Biology subjects

Oggenfuss, U.

Publications and source records attributed to Oggenfuss, U..

12 recordsLinked to original sources

bioRxiv2025

Massive proliferation of retrotransposons contributes to genome size expansion in species of the Pseudocercospora genus

Genome size expansions are common among eukaryotic lineages. Enlarged genomes can be bioenergetically demanding, and active mobile elements can trigger chromosomal rearrangements and loss of gene function. What triggers genome size expansions remains largely unexplored in many biological clades, particularly within the fungal kingdom. Activation of large transposable elements (TEs), such as long-terminal repeats (LTRs), is a common contributor. Yet the mechanisms of LTR activation remain poorly understood. Here, we focus on the fungal genus Pseudocercospora and closely related species with known variation in genome size. In using an assembly-free approach, we found that TE content is highly variable among species, with species-specific retrotransposon families being the main drivers of independent genome expansions. We further focussed on the two species with the most expanded genomes and reference-quality genomes, P. fijiensis and P. ulei. We found that the P. ulei genome is compartmentalized, with highly variable TE densities among chromosomal regions, and a striking reduction in pathogenicity-associated genes. Overall, our study indicates that species of Pseudocercospora originally had reduced genome sizes, and genome expansions are species-specific, driven by heterogeneous sets of TE families. Furthermore, we found that in the species with the most expanded genome, TE activity might not have ceased yet as indicated by resequencing data analysis of six strains from diverse locations in Colombia. We discuss what might have caused TE activation and subsequent proliferation in the genus, including stress conditions and host adaptation. Surveys of clades with highly dynamic genome sizes are crucial for the investigation of causal factors driving long-term TE dynamics.

genomics↗

bioRxiv2025

Transposable elements hitchhike on Starships across fungal genomes

Horizontal transfer (HT) of transposable elements (TEs) is a widespread phenomenon in eukaryotes and is often associated with bursts of TE activity. This process profoundly influences genome evolution by introducing novel genetic material and driving genetic variation. However, the precise mechanisms facilitating these transfers remain largely uncharacterized. Here, we report a recent TE burst in the insect-pathogenic fungus Metarhizium anisopliae. Our analysis reveals that the actively transposing TEs were introduced via hitchhiking on a so-called Starship--a class of large, themselves horizontally transferable transposons found within the fungal subphylum Pezizomycotina. This particular Starship carried 73 TEs, 43 of which exhibited increased copy numbers in the recipient genome, including 508 perfect copies. This expansion triggered extensive structural reshuffling across all chromosomes and led to the formation of a novel chromosome. Remarkably, this structural reorganization was associated with a dramatic phenotypic shift: the loss of pathogenicity. Expanding our analysis to other fungi, we found that Starship-mediated horizontal transfer of TEs is a general phenomenon. A majority (74%) of 618 published Starships also harbor TEs, which can constitute up to 72% of their content. Moreover, Starships serve as sources of actively transposing TEs: 16% of Starships carried at least one TE with a perfect copy found elsewhere in the genome, and identical TEs were observed on Starships from different species. Collectively, our results establish Starships as major vectors of horizontal TE transfer within Pezizomycotina and further highlight their profound impact on recipient fungal genomes through TE piggybacking.

evolutionary biology↗

bioRxiv2023

A systematic screen for co-option of transposable elements across the fungal kingdom

How novel protein functions are acquired is a central question in molecular biology. Key paths to novelty include gene duplications, recombination or horizontal acquisition. Transposable elements (TEs) are increasingly recognized as a major source of novel domain-encoding sequences. However, the impact of TE coding sequences on the evolution of the proteome remains understudied. Here, we analyzed 1,237 genomes spanning the phylogenetic breadth of the fungal kingdom. We scanned proteomes for evidence of co-occurrence of TE-derived domains along with other conventional protein functional domains. We detected more than 13,000 predicted proteins containing potentially TE-derived domain, of which 825 were identified in more than five genomes, indicating that many host-TE fusions may have persisted over long evolutionary time scales. We used the phylogenetic context to identify the origin and retention of individual TE-derived domains. The most common TE-derived domains are helicases derived from Academ, Kolobok or Helitron. We found putative TE co-options at a higher rate in genomes of the Saccharomycotina, providing an unexpected source of protein novelty in these generally TE depleted genomes. We investigated in detail a candidate host-TE fusion with a heterochromatic transcriptional silencing function that may play a role in TE and gene regulation in ascomycetes. The affected gene underwent multiple full or partial losses within the phylum. Overall, our work establishes a kingdom-wide view of how domains likely derived from TEs contribute to the evolution of protein functions.

