A Cell Fate Switch in theCaenorhabditis elegansSeam Cell Lineage Occurs Through Modulation of the Wnt Asymmetry Pathway in Response to Temperature Increase

Abstract

Populations often display consistent developmental phenotypes across individuals despite inevitable biological stochasticity. Nevertheless, developmental robustness has limits, and systems can fail upon change in the environment or the genetic background. We use here the seam cells, a population of epidermal stem cells in Caenorhabditis elegans, to study the influence of temperature change and genetic variation on cell fate. Seam cell development has mostly been studied so far in the laboratory reference strain (N2), grown at 20° temperature. We demonstrate that an increase in culture temperature to 25° introduces variability in the wild-type seam cell lineage, with a proportion of animals showing an increase in seam cell number. We map this increase to lineage-specific symmetrization events of normally asymmetric cell divisions at the fourth larval stage, leading to the retention of seam cell fate in both daughter cells. Using genetics and single-molecule imaging, we demonstrate that this symmetrization occurs via changes in the Wnt asymmetry pathway, leading to aberrant Wnt target activation in anterior cell daughters. We find that intrinsic differences in the Wnt asymmetry pathway already exist between seam cells at 20° and this may sensitize cells toward a cell fate switch at increased temperature. Finally, we demonstrate that wild isolates of C. elegans display variation in seam cell sensitivity to increased culture temperature, although their average seam cell number is comparable at 20°. Our results highlight how temperature can modulate cell fate decisions in an invertebrate model of stem cell patterning.

Visualizing the metazoan proliferation-quiescence decision in vivo

“…However, not all cell divisions that give rise to the 959 somatic cells are completely invariant. Studies have identified several lineages, including the vulva, where environmental stressors, genetic mutations and/or genetic divergence of wild isolates leads to stochastic changes in a highly invariant cell fate pattern ( Braendle and Félix, 2008 ; Hintze et al, 2020 ; Katsanos et al, 2017 ). Thus, we wondered if the CDK sensor generated here could be utilized to visualize and predict stochastic lineage decisions during C. elegans development.…”

A role for the fusogen eff-1 in epidermal stem cell number robustness in Caenorhabditis elegans

“…S2 ). However, seam cell number and variance in wild type is mildly increased at 25 °C compared to 20 °C as previously reported 10 , therefore we chose to use 20° as the temperature for all our experiments.…”

“…( k – l ) Loss of cell contact between V2 and V3 daughter cells in eff-1(icb4) at the L2 asymmetric cell division ( k ), marked with an arrowhead, in comparison to wild-type ( l ). Seam cells are visualised using the scm::GFP marker, as well as seam cell driven membrane-targeted GFP (GFP::CAAX) 10 ) ( e – j ) or ajm-1p::ajm-1::GFP ( k – l ). Scale bars in a-h, k and l are 20 µm and in i-j 100 µm.…”

“…Asymmetric cell divisions are reiterative throughout development, and the most common case involves an anterior daughter cell that differentiates into a neuron or epidermal cell, while the posterior daughter retains the seam cell fate. These division and differentiation patterns give rise to 16 seam cells per lateral side in wild-type animals at the end of larval development, a number which is robust in standard growth conditions, although it can be sensitive to temperature increase 9 , 10 .…”

Chemosensory Neurons Modulate the Response to Oomycete Recognition in Caenorhabditis elegans

“…Single molecule FISH was performed as previously described ( Hintze et al., 2020 ; Katsanos et al., 2017 ). Briefly, animals were synchronized by bleaching and treated with extract for 1 hour at mid-L2 stage.…”