Salinity is detrimental to plant growth, crop production and food security worldwide. Excess salt triggers increases in cytosolic Ca²⁺ concentration, which activate Ca²⁺-binding proteins and upregulate the Na⁺/H⁺ antiporter in order to remove Na⁺. Salt-induced increases in Ca²⁺ have long been thought to be involved in the detection of salt stress, but the molecular components of the sensing machinery remain unknown. Here, using Ca²⁺-imaging-based forward genetic screens, we isolated the Arabidopsis thaliana mutant monocation-induced [Ca^2+]_iincreases 1 (moca1), and identified MOCA1 as a glucuronosyltransferase for glycosyl inositol phosphorylceramide (GIPC) sphingolipids in the plasma membrane. MOCA1 is required for salt-induced depolarization of the cell-surface potential, Ca²⁺ spikes and waves, Na⁺/H⁺ antiporter activation, and regulation of growth. Na⁺ binds to GIPCs to gate Ca²⁺ influx channels. This salt-sensing mechanism might imply that plasma-membrane lipids are involved in adaption to various environmental salt levels, and could be used to improve salt resistance in crops.