Journal of Plant Physiology 171 (2014) 688–695

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Journal of Plant Physiology

journal homepage: www.elsevier.com/locate/jplph

Physiology

K+ uptake in plant roots. The systems involved, their regulation and

parallels in other organisms夽
Manuel Nieves-Cordones 1 , Fernando Alemán 2 , Vicente Martínez, Francisco Rubio ∗
Departamento de Nutrición Vegetal, CEBAS-CSIC, Campus de Espinardo, Murcia 30100, Spain

a r t i c l e i n f o a b s t r a c t

Article history: Potassium (K+ ) is an essential macronutrient for plants. It is taken into the plant by the transport systems
Received 24 July 2013 present in the plasma membranes of root epidermal and cortical cells. The identity of these systems
Received in revised form and their regulation is beginning to be understood and the systems of K+ transport in the model species
26 September 2013
Arabidopsis thaliana remain far better characterized than in any other plant species. Roots can activate
Accepted 28 September 2013
Available online 3 March 2014
different K+ uptake systems to adapt to their environment, important to a sessile organism that needs
to cope with a highly variable environment. The mechanisms of K+ acquisition in the model species A.
thaliana are the best characterized at the molecular level so far. According to the current model, non-
Keywords:
Channel selective channels are probably the main pathways for K+ uptake at high concentrations (>10 mM), while
Potassium at intermediate concentrations (1 mM), the inward rectifying channel AKT1 dominates K+ uptake. Under
Regulation lower concentrations of external K+ (100 ␮M), AKT1 channels, together with the high-affinity K+ uptake
Transporter system HAK5 contribute to K+ acquisition, and at extremely low concentrations (<10 ␮M) the only system
Uptake capable of taking up K+ is HAK5. Depending on the species the high-affinity system has been named HAK5
or HAK1, but in all cases it fulfills the same functions. The activation of these systems as a function of the
K+ availability is achieved by different mechanisms that include phosphorylation of AKT1 or induction
of HAK5 transcription. Some of the characteristics of the systems for root K+ uptake are shared by other
organisms, whilst others are specific to plants. This indicates that some crucial properties of the ances-
tral of K+ transport systems have been conserved through evolution while others have diverged among
different kingdoms.
© 2013 Elsevier GmbH. All rights reserved.

Introduction
Potassium is an essential macronutrient for plants, composing
up to 10% of the plant dry weight (Leigh and Wyn Jones, 1984). It ful-
fills a number of important functions related to enzyme activation,
as well as the neutralization of negative charges, the maintenance of
cell turgor, plant growth and organ movement (Marschner, 2012;
Abbreviations: APX, ascorbate peroxidase; BiFC, bimolecular fluorescence com-
plementation; CNBD, cyclic nucleotide binding domain; Vm , electrical gradient
across plasma membrane; EAG, ether-a-go-go channels; ELK, EAG-like K+ channels;
HCN, hyperpolarization-activated cyclic nucleotide-modulated channels; KCNH,
voltage-dependent eag-related K+ channels; NSCC, non-selective cation channel;
ROS, reactive oxygen species; SNARE, soluble N-ethylmaleimide-sensitive factor
protein attachment receptor; SOD, superoxide dismutase.
夽 This article is part of a Special Issue entitled “Potassium effect in plants”.
∗ Corresponding author.
E-mail address: frubio@cebas.csic.es (F. Rubio).
1
Present address: Biochimie et Physiologie Moléculaire des Plantes, Institut
de Biologie Intégrative des Plantes, Claude Grignon, UMR 5004 CNRS/UMR 0386
INRA/Montpellier SupAgro/Université Montpellier 2, 34060 Montpellier Cedex 2,
France.
2
Present address: Division of Biological Sciences, University of California San
Diego, La Jolla, California 92093-0116, USA.
see also Anschütz et al., 2014). K+ is taken up by the plant root
through the epidermal and cortical cells and once in the stele, it is
transported to the shoot and distributed to the leaves (for further
details on K+ distribution in plants see also Ahmad and Maathuis,
2014; Wigoda et al., 2014). Most of these processes involve the
movement of K+ through the plasma membrane, mediated by dif-
ferent transport systems embedded in the cell membrane.
The K+ concentration in the cytosol of plant cells is maintained at
around 100 mM, its optimal level for fulfilling metabolic functions
(Britto and Kronzucker, 2008; White and Karley, 2010). In contrast,
the K+ concentrations of the soil solution are highly variable, usu-
ally in the range of 1 to 0.1 mM, although they can sometimes be
even lower (Maathuis, 2009). To a certain extent, plants are able to
adjust to different K+ availabilities, developing adaptive responses
that mainly involve changes in root architecture and activation or
inhibition of K+ transport systems. Agricultural practices attempt to
mitigate the variability in nutrient availability using fertilizers to try
to maintain nutrients at optimal levels and K+ fertilization is a vital
input in agriculture. Even so, intensively cultured land can become
K+ deficient (Dobermann et al., 1998; Pal et al., 2001; Rengel and
Damon, 2008; Yang et al., 2004) through a greater K+ withdrawal
during crop harvest than is supplied, or losses by lixiviation in sandy
soils (Pal et al., 2001; see also Zörb et al., 2014). In addition, certain

