Molecular Genetics and Genomics

, Volume 294, Issue 1, pp 177–190 | Cite as

A gene graveyard in the genome of the fungus Podospora comata

  • Philippe SilarEmail author
  • Jean-Marc Dauget
  • Valérie Gautier
  • Pierre Grognet
  • Michelle Chablat
  • Sylvie Hermann-Le Denmat
  • Arnaud Couloux
  • Patrick Wincker
  • Robert DebuchyEmail author
Original Article


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.


Podospora anserina Podospora comata Lasiosphaeriaceae Sordariales Pseudogene Speciation 



We thank Sylvie Cangemi for expert technical assistance. We thank the eBio IFB platform for bioinformatics support (ANR-11-INSB-0013). DNA sequencing and RNAseq have benefited from the plateform and expertise of the high Throughput Sequencing core facility of I2BC (Institute of Integrative Biology of the Cell-

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

438_2018_1497_MOESM1_ESM.pptx (411 kb)
Supplementary Fig. S1. Divergence percentages for chromosomes 2 and 4 between strain S and strain T. Red and blue (for the inverted sequences) lines link the regions with the percentage of nucleotide identity indicated on the left. Similar results were found for the five other chromosomes. On chromosome 4, the region that is less than 1‰ divergent between strain S and strain T is clearly visible on the 100% and 99% lines (arrowhead). (PPTX 410 KB)
438_2018_1497_MOESM2_ESM.xlsx (24 kb)
Supplementary material 2 (XLSX 24 KB)
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Supplementary material 3 (XLSX 109 KB)
438_2018_1497_MOESM4_ESM.xlsx (18 kb)
Supplementary material 4 (XLSX 18 KB)
438_2018_1497_MOESM5_ESM.docx (30 kb)
Supplementary material 5 (DOCX 29 KB)


