Pervasive microRNA Duplication in Chelicerates: Insights from the Embryonic microRNA Repertoire of the Spider Parasteatoda tepidariorum

Abstract

MicroRNAs are small (∼22 nt) noncoding RNAs that repress translation and therefore regulate the production of proteins from specific target mRNAs. microRNAs have been found to function in diverse aspects of gene regulation within animal development and many other processes. Among invertebrates, both conserved and novel, lineage specific, microRNAs have been extensively studied predominantly in holometabolous insects such as Drosophila melanogaster. However little is known about microRNA repertoires in other arthropod lineages such as the chelicerates. To understand the evolution of microRNAs in this poorly sampled subphylum, we characterized the microRNA repertoire expressed during embryogenesis of the common house spider Parasteatoda tepidariorum. We identified a total of 148 microRNAs in P. tepidariorum representing 66 families. Approximately half of these microRNA families are conserved in other metazoans, while the remainder are specific to this spider. Of the 35 conserved microRNAs families 15 had at least two copies in the P. tepidariorum genome. A BLAST-based approach revealed a similar pattern of duplication in other spiders and a scorpion, but not among other chelicerates and arthropods, with the exception of a horseshoe crab. Among the duplicated microRNAs we found examples of lineage-specific tandem duplications, and the duplication of entire microRNA clusters in three spiders, a scorpion, and in a horseshoe crab. Furthermore, we found that paralogs of many P. tepidariorum microRNA families exhibit arm switching, which suggests that duplication was often followed by sub- or neofunctionalization. Our work shows that understanding the evolution of microRNAs in the chelicerates has great potential to provide insights into the process of microRNA duplication and divergence and the evolution of animal development.

The house spider genome reveals an ancient whole-genome duplication during arachnid evolution

“…Our study of the assembly and annotation of the P. tepidariorum genome revealed a high number of duplicated genes in accordance with previous observations (Clarke et al, 2015;Clarke et al, 2014;Di et al, 2015;Fuzita et al, 2015;Fuzita et al, 2016;Janssen et al, 2010;Leite et al, 2016;Schwager et al, 2007;Sharma et al, 2015;Sharma et al, 2014b;Turetzek et al, 2016). This finding is further supported by our detection of a colinearity signal across many of the largest P.…”

“…All 148 precursor microRNAs sequences for P. tepidariorum (Leite et al, 2016), with the inclusion of flanking sequences 20 bp up and down stream, were BLASTN-searched in the Dovetail assembly to identify scaffold ID and position from the best matches. The scaffolds and positions of C. sculpturatus microRNAs from Leite et al, (2016) were used.…”

“…tepidariorum are present as two or more copies (Leite et al, 2016). Analysis of the synteny of the paralogous P. tepidariorum microRNAs shows that only 8 out of 30 are found on the same scaffold.…”

“…Intriguingly, there is increasing evidence for extensive gene duplication among chelicerates other than horseshoe crabs, particularly in spiders and scorpions (Clarke et al, 2015;Clarke et al, 2014;Di et al, 2015;Fuzita et al, 2015;Fuzita et al, 2016;Janssen et al, 2010;Leite et al, 2016;Schwager et al, 2007;Sharma et al, 2015;Sharma et al, 2014b;Turetzek et al, 2016), indicating that large-scale gene duplications occurred during the evolution of these arachnids. However, although the genomes of some arachnids have been sequenced, including the tick Ixodes scapularis (Gulia-Nuss et al, 2016;Lawson et al, 2009), the mite Tetranychus urticae (Grbic et al, 2011), the Chinese scorpion Mesobuthus martensii (Cao et al, 2013), and two spiders -the velvet spider Stegodyphus mimosarum (Sanggaard et al, 2014) and the Brazilian whiteknee tarantula Acanthoscurria geniculata (Sanggaard et al, 2014) -a systematic analysis of genome evolution among these diverse animals has yet to be carried out ( Fig.…”

MicroRNA evolution provides new evidence for a close relationship of Diplura to Insecta

“…Some chelicerates show higher ratios of gene number to number of miRNA families, including the horseshoe crab, scorpions and spiders, consistent with the pervasive miRNA duplication proposed by a previous study (Leite et al ., ). A similar situation was also found in the proturan S. erythranum (Fig.…”