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Accueil > Départements > Biologie des Génomes > Eric ESPAGNE : Recombinaison et appariement méiotique

Publications de l’équipe

2019



  • A. Demené, L. Legrand, J. Gouzy, R. Debuchy, G. Saint-Jean, O. Fabreguettes, et C. Dutech, « Whole-genome sequencing reveals recent and frequent genetic recombination between clonal lineages of Cryphonectria parasitica in western Europe », Fungal Genetics and Biology, vol. 130, p. 122-133, sept. 2019.
    Résumé : Changes in the mode of reproduction are frequently observed in invasive fungal populations. The ascomycete Cryphonectria parasitica, which causes Chestnut Blight, was introduced to Europe from North America and Asia in the 20th century. Previous genotyping studies based on ten microsatellite markers have identified several clonal lineages which have spread throughout western Europe, suggesting that asexuality was the main reproductive mode of this species during colonization, although occasional sexual reproduction is not excluded. Based on the whole-genome sequences alignment of 46 C. parasitica isolates from France, North America and Asia, genealogy and population structure analyses mostly confirmed these lineages as clonal. However, one of these clonal lineages showed a signal of strong recombination, suggesting different strategies of reproduction in western Europe. Signatures of several recent recombination events within all the French clonal lineages studied here were also identified, indicating that gene flow is regular between these lineages. In addition, haplotype identification of seven French clonal lineages revealed that emergences of new clonal lineages during colonization were the result of hybridization between the main expanding clonal lineages and minor haplotypes non-sequenced in the present study. This whole-genome sequencing study underlines the importance of recombination events in the invasive success of these clonal populations, and suggests that sexual reproduction may be more frequent within and between the western European clonal lineages of C. parasitica than previously assumed using few genetic markers.
    Mots-clés : Bayesian inferences, Clonal evolution, DBG, Intra-haploid mating, MRP, Recombination rates, Whole genome sequencing.

  • E. Dubois, A. De Muyt, J. L. Soyer, K. Budin, M. Legras, T. Piolot, R. Debuchy, N. Kleckner, D. Zickler, et E. Espagne, « Building bridges to move recombination complexes », Proceedings of the National Academy of Sciences of the United States of America, mai 2019.
    Résumé : A central feature of meiosis is pairing of homologous chromosomes, which occurs in two stages: coalignment of axes followed by installation of the synaptonemal complex (SC). Concomitantly, recombination complexes reposition from on-axis association to the SC central region. We show here that, in the fungus Sordaria macrospora, this critical transition is mediated by robust interaxis bridges that contain an axis component (Spo76/Pds5), DNA, plus colocalizing Mer3/Msh4 recombination proteins and the Zip2-Zip4 mediator complex. Mer3-Msh4-Zip2-Zip4 colocalizing foci are first released from their tight axis association, dependent on the SC transverse-filament protein Sme4/Zip1, before moving to bridges and thus to a between-axis position. Ensuing shortening of bridges and accompanying juxtaposition of axes to 100 nm enables installation of SC central elements at sites of between-axis Mer3-Msh4-Zip2-Zip4 complexes. We show also that the Zip2-Zip4 complex has an intrinsic affinity for chromosome axes at early leptotene, where it localizes independently of recombination, but is dependent on Mer3. Then, later, Zip2-Zip4 has an intrinsic affinity for the SC central element, where it ultimately localizes to sites of crossover complexes at the end of pachytene. These and other findings suggest that the fundamental role of Zip2-Zip4 is to mediate the recombination/structure interface at all post-double-strand break stages. We propose that Zip2-Zip4 directly mediates a molecular handoff of Mer3-Msh4 complexes, from association with axis components to association with SC central components, at the bridge stage, and then directly mediates central region installation during SC nucleation.
    Mots-clés : chromosome structure, DBG, interaxis bridges, meiotic recombination, MRP, synaptonemal complex, Zip2-Zip4.

