Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans

• Published in: Molecular systems biology Vol. 16; no. 7; pp. e9498 - n/a
• Main Authors: Meeuse, Milou WM, Hauser, Yannick P, Morales Moya, Lucas J, Hendriks, Gert‐Jan, Eglinger, Jan, Bogaarts, Guy, Tsiairis, Charisios, Großhans, Helge
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.07.2020; EMBO Press; John Wiley and Sons Inc; Springer Nature
• Subjects: bifurcation; Bifurcations; Caenorhabditis elegans; checkpoint; Circadian rhythm; development; Developmental stages; EMBO11; Embryos; Gene expression; Hatching; Larvae; Larval development; Mathematical models; Molting; Nematodes; Oscillations; oscillator; Oscillators; Perturbation; SNIC; Temporal resolution; checkpoint; bifurcation; development; oscillator; SNIC
• ISSN: 1744-4292; 1744-4292
• DOI: 10.15252/msb.20209498

Gene expression oscillators can structure biological events temporally and spatially. Different biological functions benefit from distinct oscillator properties. Thus, finite developmental processes rely on oscillators that start and stop at specific times, a poorly understood behavior. Here, we have characterized a massive gene expression oscillator comprising > 3,700 genes in Caenorhabditis elegans larvae. We report that oscillations initiate in embryos, arrest transiently after hatching and in response to perturbation, and cease in adults. Experimental observation of the transitions between oscillatory and non‐oscillatory states at high temporal resolution reveals an oscillator operating near a Saddle Node on Invariant Cycle (SNIC) bifurcation. These findings constrain the architecture and mathematical models that can represent this oscillator. They also reveal that oscillator arrests occur reproducibly in a specific phase. Since we find oscillations to be coupled to developmental processes, including molting, this characteristic of SNIC bifurcations endows the oscillator with the potential to halt larval development at defined intervals, and thereby execute a developmental checkpoint function. Synopsis The authors investigate a putative developmental clock in C. elegans . Population‐ and single animal‐based analyses uncover a gene expression oscillator that may support a developmental checkpoint function. Extensive rhythmic gene expression in C. elegans larvae is initiated in embryos and is coupled to molting. The oscillator is arrested in a specific phase (normally observed at molt exit) in adults, early L1 and dauer larvae. A bifurcation of the oscillator constitutes a putative developmental checkpoint mechanism. Characteristics of oscillation onset and offset constrain potential oscillator mechanisms as well as mathematical models and their parameters. Graphical Abstract The authors investigate a putative developmental clock in C. elegans . Population‐ and single animal‐based analyses uncover a gene expression oscillator that may support a developmental checkpoint function.