Stepwise recombination suppression around the mating-type locus in an ascomycete fungus with self-fertile spores

Vittorelli, Nina; Rodríguez de la Vega, Ricardo C.; Snirc, Alodie; Levert, Emilie; Gautier, Valérie; Lalanne, Christophe; De Filippo, Elsa; Gladieux, Pierre; Guillou, Sonia; Zhang, Yu; Tejomurthula, Sravanthi; Grigoriev, Igor V.; Debuchy, Robert; Silar, Philippe; Giraud, Tatiana; Hartmann, Fanny E.

doi:10.1371/journal.pgen.1010347

Title: Stepwise recombination suppression around the mating-type locus in an ascomycete fungus with self-fertile spores

Journal Article · Fri Feb 10 00:00:00 EST 2023 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1010347· OSTI ID:2234196

Vittorelli, Nina ^[1]; Rodríguez de la Vega, Ricardo C. ^[2]; Snirc, Alodie ^[2]; Levert, Emilie ^[3]; Gautier, Valérie ^[4]; Lalanne, Christophe ^[4]; De Filippo, Elsa ^[3];

^[5]; Guillou, Sonia ^[5];

^[6]; Tejomurthula, Sravanthi ^[6]; Grigoriev, Igor V. ^[7];

^[8]; Silar, Philippe ^[4]; Giraud, Tatiana ^[2]; Hartmann, Fanny E. ^[2]

CNRS, Université Paris-Saclay, AgroParisTech, Gif-sur-Yvette (France). Ecologie Systematique et Evolution (ESE); Université Paris Cité (France). Laboratoire Interdisciplinaire des Energies de Demain; Département de Biologie, École Normale Supérieure, PSL Université Paris (France)
CNRS, Université Paris-Saclay, AgroParisTech, Gif-sur-Yvette (France). Ecologie Systematique et Evolution (ESE)
CNRS, Université Paris-Saclay, AgroParisTech, Gif-sur-Yvette (France). Ecologie Systematique et Evolution (ESE); Université Paris Cité (France). Laboratoire Interdisciplinaire des Energies de Demain
Université Paris Cité (France). Laboratoire Interdisciplinaire des Energies de Demain
PHIM Plant Health Institute, Université de Montpellier, INRAE, CIRAD, Institut Agro, IRD (France)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). USDOE Joint BioEnergy Institute
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). USDOE Joint BioEnergy Institute; University of California Berkeley, CA (United States)
Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Gif-sur-Yvette (France)

Recombination is often suppressed at sex-determining loci in plants and animals, and at self-incompatibility or mating-type loci in plants and fungi. In fungal ascomycetes, recombination suppression around the mating-type locus is associated with pseudo-homothallism, i.e. the production of self-fertile dikaryotic sexual spores carrying the two opposite mating types. This has been well studied in two species complexes from different families of Sordariales: Podospora anserina and Neurospora tetrasperma. However, it is unclear whether this intriguing association holds in other species. We show here that Schizothecium tetrasporum, a fungus from a third family in the order Sordariales, also produces mostly self-fertile dikaryotic spores carrying the two opposite mating types. This was due to a high frequency of second meiotic division segregation at the mating-type locus, indicating the occurrence of a single and systematic crossing-over event between the mating-type locus and the centromere, as in P. anserina. The mating-type locus has the typical Sordariales organization, plus a MAT1-1-1 pseudogene in the MAT1-2 haplotype. High-quality genome assemblies of opposite mating types and segregation analyses revealed a suppression of recombination in a region of 1.47 Mb around the mating-type locus. We detected three evolutionary strata, indicating a stepwise extension of recombination suppression. The three strata displayed no rearrangement or transposable element accumulation but gene losses and gene disruptions were present, and precisely at the strata margins. Our findings indicate a convergent evolution of self-fertile dikaryotic sexual spores across multiple ascomycete fungi. The particular pattern of meiotic segregation at the mating-type locus was associated with recombination suppression around this locus, that had extended stepwise. This association between pseudo-homothallism and recombination suppression across lineages and the presence of gene disruption at the strata limits are consistent with a recently proposed mechanism of sheltering deleterious alleles to explain stepwise recombination suppression.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); European Research Council (ERC)

Grant/Contract Number:: AC02-05CH11231; ANR-20-IDEES-0002; 504394; 832352

OSTI ID:: 2234196

Journal Information:: PLoS Genetics, Vol. 19, Issue 2; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (114)

