Expansion of the miRNA Pathway in the Hemipteran Insect Acyrthosiphon pisum

Abstract

The pathways that allow short noncoding RNAs such as the microRNAs (miRNAs) to mediate gene regulation and control critical cellular and developmental processes involve a limited number of key protein components. These proteins are the Dicer-like RNases, double-stranded RNA (dsRNA)-binding proteins, and the Argonaute (AGO) proteins that process stem-loop hairpin transcripts of endogenous genes to generate miRNAs or long dsRNA precursors (either exogenous or endogenous). Comparative genomics studies of metazoans have shown the pathways to be highly conserved overall; the major difference observed is that the vertebrate pathways overlap in sharing a single Dicer (DCR) and AGO proteins, whereas those of insects appear to be parallel, with distinct Dicers and AGOs required for each pathway. The genome of the pea aphid is the first available for a hemipteran insect and discloses an unexpected expansion of the miRNA pathway. It has two copies of the miRNA-specific dicr-1 and ago1 genes and four copies of pasha a cofactor of drosha involved in miRNA biosynthesis. For three of these expansions, we showed that one copy of the genes diverged rapidly and in one case (ago1b) shows signs of positive selection. These expansions occurred concomitantly within a brief evolutionary period. The pea aphid, which reproduces by viviparous parthenogenesis, is able to produce several adapted phenotypes from one single genotype. We show by reverse transcriptase-polymerase chain reaction that all the duplicated copies of the miRNA machinery genes are expressed in the different morphs. Investigating the function of these novel genes offers an exciting new challenge in aphid biology.

Instar-dependent systemic RNA interference response in Leptinotarsa decemlineata larvae

“…In D. melanogaster, DmDcr2 is involved in the siRNA pathway, whereas DmDcr1 is involved in the miRNA pathway [43]. Similar results have been reported in Acyrthosiphon pisum [44].…”

Silencing of Aphid Genes by dsRNA Feeding from Plants

“…Given that MpC002 expression is knocked down by up to 60% and is predominantly expressed in the salivary glands, the silencing signal appears to spread through the aphid. This is consistent with the finding that small RNA pathways that are highly conserved in animals are also present in aphids [36,37,38] Knockdown of Rack-1 and MpC002 reduced aphid fecundity ( Figure 3B, Figure 5B) but not survival ( Figure S1). This contrasts with the results obtained by dsRNA injection of A. pisum in which survival was reduced by silencing C002.…”

Super-induction of Dicer-2 expression by alien double-stranded RNAs: an evolutionary ancient response to viral infection?

“…In insects, both Dicer-1 and Dicer-2 are generally present in the same species. Of note, and as reported by Jaubert-Possamai et al (2010), the pea aphid A. pisum has two paralogues of Dicer-1. The functional significance of Dicer-1 and Dicer-2 paralogues remains unknown.…”