Mechanical forces orchestrate the metabolism of the developing oilseed rape embryo

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Hardy Rolletschek
  • Aleksandra Muszynska
  • Jörg Schwender
  • Volodymyr Radchuk
  • Björn Heinemann
  • Alexander Hilo
  • Iaroslav Plutenko
  • Peter Keil
  • Stefan Ortleb
  • Steffen Wagner
  • Laura Kalms
  • André Gündel
  • Hai Shi
  • Jörg Fuchs
  • Jedrzej Jakub Szymanski
  • Hans-Peter Braun
  • Ljudmilla Borisjuk

Research Organisations

External Research Organisations

  • Leibniz Institute of Plant Genetics and Crop Plant Research (IPK)
  • Genomics and Biology of Fruit Crops Department
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Details

Original languageEnglish
JournalThe new phytologist
Publication statusE-pub ahead of print - 24 Jul 2024

Abstract

The initial free expansion of the embryo within a seed is at some point inhibited by its contact with the testa, resulting in its formation of folds and borders. Although less obvious, mechanical forces appear to trigger and accelerate seed maturation. However, the mechanistic basis for this effect remains unclear. Manipulation of the mechanical constraints affecting either the in vivo or in vitro growth of oilseed rape embryos was combined with analytical approaches, including magnetic resonance imaging and computer graphic reconstruction, immunolabelling, flow cytometry, transcriptomic, proteomic, lipidomic and metabolomic profiling. Our data implied that, in vivo, the imposition of mechanical restraints impeded the expansion of testa and endosperm, resulting in the embryo's deformation. An acceleration in embryonic development was implied by the cessation of cell proliferation and the stimulation of lipid and protein storage, characteristic of embryo maturation. The underlying molecular signature included elements of cell cycle control, reactive oxygen species metabolism and transcriptional reprogramming, along with allosteric control of glycolytic flux. Constricting the space allowed for the expansion of in vitro grown embryos induced a similar response. The conclusion is that the imposition of mechanical constraints over the growth of the developing oilseed rape embryo provides an important trigger for its maturation.

Keywords

    Brassica napus, MRI, computer graphic reconstruction, embryogenesis, maturation, mechanical stress, morphogenesis, transcription factors

ASJC Scopus subject areas

Cite this

Mechanical forces orchestrate the metabolism of the developing oilseed rape embryo. / Rolletschek, Hardy; Muszynska, Aleksandra; Schwender, Jörg et al.
In: The new phytologist, 24.07.2024.

Research output: Contribution to journalArticleResearchpeer review

Rolletschek, H, Muszynska, A, Schwender, J, Radchuk, V, Heinemann, B, Hilo, A, Plutenko, I, Keil, P, Ortleb, S, Wagner, S, Kalms, L, Gündel, A, Shi, H, Fuchs, J, Szymanski, JJ, Braun, H-P & Borisjuk, L 2024, 'Mechanical forces orchestrate the metabolism of the developing oilseed rape embryo', The new phytologist. https://doi.org/10.1111/nph.19990
Rolletschek, H., Muszynska, A., Schwender, J., Radchuk, V., Heinemann, B., Hilo, A., Plutenko, I., Keil, P., Ortleb, S., Wagner, S., Kalms, L., Gündel, A., Shi, H., Fuchs, J., Szymanski, J. J., Braun, H.-P., & Borisjuk, L. (2024). Mechanical forces orchestrate the metabolism of the developing oilseed rape embryo. The new phytologist. Advance online publication. https://doi.org/10.1111/nph.19990
Rolletschek H, Muszynska A, Schwender J, Radchuk V, Heinemann B, Hilo A et al. Mechanical forces orchestrate the metabolism of the developing oilseed rape embryo. The new phytologist. 2024 Jul 24. Epub 2024 Jul 24. doi: 10.1111/nph.19990
Rolletschek, Hardy ; Muszynska, Aleksandra ; Schwender, Jörg et al. / Mechanical forces orchestrate the metabolism of the developing oilseed rape embryo. In: The new phytologist. 2024.
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AU - Rolletschek, Hardy

AU - Muszynska, Aleksandra

AU - Schwender, Jörg

AU - Radchuk, Volodymyr

AU - Heinemann, Björn

AU - Hilo, Alexander

AU - Plutenko, Iaroslav

AU - Keil, Peter

AU - Ortleb, Stefan

AU - Wagner, Steffen

AU - Kalms, Laura

AU - Gündel, André

AU - Shi, Hai

AU - Fuchs, Jörg

AU - Szymanski, Jedrzej Jakub

AU - Braun, Hans-Peter

AU - Borisjuk, Ljudmilla

N1 - © 2024 The Author(s). New Phytologist © 2024 New Phytologist Foundation.

PY - 2024/7/24

Y1 - 2024/7/24

N2 - The initial free expansion of the embryo within a seed is at some point inhibited by its contact with the testa, resulting in its formation of folds and borders. Although less obvious, mechanical forces appear to trigger and accelerate seed maturation. However, the mechanistic basis for this effect remains unclear. Manipulation of the mechanical constraints affecting either the in vivo or in vitro growth of oilseed rape embryos was combined with analytical approaches, including magnetic resonance imaging and computer graphic reconstruction, immunolabelling, flow cytometry, transcriptomic, proteomic, lipidomic and metabolomic profiling. Our data implied that, in vivo, the imposition of mechanical restraints impeded the expansion of testa and endosperm, resulting in the embryo's deformation. An acceleration in embryonic development was implied by the cessation of cell proliferation and the stimulation of lipid and protein storage, characteristic of embryo maturation. The underlying molecular signature included elements of cell cycle control, reactive oxygen species metabolism and transcriptional reprogramming, along with allosteric control of glycolytic flux. Constricting the space allowed for the expansion of in vitro grown embryos induced a similar response. The conclusion is that the imposition of mechanical constraints over the growth of the developing oilseed rape embryo provides an important trigger for its maturation.

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