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 38
  • Views 4,878
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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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Further reading

    1. Developmental Biology
    2. Genetics and Genomics

    Genome editing enables reverse genetics of multicellular development in the choanoflagellate Salpingoeca rosetta

    David S Booth, Nicole King
    Research Advance Updated

    In a previous study, we established a forward genetic screen to identify genes required for multicellular development in the choanoflagellate, Salpingoeca rosetta (Levin et al., 2014). Yet, the paucity of reverse genetic tools for choanoflagellates has hampered direct tests of gene function and impeded the establishment of choanoflagellates as a model for reconstructing the origin of their closest living relatives, the animals. Here we establish CRISPR/Cas9-mediated genome editing in S. rosetta by engineering a selectable marker to enrich for edited cells. We then use genome editing to disrupt the coding sequence of a S. rosetta C-type lectin gene, rosetteless, and thereby demonstrate its necessity for multicellular rosette development. This work advances S. rosetta as a model system in which to investigate how genes identified from genetic screens and genomic surveys function in choanoflagellates and evolved as critical regulators of animal biology.

    1. Evolutionary Biology
    2. Genetics and Genomics

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

    Laura A Wetzel et al.
    Research Advance Updated

    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.

    1. Developmental Biology
    2. Genetics and Genomics

    Multicellularity: Forward genetics for back-in-time questions

    Alex de Mendoza, Iñaki Ruiz-Trillo
    Insight

    A genetic screen has revealed one of the molecules that allow choanoflagellates, the closest unicellular relative of animals, to form colonies, which could help researchers to answer questions about the earliest days of animal evolution.