0176-1617/$ – see front matter © 2013 Elsevier GmbH. All rights reserved.
http://dx.doi.org/10.1016/j.jplph.2013.09.021
 M. Nieves-Cordones et al. / Journal of Plant Physiology 171 (2014) 688–695
environmental stresses such as salinity impair K+ nutrition caus-
ing deficiency (Alemán et al., 2009b; Botella et al., 1997; Cuin et al.,
2003). Furthermore, demand for K+ fertilization is likely to increase;
in Africa for example, K+ demands will only be met by doubling
the word production of potash fertilizers (Manning, 2010). There
is a need to reduce the costs derived from K+ fertilization, and
this may be achieved by obtaining crop varieties more efficient
in their use of K+ (Rengel and Damon, 2008). Reaching this goal
is likely to only be made possible if we can identify and charac-
terize the systems involved in K+ acquisition in plants (Schroeder
et al., 2013). In this review, the main properties of K+ uptake at the
root level, the molecular systems involved in its transport and their
characteristics in comparison with other organisms are presented.
K+ absorption in the root
Major systems for K+ uptake
More than 60 years ago, Epstein proposed that the systems
involved in ion transport are enzymes and his group analyzed the
kinetics of nutrient uptake in barley roots (Epstein and Hagen,
1952). By applying the concept of enzyme kinetics to the study
of root K+ absorption, they observed a biphasic response to
the increase in external K+ concentration (Epstein et al., 1963).
Their results suggested that at least two transport systems are
involved K+ in uptake: a high-affinity system that operates at
low external concentrations and a low-affinity system at higher
concentrations. This biphasic behavior has since been observed
in many plant species, although some exceptions do occur;
maize for example, shows a linear non-saturating response in the
low-affinity range (Kochian and Lucas, 1982). In the high affin-
ity range of concentrations, K+ uptake is most likely mediated
by a K+ /H+ symporter, whilst the low-affinity uptake appears
to be mediated by inwardly rectifying K+ channels (Maathuis
et al., 1997; Maathuis and Sanders, 1996; Rodríguez-Navarro,
2000).
An increasing number of molecular approaches and tools have
provided researchers with the means of elucidating the molecular
entities involved in root K+ uptake. The initial functional character-
ization was based on the expression of cDNAs that encode putative
K+ transport systems in heterologous organisms such as yeast or
Xenopus oocytes, and also on studies of the expression patterns of
the corresponding genes. These studies pointed toward a mem-
ber of the KT/HAK/KUP family, named HAK1 in some species such
as barley (Santa-María et al., 1997), rice (Bañuelos et al., 2002) or
pepper (Martínez-Cordero et al., 2004), or HAK5 in others such
as Arabidopsis (Rubio et al., 2000) or tomato (Nieves-Cordones
et al., 2007), as a candidate for the high-affinity K+ uptake sys-
tem. For the low-affinity one, an inwardly-rectifying K+ channel
of the Shaker family, AKT1 (Lagarde et al., 1996; Sentenac et al.,
1992), has been postulated. Using Arabidopsis T-DNA insertional
knock-out mutants that disrupt the genes encoding the HAK5 and
the AKT1 K+ transport systems, a clear demonstration for the role
of each of them has been possible (Hirsch et al., 1998; Qi et al.,
2008; Rubio et al., 2008; Spalding et al., 1999). While AtHAK5
seems to be the only system for K+ uptake at external concentra-
tions below 10 ␮M, both AtHAK5 and AKT1 mediate uptake in the
range of 10–200 ␮M. At higher concentrations, AKT1 largely con-
