Reversal of Salt Preference Is Directed by the Insulin/PI3K and Gq/PKC Signaling inCaenorhabditis elegans

Abstract

Animals search for foods and decide their behaviors according to previous experience. Caenorhabditis elegans detects chemicals with a limited number of sensory neurons, allowing us to dissect roles of each neuron for innate and learned behaviors. C. elegans is attracted to salt after exposure to the salt (NaCl) with food. In contrast, it learns to avoid the salt after exposure to the salt without food. In salt-attraction behavior, it is known that the ASE taste sensory neurons (ASEL and ASER) play a major role. However, little is known about mechanisms for learned salt avoidance. Here, through dissecting contributions of ASE neurons for salt chemotaxis, we show that both ASEL and ASER generate salt chemotaxis plasticity. In ASER, we have previously shown that the insulin/PI 3-kinase signaling acts for starvation-induced salt chemotaxis plasticity. This study shows that the PI 3-kinase signaling promotes aversive drive of ASER but not of ASEL. Furthermore, the G q signaling pathway composed of G q a EGL-30, diacylglycerol, and nPKC (novel protein kinase C) TTX-4 promotes attractive drive of ASER but not of ASEL. A putative salt receptor GCY-22 guanylyl cyclase is required in ASER for both salt attraction and avoidance. Our results suggest that ASEL and ASER use distinct molecular mechanisms to regulate salt chemotaxis plasticity.

A Gustatory Neural Circuit ofCaenorhabditis elegansGenerates Memory-Dependent Behaviors in Na+Chemotaxis

“…All strains used for optogenetics carried the lite-1(ce314 ) mutation to diminish the innate avoidance of blue light (Edwards et al, 2008;Ward et al, 2008;Liu et al, 2010;Li et al, 2014). Fast-growing E. coli NA22 was used as food source in behavioral assays and chemotaxis assays to avoid starvation (Tomioka et al, 2006;Adachi et al, 2010;Kunitomo et al, 2013). OP50 was used for imaging experiments because animals cultivated with NA22 tended to exhibit high background fluorescence in the intestine (Oda et al, 2011;Kunitomo et al, 2013).…”

“…The C. elegans strains and transgenic lines used in this study are listed in Table 1. ASEL-, AWC-, AIY-, AIAand AIB-ablated animals were described previously (Table 1; Adachi et al, 2010;Yoshida et al, 2012;Kunitomo et al, 2013;Satoh et al, 2014). Chemotaxis assay and tracking assay.…”

“…In contrast, the role and properties of the ASEL neuron in salt chemotaxis plasticity has not yet been examined thoroughly, although our previous study showed that, together with ASER, ASEL is important for NaCl chemotaxis learning (Adachi et al, 2010). To keep balance between external and internal conditions in the body, C. elegans, much like flies (Zhang et al, 2013) and mammals (Chandrashekar et al, 2010), prefers relatively low NaCl concentrations (Saeki et al, 2001;Bargmann, 2006).…”

“…egl-30, which encodes an ortholog of the ␣ subunit of heterotrimetric G-protein Gq, regulates locomotory movements positively (Brundage et al, 1996;Lackner et al, 1999;Adachi et al, 2010). The Gq/DAG/PKC pathway modulates NaCl chemotaxis and counteracts phophatidylinositol 3-kinase signaling (Tomioka et al, 2006;Adachi et al, 2010;Kunitomo et al, 2013).…”

“…When nematodes are grown in medium containing NaCl and food, they show attraction to NaCl via ASE neurons (Kunitomo et al, 2013). However, when they are starved with NaCl, the chemotaxis to NaCl falls dramatically or even becomes negative to avoid NaCl (Tomioka et al, 2006;Adachi et al, 2010).…”