Generic injuries are sufficient to induce ectopic Wnt organizers in Hydra

  1. Jack F Cazet
  2. Adrienne Cho
  3. Celina Juliano  Is a corresponding author
  1. University of California, Davis, United States

Abstract

During whole-body regeneration, a bisection injury can trigger two different types of regeneration. To understand the transcriptional regulation underlying this adaptive response we characterized transcript abundance and chromatin accessibility during oral and aboral regeneration in the cnidarian Hydra vulgaris. We found that the initial response to amputation at both wound sites is identical and includes widespread apoptosis and the activation of the oral-specifying Wnt signaling pathway. By 8 hours post-amputation, Wnt signaling became restricted to oral regeneration. Wnt pathway genes were also upregulated in puncture wounds and these wounds induced the formation of ectopic oral structures if pre-existing organizers were simultaneously amputated. Our work suggests that oral patterning is activated as part of a generic injury response in Hydra, and that alternative injury outcomes are dependent on signals from the surrounding tissue. Furthermore, Wnt signaling is likely part of a conserved wound response predating the split of cnidarians and bilaterians.

Data availability

All code used in this study is available both as a git repository at github.com/cejuliano/jcazet_regeneration_patterning and on Dryad at doi.org/10.25338/B8S612. FASTQ files of raw ATAC-seq and RNA-seq reads, expression matrices for ATAC-seq and RNA-seq reads mapped to the Hydra 2.0 genome reference, consensus peak files, and bigwig genome tracks of individual and pooled ATAC-seq replicates are available through the Gene Expression Omnibus under the accession GSE152994. The Hydra 2.0 genome gene model IDs associated with the gene names used throughout this study are provided in Figure 1-Figure Supplement 8. Full differential gene expression results are available in Supplementary Files 1 and 2. Motif enrichment and variability results are available in Supplementary File 3.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Jack F Cazet

    Molecular and Cellular Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7331-5631
  2. Adrienne Cho

    Molecular and Cellular Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Celina Juliano

    Molecular and Cellular Biology, University of California, Davis, Davis, United States
    For correspondence
    cejuliano@ucdavis.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4222-0987

Funding

National Institutes of Health (R35 GM133689)

  • Celina Juliano

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2021, Cazet 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.

Metrics

  • 3,771
    views
  • 386
    downloads
  • 38
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Jack F Cazet
  2. Adrienne Cho
  3. Celina Juliano
(2021)
Generic injuries are sufficient to induce ectopic Wnt organizers in Hydra
eLife 10:e60562.
https://doi.org/10.7554/eLife.60562

Share this article

https://doi.org/10.7554/eLife.60562

Further reading

    1. Cell Biology
    2. Developmental Biology
    Sarah Y Coomson, Salil A Lachke
    Insight

    A study in mice reveals key interactions between proteins involved in fibroblast growth factor signaling and how they contribute to distinct stages of eye lens development.

    1. Developmental Biology
    Jing Lu, Hao Xu ... Kai Lei
    Tools and Resources

    The intricate coordination of the neural network in planarian growth and regeneration has remained largely unrevealed, partly due to the challenges of imaging the CNS in three dimensions (3D) with high resolution and within a reasonable timeframe. To address this gap in systematic imaging of the CNS in planarians, we adopted high-resolution, nanoscale imaging by combining tissue expansion and tiling light-sheet microscopy, achieving up to fourfold linear expansion. Using an automatic 3D cell segmentation pipeline, we quantitatively profiled neurons and muscle fibers at the single-cell level in over 400 wild-type planarians during homeostasis and regeneration. We validated previous observations of neuronal cell number changes and muscle fiber distribution. We found that the increase in neuron cell number tends to lag behind the rapid expansion of somatic cells during the later phase of homeostasis. By imaging the planarian with up to 120 nm resolution, we also observed distinct muscle distribution patterns at the anterior and posterior poles. Furthermore, we investigated the effects of β-catenin-1 RNAi on muscle fiber distribution at the posterior pole, consistent with changes in anterior-posterior polarity. The glial cells were observed to be close in contact with dorsal-ventral muscle fibers. Finally, we observed disruptions in neural-muscular networks in inr-1 RNAi planarians. These findings provide insights into the detailed structure and potential functions of the neural-muscular system in planarians and highlight the accessibility of our imaging tool in unraveling the biological functions underlying their diverse phenotypes and behaviors.