tributes to K+ uptake, with other systems, probably non-selective
cation channels (NSCCs), contributing when the external K+ con-
centration is sufficiently high (Alemán et al., 2011; Caballero et al.,
2012; Rubio et al., 2010; see also Pottosin and Dobrovinskaya,
2014).
These results show clearly that a channel was indeed operat-
ing in the high-affinity range of concentrations, as described by
689
Epstein et al. (1963). These results are surprising, but they can be
clarified when the bioenergetic properties of cell-walled eukary-
otic cells are considered. The soil concentration of K+ is between 0.1
and 1 mM and cytoplasmic K+ is approximately 100 mM (Britto and
Kronzucker, 2008; White and Karley, 2010), so K+ enters the root
cell against its concentration gradient. To be energetically favor-
able, the plasma membrane of plant cells is energized by the activity
of a H+ -ATPase that, by consuming ATP, pumps H+ out of the cell.
Thus, a potential consisting of a H+ gradient (pH) (pHext = 5.5,
pHcyt = 7.3) and an electrical gradient (Vm , negative inside) is cre-
ated. As a cation, K+ can be passively driven into the cell down the
Vm ; a process that can occur via a secondary transport system
such as a uniport, as for example, an inward-rectifying K+ channel,
i.e., AKT1. The membrane potential of a plant cell not only depends
on the action of the H+ -ATPase, but it is also greatly affected by the
depolarizing effect of K+ -uptake through these channels. Thus, the
membrane potential also depends on the external K+ concentra-
tion (Wang and Wu, 2010) and a weak linear relationship between
the membrane potential and the log of [K+ ]ext, over several orders
of magnitude, has been observed (Cheeseman and Hanson, 1979;
Etherton and Higinbotham, 1960; Maathuis and Sanders, 1993).
The limit to which a K+ channel can concentrate K+ in the
cell depends on both the values of the K+ gradient and the Vm
across the plasma membrane. By using multibarreled microelec-
trodes, the cytosolic K+ activity, pH and the membrane potential
of epidermal and cortical root cells have been determined in bar-
ley grown under different K+ supplies; in plants grown at 5 mM K+ ,
the resulting Vm of −83 mV allowed a passive system that was
sufficient for accumulating K+ (Walker et al., 1996). Studies with
other species and differing growth conditions have also reported
Vm values negative enough to allow passive K+ uptake from lower
external K+ concentrations (Caballero et al., 2012; Nieves-Cordones
et al., 2008; Volkov and Amtmann, 2006). Indeed, membrane poten-
tials more negative than −200 mV have been reported in tomato
(Nieves-Cordones et al., 2008) and Arabidopsis (Spalding et al.,
1999) K+ -starved plants. These Vm values would allow passive K+
uptake from an external concentration as low as 30 ␮M K+ : a con-
centration much lower than initially thought (White and Karley,
2010). By using the hak5 and akt1 Arabidopsis knock-out mutant
lines described above, the external K+ concentration that sets the
limit for passive K+ uptake has been accurately established (Coskun
et al., 2013; Pyo et al., 2010; Rubio et al., 2008). Below 100 ␮M K+ ,
the AtHAK5 transporter and the AKT1 channel are the only systems
involved in K+ uptake (Rubio et al., 2010); athak5 plants, with the
AKT1 channel as the only remaining system for K+ uptake, can take
up K+ and grow at K+ concentrations as low as 30 ␮M (Pyo et al.,
2010; Rubio et al., 2008). This is likely due to the highly hyperpo-
larized membrane potentials registered in root cells of these athak5
