title: Seed architecture shapes embryo metabolism in oilseed rape.
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 high-light 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.
authors.affiliation: Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, D-06466 Gatersleben, Germany.
authors.forename: Ljudmilla
authors.initials: L
authors.lastname: Borisjuk
authors.forename: Thomas
authors.initials: T
authors.lastname: Neuberger
authors.forename: Jörg
authors.initials: J
authors.lastname: Schwender
authors.forename: Nicolas
authors.initials: N
authors.lastname: Heinzel
authors.forename: Stephanie
authors.initials: S
authors.lastname: Sunderhaus
authors.forename: Johannes
authors.initials: J
authors.lastname: Fuchs
authors.forename: Jordan O
authors.initials: JO
authors.lastname: Hay
authors.forename: Henning
authors.initials: H
authors.lastname: Tschiersch
authors.forename: Hans-Peter
authors.initials: HP
authors.lastname: Braun
authors.forename: Peter
authors.initials: P
authors.lastname: Denolf
authors.forename: Bart
authors.initials: B
authors.lastname: Lambert
authors.forename: Peter M
authors.initials: PM
authors.lastname: Jakob
authors.forename: Hardy
authors.initials: H
authors.lastname: Rolletschek
mesh_terms: D029688:Brassica napus / Q000033:anatomy & histology / Q000254:growth & development / Q000378:metabolism*; D018548:Cotyledon / Q000033:anatomy & histology / Q000254:growth & development / Q000378:metabolism*; D004579:Electron Transport; D015180:Electrophoresis, Gel, Two-Dimensional; D050356:Lipid Metabolism; D008279:Magnetic Resonance Imaging; D013058:Mass Spectrometry; D055442:Metabolome; D055432:Metabolomics / Q000379:methods; D008953:Models, Anatomic; D008954:Models, Biological; D010788:Photosynthesis; D010940:Plant Proteins / Q000378:metabolism; D020543:Proteome / Q000378:metabolism; D040901:Proteomics / Q000379:methods; D012274:Ribulosephosphates / Q000378:metabolism; D012639:Seeds / Q000033:anatomy & histology / Q000254:growth & development / Q000378:metabolism*
chemical_list: D010940:Plant Proteins; D020543:Proteome; D012274:Ribulosephosphates; C001933:ribulose-1,5 diphosphate