Edited by: Sergey Shabala, University of Tasmania, Australia
Reviewed by: Nava Moran, The Hebrew University of Jerusalem, Israel; Igor Pottosin, Universidad de Colima, Mexico
*Correspondence: Ingo Dreyer, Plant Biophysics, Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, Campus de Montegancedo, Carretera M-40, km 37.7, Pozuelo de Alarcón, Madrid E-28223, Spain e-mail:
Janin Riedelsberger, Molecular Biology, Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24/25, House 20, D-14476 Potsdam, Germany e-mail:
This article was submitted to Frontiers in Plant Physiology, a specialty of Frontiers in Plant Science.
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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
Potassium (K+) is essential for growth and development of an organism. It is involved in various important cellular processes, like stabilization of protein synthesis, activation of enzymes, neutralization of negative charges on proteins and many more. In addition to the above mentioned tasks, in plants it is a key player in osmotic processes contributing to cellular turgor, cell elongation, translocation of photosynthates, maintenance of cytosolic pH homeostasis, and the setting of the membrane potential along with the proton motive force (Maathuis,
Potassium is a major factor in resistance to drought, salinity, and fungal diseases (Amtmann et al.,
The transport of potassium is accomplished by a variety of transporter proteins. In the plant model organism
The three identified families of K+ channels are
In 1992, AKT1 and KAT1, two inward rectifying channels from
In 1997, a first member of the TPK channel family was identified by
The Tandem-Pore K+ (TPK) channel family comprises six members (TPK1-TPK5 and KCO3, see also below for this special case) in the model plant
The first TPK channel (AtTPK1) was cloned via an
Functional TPK channels are built of two of such subunits and exist as dimers (Maitrejean et al.,
Expression analysis of TPKs through quantitative real-time PCR experiments evidenced their presence in different plant tissues like roots, leaves and flowers (Deeken et al.,
Promoter-reporter gene studies and qRT-PCR experiments revealed overlapping expression patterns for members of the TPK/KCO3 channel family (Czempinski et al.,
Dimerization of TPK channels has been shown experimentally by using velocity sucrose gradient centrifugation of leaf homogenates expressing TPK1-GFP. This confirms the contribution of four pore domains to the K+ selectivity filter of the TPK1 channel (Maitrejean et al.,
With the aim of studying the assembly status of TPK/KCO family members, various experiments have been performed employing techniques like FRET and BiFC (split-YFP). Results from these approaches indicated the existence of homomeric TPK/KCO3 channels, as e.g., in the case of TPK1 or TPK5 (Voelker et al.,
In a first approach to detect the subcellular localization, the TPK1 channel has been stably over-expressed in tobacco BY-2 cells. After protein fractionation with a sucrose gradient, this K+ channel was found to co-fractionate with tonoplast markers, giving a first clue of its localization on the vacuolar membrane (Czempinski et al.,
Unfortunately till now, no general targeting sequence is known that “guides” TPK channels to the appropriate membrane (Vitale and Hinz,
Retention of TPK1 channel protein in the ER also occurred when plant leaves were treated with Brefeldin A, a fungal toxin which causes redistribution of Golgi membranes. From this observation it was inferred that the transport of TPK channel proteins to the vacuolar membrane is through a Golgi-dependent pathway and that the Golgi apparatus is the first compartment crossed by the protein after it leaves the ER (Dunkel et al.,
At present the knowledge on function and regulation of plant TPKs is limited. Research is often fuelled by comparison with related channels from other kingdoms. Animal two-pore channel activity has been shown to be regulated by interacting 14-3-3 proteins (Rajan et al.,
TPK channels are proposed to be involved in the K+ homeostasis of plant cells by allowing the controlled intracellular K+ transport from and into organelles. Recent experiments employing the patch clamp technique have demonstrated a mechano-sensitive nature of TPK channels suggesting especially a role in osmoregulation. This concept was further supported by protoplast disruption assays (Maathuis,
AtTPK1 is ubiquitously expressed in
AtTPK4 is an instantaneously activating, K+ selective channel that is also found in the plasma membrane when expressed in
AtTPK5 is targeted to the tonoplast. At the mRNA level,
Recently AtTPK1, AtTPK2, and AtTPK5 were functionally characterized in
Tandem-pore K+ channels have also been identified and characterized in plant species other than
Plant Kir-like channels were initially classified as an own group although they are similar to TPK channels. To date, they have been found only in the genus
The so-called plant
Functional plant
Versatile physiological roles of plant
K+ uptake from soil is performed by a well-organized system of transport proteins each contributing in its own manner (Alemán et al.,
AKT1 and AtHAK5 are affected by different environmental conditions. Both transport proteins work at different K+ concentration spectra and exhibit individual sensitivity toward other ions. For instance, AtHAK5 is sensitive to ammonium (NH+4) whereas AKT1 remains unaffected in the presence of NH+4. On the contrary, Ba2+ blocks AKT1 while AtHAK5 remains unaffected, and Na+ and H+ stimulate activity of AtHAK5 (Hirsch et al.,
AKT1 itself contributes to high and low affinity K+ uptake and is target of a regulatory network. Xu et al. and Li et al. showed in 2006 that CIPK23 and CBL1 or CBL9 are required to activate AKT1. The two calcineurin B-like calcium sensors CBL1 and CBL9 bind to the CBL-interacting protein kinase CIPK23, which then in turn phosphorylates AKT1. All three components (AKT1-CIPK23-CBL1/9) are essential for a functional expression of AKT1 in oocytes of
Shortly after, further components of this highly complex and flexible regulatory network were discovered. Besides several CIP kinases a 2C-type protein phosphatase (PP2C), AIP1, was shown to bind and inactivate AKT1 (Lee et al.,
