Abstract
MicroRNAs (miRNAs) are involved in posttranscriptional regulation of gene expression. Because several miRNAs are known to affect the stability or translation of developmental regulatory genes, the origin of novel miRNAs may have contributed to the evolution of developmental processes and morphology. Lepidoptera (butterflies and moths) is a species-rich clade with a well-established phylogeny and abundant genomic resources, thereby representing an ideal system in which to study miRNA evolution. We sequenced small RNA libraries from developmental stages of two divergent lepidopterans, Cameraria ohridella (Horse chestnut Leafminer) and Pararge aegeria (Speckled Wood butterfly), discovering 90 and 81 conserved miRNAs, respectively, and many species-specific miRNA sequences. Mapping miRNAs onto the lepidopteran phylogeny reveals rapid miRNA turnover and an episode of miRNA fixation early in lepidopteran evolution, implying that miRNA acquisition accompanied the early radiation of the Lepidoptera. One lepidopteran-specific miRNA gene, miR-2768, is located within an intron of the homeobox gene invected, involved in insect segmental and wing patterning. We identified cubitus interruptus (ci) as a likely direct target of miR-2768, and validated this suppression using a luciferase assay system. We propose a model by which miR-2768 modulates expression of ci in the segmentation pathway and in patterning of lepidopteran wing primordia.
Highlights
IntroductionThe information in an organism’s genome is used to coordinate the generation of morphology
During development, the information in an organism’s genome is used to coordinate the generation of morphology
Using small RNA sequencing, we identified 113 and 139 miRNA genes in the Horse chestnut Leafminer moth C. ohridella and the Speckled Wood butterfly Pa. aegeria, respectively
Summary
The information in an organism’s genome is used to coordinate the generation of morphology. Evolutionary modification of this developmental process in different animal lineages has given rise to the vast diversity of body form and function observed across the Metazoa today. Many evolutionary changes to genes have been documented including gene duplications (Brooke et al 1998; Putnam et al 2008), coding sequence alterations (Fondon and Garner 2004), and modifications to gene expression (Jeong et al 2006). The mature miRNA functions to guide RISC to specific messenger RNA transcripts to bring about downregulation of gene expression, by binding to specific target sequences primarily in the 30-untranslated regions (30-UTRs) of protein-coding genes (Kenny et al 2013). Several miRNAs are known to target genes involved in developmental processes (Yekta et al 2004; Moran et al 2014), and a general role in stabilization of developmental pathways in the face of fluctuating environmental conditions has been proposed (Peterson et al 2009; Herranz and Cohen 2010)
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