Salinity reduces the growth and productivity of crop plants worldwide. Mangroves have evolved efficient ion homeostasis mechanisms to survive under their natural saline growth habitat. Information obtained from them may be utilized for increasing the salt tolerance of crop plants. We identified and characterized a high-affinity potassium transporter gene (AoHKT1) from Avicennia officinalis. The expression of AoHKT1 was induced by NaCl mainly in the leaves. Functional study by heterologous expression of AoHKT1 in Arabidopsis T-DNA insertional mutants athkt1-1 and athkt1-4 revealed that it could enhance the salt tolerance of the mutant plants. This was accompanied by an increase in K+ accumulation in the leaves. AoHKT1 was localized to the plasma membrane in Arabidopsis, and when expressed in yeast, it could complement the functions of both Na+ and K+ transporters. An attempt was made to identify the upstream regulator of AtHKT1, a close homolog of AoHKT1. Using chromatin immunoprecipitation, luciferase assay and yeast one-hybrid assays, WRKY9 was identified as the main transcription factor in the process. Furthermore, this was corroborated by the observation that AtHKT1 levels were significantly reduced in the atwrky9 seedlings. These findings revealed a part of the molecular regulatory mechanism of HKT1 induction in response to salt treatment in Arabidopsis. Our study suggests that AoHKT1 is a potential candidate for generating crop plants with increased salt tolerance.