The steroid-hormone ecdysone coordinates parallel pupariation neuromotor and morphogenetic subprograms via epidermis-to-neuron Dilp8-Lgr3 signal induction

Nat Commun. 2021 Jun 7;12(1):3328. doi: 10.1038/s41467-021-23218-5.

Abstract

Innate behaviors consist of a succession of genetically-hardwired motor and physiological subprograms that can be coupled to drastic morphogenetic changes. How these integrative responses are orchestrated is not completely understood. Here, we provide insight into these mechanisms by studying pupariation, a multi-step innate behavior of Drosophila larvae that is critical for survival during metamorphosis. We find that the steroid-hormone ecdysone triggers parallel pupariation neuromotor and morphogenetic subprograms, which include the induction of the relaxin-peptide hormone, Dilp8, in the epidermis. Dilp8 acts on six Lgr3-positive thoracic interneurons to couple both subprograms in time and to instruct neuromotor subprogram switching during behavior. Our work reveals that interorgan feedback gates progression between subunits of an innate behavior and points to an ancestral neuromodulatory function of relaxin signaling.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Drosophila / metabolism
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism*
  • Ecdysone / genetics
  • Ecdysone / pharmacology*
  • Epidermal Cells / metabolism
  • Epidermis / metabolism*
  • Intercellular Signaling Peptides and Proteins
  • Larva / metabolism
  • Metamorphosis, Biological
  • Morphogenesis / drug effects*
  • Morphogenesis / genetics
  • Neurons / metabolism*
  • Receptors, G-Protein-Coupled / genetics
  • Receptors, G-Protein-Coupled / metabolism*
  • Relaxin / metabolism

Substances

  • Drosophila Proteins
  • Intercellular Signaling Peptides and Proteins
  • Lgr3 protein, Drosophila
  • Receptors, G-Protein-Coupled
  • insulin-like peptide 8, Drosophila
  • Ecdysone
  • Relaxin