IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-56528-z.html
   My bibliography  Save this article

Nutrient status alters developmental fates via a switch in mitochondrial homeodynamics

Author

Listed:
  • Jie Zhang

    (South China Normal University
    Zhejiang Chinese Medical University)

  • Suning Liu

    (South China Normal University
    South China Normal University)

  • Yang Li

    (South China Normal University)

  • Guanfeng Xu

    (South China Normal University)

  • Huimin Deng

    (South China Normal University)

  • Kirst King-Jones

    (University of Alberta)

  • Sheng Li

    (South China Normal University
    South China Normal University)

Abstract

Steroid hormones are powerful endocrine regulators, but little is known about how environmental conditions modulate steroidogenesis to reprogram developmental fates. Here, we use the Drosophila prothoracic gland (PG) to investigate how a nutrient restriction checkpoint (NRC) ensures or blocks developmental progression and sexual maturation via regulating steroidogenesis. Extensive transcriptome analysis of the PG reveals that pre-NRC starvation significantly downregulates mitochondria-associated genes. Pre-NRC starvation reduces prothoracicotropic neuropeptide hormone signaling, insulin signaling, and TORC1 activity in PG cells, which prevent mitochondrial fragmentation and import of Disembodied, a key steroidogenic enzyme. Ultimately, pre-NRC starvation causes severe mitophagy and proteasome dysfunction, blocking steroidogenesis and metamorphosis. By contrast, post-NRC starvation does not impair mitochondrial homeostasis in PG cells but reduces sit expression and induces moderate autophagy to promote steroidogenesis, leading to precocious metamorphosis. This study constitutes a paradigm for exploring how steroid hormone levels are controlled in response to environmental stress during developmental checkpoints.

