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WIREs Dev Biol

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Phenotypic plasticity and remodeling in the stress‐induced Caenorhabditis elegans dauer

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Rebecca J. Androwski, Kristen M. Flatt, Nathan E. Schroeder

Published Online: May 24 2017

DOI: 10.1002/wdev.278

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Organisms are often capable of modifying their development to better suit their environment. Under adverse conditions, the nematode Caenorhabditis elegans develops into a stress‐resistant alternative larval stage called dauer. The dauer stage is the primary survival stage for C. elegans in nature. Large‐scale tissue remodeling during dauer conveys resistance to harsh environments. The environmental and genetic regulation of the decision to enter dauer has been extensively studied. However, less is known about the mechanisms regulating tissue remodeling. Changes to the cuticle and suppression of feeding in dauers lead to an increased resistance to external stressors. Meanwhile reproductive development arrests during dauer while preserving the ability to reproduce once favorable environmental conditions return. Dramatic remodeling of neurons, glia, and muscles during dauer likely facilitate dauer‐specific behaviors. Dauer‐specific pulsation of the excretory duct likely mediates a response to osmotic stress. The power of C. elegans genetics has uncovered some of the molecular pathways regulating dauer tissue remodeling. In addition to genes that regulate single remodeling events, several mutants result in pleiotropic defects in dauer remodeling. This review details the individual aspects of morphological changes that occur during dauer formation and discusses molecular mechanisms regulating these processes. The dauer stage provides us with an excellent model for understanding phenotypic plasticity and remodeling from the individual cell to an entire animal. WIREs Dev Biol 2017, 6:e278. doi: 10.1002/wdev.278 This article is categorized under: Invertebrate Organogenesis > Worms Comparative Development and Evolution > Model Systems

The life cycle of C. elegans. In an environment of plentiful food and low dauer pheromone, C. elegans molts through four larval stages followed by the reproductive adult. Under conditions of low levels of food and high levels of pheromone (signaling population density) during L1 they will enter into a developmentally arrested dauer stage. Following a return to favorable environmental conditions, they will recover from dauer and resume development into a reproductive adult.

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The nonfeeding dauer stage is characterized by buccal cavity occlusion and pharyngeal bulb shrinkage. DIC micrographs of L3 (top) and dauer (bottom) animals demonstrating changes to the buccal cavity (a, red arrow) and the pharynx (b). Shrinkage of the pharynx is most obvious in the terminal bulb (red arrow). Scale bars, 10 µm.

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IL2 dendrites arborize during dauer. Confocal micrographs of an L3 (a) and dauer (b) animal expressing klp‐6p::gfp in the six IL2 neurons. During nondauer stages the IL2s are unbranched with a single dendrite projecting anteriorly (left) and a single axon projecting posteriorly (right) from the cell body. During dauer the IL2s arborize extensively, increasing their total dendritic length threefold, with the bulk of their arbors originating from just four of the six cells. Scale bars, 10 µm.

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Seam cell shrinkage and cuticle remodeling occur during dauer formation. Nomarski (a) and fluorescent (b) images of nondauer L3 (top) and dauer (bottom) ajm‐1::gfp larvae. During dauer the lateral cuticle contains raised ridges called alae (red arrows). Production of alae is correlated with shrinkage of the underlying epithelial seam cells as seen with the ajm‐1::gfp transgene. Scale bars, 10 µm.

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The dauer formation decision pathway. The decision to enter dauer begins with environmental components and proceeds through two parallel pathways before converging onto a lipid hormone signaling pathway. Mutating the encoding genes of this pathway may lead to either constitutive dauer formation (daf‐c, dauer formation constitutive) or an inability to form dauers (daf‐d, dauer formation defective). Lines ending with arrows indicate increased activity of the downstream component. Lines ending with bars indicate suppression or downregulation of the downstream component.

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Nictation and swarming are dauer‐specific behaviors. Micrographs (left) and cartoon schematics (right) of an individual nictating dauer (a) and a swarm of elevated dauers (b) on top of a polydimethylsiloxane (PDMS) pedestal. Individual dauers are capable of standing on their tail while remaining in a rigid posture for several seconds. Swarms consist of tens of dauers undulating in the air together, essentially using the neighboring animal as a structure to climb. The base of the swarm is indicated with a red arrow while the top is indicated with a yellow arrow.

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