Evidence of a key role for photosynthetic oxygen release in oil storage in developing soybean seeds.

Based on the topographical analysis of photosynthesis and oil storage, we propose in a companion paper that photosynthetic oxygen release plays a key role in the local energy state, storage metabolism and flux toward lipid biosynthesis in developing soybean seeds. To test this hypothesis, we combined topographical analysis of ATP gradients across tissues, microsensor quantifications of internal O2 levels, assays of energy balance, metabolite profiles and isotope-labelling studies. Seeds show a marked degree of oxygen starvation in vivo (minimum O2 levels 0.1 kPa, approximately 1.3 microm), affecting ATP gradients, overall energy state, metabolite pools and storage activity. Despite the low light availability, photosynthesis supplies significant amounts of oxygen to the hypoxic seed tissue. This is followed by an increase in local ATP levels, most prominently within the lipid-synthesizing (inner) regions of the embryo. Concomitantly, partitioning of 14C-sucrose to lipids is increased, suggesting higher rates of lipid biosynthesis. It is concluded that both respiratory and biosynthetic fluxes are dynamically adjusted to photosynthetic oxygen supply.

[1]  Layzell,et al.  Evidence for light-stimulated fatty acid synthesis in soybean fruit , 1999, Plant physiology.

[2]  Jörg Schwender,et al.  Probing in Vivo Metabolism by Stable Isotope Labeling of Storage Lipids and Proteins in Developing Brassica napusEmbryos1 , 2002, Plant Physiology.

[3]  M. Jackson,et al.  Mechanisms of flood tolerance in plants , 1994 .

[4]  Tim Dwyer,et al.  Representing Experimental Biological Data in Metabolic Networks , 2004, APBC.

[5]  Winfriede Weschke,et al.  Energy state and its control on seed development: starch accumulation is associated with high ATP and steep oxygen gradients within barley grains. , 2004, Journal of experimental botany.

[6]  H. Rolletschek,et al.  Antisense-inhibition of ADP-glucose pyrophosphorylase in Vicia narbonensis seeds increases soluble sugars and leads to higher water and nitrogen uptake , 2002, Planta.

[7]  Ganesh Sriram,et al.  Quantification of Compartmented Metabolic Fluxes in Developing Soybean Embryos by Employing Biosynthetically Directed Fractional 13C Labeling, Two-Dimensional [13C, 1H] Nuclear Magnetic Resonance, and Comprehensive Isotopomer Balancing1[w] , 2004, Plant Physiology.

[8]  Thomas Girke,et al.  Contrapuntal Networks of Gene Expression during Arabidopsis Seed Filling Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000877. , 2002, The Plant Cell Online.

[9]  Joost T. van Dongen,et al.  Lipid Storage Metabolism Is Limited by the Prevailing Low Oxygen Concentrations within Developing Seeds of Oilseed Rape1 , 2003, Plant Physiology.

[10]  F.W.T. Penning de Vries,et al.  A rapid method for determining the efficiency of biosynthesis of plant biomass , 1987 .

[11]  W. J. Dyer,et al.  A rapid method of total lipid extraction and purification. , 1959, Canadian journal of biochemistry and physiology.

[12]  U. Wobus,et al.  Molecular physiology of legume seed development. , 2005, Annual review of plant biology.

[13]  R. Ratcliffe,et al.  An in vivo 31P NMR study of the phosphorus metabolites in developing seeds of wheat, soybean and mustard , 1997 .

[14]  F. Carrari,et al.  Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. , 2004, Current opinion in plant biology.

[15]  M. Dieuaide-Noubhani,et al.  Quantification of Compartmented Metabolic Fluxes in Maize Root Tips Using Isotope Distribution from 13C- or 14C-Labeled Glucose (*) , 1995, The Journal of Biological Chemistry.

[16]  K. Koch,et al.  Positional cues for the starch/lipid balance in maize kernels and resource partitioning to the embryo. , 2005, The Plant journal : for cell and molecular biology.

[17]  J. H. Thorne.  Temperature and oxygen effects on C-photosynthate unloading and accumulation in developing soybean seeds. , 1982, Plant physiology.

[18]  J. Schwender,et al.  The Capacity of Green Oilseeds to Utilize Photosynthesis to Drive Biosynthetic Processes1 , 2004, Plant Physiology.

[19]  F. Goffman,et al.  Carbon dioxide concentrations are very high in developing oilseeds. , 2004, Plant physiology and biochemistry : PPB.

[20]  M. Hills.  Control of storage-product synthesis in seeds. , 2004, Current opinion in plant biology.

[21]  J. Ohlrogge,et al.  A new set of Arabidopsis expressed sequence tags from developing seeds. The metabolic pathway from carbohydrates to seed oil. , 2000, Plant physiology.

[22]  Malcolm C. Drew,et al.  OXYGEN DEFICIENCY AND ROOT METABOLISM: Injury and Acclimation Under Hypoxia and Anoxia. , 1997, Annual review of plant physiology and plant molecular biology.

[23]  M. Emes,et al.  NONPHOTOSYNTHETIC METABOLISM IN PLASTIDS. , 2003, Annual review of plant physiology and plant molecular biology.

[24]  H. Rolletschek,et al.  Spatial analysis of plant metabolism: sucrose imaging within Vicia faba cotyledons reveals specific developmental patterns. , 2002, The Plant journal : for cell and molecular biology.

[25]  H. Rolletschek,et al.  Energy status and its control on embryogenesis of legumes: ATP distribution within Vicia faba embryos is developmentally regulated and correlated with photosynthetic capacity. , 2003, The Plant journal : for cell and molecular biology.

[26]  A. Rasmusson,et al.  Light Regulation of the Arabidopsis Respiratory Chain. Multiple Discrete Photoreceptor Responses Contribute to Induction of Type II NAD(P)H Dehydrogenase Genes1 , 2004, Plant Physiology.

[27]  Falk Schreiber,et al.  Integrating data from biological experiments into metabolic networks with the DBE information system , 2004, Silico Biol..

[28]  A. Leopold,et al.  Respiration during seed maturation , 1983 .

[29]  A. Webb,et al.  Gradients of lipid storage, photosynthesis and plastid differentiation in developing soybean seeds. , 2005, The New phytologist.

[30]  C. Raper,et al.  Responses to sucrose and glutamine by soybean embryos grown in vitro , 1995 .

[31]  H. Rolletschek,et al.  Legume embryos develop in a hypoxic environment. , 2002, Journal of experimental botany.

[32]  W. Snedden,et al.  Gaba shunt in developing soybean seeds is associated with hypoxia , 1995 .

[33]  H. Rolletschek,et al.  Energy Status and Its Control on Embryogenesis of Legumes. Embryo Photosynthesis Contributes to Oxygen Supply and Is Coupled to Biosynthetic Fluxes1 , 2003, Plant Physiology.

[34]  Jay J Thelen,et al.  Arabidopsis Genes Involved in Acyl Lipid Metabolism. A 2003 Census of the Candidates, a Study of the Distribution of Expressed Sequence Tags in Organs, and a Web-Based Database1 , 2003, Plant Physiology.

[35]  P. Geigenberger,et al.  Response of plant metabolism to too little oxygen. , 2003, Current opinion in plant biology.