Molecular basis of tactile specialization in the duck bill

Proc Natl Acad Sci U S A. 2017 Dec 5;114(49):13036-13041. doi: 10.1073/pnas.1708793114. Epub 2017 Nov 6.

Abstract

Tactile-foraging ducks are specialist birds known for their touch-dependent feeding behavior. They use dabbling, straining, and filtering to find edible matter in murky water, relying on the sense of touch in their bill. Here, we present the molecular characterization of embryonic duck bill, which we show contains a high density of mechanosensory corpuscles innervated by functional rapidly adapting trigeminal afferents. In contrast to chicken, a visually foraging bird, the majority of duck trigeminal neurons are mechanoreceptors that express the Piezo2 ion channel and produce slowly inactivating mechano-current before hatching. Furthermore, duck neurons have a significantly reduced mechano-activation threshold and elevated mechano-current amplitude. Cloning and electrophysiological characterization of duck Piezo2 in a heterologous expression system shows that duck Piezo2 is functionally similar to the mouse ortholog but with prolonged inactivation kinetics, particularly at positive potentials. Knockdown of Piezo2 in duck trigeminal neurons attenuates mechano current with intermediate and slow inactivation kinetics. This suggests that Piezo2 is capable of contributing to a larger range of mechano-activated currents in duck trigeminal ganglia than in mouse trigeminal ganglia. Our results provide insights into the molecular basis of mechanotransduction in a tactile-specialist vertebrate.

Keywords: Piezo2; mechano-gating; mechanoreception; mechanosensitivity; trigeminal ganglia.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Avian Proteins / antagonists & inhibitors
  • Avian Proteins / genetics*
  • Avian Proteins / metabolism
  • Beak / cytology
  • Beak / innervation
  • Beak / physiology*
  • Chickens
  • Cloning, Molecular
  • Ducks / physiology*
  • Embryo, Nonmammalian
  • Gene Expression
  • Genetic Vectors / genetics
  • Genetic Vectors / metabolism
  • HEK293 Cells
  • Humans
  • Ion Channels / antagonists & inhibitors
  • Ion Channels / genetics
  • Ion Channels / metabolism
  • Kinetics
  • Mechanoreceptors / cytology
  • Mechanoreceptors / metabolism*
  • Mechanotransduction, Cellular
  • Mice
  • Patch-Clamp Techniques
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Sequence Homology, Amino Acid
  • Species Specificity
  • Touch / physiology*
  • Touch Perception / physiology*
  • Trigeminal Ganglion / cytology
  • Trigeminal Ganglion / metabolism

Substances

  • Avian Proteins
  • Ion Channels
  • Piezo2 protein, mouse
  • RNA, Small Interfering
  • Recombinant Proteins

Associated data

  • GENBANK/KY012733