Regulation of glucosylceramide synthase and sphingolipid remodeling in the plant response to phosphate deficiency

Sphingolipids are important and abundant lipids in the plasma membrane, and their homeostasis plays a key role in plant growth, development, and stress responses. We previously found that nonspecific phospholipase C4 (NPC4) hydrolyzes sphingophospholipids upon phosphate starvation. Here, we defined the downstream steps of sphingolipid remodeling by identifying glucosylceramide synthase (GCS) and its regulatory mechanisms in Arabidopsis thaliana. Phosphate deficiency induces the expression of GCS, and the encoded GCS enzyme mediates glucosylceramide biosynthesis. Downregulation of GCS severely affects sphingolipid homeostasis and hinders plant growth under phosphate starvation. Accordingly, GCS overexpression promotes sphingolipid remodeling to maintain plant growth. In addition, PHOSPHATE STARVATION RESPONSE1 (PHR1), a key regulator of phosphate homeostasis, directly affects the expression of NPC4 and GCS to regulate sphingolipid remodeling during phosphate starvation. Together, these results identify the PHR1-NPC4-GCS module as a regulatory mechanism that fine-tunes sphingolipid homeostasis and reveal the importance of sphingolipid homeostasis in the plant response to phosphate deficiency.