Temporal changes in pathogen diversity in a perennial plant–pathogen–hyperparasite system Stauber, Lea; Croll, Daniel; Prospero, Simone Molecular Ecology, Vol. 31, Issue 7 https://doi.org/10.1111/mec.16386	journal	February 2022
QUAST: quality assessment tool for genome assemblies Gurevich, Alexey; Saveliev, Vladislav; Vyahhi, Nikolay Bioinformatics, Vol. 29, Issue 8 https://doi.org/10.1093/bioinformatics/btt086	journal	February 2013
Maintaining Two Mating Types: Structure of the Mating Type Locus and Its Role in Heterokaryosis in Podospora anserina Grognet, Pierre; Bidard, Frédérique; Kuchly, Claire Genetics, Vol. 197, Issue 1 https://doi.org/10.1534/genetics.113.159988	journal	May 2014
Genetic Mapping of Magnaporthe grisea Avirulence Gene Corresponding to Leaf and Panicle Blast Resistant QTLs in Jao Hom Nin Rice Cultivar Sreewongchai, Tanee; Sriprakhon, Siangchai; Wongsaprom, Chankarn Journal of Phytopathology, Vol. 157, Issue 6 https://doi.org/10.1111/j.1439-0434.2008.01495.x	journal	May 2009
Suppression of crossing-over by DNA methylation in Ascobolus Maloisel, L.; Rossignol, J. -L. Genes & Development, Vol. 12, Issue 9 https://doi.org/10.1101/gad.12.9.1381	journal	May 1998
A new technique for using spermatia in the production of mutants in Podospora Esser, Karl; Prillinger, Hansjörg Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 16, Issue 4 https://doi.org/10.1016/0027-5107(72)90211-4	journal	December 1972
The genome sequence of the model ascomycete fungus Podospora anserina Espagne, Eric; Lespinet, Olivier; Malagnac, Fabienne Genome Biology, Vol. 9, Issue 5 https://doi.org/10.1186/gb-2008-9-5-r77	journal	January 2008
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations Charlesworth, Deborah Evolutionary Applications, Vol. 9, Issue 1 https://doi.org/10.1111/eva.12291	journal	August 2015
Allorecognition genes drive reproductive isolation in Podospora anserina Ament-Velásquez, S. Lorena; Vogan, Aaron A.; Granger-Farbos, Alexandra Nature Ecology & Evolution, Vol. 6, Issue 7 https://doi.org/10.1038/s41559-022-01734-x	journal	May 2022
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Size Variation of the Nonrecombining Region on the Mating-Type Chromosomes in the Fungal Podospora anserina Species Complex Hartmann, Fanny E.; Ament-Velásquez, Sandra Lorena; Vogan, Aaron A. Molecular Biology and Evolution, Vol. 38, Issue 6 https://doi.org/10.1093/molbev/msab040	journal	February 2021
Molecular Genetics of Mating Recognition in Basidiomycete Fungi Casselton, Lorna A.; Olesnicky, Natalie S. Microbiology and Molecular Biology Reviews, Vol. 62, Issue 1 https://doi.org/10.1128/MMBR.62.1.55-70.1998	journal	March 1998
A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi Hane, James K.; Rouxel, Thierry; Howlett, Barbara J. Genome Biology, Vol. 12, Issue 5 https://doi.org/10.1186/gb-2011-12-5-r45	journal	January 2011
pycoQC, interactive quality control for Oxford Nanopore Sequencing Leger, Adrien; Leonardi, Tommaso Journal of Open Source Software, Vol. 4, Issue 34 https://doi.org/10.21105/joss.01236	journal	February 2019
BUSCO: Assessing Genomic Data Quality and Beyond Manni, Mosè; Berkeley, Matthew R.; Seppey, Mathieu Current Protocols, Vol. 1, Issue 12 https://doi.org/10.1002/cpz1.323	journal	December 2021
Tracing the Origin of the Fungal α1 Domain Places Its Ancestor in the HMG-Box Superfamily: Implication for Fungal Mating-Type Evolution Martin, Tom; Lu, Shun-Wen; van Tilbeurgh, Herman PLoS ONE, Vol. 5, Issue 12 https://doi.org/10.1371/journal.pone.0015199	journal	December 2010
Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes Hartmann, Fanny E.; Duhamel, Marine; Carpentier, Fantin New Phytologist, Vol. 229, Issue 5 https://doi.org/10.1111/nph.17039	journal	December 2020
Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom Agaricus bisporus Foulongne-Oriol, Marie; Taskent, Ozgur; Kües, Ursula Genes, Vol. 12, Issue 7 https://doi.org/10.3390/genes12071079	journal	July 2021
Species Delimitation in thePodospora anserina/ p. pauciseta/p. comataSpecies Complex (Sordariales) Boucher, Charlie; Nguyen, Tinh-Suong; Silar, Philippe Cryptogamie, Mycologie, Vol. 38, Issue 4 https://doi.org/10.7872/crym/v38.iss4.2017.485	journal	December 2017
Little Evidence of Antagonistic Selection in the Evolutionary Strata of Fungal Mating-Type Chromosomes (Microbotryum lychnidis-dioicae) Bazzicalupo, Anna Liza; Carpentier, Fantin; Otto, Sarah Perin G3 Genes\|Genomes\|Genetics, Vol. 9, Issue 6 https://doi.org/10.1534/g3.119.400242	journal	June 2019
Mating-type heterokaryosis and selfing in Cryphonectria parasitica McGuire, I. Cristina; Marra, Robert E.; Milgroom, Michael G. Fungal Genetics and Biology, Vol. 41, Issue 5 https://doi.org/10.1016/j.fgb.2003.12.007	journal	May 2004
Contrasted patterns in mating-type chromosomes in fungi: Hotspots versus coldspots of recombination Idnurm, Alexander; Hood, Michael E.; Johannesson, Hanna Fungal Biology Reviews, Vol. 29, Issue 3-4 https://doi.org/10.1016/j.fbr.2015.06.001	journal	December 2015
Increased longevity of EF-1α high-fidelity mutants in Podospora anserina Silar, Philippe; Picard, Marguerite Journal of Molecular Biology, Vol. 235, Issue 1 https://doi.org/10.1016/S0022-2836(05)80029-4	journal	January 1994
InterProScan 5: genome-scale protein function classification Jones, P.; Binns, D.; Chang, H. -Y. Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu031	journal	January 2014
Sheltering of deleterious mutations explains the stepwise extension of recombination suppression on sex chromosomes and other supergenes Jay, Paul; Tezenas, Emilie; Véber, Amandine PLOS Biology, Vol. 20, Issue 7 https://doi.org/10.1371/journal.pbio.3001698	journal	July 2022
Markers linked to vegetative incompatibility (vic) genes and a region of high heterogeneity and reduced recombination near the mating type locus (MAT) in Cryphonectria parasitica Kubisiak, Thomas L.; Milgroom, Michael G. Fungal Genetics and Biology, Vol. 43, Issue 6 https://doi.org/10.1016/j.fgb.2006.02.002	journal	June 2006
ami1, an Orthologue of the Aspergillus nidulans apsA Gene, Is Involved in Nuclear Migration Events Throughout the Life Cycle of Podospora anserina Graïa, Fatima; Berteaux-Lecellier, Véronique; Zickler, Denise Genetics, Vol. 155, Issue 2 https://doi.org/10.1093/genetics/155.2.633	journal	June 2000
The Enterprise, a massive transposon carrying Spok meiotic drive genes Vogan, Aaron A.; Ament-Velásquez, S. Lorena; Bastiaans, Eric Genome Research, Vol. 31, Issue 5 https://doi.org/10.1101/gr.267609.120	journal	April 2021
MUMmer4: A fast and versatile genome alignment system Marçais, Guillaume; Delcher, Arthur L.; Phillippy, Adam M. PLOS Computational Biology, Vol. 14, Issue 1 https://doi.org/10.1371/journal.pcbi.1005944	journal	January 2018
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
A global multilocus analysis of the model fungus Neurospora reveals a single recent origin of a novel genetic system Corcoran, Pádraic; Dettman, Jeremy R.; Sun, Yu Molecular Phylogenetics and Evolution, Vol. 78 https://doi.org/10.1016/j.ympev.2014.05.007	journal	September 2014
Complete genetic linkage maps from an interspecific cross between Fusarium circinatum and Fusarium subglutinans De Vos, L.; Myburg, A. A.; Wingfield, M. J. Fungal Genetics and Biology, Vol. 44, Issue 8 https://doi.org/10.1016/j.fgb.2007.02.007	journal	August 2007
The effect of linkage on limits to artificial selection Hill, W. G.; Robertson, Alan Genetical Research, Vol. 8, Issue 3 https://doi.org/10.1017/S0016672300010156	journal	December 1966