  • P. Grognet, H. Timpano, F. Carlier, J. Aït-Benkhali, V. Berteaux-Lecellier, R. Debuchy, F. Bidard, et F. Malagnac, « A RID-like putative cytosine methyltransferase homologue controls sexual development in the fungus Podospora anserina », PLoS genetics, vol. 15, nᵒ 8, p. e1008086, août 2019.
    Résumé : 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.
    Mots-clés : DBG, EDC, MRP.
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  • B. Le Cam, D. Sargent, J. Gouzy, J. Amselem, M. - N. Bellanger, O. Bouchez, S. Brown, V. Caffier, M. De Gracia Coquerel, R. Debuchy, L. Duvaux, T. Payen, M. Sannier, J. Shiller, J. Collemare, et C. Lemaire, « Population Genome Sequencing of the Scab Fungal Species Venturia inaequalis, Venturiapirina, Venturia aucupariae and Venturia asperata », G3-Genes Genomes Genetics, vol. 9, nᵒ 8, p. 2405-2414, août 2019.
    Résumé : The Venturia genus comprises fungal species that are pathogens on Rosaceae host plants, including V. inaequalis and V. asperata on apple, V. aucupariae on sorbus and V. pirina on pear. Although the genetic structure of V. inaequalis populations has been investigated in detail, genomic features underlying these subdivisions remain poorly understood. Here, we report whole genome sequencing of 87 Venturia strains that represent each species and each population within V. inaequalis We present a PacBio genome assembly for the V. inaequalis EU-B04 reference isolate. The size of selected genomes was determined by flow cytometry, and varied from 45 to 93 Mb. Genome assemblies of V. inaequalis and V. aucupariae contain a high content of transposable elements (TEs), most of which belong to the Gypsy or Copia LTR superfamilies and have been inactivated by Repeat-Induced Point mutations. The reference assembly of V. inaequalis presents a mosaic structure of GC-equilibrated regions that mainly contain predicted genes and AT-rich regions, mainly composed of TEs. Six pairs of strains were identified as clones. Single-Nucleotide Polymorphism (SNP) analysis between these clones revealed a high number of SNPs that are mostly located in AT-rich regions due to misalignments and allowed determining a false discovery rate. The availability of these genome sequences is expected to stimulate genetics and population genomics research of Venturia pathogens. Especially, it will help understanding the evolutionary history of Venturia species that are pathogenic on different hosts, a history that has probably been substantially influenced by TEs.
    Mots-clés : apple, apple scab, DBG, effectors, formae specialis, Fusicladium, MRP, pear, transposable elements, Venturia.

  • A. Mercier, C. Clairet, R. Debuchy, D. Morais, P. Silar, et S. Brun, « The mitochondrial translocase of the inner membrane PaTim54 is involved in defense response and longevity in Podospora anserina », Fungal genetics and biology: FG & B, vol. 132, p. 103257, juill. 2019.
    Résumé : Fungi are very successful microorganisms capable of colonizing virtually any ecological niche where they must constantly cope with competitors including fungi, bacteria and nematodes. We have shown previously that the ascomycete Podopora anserina exhibits Hyphal Interference (HI), an antagonistic response triggered by direct contact of competing fungal hyphae. When challenged with Penicillium chrysogenum, P. anserina produces hydrogen peroxide at the confrontation and kills the hyphae of P. chrysogenum. Here, we report the characterization of the PDC2218 mutant affected in HI. When challenged with P. chrysogenum, the PDC2218 mutant produces a massive oxidative burst at the confrontation. However, this increased production of hydrogen peroxide is not correlated to increased cell death in P. chrysogenum. Hence, the oxidative burst and cell death in the challenger are uncoupled in PDC2218. The gene affected in PDC2218 is PaTim54, encoding the homologue of the budding yeast mitochondrial inner membrane import machinery component Tim54p. We show that PaTim54 is essential in P. anserina and that the phenotypes displayed by the PDC2218 mutant, renamed PaTim542218, are the consequence of a drastic reduction in the expression of PaTim54. Among these pleiotropic phenotypes, PDC2218-PaTim542218- displays increased lifespan, a phenotype in line with the observed mitochondrial defects in the mutant.
    Mots-clés : Aging, DBG, Fungi, Hyphal Interference, Mitochondria, MRP, Podospora anserina, Tim54.

