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The evolutionary interplay between transposable elements and genome defense in filamentous fungi
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.ORCID iD: 0009-0003-2602-7420
2025 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Transposable elements (TEs), so called “jumping-genes”, are DNA sequences that are able to proliferate in the genomes of organisms. Their movement in the genome can be disruptive by inserting either into or near genes, but sometimes they provide beneficial mutational variation that natural selection, the ultimate force in evolution, can act upon. Despite their potential benefits for the organism, their overall movement is often thought to be at odds with the rest of the genome leading to them having been referred to as selfish. To counteract the negative effects of TE’s movement, hosts have evolved defenses to control and prevent TE-related damage. In this thesis, I have studied TEs in fungi and their interaction with a fungal specific defense called repeat induced point mutation (RIP). RIP induces C-to-T mutations in any repeated region of the genome, including both TEs and duplicate genes. One of the key species where RIP has been described is the filamentous ascomycete Podospora anserina, which has been used as a model organism within genetics and evolution for over a century. In chapter I we were able to dive deeply into the interaction between a specific TE called crapaud and its evolutionary history, and discuss its potential interaction with RIP. In chapter II we discovered that RIP have been lost in a close relative to P. anserina called Podospora pseudocomata and that this loss may have been the cause of a total shift in both types and amount of TEs in its genome. This species also has smaller centromere regions than P. anserina. The centromere regions are the anchoring points when the chromosomes are pulled apart in every cell division. In many fungi the DNA of this region contains many TEs, and our result hints at a connection between the centromeres and RIP. P.anserina and P. pseudocomata are both part of an order known as Sordariales, which have species important to industry and contain model organisms such as P. anserina and Neurospora crassa. In chapter III we compared the genomes of nine families from this order using whole genomes and constructed a phylogeny of the order using phylogenomics. In chapter IV we developed in-depth methods to continue investigating RIP in the order Sordariales and discovered that P. pseudocomata is not the only species that has lost the RIP mutation pattern. We find 17 species lacking RIP, spread across the Sordariales phylogeny. In conclusion, this thesis presents a glimpse into the world of TEs and host genomes and their defense against TEs in filamentous ascomycetes, and the balance and conflict between them.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University , 2025. , p. 62
Keywords [en]
transposable elements, genome defense, filamentous fungi, centromeres, comparative genomics, evolution
National Category
Evolutionary Biology Genetics and Genomics
Research subject
Ecology and Evolution
Identifiers
URN: urn:nbn:se:su:diva-241326ISBN: 978-91-8107-190-0 (print)ISBN: 978-91-8107-191-7 (electronic)OAI: oai:DiVA.org:su-241326DiVA, id: diva2:1948111
Public defence
2025-05-16, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 13:00 (English)
Opponent
Supervisors
Available from: 2025-04-23 Created: 2025-03-27 Last updated: 2025-04-09Bibliographically approved
List of papers
1. Evolutionary dynamics of the LTR-retrotransposon crapaud in the Podospora anserina species complex and the interaction with repeat-induced point mutations
Open this publication in new window or tab >>Evolutionary dynamics of the LTR-retrotransposon crapaud in the Podospora anserina species complex and the interaction with repeat-induced point mutations
2024 (English)In: Mobile DNA, E-ISSN 1759-8753, Vol. 15, no 1, article id 1Article in journal (Refereed) Published
Abstract [en]

