2, genes encoding transcription factors with an HMG domain (phylogenetically related genes are boxed); HOM1, genes encoding transcription factor with a TALE homeodomain (reviewed by ); HOM2, genes encoding a transcription factor with a typical homeodomain; other, genes encoding proteins with uncharacterized features. Mating-type structures from . , and were compiled from works of Butler and others ( ). The mating-type structures of , and were obtained from studies by ), and , respectively.

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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FIGURE 4
Amino acid alignment of the α1 domain of deduced MAT1-1-1 proteins of selected pezizomycotina with the MATα1 protein of . : . (AAC37478), . (CAA71623), . (CAA45519), . (EAQ89967), . (strain 70-6) (BAC65087), . (AAK83346), sp. W (BAE93750), sp. G (AB93756), . (AAC71055), . (AAG42809), . (BAC67541), . (CAA06844), . (AAX83122), . (EAA63189), . (AB087596), . (CAA48465), . (AAD33439), (AAR04470), and . (P01365). Stars indicate the residues of the α1 proteins that may interact with MCM1 (adapted from ). Fraction that must agree for shading is 0.7. Alignment was performed with Clustal version 2 ( ), and shading was done with BOXSHADE version 3.21.
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FIGURE 4

Amino acid alignment of the α1 domain of deduced MAT1-1-1 proteins of selected pezizomycotina with the MATα1 protein of . : . (AAC37478), . (CAA71623), . (CAA45519), . (EAQ89967), . (strain 70-6) (BAC65087), . (AAK83346), sp. W (BAE93750), sp. G (AB93756), . (AAC71055), . (AAG42809), . (BAC67541), . (CAA06844), . (AAX83122), . (EAA63189), . (AB087596), . (CAA48465), . (AAD33439), (AAR04470), and . (P01365). Stars indicate the residues of the α1 proteins that may interact with MCM1 (adapted from ). Fraction that must agree for shading is 0.7. Alignment was performed with Clustal version 2 ( ), and shading was done with BOXSHADE version 3.21.

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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FIGURE 5
Amino acid alignment of the PPF domain of deduced MAT1-1-2 proteins of various pezizomycotina: . (AAC37477), (CAA71626), . (CAA52052), . MAT1-1 (EAQ89966), . MAT1-2 (EAQ91646), . (strain 70-6) (BAC65088), . (AAK83345), sp. W mat1 (BAE93749), sp. W mat2 (BAE93752), sp. G mat1 (BAE93755), sp. G mat2 (BAE93758), . (AAC71054), . (( ), . (AAG42811), . (BAC67540), and . (BAD72603). Fraction that must agree for shading is 0.7. Alignment was performed with Clustal version 2 ( ), and shading was done with BOXSHADE version 3.21.
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FIGURE 5

Amino acid alignment of the PPF domain of deduced MAT1-1-2 proteins of various pezizomycotina: . (AAC37477), (CAA71626), . (CAA52052), . MAT1-1 (EAQ89966), . MAT1-2 (EAQ91646), . (strain 70-6) (BAC65088), . (AAK83345), sp. W mat1 (BAE93749), sp. W mat2 (BAE93752), sp. G mat1 (BAE93755), sp. G mat2 (BAE93758), . (AAC71054), . (( ), . (AAG42811), . (BAC67540), and . (BAD72603). Fraction that must agree for shading is 0.7. Alignment was performed with Clustal version 2 ( ), and shading was done with BOXSHADE version 3.21.

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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FIGURE 6
Amino acid alignment of the HMG domain of deduced MAT1-1-3 proteins of selected pezizomycotina. (AAC37476), (CAA52051), (EAQ89965), (BAC65085), (AAK83344), sp. W mat1 (BAE93748), sp. W mat2 (BAE93751), sp. G mat1 (BAE93754), sp. G mat2 (BAE93757), (AAC71053), (AAG42812), and (CAA06846). Fraction that must agree for shading is 0.7. Alignment was performed with Clustal version 2 ( ), and shading was done with BOXSHADE version 3.21.
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FIGURE 6

Amino acid alignment of the HMG domain of deduced MAT1-1-3 proteins of selected pezizomycotina. (AAC37476), (CAA52051), (EAQ89965), (BAC65085), (AAK83344), sp. W mat1 (BAE93748), sp. W mat2 (BAE93751), sp. G mat1 (BAE93754), sp. G mat2 (BAE93757), (AAC71053), (AAG42812), and (CAA06846). Fraction that must agree for shading is 0.7. Alignment was performed with Clustal version 2 ( ), and shading was done with BOXSHADE version 3.21.

