IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51228-6.html
   My bibliography  Save this article

Cellular sex throughout the organism underlies somatic sexual differentiation

Author

Listed:
  • Chloé Hérault

    (Institut de Biologie Valrose)

  • Thomas Pihl

    (Institut de Biologie Valrose)

  • Bruno Hudry

    (Institut de Biologie Valrose)

Abstract

Sex chromosomes underlie the development of male or female sex organs across species. While systemic signals derived from sex organs prominently contribute to sex-linked differences, it is unclear whether the intrinsic presence of sex chromosomes in somatic tissues has a specific function. Here, we use genetic tools to show that cellular sex is crucial for sexual differentiation throughout the body in Drosophila melanogaster. We reveal that every somatic cell converts the intrinsic presence of sex chromosomes into the active production of a sex determinant, a female specific serine- and arginine-rich (SR) splicing factor. This discovery dismisses the mosaic model which posits that only a subset of cells has the potential to sexually differentiate. Using cell-specific sex reversals, we show that this prevalence of cellular sex drives sex differences in organ size and body weight and is essential for fecundity. These findings demonstrate that cellular sex drives differentiation programs at an organismal scale and highlight the importance of cellular sex pathways in sex trait evolution.

Suggested Citation

  • Chloé Hérault & Thomas Pihl & Bruno Hudry, 2024. "Cellular sex throughout the organism underlies somatic sexual differentiation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51228-6
    DOI: 10.1038/s41467-024-51228-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51228-6
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-51228-6?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. Xiaoying Zheng & Dongjing Zhang & Yongjun Li & Cui Yang & Yu Wu & Xiao Liang & Yongkang Liang & Xiaoling Pan & Linchao Hu & Qiang Sun & Xiaohua Wang & Yingyang Wei & Jian Zhu & Wei Qian & Ziqiang Yan , 2019. "Incompatible and sterile insect techniques combined eliminate mosquitoes," Nature, Nature, vol. 572(7767), pages 56-61, August.
    2. Bruno Hudry & Sanjay Khadayate & Irene Miguel-Aliaga, 2016. "The sexual identity of adult intestinal stem cells controls organ size and plasticity," Nature, Nature, vol. 530(7590), pages 344-348, February.
    3. Zhiping Zhang & Bongmin Bae & Winston H. Cuddleston & Pedro Miura, 2023. "Coordination of alternative splicing and alternative polyadenylation revealed by targeted long read sequencing," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Daniah Trabzuni & Adaikalavan Ramasamy & Sabaena Imran & Robert Walker & Colin Smith & Michael E. Weale & John Hardy & Mina Ryten, 2013. "Widespread sex differences in gene expression and splicing in the adult human brain," Nature Communications, Nature, vol. 4(1), pages 1-7, December.
    5. Jiexi Li & Zhengdao Lan & Wenting Liao & James W. Horner & Xueping Xu & Jielin Liu & Yohei Yoshihama & Shan Jiang & Hong Seok Shim & Max Slotnik & Kyle A. LaBella & Chang-Jiun Wu & Kenneth Dunner & We, 2023. "Histone demethylase KDM5D upregulation drives sex differences in colon cancer," Nature, Nature, vol. 619(7970), pages 632-639, July.
    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. Qian Liu & Emma Adhikari & Daniel K. Lester & Bin Fang & Joseph O. Johnson & Yijun Tian & Andrea T. Mockabee-Macias & Victoria Izumi & Kelly M. Guzman & Michael G. White & John M. Koomen & Jennifer A., 2024. "Androgen drives melanoma invasiveness and metastatic spread by inducing tumorigenic fucosylation," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Xiaomei Sun & Yanhong Wang & Fei Yuan & Yanan Zhang & Xun Kang & Jian Sun & Pengcheng Wang & Tengfei Lu & Fanny Sae Wang & Jinbao Gu & Jinglin Wang & Qianfeng Xia & Aihua Zheng & Zhen Zou, 2024. "Gut symbiont-derived sphingosine modulates vector competence in Aedes mosquitoes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Xingtong Liu & Yuanshun Tan & Bo Zheng, 2022. "Dynamic Behavior of an Interactive Mosquito Model under Stochastic Interference," Mathematics, MDPI, vol. 10(13), pages 1-18, June.
