Tissue-specific responses of the central carbon metabolism in tomato fruit to low oxygen stress

Abstract

Tomato (Solanum lycopersicum L.) is an important model plant whose fleshy fruit consists of well-differentiated tissues. Recently it was shown that these tissues develop hypoxia during fruit development and ripening. Therefore, we employed a combination of metabolomics and isotopic labeling to investigate the central carbon metabolic response of tomato fruit tissues (columella, septa and mesocarp) to low O2 stress. The concentration and 13C-label enrichment of intermediates from the central carbon metabolism were analyzed using gas chromatography-mass spectrometry. The results showed an increase in glycolytic activity and the initiation of fermentation in response to low O2 conditions. In addition, the up-regulation of the GABA shunt and accumulation of amino acids, alanine and glycine, were observed under low O2 conditions. Notably, tissue specificity was observed at the metabolite level, with concentrations of most metabolites being highest in columella tissue. In addition, there were tissue-specific differences in the central carbon metabolism with the columella exhibiting the highest metabolic activity and sensitivity to the changes in O2 concentration, followed by septa and mesocarp tissues. Our results are consistent with common plant responses and adaptive mechanisms to low O2 stress, while unravelling some tissue-specific differences, increasing our understanding of the intact fruit response to low O2 stress.