evolutionary biology↗

bioRxiv2023

Recurrent chromosome destabilization through repeat-mediated rearrangements in a fungal pathogen

Genomic instability caused by chromosomal rearrangements has severe consequences for organismal fitness and progression of cancerous cell lines. The triggers of destabilized chromosomes remain poorly understood but likely co-locate with fragile sites. Here, we retrace a runaway chromosomal degeneration process observed in a fungal pathogen using telomere-to-telomere assemblies across an experimental progeny. We show that the same fragile sites triggered reproducible, large-scale rearrangements through non-allelic recombination. Across our four-generation progeny, chromosomal rearrangements were accompanied by non-disjunction events leading to aneuploid progeny with up to four chromosomal copies. We identify a specific transposable element family co-locating with fragile sites, likely triggering ongoing repeated chromosomal degeneration. The element has recently been associated with lower virulence of the pathogen and has undergone an expansion of copy numbers across the genome. Chromosome sequences are also targeted by repeat-induced point mutation, a genome defense mechanism actively leading to hypermutation on duplicated sequences. Our work identifies the exact sequence triggers that initiate chromosome instability and perpetuate degenerative cycles. Dissecting proximate causes leading to runaway chromosomal degeneration could expand our understanding of chromosomal evolution beyond fungal pathogens.

genomics↗

bioRxiv2023

Population-level transposable element expression dynamics influence trait evolution in a fungal crop pathogen

Rapid adaptive evolution is driven by strong selection pressure acting on standing genetic variation within populations. How adaptive genetic variation is generated within species and how such variation influences phenotypic trait expression is often not well understood though. Here, we focused on recent activity of transposable elements (TEs) using deep population genomics and transcriptomics analyses of a fungal plant pathogen with a highly active content of TEs in the genome. Zymoseptoria tritici causes one of the most damaging diseases on wheat, with recent adaptation to the host and environment being facilitated by TE-associated mutations. We obtained genomic and RNA-sequencing data from 146 isolates collected from a single wheat field. We established a genome-wide map of TE insertion polymorphisms in the population by analyzing recent TE insertions among individuals. We quantified the locus-specific transcription of individual TEs within the population and revealed considerable variation in transcription across individual TE loci. About 20% of all TE copies show activity in the genome implying that genomic defenses such as repressive epigenetic marks and repeat-induced polymorphisms are ineffective at preventing the proliferation of TEs in the genome. A quarter of recent TE insertions are associated with expression variation of neighboring genes providing broad potential to influence trait expression. We indeed found that TE insertions are likely responsible for variation in virulence on the host and secondary metabolite production. Our study emphasizes how TE-derived polymorphisms segregate even in individual populations and broadly underpin transcription and adaptive trait variation in a species.

genomics↗

bioRxiv2022

Recent transposable element bursts triggered by insertions near genes in a fungal pathogen

The activity of transposable elements (TEs) contributes significantly to genome evolution. TEs often destabilize genome integrity but may also confer adaptive variation in phenotypic traits. De-repression of epigenetically silenced TEs often initiates bursts of transposition activity that may be counteracted by purifying selection and genome defenses. However, how these forces interact to determine the expansion routes of TEs within a species remains largely unknown. Here, we analyzed a set of 19 telomere-to-telomere genomes of the fungal wheat pathogen Zymoseptoria tritici. Phylogenetic reconstruction and ancestral state estimates of individual TE families revealed that TEs have undergone distinct activation and repression periods resulting in highly uneven copy numbers between genomes of the same species. Most TEs are clustered in gene poor niches, indicating strong purifying selection against insertions near coding sequences. TE families with high copy numbers have low sequence divergence and strong signatures of defense mechanisms (i.e., RIP). In contrast, small non-autonomous TEs (i.e., MITEs) are less impacted by defense mechanisms and are often located in close proximity to genes. Individual TE families have experienced multiple distinct burst events that generated many nearly identical copies. We found that a Copia element burst was initiated from recent copies inserted substantially closer to genes compared to older insertions. Overall, TE bursts tended to initiate from copies in GC-rich niches that escaped inactivation by genomic defenses. Our work shows how specific genomic environments features provide triggers for TE proliferation.

genomics↗

bioRxiv2021

The population genetics of adaptation through copy-number variation in a fungal plant pathogen

