1. Developmental Biology
  2. Genetics and Genomics
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The rosetteless gene controls development in the choanoflagellate S. rosetta

  1. Tera C Levin
  2. Allison J Greaney
  3. Laura Wetzel
  4. Nicole King  Is a corresponding author
  1. Howard Hughes Medical Institute, University of California, Berkeley, United States
Research Article
  • Cited 30
  • Views 4,450
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Cite this article as: eLife 2014;3:e04070 doi: 10.7554/eLife.04070

Abstract

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 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.

Article and author information

Author details

  1. Tera C Levin

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

  2. Allison J Greaney

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

  3. Laura Wetzel

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

  4. Nicole King

    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.

Reviewing Editor

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

Publication history

  1. Received: July 17, 2014
  2. Accepted: October 8, 2014
  3. Accepted Manuscript published: October 9, 2014 (version 1)
  4. Accepted Manuscript updated: October 10, 2014 (version 2)
  5. Version of Record published: November 4, 2014 (version 3)

Copyright

© 2014, Levin 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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    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 and 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.

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