Mechanical forces orchestrate the metabolism of the developing oilseed rape embryo

authored by

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

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.

Organisation(s)

Institute of Plant Genetics

External Organisation(s)

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

Type

Article

Journal

The new phytologist

Volume

244

Pages

1328-1344

No. of pages

17

ISSN

0028-646X

Publication date

16.10.2024

Publication status

Published

Peer reviewed

Yes

ASJC Scopus subject areas

Physiology, Plant Science

Electronic version(s)

https://doi.org/10.1111/nph.19990 (Access: Open)