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Na⁺/H⁺ antiporters (NHXs) are integral membrane transporters that catalyze the electroneutral exchange of K⁺ or Na⁺ for H⁺ and are implicated in cell expansion, development, pH and ion homeostasis and salt tolerance. Arabidopsis contains four vacuolar NHX isoforms (NHX1-NHX4), but only the functional roles for NHX1 and NHX2 have been assessed thus far. Colocalization studies indicated that NHX3 and NHX4 colocalize to the tonoplast. To investigate the role of all vacuolar NHX isoforms, a quadruple knockout nhx1nhx2nhx3nhx4, lacking all vacuolar NHXs, was generated. Seedlings of nhx1nhx2nhx3nhx4 displayed significantly reduced growth, with markedly shorter hypocotyls. Under high K⁺, but not Na⁺, pronounced root skewing occurred in nhx1nhx2nhx3nhx4, suggesting that the organization of the cytoskeleton might be perturbed. Whole mount immunolabeling of cortical microtubules indicated that high K⁺ caused significant microtubule reorganization in nhx1nhx2nhx3nhx4 root cells of the elongation zone. Using microtubule stabilizing (Taxol) and destabilizing (propyzamide) drugs, we found that the effect of K⁺ on nhx1nhx2nhx3nhx4 root growth was antagonistic to that of Taxol, whereas elevated K⁺ exacerbated the endogenous effect of propyzamide on root skewing. Collectively, our results suggest that altered K⁺ homeostasis leads to an increase in the dynamics of cortical microtubule reorganization in nhx1nhx2nhx3nhx4 root epidermal cells of the elongation zone.

Vacuolar Na+/H+ NHX-Type Antiporters Are Required for Cellular K+ Homeostasis, Microtubule Organization and Directional Root Growth