A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen
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Evaluation Summary:
This study is of potential interest to a broad audience on evolutionary and population genomics, particularly scientists studying genome dynamics, including transposable elements (TE) and their evolution. It takes advantage of genomics datasets from a large population of wheat pathogens collected across the globe at different times (decades) to detect ongoing processes of genome expansion and potential selection mediated by TE insertions. The work provides empirical evidence that drastic demographic processes shape TE dynamics in nature and that these contribute to intraspecific variation in genome sizes, recapitulating the well-stablished association between TE content and genome size observed across the diversity of life forms.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1, Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)
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Abstract
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.
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Reviewer #3 (Public Review):
The manuscript of Oggenfuss et al presents a comprehensive analysis of TE insertion polymorphisms detected in the genome of ~300 isolates of the wheat fungus Zymoseptoria tritici. The article shows that numerous TE families generated thousands of polymorphic insertions and the authors propose that some of these insertions might potentially be linked to adaptation. They identified a recent burst of transposition in a rapidly expanding population, providing empirical evidence that drastic demographic process shape TE dynamics in nature. Last, they show that intra-specific variation in genome size can be accounted by variation in the number of polymorphic TE insertions, which recapitulate the well stablished association between TE content and genome size variation observed across the diversity of life forms.
The…
Reviewer #3 (Public Review):
The manuscript of Oggenfuss et al presents a comprehensive analysis of TE insertion polymorphisms detected in the genome of ~300 isolates of the wheat fungus Zymoseptoria tritici. The article shows that numerous TE families generated thousands of polymorphic insertions and the authors propose that some of these insertions might potentially be linked to adaptation. They identified a recent burst of transposition in a rapidly expanding population, providing empirical evidence that drastic demographic process shape TE dynamics in nature. Last, they show that intra-specific variation in genome size can be accounted by variation in the number of polymorphic TE insertions, which recapitulate the well stablished association between TE content and genome size variation observed across the diversity of life forms.
The article is well written, present novel as well as relevant results, and provide insights to our understanding of the role of TEs in microevolutionary processes. In addition, it provides an important amount of population genomic data that will serve as a resource. Thus, this manuscript is of potential interest to a broad audience on evolutionary and population genomics.
My major concern is the lack of strong evidence supporting positive selection and/or functional relevance of the TE insertions detected. In particular, the selective sweep scans performed ignored other types of variants (such as SNPs and INDELs), preventing the identification of the actual targets of natural selection.
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Reviewer #2 (Public Review):
Transposable elements (TEs) have been shown to play an important role in genome evolution, in shaping genomic organization, structure, and genome size. The importance of TEs in evolutionary processes such as adaptation, has been rather limited so far. Here, Oggenfuss et al. used intraspecies data from six global populations of the wheat pathogen Zymoseptoria tritici to study the process of TE insertion dynamics, to detect candidate adaptive regions associated with TE insertions, and to show that TE expansion has driven to genome size of some populations in about 25 years. Using publicly available short read sequencing, as well as newly sequenced populations, they created a pipeline to specifically identify TE insertions, then used TE frequency insertions to infer patterns of selection, which they hypothesize …
Reviewer #2 (Public Review):
Transposable elements (TEs) have been shown to play an important role in genome evolution, in shaping genomic organization, structure, and genome size. The importance of TEs in evolutionary processes such as adaptation, has been rather limited so far. Here, Oggenfuss et al. used intraspecies data from six global populations of the wheat pathogen Zymoseptoria tritici to study the process of TE insertion dynamics, to detect candidate adaptive regions associated with TE insertions, and to show that TE expansion has driven to genome size of some populations in about 25 years. Using publicly available short read sequencing, as well as newly sequenced populations, they created a pipeline to specifically identify TE insertions, then used TE frequency insertions to infer patterns of selection, which they hypothesize is under strong purifying selection for regions into genes. They further tried to detect evidence for positive selection at loci associated with adaptation to new environment or resistance to fungicide, and finally contrasted the TE expansion in a window of 25 years to show that two populations have increased their genome size due to TE expansion.
Strengths:
The dataset used in this study with different global populations at different time makes the authors in an ideal position to detect TE expansion in a short timeframe of 25 years. While it has been shown in multiple eukaryotic genomes that TEs contribute substantially to variation in genome size, the evidence provided in this paper is compelling and shows that it is unlikely due to genome duplication events.
The pipeline to identify TE insertions from short read sequencing provides a well detailed path to apply in other genomes, and provide logical reasoning detecting TEs absent from the reference or absent from the isolates but present in the reference. Providing validation for some of the steps would be desired if well-known regions can be used.
The authors explored the interesting perspective of identifying TEs under positive selection by focusing on loci with increased frequency in specific populations. They also added a level of functional validation to better understand specific TE insertions under selection, which is often not included. They identified three loci that did confer resistance to fungicide according to their assay. These results would benefit from additional key details in the methods and the rationale behind the choice of loci in order to fully measure the impact of this finding.
