Abstract
SummaryLong non-coding RNAs (lncRNAs) can often function in the regulation of gene expression during development; however, their generality as essential regulators in developmental processes and organismal phenotypes remains unclear. Here, we performed a tailored investigation of lncRNA expression and function during Drosophila embryogenesis, interrogating multiple stages, tissue specificity, nuclear localization, and genetic backgrounds. Our results almost double the number of annotated lncRNAs expressed at these embryonic stages. lncRNA levels are generally positively correlated with those of their neighboring genes, with little evidence of transcriptional interference. Using fluorescent in situ hybridization, we report the spatiotemporal expression of 15 new lncRNAs, revealing very dynamic tissue-specific patterns. Despite this, deletion of selected lncRNA genes had no obvious developmental defects or effects on viability under standard and stressed conditions. However, two lncRNA deletions resulted in modest expression changes of a small number of genes, suggesting that they fine-tune expression of non-essential genes. Several lncRNAs have strain-specific expression, indicating that they are not fixed within the population. This intra-species variation across genetic backgrounds may thereby be a useful tool to distinguish rapidly evolving lncRNAs with as yet non-essential roles.
Highlights
In addition to protein-coding genes, metazoan genomes contain many transcribed non-coding regions [1]
Identification of New Non-coding Transcripts during Embryonic Development To obtain a comprehensive view of the transcriptional landscape during early and mid-stages of embryogenesis, we deeply sequenced rRNA-depleted total RNA samples from multiple developmental stages, cellular contexts, and subcellular compartments
As we were interested in RNA with a potential function in transcriptional regulation, we prepared RNA sequencing (RNA-seq) libraries from purified nuclear RNA from mesodermal cells at 3–4 hr and 6–8 hr
Summary
In addition to protein-coding genes, metazoan genomes contain many transcribed non-coding regions [1]. In comparison to protein-coding genes, genes encoding lncRNAs are more rapidly evolving [4,5,6] and tend to have more restricted expression in specific tissues [2, 7, 8] and developmental stages [9, 10]. Extensive non-coding transcription of higher eukaryotes genomes is widely recognized, whether and how most lncRNA molecules function is actively debated. The highly specific spatiotemporal expression patterns of many characterized lncRNAs are suggestive of function [11], this could reflect bystander transcription during the regulation of tissuespecific protein-coding genes [12, 13]. Even without accumulating to high levels, the transcription of some lncRNAs may affect expression of neighboring genes in cis, through mechanisms such as antisense-mediated repression [16, 17], RNA-mediated enhancement [18], activation of divergent genes in bidirectional promoters [19], and genomic imprinting [20]
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