Suggested Citation

  • Jie Zhang & Suning Liu & Yang Li & Guanfeng Xu & Huimin Deng & Kirst King-Jones & Sheng Li, 2025. "Nutrient status alters developmental fates via a switch in mitochondrial homeodynamics," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-56528-z
    DOI: 10.1038/s41467-025-56528-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-56528-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-025-56528-z?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. Po-Lin Chen & Kai-Ting Huang & Chu-Ya Cheng & Jian-Chiuan Li & Hsiao-Yen Chan & Tzu-Yang Lin & Matthew P. Su & Wei-Yuan Yang & Henry C. Chang & Horng-Dar Wang & Chun-Hong Chen, 2020. "Vesicular transport mediates the uptake of cytoplasmic proteins into mitochondria in Drosophila melanogaster," Nature Communications, Nature, vol. 11(1), pages 1-19, December.
    2. Deniz Senyilmaz & Sam Virtue & Xiaojun Xu & Chong Yew Tan & Julian L. Griffin & Aubry K. Miller & Antonio Vidal-Puig & Aurelio A. Teleman, 2015. "Regulation of mitochondrial morphology and function by stearoylation of TFR1," Nature, Nature, vol. 525(7567), pages 124-128, September.
    3. Michael Lazarou & Danielle A. Sliter & Lesley A. Kane & Shireen A. Sarraf & Chunxin Wang & Jonathon L. Burman & Dionisia P. Sideris & Adam I. Fogel & Richard J. Youle, 2015. "The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy," Nature, Nature, vol. 524(7565), pages 309-314, August.
    4. Toby Lieber & Swathi P. Jeedigunta & Jonathan M. Palozzi & Ruth Lehmann & Thomas R. Hurd, 2019. "Mitochondrial fragmentation drives selective removal of deleterious mtDNA in the germline," Nature, Nature, vol. 570(7761), pages 380-384, June.
    5. Yue Li & Pengzhen Dong & Yang Yang & Tianyu Guo & Quanyi Zhao & Dan Miao & Huanle Li & Tianfeng Lu & Fanning Xia & Jialan Lyu & Jun Ma & Thomas B. Kornberg & Qiang Zhang & Hai Huang, 2022. "Metabolic control of progenitor cell propagation during Drosophila tracheal remodeling," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. Tommy L. Lewis & Seok-Kyu Kwon & Annie Lee & Reuben Shaw & Franck Polleux, 2018. "MFF-dependent mitochondrial fission regulates presynaptic release and axon branching by limiting axonal mitochondria size," Nature Communications, Nature, vol. 9(1), pages 1-15, 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. Kyla Germain & Raphaella W. L. So & Laura F. DiGiovanni & Joel C. Watts & Robert H. J. Bandsma & Peter K. Kim, 2024. "Upregulated pexophagy limits the capacity of selective autophagy," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Taeko Sasaki & Yasuharu Kushida & Takuya Norizuki & Hidetaka Kosako & Ken Sato & Miyuki Sato, 2024. "ALLO-1- and IKKE-1-dependent positive feedback mechanism promotes the initiation of paternal mitochondrial autophagy," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Marine Lanfranchi & Sozerko Yandiev & Géraldine Meyer-Dilhet & Salma Ellouze & Martijn Kerkhofs & Raphael Dos Reis & Audrey Garcia & Camille Blondet & Alizée Amar & Anita Kneppers & Hélène Polvèche & , 2024. "The AMPK-related kinase NUAK1 controls cortical axons branching by locally modulating mitochondrial metabolic functions," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Lu Jin & Shuang Han & Xue Lv & Xiaofei Li & Ziyin Zhang & Henry Kuang & Zhimin Chen & Cheng-an Lv & Wei Peng & Zhuoying Yang & Miqi Yang & Lin Mi & Tongyu Liu & Shengshan Ma & Xinyuan Qiu & Qintao Wan, 2023. "The muscle-enriched myokine Musclin impairs beige fat thermogenesis and systemic energy homeostasis via Tfr1/PKA signaling in male mice," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    5. Qiang Zhu & Matthew E. Combs & Juan Liu & Xue Bai & Wenbo B. Wang & Laura E. Herring & Jiandong Liu & Jason W. Locasale & Dawn E. Bowles & Ryan T. Gross & Michelle Mendiola Pla & Christopher P. Mack &, 2023. "GRAF1 integrates PINK1-Parkin signaling and actin dynamics to mediate cardiac mitochondrial homeostasis," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    6. Foozhan Tahmasebinia & Yinglu Tang & Rushi Tang & Yi Zhang & Will Bonderer & Maisa Oliveira & Bretton Laboret & Songjie Chen & Ruiqi Jian & Lihua Jiang & Michael Snyder & Chun-Hong Chen & Yawei Shen &, 2025. "The 40S ribosomal subunit recycling complex modulates mitochondrial dynamics and endoplasmic reticulum - mitochondria tethering at mitochondrial fission/fusion hotspots," Nature Communications, Nature, vol. 16(1), pages 1-24, December.