  1. Belcour L, Rossignol M, Koll F, Sellem CH, Oldani C (1997) Plasticity of the mitochondrial genome in Podospora. Polymorphism for 15 optional sequences: group-I, group-II introns, intronic ORFs and an intergenic region. Curr Genet 31:308–317CrossRefGoogle Scholar
  2. Bernet J (1967) Les systèmes d’incompatibilité chez le Podospora anserina. C R Acad Sci Paris Sér D265:1330–1333Google Scholar
  3. Bidard F, Ait Benkhali J, Coppin E, Imbeaud S, Grognet P, Delacroix H, Debuchy R (2011) Genome-wide gene expression profiling of fertilization competent mycelium in opposite mating types in the heterothallic fungus Podospora anserina. PLoS One 6:e21476CrossRefGoogle Scholar
  4. Blackwell M (2011) The Fungi: 1, 2, 3 … million species? Am J Bot 98:426–438CrossRefGoogle Scholar
  5. Boetzer M, Pirovano W (2012) Toward almost closed genomes with GapFiller. Genome Biol 13:R56–R56CrossRefGoogle Scholar
  6. Boucher C, Nguyen T-S, Silar P (2017) Species delimitation in the Podospora anserina/P. pauciseta/P. comata species complex (Sordariales). Cryptogam Mycol 38(4):485–506CrossRefGoogle Scholar
  7. Carvunis A-R, Rolland T, Wapinski I, Calderwood MA, Yildirim MA, Simonis N, Charloteaux B, Hidalgo CA, Barbette J, Santhanam B, Brar GA, Weissman JS, Regev A, Thierry-Mieg N, Cusick ME, Vidal M (2012) Proto-genes and de novo gene birth. Nature 487:370–374CrossRefGoogle Scholar
  8. Clark RM, Schweikert G, Toomajian C, Ossowski S, Zeller G, Shinn P, Warthmann N, Hu TT, Fu G, Hinds DA, Chen H, Frazer KA, Huson DH, Scholkopf B, Nordborg M, Ratsch G, Ecker JR, Weigel D (2007) Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317:338–342CrossRefGoogle Scholar
  9. Daverdin G, Rouxel T, Gout L, Aubertot J-N, Fudal I, Meyer M, Parlange F, Carpezat J, Balesdent M-H (2012) Genome structure and reproductive behaviour influence the evolutionary potential of a fungal phytopathogen. PLoS Pathog 8:e1003020CrossRefGoogle Scholar
  10. Espagne E, Lespinet O, Malagnac F, Da Silva C, Jaillon O, Porcel BM, Couloux A, Aury JM, Segurens B, Poulain J, Anthouard V, Grossetete S, Khalili H, Coppin E, Dequard-Chablat M, Picard M, Contamine V, Arnaise S, Bourdais A, Berteaux-Lecellier V, Gautheret D, de Vries RP, Battaglia E, Coutinho PM, Danchin EG, Henrissat B, Khoury RE, Sainsard-Chanet A, Boivin A, Pinan-Lucarre B, Sellem CH, Debuchy R, Wincker P, Weissenbach J, Silar P (2008) The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol 9:R77CrossRefGoogle Scholar
  11. Ferrari R, Lacaze I, Le Faouder P, Bertrand-Michel J, Oger C, Galano JM, Durand T, Moularat S, Chan Ho Tong L, Boucher C, Kilani J, Petit Y, Vanparis O, Trannoy C, Brun S, Lalucque H, Malagnac F, Silar P (2018) Cyclooxygenases and lipoxygenases are used by the fungus Podospora anserina to repel nematodes. Biochim Biophys Acta 1862:2174–2182CrossRefGoogle Scholar
  12. Golicz AA, Martinez PA, Zander M, Patel DA, Van De Wouw AP, Visendi P, Fitzgerald TL, Edwards D, Batley J (2015) Gene loss in the fungal canola pathogen Leptosphaeria maculans. Funct Integr Genom 15:189–196CrossRefGoogle Scholar
  13. Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH, Hansen NF, Durand EY, Malaspinas AS, Jensen JD, Marques-Bonet T, Alkan C, Prufer K, Meyer M, Burbano HA, Good JM, Schultz R, Aximu-Petri A, Butthof A, Hober B, Hoffner B, Siegemund M, Weihmann A, Nusbaum C, Lander ES, Russ C, Novod N, Affourtit J, Egholm M, Verna C, Rudan P, Brajkovic D, Kucan Z, Gusic I, Doronichev VB, Golovanova LV, Lalueza-Fox C, de la Rasilla M, Fortea J, Rosas A, Schmitz RW, Johnson PLF, Eichler EE, Falush D, Birney E, Mullikin JC, Slatkin M, Nielsen R, Kelso J, Lachmann M, Reich D, Paabo S (2010) A draft sequence of the Neandertal genome. Science 328:710–722CrossRefGoogle Scholar
  14. Grognet P, Bidard F, Kuchly C, Tong LC, Coppin E, Benkhali JA, Couloux A, Wincker P, Debuchy R, Silar P (2014a) Maintaining two mating types: structure of the mating type locus and its role in heterokaryosis in Podospora anserina. Genetics 197:421–432CrossRefGoogle Scholar
