Insulin signaling and osmotic stress response regulate arousal and developmental progression of <i>C. elegans</i> at hatching

Bayer, Emily A.; Liberatore, Katarina; Schneider, Jordan R; Schlesinger, Evan; He, Zhengying; Birnbaum, Susanna; Wightman, Bruce

doi:10.1093/genetics/iyab202

Cited by 6 publications

(12 citation statements)

References 72 publications

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“…We identify SWT as a new form of behavioral quiescence, occurring during embryogenesis. Osmotic stress and reduced insulin signalling cause behavioral quiescence around hatching, which is accompanied by developmental arrest (Bayer et al, 2021). The salt and insulin regulated quiescence and SWT quiescence occur at a similar stage of embryonic development and both require FLP-11, suggesting that these two forms of quiescence are mechanistically related.…”

Section: Discussionmentioning

confidence: 99%

“…A PREPRINT -JULY 19,2022 Early flipping behavior is followed by a period of decreased motion. This slowdown is apparently not neuronally evoked, as it requires neither neuropeptide processing enzymes nor UNC-13 (Fig.…”

Section: Three Phases Of Embryonic Behaviormentioning

confidence: 99%

“…A PREPRINT -JULY 19,2022 For calcium imaging in RIS, plasmid KP#4525 was generated by inserting the flp-11 promoter (3159 bp), GCaMP6f with introns, a flexible linker (GSSTSG(AP) 7 ASEF), mCherry with introns, and the unc-54 3' UTR between the SbfI and StuI sites in pCFJ910.…”

Section: Strains and Reagentsmentioning

confidence: 99%

“…Embryos are small (~50x30x30 µm 3 ) and transparent, enabling in vivo imaging of cell migration, neurite growth, synaptogenesis, neuronal activity, and behavior during the mere ~14 hours from fertilization to hatching (Shah et al, 2017;Barnes et al, 2020;Heiman & Shaham, 2009;Fan et al, 2019;Christensen et al, 2015;McDonald et al, 2020;Sengupta et al, 2020;Ardiel et al, 2017;Hall & Hedgecock, 1991;Atakan et al, 2020;Bayer et al, 2021). C. elegans boasts a sophisticated molecular genetic toolkit, a complete neuronal wiring diagram, and a comprehensive atlas of single cell gene expression across embryogenesis (White et al, 1986;Cook et al, 2019;Witvliet et al, 2021;Packer et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…C. elegans offers several advantages for investigating the emergence of functional neuronal circuitry and behavior. Embryos are small (≈ 50 x 30 x 30 μm 3 ) and transparent, enabling in vivo imaging of cell migration, neurite growth, synaptogenesis, neuronal activity, and behavior during the mere ≈14 hours from fertilization to hatching [8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19]. In addition, C. elegans boasts a sophisticated molecular genetic toolkit, a complete neuronal wiring diagram, and a comprehensive atlas of single cell gene expression across embryogenesis [20, 21, 22, 23].…”

Section: Introductionmentioning

confidence: 99%

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Stereotyped Behavioral Maturation and Rhythmic Quiescence in C. elegans Embryos

Ardiel

Lauziere

et al. 2021

Preprint

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Systematic analysis of rich behavioral recordings is being used to uncover how circuits encode complex behaviors. Here we apply the approach to embryos. What are the first embryonic behaviors and how do they evolve as early neurodevelopment ensues? To address these questions, we present a systematic description of behavioral maturation for Caenorhabditis elegans embryos. Posture libraries were derived from a genetically encoded motion capture suit imaged with light-sheet microscopy and annotated using custom semi-automated tracking software (Multiple Hypothesis Hypergraph Tracking; MHHT). Analysis of cell trajectories, postures, and behavioral motifs revealed a stereotyped developmental progression. Early movement is dominated by flipping between dorsal and ventral coiling, which gradually slows into a period of reduced motility. Late-stage embryos exhibit sinusoidal waves of dorsoventral bends, prolonged bouts of directed motion, and a rhythmic pattern of pausing, which we designate slow wave twitch (SWT). Synaptic transmission is required for late-stage motion but not for early flipping or the intervening inactive phase. A high-throughput behavioral assay and calcium imaging revealed that SWT is elicited by the rhythmic activity of a quiescence-promoting neuron (RIS). Similar periodic quiescent states are seen prenatally in divergent animals and may play an important role in promoting normal developmental outcomes.

