Unraveling the features of somatic transposition in the Drosophila intestine

• Published in: The EMBO journal Vol. 40; no. 9; pp. e106388 - n/a
• Main Authors: Siudeja, Katarzyna, van den Beek, Marius, Riddiford, Nick, Boumard, Benjamin, Wurmser, Annabelle, Stefanutti, Marine, Lameiras, Sonia, Bardin, Allison J
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 03.05.2021; Springer Nature B.V; EMBO Press; John Wiley and Sons Inc
• Subjects: Animals; Chromatin; Clonal Evolution; Deoxyribonucleic acid; Digestive system; DNA; DNA sequencing; DNA Transposable Elements; Drosophila; Drosophila melanogaster - genetics; Drosophila midgut; Drosophila Proteins - genetics; EMBO09; EMBO11; Female; Fruit flies; Gastrointestinal tract; Gene expression; Gene Expression Profiling; Gene Silencing; Genetic diversity; Genomes; Inactivation; Insects; Intestinal Neoplasms - genetics; Intestine; Life Sciences; Male; Midgut; Mobility; Organ Specificity; Receptors, Notch - genetics; Recombination, Genetic; Retrotransposition; Ribonucleic acid; RNA; Sequence Analysis, RNA - methods; Somatic cells; somatic genome; Stem cells; Tissues; Transcription; Transcriptomics; transposable elements; Transposition; Transposons; Tumor suppressor genes; Tumors; Whole Genome Sequencing; midgut; transposable elements; somatic genome; Drosophila midgut; Development; Transcription & Genomics; transposable elements Subject Categories Chromatin
• ISSN: 0261-4189; 1460-2075; 1460-2075
• DOI: 10.15252/embj.2020106388

Transposable elements (TEs) play a significant role in evolution, contributing to genetic variation. However, TE mobilization in somatic cells is not well understood. Here, we address the prevalence of transposition in a somatic tissue, exploiting the Drosophila midgut as a model. Using whole‐genome sequencing of in vivo clonally expanded gut tissue, we have mapped hundreds of high‐confidence somatic TE integration sites genome‐wide. We show that somatic retrotransposon insertions are associated with inactivation of the tumor suppressor Notch , likely contributing to neoplasia formation. Moreover, applying Oxford Nanopore long‐read sequencing technology we provide evidence for tissue‐specific differences in retrotransposition. Comparing somatic TE insertional activity with transcriptomic and small RNA sequencing data, we demonstrate that transposon mobility cannot be simply predicted by whole tissue TE expression levels or by small RNA pathway activity. Finally, we reveal that somatic TE insertions in the adult fly intestine are enriched in genic regions and in transcriptionally active chromatin. Together, our findings provide clear evidence of ongoing somatic transposition in Drosophila and delineate previously unknown features underlying somatic TE mobility in vivo . SYNOPSIS Technical challenges with detecting somatic transposable element (TE) insertions have hampered determination of the extent of somatic transposition in adult tissues. The current study provides genomic evidence for endogenous retrotransposition events in the Drosophila intestine and uncovers underlying features of somatic TE mobility in vivo . A combination of short‐read and long‐read DNA sequencing reveals tissue‐specific differences in genome‐wide retrotransposon mobility. Somatic TE insertions in the gut are enriched in genic regions, as well as in active, enhancer‐like chromatin. TE insertions in the tumor suppressor gene Notch in intestinal stem cells may contribute to the formation of gut neoplasia. Graphical Abstract A combination of short‐read and long‐read DNA sequencing reveals tissue‐specific differences in genome‐wide retrotransposon mobility.