Microbial pathogens can rapidly adapt to changing environments such as the application of pesticides or host resistance. Copy number variations (CNV) are a major source of adaptive genetic variation for recent adaptation. Here, we analyze how a major fungal pathogen of barley, Rhynchosporium commune, has adapted to host environment, fungicide and temperature challenges. We screen the genomes of 126 isolates sampled across a worldwide set of populations and identify a total of 7879 gene duplications and 116 gene deletions. Most gene duplications result from segmental chromosomal duplications. We find that genes showing recent gains or losses are enriched in functions related to host exploitation (i.e. effectors and cell wall degrading enzymes). We perform a phylogeny-informed genome-wide association study (GWAS) and identify 191 copy-number variants associated with different pathogenesis and temperature related traits, including a large segmental duplication of CYP51A that has contributed to the emergence of azole resistance. Additionally, we use a genome-wide SNP dataset to replicate the GWAS and contrast it with the CNV-focused analysis. We find that frequencies of adaptive CNV alleles show high variation among populations for traits under strong selection such as fungicide resistance. In contrast, adaptive CNV alleles underpinning temperature adaptation tend to be near fixation. Finally, we show that transposable elements are important drivers of recent gene copy-number variation. Loci showing signatures of recent positive selection are enriched in miniature inverted repeat transposons. Our findings show how extensive segmental duplications create the raw material for recent adaptation in global populations of a fungal pathogen.

evolutionary biology↗

bioRxiv2020

The population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen

The activity of transposable elements (TEs) can be an important driver of genetic diversity with TE-mediated mutations having a wide range of fitness consequences. To avoid deleterious effects of TE activity, some fungi evolved highly sophisticated genomic defences to reduce TE proliferation across the genome. Repeat-induced point (RIP) mutations is a fungal-specific TE defence mechanism efficiently targeting duplicated sequences. The rapid accumulation of RIP mutations is expected to deactivate TEs over the course of a few generations. The evolutionary dynamics of TEs at the population level in a species with highly repressive genome defences is poorly understood. Here, we analyze 366 whole-genome sequences of Parastagonospora nodorum, a fungal pathogen of wheat with efficient RIP. A global population genomics analysis revealed high levels of genetic diversity and signs of frequent sexual recombination. Contrary to expectations for a species with RIP, we identified recent TE activity in multiple populations. The TE composition and copy numbers showed little divergence among global populations regardless of the demographic history. Miniature inverted-repeat transposable elements (MITEs) and terminal repeat retrotransposons in miniature (TRIMs) were largely underlying recent intra-species TE expansions. We inferred RIP footprints in individual TE families and found that recently active, high-copy TEs have possibly evaded genomic defences. We find no evidence that recent positive selection acted on TE-mediated mutations rather that purifying selection maintained new TE insertions at low insertion frequencies in populations. Our findings highlight the complex evolutionary equilibria established by the joint action of TE activity, selection and genomic repression. Data SummaryAll Illumina sequence data is available from the NCBI SRA BioProject numbers PRJNA606320, PRJNA398070 and PRJNA476481 (https://www.ncbi.nlm.nih.gov/bioproject). The Methods and Supplementary Figures S1-S11 and Supplementary Tables S1-S4 provide all information on strain locations and outcomes of genome analyses.

genomics↗

bioRxiv2020

A population-level invasion by transposable elements in a fungal pathogen

AO_SCPLOWBSTRACTC_SCPLOWGenome evolution is driven by the activity of transposable elements (TEs). The spread of TEs can have deleterious effects including the destabilization of genome integrity and expansions. However, the precise triggers of genome expansions remain poorly understood because genome size evolution is typically investigated only among deeply divergent lineages. Here, we use a large population genomics dataset of 284 individuals from populations across the globe of Zymoseptoria tritici, a major fungal wheat pathogen. We built a robust map of genome-wide TE insertions and deletions to track a total of 2,456 polymorphic loci within the species. We show that purifying selection substantially depressed TE frequencies in most populations but some rare TEs have recently risen in frequency and likely confer benefits. We found that specific TE families have undergone a substantial genome-wide expansion from the pathogens center of origin to more recently founded populations. The most dramatic increase in TE insertions occurred between a pair of North American populations collected in the same field at an interval of 25 years. We find that both genome-wide counts of TE insertions and genome size have increased with colonization bottlenecks. Hence, the demographic history likely played a major role in shaping genome evolution within the species. We show that both the activation of specific TEs and relaxed purifying selection underpin this incipient expansion of the genome. Our study establishes a model to recapitulate TE-driven genome evolution over deeper evolutionary timescales.

