Regulation of K+ Nutrition in Plants

Abstract

Modern agriculture relies on mineral fertilization. Unlike other major macronutrients, potassium (K⁺) is not incorporated into organic matter but remains as soluble ion in the cell sap contributing up to 10% of the dry organic matter. Consequently, K⁺ constitutes a chief osmoticum to drive cellular expansion and organ movements, such as stomata aperture. Moreover, K⁺ transport is critical for the control of cytoplasmic and luminal pH in endosomes, regulation of membrane potential, and enzyme activity. Not surprisingly, plants have evolved a large ensemble of K⁺ transporters with defined functions in nutrient uptake by roots, storage in vacuoles, and ion translocation between tissues and organs. This review describes critical transport proteins governing K⁺ nutrition, their regulation, and coordinated activity, and summarizes our current understanding of signaling pathways activated by K⁺ starvation.

Keywords: long-distance transport; nitrate; plant nutrition; potassium; regulation.

Figure 1

Transporters involved in K⁺ uptake by roots and inter-organ partition. HAK5, AKT1, and non-selective cyclic nucleotide-gated cation channels (CNGC) all contribute to K⁺ nutrition, albeit at different ranges of substrate concentrations, from low- to high-availability, respectively. K⁺ efflux through the outward-rectifying GORK channel facilitates the fine-tuning of plasma membrane electrical potential, and allows repolarization under circumstances that promote depolarization, such as salinity stress. In the root stele, the outward-rectifying SKOR channel releases K⁺ into the xylem vessels for nutrient delivery to the shoots. The nitrate transporter NRT1.5 facilitates K⁺ uploading into the xylem either by electrical coupling with other K⁺-selective transporters or directly acting as K⁺/H⁺ antiporter. In aerial tissues, an array of K⁺-influx channels and KT/HAK/KUP carriers allow the uptake of the incoming K⁺ into green cells. K⁺ is stored inside vacuoles by NHX exchangers and released back to the cytosol by TPK and TPC1 channels, and possibly also by KT/HAK/KUP carriers at the tonoplast (the vacuole in root cells is omitted for simplicity). The plasma membrane outward K⁺ channel AKT2 releases K⁺ into the phloem for returning K⁺ to the root and to facilitate the uploading of photosynthates into the phloem sap.

Figure 2

Topological models of the main ion transporters involved in K⁺ nutrition. (A) Voltage-gated K⁺ channels contain six transmembrane domains (S1–S6); S4 is the voltage-sensor characterized by the array of positively charged amino acids (+). The long C-terminal tail contains several conserved domains: C-linker, a cyclic nucleotide binding homologous domain (CNBHD), an ankyrin domain (ANK), and a final region rich in hydrophobic and acidic residues (KHA). (B) HKT transporters have a channel-like structure that contains four identical subunits (a–d), each comprising two transmembrane helices (M1 and M2) connected by the P-loop involved in ion selectivity. (C) KT/HAK/KUP transporters have 12 putative transmembrane domains (TMs). TM1-5 and TM6-10 are predicted to fold in the same conformation but showing inverse symmetry.

Figure 3

Regulatory circuitry regulating AtHAK5 expression and activity. K⁺ starvation is probably sensed as hyperpolarization of the plasma membrane, which, together with elevated ethylene and ROS levels, leads to expression of the HAK5 gene. Several transcriptional activator and repressor factors have been identified, but their placement in specific signaling pathways is uncertain. Subsequently, calmodulin-like (CML) and calcineurin B-like (CBL) Ca²⁺-binding proteins recruit and activate protein kinases ILK1 and CIPK23 that facilitate the trafficking of HAK5 to the plasma membrane and its biochemical activation, respectively. CIPK23 also stimulates the K⁺-uptake channel AKT1. K⁺ replenishment depolarizes the membrane and returns the system to homeostatic levels.

Figure 4

Concerted regulation of nitrate, ammonium, and potassium transport. Top, under nutrient sufficiency, the nitrate transporter NRT1.1 operates in the low-affinity mode, AMTs transport any NH₄ ⁺ present in the soil solution as the preferred N source, and AKT1 ensures K⁺ influx down its electrochemical gradient. Bottom, upon nutrient scarcity, the N-myristoylated and Ca²⁺-bound CBL1/9 recruit to the plasma membrane and activate the protein kinase CIPK23 that in turn phosphorylates and activates the high-affinity mode of transport of NRT1.1 and HAK5, and stimulates K⁺ influx through AKT1. CIPK23 is also able to inhibit AMTs when the NH₄ ⁺ is at toxic levels.