Population-scale long-read sequencing uncovers transposable elements associated with gene expression variation and adaptive signatures in Drosophila

Abstract

High quality reference genomes are crucial to understanding genome function, structure and evolution. The availability of reference genomes has allowed us to start inferring the role of genetic variation in biology, disease, and biodiversity conservation. However, analyses across organisms demonstrate that a single reference genome is not enough to capture the global genetic diversity present in populations. In this work, we generate 32 high-quality reference genomes for the well-known model species D. melanogaster and focus on the identification and analysis of transposable element variation as they are the most common type of structural variant. We show that integrating the genetic variation across natural populations from five climatic regions increases the number of detected insertions by 58%. Moreover, 26% to 57% of the insertions identified using long-reads were missed by short-reads methods. We also identify hundreds of transposable elements associated with gene expression variation and new TE variants likely to contribute to adaptive evolution in this species. Our results highlight the importance of incorporating the genetic variation present in natural populations to genomic studies, which is essential if we are to understand how genomes function and evolve.

Species-specific chromatin landscape determines how transposable elements shape genome evolution

“…Comparing the expression of homologous alleles with and without TEs showing epigenetic effects also reached the same conclusion ( Figure 3C ). These observations echo previously reported lack of genome-wide associations between TE-induced enrichment of repressive epigenetic marks and the expression of neighboring genes in several model organisms ( Quadrana et al, 2016 ; Stuart et al, 2016 ; Lee and Karpen, 2017 ; Choi and Purugganan, 2018 ) and are consistent with the wider observation that TEs upstream or downstream to genes are not predominantly associated with reduced gene expression ( Goubert et al, 2020 ; Ullastres et al, 2021 ; Rech et al, 2022 , reviewed in Kelleher et al, 2020 ; Choi and Lee, 2020 ). The limited impacts of TE-mediated H3K9me2 enrichment on gene expression could have resulted from the complex relationship between repressive epigenetic modification and gene expression ( de Wit et al, 2007 ; Yasuhara and Wakimoto, 2008 ; Riddle et al, 2011 ; Meng et al, 2016 ; Caizzi et al, 2016 ), the varying sensitivity of genes to the enrichment of repressive marks ( Rudolph et al, 2007 ; Vogel et al, 2009 ; Riddle et al, 2011 ), and the presence of other types of variants that also modulate gene expression ( Stranger et al, 2007 ).…”

Rates and spectra of de novo structural mutation in Chlamydomonas reinhardtii

“…Furthermore, although certain TE families exhibited insertion biases for introns ( Chlamys PLEs) or intergenic sequence far from genes ( EnSpm DD(E/D) transposons), overall TEs exhibited a bias towards 5’ UTRs and gene proximal intergenic regions, as has been observed for various other TEs (Zhang et al 2020). Gene proximal TE insertions can have important effects on gene expression, for example via the disruption of regulatory sequences, regional effects of transcriptional silencing, or the deposition of new regulatory elements by the TE (Cridland et al 2015; Uzunović et al 2019; Rech et al 2022). The breakpoints of chromosomal rearrangements (inversions and translocations) also had a similar genomic distribution to that of TEs, due to their association.…”

The Role of Transposable Elements in Sexual Development

“…On top of the molecular functions of TEs, researchers are interested in how these molecular functions translate to the organismal level. In a recent study using natural populations of Drosophila melanogaster from five climatic regions, TEs were shown to be a likely contributor to an adaptation to the environment across evolution (Rech et al, 2022). This role Hermant and Torres-Padilla, 2021;Senft and Macfarlan, 2021;Almeida et al, 2022;Fueyo et al, 2022).…”

“…On top of the molecular functions of TEs, researchers are interested in how these molecular functions translate to the organismal level. In a recent study using natural populations of Drosophila melanogaster from five climatic regions, TEs were shown to be a likely contributor to an adaptation to the environment across evolution ( Rech et al, 2022 ). This role in helping the species adapt to environmental conditions was similarly discovered for fish diadromy, which is the migration between freshwater and the sea, in a study that investigated genomes of 24 fish species ( Carotti et al, 2021 ).…”