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1. New insights into genome annotation in Podospora anserina through re-exploiting multiple RNA-seq data

Author

Gaëlle Lelandais, Damien Remy, Fabienne Malagnac, and Pierre Grognet

Subjects
Transcriptome, RNA-seq, Fungal genome, Functional annotation, Alternative splicing, nTARs, Biotechnology, TP248.13-248.65, Genetics, QH426-470
Abstract

Abstract Background Publicly available RNA-seq datasets are often underused although being helpful to improve functional annotation of eukaryotic genomes. This is especially true for filamentous fungi genomes which structure differs from most well annotated yeast genomes. Podospora anserina is a filamentous fungal model, which genome has been sequenced and annotated in 2008. Still, the current annotation lacks information about cis-regulatory elements, including promoters, transcription starting sites and terminators, which are instrumental to integrate epigenomic features into global gene regulation strategies. Results Here we took advantage of 37 RNA-seq experiments that were obtained in contrasted developmental and physiological conditions, to complete the functional annotation of P. anserina genome. Out of the 10,800 previously annotated genes, 5’UTR and 3’UTR were defined for 7554, among which, 3328 showed differential transcriptional signal starts and/or transcriptional end sites. In addition, alternative splicing events were detected for 2350 genes, mostly due alternative 3’splice sites and 1732 novel transcriptionally active regions (nTARs) in unannotated regions were identified. Conclusions Our study provides a comprehensive genome-wide functional annotation of P. anserina genome, including chromatin features, cis-acting elements such as UTRs, alternative splicing events and transcription of non-coding regions. These new findings will likely improve our understanding of gene regulation strategies in compact genomes, such as those of filamentous fungi. Characterization of alternative transcripts and nTARs paves the way to the discovery of putative new genes, alternative peptides or regulatory non-coding RNAs.

Published
2022
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2. The taxonomy of the model filamentous fungus Podospora anserina

Author

S. Lorena Ament-Velásquez, Hanna Johannesson, Tatiana Giraud, Robert Debuchy, Sven J. Saupe, Alfons J. M. Debets, Eric Bastiaans, Fabienne Malagnac, Pierre Grognet, Leonardo Peraza-Reyes, Pierre Gladieux, Åsa Kruys, Philippe Silar, Sabine M. Huhndorf, Andrew N. Miller, and Aaron A. Vogan

Subjects
Botany, QK1-989
Abstract

The filamentous fungus Podospora anserina has been used as a model organism for more than 100 years and has proved to be an invaluable resource in numerous areas of research. Throughout this period, P. anserina has been embroiled in a number of taxonomic controversies regarding the proper name under which it should be called. The most recent taxonomic treatment proposed to change the name of this important species to Triangularia anserina. The results of past name changes of this species indicate that the broader research community is unlikely to accept this change, which will lead to nomenclatural instability and confusion in literature. Here, we review the phylogeny of the species closely related to P. anserina and provide evidence that currently available marker information is insufficient to resolve the relationships amongst many of the lineages. We argue that it is not only premature to propose a new name for P. anserina based on current data, but also that every effort should be made to retain P. anserina as the current name to ensure stability and to minimise confusion in scientific literature. Therefore, we synonymise Triangularia with Podospora and suggest that either the type species of Podospora be moved to P. anserina from P. fimiseda or that all species within the Podosporaceae be placed in the genus Podospora.

Published
2020
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3. A RID-like putative cytosine methyltransferase homologue controls sexual development in the fungus Podospora anserina.

Author

Pierre Grognet, Hélène Timpano, Florian Carlier, Jinane Aït-Benkhali, Véronique Berteaux-Lecellier, Robert Debuchy, Frédérique Bidard, and Fabienne Malagnac

Subjects
Genetics, QH426-470
Abstract

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 ΔPaRid defective mutants. Crosses involving P. anserina ΔPaRid mutants are sterile. Our results show that, although gametes are readily formed and fertilization occurs in a ΔPaRid background, sexual development is blocked just before the individualization of the dikaryotic cells leading to meiocytes. Complementation of ΔPaRid 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.

Published
2019
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4. Genes that bias Mendelian segregation.

Author

Pierre Grognet, Hervé Lalucque, Fabienne Malagnac, and Philippe Silar

Subjects
Genetics, QH426-470
Abstract

Mendel laws of inheritance can be cheated by Meiotic Drive Elements (MDs), complex nuclear genetic loci found in various eukaryotic genomes and distorting segregation in their favor. Here, we identify and characterize in the model fungus Podospora anserina Spok1 and Spok2, two MDs known as Spore Killers. We show that they are related genes with both spore-killing distorter and spore-protecting responder activities carried out by the same allele. These alleles act as autonomous elements, exert their effects independently of their location in the genome and can act as MDs in other fungi. Additionally, Spok1 acts as a resistance factor to Spok2 killing. Genetical data and cytological analysis of Spok1 and Spok2 localization during the killing process suggest a complex mode of action for Spok proteins. Spok1 and Spok2 belong to a multigene family prevalent in the genomes of many ascomycetes. As they have no obvious cellular role, Spok1 and Spok2 Spore Killer genes represent a novel kind of selfish genetic elements prevalent in fungal genome that proliferate through meiotic distortion.

Published
2014
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5. Rab-GDI complex dissociation factor expressed through translational frameshifting in filamentous ascomycetes.

Author

Fabienne Malagnac, Céline Fabret, Magali Prigent, Jean-Pierre Rousset, Olivier Namy, and Philippe Silar

Subjects
Medicine, Science
Abstract

In the model fungus Podospora anserina, the PaYIP3 gene encoding the orthologue of the Saccharomyces cerevisiae YIP3 Rab-GDI complex dissociation factor expresses two polypeptides, one of which, the long form, is produced through a programmed translation frameshift. Inactivation of PaYIP3 results in slightly delayed growth associated with modification in repartition of fruiting body on the thallus, along with reduced ascospore production on wood. Long and short forms of PaYIP3 are expressed in the mycelium, while only the short form appears expressed in the maturing fruiting body (perithecium). The frameshift has been conserved over the evolution of the Pezizomycotina, lasting for over 400 million years, suggesting that it has an important role in the wild.

Published
2013
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6. Sex in cheese: evidence for sexuality in the fungus Penicillium roqueforti.

