Plants cope with aluminum (Al) toxicity by secreting organic acids (OAs) into the apoplastic space, which is driven by proton (H⁺) pumps. Here, we show that mutation of vacuolar H⁺-translocating adenosine triphosphatase (H⁺-ATPase) subunit a2 (VHA-a2) and VHA-a3 of the vacuolar H⁺-ATPase enhances Al resistance in Arabidopsis (Arabidopsis thaliana). vha-a2 vha-a3 mutant plants displayed less Al sensitivity with less Al accumulation in roots compared to wild-type plants when grown under excessive Al³⁺ Interestingly, in response to Al³⁺ exposure, plants showed decreased vacuolar H⁺ pump activity and reduced expression of VHA-a2 and VHA-a3, which were accompanied by increased plasma membrane H⁺ pump (PM H⁺-ATPase) activity. Genetic analysis of plants with altered PM H⁺-ATPase activity established a correlation between Al-induced increase in PM H⁺-ATPase activity and enhanced Al resistance in vha-a2 vha-a3 plants. We determined that external OAs, such as malate and citrate whose secretion is driven by PM H⁺-ATPase, increased with PM H⁺-ATPase activity upon Al stress. On the other hand, elevated secretion of malate and citrate in vha-a2 vha-a3 root exudates appeared to be independent of OAs metabolism and tolerance of phosphate starvation but was likely related to impaired vacuolar sequestration. These results suggest that coordination of vacuolar H⁺-ATPase and PM H⁺-ATPase dictates the distribution of OAs into either the vacuolar lumen or the apoplastic space that, in turn, determines Al tolerance capacity in plants.

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