  • P. Silar, J. - M. Dauget, V. Gautier, P. Grognet, M. Chablat, S. Hermann-Le Denmat, A. Couloux, P. Wincker, et R. Debuchy, « A gene graveyard in the genome of the fungus Podospora comata », Molecular Genetics and Genomics, vol. 294, nᵒ 1, p. 177-190, févr. 2019.
    Résumé : Mechanisms involved in fine adaptation of fungi to their environment include differential gene regulation associated with single nucleotide polymorphisms and indels (including transposons), horizontal gene transfer, gene copy amplification, as well as pseudogenization and gene loss. The two Podospora genome sequences examined here emphasize the role of pseudogenization and gene loss, which have rarely been documented in fungi. Podospora comata is a species closely related to Podospora anserina, a fungus used as model in several laboratories. Comparison of the genome of P. comata with that of P. anserina, whose genome is available for over 10 years, should yield interesting data related to the modalities of genome evolution between these two closely related fungal species that thrive in the same types of biotopes, i.e., herbivore dung. Here, we present the genome sequence of the mat+isolate of the P. comata reference strain T. Comparison with the genome of the mat+isolate of P. anserina strain S confirms that P. anserina and P. comata are likely two different species that rarely interbreed in nature. Despite having a 94-99% of nucleotide identity in the syntenic regions of their genomes, the two species differ by nearly 10% of their gene contents. Comparison of the species-specific gene sets uncovered genes that could be responsible for the known physiological differences between the two species. Finally, we identified 428 and 811 pseudogenes (3.8 and 7.2% of the genes) in P. anserina and P. comata, respectively. Presence of high numbers of pseudogenes supports the notion that difference in gene contents is due to gene loss rather than horizontal gene transfers. We propose that the high frequency of pseudogenization leading to gene loss in P. anserina and P. comata accompanies specialization of these two fungi. Gene loss may be more prevalent during the evolution of other fungi than usually thought.
    Mots-clés : anserina, BIOCELL, biodiversity, DBG, DSMC, EDC, FDMITO, Lasiosphaeriaceae, MRP, neanderthal, Podospora anserina, Podospora comata, Pseudogene, pseudogenes, sequence, Sordariales, Speciation.

  • S. Wang, C. Veller, F. Sun, A. Ruiz-Herrera, Y. Shang, H. Liu, D. Zickler, Z. Chen, N. Kleckner, et L. Zhang, « Per-Nucleus Crossover Covariation and Implications for Evolution », Cell, vol. 177, nᵒ 2, p. 326-+, avr. 2019.
    Résumé : Crossing over is a nearly universal feature of sexual reproduction. Here, analysis of crossover numbers on a per-chromosome and per-nucleus basis reveals a fundamental, evolutionarily conserved feature of meiosis: within individual nuclei, crossover frequencies covary across different chromosomes. This effect results from per-nucleus covariation of chromosome axis lengths. Crossovers can promote evolutionary adaptation. However, the benefit of creating favorable new allelic combinations must outweigh the cost of disrupting existing favorable combinations. Covariation concomitantly increases the frequencies of gametes with especially high, or especially low, numbers of crossovers, and thus might concomitantly enhance the benefits of crossing over while reducing its costs. A four-locus population genetic model suggests that such an effect can pertain in situations where the environment fluctuates: hyper-crossover gametes are advantageous when the environment changes while hypo-crossover gametes are advantageous in periods of environmental stasis. These findings reveal a new feature of the basic meiotic program and suggest a possible adaptive advantage.
    Mots-clés : adaptation, advantage, aneuploidy, chromosome axis legngth, chromosome loops, cohesin smc1-beta, crossover, crossover covariation, crossover variance, DBG, evolution of recombination, evolution of sex, frequency, genome-wide recombination rate, individual chromosomes, interference, meiosis, MRP, protein, recombination, sex.

2018


  • V. Gautier, L. C. H. Tong, T. - S. Nguyen, R. Debuchy, et P. Silar, « PaPro1 and IDC4, Two Genes Controlling Stationary Phase, Sexual Development and Cell Degeneration in Podospora anserina », Journal of Fungi, vol. 4, nᵒ 3, p. UNSP 85, sept. 2018.
    Résumé : Filamentous fungi frequently undergo bistable phenotypic switches. Crippled Growth of Podospora anserina is one such bistable switch, which seems to rely upon the mis-activation of a self-regulated PaMpk1 MAP kinase regulatory pathway. Here, we identify two new partners of this pathway: PaPro1, a transcription factor orthologous to Sordaria macrospora pro1 and Neurospora crassa ADV-1, and IDC4, a protein with an AIM24 domain. Both PaPro1 and IDC4 regulate stationary phase features, as described for the other actors of the PaMpk1 signaling pathway. However, PaPro1 is also involved in the control of fertilization by activating the transcription of the HMG8 and the mating type transcription factors, as well as the sexual pheromones and receptor genes. The roles of two components of the STRIPAK complex were also investigated by inactivating their encoding genes: PaPro22 and PaPro45. The mutants of these genes were found to have the same phenotypes as PaPro1 and IDC4 mutants as well as additional phenotypes including slow growth, abnormally shaped hyphae, pigment accumulation and blockage of the zygotic tissue development, indicating that the STRIPAK complex regulates, in addition to the PaMpk1 one, other pathways in P. anserina. Overall, the mutants of these four genes confirm the model by which Crippled Growth is due to the abnormal activation of the PaMpk1 MAP kinase cascade.
    Mots-clés : DBG, developmental mutants, developmental mutants, differentiation, DSMC, fungal development, fusion, identification, kinase, maintenance, MRP, multicellular fruiting bodies, perithecium, Podospora anserina, pro1, real-time pcr, reproduction, sordaria-macrospora, tool.

