IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-023-44411-8.html
   My bibliography  Save this article

The evolution of centriole degradation in mouse sperm

Author

Listed:
  • Sushil Khanal

    (University of Toledo)

  • Ankit Jaiswal

    (University of Toledo)

  • Rajanikanth Chowdanayaka

    (University of Mysore)

  • Nahshon Puente

    (University of Toledo)

  • Katerina Turner

    (University of Toledo)

  • Kebron Yeshitela Assefa

    (University of Toledo)

  • Mohamad Nawras

    (University of Toledo)

  • Ezekiel David Back

    (University of Toledo)

  • Abigail Royfman

    (University of Toledo)

  • James P. Burkett

    (University of Toledo)

  • Soon Hon Cheong

    (Cornell University)

  • Heidi S. Fisher

    (University of Maryland College Park)

  • Puneet Sindhwani

    (University of Toledo)

  • John Gray

    (University of Toledo)

  • Nallur Basappa Ramachandra

    (University of Mysore)

  • Tomer Avidor-Reiss

    (University of Toledo
    University of Toledo)

Abstract

Centrioles are subcellular organelles found at the cilia base with an evolutionarily conserved structure and a shock absorber-like function. In sperm, centrioles are found at the flagellum base and are essential for embryo development in basal animals. Yet, sperm centrioles have evolved diverse forms, sometimes acting like a transmission system, as in cattle, and sometimes becoming dispensable, as in house mice. How the essential sperm centriole evolved to become dispensable in some organisms is unclear. Here, we test the hypothesis that this transition occurred through a cascade of evolutionary changes to the proteins, structure, and function of sperm centrioles and was possibly driven by sperm competition. We found that the final steps in this cascade are associated with a change in the primary structure of the centriolar inner scaffold protein FAM161A in rodents. This information provides the first insight into the molecular mechanisms and adaptive evolution underlying a major evolutionary transition within the internal structure of the mammalian sperm neck.

Suggested Citation

  • Sushil Khanal & Ankit Jaiswal & Rajanikanth Chowdanayaka & Nahshon Puente & Katerina Turner & Kebron Yeshitela Assefa & Mohamad Nawras & Ezekiel David Back & Abigail Royfman & James P. Burkett & Soon , 2024. "The evolution of centriole degradation in mouse sperm," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44411-8
    DOI: 10.1038/s41467-023-44411-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-44411-8
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-44411-8?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. Dean Clift & Melina Schuh, 2015. "A three-step MTOC fragmentation mechanism facilitates bipolar spindle assembly in mouse oocytes," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
    2. Emily L. Fishman & Kyoung Jo & Quynh P. H. Nguyen & Dong Kong & Rachel Royfman & Anthony R. Cekic & Sushil Khanal & Ann L. Miller & Calvin Simerly & Gerald Schatten & Jadranka Loncarek & Vito Mennella, 2018. "Author Correction: A novel atypical sperm centriole is functional during human fertilization," Nature Communications, Nature, vol. 9(1), pages 1-1, December.
    3. Amy G Rowley & Toby S Daly-Engel & John L Fitzpatrick, 2019. "Testes size increases with sperm competition risk and intensity in bony fish and sharks," Behavioral Ecology, International Society for Behavioral Ecology, vol. 30(2), pages 364-371.
    4. Emily L. Fishman & Kyoung Jo & Quynh P. H. Nguyen & Dong Kong & Rachel Royfman & Anthony R. Cekic & Sushil Khanal & Ann L. Miller & Calvin Simerly & Gerald Schatten & Jadranka Loncarek & Vito Mennella, 2018. "A novel atypical sperm centriole is functional during human fertilization," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    5. Sushil Khanal & Miguel Ricardo Leung & Abigail Royfman & Emily L. Fishman & Barbara Saltzman & Hermes Bloomfield-Gadêlha & Tzviya Zeev-Ben-Mordehai & Tomer Avidor-Reiss, 2021. "A dynamic basal complex modulates mammalian sperm movement," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    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. Volodymyr Porokh & Drahomíra Kyjovská & Martina Martonová & Tereza Klenková & Pavel Otevřel & Soňa Kloudová & Zuzana Holubcová, 2024. "Zygotic spindle orientation defines cleavage pattern and nuclear status of human embryos," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    2. Yuki Ono & Hiromitsu Shirasawa & Kazumasa Takahashi & Mayumi Goto & Takahiro Ono & Taichi Sakaguchi & Motonari Okabe & Takeo Hirakawa & Takuya Iwasawa & Akiko Fujishima & Tae Sugawara & Kenichi Makino, 2024. "Shape of the first mitotic spindles impacts multinucleation in human embryos," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. James F. Cass & Hermes Bloomfield-Gadêlha, 2023. "The reaction-diffusion basis of animated patterns in eukaryotic flagella," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Emily R Churchill & Calvin Dytham & Jon R Bridle & Michael D F Thom, 2021. "Social and physical environment independently affect oviposition decisions in Drosophila," Behavioral Ecology, International Society for Behavioral Ecology, vol. 32(6), pages 1391-1399.
    5. Dalileh Nabi & Hauke Drechsler & Johannes Pschirer & Franz Korn & Nadine Schuler & Stefan Diez & Rolf Jessberger & Mariola Chacón, 2021. "CENP-V is required for proper chromosome segregation through interaction with spindle microtubules in mouse oocytes," Nature Communications, Nature, vol. 12(1), pages 1-16, 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_s41467-023-44411-8. 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.