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First published online August 8, 2003; 10.1105/tpc.012500

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The Plant Cell, Vol. 15, 2140-2151, September 2003, Copyright © 2003,
American Society of Plant Biologists

Enzymes of Glycolysis Are Functionally Associated with the Mitochondrion in Arabidopsis Cells

Philippe Giegéa, Joshua L. Heazlewoodb, Ute Roessner-Tunalic, A. Harvey Millarb, Alisdair R. Ferniec, Christopher J. Leaverd and Lee J. Sweetlove1,d

a Institut de Biologie Moléculaire des Plantes, Strasbourg 67084, France
b School of BioMedical and Chemical Sciences, University of Western Australia, Crawley 6009, Western Australia, Australia
c Department of Lothar Willmitzer, Max-Planck-Institute for Molecular Plant Physiology, 14476 Golm, Germany
d Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom

1 To whom correspondence should be addressed. E-mail lee.sweetlove{at}plants.ox.ac.uk; fax 44-(0)1865-275074

Mitochondria fulfill a wide range of metabolic functions in addition to the synthesis of ATP and contain a diverse array of proteins to perform these functions. Here, we present the unexpected discovery of the presence of the enzymes of glycolysis in a mitochondrial fraction of Arabidopsis cells. Proteomic analyses of this mitochondrial fraction revealed the presence of 7 of the 10 enzymes that constitute the glycolytic pathway. Four of these enzymes (glyceraldehyde-3-P dehydrogenase, aldolase, phosphoglycerate mutase, and enolase) were also identified in an intermembrane space/outer mitochondrial membrane fraction. Enzyme activity assays confirmed that the entire glycolytic pathway was present in preparations of isolated Arabidopsis mitochondria, and the sensitivity of these activities to protease treatments indicated that the glycolytic enzymes are present on the outside of the mitochondrion. The association of glycolytic enzymes with mitochondria was confirmed in vivo by the expression of enolase– and aldolase–yellow fluorescent protein fusions in Arabidopsis protoplasts. The yellow fluorescent protein fluorescence signal showed that these two fusion proteins are present throughout the cytosol but are also concentrated in punctate regions that colocalized with the mitochondrion-specific probe Mitotracker Red. Furthermore, when supplied with appropriate cofactors, isolated, intact mitochondria were capable of the metabolism of 13C-glucose to 13C-labeled intermediates of the trichloroacetic acid cycle, suggesting that the complete glycolytic sequence is present and active in this subcellular fraction. On the basis of these data, we propose that the entire glycolytic pathway is associated with plant mitochondria by attachment to the cytosolic face of the outer mitochondrial membrane and that this microcompartmentation of glycolysis allows pyruvate to be provided directly to the mitochondrion, where it is used as a respiratory substrate.




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