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J. Biol. Chem., Vol. 281, Issue 45, 34040-34047, November 10, 2006

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Mitochondrial Metabolism in Developing Embryos of Brassica napus^*

Jörg Schwender¹, Yair Shachar-Hill, and John B. Ohlrogge

From the Biology Department, Brookhaven National Laboratory, Upton, New York 11973 and the Plant Biology Department, Michigan State University, East Lansing, Michigan 48824

The metabolism of developing plant seeds is directed toward transforming primary assimilatory products (sugars and amino acids) into seed storage compounds. To understand the role of mitochondria in this metabolism, metabolic fluxes were determined in developing embryos of Brassica napus. After labeling with [1,2-¹³C₂]glucose + [U-¹³C₆]glucose, [U-¹³C₃]alanine, [U-¹³C₅]glutamine, [¹⁵N]alanine, (amino)-[¹⁵N]glutamine, or (amide)-[¹⁵N]glutamine, the resulting labeling patterns in protein amino acids and in fatty acids were analyzed by gas chromatography-mass spectrometry. Fluxes through mitochondrial metabolism were quantified using a steady state flux model. Labeling information from experiments using different labeled substrates was essential for model validation and reliable flux estimation. The resulting flux map shows that mitochondrial metabolism in these developing seeds is very different from that in either heterotrophic or autotrophic plant tissues or in most other organisms: (i) flux around the tricarboxylic acid cycle is absent and the small fluxes through oxidative reactions in the mitochondrion can generate (via oxidative phosphorylation) at most 22% of the ATP needed for biosynthesis; (ii) isocitrate dehydrogenase is reversible in vivo; (iii) about 40% of mitochondrial pyruvate is produced by malic enzyme rather than being imported from the cytosol; (iv) mitochondrial flux is largely devoted to providing precursors for cytosolic fatty acid elongation; and (v) the uptake of amino acids rather than anaplerosis via PEP carboxylase determines carbon flow into storage proteins.

Received for publication, June 30, 2006 , and in revised form, September 11, 2006.

^* This work was supported by National Science Foundation Grant MCB 0224655, United States Department of Agriculture Grant 2003-35321-12935, and by a Laboratory Directed Research and Development Award at the Brookhaven National Laboratory under contract with the United States Department of Energy (to J. S.). Acknowledgment is also made to the Michigan Agricultural Experiment Station for its support of this research. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental text, Figs. S1–S6, Tables S1–S10, and references.

This article was selected as a Paper of the Week.

¹ To whom correspondence should be addressed: Biology Dept., Brookhaven National Laboratory, Bldg. 463, Upton, NY 11973. Tel.: 631-344-3797; Fax: 631-344-3407; E-mail: Schwender{at}BNL.gov.

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