Pleiotropic effects of enhancing vacuolar K/H exchange in tomato

Abstract

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.

Regulation of K+ Nutrition in Plants

“…An informative work showed that overexpression of the AtNHX1 in tomato induced K + -deficiency symptoms despite transgenic plants having greater K + contents than controls (Leidi et al., 2010). The intense sequestration of K + in NHX1-overexpressing plants reduced cytosolic K + activity, primed the induction of the high-affinity K + uptake system, and elicited an array of metabolic and hormonal disorders related to K + deprivation (Leidi et al., 2010; De Luca et al., 2018). Notwithstanding these unintended effects resulting from NHX overexpression, NHX proteins do increase salt tolerance, presumably because retention of cellular K + is a requisite for adaptation to a saline environment (Jiang et al., 2010).…”

Genome-Wide Identification of the Gossypium hirsutum NHX Genes Reveals That the Endosomal-Type GhNHX4A Is Critical for the Salt Tolerance of Cotton

“…The result suggests that the TRV:GhNHX4A plants accumulate Na + in the stem, but not K + in the roots, in response to salt stress. The overexpression of AtNHX1 in A. thaliana increases the resistance of the transgenic plants to Na + and induces the absorption of K + [ 16 , 66 , 67 ]. Similarly, AtNHX1 -overexpressing wheat plants treated with 100–150 mM NaCl have lower Na + concentrations and higher K + concentrations than wild-type lines [ 68 ].…”

Ion transporters and their molecular regulation mechanism in plants

“…An informative work showed that overexpression of the AtNHX1 in tomato induced K + -de iciency symptoms despite transgenic plants having greater K + contents than controls [72]. The intense sequestration of K + in NHX1-overexpressing plants reduced cytosolic K + activity, primed the induction of the highaf inity K + uptake system, and elicited an array of metabolic and hormonal disorders related to K + deprivation [72,118]. Notwithstanding these unintended effects resulting from NHX overexpression, NHX proteins do increase salt tolerance, presumably because retention of cellular K + is a requisite for adaptation to a saline environment [119].…”