Automated C. elegans embryo alignments reveal brain neuropil position invariance despite lax cell body placement

PLoS One. 2018 Mar 28;13(3):e0194861. doi: 10.1371/journal.pone.0194861. eCollection 2018.

Abstract

The Caenorhabditis elegans cell lineage is nearly invariant. Whether this stereotyped cell-division pattern promotes reproducibility in cell shapes/positions is not generally known, as manual spatiotemporal cell-shape/position alignments are labor-intensive, and fully-automated methods are not described. Here, we report automated algorithms for spatiotemporal alignments of C. elegans embryos from pre-morphogenesis to motor-activity initiation. We use sparsely-labeled green-fluorescent nuclei and a pan-nuclear red-fluorescent reporter to register consecutive imaging time points and compare embryos. Using our method, we monitor early assembly of the nerve-ring (NR) brain neuropil. While NR pioneer neurons exhibit reproducible growth kinetics and axon positions, cell-body placements are variable. Thus, pioneer-neuron axon locations, but not cell-body positions, are under selection. We also show that anterior NR displacement in cam-1/ROR Wnt-receptor mutants is not an early NR assembly defect. Our results demonstrate the utility of automated spatiotemporal alignments of C. elegans embryos, and uncover key principles guiding nervous-system development in this animal.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Algorithms
  • Animals
  • Automation
  • Brain / cytology*
  • Brain / metabolism
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / growth & development*
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Body / physiology*
  • Cell Lineage*
  • Embryo, Nonmammalian / cytology*
  • Embryo, Nonmammalian / metabolism
  • Neurogenesis / physiology
  • Neuropil / cytology*
  • Neuropil / metabolism
  • Spatio-Temporal Analysis

Substances

  • Caenorhabditis elegans Proteins