Transposon expression in the Drosophila brain is driven by neighbouring genes and diversifies the neural transcriptome

Abstract

Somatic transposition in neural tissue could contribute to neuropathology and individuality, but its prevalence is debated. We used single-cell mRNA sequencing to map transposon expression in the Drosophila midbrain. We found that neural transposon expression is driven by cellular genes. Every expressed transposon is resident in at least one cellular gene with a matching expression pattern. A new long-read RNA sequencing approach revealed that coexpression is a physical link in the form of abundant chimeric transposon-gene mRNAs. We identified 148 genes where transposons introduce cryptic splice sites into the nascent transcript and thereby produce many additional mRNAs. Some genes exclusively produce chimeric mRNAs with transposon sequence and on average transposon-gene chimeras account for 20% of the mRNAs produced from a given gene. Transposons therefore significantly expand the neural transcriptome. We propose that chimeric mRNAs produced by splicing into polymorphic transposons may contribute to functional differences between individual cells and animals.