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A gene graveyard in the genome of the fungus Podospora comata

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Abstract

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.

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Acknowledgements

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-http://www.i2bc.paris-saclay.fr/).

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Correspondence to Philippe Silar or Robert Debuchy.

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Communicated by S. Hohmann.

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438_2018_1497_MOESM1_ESM.pptx

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)

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Silar, P., Dauget, JM., Gautier, V. et al. A gene graveyard in the genome of the fungus Podospora comata. Mol Genet Genomics 294, 177–190 (2019). https://doi.org/10.1007/s00438-018-1497-3

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