Abstract
Polyphenism is a successful strategy adopted by organisms to adapt to environmental changes. Brown planthoppers (BPH, Nilaparvata lugens) develop two wing phenotypes, including long-winged (LW) and short-winged (SW) morphs. Though insulin receptor (InR) and juvenile hormone (JH) have been known to regulate wing polyphenism in BPH, the interaction between these regulators remains largely elusive. Here, we discovered that a conserved microRNA, miR-34, modulates a positive autoregulatory feedback loop of JH and insulin/IGF signaling (IIS) pathway to control wing polyphenism in BPH. Nlu-miR-34 is abundant in SW BPHs and suppresses NlInR1 by targeting at two binding sites in the 3’UTR of NlInR1. Overexpressing miR-34 in LW BPHs by injecting agomir-34 induces the development towards SW BPHs, whereas knocking down miR-34 in SW BPHs by injecting antagomir-34 induces more LW BPHs when another NlInR1 suppressor, NlInR2, is also suppressed simultaneously. A cis-response element of Broad Complex (Br-C) is found in the promoter region of Nlu-miR-34, suggesting that 20-hydroxyecdysone (20E) might be involved in wing polyphenism regulation. Topic application of 20E downregulates miR-34 expression but does not change wing morphs. On the other hand, JH application upregulates miR-34 expression and induces more SW BPHs. Moreover, knocking down genes in IIS pathway changes JH titers and miR-34 abundance. In all, we showed that miRNA mediates the cross talk between JH, 20E and IIS pathway by forming a positive feedback loop, uncovering a comprehensive regulation mechanism which integrates almost all known regulators controlling wing polyphenism in insects.
Highlights
The phenomenon of polyphenism is that two or more distinct phenotypes are displayed by an organism with the same genotype
To investigate whether miRNA may play a role in regulating wing polyphenism, we carried out a bioinformatics analysis to identify miRNAs targeting at NlInR1 or NlInR2
The results showed that only Nlu-miR-34 can target NlInR1 with two putative binding sites in the 3’untranslated region (UTR) predicted by all five target prediction algorithms (Fig 1A, see methods). miR-34 is highly conserved in insects and nematodes (Fig 1B, see methods) and is predicted to have 19 target genes in BPH (S1 Table)
Summary
The phenomenon of polyphenism is that two or more distinct phenotypes are displayed by an organism with the same genotype. This phenomenon is triggered by environmental cues such as population density, host nutrition, and temperature [1]. Horn polyphenism is a nutritiondependent trait where some male beetles have fully-developed horns, while other males are completely hornless, depending on their nutrition status and body size [3]. Eusocial insects, including members of Hymenoptera, Blattodea (termites), often display caste differentiation, producing multiple types of offspring with different reproductive and morphological features [4]. Based on the physiological state of the mother, aphids produce winged adults in deteriorating environments and flightless morphs when environmental conditions are stable [5]
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