Author

Jeanne Ropars, Joëlle Dupont, Eric Fontanillas, Ricardo C Rodríguez de la Vega, Fabienne Malagnac, Monika Coton, Tatiana Giraud, and Manuela López-Villavicencio

Subjects
Medicine, Science
Abstract

Although most eukaryotes reproduce sexually at some moment of their life cycle, as much as a fifth of fungal species were thought to reproduce exclusively asexually. Nevertheless, recent studies have revealed the occurrence of sex in some of these supposedly asexual species. For industrially relevant fungi, for which inoculums are produced by clonal-subcultures since decades, the potentiality for sex is of great interest for strain improvement strategies. Here, we investigated the sexual capability of the fungus Penicillium roqueforti, used as starter for blue cheese production. We present indirect evidence suggesting that recombination could be occurring in this species. The screening of a large sample of strains isolated from diverse substrates throughout the world revealed the existence of individuals of both mating types, even in the very same cheese. The MAT genes, involved in fungal sexual compatibility, appeared to evolve under purifying selection, suggesting that they are still functional. The examination of the recently sequenced genome of the FM 164 cheese strain enabled the identification of the most important genes known to be involved in meiosis, which were found to be highly conserved. Linkage disequilibria were not significant among three of the six marker pairs and 11 out of the 16 possible allelic combinations were found in the dataset. Finally, the detection of signatures of repeat induced point mutations (RIP) in repeated sequences and transposable elements reinforces the conclusion that P. roqueforti underwent more or less recent sex events. In this species of high industrial importance, the induction of a sexual cycle would open the possibility of generating new genotypes that would be extremely useful to diversify cheese products.

Published
2012
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7. Size Variation of the Nonrecombining Region on the Mating-Type Chromosomes in the Fungal Podospora anserina Species Complex

Author

Stéphanie Le Prieur, Myriam Berramdane, Fanny E. Hartmann, Philippe Silar, Fabienne Malagnac, Sandra Lorena Ament-Velásquez, Aaron A. Vogan, Tatiana Giraud, Pierre Grognet, Valérie Gautier, Hanna Johannesson, Alodie Snirc, Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Epigénétique et développement chez les champignons (EDC), Département Biologie des Génomes (DBG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Ecologie Systématique et Evolution (ESE), Université Paris-Sud - Paris 11 (UP11)-AgroParisTech-Centre National de la Recherche Scientifique (CNRS), Uppsala Universitet [Uppsala], Laboratoire Interdisciplinaire des Energies de Demain (LIED (UMR_8236)), Centre National de la Recherche Scientifique (CNRS)-Université de Paris (UP), Université Paris-Saclay, and Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité)

Subjects
0106 biological sciences, Mating type, Linkage disequilibrium, Species complex, Heterozygote, pseudohomothallism, fungal chromosomes, [SDV]Life Sciences [q-bio], Gene Conversion, Locus (genetics), Self-Fertilization, AcademicSubjects/SCI01180, 010603 evolutionary biology, 01 natural sciences, Podospora anserina, Loss of heterozygosity, 03 medical and health sciences, Podospora, Genetics, [PHYS.COND]Physics [physics]/Condensed Matter [cond-mat], Molecular Biology, Ecology, Evolution, Behavior and Systematics, Discoveries, 030304 developmental biology, [PHYS]Physics [physics], Recombination, Genetic, 0303 health sciences, convergence, biology, sex chromosomes, AcademicSubjects/SCI01130, evolutionary strata, mating-type chromosomes, biology.organism_classification, Mating system, Genes, Mating Type, Fungal, Biological Evolution, pseudo-homothallism, Evolutionary biology, automixis, fungi, transposable elements, Chromosomes, Fungal
Abstract

Sex chromosomes often carry large nonrecombining regions that can extend progressively over time, generating evolutionary strata of sequence divergence. However, some sex chromosomes display an incomplete suppression of recombination. Large genomic regions without recombination and evolutionary strata have also been documented around fungal mating-type loci, but have been studied in only a few fungal systems. In the model fungus Podospora anserina (Ascomycota, Sordariomycetes), the reference S strain lacks recombination across a 0.8-Mb region around the mating-type locus. The lack of recombination in this region ensures that nuclei of opposite mating types are packaged into a single ascospore (pseudohomothallic lifecycle). We found evidence for a lack of recombination around the mating-type locus in the genomes of ten P. anserina strains and six closely related pseudohomothallic Podospora species. Importantly, the size of the nonrecombining region differed between strains and species, as indicated by the heterozygosity levels around the mating-type locus and experimental selfing. The nonrecombining region is probably labile and polymorphic, differing in size and precise location within and between species, resulting in occasional, but infrequent, recombination at a given base pair. This view is also supported by the low divergence between mating types, and the lack of strong linkage disequilibrium, chromosomal rearrangements, transspecific polymorphism and genomic degeneration. We found a pattern suggestive of evolutionary strata in P. pseudocomata. The observed heterozygosity levels indicate low but nonnull outcrossing rates in nature in these pseudohomothallic fungi. This study adds to our understanding of mating-type chromosome evolution and its relationship to mating systems.

Published
2021

8. Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes

Author

Fabienne Malagnac, Pierre Grognet, Fantin Carpentier, Marine Duhamel, Philippe Silar, Fanny E. Hartmann, Tatiana Giraud, Michael E. Hood, Marie Foulongne-Oriol, Centre National de la Recherche Scientifique (CNRS), AgroParisTech, Université Paris-Saclay, Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Epigénétique et développement chez les champignons (EDC), Département Biologie des Génomes (DBG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), U-Psud, Université Paris-Saclay, Université Paris Saclay (COMUE), European Project: 832352, Ecologie Systématique et Evolution (ESE), AgroParisTech-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Amherst College, Unité de recherche Mycologie et Sécurité des Aliments (MycSA), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université Paris Diderot - Paris 7 (UPD7), Centre National de la Recherche Scientifique (CNRS)-AgroParisTech-Université Paris-Sud - Paris 11 (UP11), Institut Jean-Pierre Bourgin (IJPB), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Laboratoire Interdisciplinaire des Energies de Demain (LIED (UMR_8236)), Centre National de la Recherche Scientifique (CNRS)-Université de Paris (UP), Ruhr-Universität Bochum [Bochum], and Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité)

Subjects
0106 biological sciences, 0301 basic medicine, Transposable element, mating-type loci, Mating type, supergene, neurospora, Neurospora tetrasperma, Physiology, [SDV]Life Sciences [q-bio], podospora, Plant Science, Review, 01 natural sciences, Podospora anserina, Tansley Reviews, [SDV.BDLR.RS]Life Sciences [q-bio]/Reproductive Biology/Sexual reproduction, 03 medical and health sciences, Genetic drift, ascomycetes, Gene, [SDV.MP.MYC]Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, ComputingMilieux_MISCELLANEOUS, Recombination, Genetic, Sex Chromosomes, biology, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Tansley Review, Fungi, evolutionary strata, basidiomycetes, Agaricus bisporus, biology.organism_classification, Genes, Mating Type, Fungal, Biological Evolution, Cryptococcus, 030104 developmental biology, Evolutionary biology, Microbotryum, Recombination, 010606 plant biology & botany
Abstract

