Cochliobolus and Podospora: Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle

B. Gillian Turgeon; Robert Debuchy

doi:10.1128/9781555815837.ch6

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

Authors: B. Gillian Turgeon¹, Robert Debuchy²

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Affiliations: 1: Department of Plant Pathology, Cornell University, Ithaca, NY 14853; 2: CNRS, Institut de Génétique et Microbiologie, Batiment 400, UMR 8621, and Université Paris-Sud 11, Orsay, F-91405, France

Content Type: Monograph

Publication Year: 2007

Category: Fungi and Fungal Pathogenesis

Book DOI: 10.1128/9781555815837

Chapter DOI: 10.1128/9781555815837.ch6

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Abstract:

This chapter focuses on two filamentous ascomycetes: Cochliobolus heterostrophus, which has been used extensively as a model to address questions of mating-type structure and evolution of reproductive lifestyle, and Podospora anserina, which is the most rigorously studied filamentous ascomycete, in terms of structure and function of MAT proteins. Molecular comparisons of alternate sequences at MAT show that they are nonallelic. Sexual reproduction in filamentous ascomycetes is a complex developmental process requiring self/nonself recognition between cells and between nuclei. C. heterostrophus has been developed as a model for the genus; mat deletion strains have proven to be very useful to address questions of MAT function. Heterothallic C. heterostrophus is a member of one group, which contains all known Cochliobolus pathogens of cereals, while heterothallic C. ellisii represents the other. Homothallic C. homomorphus is also in the first group but does not have a known close heterothallic relative. Homothallic C. cymbopogonis and C. kusanoi are in the second group, but neither is the closest relative of heterothallic C. ellisii. P. anserina is a self-incompatible sordariomycete which contains two allelic idiomorphs denominated mat- and mat+ and corresponding to MAT1-1 and MAT1-2 in the standard terminology.

Citation: Turgeon B, Debuchy R. 2007. Cochliobolus and Podospora: 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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Cochliobolus and Podospora: Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle

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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 Sordaria macrospora and Aspergillus nidulans 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 Podospora anserina”). The process of ascospore formation, once the diploid is formed, has been described in detail ( 66 , 93 ).

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Figure 6.1

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Figure 6.2

Reproductive biology of Cochliobolus in vitro. (Left panels) Mating of heterothallic C. heterostrophus; (right panels) selfing of homothallic C. luttrellii. (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. Cochliobolus ascospores are multicellular, multinucleate, and filamentous. Note asci from selfs (right) usually contain complete tetrads.

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Figure 6.2

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Figure 6.3

Organization of the C. heterostrophus and P. anserina MAT loci. Lines represent sequences common to MAT1-1 and MAT1-2 or mat− and mat+. Boxes represent mat-specific sequences. (Top) C. heterostrophus. Arrows indicate ORFs and direction of transcription. GAP, GTPase-activating protein; ORF1, conserved ORF of unknown function; BGL1, β-glucosidase. (Bottom) P. anserina. Arrowed boxes represent mating-type genes. P. anserina 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.

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Figure 6.3

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Figure 6.4

Organization of MAT loci in homothallic Cochliobolus, Stemphylium, and Crivellia species. (A) MAT organization. (B through D) Proposed recombination events responsible for converting heterothallic ancestors to extant homothallic species, as described in the text (“The Direction of MAT Evolution”) and references 45 , 46 , and 91 .

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Figure 6.4

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Figure 6.5

Experiments to convert heterothallic C. heterostrophus to homothallism. (A) A mat-deletion strain of C. heterostrophus carrying the MAT1-1/2 gene from homothallic C. luttrellii can self and is fertile. It can also outcross to C. heterostrophus strains of either mating type. Only a cross to a C. heterostrophus mating type 1 strain is fertile, however, perhaps reflecting the requirement that both MAT 3′ untranslated regions be present for fertility (see “C. heterostrophus”) ( 85 ). In contrast, a mat− deletion strain of C. heterostrophus carrying the MAT1-2/1 gene from homothallic C. homomorphus can self but is not fertile. It can also outcross to C. heterostrophus strains of either mating type. Only a cross to a C. heterostrophus mating type 2 strain is fertile, however, perhaps for reasons described above. (B) MAT determines reproductive style. A mat− deletion strain of C. heterostrophus is sterile. If either C. heterostrophus MAT1-1 or MAT1-2 is introduced at the native MAT site, transgenic strains are sterile but can cross to a strain of opposite mating type. If, however, the C. luttrellii MAT1-1/2 or C. homomorphus MAT1-2/1 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 MAT gene alone that determines mating style.

