A spatiotemporal reconstruction of the C. elegans pharyngeal cuticle reveals a structure rich in phase-separating proteins
- University of Toronto, Canada
- Hospital for Sick Children, Canada
- Wroclaw University of Science and Technolog, Poland
- St. Jude Children's Research Hospital, United States
- Eötvös Loránd University, Hungary
- Tsinghua University, China
- Peking University, China
- Wroclaw University of Science and Technology, Poland
Abstract
How the cuticles of the roughly 4.5 million species of ecdysozoan animals are constructed is not well understood. Here, we systematically mine gene expression datasets to uncover the spatiotemporal blueprint for how the chitin-based pharyngeal cuticle of the nematode Caenorhabditis elegans is built. We demonstrate that the blueprint correctly predicts expression patterns and functional relevance to cuticle development. We find that as larvae prepare to molt, catabolic enzymes are upregulated and the genes that encode chitin synthase, chitin cross-linkers, and homologs of amyloid regulators subsequently peak in expression. 48% of the gene products secreted during the molt are predicted to be intrinsically disordered proteins (IDPs), many of which belong to four distinct families whose transcripts are expressed in overlapping waves. These include the IDPAs, IDPBs, and IDPCs, which are introduced for the first time here. All four families have sequence properties that drive phase separation and we demonstrate phase-separation for one exemplar in vitro. This systematic analysis represents the first blueprint for cuticle construction and highlights the massive contribution that phase-separating materials make to the structure.
Data availability
All source data for the spatiotemporal reconstruction is in the Source data files
Article and author information
Author details
Jakub W Wojciechowski
Julie Deborah Forman-Kay
Funding
NKFI (127909)
- Kristóf Takács
- Vince Grolmusz
National Science Foundation (1616265)
- Michael P Hughes
National Science Centre, Poland
- Malgorzata Kotulska
Canadian Institutes of Health Research (376634)
- Peter J Roy
Canadian Institutes of Health Research (313296)
- Peter J Roy
National Science and Engineering Council of Canada
- Jessica Knox
Canada Research Chairs
- Peter J Roy
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Luisa Cochella, Johns Hopkins University School of Medicine, United States
Version history
- Preprint posted: March 14, 2022 (view preprint)
- Received: April 11, 2022
- Accepted: October 11, 2022
- Accepted Manuscript published: October 19, 2022 (version 1)
- Version of Record published: November 2, 2022 (version 2)
Copyright
© 2022, Kamal et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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A spatiotemporal reconstruction of the C. elegans pharyngeal cuticle reveals a structure rich in phase-separating proteins
eLife 11:e79396.
https://doi.org/10.7554/eLife.79396
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