Abstract
The accurate rise and fall of active hormones is important for insect development. The ecdysteroids must be cleared in a timely manner. However, the mechanism of suppressing the ecdysteroid biosynthesis at the right time remains unclear. Here, we sequenced a small RNA library of Chilo suppressalis and identified 300 miRNAs in this notorious rice insect pest. Microarray analysis yielded 54 differentially expressed miRNAs during metamorphosis development. Target prediction and in vitro dual-luciferase assays confirmed that seven miRNAs (two conserved and five novel miRNAs) jointly targeted three Halloween genes in the ecdysteroid biosynthesis pathway. Overexpression of these seven miRNAs reduced the titer of 20-hydroxyecdysone (20E), induced mortality, and retarded development, which could be rescued by treatment with 20E. Comparative analysis indicated that the miRNA regulation of metamorphosis development is a conserved process but that the miRNAs involved are highly divergent. In all, we present evidence that both conserved and lineage-specific miRNAs have crucial roles in regulating development in insects by controlling ecdysteroid biosynthesis, which is important for ensuring developmental convergence and evolutionary diversity.
Highlights
Insect metamorphosis is one of the most successful biological strategies to exploit various food resources and habitats (Truman and Riddiford 1999; Bishop et al 2006) and may be one of the primary reasons that insects have become the largest group of animals, accounting for more than 90% of the animal species on Earth (Mora et al 2011)
Some lineage-specific miRNAs such as aael-miR-2942 in Aedes albopictus and miR-2768 in lepidopterans were reported to have key roles in insect development (Puthiyakunnon et al 2013). Most of these studies were conducted with model insects, and little is understood about miRNA functionality in metamorphosis development in rice insect pests even though hundreds of miRNAs have been identified in Nilaparvata lugens, Sogatella furcifera, and C. suppressalis (Xu et al 2013; Yin et al 2014; Chang et al 2016)
The results indicated that only 2.56% were ribosomal RNA, along with 0.56% transfer RNA, 0.05% small nuclear RNA
Summary
Goodisman et al 2005; Margam et al 2006). the timing of the appearance of ecdysteroids and JHs is important in determining developmental transition. In the brown planthopper Nilaparvata lugens, Nlu-miR-8-5p and Nlu-miR-2a-3p were negatively regulated by ecdysone via BR-C These two miRNAs target genes in the chitin biosynthesis pathway, the membranebound trehalase (Tre-2) and phosphoacetylglucosamine mutase (PAGM), inducing defective moulting and high mortality (Chen et al 2013). Some lineage-specific miRNAs such as aael-miR-2942 in Aedes albopictus and miR-2768 in lepidopterans were reported to have key roles in insect development (Puthiyakunnon et al 2013) Most of these studies were conducted with model insects, and little is understood about miRNA functionality in metamorphosis development in rice insect pests even though hundreds of miRNAs have been identified in Nilaparvata lugens, Sogatella furcifera, and C. suppressalis (Xu et al 2013; Yin et al 2014; Chang et al 2016). These miRNAs ensure the accurate and timely removal of ecdysteroids and jointly modulate the C. suppressalis larvae–larvae, larvae–pupa, and pupa–adult transitions by targeting multiple genes in the ecdysone cascade
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