The Enterprise, a massive transposon carrying Spok meiotic drive genes

Vogan, Aaron A., Ament-Velásquez, S. Lorena, Bastiaans, Eric, Wallerman, Ola, Saupe, Sven J., Suh, Alexander ORCID: https://orcid.org/0000-0002-8979-9992 and Johannesson, Hanna (2021) The Enterprise, a massive transposon carrying Spok meiotic drive genes. Genome Research, 31 (5). pp. 789-798. ISSN 1088-9051

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Abstract

The genomes of eukaryotes are full of parasitic sequences known as transposable elements (TEs). Here, we report the discovery of a putative giant tyrosine-recombinase-mobilized DNA transposon, Enterprise, from the model fungus Podospora anserina. Previously, we described a large genomic feature called the Spok block which is notable due to the presence of meiotic drive genes of the Spok gene family. The Spok block ranges from 110 kb to 247 kb and can be present in at least four different genomic locations within P. anserina, despite what is an otherwise highly conserved genome structure. We propose that the reason for its varying positions is that the Spok block is not only capable of meiotic drive but is also capable of transposition. More precisely, the Spok block represents a unique case where the Enterprise has captured the Spoks, thereby parasitizing a resident genomic parasite to become a genomic hyperparasite. Furthermore, we demonstrate that Enterprise (without the Spoks) is found in other fungal lineages, where it can be as large as 70 kb. Lastly, we provide experimental evidence that the Spok block is deleterious, with detrimental effects on spore production in strains which carry it. This union of meiotic drivers and a transposon has created a selfish element of impressive size in Podospora, challenging our perception of how TEs influence genome evolution and broadening the horizons in terms of what the upper limit of transposition may be.

Item Type: Article
Additional Information: Funding Information: This work was supported by the European Research Council (ERC) grant ERC-2014-CoG (project 648143, SpoKiGen) and The Swedish Research Council (project 2015-04649) to H.J., and by the Lars Hierta Memorial Foundation and The Nilsson-Ehle Endowments of the Royal Physiographic Society of Lund to S.L.A.-V. We thank the National Genomics Infrastructure (NGI)/Uppsala Genome Center for support on massive parallel DNA sequencing. The computations were performed on resources provided by SNIC through the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) under the projects SNIC 2017/1-567 and SNIC 2019/8-371. The sequence data of Melanconium sp. NRRL 54901 was produced by the U.S. Department of Energy Joint Genome Institute (http://www.jgi.doe.gov/) in collaboration with the user community. We also thank Sergio Tusso and the TE Jamboree of the Suh Lab for useful advice, and three anonymous reviewers for comments that improved this manuscript. Publisher Copyright: © 2021 Vogan et al.
Uncontrolled Keywords: genetics,genetics(clinical) ,/dk/atira/pure/subjectarea/asjc/1300/1311
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 21 Sep 2022 09:30
Last Modified: 26 Sep 2022 06:02
URI: https://ueaeprints.uea.ac.uk/id/eprint/88542
DOI: 10.1101/GR.267609.120

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