International audience; Genomic regions determining sexual compatibility often display recombination suppression, as occurs in sex chromosomes, plant self‐incompatibility loci and fungal mating‐type loci. Regions lacking recombination can extend beyond the genes determining sexes or mating types, by several successive steps of recombination suppression. Here we review the evidence for recombination suppression around mating‐type loci in fungi, sometimes encompassing vast regions of the mating‐type chromosomes. The suppression of recombination at mating‐type loci in fungi has long been recognized and maintains the multiallelic combinations required for correct compatibility determination. We review more recent evidence for expansions of recombination suppression beyond mating‐type genes in fungi (‘evolutionary strata’), which have been little studied and may be more pervasive than commonly thought. We discuss testable hypotheses for the ultimate (evolutionary) and proximate (mechanistic) causes for such expansions of recombination suppression, including (1) antagonistic selection, (2) association of additional functions to mating‐type, such as uniparental mitochondria inheritance, (3) accumulation in the margin of nonrecombining regions of various factors, including deleterious mutations or transposable elements resulting from relaxed selection, or neutral rearrangements resulting from genetic drift. The study of recombination suppression in fungi could thus contribute to our understanding of recombination suppression expansion across a broader range of organisms.

Published
2020

9. Loss of EZH2-like or SU(VAR)3–9-like proteins causes simultaneous perturbations in H3K27 and H3K9 tri-methylation and associated developmental defects in the fungus Podospora anserina

Author

Fabienne Malagnac, F. Carlier, C. Souaid, L. Maroc, M. Li, Robert Debuchy, Pierre Grognet, Daan Noordermeer, Spinelli, Lionel, Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Génétique Quantitative et Evolution - Le Moulon (Génétique Végétale) (GQE-Le Moulon), AgroParisTech-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Theories and Approaches of Genomic Complexity (TAGC), and Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)

Subjects
Heterochromatin, [SDV]Life Sciences [q-bio], macromolecular substances, QH426-470, Cell fate determination, Podospora anserina, Histone methylation, 03 medical and health sciences, 0302 clinical medicine, Podospora, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], Gene expression, Genetics, Molecular Biology, 030304 developmental biology, 0303 health sciences, biology, Research, EZH2, Methyltransferases, DNA Methylation, biology.organism_classification, Cell biology, Sexual development, ChIP-seq, [SDV] Life Sciences [q-bio], Histone, Histone methyltransferase, biology.protein, [SDV.BBM.GTP] Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], 030217 neurology & neurosurgery
Abstract

Background Selective gene silencing is key to development. It is generally accepted that H3K27me3-enriched heterochromatin maintains transcriptional repression established during early development and regulates cell fate. Conversely, H3K9me3-enriched heterochromatin prevents differentiation but constitutes protection against transposable elements. We exploited the fungus Podospora anserina, a valuable alternative to higher eukaryote models, to question the biological relevance and functional interplay of these two distinct heterochromatin conformations. Results We established genome-wide patterns of H3K27me3 and H3K9me3 modifications, and found these marks mutually exclusive within gene-rich regions but not within repeats. We generated the corresponding histone methyltransferase null mutants and showed an interdependence of H3K9me3 and H3K27me3 marks. Indeed, removal of the PaKmt6 EZH2-like enzyme resulted not only in loss of H3K27me3 but also in significant H3K9me3 reduction. Similarly, removal of PaKmt1 SU(VAR)3–9-like enzyme caused loss of H3K9me3 and substantial decrease of H3K27me3. Removal of the H3K9me binding protein PaHP1 provided further support to the notion that each type of heterochromatin requires the presence of the other. We also established that P. anserina developmental programs require H3K27me3-mediated silencing, since loss of the PaKmt6 EZH2-like enzyme caused severe defects in most aspects of the life cycle including growth, differentiation processes and sexual reproduction, whereas loss of the PaKmt1 SU(VAR)3–9-like enzyme resulted only in marginal defects, similar to loss of PaHP1. Conclusions Our findings support a conserved function of the PRC2 complex in fungal development. However, we uncovered an intriguing evolutionary fluidity in the repressive histone deposition machinery, which challenges canonical definitions of constitutive and facultative heterochromatin.

Published
2021

10. Loss of Polycomb Protein EZH2 causes major depletion of H3K27 and H3K9 tri-methylation and developmental defects in the fungus Podospora anserina

Author

Pierre Grognet, F. Carlier, Daan Noordermeer, Robert Debuchy, Fabienne Malagnac, L. Maroc, C. Souaid, Institut de Biologie Intégrative de la Cellule (I2BC), and Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)

Subjects
Transposable element, 0303 health sciences, biology, Heterochromatin, macromolecular substances, Cell fate determination, biology.organism_classification, Podospora anserina, Histone methylation, Chromatin, Cell biology, ChIP-seq, 03 medical and health sciences, 0302 clinical medicine, Histone, sexual development, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], biology.protein, Gene silencing, Eukaryote, 030217 neurology & neurosurgery, 030304 developmental biology
Abstract

Selective gene silencing is key to development. The H3K27me3 enriched heterochromatin maintains transcription repression established during early development and regulates cell fate. Conversely, H3K9me3 enriched heterochromatin prevents differentiation but constitutes a permanent protection against transposable element. We exploited the fungusPodospora anserina, a valuable alternative to higher eukaryote models to question the biological relevance and interplay of these two distinct heterochromatin conformations. We found that H3K27me3 and H3K9me3 modifications are mutually exclusive within gene-rich regions but not within repeats. Lack of PaKmt6 EZH2-like enzyme resulted in loss of H3K27me3 and in significant H3K9me3 reduction, whereas lack of PaKmt1 SU(VAR)3-9-like enzyme caused loss of H3K9me3 only. We established thatP. anserinadevelopmental programs require H3K27me3 mediated silencing unlike most fungi studied to date. Our findings provide new insight into roles of these histone marks and into the relationship between chromatin modifications and development.