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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FIGURE 7
Amino acid alignment of the HMG domain of deduced MAT1-2-1 proteins of selected pezizomycotina: (AAA33598), (CAA71624), (CAA45520), (EAQ91645), (BAC65090), (AAK83343), sp. W2 (BAE93753), sp. G2 (BAE93759), (AAC71056), (AAG42810), (BAC66503), (AAF00498), (CAA06843), (EAL92951), (AAQ07985), (ABO87595), (CAA48464), (AAD33439), () (AAR04483), (AAL30836). Fraction that must agree for shading is 0.7. Alignment was performed with Clustal version 2 ( ), and shading was done with BOXSHADE version 3.21.
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FIGURE 7

Amino acid alignment of the HMG domain of deduced MAT1-2-1 proteins of selected pezizomycotina: (AAA33598), (CAA71624), (CAA45520), (EAQ91645), (BAC65090), (AAK83343), sp. W2 (BAE93753), sp. G2 (BAE93759), (AAC71056), (AAG42810), (BAC66503), (AAF00498), (CAA06843), (EAL92951), (AAQ07985), (ABO87595), (CAA48464), (AAD33439), () (AAR04483), (AAL30836). Fraction that must agree for shading is 0.7. Alignment was performed with Clustal version 2 ( ), and shading was done with BOXSHADE version 3.21.

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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FIGURE 8
Phylogenetic tree of deduced MAT1-1-3 and MAT1-2-1 proteins of selected pezizomycotina. The neighbor-joining tree for the HMG proteins encoded by mating types indicates that MAT1-1-3 and MAT1-2-1 transcription factors form two distinct families. For the accession numbers of proteins, see Fig. 6 and 7 . Phylogenetic analysis was conducted with MEGA 4 ( ).
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FIGURE 8

Phylogenetic tree of deduced MAT1-1-3 and MAT1-2-1 proteins of selected pezizomycotina. The neighbor-joining tree for the HMG proteins encoded by mating types indicates that MAT1-1-3 and MAT1-2-1 transcription factors form two distinct families. For the accession numbers of proteins, see Fig. 6 and 7 . Phylogenetic analysis was conducted with MEGA 4 ( ).

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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FIGURE 9
Structure of locus in selected self-incompatible and asexual pezizomycotina. The phylogenic tree has been built upon previous studies by . Mating-type locus structures are not to scale.
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FIGURE 9

Structure of locus in selected self-incompatible and asexual pezizomycotina. The phylogenic tree has been built upon previous studies by . Mating-type locus structures are not to scale.

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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FIGURE 10
Structure of locus in self-compatible pezizomycotina. The phylogenic tree has been built upon previous studies by . Mating-type locus structures are not to scale.
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FIGURE 10

Structure of locus in self-compatible pezizomycotina. The phylogenic tree has been built upon previous studies by . Mating-type locus structures are not to scale.