plants when deprived of K+ (our unpublished results). At external
K+ concentrations lower than 30 ␮M, an active system, probably
a K+ –H+ symporter like the high-affinity HAK5 transporter, needs
to be evoked (Maathuis and Sanders, 1994; Walker et al., 1996).
Under such conditions, the pH needs to be considered along with
the electrical membrane potential, in order to understand how the
high concentrative capacities can be reached by the plant. Indeed,
pepper and tomato plants are capable of depleting K+ at exter-
nal concentrations below 0.1 ␮M (Martínez-Cordero et al., 2004;
Nieves-Cordones et al., 2007); and tomato plants grown in hydro-
ponics under a constant supply of 20 ␮M K+ show similar vegetative
growth parameters than when grown with 1 mM K+ (our unpub-
lished results).
K+ sensing and regulation of K+ transport systems
Sensing of and response to K+ by the plant appears to be
mediated by a number of different means. These include the cell
690 M. Nieves-Cordones et al. / Journal of Plant Physiology 171 (2014) 688–695
Fig. 1. Elements involved in low K+ response of root cells. Low external K+ produces a
plasma membrane hyperpolarization, an increase in ethylene, cytokinin and reactive
oxygen species (ROS) and a Ca2+ signal. The plasma membrane hyperpolarization
is one of the first steps in low K+ sensing and, by unknown mechanisms, leads
to the induction of the HAK5 gene. In addition, low K+ induces on the one hand
an ethylene–cytokinin–ROS cascade that up-regulates HAK5 and on the other, the
CIPK23 gene. The Ca2+ signal is registered by the CBL1-Ca2+ -binding protein that,
by recruiting CIPK23 to the plasma membrane, results in the activation of AKT1 by
phosphorylation. In addition, AKT1 interacts with AtKC1 to form heterotetrameric
channels and AtKC1 with the syntaxin SYP121.
membrane potential, reactive oxygen species (ROS), Ca2+ , hor-
mones such as ethylene, jasmonic acid or cytokinins and direct
sensing of the environmental K+ concentrations by K+ channels
(Fig. 1). Arabidopsis HAK5 and its homologues from other plant
species are transcriptionally up-regulated by K+ starvation (Ahn
et al., 2004; Alemán et al., 2009a; Gierth et al., 2005; Martínez-
Cordero et al., 2004; Nieves-Cordones et al., 2007; Santa-María
et al., 1997; Wang et al., 2002) and repressed after K+ resupply
(Ahn et al., 2004; Armengaud et al., 2004; Gierth et al., 2005;
Nieves-Cordones et al., 2008). One of the first effects of root cells to
K+ deprivation is a hyperpolarization of their membrane poten-
tial (Amtmann et al., 2006), and a correlation between Vm and
the expression of the gene encoding the tomato HAK5 transporter,
LeHAK5, has been shown (Nieves-Cordones et al., 2008). This sug-
gests a role for the membrane potential in the regulation of this
type of genes. In addition, K+ deprived plants rapidly accumulate
ROS (Hernandez et al., 2012; Shin et al., 2005; Shin and Schachtman,
2004; see also Demidchik, 2014), and AtHAK5 expression is thought
to be dependent on ROS production (Fig. 1; Shin and Schachtman,
2004). Epidermal cells in the root tip could be acting as sensors
of the cellular K+ status by a rapid accumulation of ROS at 24 h of
K+ starvation, initiating the signal cascades that lead to the activa-
tion of K+ uptake. After the initial peak in the accumulation of ROS,
the activity of the antioxidative enzyme SOD, peroxidase and APX
is increased (Hernandez et al., 2012) although prolonged K+ star-
vation could result in oxidative damage (Hernandez et al., 2012).
Interestingly, the Arabidopsis class III peroxidase RCI3 (for Rare Cold