    4. Qiming Huang & Lijie Chang & Zhaowang Zhang & Bo Zheng, 2023. "Global Dynamics for Competition between Two Wolbachia Strains with Bidirectional Cytoplasmic Incompatibility," Mathematics, MDPI, vol. 11(7), pages 1-21, April.
    5. Zhongcai Zhu & Yantao Shi & Rong Yan & Linchao Hu, 2022. "Periodic Orbits of a Mosquito Suppression Model Based on Sterile Mosquitoes," Mathematics, MDPI, vol. 10(3), pages 1-21, January.
    6. Dongjing Zhang & Hamidou Maiga & Yongjun Li & Mame Thierno Bakhoum & Gang Wang & Yan Sun & David Damiens & Wadaka Mamai & Nanwintoum Séverin Bimbilé Somda & Thomas Wallner & Odet Bueno-Masso & Claudia, 2024. "Mating harassment may boost the effectiveness of the sterile insect technique for Aedes mosquitoes," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Tom W. Andrew & Lauren S. Koepke & Yuting Wang & Michael Lopez & Holly Steininger & Danielle Struck & Tatiana Boyko & Thomas H. Ambrosi & Xinming Tong & Yuxi Sun & Gunsagar S. Gulati & Matthew P. Murp, 2022. "Sexually dimorphic estrogen sensing in skeletal stem cells controls skeletal regeneration," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    8. Oksana Netschitailo & Yidong Wang & Anna Wagner & Vivien Sommer & Eveline C. Verhulst & Martin Beye, 2023. "The function and evolution of a genetic switch controlling sexually dimorphic eye differentiation in honeybees," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    9. Dan Wen & Limin S. Ding & Yanan Zhang & Xiaoye Li & Xing Zhang & Fei Yuan & Tongbiao Zhao & Aihua Zheng, 2022. "Suppression of flavivirus transmission from animal hosts to mosquitoes with a mosquito-delivered vaccine," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    10. Kynon J. M. Benjamin & Ria Arora & Arthur S. Feltrin & Geo Pertea & Hunter H. Giles & Joshua M. Stolz & Laura D’Ignazio & Leonardo Collado-Torres & Joo Heon Shin & William S. Ulrich & Thomas M. Hyde &, 2024. "Sex affects transcriptional associations with schizophrenia across the dorsolateral prefrontal cortex, hippocampus, and caudate nucleus," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. Masato Tsuji & Takanori Kawasaki & Takeru Matsuda & Tomio Arai & Satoshi Gojo & Jun K Takeuchi, 2017. "Sexual dimorphisms of mRNA and miRNA in human/murine heart disease," PLOS ONE, Public Library of Science, vol. 12(7), pages 1-21, July.
    12. Haramboure, Marion & Labbé, Pierrick & Baldet, Thierry & Damiens, David & Gouagna, Louis Clément & Bouyer, Jérémy & Tran, Annelise, 2020. "Modelling the control of Aedes albopictus mosquitoes based on sterile males release techniques in a tropical environment," Ecological Modelling, Elsevier, vol. 424(C).
    13. Omid Omrani & Anna Krepelova & Seyed Mohammad Mahdi Rasa & Dovydas Sirvinskas & Jing Lu & Francesco Annunziata & George Garside & Seerat Bajwa & Susanne Reinhardt & Lisa Adam & Sandra Käppel & Nadia D, 2023. "IFNγ-Stat1 axis drives aging-associated loss of intestinal tissue homeostasis and regeneration," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    14. Yijie Li & Zhiming Guo, 2022. "Wolbachia Invasion Dynamics by Integrodifference Equations," Mathematics, MDPI, vol. 10(22), pages 1-13, November.
    15. Xiaomei Sun & Xueli Wang & Kai Shi & Xiangyang Lyu & Jian Sun & Alexander S. Raikhel & Zhen Zou, 2024. "Leucine aminopeptidase1 controls egg deposition and hatchability in male Aedes aegypti mosquitoes," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    16. Lijie Chang & Yantao Shi & Bo Zheng, 2021. "Existence and Uniqueness of Nontrivial Periodic Solutions to a Discrete Switching Model," Mathematics, MDPI, vol. 9(19), pages 1-13, September.

    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_s41467-024-51228-6. 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.