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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FIGURE 11
Crozier formation in mutant strains. (A) Wild-type-like ascus development. Dikaryotic hyphae emerge from a plurinucleate cell and form, after one or two divisions, the crozier cells in which the two nuclei divide. This coordinate mitosis gives rise, after septum formation, to three cells: an upper binucleated cell (long arrow) and two uninucleated cells, one lateral (arrowhead) and one basal (arrow). Karyogamy will take place in the upper cells, which contain two nuclei of opposite mating types. Nuclear fusion is followed by meiosis and elongation of this upper cell, now called an ascus (a through d). A young small ascus where karyogamy has just occurred (a) and a midprophase ascus () are visible. (B) In a cross between a mutant and the wild type, uni-nucleated croziers are formed (arrow); the arrowhead points to an enlarged cell that might evolve into an ascus. (C) Crozier phenotype of a mutant cross. Most croziers are plurinucleated and often form giant croziers (arrow), in which nuclei divide synchronously, but no septa are formed. On the left of this large crozier is a smaller one (arrowhead), still containing an abnormally high number of nuclei but exhibiting a normal size (when compared with the wild-type crozier size in A). (D) Binucleated croziers issued from a ▵ mutant cross. Differentiation of the dikaryotic cells is similar to that in the wild type; however, instead of undergoing karyogamy, the two nuclei isolated in the upper binucleated cell (long arrows) divide again to form another crozier cell. Lateral and basal cells are indicated by an arrowhead and an arrow, respectively. Scale bar, 5 μm. Light micrographs are a kind gift from D. Zickler (IGM; Université Paris Sud-11, France); rosettes of asci are stained by hematoxylin (see , for details).
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FIGURE 11

Crozier formation in mutant strains. (A) Wild-type-like ascus development. Dikaryotic hyphae emerge from a plurinucleate cell and form, after one or two divisions, the crozier cells in which the two nuclei divide. This coordinate mitosis gives rise, after septum formation, to three cells: an upper binucleated cell (long arrow) and two uninucleated cells, one lateral (arrowhead) and one basal (arrow). Karyogamy will take place in the upper cells, which contain two nuclei of opposite mating types. Nuclear fusion is followed by meiosis and elongation of this upper cell, now called an ascus (a through d). A young small ascus where karyogamy has just occurred (a) and a midprophase ascus () are visible. (B) In a cross between a mutant and the wild type, uni-nucleated croziers are formed (arrow); the arrowhead points to an enlarged cell that might evolve into an ascus. (C) Crozier phenotype of a mutant cross. Most croziers are plurinucleated and often form giant croziers (arrow), in which nuclei divide synchronously, but no septa are formed. On the left of this large crozier is a smaller one (arrowhead), still containing an abnormally high number of nuclei but exhibiting a normal size (when compared with the wild-type crozier size in A). (D) Binucleated croziers issued from a ▵ mutant cross. Differentiation of the dikaryotic cells is similar to that in the wild type; however, instead of undergoing karyogamy, the two nuclei isolated in the upper binucleated cell (long arrows) divide again to form another crozier cell. Lateral and basal cells are indicated by an arrowhead and an arrow, respectively. Scale bar, 5 μm. Light micrographs are a kind gift from D. Zickler (IGM; Université Paris Sud-11, France); rosettes of asci are stained by hematoxylin (see , for details).

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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FIGURE 12
Cross talk between mycelium and perithecium envelope. The model is based on data obtained with and . After differentiation, the ascogonium sends a signal to neighboring hyphae to form a protective envelope. The signaling pathway containing PaNox1, IDC1, and the PaMpk1 module is necessary to mobilize these hyphae. Then, in the absence of fertilization, development stops. After fertilization, the same signaling pathway is necessary for the development of the fructification. PaNox1 and IDC1 act in the wall of the fructification, whereas the MAPK module acts in the surrounding hyphae. Signaling then results in the transfer of nutrients to the developing fructification. At later stages of development, a neck is formed under the control of the BEK-1 transcription factor and GPR-1 receptor.
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Image of FIGURE 12
FIGURE 12

Cross talk between mycelium and perithecium envelope. The model is based on data obtained with and . After differentiation, the ascogonium sends a signal to neighboring hyphae to form a protective envelope. The signaling pathway containing PaNox1, IDC1, and the PaMpk1 module is necessary to mobilize these hyphae. Then, in the absence of fertilization, development stops. After fertilization, the same signaling pathway is necessary for the development of the fructification. PaNox1 and IDC1 act in the wall of the fructification, whereas the MAPK module acts in the surrounding hyphae. Signaling then results in the transfer of nutrients to the developing fructification. At later stages of development, a neck is formed under the control of the BEK-1 transcription factor and GPR-1 receptor.

Citation: Debuchy R, Berteaux-Lecellier* V, Silar P. 2010. Mating Systems and Sexual Morphogenesis in Ascomycetes, p 501-535. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch33
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