Phosphate starvation causes different stress responses in the lipid metabolism of tomato leaves and roots

Abstract

Plants have evolved various acclimation responses to cope with phosphate depletion, including several changes in lipid metabolism. Thereby membrane phospholipids are dephosphorylated and can be used as an internal phosphate source, while galactolipids are incorporated into the membrane to maintain membrane functionality. Still little is known about the lipidomic and transcriptomic response of plants other than Arabidopsis thaliana upon phosphate starvation. Therefore, we employed lipidomics and transcriptomics to characterize the phosphate starvation response of lipid metabolism in tomato leaves and roots. Overall, phospholipid levels decreased and galactolipids increased during the acclimation response. In addition, an early increase of triacylglycerol was observed. Interestingly, there were major differences in the acclimation response of tomato leaves and roots: leaves mainly accumulated polyunsaturated triacylglycerol, while roots showed a massive increase in galactolipid content. In line with these results, we observed transcriptional induction of phospholipid degradation and galactolipid synthesis pathways in both analyzed tissues. In contrast, other aspects of the transcriptional response, in particular, the induction of phospholipid degradation, ER-localized fatty acid desaturation and triacylglycerol assembly differed between tomato leaves and roots. These results suggest a different modulation of degraded phospholipids toward triacylglycerols and galactolipids in phosphate-starved tomato leaves and roots. Possibly the availability and composition of acyl-CoA pools and ER-derived precursors trigger the synthesis of triacylglycerols or galactolipids. As the mechanism of triacylglycerol accumulation is poorly characterized outside of seed oil formation, these findings enhance our understanding of the phosphate starvation response and of how storage lipids accumulate under stress in vegetative tissue.

Keywords: Acyl-CoA pool; Lipid remodeling; Lipidomics; Phosphate starvation; Tomato; Triacylglycerol.