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Maternal inheritance of functional centrioles in two parthenogenetic nematodes

Author

Listed:
  • Aurélien Perrier

    (Institut Jacques Monod)

  • Nadège Guiglielmoni

    (University of Cologne)

  • Delphine Naquin

    (Institute for Integrative Biology of the Cell (I2BC))

  • Kevin Gorrichon

    (US 039 CEA/INRIA/INSERM
    Direction de la Recherche Fondamentale)

  • Claude Thermes

    (Institute for Integrative Biology of the Cell (I2BC))

  • Sonia Lameiras

    (ICGex Next-Generation Sequencing Platform)

  • Alexander Dammermann

    (Vienna Biocenter Campus (VBC)
    Immunobiology and Genetics)

  • Philipp H. Schiffer

    (University of Cologne)

  • Maia Brunstein

    (Institut de l’Audition)

  • Julie C. Canman

    (Columbia University Irving Medical Center; Department of Pathology and Cell Biology)

  • Julien Dumont

    (Institut Jacques Monod)

Abstract

Centrioles are the core constituent of centrosomes, microtubule-organizing centers involved in directing mitotic spindle assembly and chromosome segregation in animal cells. In sexually reproducing species, centrioles degenerate during oogenesis and female meiosis is usually acentrosomal. Centrioles are retained during male meiosis and, in most species, are reintroduced with the sperm during fertilization, restoring centriole numbers in embryos. In contrast, the presence, origin, and function of centrioles in parthenogenetic species is unknown. We found that centrioles are maternally inherited in two species of asexual parthenogenetic nematodes and identified two different strategies for maternal inheritance evolved in the two species. In Rhabditophanes diutinus, centrioles organize the poles of the meiotic spindle and are inherited by both the polar body and embryo. In Disploscapter pachys, the two pairs of centrioles remain close together and are inherited by the embryo only. Our results suggest that maternally-inherited centrioles organize the embryonic spindle poles and act as a symmetry-breaking cue to induce embryo polarization. Thus, in these parthenogenetic nematodes, centrioles are maternally-inherited and functionally replace their sperm-inherited counterparts in sexually reproducing species.

Suggested Citation

  • Aurélien Perrier & Nadège Guiglielmoni & Delphine Naquin & Kevin Gorrichon & Claude Thermes & Sonia Lameiras & Alexander Dammermann & Philipp H. Schiffer & Maia Brunstein & Julie C. Canman & Julien Du, 2024. "Maternal inheritance of functional centrioles in two parthenogenetic nematodes," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50427-5
    DOI: 10.1038/s41467-024-50427-5
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    References listed on IDEAS

    as
    1. Mark L. Blaxter & Paul De Ley & James R. Garey & Leo X. Liu & Patsy Scheldeman & Andy Vierstraete & Jacques R. Vanfleteren & Laura Y. Mackey & Mark Dorris & Linda M. Frisse & J. T. Vida & W. Kelley Th, 1998. "A molecular evolutionary framework for the phylum Nematoda," Nature, Nature, vol. 392(6671), pages 71-75, March.
    2. Meng-Fu Bryan Tsou & Tim Stearns, 2006. "Mechanism limiting centrosome duplication to once per cell cycle," Nature, Nature, vol. 442(7105), pages 947-951, August.
    3. Carrie R. Cowan & Anthony A. Hyman, 2004. "Centrosomes direct cell polarity independently of microtubule assembly in C. elegans embryos," Nature, Nature, vol. 431(7004), pages 92-96, September.
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