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Peer-reviewedCC BYScience Advances

Progressive oxygenation of developing leaves directs morphogenesis

  • Gabriele Panicucci1
  • Vinay Shukla2,3
  • Viktoriia Voloboeva1
  • Leonardo Jo1,4
  • Kees van Kollenburg1
  • Sara Buti1
  • Laura Dalle Carbonare2
  • Federico Manuel Giorgi5
  • Francesco Licausi2
  • Daan A. Weits1
5 affiliations
  1. 1Experimental and Computational Plant Development, Institute of Environment Biology, Utrecht University, Utrecht, Netherlands
  2. 2Department of Biology, University of Oxford, Oxford, UK
  3. 3School of Biosciences, University of Nottingham, Loughborough LE12 5RD, UK
  4. 4Plant Stress Resilience, Institute of Environment Biology, Utrecht University, Utrecht, Netherlands
  5. 5Department of Pharmacy and Biotechnology, University of Bologna, Bologna, Italy
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Abstract

Oxygen availability underpins energy production in multicellular organisms, yet internal oxygen gradients arise in both plants and animals. Plants sense these variations via the plant cysteine oxidase branch of the N-degron pathway, which regulates the stability of key transcription factors. Originally linked to metabolic control, this pathway recently emerged as a development regulator. While the shoot apical meristem was shown to be hypoxic, the oxygen dynamics of organs originating from this low-oxygen niche remain unknown. Here, we show that developing leaves form a spatiotemporal oxygen gradient that is sensed through the oxygen-sensing machinery. This pathway integrates local oxygen availability to regulate leaf morphogenesis: Early hypoxia restricts cell expansion, whereas subsequent distal-to-proximal oxygenation depletes group VII ethylene response factors enabling specialized cell-fate acquisition and controlling proliferation. Our findings reveal that oxygen acts as a positional cue in normal growth, guiding developmental trajectories. This highlights opportunities to harness oxygen gradients and sensing to direct plant form and function.

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Cite

BibTeXRIS
BibTeX
@article{panicucci2026progressive,
  title = {{Progressive oxygenation of developing leaves directs morphogenesis}},
  author = {Gabriele Panicucci and Vinay Shukla and Viktoriia Voloboeva and Leonardo Jo and Kees van Kollenburg and Sara Buti and Laura Dalle Carbonare and Federico Manuel Giorgi and Francesco Licausi and Daan A. Weits},
  journal = {Science Advances},
  year = {2026},
  month = aug,
  doi = {10.1126/sciadv.aef2430},
  url = {https://doi.org/10.1126/sciadv.aef2430},
  note = {CC BY},
}
RIS
TY  - JOUR
TI  - Progressive oxygenation of developing leaves directs morphogenesis
AU  - Gabriele Panicucci
AU  - Vinay Shukla
AU  - Viktoriia Voloboeva
AU  - Leonardo Jo
AU  - Kees van Kollenburg
AU  - Sara Buti
AU  - Laura Dalle Carbonare
AU  - Federico Manuel Giorgi
AU  - Francesco Licausi
AU  - Daan A. Weits
PY  - 2026
DA  - 2026/08/28
JO  - Science Advances
DO  - 10.1126/sciadv.aef2430
UR  - https://doi.org/10.1126/sciadv.aef2430
AB  - Oxygen availability underpins energy production in multicellular organisms, yet internal oxygen gradients arise in both plants and animals. Plants sense these variations via the plant cysteine oxidase branch of the N-degron pathway, which regulates the stability of key transcription factors. Originally linked to metabolic control, this pathway recently emerged as a development regulator. While the shoot apical meristem was shown to be hypoxic, the oxygen dynamics of organs originating from this low-oxygen niche remain unknown. Here, we show that developing leaves form a spatiotemporal oxygen gradient that is sensed through the oxygen-sensing machinery. This pathway integrates local oxygen availability to regulate leaf morphogenesis: Early hypoxia restricts cell expansion, whereas subsequent distal-to-proximal oxygenation depletes group VII ethylene response factors enabling specialized cell-fate acquisition and controlling proliferation. Our findings reveal that oxygen acts as a positional cue in normal growth, guiding developmental trajectories. This highlights opportunities to harness oxygen gradients and sensing to direct plant form and function.
SN  - 2375-2548
ER  -