Published
2020

11. Cyclooxygenases and lipoxygenases are used by the fungus Podospora anserina to repel nematodes

Author

Charlie Boucher, Fabienne Malagnac, Laetitia Chan Ho Tong, Isabelle Lacaze, César Trannoy, Hervé Lalucque, Yohann Petit, Roselyne Ferrari, Stéphane Moularat, Camille Oger, Jean-Marie Galano, Océane Vanparis, Justine Bertrand-Michel, Thierry Durand, Sylvain Brun, Philippe Silar, Jaafar Kilani, Pauline Le Faouder, Laboratoire Interdisciplinaire des Energies de Demain (LIED (UMR_8236)), Université Paris Diderot - Paris 7 (UPD7)-Centre National de la Recherche Scientifique (CNRS), Centre de Physiopathologie Toulouse Purpan (CPTP), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Institut des Biomolécules Max Mousseron [Pôle Chimie Balard] (IBMM), Ecole Nationale Supérieure de Chimie de Montpellier (ENSCM)-Institut de Chimie du CNRS (INC)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Plateforme d'Analyse Protéomique de Paris Sud Ouest (PAPPSO), Institut de génétique et microbiologie [Orsay] (IGM), Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS), Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Département Biologie des Génomes (DBG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Université de Paris (UP), Centre Scientifique et Technique du Bâtiment (CSTB), Institut des Maladies Métaboliques et Cardiovasculaires (I2MC), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, MetaToul-MetaboHUB, Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie du CNRS (INC)-Université de Montpellier (UM)-Ecole Nationale Supérieure de Chimie de Montpellier (ENSCM), Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPC), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM), MetaboHUB-MetaToul, MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Centre de Physiopathologie Toulouse Purpan ex IFR 30 et IFR 150 (CPTP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Ecole Nationale Supérieure de Chimie de Montpellier (ENSCM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), and Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)

Subjects
0301 basic medicine, aspergillus-fumigatus, Nematoda, [SDV]Life Sciences [q-bio], 030106 microbiology, Mutant, Lipoxygenase, Biophysics, Fungus, Biochemistry, Podospora anserina, Fungal Proteins, 03 medical and health sciences, chemistry.chemical_compound, Podospora, Gene Expression Regulation, Fungal, Animals, Oxylipins, lc-ms/ms, Volatile organic compounds, Mycotoxin, Molecular Biology, Gene, metabolites, chemistry.chemical_classification, endophytic fungus, biology, Wild type, Fungi, Lipoxygenases, phytoprostanes, biology.organism_classification, volatile organic-compounds, Cyclooxygenase, Enzyme, plant-growth, chemistry, Prostaglandin-Endoperoxide Synthases, Insect Repellents, biology.protein, chromatography, Lipid Peroxidation, polyunsaturated fatty-acids
Abstract

WOS:000443665300007; International audience; Oxylipins are secondary messengers used universally in the living world for communication and defense. The paradigm is that they are produced enzymatically for the eicosanoids and non-enzymatically for the isoprostanoids. They are supposed to be degraded into volatile organic compounds (VOCs) and to participate in aroma production. Some such chemicals composed of eight carbons are also envisoned as alternatives to fossil fuels. In fungi, oxylipins have been mostly studied in Aspergilli and shown to be involved in signalling asexual versus sexual development, mycotoxin production and interaction with the host for pathogenic species. Through targeted gene deletions of genes encoding oxylipin-producing enzymes and chemical analysis of oxylipins and volatile organic compounds, we show that in the distantly-related ascomycete Podospora anserina, isoprostanoids are likely produced enzymatically. We show the disappearance in the mutants lacking lipoxygenases and cyclooxygenases of the production of 10-hydroxy-octadecadienoic acid and that of 1-octen-3-ol, a common volatile compound. Importantly, this was correlated with the inability of the mutants to repel nematodes as efficiently as the wild type. Overall, our data show that in this fungus, oxylipins are not involved in signalling development but may rather be used directly or as precursors in the production of odors against potential agressors. Significance: We analyzse the role in inter-kingdom communication of lipoxygenase (lox) and cyclooxygenase (cox) genes in the model fungus Podospora anserina. Through chemical analysis we define the oxylipins and volatile organic compounds (VOCs)produce by wild type and mutants for cox and lox genes, We show that the COX and LOX genes are required for the production of some eight carbon VOCs. We show that COX and LOX genes are involved in the production of chemicals repelling nematodes. This role is very different from the ones previously evidenced in other fungi.