    7. Fumika Koyano & Koji Yamano & Tomoyuki Hoshina & Hidetaka Kosako & Yukio Fujiki & Keiji Tanaka & Noriyuki Matsuda, 2024. "AAA+ ATPase chaperone p97/VCPFAF2 governs basal pexophagy," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. Yue Li & Tianfeng Lu & Pengzhen Dong & Jian Chen & Qiang Zhao & Yuying Wang & Tianheng Xiao & Honggang Wu & Quanyi Zhao & Hai Huang, 2024. "A single-cell atlas of Drosophila trachea reveals glycosylation-mediated Notch signaling in cell fate specification," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    9. Remzi Onur Eren & Göksu Gökberk Kaya & Robin Schwarzer & Manolis Pasparakis, 2024. "IKKε and TBK1 prevent RIPK1 dependent and independent inflammation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    10. Dong Liu & Hannah C. Webber & Fuyun Bian & Yangfan Xu & Manjari Prakash & Xue Feng & Ming Yang & Hang Yang & In-Jee You & Liang Li & Liping Liu & Pingting Liu & Haoliang Huang & Chien-Yi Chang & Liang, 2025. "Optineurin-facilitated axonal mitochondria delivery promotes neuroprotection and axon regeneration," Nature Communications, Nature, vol. 16(1), pages 1-23, December.
    11. Daniel M. Virga & Stevie Hamilton & Bertha Osei & Abigail Morgan & Parker Kneis & Emiliano Zamponi & Natalie J. Park & Victoria L. Hewitt & David Zhang & Kevin C. Gonzalez & Fiona M. Russell & D. Grah, 2024. "Activity-dependent compartmentalization of dendritic mitochondria morphology through local regulation of fusion-fission balance in neurons in vivo," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    12. Huan Yang & Caroline Sibilla & Raymond Liu & Jina Yun & Bruce A. Hay & Craig Blackstone & David C. Chan & Robert J. Harvey & Ming Guo, 2022. "Clueless/CLUH regulates mitochondrial fission by promoting recruitment of Drp1 to mitochondria," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    13. Zhen Yuan & Kun Cai & Jiajia Li & Ruifeng Chen & Fuhai Zhang & Xuan Tan & Yaming Jiu & Haishuang Chang & Bing Hu & Weiyi Zhang & Binbin Ding, 2024. "ATG14 targets lipid droplets and acts as an autophagic receptor for syntaxin18-regulated lipid droplet turnover," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    14. Na Yeon Park & Doo Sin Jo & Jae-Yoon Yang & Ji-Eun Bae & Joon Bum Kim & Yong Hwan Kim & Seong Hyun Kim & Pansoo Kim & Dong-Seok Lee & Tamotsu Yoshimori & Eun-Kyeong Jo & Eunbyul Yeom & Dong-Hyung Cho, 2025. "Activation of lysophagy by a TBK1-SCFFBXO3-TMEM192-TAX1BP1 axis in response to lysosomal damage," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    15. Michael J. Munson & Benan J. Mathai & Matthew Yoke Wui Ng & Laura Trachsel-Moncho & Laura R. Ballina & Sebastian W. Schultz & Yahyah Aman & Alf H. Lystad & Sakshi Singh & Sachin Singh & Jørgen Wesche , 2021. "GAK and PRKCD are positive regulators of PRKN-independent mitophagy," Nature Communications, Nature, vol. 12(1), pages 1-22, December.
    16. Andrea Irazoki & Isabel Gordaliza-Alaguero & Emma Frank & Nikolaos Nikiforos Giakoumakis & Jordi Seco & Manuel Palacín & Anna Gumà & Lykke Sylow & David Sebastián & Antonio Zorzano, 2023. "Disruption of mitochondrial dynamics triggers muscle inflammation through interorganellar contacts and mitochondrial DNA mislocation," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    17. Shuang-zhou Peng & Xiao-hui Chen & Si-jie Chen & Jie Zhang & Chuan-ying Wang & Wei-rong Liu & Duo Zhang & Ying Su & Xiao-kun Zhang, 2021. "Phase separation of Nur77 mediates celastrol-induced mitophagy by promoting the liquidity of p62/SQSTM1 condensates," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    18. Su Jin Ham & Heesuk Yoo & Daihn Woo & Da Hyun Lee & Kyu-Sang Park & Jongkyeong Chung, 2023. "PINK1 and Parkin regulate IP3R-mediated ER calcium release," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    19. Bryan L. Gitschlag & Claudia V. Pereira & James P. Held & David M. McCandlish & Maulik R. Patel, 2024. "Multiple distinct evolutionary mechanisms govern the dynamics of selfish mitochondrial genomes in Caenorhabditis elegans," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    20. Kazuhiro Yamada & Claudette Croix & Donna B. Stolz & Yulia Y. Tyurina & Vladimir A. Tyurin & Laura R. Bradley & Alexander A. Kapralov & Yanhan Deng & Xiuxia Zhou & Qi Wei & Bo Liao & Nobuhiko Fukuda &, 2024. "Compartmentalized mitochondrial ferroptosis converges with optineurin-mediated mitophagy to impact airway epithelial cell phenotypes and asthma outcomes," Nature Communications, Nature, vol. 15(1), pages 1-17, 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:16:y:2025:i:1:d:10.1038_s41467-025-56528-z. 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.