16 Sexual Development in Fungi

Peraza-Reyes, Leonardo; Malagnac, Fabienne

doi:10.1007/978-3-319-25844-7_16

Cited by 16 publications

(15 citation statements)

References 317 publications

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“…Mating compatibility in fungi is governed by mating-type genes, which are located in mating-type (MAT) loci [11,12]. While ascomycetes and the Mucoromycotina are bipolar (unifactorial), i.e.…”

Section: Introductionmentioning

confidence: 99%

Convergent evolution of linked mating-type loci in basidiomycete fungi

et al. 2019

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Sexual development is a key evolutionary innovation of eukaryotes. In many species, mating involves interaction between compatible mating partners that can undergo cell and nuclear fusion and subsequent steps of development including meiosis. Mating compatibility in fungi is governed by the mating type (MAT) loci. In basidiomycetes, the ancestral state is hypothesized to be tetrapolar, with two genetically unlinked MAT loci containing homeodomain transcription factor genes (HD locus) and pheromone and pheromone receptor genes (P/R locus), respectively. Alleles at both loci must differ between mating partners for completion of sexual development. However, there are also basidiomycetes with bipolar mating systems, which can arise through genomic linkage of the HD and P/R loci. In the order Tremellales, bipolarity is found only in the pathogenic Cryptococcus species. Here, we describe the analysis of MAT loci from 24 species of the Trichosporonales, a sister order to the Tremellales. In all of the species analyzed, the MAT loci are fused and a single HD gene is present in each mating type, similar to the organization in the pathogenic Cryptococci. However, the HD and P/R allele combinations in the Trichosporonales are different from those in the pathogenic Cryptococci. This and the existence of tetrapolar species in the Tremellales suggest that fusion of the HD and P/R loci occurred independently in the Trichosporonales and pathogenic Cryptococci, supporting the hypothesis of convergent evolution towards fused MAT regions, similar to previous findings in other fungal groups. Unlike the fused MAT loci in several other basidiomycete lineages though, the gene content and gene order within the fused MAT loci are highly conserved in the Trichosporonales, and there is no apparent suppression of recombination extending from the MAT loci to adjacent chromosomal regions, suggesting different mechanisms for the evolution of physically linked MAT loci in these groups.

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Section: Introductionmentioning

confidence: 99%

Convergent evolution of linked mating-type loci in basidiomycete fungi

et al. 2019

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“…Fruiting bodies in Pezizomycotina are integrated structure made of two major kinds of tissues. The outer part, also called envelope or peridium, is exclusively made of maternal tissue whereas the inner part, the zygotic tissue is issued from fusion of the two parental haploid gametes [38]. To check whether the Δ PaRid sterility resulted from a peridium defect or from a developmental defect of the zygotic tissue, we set up trikaryon crosses involving the Δ mat strain [39,40].…”

Section: Resultsmentioning

confidence: 99%

A RID-like putative cytosine methyltransferase homologue controls sexual development in the fungus Podospora anserina

et al. 2019

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DNA methyltransferases are ubiquitous enzymes conserved in bacteria, plants and opisthokonta. These enzymes, which methylate cytosines, are involved in numerous biological processes, notably development. In mammals and higher plants, methylation patterns established and maintained by the cytosine DNA methyltransferases (DMTs) are essential to zygotic development. In fungi, some members of an extensively conserved fungal-specific DNA methyltransferase class are both mediators of the Repeat Induced Point mutation (RIP) genome defense system and key players of sexual reproduction. Yet, no DNA methyltransferase activity of these purified RID (RIP deficient) proteins could be detected in vitro . These observations led us to explore how RID-like DNA methyltransferase encoding genes would play a role during sexual development of fungi showing very little genomic DNA methylation, if any. To do so, we used the model ascomycete fungus Podospora anserina . We identified the PaRid gene, encoding a RID-like DNA methyltransferase and constructed knocked-out Δ PaRid defective mutants. Crosses involving P . anserina Δ PaRid mutants are sterile. Our results show that, although gametes are readily formed and fertilization occurs in a Δ PaRid background, sexual development is blocked just before the individualization of the dikaryotic cells leading to meiocytes. Complementation of Δ PaRid mutants with ectopic alleles of PaRid , including GFP-tagged, point-mutated and chimeric alleles, demonstrated that the catalytic motif of the putative PaRid methyltransferase is essential to ensure proper sexual development and that the expression of PaRid is spatially and temporally restricted. A transcriptomic analysis performed on mutant crosses revealed an overlap of the PaRid-controlled genetic network with the well-known mating-types gene developmental pathway common to an important group of fungi, the Pezizomycotina.

