title: Metabolic Architecture of the Cereal Grain and Its Relevance to Maximize Carbon Use Efficiency.
abstract: Here, we have characterized the spatial heterogeneity of the cereal grain's metabolism and demonstrated how, by integrating a distinct set of metabolic strategies, the grain has evolved to become an almost perfect entity for carbon storage. In vivo imaging revealed light-induced cycles in assimilate supply toward the ear/grain of barley (Hordeum vulgare) and wheat (Triticum aestivum). In silico modeling predicted that, in the two grain storage organs (the endosperm and embryo), the light-induced shift in solute influx does cause adjustment in metabolic flux without changes in pathway utilization patterns. The enveloping, leaf-like pericarp, in contrast, shows major shifts in flux distribution (starch metabolism, photosynthesis, remobilization, and tricarboxylic acid cycle activity) allow to refix 79% of the CO2 released by the endosperm and embryo, allowing the grain to achieve an extraordinary high carbon conversion efficiency of 95%. Shading experiments demonstrated that ears are autonomously able to raise the influx of solutes in response to light, but with little effect on the steady-state levels of metabolites or transcripts or on the pattern of sugar distribution within the grain. The finding suggests the presence of a mechanism(s) able to ensure metabolic homeostasis in the face of short-term environmental fluctuation. The proposed multicomponent modeling approach is informative for predicting the metabolic effects of either an altered level of incident light or a momentary change in the supply of sucrose. It is therefore of potential value for assessing the impact of either breeding and/or biotechnological interventions aimed at increasing grain yield.
authors.affiliation: Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany (H.R., E.M., V.R., H.T., L.B.);Institut für Pharmazie, Martin-Luther-University of Halle, 06120 Halle, Germany (E.G.-B.);Institute of Experimental Physics 5, University of Würzburg, 97074 Würzburg, Germany (E.M., P.M.J.);Research Center Magnetic Resonance Bavaria, 97074 Wurzburg, Germany (R.K., P.M.J.);Department of Medical Imaging, University of Ottawa, Ottawa, Ontario, Canada K1Y 4E9 (G.M.); andClayton School of IT, Monash University, Melbourne, Victoria 3800, Australia (F.S.).
authors.forename: Hardy
authors.identifier: http://orcid.org/0000-0002-8619-1391
authors.initials: H
authors.lastname: Rolletschek
authors.affiliation: Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany (H.R., E.M., V.R., H.T., L.B.);Institut für Pharmazie, Martin-Luther-University of Halle, 06120 Halle, Germany (E.G.-B.);Institute of Experimental Physics 5, University of Würzburg, 97074 Würzburg, Germany (E.M., P.M.J.);Research Center Magnetic Resonance Bavaria, 97074 Wurzburg, Germany (R.K., P.M.J.);Department of Medical Imaging, University of Ottawa, Ottawa, Ontario, Canada K1Y 4E9 (G.M.); andClayton School of IT, Monash University, Melbourne, Victoria 3800, Australia (F.S.).
authors.forename: Eva
authors.initials: E
authors.lastname: Grafahrend-Belau
authors.affiliation: Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany (H.R., E.M., V.R., H.T., L.B.);Institut für Pharmazie, Martin-Luther-University of Halle, 06120 Halle, Germany (E.G.-B.);Institute of Experimental Physics 5, University of Würzburg, 97074 Würzburg, Germany (E.M., P.M.J.);Research Center Magnetic Resonance Bavaria, 97074 Wurzburg, Germany (R.K., P.M.J.);Department of Medical Imaging, University of Ottawa, Ottawa, Ontario, Canada K1Y 4E9 (G.M.); andClayton School of IT, Monash University, Melbourne, Victoria 3800, Australia (F.S.).
authors.forename: Eberhard
authors.identifier: http://orcid.org/0000-0002-4994-3304
authors.initials: E
authors.lastname: Munz
authors.affiliation: Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany (H.R., E.M., V.R., H.T., L.B.);Institut für Pharmazie, Martin-Luther-University of Halle, 06120 Halle, Germany (E.G.-B.);Institute of Experimental Physics 5, University of Würzburg, 97074 Würzburg, Germany (E.M., P.M.J.);Research Center Magnetic Resonance Bavaria, 97074 Wurzburg, Germany (R.K., P.M.J.);Department of Medical Imaging, University of Ottawa, Ottawa, Ontario, Canada K1Y 4E9 (G.M.); andClayton School of IT, Monash University, Melbourne, Victoria 3800, Australia (F.S.).
authors.forename: Volodymyr
authors.initials: V
authors.lastname: Radchuk
authors.affiliation: Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany (H.R., E.M., V.R., H.T., L.B.);Institut für Pharmazie, Martin-Luther-University of Halle, 06120 Halle, Germany (E.G.-B.);Institute of Experimental Physics 5, University of Würzburg, 97074 Würzburg, Germany (E.M., P.M.J.);Research Center Magnetic Resonance Bavaria, 97074 Wurzburg, Germany (R.K., P.M.J.);Department of Medical Imaging, University of Ottawa, Ottawa, Ontario, Canada K1Y 4E9 (G.M.); andClayton School of IT, Monash University, Melbourne, Victoria 3800, Australia (F.S.).
