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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
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    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.
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