Mechanical forces orchestrate the metabolism of the developing oilseed rape embryo

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

doi:10.1111/nph.19990

Title: Mechanical forces orchestrate the metabolism of the developing oilseed rape embryo

Journal Article · 24 July 2024 · New Phytologist

DOI: https://doi.org/10.1111/nph.19990 · OSTI ID:2472669

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Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben (Germany)
Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben (Germany); Amatera Biosciences, Evry (France)
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Universität Hannover (Germany)
Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben (Germany); Stockholm Univ. (Sweden)
Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben (Germany); Forschungszentrum Juelich (Germany). Institute of Bio- and Geosciences; Cluster of Excellence on Plant Sciences (CEPLAS), Düsseldorf (Germany)

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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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: Deutsche Forschungsgemeinschaft; European Regional Development Fund; USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0012704

OSTI ID:: 2472669

Report Number(s):: BNL-225749-2024-JAAM

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 4 Vol. 244; ISSN 0028-646X; ISSN 1469-8137

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Brassica napus
MRI
computer graphic reconstruction
embryogenesis
maturation
mechanical stress
morphogenesis
transcription factors

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