genomics↗

bioRxiv2019

A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici

BackgroundThe gene content of a species largely governs its ecological interactions and adaptive potential. A species is therefore defined by both core genes shared between all individuals and accessory genes segregating presence-absence variation. There is growing evidence that eukaryotes, similar to bacteria, show intra-specific variability in gene content. However, it remains largely unknown how functionally relevant such a pangenome structure is for eukaryotes and what mechanisms underlie the emergence of highly polymorphic genome structures. ResultsHere, we establish a reference-quality pangenome of a fungal pathogen of wheat based on 19 complete genomes from isolates sampled across six continents. Zymoseptoria tritici causes substantial worldwide losses to wheat production due to rapidly evolved tolerance to fungicides and evasion of host resistance. We performed transcriptome-assisted annotations of each genome to construct a global pangenome. Major chromosomal rearrangements are segregating within the species and underlie extensive gene presence-absence variation. Conserved orthogroups account for only [~]60% of the species pangenome. Investigating gene functions, we find that the accessory genome is enriched for pathogenesis-related functions and encodes genes involved in metabolite production, host tissue degradation and manipulation of the immune system. De novo transposon annotation of the 19 complete genomes shows that the highly diverse chromosomal structure is tightly associated with transposable elements content. Furthermore, transposable element expansions likely underlie recent genome expansions within the species. ConclusionsTaken together, our work establishes a highly complex eukaryotic pangenome providing an unprecedented toolbox to study how pangenome structure impacts crop-pathogen interactions.

genomics↗

bioRxiv2019

Complex evolutionary origins of specialized metabolite gene cluster diversity among the plant pathogenic fungi of the Fusarium graminearum species complex

Fungal genomes encode highly organized gene clusters that underlie the production of specialized (or secondary) metabolites. Gene clusters encode key functions to exploit plant hosts or environmental niches. Promiscuous exchange among species and frequent reconfigurations make gene clusters some of the most dynamic elements of fungal genomes. Despite evidence for high diversity in gene cluster content among closely related strains, the microevolutionary processes driving gene cluster gain, loss and neofunctionalization are largely unknown. We analyzed the Fusarium graminearum species complex (FGSC) composed of plant pathogens producing potent mycotoxins and causing Fusarium head blight on cereals. We de novo assembled genomes of previously uncharacterized FGSC members (two strains of F. austroamericanum, F. cortaderiae and F. meridionale). Our analyses of eight species of the FGSC in addition to 15 other Fusarium species identified a pangenome of 54 gene clusters within FGSC. We found that multiple independent losses were a key factor generating extant cluster diversity within the FGSC and the Fusarium genus. We identified a modular gene cluster conserved among distantly related fungi, which was likely reconfigured to encode different functions. We also found strong evidence that a rare cluster in FGSC was gained through an ancient horizontal transfer between bacteria and fungi. Chromosomal rearrangements underlying cluster loss were often complex and were likely facilitated by an enrichment in specific transposable elements. Our findings identify important transitory stages in the birth and death process of specialized metabolism gene clusters among very closely related species.

genomics↗

bioRxiv2019

Stress-driven transposable element de-repression dynamics in a fungal pathogen

Transposable elements (TEs) are drivers of genome evolution and affect the expression landscape of the host genome. Stress is a major factor inducing TE activity, however the regulatory mechanisms underlying de-repression are poorly understood. Key unresolved questions are whether different types of stress differentially induce TE activity and whether different TEs respond differently to the same stress. Plant pathogens are excellent models to dissect the impact of stress on TEs, because lifestyle transitions on and off the host impose exposure to a variety of stress conditions. We analyzed the TE expression landscape of four well-characterized strains of the major wheat pathogen Zymoseptoria tritici. We experimentally exposed strains to nutrient starvation and host infection stress. Contrary to expectations, we show that the two distinct conditions induce the expression of different sets of TEs. In particular, the most highly expressed TEs, including MITE and LTR-Gypsy elements, show highly distinct de-repression across stress conditions. Both the genomic context of TEs and the genetic background stress (i.e. different strains harboring the same TEs) were major predictors of de-repression dynamics under stress. Genomic defenses inducing point mutations in repetitive regions were largely ineffective to prevent TE de-repression. Consistent with TE de-repression being governed by epigenetic effects, we found that gene expression profiles under stress varied significantly depending on the proximity to the closest TEs. The unexpected complexity in TE responsiveness to stress across genetic backgrounds and genomic locations shows that species harbor substantial genetic variation to control TEs.

genomics↗