Published
2018

12. Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle

Author

Alan Kuo, Rhyan B. Dockter, Juan Chen, Shingo Miyauchi, Thibaut Payen, Benjamin Noel, François Le Tacon, Jean-Marc Aury, Minou Nowrousian, Mei Wang, Emmanuelle Morin, Annegret Kohler, Claude Murat, Petr Baldrian, Laure Fauchery, Julie Poulain, Lucia Žifčáková, Julie Guy, Claudia Riccioni, Corinne Da Silva, Francis Martin, László Nagy, Patrick Wincker, Richard Splivallo, Beatrice Belfiori, Fabienne Malagnac, Anna Lipzen, Paola Bonfante, Stefanie Traeger, Francesco Paolocci, Alicia Clum, Mirco Iotti, Yaron Sitrit, Elisabetta Levati, Igor V. Grigoriev, Alessandra Zambonelli, Barbara Montanini, Erika Lindquist, Joseph W. Spatafora, Kerrie Barry, Mathieu Hainaut, Andrea Rubini, Simone Ottonello, Virginie Molinier, Krisztina Krizsán, Raffaella Balestrini, Nicolas Cichocki, Daniel Wipf, Bernard Henrissat, Antonietta Mello, Interactions Arbres-Microorganismes (IAM), Institut National de la Recherche Agronomique (INRA)-Université de Lorraine (UL), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), US Department of Energy Joint Genome Institute, U.S Department of Energy, U.S. Department of Energy [Washington] (DOE)-U.S. Department of Energy [Washington] (DOE), Institute of medicinal plant development, Chinese Academy of Medical Sciences, Synthet & Syst Biol Unit, Hungarian Academy of Sciences (MTA), CNR, Ist Protez Piante, UOS Torino, Laboratory of Functional Genomics and Protein Engineering, Biochemistry and Molecular Biology Unit, Department of Life Sciences, University of Parma = Università degli studi di Parma [Parme, Italie], Dept Life Sci, Biochem & Mol Biol Unit, Lab Funct Genom & Prot Engn, Joint Genome Institute, United States Department of Energy, Plant Genetics Institute, Consiglio Nazionale delle Ricerche [Roma] (CNR), Department of Energy / Joint Genome Institute (DOE), Los Alamos National Laboratory (LANL), Génomique métabolique (UMR 8030), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université d'Évry-Val-d'Essonne (UEVE), Dipartimento Protez & Valorizzaz Agroalimentare, Alma Mater Studiorum University of Bologna (UNIBO), Institut de génétique et microbiologie [Orsay] (IGM), Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS), Istituto per la Protezione delle Piante, Agroécologie [Dijon], Université de Bourgogne (UB)-Institut National de la Recherche Agronomique (INRA)-Université Bourgogne Franche-Comté [COMUE] (UBFC)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement, IPF – Integrative Fungal Research, Goethe-Universität Frankfurt am Main, Institut für biologie und biotechnologie der pflanzen, Westfälische Wilhelms-Universität Münster (WWU), 0977 Unité associée de Biologie forestière, Institut National de la Recherche Agronomique (INRA), Institute of Microbiology of the CAS, Department of Botany and Plant Pathology, Oregon State University (OSU), Architecture et fonction des macromolécules biologiques (AFMB), Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU)-Institut National de la Recherche Agronomique (INRA), Department of Biochemistry and Molecular Biology, Medical and Health Science Center, Institut de Génomique d'Evry (IG), Institut de Biologie François JACOB (JACOB), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, Dipartimento di Biologia Vegetale, Università degli studi di Torino (UNITO), French National Research Agency through the project SYSTRUF ANR-14-CE06-0020, ANR-09-STRA-10, French National Research Agency through the project SYMWOOD (Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems) ANR-11-LABX 0002 01, Office of Science of the US Department of Energy DE-AC02-05CH11231, France Genomique ANR-10-INBS-09, Region Lorraine Research Council, European Commission (European Regional Development Fund), University of Parma, Interuniversity Consortium for Biotechnologies, Piedmont Region, Czech Science Foundation 16-08916S, German Research Foundation NO407/7-1, Department of General and Molecular Botany, ANR-14-CE06-0020,FUNTUNE,Cocktails enzymatiques inspirés de modèles fongiques pour la déconstruction contrôlée de la biomasse végétale(2014), ANR-10-STRA-0010,COMANCHE,Interactions écosystémiques et impacts anthropiques dans les populations de Coquilles St-Jacques de la Manche(2010), ANR-11-LABX-0002,ARBRE,Recherches Avancées sur l'Arbre et les Ecosytèmes Forestiers(2011), ANR-10-INBS-0009,France-Génomique,Organisation et montée en puissance d'une Infrastructure Nationale de Génomique(2010), Université de Lorraine (UL)-Institut National de la Recherche Agronomique (INRA), U.S. Department of Energy (DOE)-U.S. Department of Energy (DOE), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique (INRA)-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement, Institut National de la Recherche Agronomique (INRA)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), ANR-10-INBS-09-01/10-INBS-0009,France-Génomique,Organisation et montée en puissance d'une Infrastructure Nationale de Génomique(2010), Murat, Claude, Payen, Thibaut, Noel, Benjamin, Kuo, Alan, Morin, Emmanuelle, Chen, Juan, Kohler, Annegret, Krizsán, Krisztina, Balestrini, Raffaella, Da Silva, Corinne, Montanini, Barbara, Hainaut, Mathieu, Levati, Elisabetta, Barry, Kerrie W., Belfiori, Beatrice, Cichocki, Nicola, Clum, Alicia, Dockter, Rhyan B., Fauchery, Laure, Guy, Julie, Iotti, Mirco, Le Tacon, Françoi, Lindquist, Erika A., Lipzen, Anna, Malagnac, Fabienne, Mello, Antonietta, Molinier, Virginie, Miyauchi, Shingo, Poulain, Julie, Riccioni, Claudia, Rubini, Andrea, Sitrit, Yaron, Splivallo, Richard, Traeger, Stefanie, Wang, Mei, Žifčáková, Lucia, Wipf, Daniel, Zambonelli, Alessandra, Paolocci, Francesco, Nowrousian, Minou, Ottonello, Simone, Baldrian, Petr, Spatafora, Joseph W., Henrissat, Bernard, Nagy, Laszlo G., Aury, Jean-Marc, Wincker, Patrick, Grigoriev, Igor V., Bonfante, Paola, Martin, Francis M., Università degli studi di Parma = University of Parma (UNIPR), National Research Council of Italy | Consiglio Nazionale delle Ricerche (CNR), Institut National de la Recherche Agronomique (INRA)-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Université Bourgogne Franche-Comté [COMUE] (UBFC), Westfälische Wilhelms-Universität Münster = University of Münster (WWU), Unité associée de biologie forestière, Université Paris-Saclay-Institut de Biologie François JACOB (JACOB), Università degli studi di Torino = University of Turin (UNITO), and MURAT-FURMINIEUX, Claude

Subjects
0301 basic medicine, volatile organic compound, tuber (truffles), [SDV]Life Sciences [q-bio], champignon, Pezizomycetes, truffle, Tuber aestivum, Mycorrhizae, DNA, Fungal, Life History Traits, Phylogeny, 2. Zero hunger, Truffle, Genome, biology, Ecology, composé organique volatil, food and beverages, Ecology, Evolution, Behavior and Systematics, Tuberaceae, Fungal, expression différentielle, Genome, Fungal, Sequence Analysis, tuber, Evolution, no key words, 03 medical and health sciences, truffe, Behavior and Systematics, Ascomycota, Phylogenetics, ddc:570, Botany, Choiromyces, Genetics, Symbiosis, Comparative genomics, Human Genome, fungi, Sequence Analysis, DNA, DNA, champignon ectomycorhizien, 15. Life on land, biology.organism_classification, Ecology, Evolution, Behavior and Systematic, 030104 developmental biology, Tuber melanosporum
Abstract

Tuberaceae is one of the most diverse lineages of symbiotic truffle-forming fungi. To understand the molecular underpinning of the ectomycorrhizal truffle lifestyle, we compared the genomes of Piedmont white truffle (Tuber magnatum), Périgord black truffle (Tuber melanosporum), Burgundy truffle (Tuber aestivum), pig truffle (Choiromyces venosus) and desert truffle (Terfezia boudieri) to saprotrophic Pezizomycetes. Reconstructed gene duplication/loss histories along a time-calibrated phylogeny of Ascomycetes revealed that Tuberaceae-specific traits may be related to a higher gene diversification rate. Genomic features in Tuber species appear to be very similar, with high transposon content, few genes coding lignocellulose-degrading enzymes, a substantial set of lineage-specific fruiting-body-upregulated genes and high expression of genes involved in volatile organic compound metabolism. Developmental and metabolic pathways expressed in ectomycorrhizae and fruiting bodies of T. magnatum and T. melanosporum are unexpectedly very similar, owing to the fact that they diverged ~100 Ma. Volatile organic compounds from pungent truffle odours are not the products of Tuber-specific gene innovations, but rely on the differential expression of an existing gene repertoire. These genomic resources will help to address fundamental questions in the evolution of the truffle lifestyle and the ecology of fungi that have been praised as food delicacies for centuries.