2017


  • S. Tessé, H. - M. Bourbon, R. Debuchy, K. Budin, E. Dubois, Z. Liangran, R. Antoine, T. Piolot, N. Kleckner, D. Zickler, et E. Espagne, « Asy2/Mer2: an evolutionarily conserved mediator of meiotic recombination, pairing, and global chromosome compaction », Genes & Development, oct. 2017.
    Résumé : Meiosis is the cellular program by which a diploid cell gives rise to haploid gametes for sexual reproduction. Meiotic progression depends on tight physical and functional coupling of recombination steps at the DNA level with specific organizational features of meiotic-prophase chromosomes. The present study reveals that every step of this coupling is mediated by a single molecule: Asy2/Mer2. We show that Mer2, identified so far only in budding and fission yeasts, is in fact evolutionarily conserved from fungi (Mer2/Rec15/Asy2/Bad42) to plants (PRD3/PAIR1) and mammals (IHO1). In yeasts, Mer2 mediates assembly of recombination-initiation complexes and double-strand breaks (DSBs). This role is conserved in the fungus Sordaria However, functional analysis of 13 mer2 mutants and successive localization of Mer2 to axis, synaptonemal complex (SC), and chromatin revealed, in addition, three further important functions. First, after DSB formation, Mer2 is required for pairing by mediating homolog spatial juxtaposition, with implications for crossover (CO) patterning/interference. Second, Mer2 participates in the transfer/maintenance and release of recombination complexes to/from the SC central region. Third, after completion of recombination, potentially dependent on SUMOylation, Mer2 mediates global chromosome compaction and post-recombination chiasma development. Thus, beyond its role as a recombinosome-axis/SC linker molecule, Mer2 has important functions in relation to basic chromosome structure.
    Mots-clés : chromatin compaction SUMOylation, DBG, DSMC, Meiosis, Mer2, MRP, Pairing, Recombination, Sordaria.

  • S. Wang, T. Hassold, P. Hunt, M. A. White, D. Zickler, N. Kleckner, et L. Zhang, « Inefficient Crossover Maturation Underlies Elevated Aneuploidy in Human Female Meiosis », Cell, vol. 168, nᵒ 6, p. 977-989.e17, mars 2017.
    Résumé : Meiosis is the cellular program that underlies gamete formation. For this program, crossovers between homologous chromosomes play an essential mechanical role to ensure regular segregation. We present a detailed study of crossover formation in human male and female meiosis, enabled by modeling analysis. Results suggest that recombination in the two sexes proceeds analogously and efficiently through most stages. However, specifically in female (but not male), ∼25% of the intermediates that should mature into crossover products actually fail to do so. Further, this "female-specific crossover maturation inefficiency" is inferred to make major contributions to the high level of chromosome mis-segregation and resultant aneuploidy that uniquely afflicts human female oocytes (e.g., giving Down syndrome). Additionally, crossover levels on different chromosomes in the same nucleus tend to co-vary, an effect attributable to global per-nucleus modulation of chromatin loop size. Maturation inefficiency could potentially reflect an evolutionary advantage of increased aneuploidy for human females.
    Mots-clés : DBG, DSMC, MRP.

  • N. Xie, G. Ruprich-Robert, F. Chapeland-Leclerc, E. Coppin, H. Lalucque, S. Brun, R. Debuchy, et P. Silar, « Inositol-phosphate signaling as mediator for growth and sexual reproduction in Podospora anserina », Developmental Biology, juin 2017.
    Résumé : The molecular pathways involved in the development of multicellular fruiting bodies in fungi are still not well known. Especially, the interplay between the mycelium, the female tissues and the zygotic tissues of the fruiting bodies is poorly documented. Here, we describe PM154, a new strain of the model ascomycetes Podospora anserina able to mate with itself and that enabled the easy recovery of new mutants affected in fruiting body development. By complete genome sequencing of spod1, one of the new mutants, we identified an inositol phosphate polykinase gene as essential, especially for fruiting body development. A factor present in the wild type and diffusible in mutant hyphae was able to induce the development of the maternal tissues of the fruiting body in spod1, but failed to promote complete development of the zygotic ones. Addition of myo-inositol in the growth medium was able to increase the number of developing fruiting bodies in the wild type, but not in spod1. Overall, the data indicated that inositol and inositol polyphosphates were involved in promoting fruiting body maturation, but also in regulating the number of fruiting bodies that developed after fertilization. The same effect of inositol was seen in two other fungi, Sordaria macrospora and Chaetomium globosum. Key role of the inositol polyphosphate pathway during fruiting body maturation appears thus conserved during the evolution of Sordariales fungi.
    Mots-clés : DBG, Developmental mutants, DSMC, Fungal development, Inositol, Inositol kinase, MRP, Multicellular fruiting bodies, Perithecium, Podospora anserina.

