Arabidopsis lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation

Abstract

Phosphate is an essential nutrient for plant viability. It is well-established that phosphate starvation triggers membrane lipid remodeling, a process that converts significant portion of phospholipids to non-phosphorus-containing galactolipids. This remodeling is mediated by either phospholipase C (PLC) or phospholipase D (PLD) in combination with phosphatidate phosphatase (PAP). Two PLC genes, NPC4 and NPC5, and PLD genes, PLDζ1 and PLDζ2, are shown to be involved in the remodeling. However, gene knockout studies show that none of them plays decisive roles in the remodeling. Thus, although this phenomenon is widely observed among plants, the key enzyme(s) responsible for the lipid remodeling in a whole plant body is unknown; therefore, the physiological significance of this conversion process has remained to be elucidated. We herein focused on PAP as a key enzyme for this adaptation, and identified Arabidopsis lipin homologs, AtPAH1 and AtPAH2, that encode the PAPs involved in galactolipid biosynthesis. Double mutant pah1pah2 plants had decreased phosphatidic acid hydrolysis, thus affecting the eukaryotic pathway of galactolipid synthesis. Upon phosphate starvation, pah1pah2 plants were severely impaired in growth and membrane lipid remodeling. These results indicate that PAH1 and PAH2 are the PAP responsible for the eukaryotic pathway of galactolipid synthesis, and the membrane lipid remodeling mediated by these two enzymes is an essential adaptation mechanism to cope with phosphate starvation.