Mitochondrial glutamine synthetase overexpression in tomato source leaves increases assimilate export and fruit yield

To identify potential strategies for increasing the efficiency of tomato leaf metabolism, with a focus on the links between nitrogen/carbon metabolism, we explored a diel Flux Balance Analysis (FBA) model of a source leaf in which the metabolic output was varied up to the theoretically-achievable maximum. We noticed a potentially interesting switch in the use of glutamine synthetase (GS) isoforms -from the chloroplast isoform to the mitochondrial one- for nitrogen assimilation. To further explore this prediction, we characterized transgenic tomato plants over-expressing two tomato GS genes, GS1 and GS2, targeted to mitochondria. Both sets of transgenic plants were characterized as displaying faster growth rate, early flowering and increased fruit yield. In leaves, metabolomic profiling and enzyme activity analysis pointed that GS activity in mitochondria plays a role in increasing the intracellular synthesis and subsequent export of sugar. Consistent with these changes, higher sucrose concentration in leaf exudates and reduced activities of enzymes involved in leaf starch synthesis were observed. Moreover, mitochondrial GS activity affected chloroplast redox status in a manner that modulated photorespiration and nitrogen metabolism. The combined data reveal the influence of mitochondrial GS activity on both foliar carbon/nitrogen balance and regulation of source-sink metabolism in tomato plants.