2016


  • K. Bomblies, G. Jones, C. Franklin, D. Zickler, et N. Kleckner, « The challenge of evolving stable polyploidy: could an increase in "crossover interference distance" play a central role? », Chromosoma, vol. 125, nᵒ 2, p. 287-300, juin 2016.
    Résumé : Whole genome duplication is a prominent feature of many highly evolved organisms, especially plants. When duplications occur within species, they yield genomes comprising multiple identical or very similar copies of each chromosome ("autopolyploids"). Such genomes face special challenges during meiosis, the specialized cellular program that underlies gamete formation for sexual reproduction. Comparisons between newly formed (neo)-autotetraploids and fully evolved autotetraploids suggest that these challenges are solved by specific restrictions on the positions of crossover recombination events and, thus, the positions of chiasmata, which govern the segregation of homologs at the first meiotic division. We propose that a critical feature in the evolution of these more effective chiasma patterns is an increase in the effective distance of meiotic crossover interference, which plays a central role in crossover positioning. We discuss the findings in several organisms, including the recent identification of relevant genes in Arabidopsis arenosa, that support this hypothesis.
    Mots-clés : Chiasmata, Chromosomes, Plant, Crossing Over, Genetic, Crossover interference, DBG, DSMC, Evolution, Molecular, Homologous chromosomes, Meiosis, MRP, plants, Polyploidy, Recombination.

  • H. Takano-Rojas, D. Zickler, et L. Peraza-Reyes, « Peroxisome dynamics during development of the fungus Podospora anserina », Mycologia, vol. 108, nᵒ 3, p. 590-602, juin 2016.
    Résumé : Peroxisomes are versatile and dynamic organelles that are required for the development of diverse eukaryotic organisms. We demonstrated previously that in the fungus Podospora anserina different peroxisomal functions are required at distinct stages of sexual development, including the initiation and progression of meiocyte (ascus) development and the differentiation and germination of sexual spores (ascospores). Peroxisome assembly during these processes relies on the differential activity of the protein machinery that drives the import of proteins into the organelle, indicating a complex developmental regulation of peroxisome formation and activity. Here we demonstrate that peroxisome dynamics is also highly regulated during development. We show that peroxisomes in P. anserina are highly dynamic and respond to metabolic and environmental cues by undergoing changes in size, morphology and number. In addition, peroxisomes of vegetative and sexual cell types are structurally different. During sexual development peroxisome number increases at two stages: at early ascus differentiation and during ascospore formation. These processes are accompanied by changes in peroxisome structure and distribution, which include a cell-polarized concentration of peroxisomes at the beginning of ascus development, as well as a morphological transition from predominantly spherical to elongated shapes at the end of the first meiotic division. Further, the mostly tubular peroxisomes present from second meiotic division to early ascospore formation again become rounded during ascospore differentiation. Ultimately the number of peroxisomes dramatically decreases upon ascospore maturation. Our results reveal a precise regulation of peroxisome dynamics during sexual development and suggest that peroxisome constitution and function during development is defined by the coordinated regulation of the proteins that control peroxisome assembly and dynamics.
    Mots-clés : Cell Differentiation, DBG, DSMC, Fungal Proteins, Fungi, Gene Expression Regulation, Developmental, Gene Expression Regulation, Fungal, Genes, Mating Type, Fungal, Meiosis, MRP, peroxisome dynamics, Peroxisomes, Podospora, sexual development, Spores, Fungal.


  • P. S. Dyer, P. Inderbitzin, et Debuchy, Robert, « 14 Mating-Type Structure, Function, Regulation and Evolution in the Pezizomycotina », in Growth, Differentiation and Sexuality, J. Wendland, Éd. Cham: Springer International Publishing, 2016, p. 351-385.

