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Promoter activity profiling throughout the Drosophila life cycle reveals role of transposons in regulatory innovation

ABSTRACT: Since their discovery, transposable elements have been proposed to play a central role in the evolution of their host genomes through their ability to regulate gene expression, in particular by providing transcription start sites (TSSs) for host genes. To investigate their contribution to developmental gene expression, we developed RAMPAGE, a high-throughput 5'-complete cDNA sequencing approach to accurately discover TSSs, characterize their transcripts, and quantify their expression. This strategy, which directly delineates the expression profiles of individual promoters and was designed to offer optimal sample multiplexing capabilities, represents an advantageous alternative to standard RNA-Seq for a wide range of transcriptome profiling applications. We used RAMPAGE in a genome-wide study of promoter activity throughout 36 stages of the life cycle of Drosophila melanogaster, and describe here a comprehensive dataset that represents the first developmental timecourse of promoter usage. We found that over 40% of developmentally expressed genes have at least 2 promoters, and that alternative promoters generally implement distinct regulatory programs. Transposons harbor TSSs driving the expression of hundreds of annotated genes, and they often impart their own expression specificity upon the genes they regulate. Detailed analysis of particular transposons identified sequence elements encoding these regulatory properties. Our results show that transposable elements contribute significantly to the generation of standing variation and to the evolution of gene regulatory networks, by distributing stereotyped regulatory modules throughout the genome.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE36212 | GEO | 2012/08/30

SECONDARY ACCESSION(S): PRJNA155825

REPOSITORIES: GEO

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Project description:Since their discovery, transposable elements have been proposed to play a central role in the evolution of their host genomes through their ability to regulate gene expression, in particular by providing transcription start sites (TSSs) for host genes. To investigate their contribution to developmental gene expression, we developed RAMPAGE, a high-throughput 5'-complete cDNA sequencing approach to accurately discover TSSs, characterize their transcripts, and quantify their expression. This strategy, which directly delineates the expression profiles of individual promoters and was designed to offer optimal sample multiplexing capabilities, represents an advantageous alternative to standard RNA-Seq for a wide range of transcriptome profiling applications. We used RAMPAGE in a genome-wide study of promoter activity throughout 36 stages of the life cycle of Drosophila melanogaster, and describe here a comprehensive dataset that represents the first developmental timecourse of promoter usage. We found that over 40% of developmentally expressed genes have at least 2 promoters, and that alternative promoters generally implement distinct regulatory programs. Transposons harbor TSSs driving the expression of hundreds of annotated genes, and they often impart their own expression specificity upon the genes they regulate. Detailed analysis of particular transposons identified sequence elements encoding these regulatory properties. Our results show that transposable elements contribute significantly to the generation of standing variation and to the evolution of gene regulatory networks, by distributing stereotyped regulatory modules throughout the genome. This dataset represents a whole-genome, single-base resolution profiling of transcription start site (TSS) expression throughout 36 stages of the life cycle of Drosophila melanogaster. These profiles were established using RAMPAGE, a high-throughput, high-accuracy 5'-complete cDNA sequencing method implemented on the Illumina platform. Embryos, larvae, pupae and adult flies were collected at specific stages of development, and RAMPAGE profiles were established for pools of whole organisms. The data was analyzed using custom scripts and algorithms that are all available upon request. Supplementary files: Dmel_Combined_+.bw: bigWig coverage by cDNA 5' ends (+ strand). Dmel_Combined_-.bw: bigWig coverage by cDNA 5' ends (- strand). Dmel_All_RAMPAGE_peaks.bed: BED file describing all RAMPAGE peaks. Dmel_GeneTSS_RAMPAGE_peaks.bed: BED file describing all peaks attributed to annotated genes. GeneTSS_expression_RAMPAGE_RPM.txt: Expression matrix for all genic peaks (RPM: reads per million). Transposon_expression_RAMPAGE_RPM.txt: Expression matrix for all RepeatMasker-annotated transposon classes (RPM: reads per million). Genome build: dm3

Project description:Background: Transposable elements (TEs) represent a substantial fraction of the genomes, playing a major role in evolution, as sources of genetic variability. To fully appraise the role of TE in the acquisition of genetic novelty in genome evolution, we must also consider the impact of their own transcriptional activity. Results: We studied impact of TE transcriptional activity on gene using high-throughput RNA-Seq sequencing in Drosophila melanogaster. TEs, which turn out to be expressed in euchromatin as well as in heterochromatin, interact with genes at different levels. The observed transcription from TEs involve canonical or non-canonical transcription start sites (TSSs) distributed along their sequence. We also find evidences for potential bidirectional transcription from the TE promoter regions where the antisense transcript is co-opted by the host genome as TSSs of a gene. We found that active TEs seem to accumulate in the 5' upstream regions of the genes, and possibly provide an alternative transcript of the nearby gene. Indeed, predominantly, the TE transcript is collinear and overlapping the gene. Apart from the 5' upstream regions, we also found that most active TEs are transcribed on the gene transcript strand. Conversely, few transcripts from TE are anti sense with respect to the gene. This suggests that they have a disruptive action and are counter-selected. The only exceptions are for TEs located into introns, where they could provide another complex way of gene regulation, and in the 3' downstream region, where other mechanisms akin to siRNAs could take place. Finally, we noted several cases where the cryptic TSS is located on TE fragments corresponding to a low complexity sequence. Frequently these TE fragments appear to be over-represented when close to genes, suggesting a possible selected role. Conclusion: Altogether, these results suggest that active transposable elements influence host gene transcription. It is likely that some features of transposable elements have been exaptated in order to enrich the genes repertoire by opening routes to sub- or neo-functionalization. Examination of the transcription produced by transposable elements in D. melanogaster

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Promoter activity profiling throughout the Drosophila life cycle reveals role of transposons in regulatory innovation

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