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Section: Discussionmentioning

confidence: 99%

Section: Three Phases Of Embryonic Behaviormentioning

confidence: 99%

Section: Strains and Reagentsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Stereotyped Behavioral Maturation and Rhythmic Quiescence in C. elegans Embryos

Ardiel

Lauziere

et al. 2021

Preprint

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A spiral microfluidic device for rapid sorting, trapping, and long-term live imaging of Caenorhabditis elegans embryos

Pan

Qin

Sun³

et al. 2023

Microsyst Nanoeng

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Caenorhabditis elegans embryos have been widely used to study cellular processes and developmental regulation at early stages. However, most existing microfluidic devices focus on the studies of larval or adult worms rather than embryos. To accurately study the real-time dynamics of embryonic development under different conditions, many technical barriers must be overcome; these can include single-embryo sorting and immobilization, precise control of the experimental environment, and long-term live imaging of embryos. This paper reports a spiral microfluidic device for effective sorting, trapping, and long-term live imaging of single C. elegans embryos under precisely controlled experimental conditions. The device successfully sorts embryos from a mixed population of C. elegans at different developmental stages via Dean vortices generated inside a spiral microchannel and traps the sorted embryos at single-cell resolution through hydrodynamic traps on the sidewall of the spiral channel for long-term imaging. Through the well-controlled microenvironment inside the microfluidic device, the response of the trapped C. elegans embryos to mechanical and chemical stimulation can be quantitatively measured. The experimental results show that a gentle hydrodynamic force would induce faster growth of embryos, and embryos developmentally arrested in the high-salinity solution could be rescued by the M9 buffer. The microfluidic device provides new avenues for easy, rapid, high-content screening of C. elegans embryos.

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Periods of environmental sensitivity couple larval behavior and development

Faerberg¹,

Aprison²,

Ruvinsky³

2023

Preprint

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SummaryThe typical life cycle in most animal phyla includes a larval period that bridges embryogenesis and adulthood1. Despite the great diversity of larval forms, all larvae grow, acquire adult morphology and function, while navigating their habitats to obtain resources necessary for development. How larval development is coordinated with behavior remains substantially unclear. Here, we describe features of the iterative organization of larval stages that serve to assess the environment and procure resources prior to costly developmental commitments. We found that male-excreted pheromones accelerate2-4the onset of adulthood inC. eleganshermaphrodites by coordinately advancing multiple developmental events and growth during the last larval stage. The larvae are sensitive to the accelerating male pheromones only at the end of the penultimate larval stage, just before the acceleration begins. Other larval stages also contain windows of sensitivity to environmental inputs. Importantly, behaviors associated with search and consumption of food are distinct between early and late portions of larval stages. We infer that each larval stage inC. elegansis subdivided into two epochs: A) global assessment of the environment to identify the most suitable patch and B) consumption of sufficient food and acquisition of salient information for developmental events in the next stage. We predict that in larvae of other species behavior is also divided into distinct epochs optimized either for assessing the habitat or obtaining the resources. Thus, a major role of larval behavior is to coordinate the orderly progression of development in variable environments.“Life is what happens to you when you’re busy making other plans.”Allen Saunders (popularized by John Lennon)

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Insulin signaling and osmotic stress response regulate arousal and developmental progression of C. elegans at hatching

Cited by 6 publications

References 72 publications

Stereotyped Behavioral Maturation and Rhythmic Quiescence in C. elegans Embryos

Stereotyped Behavioral Maturation and Rhythmic Quiescence in C. elegans Embryos

A spiral microfluidic device for rapid sorting, trapping, and long-term live imaging of Caenorhabditis elegans embryos

Periods of environmental sensitivity couple larval behavior and development

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