Lipidomic and transcriptomic analysis of glycerolipid metabolism in phosphate-starved Solanum lycopersicum

Phosphorus is an essential element influencing plant growth and development. To cope with phosphate depletion plants have evolved various acclimation responses including the activation of several changes in lipid metabolism. Through these changes, membrane phospholipids serve as internal phosphate source, whereby phospholipids are replaced by galactolipids to maintain membrane functionality. Mostly in Arabidopsis thaliana this process was investigated by lipidomic and transcriptomic analysis. Some phosphate depletion activated genes were identified, responsible for the remodeling process within the plant, but still little is known about the transcriptional response of lipid metabolism in detail. Furthermore, the membrane remodeling process occurs in a wide variety of plants other than Arabidopsis thaliana making it important to explore this process to agricultural relevant crop plants. Therefore, a combined survey of glycerolipid and differential expression analysis was conducted using mass spectrometric and RNA-sequencing based methods to investigate the adaption of Solanum lycopersicum leaves and roots to phosphate starvation. Data revealed decreased amounts of phospholipids while galactolipid levels increased and in addition an early increase of triacylglycerol in parallel to galactolipid accumulation was observed. Interestingly, lipid analysis further revealed major differences in the adaption of tomato leaves compared to roots as leaves mainly accumulated polyunsaturated triacylglycerol, while roots showed massive increase in galactolipid content. In line with these results, differential expression analysis exhibited transcriptional induction of phospholipid degradation and galactolipid synthesis pathway, but also showed different transcriptional responses of tomato leaves and roots. In particular, the induction of phospholipid degradation, triacylglycerol assembly and ER-localized fatty acid desaturation were different. In the present study, results suggest a different flux of degraded phospholipids toward triacylglycerol and galactolipids in phosphate-starved tomato leaves and roots. Possibly the availability and composition of acyl-CoA pools and ER-derived precursors triggers the flux of degraded phospholipids toward triacylglycerol or galactolipid synthesis. These findings enhance our knowledge about molecular processes within the plant associated with phosphate deficiency and enable the identification of further key molecular compounds. In addition, the combination of lipidomic and transcriptomic analysis in two different tissues of tomato plants, promote the understanding of how plants respond to phosphate starvation and how storage lipid accumulation is regulated in vegetative tissue