Many different associations of AKT1 with CBLs, CIPKs, and PP2Cs have been reported. Grefen and Blatt (
Besides the regulation by kinases and phosphatases another member of the
On top of that, the association of CIPK23 with the heteromeric AKT1-AtKC1 channel has been suggested from interaction analyses in yeast (Grefen and Blatt,
Alongside the inward rectifying K+ channel AKT1, the outward rectifying K+ channel GORK is expressed in root epidermal cells (Ivashikina et al.,
K+ is transported from roots to the upper parts of the plant via the xylem. The outward rectifying
In addition to the membrane voltage, SKOR is modulated by the external K+ concentration. In the presence of ample external K+, the channel needs a higher membrane voltage to open and thus minimizes the risk to serve as an undesirable K+-influx pathway. Such behavior is achieved by a complex interplay between the pore region and the last transmembrane domain of the channel that is responsible for final channel opening and closure. When the external K+ concentration is high, the pore region is quite rigid and strongly interacts with the last transmembrane domain of the channel. As a consequence the channel is stabilized in a closed state. Under low external K+ conditions the pore region is less occupied by K+ ions. As a consequence, the pore is more flexible and does not interact with the surrounding transmembrane domains anymore. Opening of the channel is possible with less energy input, i.e., at less positive membrane voltages. If the last transmembrane domains rearrange and unclench the conduction pathway, intracellular K+ ions can re-enter the pore, stabilize it in a permeable conformation and thus enable a K+ outward current (the K+-sensing mechanisms has been animated in the supplementary material of Johansson et al.,
K+ distribution is also influenced by factors that are involved in stress signaling. SKOR expression is inhibited by abscisic acid (ABA). It was proposed that the reduced K+ release to the xylem in response to ABA could be a possibility to adjust osmotic conditions by roots in stress situations (Gaymard et al.,
Hydrogen peroxide (H2O2) exhibits a contrary effect on SKOR currents. Reactive oxygen species function as signal and regulator in plant development and in responses to environmental stress situations (Torres and Dangl,
Once loaded into the xylem, K+ circulates within the whole plant. There, other K+ channels contribute to the further distribution. The
As the only member of the
Summing up, AKT2 can modulate the membrane voltage by switching between its modes of an inward or a non-rectifying channel, respectively, and phosphorylation acts as a tool for fine tuning (Deeken et al.,
In addition to the gating mode modulations, AKT2 was also demonstrated to act on diverse signals involved in stress responses. The expression level of AKT2 increases in the presence of ABA, light and CO2 assimilates (Deeken et al.,
Macroscopic K+currents mediated by AKT2 are modulated by changes in internal and external pH and external Ca2+ (Marten et al.,
Recently, Held et al. (
Two third of the
Although KAT1 represents the dominant Kin channel in guard cells, it is not essential for stomatal opening (Ichida et al.,
For activation of Kin channels the membrane potential needs to be hyperpolarized. Hyperpolarization is achieved through the activity of H+-ATPases that transport protons under ATP consumption out of the cell. The membrane voltage is sensed by the intrinsic voltage sensor that is formed by the transmembrane regions S1–S4. An important role is played especially by the positive charges in S4 (Figure
Another regulator of guard cell Kin currents might be extracellular Ca2+. Here, AKT2 is the only channel affected directly by external Ca2+ (Marten et al.,
Furthermore, effects of regulatory proteins on KAT1 have been shown. For instance, KAT1 is phosphorylated in a Ca2+-dependent manner in the presence of CDPK-a Ca2+-dependent protein kinase with a calmodulin-like domain (Li et al.,
Additionally it was found that the channel population within the membrane undergoes regulation as well (Mikosch et al.,
Kout channels are activated upon depolarization. Such a membrane voltage change is achieved by inhibition of the H+-ATPase and activation of anion channels. GORK is the only Kout channel identified in guard cells and is responsible for stomatal closure (Szyroki et al.,
Alongside the activation of Kout channels during stomatal closure, Kin channels are deactivated (Blatt,
The phytohormones auxin and ABA cause opposing effects on stomata. Auxin is involved in plant developmental processes and promotes stomatal opening, whereas, ABA is involved in various stress responses. It prevents the opening and promotes the closure of stomata (Gehring et al.,
Auxin, on the other hand, stimulates the transcription of
The
K+ channels are important for K+ uptake from the soil, its distribution within the plant and processes to maintain and support plant growth. The past two decades revealed crucial information especially for plant
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
This work was supported by grants from the Spanish Ministerio de Economía y Competitividad (BFU2011-28815), a Marie-Curie Career Integration Grant (FP7-PEOPLE-2011-CIG No. 303674—Regopoc), and by grants of the Deutsche Forschungsgemeinschaft to Ingo Dreyer (DFG grants DR430/8-1 and DR430/9-1). Tripti Sharma and Janin Riedelsberger were recipients of doctoral fellowships from the International Max-Planck Research School “Primary Metabolism and Plant Growth”. The authors are grateful to the reviewers for their helpful comments.
abscisic acid
adenosine triphosphate
calcineurin B-like calcium sensor
Ca2+ dependent protein kinase
cyclic guanosine monophosphate
CBL-interacting protein kinase
endoplasmic reticulum
green fluorescent protein
pore
protein kinase C
2C-type protein phosphatase
soluble N-ethylmaleimide–sensitive factor protein attachment protein receptor
transmembrane
yellow fluorescent protein.
1pS/pT indicate the potential phosphorylation of the serine or threonine residue, respectively.
2In literature, the gene encoded by the locus At4g22200 has been named AKT2, AKT3 and AKT2/3. To avoid confusions, we will summarize the data under the name AKT2 irrespective of the alternative names used in the original publications.