Distinct functions of three Wnt proteins control mirror-symmetric organogenesis in the C. elegans gonad

  1. Shuhei So
  2. Masayo Asakawa
  3. Hitoshi Sawa  Is a corresponding author
  1. Hamamatsu University School of Medicine, Japan
  2. National Institute of Genetics, Japan

Abstract

Organogenesis requires the proper production of diverse cell types and their positioning/migration. However, the coordination of these processes during development remains poorly understood. The gonad in C. elegans exhibits a mirror-symmetric structure guided by the migration of distal tip cells (DTCs), which result from asymmetric divisions of somatic gonadal precursors (SGPs; Z1 and Z4). We found that the polarity of Z1 and Z4, which possess mirror-symmetric orientation, is controlled by the redundant functions of the LIN-17/Frizzled receptor and three Wnt proteins (CWN-1, CWN-2, and EGL-20) with distinct functions. In lin-17 mutants, CWN-2 promotes normal polarity in both Z1 and Z4, while CWN-1 promotes reverse and normal polarity in Z1 and Z4, respectively. In contrast, EGL-20 inhibits the polarization of both Z1 and Z4. In lin-17 egl-20 cwn-2 triple mutants with a polarity reversal of Z1, DTCs from Z1 frequently miss-migrate to the posterior side. Our further analysis demonstrates that the mis-positioning of DTCs in the gonad due to the polarity reversal of Z1 leads to mis-migration. Similar mis-migration was also observed in cki-1(RNAi) animals producing ectopic DTCs. These results highlight the role of Wnt signaling in coordinating the production and migration of DTCs to establish a mirror-symmetric organ.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files; source data files have been provided for Figures 3 and 4.

Article and author information

Author details

  1. Shuhei So

    Hamamatsu University School of Medicine, Hamamatsu, Japan
    Competing interests
    The authors declare that no competing interests exist.
  2. Masayo Asakawa

    National Institute of Genetics, Mishima, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Hitoshi Sawa

    National Institute of Genetics, Mishima, Japan
    For correspondence
    hisawa@nig.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9774-7976

Funding

Japan Society for the Promotion of Science (JP16H04797)

  • Hitoshi Sawa

Takeda Science Foundation

  • Hitoshi Sawa

NIG-JOINT (88A2024)

  • Shuhei So

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

Copyright

© 2024, So et al.

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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  1. Shuhei So
  2. Masayo Asakawa
  3. Hitoshi Sawa
(2024)
Distinct functions of three Wnt proteins control mirror-symmetric organogenesis in the C. elegans gonad
eLife 13:e103035.
https://doi.org/10.7554/eLife.103035

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https://doi.org/10.7554/eLife.103035

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