The role of K(+) channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana

Abstract

Potassium (K(+)) is inevitable for plant growth and development. It plays a crucial role in the regulation of enzyme activities, in adjusting the electrical membrane potential and the cellular turgor, in regulating cellular homeostasis and in the stabilization of protein synthesis. Uptake of K(+) from the soil and its transport to growing organs is essential for a healthy plant development. Uptake and allocation of K(+) are performed by K(+) channels and transporters belonging to different protein families. In this review we summarize the knowledge on the versatile physiological roles of plant K(+) channels and their behavior under stress conditions in the model plant Arabidopsis thaliana.

Keywords: Arabidopsis thaliana; Kir-like; Shaker; TPK; plant potassium channel; voltage-dependent; voltage-independent.

Figure 1

Structure and function of K⁺ channel families in plants. The two plant K⁺ channel families vary in (A) structure and (B) function. Shaker channels form the most versatile family among plant K⁺ channels. Nine members segregate into inwardly, outwardly and weakly rectifying channels. Functional channels are tetramers and operate in a voltage dependent manner. One subunit consists of six transmembrane domains (S1–S6) and one pore domain (P). The fourth transmembrane region S4 is rich in positively charged amino acids and acts together with S1, S2, and S3 as voltage sensor. Five TPK channels have been identified. One subunit contains two pore domains (P1 and P2) and two subunits are sufficient to form a functional channel. TPKs act in a largely voltage independent manner and exhibit leak like currents. KCO3 was initially classified as a K_ir-like channel showing two transmembrane regions and one pore domain. In fact, “plant K_ir-like channels” originate from TPKs by partial deletion of one selectivity-filter and two transmembrane domains. In line with this notion, only stable dimers have been detected. A K⁺ transport function has not been shown for these truncated channels. Abbreviations: extra, extracellular side; intra, intracellular side; SU, subunit; +, positively charged amino acids; cNBD, cyclic nucleotide binding domain; anky, ankyrin repeat domain; K_(T)/HA, acidic domain; EF, EF hand domain.

Figure 2

K⁺ uptake into Arabidopsis roots and its regulation. Depending on the actual K⁺ concentration in the soil different low or high affinity K⁺ uptake systems are active. At K⁺ concentrations below 0.01 mM only the high affinity transporter AtHAK5 is active. It is blocked by extracellular NH⁺₄ and stimulated by extracellular Na⁺ and H⁺. The Shaker-like K⁺ channel AKT1 is involved in high and low affinity K⁺ uptake. It is a target of an extensive regulatory network that includes calcium sensors (CBLs), kinases (CIPKs), phosphatases (PP2Cs), and the ability to form heterotetramers with AtKC1. In the presence of CBL1 or CBL9, CIPK23 phosphorylates and activates AKT1. The interaction of CIPK 6, 16, and 23 each with CBL1, 2, 3, and 9 and its effect on AKT1 were shown in yeast two-hybrid assays and Xenopus laevis oocytes (Lee et al., 2007). AKT1 is deactivated by a direct interaction with CBL10, external Ba²⁺, or dephosphorylation via PP2C phosphatases. Phosphatases act directly on AKT1 or on the CIPK-CBL machinery to inactivate AKT1 (Lan et al., 2011). Furthermore, AKT1 is able to form heterotetramers with AtKC1. The heteromeric channel exhibits changed gating and permeation properties that block efficiently potential K⁺ release under low external K⁺ concentrations (Geiger et al., 2009). In addition, an interaction of CIPK23 with the heteromeric AKT1-AtKC1 was suggested and the contribution of SYP121 to the native characteristics of AKT1-AtKC1 was described (Honsbein et al., 2009).

Figure 3

K⁺ channels in Arabidopsis guard cells and their effectors. Changes in membrane potential lead to stomatal opening or closure, respectively. Membrane hyperpolarisation in response to H⁺-ATPase activity activates inward-rectifying K⁺ channels. Transcripts for KAT1, KAT2, AKT1, AKT2, and AtKC1 are detectable in guard cells (Szyroki et al., 2001). All these K⁺ channel subunits form heterotetrameric channels like KAT1-KAT2, AKT2-KAT2, and AKT1-AtKC1. The impact of AKT1 and K_in-AtKC1 on stomatal movement has not been investigated in detail. Acidification affects directly the currents through K⁺ channels in guard cells. K_in channels are activated upon extracellular acidification, while currents through K_weak channels decrease. Besides, the K_weak channel AKT2 is negatively affected by extracellular Ca²⁺. KAT1 currents are furthermore modulated by intracellular pH, ATP, and cGMP. ATP and cGMP have antagonistic effects. Moreover, stomatal K⁺ channels are affected by signals via signal transduction cascades. Effects of 14-3-3 proteins, Ca²⁺ and kinases have been reported. Membrane depolarization, on the other hand, caused by the inactivation of H⁺-ATPases and activation of anion channels activates the K_out channel GORK. GORK currents are positively influenced by extra- and intra-cellular alkalinisation. Furthermore, the current enhancing effect of H₂O₂ is under investigation. Both, stomatal opening and closure are affected by phytohormones. While Auxin evokes stomatal opening, ABA inhibits its opening but evokes closure of stomata. Abbreviations: pH_ac, acidification; pH_ba, alkalinisation.