Seed Architecture Shapes Embryo Metabolism in Oilseed Rape

authored by

Ljudmilla Borisjuk, Thomas Neuberger, Jörg Schwender, Nicolas Heinzel, Stephanie Sunderhaus, Johannes Fuchs, Jordan O. Hay, Henning Tschiersch, Hans Peter Braun, Peter Denolf, Bart Lambert, Peter M. Jakob, Hardy Rolletschek

Abstract

Constrained to develop within the seed, the plant embryo must adapt its shape and size to fit the space available. Here, we demonstrate how this adjustment shapes metabolism of photosynthetic embryo. Noninvasive NMR-based imaging of the developing oilseed rape (Brassica napus) seed illustrates that, following embryo bending, gradients in lipid concentration became established. These were correlated with the local photosynthetic electron transport rate and the accumulation of storage products. Experimentally induced changes in embryo morphology and/or light supply altered these gradients and were accompanied by alterations in both proteome and metabolome. Tissue-specific metabolic models predicted that the outer cotyledon and hypocotyl/radicle generate the bulk of plastidic reductant/ATP via photosynthesis, while the inner cotyledon, being enclosed by the outer cotyledon, is forced to grow essentially heterotrophically. Under field-relevant highlight conditions, major contribution of the ribulose-1,5-bisphosphate carboxylase/oxygenase-bypass to seed storage metabolism is predicted for the outer cotyledon and the hypocotyl/radicle only. Differences between in vitro- versus in planta-grown embryos suggest that metabolic heterogeneity of embryo is not observable by in vitro approaches. We conclude that in vivo metabolic fluxes are locally regulated and connected to seed architecture, driving the embryo toward an efficient use of available light and space.

Organisation(s)

Institute of Plant Genetics

External Organisation(s)

Leibniz Institute of Plant Genetics and Crop Plant Research (IPK)
Pennsylvania State University
Brookhaven National Laboratory (BNL)
Julius Maximilian University of Würzburg
Bayer Corporation - USA
Research Center Magnetic Resonance Bavaria

Type

Article

Journal

PLANT CELL

Volume

25

Pages

1625-1640

No. of pages

16

ISSN

1040-4651

Publication date

05.2013

Publication status

Published

Peer reviewed

Yes

ASJC Scopus subject areas

Plant Science, Cell Biology

Electronic version(s)

https://doi.org/10.1105/tpc.113.111740 (Access: Open)
https://doi.org/10.15488/11686 (Access: Open)