The RIPper, a web-based tool for genome-wide quantification of Repeat-Induced Point (RIP) mutations van Wyk, Stephanie; Harrison, Christopher H.; Wingfield, Brenda D. PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7447	journal	January 2019
A Genetic Map of Blumeria graminis Based on Functional Genes, Avirulence Genes, and Molecular Markers Pedersen, Carsten; Rasmussen, Søren W.; Giese, Henriette Fungal Genetics and Biology, Vol. 35, Issue 3 https://doi.org/10.1006/fgbi.2001.1326	journal	April 2002
Genetic mapping of 14 avirulence genes in an EU-B04×1639 progeny of Venturia inaequalis Broggini, Giovanni A. L.; Bus, Vincent G. M.; Parravicini, Gabriella Fungal Genetics and Biology, Vol. 48, Issue 2 https://doi.org/10.1016/j.fgb.2010.09.001	journal	February 2011
A RID-like putative cytosine methyltransferase homologue controls sexual development in the fungus Podospora anserina Grognet, Pierre; Timpano, Hélène; Carlier, Florian PLOS Genetics, Vol. 15, Issue 8 https://doi.org/10.1371/journal.pgen.1008086	journal	August 2019
Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete Neurospora tetrasperma Sun, Yu; Corcoran, Pádraic; Menkis, Audrius PLoS Genetics, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pgen.1002820	journal	July 2012
Minimap2: pairwise alignment for nucleotide sequences Li, Heng Bioinformatics, Vol. 34, Issue 18 https://doi.org/10.1093/bioinformatics/bty191	journal	May 2018
Diverse programs of ascus development in pseudohomothallic species of Neurospora, Gelasinospora, and Podospora Raju, Namboori B.; Perkins, David D. Developmental Genetics, Vol. 15, Issue 1 https://doi.org/10.1002/dvg.1020150111	journal	January 1994
Nuclear dynamics in a fungal chimera Roper, M.; Simonin, A.; Hickey, P. C. Proceedings of the National Academy of Sciences, Vol. 110, Issue 32 https://doi.org/10.1073/pnas.1220842110	journal	July 2013
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen Krogh, Anders; Larsson, Björn; von Heijne, Gunnar Journal of Molecular Biology, Vol. 305, Issue 3 https://doi.org/10.1006/jmbi.2000.4315	journal	January 2001
Fungal Sex: The Basidiomycota Coelho, Marco A.; Bakkeren, Guus; Sun, Sheng Microbiology Spectrum, Vol. 5, Issue 3 https://doi.org/10.1128/microbiolspec.FUNK-0046-2016	journal	May 2017
Evolution under tight linkage to mating type Uyenoyama, Marcy K. New Phytologist, Vol. 165, Issue 1 https://doi.org/10.1111/j.1469-8137.2004.01246.x	journal	December 2004
Contrasted Patterns of Molecular Evolution in Dominant and Recessive Self-Incompatibility Haplotypes in Arabidopsis Goubet, Pauline M.; Bergès, Hélène; Bellec, Arnaud PLoS Genetics, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pgen.1002495	journal	March 2012
Re-Evaluation of the Order Sordariales: Delimitation of Lasiosphaeriaceae s. str., and Introduction of the New Families Diplogelasinosporaceae, Naviculisporaceae, and Schizotheciaceae Marin-Felix, Yasmina; Miller, Andrew N.; Cano-Lira, José F. Microorganisms, Vol. 8, Issue 9 https://doi.org/10.3390/microorganisms8091430	journal	September 2020
Evolution of uni- and bifactorial sexual compatibility systems in fungi Nieuwenhuis, B. P. S.; Billiard, S.; Vuilleumier, S. Heredity, Vol. 111, Issue 6 https://doi.org/10.1038/hdy.2013.67	journal	July 2013
Proposed Nomenclature for Mating Type Genes of Filamentous Ascomycetes Turgeon, B. Gillian; Yoder, O. C. Fungal Genetics and Biology, Vol. 31, Issue 1 https://doi.org/10.1006/fgbi.2000.1227	journal	October 2000
Rapid genetic mapping in Neurospora crassa Jin, Yuan; Allan, Sabrina; Baber, Lauren Fungal Genetics and Biology, Vol. 44, Issue 6 https://doi.org/10.1016/j.fgb.2006.09.002	journal	June 2007
Genetic Linkage Maps and Genomic Organization in Leptosphaeria maculans Kuhn, Marie-Line; Gout, Lilian; Howlett, Barbara J. European Journal of Plant Pathology, Vol. 114, Issue 1 https://doi.org/10.1007/s10658-005-3168-6	journal	January 2006
