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

Mol Syst Biol. 2020 Jul;16(7):e9498. doi: 10.15252/msb.20209498.

Abstract

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.

Keywords: SNIC; bifurcation; checkpoint; development; oscillator.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biological Clocks / genetics*
  • Caenorhabditis elegans / embryology
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / growth & development
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Gastrulation / genetics
  • Gene Expression Profiling
  • Gene Expression Regulation, Developmental / genetics
  • Gene Ontology
  • Genes, Reporter
  • Humans
  • Larva / genetics
  • Larva / growth & development
  • Larva / metabolism*
  • Models, Theoretical
  • Molting / genetics*
  • Organ Specificity
  • RNA-Seq
  • Spatio-Temporal Analysis
  • Time Factors

Substances

  • Caenorhabditis elegans Proteins

Associated data

  • GEO/GSE133576