Mutually exclusive dendritic arbors in C. elegans neurons share a common architecture and convergent molecular cues

Abstract

Stress-induced changes to the dendritic architecture of neurons have been demonstrated in numerous mammalian and invertebrate systems. Remodeling of dendrites varies tremendously among neuron types. During the stress-induced dauer stage of Caenorhabditis elegans, the IL2 neurons arborize to cover the anterior body wall. In contrast, the FLP neurons arborize to cover an identical receptive field during reproductive development. Using timecourse imaging, we show that branching between these two neuron types is highly coordinated. Furthermore, we find that the IL2 and FLP arbors have a similar dendritic architecture and use an identical downstream effector complex to control branching; however, regulation of this complex differs between stress-induced IL2 branching and FLP branching during reproductive development. We demonstrate that the unfolded protein response (UPR) sensor IRE-1, required for localization of the complex in FLP branching, is dispensable for IL2 branching at standard cultivation temperatures. Exposure of ire-1 mutants to elevated temperatures results in defective IL2 branching, thereby demonstrating a previously unknown genotype by environment interaction within the UPR. We find that the FOXO homolog, DAF-16, is required cell-autonomously to control arborization during stress-induced arborization. Likewise, several aspects of the dauer formation pathway are necessary for the neuron to remodel, including the phosphatase PTEN/DAF-18 and Cytochrome P450/DAF-9. Finally, we find that the TOR associated protein, RAPTOR/DAF-15 regulates mutually exclusive branching of the IL2 and FLP dendrites. DAF-15 promotes IL2 branching during dauer and inhibits precocious FLP growth. Together, our results shed light on molecular processes that regulate stress-mediated remodeling of dendrites across neuron classes.

Structural analysis of the C. elegans dauer larval anterior sensilla by Focused Ion Beam-Scanning Electron Microscopy

“…Furthermore, IL2QV's midline dendrites (Figure 4A) shared the trajectory of AVM what contributes to gentle touch responses (Chalfie and Sulston, 1981), suggesting similar mechanosensitive functionalities for IL2Qs which are slightly different to IL2Ls. Previously, dauer IL2 neurons were proposed to play similar roles as mechano-and temperature-sensitive FLP neurons (Kaplan and Horvitz, 1993;Chatzigeorgiou and Schafer, 2011;Liu et al, 2012) in non-dauers, as they build dendritic branches in a similar receptive field (Albeg et al, 2011;Schroeder et al, 2013;Androwski et al, 2020). The morphological appearance of IL2L crown-like dendrites is fairly stable across dauers, with only slight differences in the 4° dendrites in one individual (Supplementary Figure S2B-D).…”

“…AVM ends more posterior in non-dauers, approximately at the level of the pharyngeal metacorpus (Chalfie and Sulston, 1981;White et al, 1986). In the future, these observations should be further quantified by analyzing more individuals with imaging techniques that allow much larger sampling such as fluorescence microscopy with specific reporter lines (Ch'ng et al, 2003;Androwski et al, 2020).…”

“…IL2's dendrites show increased branching specifically in dauers revealing life-cycle depending phenotypic plasticity (Schroeder et al, 2013). In non-dauers, all six IL2 neurons have a single primary (1°) dendrite that projects anterior along the labial bundles (Schroeder et al, 2013;Androwski et al, 2020). In dauers, two dorsal and two ventral IL2 neurons (together called IL2Q) emanate in subsequent order of dendritic branches along 1° dendrites, some projecting between body wall muscle (BWM) and Hyp cell into the midline (radial dendrites) and then along the body wall (body wall dendrites), others (midline dendrites) projecting along the midline (Schroeder et al, 2013;Androwski et al, 2020), and additional branches (dauer-specific 1° dendrites) appear from IL2 soma (Schroeder et al, 2013).…”

“…In non-dauers as well as dauers, anterior endings of lateral ILso (ILLso) cells have two branches that are enclosed by respective BAG and FLP neurons, while others (ILQso) do not feature such branches or interactions (Ward et al, 1975;Ware et al, 1975;Albert and Riddle, 1983;Perkins et al, 1986;Doroquez et al, 2014;Cebul et al, 2020). FLP neurons are highly branched along their dendrites and close to their cilia endings in adults (Albeg et al, 2011;Doroquez et al, 2014) while they only branch minimally in dauer larvae (Androwski et al, 2020). There was conflicting reporting on the sensory ending of URX neurons.…”

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“…Dendrites of IL2 show increased branching specifically in dauers revealing life-cycle depending phenotypic plasticity (Schroeder et al, 2013). In non-dauers, all six IL2 neurons have a single primary (1 • ) dendrite that projects anterior along the labial bundles (Schroeder et al, 2013;Androwski et al, 2020). In dauers, two dorsal and two ventral IL2 neurons (together called IL2Q) emanate in the subsequent order of dendritic branches along 1 • dendrites, some projecting between body wall muscle (BWM) and hypodermis (Hyp) cell into the midline (radial dendrites) and then along the body wall (body wall dendrites), others (midline dendrites) projecting along the midline (Schroeder et al, 2013;Androwski et al, 2020), and additional branches (dauer-specific 1 • dendrites) appear from IL2 soma (Schroeder et al, 2013).…”