Aquaporins play essential roles in growth and development including stem elongation in plants. Tonoplast aquaporin AtTIP5;1 has been proposed to positively regulate hypocotyl elongation under high concentrations of boron (high-B) in Arabidopsis thaliana (L.) Heynh. However, the mechanism underlying this process remains unanswered. Here, we show that paclobatrazol, an inhibitor of GA biosynthesis, significantly suppressed the hypocotyl cell elongation of wild-type (WT) seedlings, and more strongly suppressed that of AtTIP5;1 overexpressors under high-B stress. Two AtTIP5;1 null mutants displayed arrested elongation of cells in the upper part of hypocotyls compared with the WT in the presence of high-B or GA3. Moreover, paclobatrazol treatment completely inhibited the increases in AtTIP5;1 transcripts induced by high-B, whereas GA3 application upregulated AtTIP5;1 expression in the WT. In addition, treatment with high-B remarkably elevated the expression levels of GA3ox1, GA20ox1 and GA20ox2 - key biosynthesis genes of GAs - in WT seedlings. The GA3 and GA4 content also increased in WT seedlings grown in MS medium containing high-B. Additionally, application of high-B failed to enhance AtTIP5;1 expression in the double mutant rga-24-gai-t6 of DELLA genes. Together, these results suggest that AtTIP5;1 is an essential downstream target of GAs. High-B induces the accumulation of GAs, which activates AtTIP5;1 through modulation of the DELLA proteins Repressor of ga1-3 and GA-insensitive, further promoting hypocotyl elongation in A. thaliana.