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Previously, we reported that overexpression of <i>AtRH17</i>, an Arabidopsis DEAD-box RNA helicase gene, confers salt stress-tolerance via a pathway other than the well-known salt stress-responsive pathways. To decipher the salt stress-responsive pathway in <i>AtRH17</i>-overexpressing transgenic plants (OXs), we performed RNA-Sequencing and identified 397 differentially expressed genes between wild type (WT) and <i>AtRH17</i> OXs. Among them, 286 genes were upregulated and 111 genes were downregulated in <i>AtRH17</i> OXs relative to WT. Gene ontology annotation enrichment and KEGG pathway analysis showed that the 397 upregulated and downregulated genes are involved in various biological functions including secretion, signaling, detoxification, metabolic pathways, catabolic pathways, and biosynthesis of secondary metabolites as well as in stress responses. Genevestigator analysis of the upregulated genes showed that nine genes, namely, <i>LEA4-5</i>, <i>GSTF6</i>, <i>DIN2</i>/<i>BGLU30</i>, <i>TSPO</i>, <i>GSTF7</i>, <i>LEA18</i>, <i>HAI1</i>, <i>ABR</i>, and <i>LTI30</i>, were upregulated in Arabidopsis under salt, osmotic, and drought stress conditions. In particular, the expression levels of <i>LEA4-5</i>, <i>TSPO</i>, and <i>ABR</i> were higher in <i>AtRH17</i> OXs than in WT under salt stress condition. Taken together, our results suggest that a high <i>AtRH17</i> expression confers salt stress-tolerance through a novel salt stress-responsive pathway involving nine genes, other than the well-known ABA-dependent and ABA-independent pathways.