IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50427-5.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50427-5
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-50427-5?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Devashish Dwivedi & Daniela Harry & Patrick Meraldi, 2023. "Mild replication stress causes premature centriole disengagement via a sub-critical Plk1 activity under the control of ATR-Chk1," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Zimai Li & Bhoomika Bhat & Erik T. Frank & Thalita Oliveira-Honorato & Fumika Azuma & Valérie Bachmann & Darren J. Parker & Thomas Schmitt & Evan P. Economo & Yuko Ulrich, 2023. "Behavioural individuality determines infection risk in clonal ant colonies," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    3. Ryoji Shinya & Simo Sun & Mehmet Dayi & Isheng Jason Tsai & Atsushi Miyama & Anthony Fu Chen & Koichi Hasegawa & Igor Antoshechkin & Taisei Kikuchi & Paul W. Sternberg, 2022. "Possible stochastic sex determination in Bursaphelenchus nematodes," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Vasileios Kotsinis & Alexandros Dritsoulas & Dionysios Ntinokas & Ioannis O. Giannakou, 2023. "Nematicidal Effects of Four Terpenes Differ among Entomopathogenic Nematode Species," Agriculture, MDPI, vol. 13(6), pages 1-11, May.
    5. Dominique A Cowart & Miguel Pinheiro & Olivier Mouchel & Marion Maguer & Jacques Grall & Jacques Miné & Sophie Arnaud-Haond, 2015. "Metabarcoding Is Powerful yet Still Blind: A Comparative Analysis of Morphological and Molecular Surveys of Seagrass Communities," PLOS ONE, Public Library of Science, vol. 10(2), pages 1-26, February.
    6. Maria E Gallegos & Sanjeev Balakrishnan & Priya Chandramouli & Shaily Arora & Aruna Azameera & Anitha Babushekar & Emilee Bargoma & Abdulmalik Bokhari & Siva Kumari Chava & Pranti Das & Meetali Desai , 2012. "The C. elegans Rab Family: Identification, Classification and Toolkit Construction," PLOS ONE, Public Library of Science, vol. 7(11), pages 1-19, November.
    7. Dadong Dai & Chuanshuai Xie & Yayi Zhou & Dexin Bo & Shurong Zhang & Shengqiang Mao & Yucheng Liao & Simeng Cui & Zhaolu Zhu & Xueyu Wang & Fanling Li & Donghai Peng & Jinshui Zheng & Ming Sun, 2023. "Unzipped chromosome-level genomes reveal allopolyploid nematode origin pattern as unreduced gamete hybridization," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    8. Maxim V. Zagoskin & Jianbin Wang & Ashley T. Neff & Giovana M. B. Veronezi & Richard E. Davis, 2022. "Small RNA pathways in the nematode Ascaris in the absence of piRNAs," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50427-5. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.