Sexually dimorphic control of gene expression in sensory neurons regulates decision-making behavior in C. elegans

Dennis H Kim,Zoë A Hilbert

doi:10.7554/elife.21166

Dennis H Kim, Zoë A Hilbert

Open Access

https://doi.org/10.7554/elife.21166

Copy DOI

Journal: eLife	Publication Date: Jan 24, 2017
Citations: 61	License type: CC BY 4.0

Affiliation: Massachusetts Institute of Technology

Abstract

Animal behavior is directed by the integration of sensory information from internal states and the environment. Neuroendocrine regulation of diverse behaviors of Caenorhabditis elegans is under the control of the DAF-7/TGF-β ligand that is secreted from sensory neurons. Here, we show that C. elegans males exhibit an altered, male-specific expression pattern of daf-7 in the ASJ sensory neuron pair with the onset of reproductive maturity, which functions to promote male-specific mate-searching behavior. Molecular genetic analysis of the switch-like regulation of daf-7 expression in the ASJ neuron pair reveals a hierarchy of regulation among multiple inputs-sex, age, nutritional status, and microbial environment-which function in the modulation of behavior. Our results suggest that regulation of gene expression in sensory neurons can function in the integration of a wide array of sensory information and facilitate decision-making behaviors in C. elegans.

Highlights

In order to effectively adapt to an environment, organisms need to be able to analyze both their internal state and external surroundings to make behavioral decisions that will maximize their chances of survival
Recent work in a number of animal species has demonstrated that modulation of gene expression and neuronal activity by both environmental cues and internal state can occur at the level of sensory neurons, suggesting that aspects of behavioral decision making may occur in the peripheral nervous system (Dey et al, 2015; Farhadian et al, 2012; Ryan et al, 2014)
While expression of the DAF-7/TGF-b ligand was long thought to be confined to the ASI chemosensory neurons (Ren et al, 1996; Schackwitz et al, 1996), we recently reported that a change in the microbial environment of the worm—namely, the introduction of the pathogen P. aeruginosa—can alter the neuronal expression pattern of daf-7, inducing expression in the ASJ neuron pair of hermaphrodite animals (Meisel et al, 2014)

Summary

Introduction

In order to effectively adapt to an environment, organisms need to be able to analyze both their internal state and external surroundings to make behavioral decisions that will maximize their chances of survival. Recent work in a number of animal species has demonstrated that modulation of gene expression and neuronal activity by both environmental cues and internal state can occur at the level of sensory neurons, suggesting that aspects of behavioral decision making may occur in the peripheral nervous system (Dey et al, 2015; Farhadian et al, 2012; Ryan et al, 2014). Starvation or nutritional deprivation can have less direct effects on feeding behaviors as in Drosophila, where periods of starvation have been demonstrated to both enhance odor sensitivity and attraction as well as abrogate avoidance responses to normally aversive stimuli (Bracker et al, 2013; Inagaki et al, 2014; Ko et al, 2015; Root et al, 2011).

Methods

Results

Conclusion