  • D. Zickler et E. Espagne, « Sordaria, a model system to uncover links between meiotic pairing and recombination », Seminars in Cell & Developmental Biology, vol. 54, p. 149-157, juin 2016.
    Résumé : The mycelial fungus Sordaria macrospora was first used as experimental system for meiotic recombination. This review shows that it provides also a powerful cytological system for dissecting chromosome dynamics in wild-type and mutant meioses. Fundamental cytogenetic findings include: (1) the identification of presynaptic alignment as a key step in pairing of homologous chromosomes. (2) The discovery that biochemical complexes that mediate recombination at the DNA level concomitantly mediate pairing of homologs. (3) This pairing process involves not only resolution but also avoidance of chromosomal entanglements and the resolution system includes dissolution of constraining DNA recombination interactions, achieved by a unique role of Mlh1. (4) Discovery that the central components of the synaptonemal complex directly mediate the re-localization of the recombination proteins from on-axis to in-between homologue axis positions. (5) Identification of putative STUbL protein Hei10 as a structure-based signal transduction molecule that coordinates progression and differentiation of recombinational interactions at multiple stages. (6) Discovery that a single interference process mediates both nucleation of the SC and designation of crossover sites, thereby ensuring even spacing of both features. (7) Discovery of local modulation of sister-chromatid cohesion at sites of crossover recombination.
    Mots-clés : Bouquet, DBG, DSMC, Meiotic recombination, MRP, Pairing, Sordaria, Synaptonemal Complex.


  • D. Zickler et N. Kleckner, « A few of our favorite things: Pairing, the bouquet, crossover interference and evolution of meiosis », Seminars in Cell & Developmental Biology, vol. 54, p. 135-148, 2016.
    Mots-clés : Bouquet, Crossover interference, DBG, DSMC, Meiosis, MRP, Pairing.

2015


  • Z. Liang, D. Zickler, M. Prentiss, F. S. Chang, G. Witz, K. Maeshima, et N. Kleckner, « Chromosomes Progress to Metaphase in Multiple Discrete Steps via Global Compaction/Expansion Cycles », Cell, vol. 161, nᵒ 5, p. 1124-1137, mai 2015.
    Résumé : Mammalian mitotic chromosome morphogenesis was analyzed by 4D live-cell and snapshot deconvolution fluorescence imaging. Prophase chromosomes, whose organization was previously unknown, are revealed to comprise co-oriented sister linear loop arrays displayed along a single, peripheral, regularly kinked topoisomerase II/cohesin/condensin II axis. Thereafter, rather than smooth, progressive compaction as generally envisioned, progression to metaphase is a discontinuous process involving chromosome expansion as well as compaction. At late prophase, dependent on topoisomerase II and with concomitant cohesin release, chromosomes expand, axes split and straighten, and chromatin loops transit to a radial disposition around now-central axes. Finally, chromosomes globally compact, giving the metaphase state. These patterns are consistent with the hypothesis that the molecular events of chromosome morphogenesis are governed by accumulation and release of chromosome stress, created by chromatin compaction and expansion. Chromosome state could evolve analogously throughout the cell cycle.
    Mots-clés : Adenosine Triphosphatases, Animals, Cell Cycle Proteins, Cell Line, Chromosomal Proteins, Non-Histone, Chromosomes, Mammalian, DBG, Deer, DNA Topoisomerases, Type II, DNA-Binding Proteins, DSMC, HeLa Cells, Humans, Metaphase, Microscopy, Fluorescence, Mitosis, MRP, Multiprotein Complexes, Swine.

