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A nuclear-encoded endonuclease governs the paternal transmission of mitochondria in Cucumis plants

Author

Listed:
  • Jia Shen

    (Zhejiang Academy of Agricultural Sciences
    Key Laboratory of Vegetable Germplasm Innovation and Quality Breeding in the Province)

  • Xiaolong Lyu

    (Key Laboratory of Vegetable Germplasm Innovation and Quality Breeding in the Province
    Zhejiang University
    Zhejiang University)

  • Xinyang Xu

    (Zhejiang Academy of Agricultural Sciences
    Key Laboratory of Vegetable Germplasm Innovation and Quality Breeding in the Province)

  • Zheng Wang

    (Zhejiang Academy of Agricultural Sciences
    Key Laboratory of Vegetable Germplasm Innovation and Quality Breeding in the Province)

  • Yuejian Zhang

    (Zhejiang Academy of Agricultural Sciences
    Key Laboratory of Vegetable Germplasm Innovation and Quality Breeding in the Province)

  • Chenhao Wang

    (Key Laboratory of Vegetable Germplasm Innovation and Quality Breeding in the Province
    Zhejiang University
    Zhejiang University)

  • Eduardo D. Munaiz

    (AGHYLE UP 2018.C101)

  • Mingfang Zhang

    (Key Laboratory of Vegetable Germplasm Innovation and Quality Breeding in the Province
    Zhejiang University
    Zhejiang University
    Hainan Institute of Zhejiang University)

  • Michael J. Havey

    (University of Wisconsin)

  • Weisong Shou

    (Zhejiang Academy of Agricultural Sciences
    Key Laboratory of Vegetable Germplasm Innovation and Quality Breeding in the Province)

Abstract

Non-Mendelian transmission of mitochondria has been well established across most eukaryotes, however the genetic mechanism that governs this uniparental inheritance remains unclear. Plants in the genus Cucumis, specifically melon and cucumber, exhibit paternal transmission of the mitochondrial (mt) DNA, making them excellent models for exploring the molecular mechanisms underlying mitochondrial transmission. Here, we develop a toolkit to screen for mutants in mitochondrial inheritance (mti), and use fine mapping to successfully identify a mitochondrially targeted endonuclease gene (MTI1) controlling mitochondrial transmission. Knockout of MTI1 results in a shift from paternal to bi-parental inheritance of the mtDNA, confirming the crucial role of MTI1 in uniparental inheritance of mitochondria. Moreover, we demonstrate that MTI1 exhibits robust endonuclease activity both in vitro and in vivo, specifically expresses in mitochondria of the fertilized ovule within 24 h of pollination. Collectively, this study reveals that a nuclear-encoded but mitochondria-targeted gene plays a causative role in governing the non-Mendelian mitochondrial inheritance, revolutionizing our knowledge about mitochondrial DNA transmission.

Suggested Citation

  • Jia Shen & Xiaolong Lyu & Xinyang Xu & Zheng Wang & Yuejian Zhang & Chenhao Wang & Eduardo D. Munaiz & Mingfang Zhang & Michael J. Havey & Weisong Shou, 2025. "A nuclear-encoded endonuclease governs the paternal transmission of mitochondria in Cucumis plants," Nature Communications, Nature, vol. 16(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-59568-7
    DOI: 10.1038/s41467-025-59568-7
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    References listed on IDEAS

    as
    1. Peter Sutovsky & Ricardo D. Moreno & João Ramalho-Santos & Tanja Dominko & Calvin Simerly & Gerald Schatten, 1999. "Ubiquitin tag for sperm mitochondria," Nature, Nature, vol. 402(6760), pages 371-372, November.
    2. Wei Wei & Katherine R. Schon & Greg Elgar & Andrea Orioli & Melanie Tanguy & Adam Giess & Marc Tischkowitz & Mark J. Caulfield & Patrick F. Chinnery, 2022. "Nuclear-embedded mitochondrial DNA sequences in 66,083 human genomes," Nature, Nature, vol. 611(7934), pages 105-114, November.
    3. Sharon Ben-Hur & Shoshana Sernik & Sara Afar & Alina Kolpakova & Yoav Politi & Liron Gal & Anat Florentin & Ofra Golani & Ehud Sivan & Nili Dezorella & David Morgenstern & Shmuel Pietrokovski & Eyal S, 2024. "Egg multivesicular bodies elicit an LC3-associated phagocytosis-like pathway to degrade paternal mitochondria after fertilization," Nature Communications, Nature, vol. 15(1), pages 1-25, December.
    4. Ignacia Fuentes & Sandra Stegemann & Hieronim Golczyk & Daniel Karcher & Ralph Bock, 2014. "Horizontal genome transfer as an asexual path to the formation of new species," Nature, Nature, vol. 511(7508), pages 232-235, July.
    5. Antoine Martin & Christelle Troadec & Adnane Boualem & Mazen Rajab & Ronan Fernandez & Halima Morin & Michel Pitrat & Catherine Dogimont & Abdelhafid Bendahmane, 2009. "A transposon-induced epigenetic change leads to sex determination in melon," Nature, Nature, vol. 461(7267), pages 1135-1138, October.
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