Systematic identification of cargo-mobilizing genetic elements reveals new dimensions of eukaryotic diversity

Nucleic Acids Research, Journal Year: 2024, Volume and Issue: 52(10), P. 5496 - 5513

Published: April 15, 2024

Abstract Cargo-mobilizing mobile elements (CMEs) are genetic entities that faithfully transpose diverse protein coding sequences. Although common in bacteria, we know little about eukaryotic CMEs because no appropriate tools exist for their annotation. For example, Starships giant fungal whose functions largely unknown they require time-intensive manual curation. To address this knowledge gap, developed starfish, a computational workflow high-throughput CME We applied starfish to 2 899 genomes of 1 649 species and found recovers known with 95% combined precision recall while expanding the number annotated ten-fold. Extant Starship diversity is partitioned into 11 families differ enrichment patterns across classes. cargo changes rapidly such from same family substantially functional repertoires, which predicted contribute biological processes as metabolism. Many have convergently evolved insert 5S rDNA AT-rich sequence others integrate random locations, revealing both specialist generalist strategies persistence. Our work establishes framework advancing element biology provides means investigate an emerging dimension diversity, within genomes.

Language: Английский

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

mBio, Journal Year: 2024, Volume and Issue: 15(3)

Published: Feb. 13, 2024

ABSTRACT The rapid adaptive evolution of microbes is driven by strong selection pressure acting on genetic variation. How variation generated within species and how such influences phenotypic trait expression often not well understood though. We focused the recent activity transposable elements (TEs) using deep population genomics transcriptomics analyses a fungal plant pathogen with highly active content TEs in genome. Zymoseptoria tritici causes one most damaging diseases wheat, adaptation to host environment being facilitated TE-associated mutations. obtained genomic RNA-sequencing data from 146 isolates collected single wheat field. established genome-wide map TE insertion polymorphisms analyzing insertions among individuals. quantified locus-specific transcription individual copies found considerable at loci population. About 20% all show genome suggesting that defenses as repressive epigenetic marks repeat-induced are least partially ineffective preventing proliferation A quarter associated neighboring genes providing broad potential influence expression. indeed likely responsible for virulence potentially diverse components secondary metabolite production. Our large-scale study emphasizes TE-derived segregate even microbial populations can broadly underpin pathogens. IMPORTANCE Pathogens rapidly adapt new hosts, antimicrobials, or changes environment. Adaptation arises mutations genome; however, remains poorly understood. investigated dynamic regions tritici, major wheat. elements. large proportion only signatures but also variable pathogen. find this influencing many important traits Hence, our work provides insights into over shortest time periods based

Language: Английский

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Analyses of Transposable Elements in Arbuscular Mycorrhizal Fungi Support Evolutionary Parallels With Filamentous Plant Pathogens

Genome Biology and Evolution, Journal Year: 2025, Volume and Issue: 17(3)

Published: March 1, 2025

Abstract Transposable elements are repetitive DNA sequences that excise or create copies inserted elsewhere in the genome. Their expansion shapes genome variability and evolution by impacting gene expression rearrangement rates. Arbuscular mycorrhizal fungi beneficial plant symbionts with large, transposable element-rich genomes, recent findings showed these vary significantly abundance, evolution, regulation among model strains. Here, we aimed to obtain a more comprehensive understanding of element function arbuscular investigating assembled genomes from representatives all known families. We uncovered multiple, family-specific bursts insertions different species, indicating variable past ongoing activity contributing diversification lineages. also found preferentially located within around candidate effectors/secreted proteins, as well proximity promoters. Altogether, support role promoting diversity proteins involved molecular dialogs hosts and, generally, driving regulation. The mechanisms observed prominent bear striking similarities those many filamentous pathogens.

Language: Английский

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Diversification, loss, and virulence gains of the major effector AvrStb6 during continental spread of the wheat pathogen Zymoseptoria tritici

PLoS Pathogens, Journal Year: 2025, Volume and Issue: 21(3), P. e1012983 - e1012983

Published: March 31, 2025

Interactions between plant pathogens and their hosts are highly dynamic mainly driven by pathogen effectors receptors. Host-pathogen co-evolution can cause rapid diversification or loss of genes encoding host-exposed proteins. The molecular mechanisms that underpin such sequence dynamics remains poorly investigated at the scale entire species. Here, we focus on AvrStb6, a major effector global wheat Zymoseptoria tritici, evolving in response to cognate receptor Stb6, resistance widely deployed wheat. We comprehensively captured gene evolution analyzing thousand-genome panel using reference-free analyses. found AvrStb6 has diversified into 59 protein isoforms with strong association spreading new continents. Across Europe, strongest differentiation consistent high rates Stb6 deployment. locus showed also remarkable transposable element content specific expansion patterns across globe. detected losses evidence for element-mediated disruptions. used virulence datasets genome-wide mapping studies predict changes panel. Genomic predictions suggested marked increases cultivars concomitant spread Europe subsequent further Finally, genotyped French bread monitored resistant cultivar deployment evolution. Taken together, our data provides comprehensive view how rapidly diversifying undergo large-scale gains cultivars. analyses highlight need sequencing panels assess durability improve sustainability strategies.

Language: Английский

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Lifestyles shape genome size and gene content in fungal pathogens

Published: April 2, 2025

Fungi display a wide range of lifestyles and hosts. We still know little about the impact lifestyles, including pathogenicity, on their genome architecture. Here, we combined annotated 552 fungal genomes from class Sordariomycetes examined association between 12 genomic features two lifestyle traits: pathogenicity insect association. found that pathogens average tend to have larger number protein-coding genes, effectors, tRNA genes. In addition, non-repetitive size is than non-pathogenic species. However, this pattern not consistent across all groups. Insect endoparasites symbionts smaller sizes genes with longer exons; moreover, insect-vectored possess fewer compared those transmitted by insects. Our study shows are main contributors variation in seemingly similar can exhibit distinct architectures, depending host vector interactions.

