Sensory mechanisms controlling the timing of larval developmental and behavioral transitions require the Drosophila DEG/ENaC subunit, Pickpocket1

Joshua A. Ainsley, Myung Jun Kim, Lauren J. Wegman, Janette M. Pettus, Wayne A. Johnson

Research output: Contribution to journalArticlepeer-review

35 Scopus citations

Abstract

Growth of multicellular organisms proceeds through a series of precisely timed developmental events requiring coordination between gene expression, behavioral changes, and environmental conditions. In Drosophila melanogaster larvae, the essential midthird instar transition from foraging (feeding) to wandering (non-feeding) behavior occurs prior to pupariation and metamorphosis. The timing of this key transition is coordinated with larval growth and size, but physiological mechanisms regulating this process are poorly understood. Results presented here show that Drosophila larvae associate specific environmental conditions, such as temperature, with food in order to enact appropriate foraging strategies. The transition from foraging to wandering behavior is associated with a striking reversal in the behavioral responses to food-associated stimuli that begins early in the third instar, well before food exit. Genetic manipulations disrupting expression of the Degenerin/Epithelial Sodium Channel subunit, Pickpocket1(PPK1) or function of PPK1 peripheral sensory neurons caused defects in the timing of these behavioral transitions. Transient inactivation experiments demonstrated that sensory input from PPK1 neurons is required during a critical period early in the third instar to influence this developmental transition. Results demonstrate a key role for the PPK1 sensory neurons in regulation of important behavioral transitions associated with developmental progression of larvae from foraging to wandering stage.

Original languageEnglish (US)
Pages (from-to)46-55
Number of pages10
JournalDevelopmental Biology
Volume322
Issue number1
DOIs
StatePublished - Oct 1 2008
Externally publishedYes

Bibliographical note

Funding Information:
The authors would like to thank Melissa Contreras and Sophie Krajewski for excellent technical assistance. We would also like to thank Dr. Toshihiro Kitamoto (U. of Iowa) and Dr. Cynthia Hughes (The Neurosciences Institute, San Diego, CA) for fly stocks. This work was supported by a grant from the American Heart Association to WAJ (0455638Z). JAA is supported by a predoctoral fellowship from the American Heart Association (0610138Z).

Keywords

  • Critical period
  • Foraging
  • Multiple dendritic neurons
  • Thermotaxis
  • Wandering

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