Reduced Expression of Succinyl-Coenzyme A Ligase Can Be Compensated for by Up-Regulation of the γ-Aminobutyrate Shunt in Illuminated Tomato Leaves

Abstract

Increasing experimental evidence suggests that the tricarboxylic acid cycle in plants is of greater importance in illuminated photosynthetic tissues than previously thought. In this study, transgenic tomato (Solanum lycopersicum) plants expressing a fragment of the β-subunit of succinyl-coenzyme A ligase in either the antisense orientation or using the RNA interference approach, however, revealed little alteration in either photosynthesis or plant growth despite exhibiting dramatic reductions in activity. Moreover, the rate of respiration was only moderately affected in the transformants, suggesting that this enzyme does not catalyze a crucial step in mitochondrial respiration. However, metabolite and transcript profiling of these lines alongside enzyme and label redistribution experiments revealed that, whereas considerable activity of this enzyme appears to be dispensable, the reason for such a mild phenotype in extremely inhibited lines was an up-regulation of an alternative pathway for succinate production—that offered by the γ-aminobutyric acid shunt. When taken together, these data highlight the importance both of succinate production for mitochondrial metabolism and the interplay between various routes of its production. The results are discussed in the context of current models of plant respiration in mitochondrial and cellular metabolism of the illuminated leaf.