Phosphatidic acid phosphohydrolase modulates glycerolipid synthesis in Marchantia polymorpha and is crucial for growth under both nutrient-replete and -deficient conditions.

ABSTRACT

MAIN CONCLUSION: The phosphatidic acid phosphohydrolase of Marchantia polymorpha modulates plastid glycolipid synthesis through the ER pathway and is essential for normal plant development regardless of nutrient availability. Membrane lipid remodeling is one of the strategies plant cells use to secure inorganic phosphate (Pi) for plant growth, but many aspects of the molecular mechanism and its regulation remain unclear. Here we analyzed membrane lipid remodeling using a non-vascular plant, Marchantia polymorpha. The lipid composition and fatty acid profile during Pi starvation in M. polymorpha revealed a decrease in phospholipids and an increase in both galactolipids and betaine lipids. In Arabidopsis thaliana, phosphatidic acid phosphohydrolase (PAH) is involved in phospholipid degradation and is crucial for tolerance to both Pi and nitrogen starvation. We produced two M. polymorpha PAH (MpPAH) knockout mutants (Mppah-1 and Mppah-2) and found that, unlike Arabidopsis mutants, Mppah impaired plant growth with shorter rhizoids compared with wild-type plants even under nutrient-replete conditions. Mutation of MpPAH did not significantly affect the mole percent of each glycerolipid among total membrane glycerolipids from whole plants under both Pi-replete and Pi-deficient conditions. However, the fatty acid composition of monogalactosyldiacylglycerol indicated that the amount of plastid glycolipids produced through the endoplasmic reticulum pathway was suppressed in Mppah mutants. Phospholipids accumulated in the mutants under N starvation. These results reveal that MpPAH modulates plastid glycolipid synthesis through the endoplasmic reticulum pathway more so than what has been observed for Arabidopsis PAH; moreover, unlike Arabidopsis, MpPAH is crucial for M. polymorpha growth regardless of nutrient availability.