The ranking of fungi: a tribute to David L. Hawksworth on his 70th birthday Hyde, Kevin D.; Maharachchikumbura, Sajeewa S. N.; Hongsanan, Sinang Fungal Diversity, Vol. 84, Issue 1 https://doi.org/10.1007/s13225-017-0383-3	journal	May 2017
Some Genetic Aspects of Sex Muller, H. J. The American Naturalist, Vol. 66, Issue 703 https://doi.org/10.1086/280418	journal	March 1932
PAML 4: Phylogenetic Analysis by Maximum Likelihood Yang, Z. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm088	journal	April 2007
Sme4 coiled-coil protein mediates synaptonemal complex assembly, recombinosome relocalization, and spindle pole body morphogenesis Espagne, Eric; Vasnier, Christelle; Storlazzi, Aurora Proceedings of the National Academy of Sciences, Vol. 108, Issue 26 https://doi.org/10.1073/pnas.1107272108	journal	June 2011
Fast and accurate de novo genome assembly from long uncorrected reads Vaser, Robert; Sović, Ivan; Nagarajan, Niranjan Genome Research, Vol. 27, Issue 5 https://doi.org/10.1101/gr.214270.116	journal	January 2017
RNA silencing in fungi: Mechanisms and applications Nakayashiki, Hitoshi FEBS Letters, Vol. 579, Issue 26 https://doi.org/10.1016/j.febslet.2005.08.016	journal	August 2005
Jalview Version 2--a multiple sequence alignment editor and analysis workbench Waterhouse, A. M.; Procter, J. B.; Martin, D. M. A. Bioinformatics, Vol. 25, Issue 9 https://doi.org/10.1093/bioinformatics/btp033	journal	January 2009
Repeat-induced G-C to A-T mutations in Neurospora Cambareri, E.; Jensen, B.; Schabtach, E. Science, Vol. 244, Issue 4912 https://doi.org/10.1126/science.2544994	journal	June 1989
Genomic architecture of supergenes: connecting form and function Berdan, Emma L.; Flatt, Thomas; Kozak, Genevieve M. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 377, Issue 1856 https://doi.org/10.1098/rstb.2021.0192	journal	June 2022
No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution Ironside, Joseph E. BioEssays, Vol. 32, Issue 8 https://doi.org/10.1002/bies.200900124	journal	July 2010
ATM Promotes the Obligate XY Crossover and both Crossover Control and Chromosome Axis Integrity on Autosomes Barchi, Marco; Roig, Ignasi; Di Giacomo, Monica PLoS Genetics, Vol. 4, Issue 5 https://doi.org/10.1371/journal.pgen.1000076	journal	May 2008
Convergent Evolution of Chromosomal Sex-Determining Regions in the Animal and Fungal Kingdoms Fraser, James A.; Diezmann, Stephanie; Subaran, Ryan L. PLoS Biology, Vol. 2, Issue 12 https://doi.org/10.1371/journal.pbio.0020384	journal	November 2004
Genetics of mating in members of the Chaetomiaceae as revealed by experimental and genomic characterization of reproduction in Myceliophthora heterothallica Hutchinson, Miriam I.; Powell, Amy J.; Tsang, Adrian Fungal Genetics and Biology, Vol. 86 https://doi.org/10.1016/j.fgb.2015.11.007	journal	January 2016
Multiple convergent supergene evolution events in mating-type chromosomes Branco, Sara; Carpentier, Fantin; Rodríguez de la Vega, Ricardo C. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04380-9	journal	May 2018
Tempo of Degeneration Across Independently Evolved Nonrecombining Regions Carpentier, Fantin; Rodríguez de la Vega, Ricardo C.; Jay, Paul Molecular Biology and Evolution, Vol. 39, Issue 4 https://doi.org/10.1093/molbev/msac060	journal	March 2022
STAR: ultrafast universal RNA-seq aligner Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix Bioinformatics, Vol. 29, Issue 1 https://doi.org/10.1093/bioinformatics/bts635	journal	October 2012
Sex, outcrossing and mating types: unsolved questions in fungi and beyond: Sexy fungi Billiard, S.; LÓPez-Villavicencio, M.; Hood, M. E. Journal of Evolutionary Biology, Vol. 25, Issue 6 https://doi.org/10.1111/j.1420-9101.2012.02495.x	journal	April 2012
