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Phospholipase Dα (PLDα), which produces signaling molecules phosphatidic acid (PA), has been shown to play a critical role in plants adapting to salt environments. However, it is unclear whether phospholipase Dδ (PLDδ) can mediate the salt response in higher plants. <i>PePLDδ</i> was isolated from salt-resistant <i>Populus euphratica</i> and transferred to <i>Arabidopsis thaliana</i> to testify the salt tolerance of transgenic plants. The NaCl treatment (130 mM) reduced the root growth and whole-plant fresh weight of wild-type (WT) <i>A. thaliana</i>, vector controls (VC) and <i>PePLDδ</i>-overexpressed lines, although a less pronounced effect was observed in transgenic plants. Under salt treatment, <i>PePLDδ</i>-transgenic Arabidopsis exhibited lower electrolyte leakage, malondialdehyde content and H₂O₂ levels than WT and VC, resulting from the activated antioxidant enzymes and upregulated transcripts of genes encoding superoxide dismutase, ascorbic acid peroxidase and peroxidase. In addition, <i>PePLDδ</i>-overexpressed plants increased the transcription of genes encoding the plasma membrane Na⁺/H⁺ antiporter (<i>AtSOS1</i>) and H⁺-ATPase (<i>AtAHA2</i>), which enabled transgenic plants to proceed with Na⁺ extrusion and reduce K⁺ loss under salinity. The capacity to regulate reactive oxygen species (ROS) and K⁺/Na⁺ homeostasis was associated with the abundance of specific PA species in plants overexpressing <i>PePLDδ</i>. <i>PePLDδ</i>-transgenic plants retained a typically higher abundance of PA species, 34:2 (16:0–18:2), 34:3 (16:0–18:3), 36:4 (18:2–18:2), 36:5 (18:2–18:3) and 36:6 (18:3–18:3), under control and saline conditions. It is noteworthy that PA species 34:2 (16:0–18:2), 34:3 (16:0–18:3), 36:4 (18:2–18:2) and 36:5 (18:2–18:3) markedly increased in response to NaCl in transgenic plants. In conclusion, we suppose that <i>PePLDδ</i>-derived PA enhanced the salinity tolerance by regulating ROS and K⁺/Na⁺ homeostasis in Arabidopsis.