Pleiotropic effects of enhancing vacuolar K/H exchange in tomato

Cation antiporters of the NHX family are widely regarded as determinants of salt tolerance due to their capacity to drive sodium (Na) and sequester it into vacuoles. Recent work shows, however, that NHX transporters are primarily involved in vacuolar potassium (K) storage. Over-expression of the K/H antiporter AtNHX1 in tomato increases K accumulation into vacuoles and plant sensitivity to K deprivation. Here we show that the appearance of early leaf symptoms of K deficiency was associated with higher concentration of polyamines. Transgenic roots exhibited a greater sensitivity than shoots to K deprivation with changes in the composition of the free amino acids pool, total sugars and organic acids. Concentrations of amides (glutamine), amino acids (arginine) and sugars significantly increased in root, together with a reduction in malate and succinate concentrations. The concentration of pyruvate and the activity of pyruvate kinase were greater in the transgenic roots before K withdrawal although both parameters were depressed by K deprivation and approached wild-type levels. In the longer term, the over-expression of the NHX1 antiporter affected root growth and biomass partitioning (shoot/root ratio). Greater ethylene release produced longer stem internodes and leaf curling in the transgenic line. Our data show that enhanced sequestration of K by the NHX antiporter in the vacuoles altered cellular K homeostasis and had deeper physiological consequences than expected. Early metabolic changes lead later on to profound morphological and physiological adjustments resulting eventually in the loss of nutrient use efficiency.