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Figure 6.5

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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 Cochliobolus (Bipolaris), Pleospora (Stemphylium), Phaeosphaeria (Stagonospora), Leptosphaeria maculans, and Alternaria alternata. 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.

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Figure 6.6

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Figure 6.7

Chromocrea spinulosa mating scheme. Selfs and crosses both yield progeny that are 50% homothallic and 50% heterothallic. The latter are all MAT1-1.

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Figure 6.7

Chromocrea spinulosa mating scheme. Selfs and crosses both yield progeny that are 50% homothallic and 50% heterothallic. The latter are all MAT1-1.

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Figure 6.8

Organization of the C. spinulosa mating-type loci in homothallic and heterothallic strains. Heterothallic strains all carry the three-gene complement typical of Pyrenomycete MAT1-1 strains. Homothallic strains carry two types of MAT 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 MAT locus that carries both MAT1-1 and MAT1-2. One hypothesis is that these repeated sequences may promote an intramolecular recombination that would eliminate MAT1-2, leaving all three MAT1-1 genes.

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Figure 6.8

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Figure 6.9

Control of fertilization by mating-type genes in P. anserina. 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).

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Figure 6.9

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Figure 6.10

Internuclear recognition model. Gene actions are symbolized as in Fig. 6.9 . The mat+ and mat− 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 mat− nuclei. The mat+ nuclear identity is determined by the FPR1 homodimer that returns specifically to mat+ nuclei. Internuclear recognition results from the superimposition of the nuclear identity of mat− and mat+ nuclei, which triggers nuclear migration and expression of the genes required for ascogenous hyphae formation. The developmental arrest is overcome by the action of SMR1. Uniparental mat− 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 mat mutant nucleus and development of uninucleate ascogenous hypha. A similar rationale is applied to mat+ mutations that yield a uniparental mat+ progeny (see “The Internuclear Recognition Model” for more details).

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Figure 6.10

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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 mat−/mat− and mat+/mat+ pairs which do not undergo further development, while mat+/mat− pairs produce a regulatory product specified by cooperation of the mat+ and mat− idiomorphs. This product is symbolized by MAT+/MAT−. It activates the expression of the genes required for ascogenous hyphae formation. Uniparental mat− 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 mat− uniparental progeny. A similar rationale is applied to mat+ mutations that yield uniparental mat+ progeny (see “The Random Segregation Model” for more details).

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Figure 6.11

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Tables

Cochliobolus and Podospora: Mechanisms of Sex Determination and the Evolution of Reproductive Lifestyle

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Table 6.1

Function of heterologous Cochliobolus MAT genes a

Table 6.1

Function of heterologous Cochliobolus MAT genes a

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Table 6.2

Genes adjacent to MAT in Dothideomycetes

Table 6.2

Genes adjacent to MAT in Dothideomycetes

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Table 6.3

Percent nucleotide and amino acid identities of Cochliobolus MAT1-1-1 and MAT1-2-1 genes and encoded proteins a

Table 6.3

Percent nucleotide and amino acid identities of Cochliobolus MAT1-1-1 and MAT1-2-1 genes and encoded proteins a

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Table 6.4

Intergenic distance is conserved in the Cochliobolus species a

Table 6.4

Intergenic distance is conserved in the Cochliobolus species a

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Table 6.5

Functional analysis of MAT genes from asexual species a

Table 6.5

Functional analysis of MAT genes from asexual species a

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Table 6.6

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

Table 6.6

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

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Table 6.7

Phenotype of mating-type gene mutations in P. anserinaa

Table 6.7

Phenotype of mating-type gene mutations in P. anserinaa