  15. Grognet P, Lalucque H, Malagnac F, Silar P (2014b) Genes that bias mendelian segregation. PLoS Genet 10:e1004387CrossRefGoogle Scholar
  16. Hartmann FE, Sánchez-Vallet A, McDonald BA, Croll D (2017) A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements. Isme J 11:1189CrossRefGoogle Scholar
  17. Hawksworth DL (1991) The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol Res 95:641–655CrossRefGoogle Scholar
  18. Hermanns J, Osiewacz HD (1992) The linear mitochondrial plasmid pAL2-1 of a long-lived Podospora anserina mutant is an invertron encoding a DNA and RNA polymerase. Curr Genet 22:491–500CrossRefGoogle Scholar
  19. Lafontaine I, Dujon B (2010) Origin and fate of pseudogenes in Hemiascomycetes: a comparative analysis. BMC Genom 11:260–260CrossRefGoogle Scholar
  20. Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6:41CrossRefGoogle Scholar
  21. Liu H, Wang Q, He Y, Chen L, Hao C, Jiang C, Li Y, Dai Y, Kang Z, Xu J-R (2016) Genome-wide A-to-I RNA editing in fungi independent of ADAR enzymes. Genome Res 26:499–509CrossRefGoogle Scholar
  22. Liu H, Li Y, Chen D, Qi Z, Wang Q, Wang J, Jiang C, Xu J-R (2017) A-to-I RNA editing is developmentally regulated and generally adaptive for sexual reproduction in Neurospora crassa. Proc Natl Acad Sci 114:E7756–E7765CrossRefGoogle Scholar
  23. Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, Tang J, Wu G, Zhang H, Shi Y, Liu Y, Yu C, Wang B, Lu Y, Han C, Cheung DW, Yiu S-M, Peng S, Xiaoqian Z, Liu G, Liao X, Li Y, Yang H, Wang J, Lam T-W, Wang J (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 1:18–18CrossRefGoogle Scholar
  24. Malagnac F, Fabret C, Prigent M, Rousset JP, Namy O, Silar P (2013) Rab-GDI complex dissociation factor expressed through translational frameshifting in filamentous ascomycetes. PLoS One 8:e73772CrossRefGoogle Scholar
  25. Morel G, Sterck L, Swennen D, Marcet-Houben M, Onesime D, Levasseur A, Jacques N, Mallet S, Couloux A, Labadie K, Amselem J, Beckerich J-M, Henrissat B, Van de Peer Y, Wincker P, Souciet J-L, Gabaldón T, Tinsley CR, Casaregola S (2015) Differential gene retention as an evolutionary mechanism to generate biodiversity and adaptation in yeasts. Sci Rep 5:11571CrossRefGoogle Scholar
  26. Namy O, Rousset JP, Napthine S, Brierley I (2004) Reprogrammed genetic decoding in cellular gene expression. Mol Cell 13:157–168CrossRefGoogle Scholar
  27. Otto TD, Dillon GP, Degrave WS, Berriman M (2011) RATT: rapid annotation transfer tool. Nucleic Acids Res 39:e57–e57CrossRefGoogle Scholar
  28. Pei B, Sisu C, Frankish A, Howald C, Habegger L, Mu XJ, Harte R, Balasubramanian S, Tanzer A, Diekhans M, Reymond A, Hubbard TJ, Harrow J, Gerstein MB (2012) The GENCODE pseudogene resource. Genome Biol 13:R51CrossRefGoogle Scholar
  29. Picard-Bennoun M, Coppin-Raynal E (1983) Translational ambiguity and cell differentiation in a lower eucaryote. In: Abraham KA, Eikhom TS, Pryme IF (eds) Protein synthesis. Humana Press Inc., Clifton, NJ, USA, pp 221–232Google Scholar
  30. Prufer K, Racimo F, Patterson N, Jay F, Sankararaman S, Sawyer S, Heinze A, Renaud G, Sudmant PH, de Filippo C, Li H, Mallick S, Dannemann M, Fu Q, Kircher M, Kuhlwilm M, Lachmann M, Meyer M, Ongyerth M, Siebauer M, Theunert C, Tandon A, Moorjani P, Pickrell J, Mullikin JC, Vohr SH, Green RE, Hellmann I, Johnson PL, Blanche H, Cann H, Kitzman JO, Shendure J, Eichler EE, Lein ES, Bakken TE, Golovanova LV, Doronichev VB, Shunkov MV, Derevianko AP, Viola B, Slatkin M, Reich D, Kelso J, Paabo S (2014) The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505:43–49CrossRefGoogle Scholar
  31. Rissman AI, Mau B, Biehl BS, Darling AE, Glasner JD, Perna NT (2009) Reordering contigs of draft genomes using the Mauve Aligner. Bioinformatics 25:2071–2073CrossRefGoogle Scholar