Published
2018

13. Prions and Prion-like Phenomena in Epigenetic Inheritance

Author

Hervé Lalucque, Philippe Silar, Fabienne Malagnac, Tinh-Suong Nguyen, Canadian Nuclear Safety Commission (CNSC), Canadian Nuclear Safety Commission, Laboratoire Interdisciplinaire des Energies de Demain (LIED (UMR_8236)), and Centre National de la Recherche Scientifique (CNRS)-Université de Paris (UP)

Subjects
0301 basic medicine, biology, [SDV]Life Sciences [q-bio], Saccharomyces cerevisiae, Inheritance (genetic algorithm), Computational biology, biology.organism_classification, Hereditary traits, 03 medical and health sciences, 030104 developmental biology, 0302 clinical medicine, Dna encoding, Epigenetics, Prion protein, Gene, 030217 neurology & neurosurgery, Function (biology), ComputingMilieux_MISCELLANEOUS
Abstract

At the time that the concept of gene as a stretch of DNA encoding a function was not fully established, several models proposed that regulatory networks or macromolecular structures could also generate hereditary traits. Long forgotten, this kind of epigenetic inheritance has been revived by the discovery that some non-mendelian inheritance in the yeast Saccharomyces cerevisiae is due to proteins able to switch their structure in an autocatalytic manner, now called prion. We review here what we know about these cellular prions; and also about additional phenomena, which in their genetic determinism resemble prions, however, based on alternative states of macromolecular complexes or regulatory networks.

Published
2017

14. 16 Sexual Development in Fungi

Author

Fabienne Malagnac, Leonardo Peraza-Reyes, Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Différenciation sexuée et méiose chez les champignons (DSMC), Département Biologie des Génomes (DBG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), and Wendland, Jürgen

Subjects
0301 basic medicine, [SDV]Life Sciences [q-bio], 030106 microbiology, Plasmogamy, Fungus, Biology, biology.organism_classification, Sexual reproduction, Karyogamy, 03 medical and health sciences, Multicellular organism, 030104 developmental biology, Meiosis, Evolutionary biology, Ploidy, Mating, ComputingMilieux_MISCELLANEOUS
Abstract

Sexual development is the process that allows species to reproduce with the potential of generating genetically recombinant progeny. In fungi, sexual reproduction is sustained by a large diversity of developmental processes, which include different mating strategies both at the level of genetic determination and structural organization, as well as diverse morphogenetic systems exhibiting complex temporal and developmental regulation. Sexual reproduction involves the succession of a number of developmental events, which include the differentiation of mating structures, the recognition and attraction of mating partners, and the subsequent alternation of haploid and diploid phases sustained by the progression of plasmogamy, karyogamy, and meiosis. Different temporal organization between these processes can generate distinct genetic constitutions and recombinant genotypes throughout the life cycle of a fungus, as well as amplify the genetic exchange resulting from a single mating event. Sexual reproduction in fungi is often associated to the differentiation of complex multicellular structures, and the progression through the sexual stages requires precise coordination with the differentiation of multiple cell types. In addition, sexual development is also a major process where genome integrity is scrutinized and preserved. The fundamental processes governing sexual development in fungi are now significantly understood at the cellular and molecular level, and increasing comparative analyses among different fungal lineages have started to expose some essential differences in the orchestration of their developmental processes, which account for the diversity of sexual reproductive strategies that have evolved in fungi.

Published
2016

15. Genes that bias mendelian segregation

Author

Fabienne Malagnac, Hervé Lalucque, Philippe Silar, Pierre Grognet, Institut de génétique et microbiologie [Orsay] (IGM), and Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Cancer Research, lcsh:QH426-470, Yeast and Fungal Models, Mycology, Research and Analysis Methods, Microbiology, Genome, Podospora anserina, Fungal Proteins, 03 medical and health sciences, symbols.namesake, Model Organisms, 0302 clinical medicine, Podospora, Chromosome Segregation, Genetics, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, Allele, Genome Evolution, Molecular Biology, Gene, Alleles, Crosses, Genetic, Genetics (clinical), Ecology, Evolution, Behavior and Systematics, 030304 developmental biology, Evolutionary Biology, 0303 health sciences, Fungal protein, biology, fungi, Fungal genetics, Biology and Life Sciences, Computational Biology, Spores, Fungal, biology.organism_classification, lcsh:Genetics, Meiosis, Meiotic drive, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Mendelian inheritance, symbols, Gene Function, 030217 neurology & neurosurgery, Research Article
Abstract

Mendel laws of inheritance can be cheated by Meiotic Drive Elements (MDs), complex nuclear genetic loci found in various eukaryotic genomes and distorting segregation in their favor. Here, we identify and characterize in the model fungus Podospora anserina Spok1 and Spok2, two MDs known as Spore Killers. We show that they are related genes with both spore-killing distorter and spore-protecting responder activities carried out by the same allele. These alleles act as autonomous elements, exert their effects independently of their location in the genome and can act as MDs in other fungi. Additionally, Spok1 acts as a resistance factor to Spok2 killing. Genetical data and cytological analysis of Spok1 and Spok2 localization during the killing process suggest a complex mode of action for Spok proteins. Spok1 and Spok2 belong to a multigene family prevalent in the genomes of many ascomycetes. As they have no obvious cellular role, Spok1 and Spok2 Spore Killer genes represent a novel kind of selfish genetic elements prevalent in fungal genome that proliferate through meiotic distortion., Author Summary Chromosome segregation during meiosis ensures that paternal and maternal chromosomes are equally transmitted to the progeny. Meiotic Drive Elements (MDs) are known to distort this 1∶1 ratio in many animal, plant, and fungal species by killing the gametes not carrying them. Most of the known MDs are complex genetic loci with separate genes for the killing activity and the resistance to said killing. Here, we report in a model fungus on two genes endowed with MD properties previously unreported. Both genes produce a single polypeptide and confer both killing and resistance. They exert their effect irrespective of their position in the genome. They can cross species barriers and promote bias in segregation in other species. As related genes are frequently observed in fungal genomes, we propose that they are representative of a novel kind of selfish genes that propagate by distorting the Mendel laws of segregation.