  • J. Ropars, R. C. Rodríguez de la Vega, M. López-Villavicencio, J. Gouzy, E. Sallet, É. Dumas, S. Lacoste, R. Debuchy, J. Dupont, A. Branca, et T. Giraud, « Adaptive Horizontal Gene Transfers between Multiple Cheese-Associated Fungi », Current biology: CB, vol. 25, nᵒ 19, p. 2562-2569, oct. 2015.
    Résumé : Domestication is an excellent model for studies of adaptation because it involves recent and strong selection on a few, identified traits [1-5]. Few studies have focused on the domestication of fungi, with notable exceptions [6-11], despite their importance to bioindustry [12] and to a general understanding of adaptation in eukaryotes [5]. Penicillium fungi are ubiquitous molds among which two distantly related species have been independently selected for cheese making-P. roqueforti for blue cheeses like Roquefort and P. camemberti for soft cheeses like Camembert. The selected traits include morphology, aromatic profile, lipolytic and proteolytic activities, and ability to grow at low temperatures, in a matrix containing bacterial and fungal competitors [13-15]. By comparing the genomes of ten Penicillium species, we show that adaptation to cheese was associated with multiple recent horizontal transfers of large genomic regions carrying crucial metabolic genes. We identified seven horizontally transferred regions (HTRs) spanning more than 10 kb each, flanked by specific transposable elements, and displaying nearly 100% identity between distant Penicillium species. Two HTRs carried genes with functions involved in the utilization of cheese nutrients or competition and were found nearly identical in multiple strains and species of cheese-associated Penicillium fungi, indicating recent selective sweeps; they were experimentally associated with faster growth and greater competitiveness on cheese and contained genes highly expressed in the early stage of cheese maturation. These findings have industrial and food safety implications and improve our understanding of the processes of adaptation to rapid environmental changes.
    Mots-clés : Adaptation, Biological, Cheese, CheesyTer, convergence, DBG, DNA, Fungal, DSMC, Food Microbiology, food spoiler, Fungi, gene expression, Gene Transfer, Horizontal, HGT, MRP, parallel adaptation, Penicillium, Phenotype, Wallaby.


  • S. Wang, D. Zickler, N. Kleckner, et L. Zhang, « Meiotic crossover patterns: Obligatory crossover, interference and homeostasis in a single process », Cell Cycle, vol. 14, nᵒ 3, p. 305-314, 2015.

  • D. Zickler et N. Kleckner, « Recombination, Pairing, and Synapsis of Homologs during Meiosis », Cold Spring Harbor Perspectives in Biology, vol. 7, nᵒ 6, mai 2015.
    Résumé : Recombination is a prominent feature of meiosis in which it plays an important role in increasing genetic diversity during inheritance. Additionally, in most organisms, recombination also plays mechanical roles in chromosomal processes, most notably to mediate pairing of homologous chromosomes during prophase and, ultimately, to ensure regular segregation of homologous chromosomes when they separate at the first meiotic division. Recombinational interactions are also subject to important spatial patterning at both early and late stages. Recombination-mediated processes occur in physical and functional linkage with meiotic axial chromosome structure, with interplay in both directions, before, during, and after formation and dissolution of the synaptonemal complex (SC), a highly conserved meiosis-specific structure that links homolog axes along their lengths. These diverse processes also are integrated with recombination-independent interactions between homologous chromosomes, nonhomology-based chromosome couplings/clusterings, and diverse types of chromosome movement. This review provides an overview of these diverse processes and their interrelationships.
    Mots-clés : Animals, Chromosome Pairing, Chromosomes, DBG, DNA Breaks, Double-Stranded, DSMC, Humans, Meiosis, MRP, Recombination, Genetic, Synaptonemal Complex.
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Publications Principales avant 2015

- Zhang L, Espagne E, de Muyt A, Zickler D and Kleckner NE (2014) Interference-mediated synaptonemal complex formation with embedded crossover designation. Proc Natl Acad Sci U S A. 111:E5059-68.

- Vasnier C, de Muyt A, Zhang L, Tessé S, Kleckner NE, Zickler D and Espagne E (2014) Absence of SUN-domain protein Slp1 blocks karyogamy and switches meiotic recombination and synapsis from homologs to sister chromatids. Proc Natl Acad Sci U S A.111:E4015-23.

- De Muyt A, Zhang L, Piolot T, Kleckner N, Espagne E and Zickler D (2014) E3 ligase Hei10 : a multifaceted structure-based signaling molecule with roles within and beyond meiosis. Genes Dev. 28:1111-23.

- Grognet P, Bidard F, Kuchly C, Tong LC, Coppin E, Benkhali JA, Couloux A, Wincker P, Debuchy R and Silar P (2014) Maintaining two mating types : structure of the mating type locus and its role in heterokaryosis in Podospora anserina. Genetics. 197(1):421-32. doi : 10.1534/genetics.113.159988.

- Cheeseman K, Ropars J, Renault P, Dupont J, Gouzy J, Branca A, Abraham AL, Ceppi M, Conseiller E, Debuchy R, Malagnac F, Goarin A, Silar P, Lacoste S, Sallet E, Bensimon A, Giraud T and Brygoo Y (2014) Multiple recent horizontal transfers of a large genomic region in cheese making fungi. Nat Commun.5:2876.doi : 10.1038/ncomms3876.

- Kleckner N, Zickler D and Witz G (2013) Molecular biology. Chromosome capture brings it all together. Science 342:940-941.

