Transposable elements domestication in Drosophila through chimeric transcripts

Introduction: Transposable elements (TEs) are DNA sequences that can mobilize across genomes and originate genetic variation, which can be deleterious, neutral or beneficial to the organisms. Through events such as domestication they can contribute to genomic evolution by influencing gene expression and producing new gene sequences. Its co-transcription with gene sequences relies on the TE insertion sites, within or nearby genes, producing chimeric transcripts. Although chimeric transcripts are mainly deleterious and neutral, few cases are adaptive, mainly associated to stressfull conditions or in natural populations adapted to different environments. Objectives: We investigated the extension of chimeric transcripts occurrence by analyzing ovary transcriptomes of four D. melanogaster and D. simulans wild-type strains, from Gotheron (France) and São José do Rio Preto (Brazil), two strains of each location, raised under cold-shock and starvation stresses. downloadIn order to investigate possible adaptive polymorphic TE insertions, ChimeraTE, a pipeline able to detect chimeric transcripts in paired-end RNA-seq data was employed. According to the TE insertion site in relation to the gene, each transcript is classified as TE-initiated, TE-exonized and TE-terminated. The differential expression analysis of genes allowed us to identify TE-driven modulation of gene expression oriented by the stresses. Results: Among the experimental conditions we found a total average of 304 and 235 chimeric transcripts in D. melanogaster and D. simulans, respectively, for which ~ 90% were TE-exonized. The DNA transposons of roo, INE-1 and 1360 families were not only the most abundant in the genomes, but also the most frequent in the chimeras. Genes producing chimeric transcripts comprehend only ~1% of all genes in each species, of those 19 in D. melanogaster and 21 in D. simulans were differentially expressed between control and treatments. Regarding potential cases of stress related adaptive insertions, three genes stand out. The gene Paris, which is expressed in one strain of D. melanogaster from Gotheron, has a 2,575 bp TE fragment from Burdock (LTR, Gypsy) inserted in the promoter region. It seems that the TE insertion is responsible for Paris upregulation, since significant change observed in gene expression after cold-shock treatment was exclusive to the chimeric transcript. Sulf1 gene, in the same strain, has a large (3,953 bp) Micropia (LTR, Gypsy) fragment inserted within an intron, and exhibits a significantly higher expression after exposure to both treatments, only regarding the chimeric transcript. Both TE insertions are exclusive to the European strains (temperate region), and absent in D. melanogaster’s public genome, as well as in D. melanogaster strains from Brazil (tropical region). The gene GD24271, in D. simulans, has an upstream 112 bp insertion of G5A (LINE, Jockey), also present in all the other D. simulans genomes, but it is only upregulated in one Gotheron’s strain, where G5A is co-transcribed alongside this gene, after cold-shock exposure. Conclusions: These candidates to adaptive TE insertions, may help us demonstrate how gene-TE chimeric transcripts can modulate stress response and may contribute to both genomic and transcriptomic evolution. Illustrating how stress can induce TE domestication, these results may contribute to a broader understanding of organisms’s adaptation.