ORM: A Central Regulator of Sphingolipid Homeostasis and Composition in Arabidopsis

Abstract

The sphingolipid metabolic network in Arabidopsis is tightly regulated to ensure sufficient biosynthetic flux to support cell viability and growth but to also rapidly respond to perturbations such as those induced by bacterial pathogenesis that trigger production of the bioactive sphingolipid metabolites. These metabolites include long‐chain bases and ceramides that signal programmed cell death (PCD) for plant defense. Regulation of sphingolipid biosynthesis is mediated primarily through reversible physical interactions, of serine palmitoyltransferase (SPT), the initial enzyme in long‐chain base biosynthesis, with ORM proteins (orosomucoid‐like proteins). Consistent with a role of ORMs as repressors of SPT activity, overexpression of the two Arabidopsis ORM proteins AtORM1 and AtORM2 strongly reduced the accumulation of free long‐chain bases in response to treatment with the mycotoxin fumonisin B1 (FB1), a ceramide synthase inhibitor. These plants also displayed increased resistance to the PCD‐inducing cytotoxicity of FB1. Conversely, RNAi suppression of AtORM1/2 resulted in large increases in long‐chain bases in response to FB1 treatment and increased sensitivity to FB1. AtORM1 and 2 overexpressing plants also had decreased activity of Class I ceramide synthase that generates ceramides with C16 fatty acids and dihydroxy long‐chain bases and increased activity of Class II ceramide synthases that produce ceramides with very‐long chain fatty acids and trihydroxy long‐chain bases. The reverse effect on ceramide synthase activities was observed in AtORM RNAi lines. These findings suggest an extended role of ORMs as regulators of the production of structurally and functionally distinct ceramides for glycosphingolipid synthesis to support plant growth and long‐chain base homeostasis.