Published
2014

16. Multiple recent horizontal transfers of a large genomic region in cheese making fungi

Author

Anne-Laure Abraham, Anne Goarin, Jeanne Ropars, Maurizio Ceppi, Fabienne Malagnac, Jérôme Gouzy, Aaron Bensimon, Emmanuel Conseiller, Sandrine Lacoste, Erika Sallet, Yves Brygoo, Kevin Cheeseman, Philippe Silar, Tatiana Giraud, Robert Debuchy, Pierre Renault, Joëlle Dupont, Antoine Branca, MICrobiologie de l'ALImentation au Service de la Santé (MICALIS), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Département Systématique et Évolution, Muséum national d'Histoire naturelle (MNHN), Interactions plantes-microorganismes et santé végétale, Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), Université Paris-Sud - Paris 11 (UP11), Centre d'Immunologie de Marseille - Luminy (CIML), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU), Centre National de la Recherche Scientifique (CNRS), Institut de génétique et microbiologie [Orsay] (IGM), Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS), Laboratoire Interdisciplinaire des Energies de Demain (LIED (UMR_8236)), Université Paris Diderot - Paris 7 (UPD7)-Centre National de la Recherche Scientifique (CNRS), Univ. Paris-Sud, Université Paris-Saclay, AgroParisTech, Institut National de la Recherche Agronomique (INRA), ANR: FoodMicrobiome,ANR-08-ALIA-007-02, ANR-12-PDOC-0030,FROMA-GEN,Adaptation génomique chez les champignons du fromage (Penicillium)(2012), European Project: 309403,EC:FP7:ERC,ERC-2012-StG_20111109,GENOMEFUN(2013), Ecologie Systématique et Evolution (ESE), Ecole Nationale du Génie Rural, des Eaux et des Forêts (ENGREF)-Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS), Origine, structure et évolution de la biodiversité (OSEB), Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS), Physiologie de la reproduction et des comportements [Nouzilly] (PRC), Institut National de la Recherche Agronomique (INRA)-Institut Français du Cheval et de l'Equitation [Saumur]-Université de Tours-Centre National de la Recherche Scientifique (CNRS), Unité mixte de recherche interactions plantes-microorganismes, Institut National de la Recherche Agronomique (INRA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Laboratoire des interactions plantes micro-organismes (LIPM), Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Université Paris Diderot, Sorbonne Paris Cité, Paris, France, Université Paris Diderot - Paris 7 (UPD7), Centre National de la Recherche Scientifique (CNRS)-Université de Paris (UP), Aigrefoin, ANR-08-ALIA-0007,FOOD-MICROBIOMES,Outils innovants pour favoriser, en toute sécurité, l'utilisation des microorganismes naturels dans l'alimentation(2008), Université Paris-Sud - Paris 11 (UP11)-AgroParisTech-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-AgroParisTech-Université Paris-Sud - Paris 11 (UP11), Centre National de la Recherche Scientifique (CNRS)-Université de Tours-Institut Français du Cheval et de l'Equitation [Saumur]-Institut National de la Recherche Agronomique (INRA), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Giraud, Tatiana, Alimentation et industries alimentaires - Outils innovants pour favoriser, en toute sécurité, l'utilisation des microorganismes naturels dans l'alimentation - - FOOD-MICROBIOMES2008 - ANR-08-ALIA-0007 - ALIA - VALID, Retour Post-Doctorant - Adaptation génomique chez les champignons du fromage (Penicillium) - - FROMA-GEN2012 - ANR-12-PDOC-0030 - PDOC - VALID, and Genomics of adaptive divergence in Fungi - GENOMEFUN - - EC:FP7:ERC2013-03-01 - 2018-02-28 - 309403 - VALID

Subjects
Gene Transfer, Horizontal, Genomic Islands, media_common.quotation_subject, Microorganism, Applied Microbiology, [SDV]Life Sciences [q-bio], Molecular Sequence Data, General Physics and Astronomy, Biology, Microbiology, General Biochemistry, Genetics and Molecular Biology, Competition (biology), genomic, cheese, domestication, Saccharomyces, Genomic island, Genetics, [SDV.BBM] Life Sciences [q-bio]/Biochemistry, Molecular Biology, Base sequence, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, DNA, Fungal, Gene, Molecular Biology, media_common, adaptive divergence, Multidisciplinary, region, Base Sequence, food, Fungal genetics, Penicillium, General Chemistry, biology.organism_classification, [SDV] Life Sciences [q-bio], [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, fungi, Food environment
Abstract

Horizontal gene transfers (HGT), i.e., the transmission of genetic material between species not directly attributable to meiotic gene exchange, have long been acknowledged as a major driver of prokaryotic evolution and is increasingly recognized as an important source of adaptation in eukaryotes. In fungi in particular, many convincing examples of HGT have been reported to confer selective advantages on the recipient fungal host, either promoting fungal pathogenicity on plants or increasing their toxicity by the acquisition of secondary metabolic clusters, resulting in adaptation to new niches and in some cases eventually even in speciation. These horizontal gene transfers involve single genes, complete metabolic pathways or even entire chromosomes. A recent study has uncovered multiple recent horizontal transfers of a 575 kb genomic island in cheese Penicillium fungi, representing ca. 2% of the Penicillium roqueforti’s genome, that may confer selective advantage in the competing cheese environment where bacteria and fungi occur. Novel phylogenomic methods are being developed, revealing massive HGT among fungi. Altogether, these recent studies indicate that HGT is a crucial mechanism of rapid adaptation, even among eukaryotes.

Published
2014

17. Sex in Cheese: Evidence for Sexuality in the Fungus Penicillium roqueforti

Author

Ricardo C. Rodríguez de la Vega, Jeanne Ropars, Monika Coton, Manuela López-Villavicencio, Fabienne Malagnac, Tatiana Giraud, Joëlle Dupont, Eric Fontanillas, Institut de génétique et microbiologie [Orsay] (IGM), and Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Evolutionary Genetics, Mating type, Plant Science, Genome, Fungal Reproduction, Cheese, Fungal Evolution, DNA, Fungal, Recombination, Genetic, Genetics, Evolutionary Theory, 0303 health sciences, Multidisciplinary, Natural selection, biology, Meiosis, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Penicillium, Medicine, Research Article, Genotype, Blue cheese, Science, Molecular Sequence Data, Mycology, Microbiology, 03 medical and health sciences, food, Point Mutation, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, Amino Acid Sequence, food.cheese, Biology, 030304 developmental biology, Evolutionary Biology, Models, Genetic, 030306 microbiology, Fungi, Botany, Genomic Evolution, Penicillium roqueforti, Sequence Analysis, DNA, Genes, Mating Type, Fungal, biology.organism_classification, Organismal Evolution, Sexual reproduction, Microbial Evolution, DNA Transposable Elements
Abstract

International audience; Although most eukaryotes reproduce sexually at some moment of their life cycle, as much as a fifth of fungal species were thought to reproduce exclusively asexually. Nevertheless, recent studies have revealed the occurrence of sex in some of these supposedly asexual species. For industrially relevant fungi, for which inoculums are produced by clonal-subcultures since decades, the potentiality for sex is of great interest for strain improvement strategies. Here, we investigated the sexual capability of the fungus Penicillium roqueforti, used as starter for blue cheese production. We present indirect evidence suggesting that recombination could be occurring in this species. The screening of a large sample of strains isolated from diverse substrates throughout the world revealed the existence of individuals of both mating types, even in the very same cheese. The MAT genes, involved in fungal sexual compatibility, appeared to evolve under purifying selection, suggesting that they are still functional. The examination of the recently sequenced genome of the FM 164 cheese strain enabled the identification of the most important genes known to be involved in meiosis, which were found to be highly conserved. Linkage disequilibria were not significant among three of the six marker pairs and 11 out of the 16 possible allelic combinations were found in the dataset. Finally, the detection of signatures of repeat induced point mutations (RIP) in repeated sequences and transposable elements reinforces the conclusion that P. roqueforti underwent more or less recent sex events. In this species of high industrial importance, the induction of a sexual cycle would open the possibility of generating new genotypes that would be extremely useful to diversify cheese products.

