Evolution of New cis-Regulatory Motifs Required for Cell-Specific Gene Expression in Caenorhabditis

Abstract : Patterning of C. elegans vulval cell fates relies on inductive signaling. In this induction event, a single cell, the gonadal anchor cell, secretes LIN-3/EGF and induces three out of six competent precursor cells to acquire a vulval fate. We previously showed that this developmental system is robust to a four-fold variation in lin-3/EGF genetic dose. Here using single-molecule FISH, we find that the mean level of expression of lin-3 in the anchor cell is remarkably conserved. No change in lin-3 expression level could be detected among C. elegans wild isolates and only a low level of change-less than 30%-in the Caenorhabditis genus and in Oscheius tipulae. In C. elegans, lin-3 expression in the anchor cell is known to require three transcription factor binding sites, specifically two E-boxes and a nuclear-hormone-receptor (NHR) binding site. Mutation of any of these three elements in C. elegans results in a dramatic decrease in lin-3 expression. Yet only a single E-box is found in the Drosophilae supergroup of Caenorhabditis species, including C. angaria, while the NHR-binding site likely only evolved at the base of the Elegans group. We find that a transgene from C. angaria bearing a single E-box is sufficient for normal expression in C. elegans. Even a short 58 bp cis-regulatory fragment from C. angaria with this single E-box is able to replace the three transcription factor binding sites at the endogenous C. elegans lin-3 locus, resulting in the wild-type expression level. Thus, regulatory evolution occurring in cis within a 58 bp lin-3 fragment, results in a strict requirement for the NHR binding site and a second E-box in C. elegans. This single-cell, single-molecule, quantitative and functional evo-devo study demonstrates that conserved expression levels can hide extensive change in cis-regulatory site requirements and highlights the evolution of new cis-regulatory elements required for cell-specific gene expression.
Complete list of metadatas

Cited literature [72 references]  Display  Hide  Download

https://www.hal.inserm.fr/inserm-02159894
Contributor : Myriam Bodescot <>
Submitted on : Wednesday, June 19, 2019 - 10:09:47 AM
Last modification on : Thursday, June 20, 2019 - 1:35:34 AM

File

journal.pgen.1006278.PDF
Publication funded by an institution

Identifiers

Collections

Citation

Michalis Barkoulas, Amhed Vargas Velazquez, Alexandre Peluffo, Marie-Anne Félix. Evolution of New cis-Regulatory Motifs Required for Cell-Specific Gene Expression in Caenorhabditis. PLoS Genetics, Public Library of Science, 2016, 12 (9), pp.e1006278. ⟨10.1371/journal.pgen.1006278⟩. ⟨inserm-02159894⟩

Share

Metrics

Record views

25

Files downloads

51