RIP: the evolutionary cost of genome defense Galagan, James E.; Selker, Eric U. Trends in Genetics, Vol. 20, Issue 9 https://doi.org/10.1016/j.tig.2004.07.007	journal	September 2004
Evidence for non-random spatial distribution of meiotic exchanges in Podospora anserina: Comparison between linkage groups 1 and 6 Marcou, Denise; Masson, Arlette; Simonet, Jean-Marc Molecular and General Genetics MGG, Vol. 176, Issue 1 https://doi.org/10.1007/BF00334297	journal	October 1979
Massive Changes in Genome Architecture Accompany the Transition to Self-Fertility in the Filamentous Fungus Neurospora tetrasperma Ellison, Christopher E.; Stajich, Jason E.; Jacobson, David J. Genetics, Vol. 189, Issue 1 https://doi.org/10.1534/genetics.111.130690	journal	July 2011
Systematic Deletion of Homeobox Genes in Podospora anserina Uncovers Their Roles in Shaping the Fruiting Body Coppin, Evelyne; Berteaux-Lecellier, Véronique; Bidard, Frédérique PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0037488	journal	May 2012
A Molecular Genetic Map and Electrophoretic Karyotype of the Plant Pathogenic Fungus Cochliobolus sativus Zhong, Shaobin; Steffenson, Brian J.; Martinez, J. Patrick Molecular Plant-Microbe Interactions, Vol. 15, Issue 5 https://doi.org/10.1094/MPMI.2002.15.5.481	journal	May 2002
Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server Kall, L.; Krogh, A.; Sonnhammer, E. L. L. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm256	journal	May 2007
Characterization of the genomic organization of the region bordering the centromere of chromosome V of Podospora anserina by direct sequencing Silar, Philippe; Barreau, Christian; Debuchy, Robert Fungal Genetics and Biology, Vol. 39, Issue 3 https://doi.org/10.1016/S1087-1845(03)00025-2	journal	August 2003
Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data Carver, T.; Harris, S. R.; Berriman, M. Bioinformatics, Vol. 28, Issue 4 https://doi.org/10.1093/bioinformatics/btr703	journal	December 2011
Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types Billiard, Sylvain; López-Villavicencio, Manuela; Devier, Benjamin Biological Reviews, Vol. 86, Issue 2 https://doi.org/10.1111/j.1469-185X.2010.00153.x	journal	August 2010
Primer3—new capabilities and interfaces Untergasser, Andreas; Cutcutache, Ioana; Koressaar, Triinu Nucleic Acids Research, Vol. 40, Issue 15 https://doi.org/10.1093/nar/gks596	journal	June 2012
Y recombination arrest and degeneration in the absence of sexual dimorphism Lenormand, Thomas; Roze, Denis Science, Vol. 375, Issue 6581 https://doi.org/10.1126/science.abj1813	journal	February 2022
Coevolution between transposable elements and recombination Kent, Tyler V.; Uzunović, Jasmina; Wright, Stephen I. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1736 https://doi.org/10.1098/rstb.2016.0458	journal	November 2017
Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism Branco, Sara; Badouin, Hélène; Rodríguez de la Vega, Ricardo C. Proceedings of the National Academy of Sciences, Vol. 114, Issue 27 https://doi.org/10.1073/pnas.1701658114	journal	June 2017
E3 ligase Hei10: a multifaceted structure-based signaling molecule with roles within and beyond meiosis De Muyt, A.; Zhang, L.; Piolot, T. Genes & Development, Vol. 28, Issue 10 https://doi.org/10.1101/gad.240408.114	journal	May 2014
Introgression maintains the genetic integrity of the mating-type determining chromosome of the fungus Neurospora tetrasperma Corcoran, Pádraic; Anderson, Jennifer L.; Jacobson, David J. Genome Research, Vol. 26, Issue 4 https://doi.org/10.1101/gr.197244.115	journal	February 2016
TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations Abascal, Federico; Zardoya, Rafael; Telford, Maximilian J. Nucleic Acids Research, Vol. 38, Issue suppl_2 https://doi.org/10.1093/nar/gkq291	journal	April 2010
