Seed Architecture Shapes Embryo Metabolism in Oilseed Rape

Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, D-06466 Gatersleben, Germany.
The Plant Cell (Impact Factor: 9.34). 05/2013; 25(5). DOI: 10.1105/tpc.113.111740
Source: PubMed


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.

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    • "FBA represents an established technique to generate quantitative models of optimal steady-state flux distributions at large-scale metabolic networks. Appropriate FBA models involving seed metabolism (Grafahrend- Belau et al., 2009; Hay and Schwender, 2011; Hay et al., 2014) and even individual seed organs/tissues (Rolletschek et al., 2011; Borisjuk et al., 2013) have been elaborated. As yet, however, these seed models cannot account for the exchange of materials between the individual tissues/organs. "
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    • "These will greatly enhance our understanding of these enzymatic processes. Furthermore, metabolite imaging techniques, such as genetically encoded metabolite sensors (Okumoto et al., 2012), nuclear magnetic imaging (Borisjuk et al., 2013), and flux profiling techniques (Schwender et al., 2004b), alongside miniaturization of respiration measurements (Sew et al., 2013), will additionally enhance our understanding of the shifts in plant energy metabolism that occur during the process of seed development. Our potential to metabolically engineer seeds in a highly tailored manner will be radically improved once such information is available and integrated with our current knowledge. "
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