Language: Английский

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Lifestyles shape genome size and gene content in fungal pathogens

Published: April 2, 2025

Fungi display a wide range of lifestyles and hosts. We still know little about the impact lifestyles, including pathogenicity, on their genome architecture. Here, we combined annotated 552 fungal genomes from class Sordariomycetes examined association between 12 genomic features two lifestyle traits: pathogenicity insect association. found that pathogens average tend to have larger number protein-coding genes, effectors, tRNA genes. In addition, non-repetitive size is than non-pathogenic species. However, this pattern not consistent across all groups. Insect endoparasites symbionts smaller sizes genes with longer exons; moreover, insect-vectored possess fewer compared those transmitted by insects. Our study shows are main contributors variation in seemingly similar can exhibit distinct architectures, depending host vector interactions.

Language: Английский

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Recombination and transposition drive genomic structural variation potentially impacting life history traits in a host-generalist fungal plant pathogen

BMC Biology, Journal Year: 2025, Volume and Issue: 23(1)

Published: April 27, 2025

Abstract Background An understanding of plant pathogen evolution is important for sustainable management crop diseases. Plant populations must maintain adequate heritable phenotypic variability to survive. Polymorphisms ≥ 50 bp, known as structural variants (SVs), could contribute strongly this by disrupting gene activities. SV acquisition largely driven mobile genetic elements called transposons, though a less appreciated source SVs erroneous meiotic double-strand break repair. The relative impacts transposons and recombination on diversity the overall contribution elusive, especially in host generalists. Results We use 25 high-quality genomes create graphical pan-genome globally distributed host-generalist Sclerotinia sclerotiorum . Outcrossing rates self-fertile species have been debated. Using bisulfite sequencing short-read data from 190 strains, we show that S. has many hallmarks eukaryotic meiosis, including hot cold spots, centromeric genic suppression, rapid linkage disequilibrium decay. new statistic captures average pairwise variation, make distinct contributions diversity. Furthermore, despite only 5% genes being dispensable, often had stronger impact than other across 14 life history traits measured 103 strains. Conclusions Transposons Despite limited content diversity, may variability. This sheds light genomic forces shaping adaptive flexibility

Language: Английский

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Integrated Disease Management, Adaptation and Genomics of Fungal Plant Pathogens in Cropping Systems

Plant Pathology, Journal Year: 2025, Volume and Issue: unknown

Published: May 12, 2025

ABSTRACT Crop production systems contribute significantly to maintaining global food security. These often involve the cultivation of single cultivars in highly homogenised environments meet demands. Agriculturally important plant fungal pathogens can be destructive constraints such systems. Integrated disease management strategies comprising tactical use cultural, chemical and host genetic controls are deployed reduce impact pathogens. The homogenous nature these cropping combined with evolutionary forces on often‐flexible genome increases potential for rapid adaptation current integrated practices. This review explores genomic features (such as transposable elements copy number variation) that influence pathogen populations Furthermore, interactions between drive discussed relative three major components agricultural specifies need a cohesive analysis within maintain sustainable face future evolution.

Language: Английский

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Recent reactivation of a pathogenicity-associated transposable element is associated with major chromosomal rearrangements in a fungal wheat pathogen

Nucleic Acids Research, Journal Year: 2023, Volume and Issue: 52(3), P. 1226 - 1242

Published: Dec. 24, 2023

Abstract Transposable elements (TEs) are key drivers of genomic variation contributing to recent adaptation in most species. Yet, the evolutionary origins and insertion dynamics within species remain poorly understood. We recapitulate spread pathogenicity-associated Styx element across five that last diverged ∼11 000 years ago. show likely originated Zymoseptoria fungal pathogen genus underwent multiple independent reactivation events. Using a global 900-genome panel wheat tritici, we assess copy number identify renewed transposition activity Oceania South America. can mobilize create additional copies four-generation pedigree. Importantly, find new not affected by defenses suggesting minimal control against element. preferentially located recombination breakpoints triggered types large chromosomal rearrangements. Taken together, establish origin, diversification highly active TE with major consequences for integrity expression disease.

Language: Английский

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Strain-specific evolution and host-specific regulation of transposable elements in the model plant symbiont Rhizophagus irregularis

G3 Genes Genomes Genetics, Journal Year: 2024, Volume and Issue: 14(5)

Published: March 20, 2024

Abstract Transposable elements (TEs) are repetitive DNA that can create genome structure and regulation variability. The of Rhizophagus irregularis, a widely studied arbuscular mycorrhizal fungus (AMF), comprises ∼50% sequences include TEs. Despite their abundance, two-thirds TEs remain unclassified, among AMF life stages remains unknown. Here, we aimed to improve our understanding TE diversity in this model species by curating repeat datasets obtained from chromosome-level assemblies investigating expression across multiple conditions. Our analyses uncovered new superfamilies families symbiont revealed significant differences how these evolve both within between R. irregularis strains. With curated annotation, also found the number upregulated colonized roots is 4 times higher than extraradical mycelium, overall differs depending on plant host. This work provides fine-scale view evolution symbionts highlights transcriptional dynamism specificity during host–microbe interactions. We provide Hidden Markov Model profiles domains for future manual curation uncharacterized (https://github.com/jordana-olive/TE-manual-curation/tree/main).

Language: Английский

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