Metabolic and Transcriptional Responses of Glycerolipid Pathways to a Perturbation of Glycerol 3-Phosphate Metabolism in Arabidopsis*

Glycerolipid synthesis in plants involves two major metabolic pathways compartmentalized in the chloroplasts and cytosol, respectively. Although these two parallel pathways are regulated with considerable flexibility, the factors mediating this process remain unclear. To investigate the influence of glycerol 3-phosphate (Gly-3-P) on the interactions of the glycerolipid pathways, we generated transgenic Arabidopsis lines with a feedback-resistant Gly-3-P dehydrogenase gene (gpsA(FR)) from Escherichia coli. gpsA(FR) was detected in the cytosol, but augmented Gly-3-P levels were observed in the cytosol as well as in chloroplasts. Glycerolipid composition and fatty acid positional distribution analyses revealed an altered fatty acid flux that affected not only the molar ratios of glycerolipid species but also their fatty acid composition. To decipher this complex pathway, a transgenic line was subjected to lipidomic analysis and a global gene-expression survey. The results revealed that changes in Gly-3-P metabolism caused altered expression of a broad array of genes. When viewed from the perspective of glycerolipid metabolism, coherent networks emerged, revealing that many enzymatic components of the glycerolipid pathways operate in a modular manner under the influence of Gly-3-P. Transcript levels of the enzymes involved in the prokaryotic pathway were mostly induced, whereas genes of the eukaryotic pathway enzymes were largely suppressed. Hence, the gene-expression changes were consistent with the detected biochemical phenotype. Our results suggest that Gly-3-P modulates the balance of the two glycerolipid pathways in Arabidopsis by influencing both metabolic flux and gene transcription.