scholarly journals A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Ursula Oggenfuss ◽  
Thomas Badet ◽  
Thomas Wicker ◽  
Fanny E Hartmann ◽  
Nikhil Kumar Singh ◽  
...  

Genome 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 2456 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 pathogen’s 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.

Author(s):  
Ursula Oggenfuss ◽  
Thomas Badet ◽  
Thomas Wicker ◽  
Fanny E. Hartmann ◽  
Nikhil K. Singh ◽  
...  

AbstractTransposable elements (TEs) are key drivers of adaptive evolution within species. Yet, the propagation of TEs across the genome can be highly deleterious and ultimately lead to genome expansions. Hence, TE activity is likely under complex selection regimes within species. To address this, we analyzed a large whole-genome sequencing dataset of the fungal wheat pathogen Zymoseptoria tritici harboring TE-mediated adaptations to overcome host defenses and fungicides. We built a robust map of genome-wide TE insertion and deletion loci for six populations and 284 fungal individuals across the world. We identified a total of 2’456 unfixed TE loci within the species and a significant excess of rare insertions indicating strong purifying selection. A subset of TEs recently swept to near complete fixation with at least one locus likely contributing to higher levels of fungicide resistance. TE-driven adaptation was also supported by evidence for selective sweeps. In parallel, we identified a substantial genome-wide expansion of TE families from the pathogen’s center of origin to more recently founded populations, suggesting that population bottlenecks played a major role in shaping TE content of the genome. The most dramatic expansion occurred among a pair of North American populations collected in the same field at an interval of 25 years. We show that both the activation of specific TEs and relaxed purifying selection likely underpin the expansion. Our study disentangles the effects of selection and TE bursts leading to intra-specific genome expansions, providing a model to recapitulate TE-driven genome evolution over deeper evolutionary timescales.


2020 ◽  
Author(s):  
Danilo Pereira ◽  
Ursula Oggenfuss ◽  
Bruce A. McDonald ◽  
Daniel Croll

AbstractThe 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.


2021 ◽  
Vol 7 (8) ◽  
Author(s):  
Danilo Pereira ◽  
Ursula Oggenfuss ◽  
Bruce A. McDonald ◽  
Daniel Croll

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 have evolved highly sophisticated genomic defences to reduce TE proliferation across the genome. Repeat-induced point mutation (RIP) is a fungal-specific TE defence mechanism efficiently targeting duplicated sequences. The rapid accumulation of RIPs 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 analyse 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.


2021 ◽  
pp. gr.275658.121
Author(s):  
Yuyun Zhang ◽  
Zijuan Li ◽  
Yu'e Zhang ◽  
Kande Lin ◽  
Yuan Peng ◽  
...  

More than 80% of the wheat genome consists of transposable elements (TEs), which act as one major driver of wheat genome evolution. However, their contributions to the regulatory evolution of wheat adaptations remain largely unclear. Here, we created genome-binding maps for 53 transcription factors (TFs) underlying environmental responses by leveraging DAP-seq in Triticum urartu, together with epigenomic profiles. Most TF-binding sites (TFBS) located distally from genes are embedded in TEs, whose functional relevance is supported by purifying selection and active epigenomic features. About 24% of the non-TE TFBS share significantly high sequence similarity with TE-embedded TFBS. These non-TE TFBS have almost no homologous sequences in non-Triticeae species and are potentially derived from Triticeae-specific TEs. The expansion of TE-derived TFBS linked to wheat-specific gene responses, suggesting TEs are an important driving force for regulatory innovations. Altogether, TEs have been significantly and continuously shaping regulatory networks related to wheat genome evolution and adaptation.


2019 ◽  
Author(s):  
Grazyella M. Yoshida ◽  
Agustín Barria ◽  
Katharina Correa ◽  
Giovanna Cáceres ◽  
Ana Jedlicki ◽  
...  

AbstractNile tilapia (Oreochromis niloticus) is one of the most produced farmed fish in the world and represents an important source of protein for human consumption. Farmed Nile tilapia populations are increasingly based on genetically improved stocks, which have been established from admixed populations. To date, there is scarce information about the population genomics of farmed Nile tilapia, assessed by dense single nucleotide polymorphism (SNP) panels. The patterns of linkage disequilibrium (LD) may affect the success of genome-wide association studies (GWAS) and genomic selection and can also provide key information about demographic history of farmed Nile tilapia populations. The objectives of this study were to provide further knowledge about the population structure and LD patterns, as well as, estimate the effective population size (Ne) for three farmed Nile tilapia populations, one from Brazil (POP A) and two from Costa Rica (POP B and POP C). A total of 55, 56 and 57 individuals from POP A, POP B and POP C, respectively, were genotyped using a 50K SNP panel selected from a whole-genome sequencing (WGS) experiment. Two principal components explained about 20% of the total variation and clearly discriminated between the three populations. Population genetic structure analysis showed evidence of admixture, especially for POP C. The contemporary Ne values calculated based to LD values, ranged from 71 to 141. No differences were observed in the LD decay among populations, with a rapid decrease of r2 when increasing inter-marker distance. Average r2 between adjacent SNP pairs ranged from 0.03 to 0.18, 0.03 to 0.17 and 0.03 to 0.16 for POP A, POP B and POP C, respectively. Based on the number of independent chromosome segments in the Nile tilapia genome, at least 4.2 K SNP are required for the implementation of GWAS and genomic selection in farmed Nile tilapia populations.