Published
2012

18. The crucial role of the Pls1 tetraspanin during ascospore germination in Podospora anserina provides an example of the convergent evolution of morphogenetic processes in fungal plant pathogens and saprobes

Author

Marc-Henri Lebrun, Fabienne Malagnac, Philippe Silar, Crystel Barbisan, Karine Lambou, Didier Tharreau, Institut de génétique et microbiologie [Orsay] (IGM), Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS), and Tharreau, Didier

Subjects
Mutant, relation hôte-parasite, champignon pathogène, MESH: Amino Acid Sequence, biosynthèse, Podospora anserina, MESH: Plant Diseases, MESH: Melanins, Gene Expression Regulation, Fungal, tetraspanines Pls 1, MESH: Magnaporthe, MESH: Phylogeny, Phylogeny, MESH: Evolution, Molecular, Sequence Deletion, 0303 health sciences, Podospora, Vegetal Biology, biology, General Medicine, Articles, Spores, Fungal, MESH: Sequence Deletion, Magnaporthe grisea, Spore fongique, Cell biology, Magnaporthe, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, MESH: Fungal Proteins, MESH: Gene Expression Regulation, Fungal, MESH: Fungi, Hypha, Molecular Sequence Data, MESH: Sequence Alignment, Germination, Fungus, Microbiology, Evolution, Molecular, Fungal Proteins, 03 medical and health sciences, podospora anserina, MESH: Spores, Fungal, MESH: Podospora, Botany, Morphogénèse, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, ascospore, Amino Acid Sequence, Molecular Biology, Transmission des maladies, 030304 developmental biology, H20 - Maladies des plantes, Plant Diseases, Melanins, Appressorium, MESH: Molecular Sequence Data, 030306 microbiology, fungi, Fungi, biology.organism_classification, Gène, Ascospore, Protéine végétale, Sequence Alignment, Biologie végétale
Abstract

Pls1 tetraspanins were shown for some pathogenic fungi to be essential for appressorium-mediated penetration into their host plants. We show here that Podospora anserina , a saprobic fungus lacking appressorium, contains PaPls1 , a gene orthologous to known PLS1 genes. Inactivation of PaPls1 demonstrates that this gene is specifically required for the germination of ascospores in P. anserina . These ascospores are heavily melanized cells that germinate under inducing conditions through a specific pore. On the contrary, MgPLS1 , which fully complements a Δ PaPls1 ascospore germination defect, has no role in the germination of Magnaporthe grisea nonmelanized ascospores but is required for the formation of the penetration peg at the pore of its melanized appressorium. P. anserina mutants with mutation of PaNox2 , which encodes the NADPH oxidase of the NOX2 family, display the same ascospore-specific germination defect as the Δ PaPls1 mutant. Both mutant phenotypes are suppressed by the inhibition of melanin biosynthesis, suggesting that they are involved in the same cellular process required for the germination of P. anserina melanized ascospores. The analysis of the distribution of PLS1 and NOX2 genes in fungal genomes shows that they are either both present or both absent. These results indicate that the germination of P. anserina ascospores and the formation of the M. grisea appressorium penetration peg use the same molecular machinery that includes Pls1 and Nox2. This machinery is specifically required for the emergence of polarized hyphae from reinforced structures such as appressoria and ascospores. Its recurrent recruitment during fungal evolution may account for some of the morphogenetic convergence observed in fungi.

Published
2008

19. The genome sequence of the model ascomycete fungus Podospora anserina

Author

Patrick Wincker, Olivier Lespinet, Antoine Boivin, Fabienne Malagnac, Bérangère Pinan-Lucarré, Jean-Marc Aury, Annie Sainsard-Chanet, Sandrine Grossetete, Ronald P. de Vries, Marguerite Picard, Pedro M. Coutinho, Etienne Danchin, Véronique Anthouard, Olivier Jaillon, Philippe Silar, Daniel Gautheret, Bernard Henrissat, Anne Bourdais, Hamid Khalili, Julie Poulain, Béatrice Segurens, Sylvie Arnaise, Eric Espagne, Robert Debuchy, Michelle Dequard-Chablat, Betina M. Porcel, Corinne Da Silva, Evy Battaglia, Véronique Contamine, Carole H. Sellem, Arnaud Couloux, Evelyne Coppin, Jean Weissenbach, Riyad El Khoury, Véronique Berteaux-Lecellier, Institut de génétique et microbiologie [Orsay] (IGM), Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS), Génomique métabolique (UMR 8030), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Centre de génétique moléculaire (CGM), Centre National de la Recherche Scientifique (CNRS), and Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université d'Évry-Val-d'Essonne (UEVE)

Subjects
Evolution, champignon, Molecular Sequence Data, Genome, Podospora anserina, Neurospora crassa, Evolution, Molecular, 03 medical and health sciences, podospora anserina, Podospora, Gene Duplication, séquençage, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, Gene, 030304 developmental biology, Synteny, Expressed Sequence Tags, Whole genome sequencing, Genetics, 0303 health sciences, Base Sequence, biology, 030306 microbiology, Research, génome, gène, Molecular, biology.organism_classification, Carbon, Fungal, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, parasite, Genome, Fungal, Orthologous Gene
Abstract

A 10X draft sequence of Podospora anserina genome shows highly dynamic evolution since its divergence from Neurospora crassa., Background The dung-inhabiting ascomycete fungus Podospora anserina is a model used to study various aspects of eukaryotic and fungal biology, such as ageing, prions and sexual development. Results We present a 10X draft sequence of P. anserina genome, linked to the sequences of a large expressed sequence tag collection. Similar to higher eukaryotes, the P. anserina transcription/splicing machinery generates numerous non-conventional transcripts. Comparison of the P. anserina genome and orthologous gene set with the one of its close relatives, Neurospora crassa, shows that synteny is poorly conserved, the main result of evolution being gene shuffling in the same chromosome. The P. anserina genome contains fewer repeated sequences and has evolved new genes by duplication since its separation from N. crassa, despite the presence of the repeat induced point mutation mechanism that mutates duplicated sequences. We also provide evidence that frequent gene loss took place in the lineages leading to P. anserina and N. crassa. P. anserina contains a large and highly specialized set of genes involved in utilization of natural carbon sources commonly found in its natural biotope. It includes genes potentially involved in lignin degradation and efficient cellulose breakdown. Conclusion The features of the P. anserina genome indicate a highly dynamic evolution since the divergence of P. anserina and N. crassa, leading to the ability of the former to use specific complex carbon sources that match its needs in its natural biotope.

Published
2008

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