Model of Cation Transportation Mediated by High-Affinity Potassium Transporters (HKTs) in Higher Plants

Abstract

Trk/Ktr/HKT transporters probably were evolved from simple K(+) channels KcsA. HKT transporters, which mediate Na(+)-uniport or Na(+)/K(+)-symport, maintain K(+)/Na(+) homeostasis and increase salinity tolerance, can be classified into three subfamilies in higher plants. In this review, we systematically analyzed the characteristics of amino acids sequences and physiological functions of HKT transporters in higher plant. Furthermore, we depicted the hypothetical models of cations selection and transportation mediated by HKT transporters according to the highly conserved structure for the goal of better understanding the cations transportation processes.

Keywords: Cation transport; HKT transporters; K+/Na+ homeostasis; Na+-uniport; Na+/K+-symport.

Figure 1

K ⁺ /Na ⁺ homeostasis in higher plants. Plant root cells generally absorb Na⁺/K⁺ from soil through different channels (NSCCs, AKT1, LCT1, CCC), transporters (KUP/HAK/KT and HKT) and apoplastic. Channel permeations and apoplastic are the main pathways of Na⁺ influx under salt stress. In the SOS pathway Na⁺ crosses the plasma membrane to the apoplast or soil solution and the NHX1 partitions Na⁺ within vacuole and jointly regulate the cytosol Na⁺ concentrations and play a vital role in response to salt stress. AtHKT1;1, OsHKT1;5, TaHKT1;5 and TmHKT1;4/5 retrieve Na⁺ from the xylem into xylem parenchyma cell and prevent the shoot from damage caused by Na⁺ over-accumulation. It is hypothesized that AtHKT1;1 mediates recycling Na⁺ from the shoot to root through removal of Na⁺ from the xylem and loading Na⁺ into the phloem sieves. These processes assure a normal K⁺/Na⁺ homeostasis and maintain a high K⁺/Na⁺ ratio to rescue plants when suffering from salt stress. NSCC, nonselective cation channels; CCC, cation-Cl − co-transporter; LCT, low-affinity cation transporter; SOS1, salt overly sensitive 1; NHX1, Na⁺/H⁺ antiporter 1.

Figure 2

Phylogenetic analysis of HKT transporters in higher plants. Subfamily I of HKT transporters are all characterized by “Ser” in the first loop (P_A). Subfamily II and III have the GlyGlyGlyGly-type characteristic in the amino acid sequences exception of OsHKT2;1. At, Arabidopsis thaliana; Ts, Thellungiella salsuginea; Pt, Populus trichocarpa; Mc, Mesembryanthemum crystallinum; Vv, Vitis vinifera; Ec, Eucalyptus camaldulensis; Sb, Sorghum bicolor; Ss, Suaeda salsa; Zm, Zea mays; Sab, Salicornia bigelovii; Os, Oryza sativa; Hv, Hordeum vulgare; Bd, Brahypodium distachyom; Tm, Triticum monococcum; Ta, Triticum aestivum; Tt, Triticum timopheevii; Gm, Glycine max; Put, Puccinellia tenuiflora; Pha, Phragmites australis; Sm, Selaginella moellendorffii; Pp, Physcomitrella patens.

Figure 3

Multiple alignment of plant HKTs. The highly conserved signature residues were marked with bold triangle. G: glycine (Gly); S: serine (Ser); C: cysteine (Cys); K: lysine (Lys); R: arginine (Arg).

Figure 4

Structure of AtHKT1;1 transporter. The letters with red font represent the highly conserved amino acid resides which may play crucial functions on cation selection and transport. H, membrane helix; I, inside loop; i, inside helix tail; O, outside loop; o, outside helix tail.

Figure 5

Functions of HKT transporters in higher plants. The transporters of HKT2;1-like, including OsHKT2;1, HvHKT2;1 and TaHKT2;1, mediate Na⁺ uptake from culturing media merely in K⁺-starved environments. HKT transporters, such as AtHKT1;1, OsHKT1;5, TaHKT1;5-D, TmHKT1;4-A2 and TmHKT1;5-A are involved in Na⁺ exclusion from xylem to xylem parenchyma cell in order to minimize the accumulation of Na⁺ in the shoot through the transpiration stream, and this is the key process for salinity tolerance of plants. OsHKT2;4 is a very special member in HKT family, and it is not only conducts as a transporter of Na⁺-K⁺ symport but also mediate Ca²⁺ (maybe other divalent cations) uptake like a cation channel. Cell types depicted include: epidermal cell (EPC), cortical cell (COC), endodermis cell (ENC), pericycle cell (PEC), parenchyma cell (PAC).

Figure 6

Model of cation trapping and selection of plant HKTs. a) Four glycine (G) residues form a trap space and allow Na⁺, K⁺, Mg²⁺ and Ca²⁺ across. Serine (S) and three glycine (G) residues form a trap space and allow Na⁺ across. b) and c) Positive arginine (R) and lysine (K) residues form a cation barrier to stop cation across.

Figure 7

Hypothesis of HKT polymer model. Two highly conserved cysteine (Cys) residues form disulfide bonds to help HKTs to assemble a dimer or tetramer and stabilize the structures. Positive arginine (Arg) and lysine (Lys) residues form a cation barrier to stop cation across. Two/four serine (Ser) or glycine (Gly) residues form a cation trap for plant HKTs specifically selecting cation. a) dimer model and b) tetramer model.