OrthoFinder: phylogenetic orthology inference for comparative genomics Emms, David M.; Kelly, Steven Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1832-y	journal	November 2019
The Compact Chromatin Structure of a Ty Repeated Sequence Suppresses Recombination Hotspot Activity in Saccharomyces cerevisiae Ben-Aroya, Shay; Mieczkowski, Piotr A.; Petes, Thomas D. Molecular Cell, Vol. 15, Issue 2 https://doi.org/10.1016/j.molcel.2004.06.002	journal	July 2004
Genetic linkage map of Phaeosphaeria nodorum, the causal agent of stagonospora nodorum blotch disease of wheat Malkus, Arkadiusz; Song, Qijian; Cregan, Perry European Journal of Plant Pathology, Vol. 124, Issue 4 https://doi.org/10.1007/s10658-009-9454-y	journal	March 2009
The evolution of restricted recombination in sex chromosomes Bergero, Roberta; Charlesworth, Deborah Trends in Ecology & Evolution, Vol. 24, Issue 2 https://doi.org/10.1016/j.tree.2008.09.010	journal	February 2009
BUSCO Update: Novel and Streamlined Workflows along with Broader and Deeper Phylogenetic Coverage for Scoring of Eukaryotic, Prokaryotic, and Viral Genomes Manni, Mosè; Berkeley, Matthew R.; Seppey, Mathieu Molecular Biology and Evolution, Vol. 38, Issue 10 https://doi.org/10.1093/molbev/msab199	journal	July 2021
Note on abnormal spores in Podospora minuta Page, Winifred M. Transactions of the British Mycological Society, Vol. 20, Issue 2 https://doi.org/10.1016/S0007-1536(36)80010-2	journal	January 1936
BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database Brůna, Tomáš; Hoff, Katharina J.; Lomsadze, Alexandre NAR Genomics and Bioinformatics, Vol. 3, Issue 1 https://doi.org/10.1093/nargab/lqaa108	journal	January 2021
Combinations of Spok genes create multiple meiotic drivers in Podospora Vogan, Aaron A.; Ament-Velásquez, S. Lorena; Granger-Farbos, Alexandra eLife, Vol. 8 https://doi.org/10.7554/eLife.46454	journal	July 2019
Estimating Synonymous and Nonsynonymous Substitution Rates Under Realistic Evolutionary Models Yang, Ziheng; Nielsen, Rasmus Molecular Biology and Evolution, Vol. 17, Issue 1 https://doi.org/10.1093/oxfordjournals.molbev.a026236	journal	January 2000
Fast preparation of fungal DNA for PCR screening Liu, Kuang-Hung; Yeh, Yu-Ling; Shen, Wei-Chiang Journal of Microbiological Methods, Vol. 85, Issue 2 https://doi.org/10.1016/j.mimet.2011.01.029	journal	May 2011
Heterokaryon formation and parasexual recombination between vegetatively incompatible lineages in a population of the chestnut blight fungus, Cryphonectria parasitica: HETEROKARYOSIS and PARASEXUALITY IN C. PARASITICA McGUIRE, I. C.; Davis, J. E.; Double, M. L. Molecular Ecology, Vol. 14, Issue 12 https://doi.org/10.1111/j.1365-294X.2005.02693.x	journal	August 2005
A unified classification system for eukaryotic transposable elements Wicker, Thomas; Sabot, François; Hua-Van, Aurélie Nature Reviews Genetics, Vol. 8, Issue 12 https://doi.org/10.1038/nrg2165	journal	December 2007
Canu: scalable and accurate long-read assembly via adaptive k -mer weighting and repeat separation Koren, Sergey; Walenz, Brian P.; Berlin, Konstantin Genome Research, Vol. 27, Issue 5 https://doi.org/10.1101/gr.215087.116	journal	March 2017
BEDTools: a flexible suite of utilities for comparing genomic features Quinlan, Aaron R.; Hall, Ira M. Bioinformatics, Vol. 26, Issue 6 https://doi.org/10.1093/bioinformatics/btq033	journal	January 2010
Meiotic Crossing-over: Obligation and Interference Jones, Gareth H.; Franklin, F. Chris H. Cell, Vol. 126, Issue 2 https://doi.org/10.1016/j.cell.2006.07.010	journal	July 2006
Does translational ambiguity increase during cell differentiation? Picard-Bennoun, Marguerite FEBS Letters, Vol. 149, Issue 2 https://doi.org/10.1016/0014-5793(82)81094-6	journal	November 1982
