Lipid signalling mediated by phospholipase D (PLD) plays essential roles in plant growth including stress and hormonal responses. Here we show that PLDζ1 and PLDζ2 have distinct effects on Arabidopsis responses to salinity. A transcriptome analysis of a double pldζ1pldζ2 mutant revealed a cluster of genes involved in abiotic and biotic stresses, such as the high salt-stress responsive genes DDF1 and RD29A. Another cluster of genes with a common expression pattern included ROS detoxification genes involved in electron transport and biotic and abiotic stress responses. Total superoxide dismutase (SOD) activity was induced early in the shoots and roots of all pldζ mutants exposed to mild or severe salinity with the highest SOD activity measured in pldζ2 at 14 days. Lipid peroxidation in shoots and roots was higher in the pldζ1 mutant upon salt treatment and pldζ1 accumulated H2O2 earlier than other genotypes in response to salt. Salinity caused less deleterious effects on K+ accumulation in shoots and roots of the pldζ2 mutant than of wild type, causing only a slight variation in Na+/K+ ratio. Relative growth rates of wild-type plants, pldζ1, pldζ2 and pldζ1pldζ2 mutants were similar in control conditions, but strongly affected by salt in WT and pldζ1. The efficiency of photosystem II, estimated by measuring the ratio of chlorophyll fluorescence (Fv/Fm ratio), was strongly decreased in pldζ1 under salt stress. In conclusion, PLDζ2 plays a key role in determining Arabidopsis sensitivity to salt stress allowing ion transport and antioxidant responses to be finely regulated.