Plant microRNAs in larval food regulate honeybee caste development

PLoS Genet. 2017 Aug 31;13(8):e1006946. doi: 10.1371/journal.pgen.1006946. eCollection 2017 Aug.

Abstract

The major environmental determinants of honeybee caste development come from larval nutrients: royal jelly stimulates the differentiation of larvae into queens, whereas beebread leads to worker bee fate. However, these determinants are not fully characterized. Here we report that plant RNAs, particularly miRNAs, which are more enriched in beebread than in royal jelly, delay development and decrease body and ovary size in honeybees, thereby preventing larval differentiation into queens and inducing development into worker bees. Mechanistic studies reveal that amTOR, a stimulatory gene in caste differentiation, is the direct target of miR162a. Interestingly, the same effect also exists in non-social Drosophila. When such plant RNAs and miRNAs are fed to Drosophila larvae, they cause extended developmental times and reductions in body weight and length, ovary size and fecundity. This study identifies an uncharacterized function of plant miRNAs that fine-tunes honeybee caste development, offering hints for understanding cross-kingdom interaction and co-evolution.

MeSH terms

  • Animals
  • Bees / drug effects
  • Bees / genetics
  • Bees / growth & development*
  • Drosophila / genetics
  • Drosophila / growth & development
  • Fatty Acids / administration & dosage
  • Fatty Acids / genetics
  • Female
  • Food
  • Gene Expression Regulation, Developmental
  • Hierarchy, Social*
  • Larva / drug effects
  • Larva / genetics
  • Larva / growth & development*
  • MicroRNAs / administration & dosage
  • MicroRNAs / genetics*

Substances

  • Fatty Acids
  • MicroRNAs
  • royal jelly

Grants and funding

This work was supported by: the National Basic Research Program of China (973 Program) (No. 2014CB542300) http://program.most.gov.cn/; the National Natural Science Foundation of China (Nos. 31271378 and 81250044) http://www.nsfc.gov.cn/; the Research Special Fund for Public Welfare Industry of Health (No. 201302018). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.