Insects ◽  
2021 ◽  
Vol 12 (9) ◽  
pp. 837
Author(s):  
Muhammad Majid ◽  
Huang Yuan

Transposable elements (TEs) play a significant role in both eukaryotes and prokaryotes genome size evolution, structural changes, duplication, and functional variabilities. However, the large number of different repetitive DNA has hindered the process of assembling reference genomes, and the genus level TEs diversification of the grasshopper massive genomes is still under investigation. The genus Calliptamus diverged from Peripolus around 17 mya and its species divergence dated back about 8.5 mya, but their genome size shows rather large differences. Here, we used low-coverage Illumina unassembled short reads to investigate the effects of evolutionary dynamics of satDNAs and TEs on genome size variations. The Repeatexplorer2 analysis with 0.5X data resulted in 52%, 56%, and 55% as repetitive elements in the genomes of Calliptamus barbarus, Calliptamus italicus, and Calliptamus abbreviatus, respectively. The LINE and Ty3-gypsy LTR retrotransposons and TcMar-Tc1 dominated the repeatomes of all genomes, accounting for 16–35% of the total genomes of these species. Comparative analysis unveiled that most of the transposable elements (TEs) except satDNAs were highly conserved across three genomes in the genus Calliptamus grasshoppers. Out of a total of 20 satDNA families, 17 satDNA families were commonly shared with minor variations in abundance and divergence between three genomes, and 3 were Calliptamus barbarus specific. Our findings suggest that there is a significant amplification or contraction of satDNAs at genus phylogeny which is the main cause that made genome size different.


2019 ◽  
Author(s):  
Braham Dhillon ◽  
Gert H. J. Kema ◽  
Richard Hamelin ◽  
Burt H. Bluhm ◽  
Stephen B. Goodwin

AbstractBackgroundTransposable elements (TEs) can be key drivers of evolution, but the mechanisms and scope of how they impact gene and genome function are largely unknown. Previous analyses revealed that TE-mediated gene amplifications can have variable effects on fungal genomes, from inactivation of function to production of multiple active copies. For example, a DNA methyltransferase gene in the wheat pathogen Zymoseptoria tritici (synonym Mycosphaerella graminicola) was amplified to tens of copies, all of which were inactivated by Repeat-Induced Point mutation (RIP) including the original, resulting in loss of cytosine methylation. In another wheat pathogen, Pyrenophora tritici-repentis, a histone H3 gene was amplified to tens of copies with little evidence of RIP, leading to many potentially active copies. To further test the effects of transposon-aided gene amplifications on genome evolution and architecture, the repetitive fraction of the significantly expanded Pseudocercospora fijiensis genome was analyzed in greater detail.ResultsThese analyses identified a housekeeping gene, histone H3, which was captured and amplified to hundreds of copies by a hAT DNA transposon, all of which were inactivated by RIP, except for the original. In P. fijiensis the original H3 gene probably was not protected from RIP, but most likely was maintained intact due to strong purifying selection. Comparative analyses revealed that a similar event occurred in five additional genomes representing the fungal genera Cercospora, Pseudocercospora and Sphaerulina.ConclusionsThese results indicate that the interplay of TEs and RIP can result in different and unpredictable fates of amplified genes, with variable effects on gene and genome evolution.


2018 ◽  
Vol 2 (4) ◽  
pp. 595-605 ◽  
Author(s):  
Siri Kellner ◽  
Anja Spang ◽  
Pierre Offre ◽  
Gergely J. Szöllősi ◽  
Celine Petitjean ◽  
...  

What determines variation in genome size, gene content and genetic diversity at the broadest scales across the tree of life? Much of the existing work contrasts eukaryotes with prokaryotes, the latter represented mainly by Bacteria. But any general theory of genome evolution must also account for the Archaea, a diverse and ecologically important group of prokaryotes that represent one of the primary domains of cellular life. Here, we survey the extant diversity of Bacteria and Archaea, and ask whether the general principles of genome evolution deduced from the study of Bacteria and eukaryotes also apply to the archaeal domain. Although Bacteria and Archaea share a common prokaryotic genome architecture, the extant diversity of Bacteria appears to be much higher than that of Archaea. Compared with Archaea, Bacteria also show much greater genome-level specialisation to specific ecological niches, including parasitism and endosymbiosis. The reasons for these differences in long-term diversification rates are unclear, but might be related to fundamental differences in informational processing machineries and cell biological features that may favour archaeal diversification in harsher or more energy-limited environments. Finally, phylogenomic analyses suggest that the first Archaea were anaerobic autotrophs that evolved on the early Earth.


2012 ◽  
Vol 2012 ◽  
pp. 1-6 ◽  
Author(s):  
J. Gordon Burleigh ◽  
W. Brad Barbazuk ◽  
John M. Davis ◽  
Alison M. Morse ◽  
Pamela S. Soltis

Gymnosperms, comprising cycads, Ginkgo, Gnetales, and conifers, represent one of the major groups of extant seed plants. Yet compared to angiosperms, little is known about the patterns of diversification and genome evolution in gymnosperms. We assembled a phylogenetic supermatrix containing over 4.5 million nucleotides from 739 gymnosperm taxa. Although 93.6% of the cells in the supermatrix are empty, the data reveal many strongly supported nodes that are generally consistent with previous phylogenetic analyses, including weak support for Gnetales sister to Pinaceae. A lineage through time plot suggests elevated rates of diversification within the last 100 million years, and there is evidence of shifts in diversification rates in several clades within cycads and conifers. A likelihood-based analysis of the evolution of genome size in 165 gymnosperms finds evidence for heterogeneous rates of genome size evolution due to an elevated rate in Pinus.


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