1. Evolutionary Biology
  2. Genetics and Genomics

Predicted glycosyltransferases promote development and prevent spurious cell clumping in the choanoflagellate S. rosetta

  1. Laura A Wetzel
  2. Tera C Levin
  3. Ryan E Hulett
  4. Daniel Chan
  5. Grant A King
  6. Reef Aldayafleh
  7. David S Booth
  8. Monika Abedin Sigg
  9. Nicole King  Is a corresponding author
  1. Howard Hughes Medical Institute, University of California, Berkeley, United States
https://doi.org/10.7554/eLife.41482
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Cite this article
  1. Laura A Wetzel
  2. Tera C Levin
  3. Ryan E Hulett
  4. Daniel Chan
  5. Grant A King
  6. Reef Aldayafleh
  7. David S Booth
  8. Monika Abedin Sigg
  9. Nicole King
(2018)
Predicted glycosyltransferases promote development and prevent spurious cell clumping in the choanoflagellate S. rosetta
eLife 7:e41482.
https://doi.org/10.7554/eLife.41482
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  3. Download .RIS

Abstract

In a previous study we established forward genetics in the choanoflagellate Salpingoeca rosetta and found that a C-type lectin gene is required for rosette development (Levin et al. 2014). Here we report on critical improvements to genetic screens in S. rosetta while also investigating the genetic basis for rosette defect mutants in which single cells fail to develop into orderly rosettes but instead aggregate promiscuously into amorphous clumps of cells. Two of the mutants, Jumble and Couscous, mapped to lesions in genes encoding two different predicted glycosyltransferases and displayed aberrant glycosylation patterns in the basal extracellular matrix (ECM). In animals, glycosyltransferases sculpt the polysaccharide-rich ECM, regulate integrin and cadherin activity, and, when disrupted, contribute to tumorigenesis. The finding that predicted glycosyltransferases promote proper rosette development and prevent cell aggregation in S. rosetta suggests a pre-metazoan role for glycosyltransferases in regulating development and preventing abnormal tumor-like multicellularity.

Data availability

Data have been deposited to the NCBI Sequence Read Archive under the project number PRJNA490902.

The following data sets were generated

Article and author information

Author details

  1. Laura A Wetzel

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Tera C Levin

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7883-8522

  3. Ryan E Hulett

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Daniel Chan

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Grant A King

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Reef Aldayafleh

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. David S Booth

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

  8. Monika Abedin Sigg

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

  9. Nicole King

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    For correspondence
    nking@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6409-1111

Funding

Howard Hughes Medical Institute

  • Laura A Wetzel
  • Tera C Levin
  • Ryan E Hulett
  • Daniel Chan
  • Grant A King
  • Reef Aldayafleh
  • David S Booth
  • Monika Abedin Sigg
  • Nicole King

Jane Coffin Childs Memorial Fund for Medical Research (Simons Fellow)

  • David S Booth

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

Reviewing Editor

  1. Alejandro Sánchez Alvarado, Stowers Institute for Medical Research, United States

Version history

  1. Received: September 5, 2018
  2. Accepted: December 14, 2018
  3. Accepted Manuscript published: December 17, 2018 (version 1)
  4. Version of Record published: January 7, 2019 (version 2)

Copyright

© 2018, Wetzel 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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  1. Laura A Wetzel
  2. Tera C Levin
  3. Ryan E Hulett
  4. Daniel Chan
  5. Grant A King
  6. Reef Aldayafleh
  7. David S Booth
  8. Monika Abedin Sigg
  9. Nicole King
(2018)
Predicted glycosyltransferases promote development and prevent spurious cell clumping in the choanoflagellate S. rosetta
eLife 7:e41482.
https://doi.org/10.7554/eLife.41482

Share this article

https://doi.org/10.7554/eLife.41482

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    The rosetteless gene controls development in the choanoflagellate S. rosetta

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    The origin of animal multicellularity may be reconstructed by comparing animals with one of their closest living relatives, the choanoflagellate Salpingoeca rosetta. Just as animals develop from a single cell–the zygote–multicellular rosettes of S. rosetta develop from a founding cell. To investigate rosette development, we established forward genetics in S. rosetta. We find that the rosette defect of one mutant, named Rosetteless, maps to a predicted C-type lectin, a class of signaling and adhesion genes required for the development and innate immunity in animals. Rosetteless protein is essential for rosette development and forms an extracellular layer that coats and connects the basal poles of each cell in rosettes. This study provides the first link between genotype and phenotype in choanoflagellates and raises the possibility that a protein with C-type lectin-like domains regulated development in the last common ancestor of choanoflagellates and animals.

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