Cytoplasmic cilia, a specialized type of cilia in which the axoneme resides within the cytoplasm rather than within the ciliary compartment, are proposed to allow for the efficient assembly of very long cilia. Despite being found diversely in male gametes (e.g., Plasmodium falciparum microgametocytes and human and Drosophila melanogaster sperm), very little is known about cytoplasmic cilia assembly. Here, we show that a novel RNP granule containing the mRNAs for axonemal dynein motor proteins becomes highly polarized to the distal end of the cilia during cytoplasmic ciliogenesis in Drosophila sperm. This allows for the incorporation of these axonemal dyneins into the axoneme directly from the cytoplasm, possibly by localizing translation. We found that this RNP granule contains the proteins Reptin and Pontin, loss of which perturbs granule formation and prevents incorporation of the axonemal dyneins, leading to sterility. We propose that cytoplasmic cilia assembly requires the precise localization of mRNAs encoding key axonemal constituents, allowing these proteins to incorporate efficiently into the axoneme.
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7 September 2020
Article|
July 24 2020
mRNA localization mediates maturation of cytoplasmic cilia in Drosophila spermatogenesis
Jaclyn M. Fingerhut
,
1
Cellular and Molecular Biology Program, University of Michigan, Ann Arbor, MI
2
Life Sciences Institute, University of Michigan, Ann Arbor, MI
Correspondence to Jaclyn M. Fingerhut: jaclynmf@umich.edu
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Yukiko M. Yamashita
1
Cellular and Molecular Biology Program, University of Michigan, Ann Arbor, MI
2
Life Sciences Institute, University of Michigan, Ann Arbor, MI
3
Department of Cell and Developmental Biology, University of Michigan, Ann Arbor, MI
4
Howard Hughes Medical Institute, University of Michigan, Ann Arbor, MI
Yukiko M. Yamashita: yukikomy@umich.edu
Search for other works by this author on:
Jaclyn M. Fingerhut
1
Cellular and Molecular Biology Program, University of Michigan, Ann Arbor, MI
2
Life Sciences Institute, University of Michigan, Ann Arbor, MI
Yukiko M. Yamashita
1
Cellular and Molecular Biology Program, University of Michigan, Ann Arbor, MI
2
Life Sciences Institute, University of Michigan, Ann Arbor, MI
3
Department of Cell and Developmental Biology, University of Michigan, Ann Arbor, MI
4
Howard Hughes Medical Institute, University of Michigan, Ann Arbor, MI
Yukiko M. Yamashita: yukikomy@umich.edu
Correspondence to Jaclyn M. Fingerhut: jaclynmf@umich.edu
Received:
March 13 2020
Revision Received:
June 10 2020
Accepted:
June 15 2020
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding:
Howard Hughes Medical Institute
(NO AWARD)
National Institutes of Health
(T32-GM007315)
© 2020 Fingerhut and Yamashita
2020
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Cell Biol (2020) 219 (9): e202003084.
Article history
Received:
March 13 2020
Revision Received:
June 10 2020
Accepted:
June 15 2020
Citation
Jaclyn M. Fingerhut, Yukiko M. Yamashita; mRNA localization mediates maturation of cytoplasmic cilia in Drosophila spermatogenesis. J Cell Biol 7 September 2020; 219 (9): e202003084. doi: https://doi.org/10.1083/jcb.202003084
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