The genome sequence of the filamentous fungus Neurospora crassa Galagan, James E.; Calvo, Sarah E.; Borkovich, Katherine A. Nature, Vol. 422, Issue 6934 https://doi.org/10.1038/nature01554	journal	April 2003
Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes Gladieux, Pierre; Ropars, Jeanne; Badouin, Hélène Molecular Ecology, Vol. 23, Issue 4 https://doi.org/10.1111/mec.12631	journal	January 2014
Unidirectional Evolutionary Transitions in Fungal Mating Systems and the Role of Transposable Elements Gioti, Anastasia; Mushegian, Alexandra A.; Strandberg, Rebecka Molecular Biology and Evolution, Vol. 29, Issue 10 https://doi.org/10.1093/molbev/mss132	journal	July 2012
Degeneration of the Nonrecombining Regions in the Mating-Type Chromosomes of the Anther-Smut Fungi Fontanillas, Eric; Hood, Michael E.; Badouin, Hélène Molecular Biology and Evolution, Vol. 32, Issue 4 https://doi.org/10.1093/molbev/msu396	journal	December 2014
The Mating-Type Chromosome in the Filamentous Ascomycete Neurospora tetrasperma Represents a Model for Early Evolution of Sex Chromosomes Menkis, Audrius; Jacobson, David J.; Gustafsson, Tim PLoS Genetics, Vol. 4, Issue 3 https://doi.org/10.1371/journal.pgen.1000030	journal	March 2008
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
Multilevel Selection in the Filamentous AscomyceteNeurospora tetrasperma Meunier, Cécile; Hosseini, Sara; Heidari, Nahid The American Naturalist, Vol. 191, Issue 3 https://doi.org/10.1086/695803	journal	March 2018
Sequencing DNA with nanopores: Troubles and biases Delahaye, Clara; Nicolas, Jacques PLOS ONE, Vol. 16, Issue 10 https://doi.org/10.1371/journal.pone.0257521	journal	October 2021
Mating type in Filamentous Fungi Kronstad, J. W.; Staben, C. Annual Review of Genetics, Vol. 31, Issue 1 https://doi.org/10.1146/annurev.genet.31.1.245	journal	December 1997
Supergenes and Complex Phenotypes Schwander, Tanja; Libbrecht, Romain; Keller, Laurent Current Biology, Vol. 24, Issue 7 https://doi.org/10.1016/j.cub.2014.01.056	journal	March 2014
Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement Walker, Bruce J.; Abeel, Thomas; Shea, Terrance PLoS ONE, Vol. 9, Issue 11 https://doi.org/10.1371/journal.pone.0112963	journal	November 2014
A first genome assembly of the barley fungal pathogen Pyrenophora teres f. teres Ellwood, Simon R.; Liu, Zhaohui; Syme, Rob A. Genome Biology, Vol. 11, Issue 11 https://doi.org/10.1186/gb-2010-11-11-r109	journal	November 2010
Correlation between pairing initiation sites, recombination nodules and meiotic recombination in Sordaria macrospora. Zickler, D.; Moreau, P. J.; Huynh, A. D. Genetics, Vol. 132, Issue 1 https://doi.org/10.1093/genetics/132.1.135	journal	September 1992

Similar Records

Massive Changes in Genome Architecture Accompany the Transition to Self-Fertility in the filamentous Fungus Neurospora tetrasperma

Journal Article · Mon May 16 00:00:00 EDT 2011 · Genetics · OSTI ID:2234196

Ellison, Christoper; Stajich, Jason; Jacobson, David; +8 more

Cryptic genetic structure and copy-number variation in the ubiquitous forest symbiotic fungus Cenococcum geophilum

Journal Article · Wed Sep 01 00:00:00 EDT 2021 · Environmental Microbiology · OSTI ID:2234196

Dauphin, Benjamin; Freitas Pereira, Maíra; Kohler, Annegret; +8 more

Pseudohomothallism and evolution of the mating-type chromosome in Neurospora tetrasperma

Journal Article · Sat Jun 01 00:00:00 EDT 1996 · Genetics · OSTI ID:2234196

Merino, S T; Nelson, M A; Natvig, D O

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Genetic loci
Genomics
Centromeres
Fungal evolution
Fungal spores
Fungi
Evolutionary genetics
Mycelium

Title: Stepwise recombination suppression around the mating-type locus in an ascomycete fungus with self-fertile spores

Citation Formats

References (114)

Similar Records

Related Subjects