- Ait Benkhali J, Coppin E, Brun S, Peraza-Reyes L, Martin T, Dixelius C, Lazar N, van Tilbeurgh H and Debuchy R (2013) A network of HMG-box transcription factors regulates sexual cycle in the fungus Podospora anserina. PLoS Genet. 9 : e1003642.

- Espagne E, Vasnier C, Storlazzi A, Kleckner N, Silar P, Zickler D and Malagnac F (2011) Sme4 coiled-coil protein mediates synaptonemal complex assembly, recombinosomerelocalization and spindle pole body morphogenesis. Proc Natl Acad Sci U S A. 26 : 10614-10619.

- Kleckner N, Zhang L, Weiner B and Zickler D (2011) Meiotic chromosome dynamics.Chapter 19 in « Genome Organization », pp1-82, ed. Rippe, John Wiley-VCH Verlag, Mannheim.

- Storlazzi A, Gargano S, Ruprich-Robert G, Falque M, David M, Kleckner N and Zickler D (2010) Recombination proteins mediate meiotic spatial chromosome organization and pairing, Cell 141(1) : 94-106.

- Nowrousian M, Stajich JE, Chu M, Engh I, Espagne E, Halliday K, Kamerewerd J, Kempken F, Knab B, Kuo HC, Osiewacz HD, Pöggeler S, Read ND, Seiler S, Smith KM, Zickler D, Kück U and Freitag M (2010) De novo assembly of a 40 Mb eukaryotic genome from short sequence reads : Sordaria macrospora, a model organism for fungal morphogenesis, PLoS Genet. 6:e1000891.

- Zickler D (2009) Observing meiosis in filamentous fungi :Sordaria and Neurospora, Methods Mol Biol. 558, 91-114, S. Keeney ed. The Human Press Inc. Totowa, New Jersey, USA.

- Storlazzi A, Tesse S, Ruprich-Robert G, Gargano S, Poggeler S, Kleckner N and Zickler D (2008) Coupling meiotic chromosome axis integrity to recombination, Genes Dev. 22 : 796-809.

- Espagne E, Lespinet O, Malagnac F et al (2008) The genome sequence of the model ascomycete fungus Podospora anserina.Genome Biol. 9:R77.

- Zickler D (2006) From early homologue recognition to synaptonemal complex formation, Chromosoma 115:158-174.

- Shiu PK, Zickler D, Raju NB, Ruprich-Robert G and Metzenberg RL (2006) SAD-2 is required for meiotic silencing by unpaired DNA and perinuclear localization of SAD-1 RNA-directed RNA polymerase, Proc Natl Acad Sci U S A. 103 : 2243-2248.

- Zickler D (2006) Meiosis in mycelialfungi. pp 415-438. The Mycota I. Growth, differentiation and sexuality. U. Kües and R. Fischer eds. Springer -Verlag Berlin Heidelberg.

- Kleckner, Zickler D, Jones GH, Henle J, Dekker J and Hutchinson J (2004) A mechanical basis for chromosome function, Proc Natl Acad Sci U S A.101 : 12592-12597.

- Bishop DK and Zickler D (2004) Meiotic crossover interference prior to stable strand exchange and synapsis, Cell 117:9-15.

- Storlazzi A, Tesse S, Gargano S, James F, Kleckner N and Zickler D (2003) Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division. Genes Dev. 17:2675–2687.

- Kleckner N, Storlazzi A and Zickler D (2003) Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length. Trends Genet. 19(11):623-628.

- Storlazzi A, Tessé S, Gargano S, James F, Kleckner N and Zickler D (2003) Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division. Genes Dev. 17, 2675-2687.

- Tessé S, Storlazzi A, Kleckner N, Gargano S and Zickler D (2003) Localization and roles of Ski8p protein in Sordaria meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition. Proc Natl Acad Sci U S A. 100, 12865-12870.

- van Heemst D, Kafer E, John T, Heyting C, van Aalderen M and Zickler D (2001) BimD/SPO76 is at the interface of cell cycle progression, chromosome morphogenesis, and recombination. Proc Natl Acad Sci U S A. 98, 6267-6272.

- van Heemst D, James F, Pöggeler S, Berteaux-Lecellier V and Zickler D (1999) Spo76p is a conserved chromosome morphogenesis protein that links the mitotic and meiotic programs. Cell 98, 261-271.

- Zickler D and Kleckner N (1999) Meiotic chromosomes : integrating structure and function. Annu. Rev. Genet. 33, 603-754.

- Zickler D and Kleckner N (1998) The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32, 619-697.

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