Distinctly localized lipid phosphate phosphatases mediate endoplasmic reticulum glycerolipid metabolism in Arabidopsis

• Published in: The Plant cell 2023-04, Vol.35 (5), p.1548-1571
• Main Authors: Nguyen, Van C, Nakamura, Yuki
• Format: Article
• Language: English
• Subjects: Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Endoplasmic Reticulum - metabolism; Lipid Metabolism - genetics; Membrane Lipids - metabolism; Phosphatidate Phosphatase - genetics; Phosphatidate Phosphatase - metabolism; Phospholipids - metabolism; Triglycerides - metabolism
• ISSN: 1040-4651; 1532-298X
• DOI: 10.1093/plcell/koad021

Abstract Inter-organelle communication is an integral subcellular process in cellular homeostasis. In plants, cellular membrane lipids are synthesized in the plastids and endoplasmic reticulum (ER). However, the crosstalk between these organelles in lipid biosynthesis remains largely unknown. Here, we show that a pair of lipid phosphate phosphatases (LPPs) with differential subcellular localizations is required for ER glycerolipid metabolism in Arabidopsis (Arabidopsis thaliana). LPPα2 and LPPε1, which function as phosphatidic acid phosphatases and thus catalyze the core reaction in glycerolipid metabolism, were differentially localized at ER and chloroplast outer envelopes despite their similar tissue expression pattern. No mutant phenotype was observed in single knockout mutants; however, genetic suppression of these LPPs affected pollen growth and ER phospholipid biosynthesis in mature siliques and seeds with compromised triacylglycerol biosynthesis. Although chloroplast-localized, LPPε1 was localized close to the ER and ER-localized LPPα2. This proximal localization is functionally relevant, because overexpression of chloroplastic LPPε1 enhanced ER phospholipid and triacylglycerol biosynthesis similar to the effect of LPPα2 overexpression in mature siliques and seeds. Thus, ER glycerolipid metabolism requires a chloroplast-localized enzyme in Arabidopsis, representing the importance of inter-organelle communication in membrane lipid homeostasis. Functionally redundant phosphate phosphatases localized in the endoplasmic reticulum and chloroplast mediate a crucial step of glycerolipid biosynthesis in pollen and seeds of Arabidopsis