Background The genome of the filamentous ascomycete Podospora anserina shows a relatively high abundance of retrotransposons compared to other interspersed repeats. The LTR-retrotransposon family crapaud is particularly abundant in the genome, and consists of multiple diverged sequence variations specifically localized in the 5' half of both long terminal repeats (LTRs). P. anserina is part of a recently diverged species-complex, which makes the system ideal to classify the crapaud family based on the observed LTR variation and to study the evolutionary dynamics, such as the diversification and bursts of the elements over recent evolutionary time.Results We developed a sequence similarity network approach to classify the crapaud repeats of seven genomes representing the P. anserina species complex into 14 subfamilies. This method does not utilize a consensus sequence, but instead it connects any copies that share enough sequence similarity over a set sequence coverage. Based on phylogenetic analyses, we found that the crapaud repeats likely diversified in the ancestor of the complex and have had activity at different time points for different subfamilies. Furthermore, while we hypothesized that the evolution into multiple subfamilies could have been a direct effect of escaping the genome defense system of repeat induced point mutations, we found this not to be the case.Conclusions Our study contributes to the development of methods to classify transposable elements in fungi, and also highlights the intricate patterns of retrotransposon evolution over short timescales and under high mutational load caused by nucleotide-altering genome defense.

Keywords
Fungi, Transposable elements, Retrotransposons, Genome defense, Classification
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:su:diva-226000 (URN)10.1186/s13100-023-00311-8 (DOI)001142858100001 ()38218923 (PubMedID)2-s2.0-85182222252 (Scopus ID)
Available from: 2024-01-31 Created: 2024-01-31 Last updated: 2025-03-27Bibliographically approved
2. Reduced centromere size and shift in transposable element composition in the fungus Podospora pseudocomata: a link to the loss of genome defense?
Open this publication in new window or tab >>Reduced centromere size and shift in transposable element composition in the fungus Podospora pseudocomata: a link to the loss of genome defense?
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(English)Manuscript (preprint) (Other academic)
National Category
Genetics and Genomics Evolutionary Biology
Research subject
Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-241332 (URN)
Available from: 2025-03-27 Created: 2025-03-27 Last updated: 2025-03-27
3. Genome-scale phylogeny and comparative genomics of the fungal order Sordariales
Open this publication in new window or tab >>Genome-scale phylogeny and comparative genomics of the fungal order Sordariales
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2023 (English)In: Molecular Phylogenetics and Evolution, ISSN 1055-7903, E-ISSN 1095-9513, Vol. 189, article id 107938Article in journal (Refereed) Published
Abstract [en]

The order Sordariales is taxonomically diverse, and harbours many species with different lifestyles and large economic importance. Despite its importance, a robust genome-scale phylogeny, and associated comparative genomic analysis of the order is lacking.In this study, we examined whole-genome data from 99 Sordariales, including 52 newly sequenced genomes, and seven outgroup taxa. We inferred a comprehensive phylogeny that resolved several contentious relationships amongst families in the order, and cleared-up intrafamily relationships within the Podosporaceae. Extensive comparative genomics showed that genomes from the three largest families in the dataset (Chae-tomiaceae, Podosporaceae and Sordariaceae) differ greatly in GC content, genome size, gene number, repeat percentage, evolutionary rate, and genome content affected by repeat-induced point mutations (RIP). All genomic traits showed phylogenetic signal, and ancestral state reconstruction revealed that the variation of the properties stems primarily from within-family evolution. Together, the results provide a thorough framework for understanding genome evolution in this important group of fungi.

Keywords
Whole-genome phylogeny, Podosporaceae, Chaetomiaceae, Sordariaceae, Genome evolution
National Category
Environmental Sciences
Identifiers
urn:nbn:se:su:diva-224234 (URN)10.1016/j.ympev.2023.107938 (DOI)001100006000001 ()37820761 (PubMedID)2-s2.0-85174351665 (Scopus ID)
Available from: 2023-12-05 Created: 2023-12-05 Last updated: 2025-03-27Bibliographically approved
4. Presence and absence of repeat induced point mutations in the order Sordariales and its influence on genome evolution
Open this publication in new window or tab >>Presence and absence of repeat induced point mutations in the order Sordariales and its influence on genome evolution
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(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology Genetics and Genomics
Identifiers
urn:nbn:se:su:diva-241333 (URN)
Available from: 2025-03-27 Created: 2025-03-27 Last updated: 2025-03-27

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