Weaknesses:
While the paper does have strengths in principle to study the evolution of TE dynamics, the weaknesses of the paper reside in the fact that the manuscript in its current form does not directly support the key conclusions presented here. Additional analyses would be required to support them. Such as :
The presence of a large percentage insertions being singleton TEs coupled with low frequency (based on an arbitrary cutoff) is used to conclude strong purifying selection is acting on these new insertions. The authors should have included evidence to convince the reader the presence of a TE in one isolate is not a case of false positive. Additional analyses such as a subset of the singleton TEs to corroborate these single loci or plotting the relationship between how many isolate with one insertion were found and read depth could be informative. Also, understanding the singleton in the context of chromosome locations (core and accessory) could help reinforce the evidence of purifying selection.
The author's conclusion of relaxed selection in accessory chromosomes and between populations are mainly based on TE density. This conclusion may be better supported by adding quantified information of the relationship between the numbers and the type of TE insertions and genomic features such as recombination, which is often found to be negatively associated with TE content. Showing the recombination rate between the chromosomes (core, accessory) would help strengthen the argument that selection acts more strongly in regions of high recombination. To make their conclusion more robust, the authors could have included information about the recombination landscape.
Overall, the authors should have provided the adequate statistical analyses to support many of the insertion frequencies that are often only mentioned qualitatively (e.g. "less than expected") without having the quantitative test. Also, the contrast between low TE insertion frequencies versus high frequency is used without providing details about what is expected, either supported by the literature or by more detailed analyses. Arbitrary threshold can be prone to give artifact results.
Context : This article comes with a number of recent papers exploiting the population genomics dataset of the major wheat pathogen Zymoseptoria tritici (Fouché et al 2020, Krishnan et al. 2018) to show that TE-mediated insertions have in part helped to colonize host plants and tolerate environmental stress. Here, the authors build upon this knowledge to attempt at characterizing the process of TE insertion dynamics, detect signatures of adaptive evolution and changes in genome size at the population level.
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Reviewer #1 (Public Review):
The field of genome dynamics is currently very hot and adaptive transposable elements insertions polymorphisms (TIPS) in wild populations are extensively looked for. Here Oggenfuss et al provide evidence that TE activity within a fungus species can vary drastically (1) in different regions of the world and (2) in the same region within a relatively short timeframe (25 years). The data are properly described and both the figures and text are clear. The authors provide examples of candidate TIPS that could adaptive.
Important findings:
- A repertoire of TIPS is provided for 284 genomes. A PCA analysis show that a small number of TIPS can better differentiate two samplings 25 years apart on the same area than the same number of SNPs.
- Increase in TE content is associated with genome size, between areas and within a …
Reviewer #1 (Public Review):
The field of genome dynamics is currently very hot and adaptive transposable elements insertions polymorphisms (TIPS) in wild populations are extensively looked for. Here Oggenfuss et al provide evidence that TE activity within a fungus species can vary drastically (1) in different regions of the world and (2) in the same region within a relatively short timeframe (25 years). The data are properly described and both the figures and text are clear. The authors provide examples of candidate TIPS that could adaptive.
Important findings:
- A repertoire of TIPS is provided for 284 genomes. A PCA analysis show that a small number of TIPS can better differentiate two samplings 25 years apart on the same area than the same number of SNPs.
- Increase in TE content is associated with genome size, between areas and within a single area 25 years apart.
- Interesting candidates for adaptative TIPS are provided and discussed.
Limitations:
- The TIPS (or a subset of them) are not validated using another technique.
- The relative expression of the adaptive TIPS is not investigated in this manuscript.
- For genomicists not familiar with fungal genomes the distinction between core chromosomes and accessories chromosomes might be difficult to appreciate.
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Evaluation Summary:
This study is of potential interest to a broad audience on evolutionary and population genomics, particularly scientists studying genome dynamics, including transposable elements (TE) and their evolution. It takes advantage of genomics datasets from a large population of wheat pathogens collected across the globe at different times (decades) to detect ongoing processes of genome expansion and potential selection mediated by TE insertions. The work provides empirical evidence that drastic demographic processes shape TE dynamics in nature and that these contribute to intraspecific variation in genome sizes, recapitulating the well-stablished association between TE content and genome size observed across the diversity of life forms.
(This preprint has been reviewed by eLife. We include the public reviews from the …
Evaluation Summary:
This study is of potential interest to a broad audience on evolutionary and population genomics, particularly scientists studying genome dynamics, including transposable elements (TE) and their evolution. It takes advantage of genomics datasets from a large population of wheat pathogens collected across the globe at different times (decades) to detect ongoing processes of genome expansion and potential selection mediated by TE insertions. The work provides empirical evidence that drastic demographic processes shape TE dynamics in nature and that these contribute to intraspecific variation in genome sizes, recapitulating the well-stablished association between TE content and genome size observed across the diversity of life forms.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1, Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)
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