The Genome Sequence of the Model Ascomycete Fungus Podospora Anserina

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.

Citing Articles

Reconstructing NOD-like receptor alleles with high internal conservation in using long-read sequencing.

Ament-Velasquez S, Furneaux B, Dheur S, Granger-Farbos A, Stelkens R, Johannesson H bioRxiv. 2025; .

PMID: 39868110 PMC: 11761791. DOI: 10.1101/2025.01.13.632504.

What are the 100 most cited fungal genera?.

Bhunjun C, Chen Y, Phukhamsakda C, Boekhout T, Groenewald J, McKenzie E Stud Mycol. 2024; 108:1-411.

PMID: 39100921 PMC: 11293126. DOI: 10.3114/sim.2024.108.01.

The massive 340 megabase genome of Anisogramma anomala, a biotrophic ascomycete that causes eastern filbert blight of hazelnut.

Cohen A, Cai G, Price D, Molnar T, Zhang N, Hillman B BMC Genomics. 2024; 25(1):347.

PMID: 38580927 PMC: 10998396. DOI: 10.1186/s12864-024-10198-1.

High-Quality Genome Assemblies of 4 Members of the Podospora anserina Species Complex.

Ament-Velasquez S, Vogan A, Wallerman O, Hartmann F, Gautier V, Silar P Genome Biol Evol. 2024; 16(3).

PMID: 38386982 PMC: 10936905. DOI: 10.1093/gbe/evae034.

Mutations in and Trigger Spontaneous Development of Barren Fruiting Bodies.

Essadik I, Boucher C, Bobee C, Cabet E, Gautier V, Lalucque H J Fungi (Basel). 2024; 10(1).

PMID: 38276025 PMC: 10819945. DOI: 10.3390/jof10010079.

References

Brown D, Cheung F, Proctor R, Butchko R, Zheng L, Lee Y . Comparative analysis of 87,000 expressed sequence tags from the fumonisin-producing fungus Fusarium verticillioides. Fungal Genet Biol. 2005; 42(10):848-61. DOI: 10.1016/j.fgb.2005.06.001. View

Vanden Wymelenberg A, Sabat G, Mozuch M, Kersten P, Cullen D, Blanchette R . Structure, organization, and transcriptional regulation of a family of copper radical oxidase genes in the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol. 2006; 72(7):4871-7. PMC: 1489383. DOI: 10.1128/AEM.00375-06. View

Saze H, Mittelsten Scheid O, Paszkowski J . Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet. 2003; 34(1):65-9. DOI: 10.1038/ng1138. View

Kouzminova E, Selker E . dim-2 encodes a DNA methyltransferase responsible for all known cytosine methylation in Neurospora. EMBO J. 2001; 20(15):4309-23. PMC: 149169. DOI: 10.1093/emboj/20.15.4309. View

El-Khoury R, Sellem C, Coppin E, Boivin A, Maas M, Debuchy R . Gene deletion and allelic replacement in the filamentous fungus Podospora anserina. Curr Genet. 2008; 53(4):249-58. DOI: 10.1007/s00294-008-0180-3. View

Catalanotto C, Azzalin G, Macino G, Cogoni C . Gene silencing in worms and fungi. Nature. 2000; 404(6775):245. DOI: 10.1038/35005169. View

Galagan J, Selker E . RIP: the evolutionary cost of genome defense. Trends Genet. 2004; 20(9):417-23. DOI: 10.1016/j.tig.2004.07.007. View

Porcel B, Delfour O, Castelli V, de Berardinis V, Friedlander L, Cruaud C . Numerous novel annotations of the human genome sequence supported by a 5'-end-enriched cDNA collection. Genome Res. 2004; 14(3):463-71. PMC: 353234. DOI: 10.1101/gr.1481104. View

Coppin E, de Renty C, Debuchy R . The function of the coding sequences for the putative pheromone precursors in Podospora anserina is restricted to fertilization. Eukaryot Cell. 2005; 4(2):407-20. PMC: 549327. DOI: 10.1128/EC.4.2.407-420.2005. View

10.

Silar P, Lalucque H, Haedens V, Zickler D, Picard M . eEF1A Controls ascospore differentiation through elevated accuracy, but controls longevity and fruiting body formation through another mechanism in Podospora anserina. Genetics. 2001; 158(4):1477-89. PMC: 1461745. DOI: 10.1093/genetics/158.4.1477. View

11.

Kamper J, Kahmann R, Bolker M, Ma L, Brefort T, Saville B . Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature. 2006; 444(7115):97-101. DOI: 10.1038/nature05248. View

12.

Butler M, Goodwin T, Poulter R . Two new fungal inteins. Yeast. 2005; 22(6):493-501. DOI: 10.1002/yea.1229. View

13.

Shiu P, Zickler D, Raju N, Ruprich-Robert G, Metzenberg R . 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. 2006; 103(7):2243-8. PMC: 1413707. DOI: 10.1073/pnas.0508896103. View

14.

Castelli V, Aury J, Jaillon O, Wincker P, Clepet C, Menard M . Whole genome sequence comparisons and "full-length" cDNA sequences: a combined approach to evaluate and improve Arabidopsis genome annotation. Genome Res. 2004; 14(3):406-13. PMC: 353228. DOI: 10.1101/gr.1515604. View

15.

Monnot F . [Localization of S gene and some peculiarities of crossing-over in Podospora anserina]. C R Hebd Seances Acad Sci. 1953; 236(24):2330-2. View

16.

Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G . Genome sequencing and analysis of Aspergillus oryzae. Nature. 2005; 438(7071):1157-61. DOI: 10.1038/nature04300. View

17.

Fraser J, Diezmann S, Subaran R, Allen A, Lengeler K, Dietrich F . Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol. 2004; 2(12):e384. PMC: 526376. DOI: 10.1371/journal.pbio.0020384. View

18.

Imamura T, Watanabe T, Kuwahara M, Koshijima T . Ester linkages between lignin and glucuronic acid in lignin-carbohydrate complexes from Fagus crenata. Phytochemistry. 1994; 37(4):1165-73. DOI: 10.1016/s0031-9422(00)89551-5. View

19.

Galagan J, Calvo S, Cuomo C, Ma L, Wortman J, Batzoglou S . Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature. 2005; 438(7071):1105-15. DOI: 10.1038/nature04341. View

20.

Cogoni C, Macino G . Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature. 1999; 399(6732):166-9. DOI: 10.1038/20215. View