Transcript length mediates developmental timing of gene expression across Drosophila

TL;DR

This study demonstrates that gene length influences developmental timing in Drosophila, with longer genes experiencing delayed expression due to transcriptional elongation constraints, impacting gene evolution and expression regulation.

Contribution

It reveals that intron delay affects gene expression timing genome-wide and influences gene structure evolution in Drosophila.

Findings

Long zygotic genes show delayed expression compared to short genes.

Delay is due to transcription elongation limitations, not initiation.

Purifying selection maintains compact gene structures for highly expressed genes.

Abstract

The time required to transcribe genes with long primary transcripts may limit their ability to be expressed in cells with short mitotic cycles, a phenomenon termed intron delay. As such short cycles are a hallmark of the earliest stages of insect development, we used Drosophila developmental timecourse expression data to test whether intron delay affects gene expression genome-wide, and to determine its consequences for the evolution of gene structure. We find that long zygotically expressed, but not maternally deposited, genes show substantial delay in expression relative to their shorter counterparts and that this delay persists over a substantial portion of the ~24 hours of embryogenesis. Patterns of RNA-seq coverage from the 5' and 3' ends of transcripts show that this delay is consistent with their inability to terminate transcription, but not with transcriptional initiation-based regulatory control. Highly expressed zygotic genes are subject to purifying selection to maintain compact transcribed regions, allowing conservation of embryonic expression patterns across the Drosophila phylogeny. We propose that intron delay is an underappreciated physical mechanism affecting both patterns of expression as well as gene structure of many genes across Drosophila.