authors.forename: Ralf
authors.initials: R
authors.lastname: Kartäusch
authors.affiliation: Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany (H.R., E.M., V.R., H.T., L.B.);Institut für Pharmazie, Martin-Luther-University of Halle, 06120 Halle, Germany (E.G.-B.);Institute of Experimental Physics 5, University of Würzburg, 97074 Würzburg, Germany (E.M., P.M.J.);Research Center Magnetic Resonance Bavaria, 97074 Wurzburg, Germany (R.K., P.M.J.);Department of Medical Imaging, University of Ottawa, Ottawa, Ontario, Canada K1Y 4E9 (G.M.); andClayton School of IT, Monash University, Melbourne, Victoria 3800, Australia (F.S.).
authors.forename: Henning
authors.initials: H
authors.lastname: Tschiersch
authors.affiliation: Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany (H.R., E.M., V.R., H.T., L.B.);Institut für Pharmazie, Martin-Luther-University of Halle, 06120 Halle, Germany (E.G.-B.);Institute of Experimental Physics 5, University of Würzburg, 97074 Würzburg, Germany (E.M., P.M.J.);Research Center Magnetic Resonance Bavaria, 97074 Wurzburg, Germany (R.K., P.M.J.);Department of Medical Imaging, University of Ottawa, Ottawa, Ontario, Canada K1Y 4E9 (G.M.); andClayton School of IT, Monash University, Melbourne, Victoria 3800, Australia (F.S.).
authors.forename: Gerd
authors.identifier: http://orcid.org/0000-0001-5387-8958
authors.initials: G
authors.lastname: Melkus
authors.affiliation: Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany (H.R., E.M., V.R., H.T., L.B.);Institut für Pharmazie, Martin-Luther-University of Halle, 06120 Halle, Germany (E.G.-B.);Institute of Experimental Physics 5, University of Würzburg, 97074 Würzburg, Germany (E.M., P.M.J.);Research Center Magnetic Resonance Bavaria, 97074 Wurzburg, Germany (R.K., P.M.J.);Department of Medical Imaging, University of Ottawa, Ottawa, Ontario, Canada K1Y 4E9 (G.M.); andClayton School of IT, Monash University, Melbourne, Victoria 3800, Australia (F.S.).
authors.forename: Falk
authors.initials: F
authors.lastname: Schreiber
authors.affiliation: Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany (H.R., E.M., V.R., H.T., L.B.);Institut für Pharmazie, Martin-Luther-University of Halle, 06120 Halle, Germany (E.G.-B.);Institute of Experimental Physics 5, University of Würzburg, 97074 Würzburg, Germany (E.M., P.M.J.);Research Center Magnetic Resonance Bavaria, 97074 Wurzburg, Germany (R.K., P.M.J.);Department of Medical Imaging, University of Ottawa, Ottawa, Ontario, Canada K1Y 4E9 (G.M.); andClayton School of IT, Monash University, Melbourne, Victoria 3800, Australia (F.S.).
authors.forename: Peter M
authors.identifier: http://orcid.org/0000-0002-3481-5545
authors.initials: PM
authors.lastname: Jakob
authors.affiliation: Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany (H.R., E.M., V.R., H.T., L.B.);Institut für Pharmazie, Martin-Luther-University of Halle, 06120 Halle, Germany (E.G.-B.);Institute of Experimental Physics 5, University of Würzburg, 97074 Würzburg, Germany (E.M., P.M.J.);Research Center Magnetic Resonance Bavaria, 97074 Wurzburg, Germany (R.K., P.M.J.);Department of Medical Imaging, University of Ottawa, Ottawa, Ontario, Canada K1Y 4E9 (G.M.); andClayton School of IT, Monash University, Melbourne, Victoria 3800, Australia (F.S.) borysyuk@ipk-gatersleben.de.
authors.forename: Ljudmilla
authors.identifier: http://orcid.org/0000-0001-6910-0841
authors.initials: L
authors.lastname: Borisjuk
mesh_terms: D050260:Carbohydrate Metabolism; D002244:Carbon / Q000378:metabolism*; D002523:Edible Grain / Q000166:cytology / Q000235:genetics / Q000378:metabolism* / Q000528:radiation effects; D001467:Hordeum / Q000166:cytology / Q000235:genetics / Q000378:metabolism* / Q000528:radiation effects; D008027:Light; D064688:Metabolic Flux Analysis; D010788:Photosynthesis; D018515:Plant Leaves / Q000166:cytology / Q000235:genetics / Q000378:metabolism / Q000528:radiation effects; D013213:Starch / Q000378:metabolism; D014908:Triticum / Q000166:cytology / Q000235:genetics / Q000378:metabolism* / Q000528:radiation effects
chemical_list: D002244:Carbon; D013213:Starch