Abstract
BackgroundLong noncoding RNAs (lncRNAs) have roles in gene regulation, epigenetics, and molecular scaffolding and it is hypothesized that they underlie some mammalian evolutionary adaptations. However, for many mammalian species, the absence of a genome assembly precludes the comprehensive identification of lncRNAs. The genome of the American beaver (Castor canadensis) has recently been sequenced, setting the stage for the systematic identification of beaver lncRNAs and the characterization of their expression in various tissues. The objective of this study was to discover and profile polyadenylated lncRNAs in the beaver using high-throughput short-read sequencing of RNA from sixteen beaver tissues and to annotate the resulting lncRNAs based on their potential for orthology with known lncRNAs in other species.ResultsUsing de novo transcriptome assembly, we found 9528 potential lncRNA contigs and 187 high-confidence lncRNA contigs. Of the high-confidence lncRNA contigs, 147 have no known orthologs (and thus are putative novel lncRNAs) and 40 have mammalian orthologs. The novel lncRNAs mapped to the Oregon State University (OSU) reference beaver genome with greater than 90% sequence identity. While the novel lncRNAs were on average shorter than their annotated counterparts, they were similar to the annotated lncRNAs in terms of the relationships between contig length and minimum free energy (MFE) and between coverage and contig length. We identified beaver orthologs of known lncRNAs such as XIST, MEG3, TINCR, and NIPBL-DT. We profiled the expression of the 187 high-confidence lncRNAs across 16 beaver tissues (whole blood, brain, lung, liver, heart, stomach, intestine, skeletal muscle, kidney, spleen, ovary, placenta, castor gland, tail, toe-webbing, and tongue) and identified both tissue-specific and ubiquitous lncRNAs.ConclusionsTo our knowledge this is the first report of systematic identification of lncRNAs and their expression atlas in beaver. LncRNAs—both novel and those with known orthologs—are expressed in each of the beaver tissues that we analyzed. For some beaver lncRNAs with known orthologs, the tissue-specific expression patterns were phylogenetically conserved. The lncRNA sequence data files and raw sequence files are available via the web supplement and the NCBI Sequence Read Archive, respectively.
Highlights
Long noncoding RNAs have roles in gene regulation, epigenetics, and molecular scaffolding and it is hypothesized that they underlie some mammalian evolutionary adaptations
Screening pipeline In order to obtain a comprehensive profile of the noncoding transcriptome of the American beaver, we paired-end sequenced polyadenylated RNA pooled from samples of sixteen different beaver tissues and de novo assembled a “pan-tissue” beaver polyadenylated RNA transcriptome using Trinity
We found that 66% of the mammalian Benchmarking Universal SingleCopy Ortholog (BUSCO) genes had highconfidence (E < 10− 5) matches to one or more contigs in the Trinity-assembled, pan-tissue, beaver polyadenylated RNA transcriptome
Summary
Long noncoding RNAs (lncRNAs) have roles in gene regulation, epigenetics, and molecular scaffolding and it is hypothesized that they underlie some mammalian evolutionary adaptations. Out of more than five thousand extant mammalian species (estimated as of 2019), less than 90 have high-quality genome assemblies available (according to the Ensembl genome database [6] release 96), and for those that do not, the absence of a genome or transcriptome sequence precludes comprehensive sequencing-based identification of lncRNAs. The genome and three tissue transcriptomes of the American beaver Castor canadensis (Order Rodentia, Family Castoridae) have recently been sequenced [7, 8], enabling the systematic search for molecular determinants of this semi-aquatic herbivore’s unique physiologic, anatomic, and behavioral adaptations. The beaver’s abilities to digest tree bark [11] and certain toxic plants [12] may depend on adaptations of detoxifying enzymes [13, 14] and lignocellulose-catabolizing gut microbes [15] Such enzymatic adaptations may involve novel lncRNAs. lncRNAs have been implicated in species-specific adaptations such as hibernation in grizzly bears [16] and adaptation to cold in zebrafish [17]. Establishing a compendium of beaver lncRNAs (both novel lncRNAs and those that are orthologous to known lncRNAs in other species) is an important starting point for efforts to understand the roles of noncoding RNAs in regulating expression of genes that underlie beaver anatomy and physiology
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