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“…Fruiting bodies in Pezizomycotina are integrated structure made of two major kinds of tissues. The outer part, also called envelope or peridium, is exclusively made of maternal tissue whereas the inner part, the zygotic tissue is issued from fusion of the two parental haploid gametes [37]. To check whether the Δ PaRid sterility resulted from a peridium defect or from a developmental defect of the zygotic tissue, we set up trikaryon crosses involving the Δ mat strain [38,39].…”

Section: Resultsmentioning

confidence: 99%

“…The MAT1-1 idiomorph ( mat -) is characterized by the MAT1-1-1 gene, which encodes the FMR1 MATα-HMG domain containing protein, while the MAT1-2 idiomorph ( mat +) is composed of the MAT1-2-1 gene, which encodes the FPR1 MATA_HMG domain containing protein (reviewed in [49]). Both proteins are transcription factors essential for fertilization in heterothallic Pezizomycotina and development of the fruiting bodies (reviewed in [37]). Microarray comparisons of wild-type mat+ versus fpr1 - mutant strains, and wild-type mat- versus fmr1 - mutant strains revealed 571 and 232 target genes of FPR1 and FMR1, respectively [48].…”

Section: Resultsmentioning

confidence: 99%

“…Our results show that the PaRid function relies on its methyltransferase activity, and that this enzymatic activity has to be present in the female partner. Ascogonia, the female gametes, are small structures of specialized hyphae that differentiate within the mycelium [37]. As such, they represented an extremely low fraction of the so-called “vegetative” tissue when four-day-old mycelium was collected to extract total RNA.…”

Section: Discussionmentioning

confidence: 99%

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A RID-like cytosine methyltransferase homologue controls sexual development in the fungusPodospora anserina

Grognet

Timpano

Carlier

et al. 2019

Preprint

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21DNA methyltransferases are ubiquitous enzymes conserved in bacteria, plants and 22 opisthokonta. These enzymes, which methylate cytosines, are involved in numerous 23 biological processes, notably development. In mammals and higher plants, methylation 24 patterns established and maintained by the cytosine DNA methyltransferases (DMTs) are 25 essential to zygotic development. In fungi, some members of an extensively conserved 26 fungal-specific DNA methyltransferase class are both mediators of the Repeat Induced Point 27 mutation (RIP) genome defense system and key players of sexual reproduction. Yet, no DNA 28 methyltransferase activity of these purified RID (RIP deficient) proteins could be detected in 29 vitro. These observations led us to explore how RID-like DNA methyltransferase encoding 30 genes would play a role during sexual development of fungi showing very little genomic DNA 31 methylation, if any. 32To do so, we used the model ascomycete fungus P. anserina. We identified the 33 PaRid gene, encoding a RID-like DNA methyltransferase and constructed knocked-out 34ΔPaRid defective mutants. Crosses involving P. anserina ΔPaRid mutants are sterile. Our 35 results show that, although gametes are readily formed and fertilization occurs in a ΔPaRid 36 background, sexual development is blocked just before the individualization of the dikaryotic 37 cells leading to meiocytes. Complementation of ΔPaRid mutants with ectopic alleles of 38 PaRid, including 39 demonstrated that the catalytic motif of the putative PaRid methyltransferase is essential to 40 ensure proper sexual development and that the expression of PaRid is spatially and 41 temporally restricted. A transcriptomic analysis performed on mutant crosses revealed an 42 overlap of the PaRid-controlled genetic network with the well-known mating-types gene 43 developmental pathway common to an important group of fungi, the Pezizomycotina. 44 45 46 3 Author Summary 47Sexual reproduction is considered to be essential for long-term persistence of 48 eukaryotic species. Sexual reproduction is controlled by strict mechanisms governing which 49 haploids can fuse (mating) and which developmental paths the resulting zygote will follow. In 50 mammals, differential genomic DNA methylation patterns of parental gametes, known as 51 'DNA methylation imprints' are essential to zygotic development, while in plants, global 52 genomic demethylation often results in female-sterility. Although animal and fungi are 53 evolutionary related, little is known about epigenetic regulation of gene expression and 54 development in multicellular fungi. Here, we report on a gene of the model fungus Podospora 55 anserina, encoding a protein called PaRid that looks like a DNA methyltrasferase. We 56 showed that expression of the catalytically functional version of the PaRid protein is required 57 in the maternal parental strain to form zygotes. By establishing the transcriptional profile of 58PaRid mutant strain, we identified a set of PaRid direct and/or indirect target genes. Half o...

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16 Sexual Development in Fungi

Cited by 16 publications

References 317 publications

Convergent evolution of linked mating-type loci in basidiomycete fungi

Convergent evolution of linked mating-type loci in basidiomycete fungi

A RID-like putative cytosine methyltransferase homologue controls sexual development in the fungus Podospora anserina

A RID-like cytosine methyltransferase homologue controls sexual development in the fungusPodospora anserina

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