miR-34 modulates wing polyphenism in planthopper

PLoS Genet. 2019 Jun 26;15(6):e1008235. doi: 10.1371/journal.pgen.1008235. eCollection 2019 Jun.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antagomirs / genetics
  • Ecdysterone / genetics
  • Gene Expression Regulation / genetics
  • Hemiptera / genetics*
  • Hemiptera / growth & development
  • Juvenile Hormones / genetics
  • MicroRNAs / genetics*
  • Phenotype
  • Promoter Regions, Genetic / genetics
  • Receptor, Insulin / genetics*
  • Wings, Animal / growth & development*
  • Wings, Animal / metabolism

Substances

  • Antagomirs
  • Juvenile Hormones
  • MicroRNAs
  • Ecdysterone
  • Receptor, Insulin

Grants and funding

FL was funded by the National Key Research and Development Program (2017YFD0200900, 2016YFC1200600) and the National Science Foundation of China (NSFC) (31772238). KH was funded by NSFC (31701785). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.