  32. Ruiz-Orera J, Hernandez-Rodriguez J, Chiva C, Sabidó E, Kondova I, Bontrop R, Marqués-Bonet T, Albà M (2015) Origins of de novo genes in human and chimpanzee. PLoS Genet 11:e1005721CrossRefGoogle Scholar
  33. Silar P (2013) Podospora anserina: from laboratory to biotechnology. In: Benjamin A, Horwitz PKM, Mukherjee M, Christian P, Kubicek (eds) Genomics of soil- and plant-associated fungi. Springer, Heidelberg, pp 283–309CrossRefGoogle Scholar
  34. Silar P, Barreau C, Debuchy R, Kicka S, Turcq B, Sainsard-Chanet A, Sellem CH, Billault A, Cattolico L, Duprat S, Weissenbach J (2003) Characterization of the genomic organization of the region bordering the centromere of chromosome V of Podospora anserina by direct sequencing. Fungal Genet Biol 39:250–263CrossRefGoogle Scholar
  35. Sisu C, Pei B, Leng J, Frankish A, Zhang Y, Balasubramanian S, Harte R, Wang D, Rutenberg-Schoenberg M, Clark W, Diekhans M, Rozowsky J, Hubbard T, Harrow J, Gerstein MB (2014) Comparative analysis of pseudogenes across three phyla. Proc Natl Acad Sci USA 111:13361–13366CrossRefGoogle Scholar
  36. Tangthirasunun N (2014) Champignons saprotrophes: diversité des coelomycètes de Thaïlande et gènes impliqués dans la dégradation de la biomasse chez Podospora anserina. In: p 1 vol. (161 p.)Google Scholar
  37. Taylor JW, Branco S, Gao C, Hann-Soden C, Montoya L, Sylvain I, Gladieux P (2017) Sources of fungal genetic variation and associating it with phenotypic diversity. Microbiol Spectr 5:1–21Google Scholar
  38. van der Burgt A, Karimi Jashni M, Bahkali AH, de Wit PJGM (2014a) Pseudogenization in pathogenic fungi with different host plants and lifestyles might reflect their evolutionary past. Mol Plant Pathol 15:133–144CrossRefGoogle Scholar
  39. van der Burgt A, Severing E, Collemare J, de Wit PJGM (2014b) Automated alignment-based curation of gene models in filamentous fungi. BMC Bioinform 15:19–19CrossRefGoogle Scholar
  40. Wang L, Si W, Yao Y, Tian D, Araki H, Yang S (2012) Genome-wide survey of pseudogenes in 80 fully re-sequenced arabidopsis thaliana accessions. PLoS One 7:e51769CrossRefGoogle Scholar
  41. Whiston E, Taylor JW (2016) Comparative phylogenomics of pathogenic and nonpathogenic species. G3 Genes Genom Genet 6:235Google Scholar
  42. Xie N, Chapeland-Leclerc F, Silar P, Ruprich-Robert G (2014) Systematic gene deletions evidences that laccases are involved in several stages of wood degradation in the filamentous fungus Podospora anserina. Environ Microbiol 16:141–161CrossRefGoogle Scholar
  43. Xie N, Ruprich-Robert G, Silar P, Chapeland-Leclerc F (2015) Bilirubin oxidase-like proteins from Podospora anserina: promising thermostable enzymes for application in transformation of plant biomass. Environ Microbiol 17:866–875CrossRefGoogle Scholar
  44. Zhang Z, Harrison PM, Liu Y, Gerstein M (2003) Millions of years of evolution preserved: a comprehensive catalog of the processed pseudogenes in the human genome. Genome Res 13:2541–2558CrossRefGoogle Scholar
  45. Zhang ZD, Frankish A, Hunt T, Harrow J, Gerstein M (2010) Identification and analysis of unitary pseudogenes: historic and contemporary gene losses in humans and other primates. Genome Biol 11:R26–R26CrossRefGoogle Scholar
  46. Zheng D, Gerstein MB (2007) The ambiguous boundary between genes and pseudogenes: the dead rise up, or do they? Trends Genet 23:219–224CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Univ Paris Diderot, Sorbonne Paris Cité, Laboratoire Interdisciplinaire des Energies de DemainParis Cedex 13France
  2. 2.Institute for Integrative Biology of the Cell (I2BC)CEA, CNRS, Univ. Paris-Sud, Université Paris-SaclayGif-sur-Yvette cedexFrance
  3. 3.Ecole Normale SupérieureParisFrance
  4. 4.CEA, Genoscope, Institut de biologie François JacobEvryFrance
  5. 5.CNRS UMR 8030EvryFrance
  6. 6.Univ. Evry, Université Paris-SaclayEvryFrance

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