Tomaz T, Bagard M, Pracharoenwattana I, Lindén P, Lee CP, Carroll AI, Ströher E, Smith SM, Gardeström P, Millar AH
Mitochondrial malate dehydrogenase lowers leaf respiration and alters photorespiration and plant growth in Arabidopsis
Plant Physiology: 2010 154: 1143-1157

Malate dehydrogenase (MDH) catalyzes a reversible NAD+-dependent-dehydrogenasereaction involved in central metabolism and redox homeostasisbetween organelle compartments. To explore the role of mitochondrialMDH (mMDH) in Arabidopsis (Arabidopsis thaliana), knockout singleand double mutants for the highly expressed mMDH1 and lowerexpressed mMDH2 isoforms were constructed and analyzed. A mmdh1mmdh2mutant has no detectable mMDH activity but is viable, albeitsmall and slow growing. Quantitative proteome analysis of mitochondriashows changes in other mitochondrial NAD-linked dehydrogenases,indicating a reorganization of such enzymes in the mitochondrialmatrix. The slow-growing mmdh1mmdh2 mutant has elevated leafrespiration rate in the dark and light, without loss of photosyntheticcapacity, suggesting that mMDH normally uses NADH to reduceoxaloacetate to malate, which is then exported to the cytosol,rather than to drive mitochondrial respiration. Increased respiratoryrate in leaves can account in part for the low net CO2 assimilationand slow growth rate of mmdh1mmdh2. Loss of mMDH also affectsphotorespiration, as evidenced by a lower postillumination burst,alterations in CO2 assimilation/intercellular CO2 curves atlow CO2, and the light-dependent elevated concentration of photorespiratorymetabolites. Complementation of mmdh1mmdh2 with an mMDH cDNArecovered mMDH activity, suppressed respiratory rate, amelioratedchanges to photorespiration, and increased plant growth. A previouslyestablished inverse correlation between mMDH and ascorbate contentin tomato (Solanum lycopersicum) has been consolidated in Arabidopsisand may potentially be linked to decreased galactonolactonedehydrogenase content in mitochondria in the mutant. Overall,a central yet complex role for mMDH emerges in the partitioningof carbon and energy in leaves, providing new directions forbioengineering of plant growth rate and a new insight into themolecular mechanisms linking respiration and photosynthesisin plants.

E-link to journal