A transposon expression burst accompanies the activation of Y-chromosome fertility genes during Drosophila spermatogenesis

Matthew A Lawlor,Weihuan Cao,Christopher E Ellison

doi:10.1038/s41467-021-27136-4

Matthew A Lawlor, Weihuan Cao + Show 1 more

Open Access

https://doi.org/10.1038/s41467-021-27136-4

Copy DOI

Abstract

Transposable elements (TEs) must replicate in germline cells to pass novel insertions to offspring. In Drosophila melanogaster ovaries, TEs can exploit specific developmental windows of opportunity to evade host silencing and increase their copy numbers. However, TE activity and host silencing in the distinct cell types of Drosophila testis are not well understood. Here, we reanalyze publicly available single-cell RNA-seq datasets to quantify TE expression in the distinct cell types of the Drosophila testis. We develop a method for identification of TE and host gene expression modules and find that a distinct population of early spermatocytes expresses a large number of TEs at much higher levels than other germline and somatic components of the testes. This burst of TE expression coincides with the activation of Y chromosome fertility factors and spermatocyte-specific transcriptional regulators, as well as downregulation of many components of the piRNA pathway. The TEs expressed by this cell population are specifically enriched on the Y chromosome and depleted on the X chromosome, relative to other active TEs. These data suggest that some TEs may achieve high insertional activity in males by exploiting a window of opportunity for mobilization created by the activation of spermatocyte-specific and Y chromosome-specific transcriptional programs.

Highlights

Transposable elements (TEs) must replicate in germline cells to pass novel insertions to offspring
We visualized cell-type-specific expression patterns of all TEs with at least three unique molecular identifier (UMI) detected across all individual cells in the Drosophila testis (Fig. 2a)
We used two approaches to determine whether this phenomenon was affecting our estimates of TE expression: (1) we explicitly searched for chimeric RNA-seq reads, where part of the read aligned to a TE and another part aligned to a host gene, and (2) we examined RNA-seq read coverage along the TE consensus sequence

Summary

Introduction

Transposable elements (TEs) must replicate in germline cells to pass novel insertions to offspring. We develop a method for identification of TE and host gene expression modules and find that a distinct population of early spermatocytes expresses a large number of TEs at much higher levels than other germline and somatic components of the testes. This burst of TE expression coincides with the activation of Y chromosome fertility factors and spermatocyte-specific transcriptional regulators, as well as downregulation of many components of the piRNA pathway. Our method for identification of TE and host gene co-expression modules shows that a subset of primary spermatocytes expresses a diverse group of TEs at high levels relative to other cell types

Methods

Results

Conclusion