Inducible 3), contributes to ROS production during Arabidopsis root
response to K+ deficiency and modulates AtHAK5 expression after
K+ starvation (Kim et al., 2010). ROS production in K+ deprived
plants is blocked by ethylene inhibitors, indicating that this hor-
mone is involved in low K+ signaling upstream ROS. In support of
this idea it has been shown that constitutive ethylene response
mutants such as ctr1-1 show higher ROS and AtHAK5 expression
levels than WT plants under complete nutrient conditions. In addi-
tion, ethylene insensitive mutants such as etr1-1, etr1-3 and ein2-1
accumulate ROS and AtHAK5 mRNA after K+ deprivation to a lesser
extent than the WT. Furthermore, the AtHAK5 promoter is acti-
vated after the addition of ethylene mimicking compounds (Jung
et al., 2009). Other hormones, such as jasmonic acid (Armengaud
et al., 2004, 2010) acid or cytokinins (Nam et al., 2012), have been
suggested to play a prominent role in K+ function as well as sens-
ing other nutrients. Several transcription factors such as RAP2.11
(an AP2/ERF transcription factor; Kim et al., 2012), DDF2 (Dwarf
and Delayed Flowering 2), JLO (Jagged Lateral Organs), TFII A (Tran-
scription initiation Factor II A gamma chain), and bHLH121 (basic
Helix-Loop-Helix 121; Hong et al., 2013), are induced by low K+
and have been shown to bind the promoter region of AtHAK5, being
involved in plant responses to low potassium.
In contrast to HAK5 genes, AKT1 transcription levels are insen-
sitive to external K+ (Lagarde et al., 1996). However, regulation
of the channel activity by phosphorylation and by interaction
with other proteins has been well described: At low K+ concen-
trations (≤1 mM), a Ca2+ signal, recognized by the Ca2+ sensors
CBL9 and CBL1 (Calcineurin B-Like proteins) activates the protein
kinase CIPK23 (CBL-Interacting Protein Kinase). Phosphorylation
of AKT1 by CIPK23 activates the channel, thus increasing AKT1-
mediated K+ uptake (Fig. 1; Cheong et al., 2007; Lee et al., 2007;
Li et al., 2006; Luan et al., 2009; Xu et al., 2006). A protein phos-
phatase 2 C, AIP1, physically interacts and inactivates AKT1 currents
in Xenopus oocytes (Lee et al., 2007). By using the mating-based
split-ubiquitin system in a yeast three hybrid assay, a direct inter-
action between CBL1, CBL9 or CBL4 with AKT1 has been observed
(Grefen and Blatt, 2012). In addition, yeast two-hybrid, BiFC and co-
inmunoprcipitation approaches show a direct interaction of CBL10
with AKT1. Moreover, CBL10 impairs AKT1-mediated currents as
shown in electrophysiological analysis in Xenopus oocytes and
Arabidopsis root cell protoplasts (Ren et al., 2013). Therefore, a reg-
ulation of AKT1 activity by these CBLs in a CIPK23-independent
manner may occur in the plant. At the channel level, AKT1 co-
assembles with the Shaker subunit AtKC1 to form heterotetrameric
channels (Fig. 1; Duby et al., 2008). AtCKC1 is a silent subunit unable
to form functional homomeric channels. The interaction of AtKC1
with AKT1 shifts the activation potential of the AKT1 channel to
more negative values, which reduces K+ uptake at a given mem-
brane potential (Wang et al., 2010). Such negative regulation may
minimize K+ loss at micromolar K+ concentrations (Duby et al.,
2008; Geiger et al., 2009). Additionally, it has been reported that
a ternary interaction of AKT1 and AtKC1 subunits with the vesicle-
trafficking syntaxin SYP121 takes place to control channel gating
and K+ transport (Honsbein et al., 2009). In addition to modulate the
K+ transport properties of AKT1, the interaction with the SYP121
syntaxin might also modulate vesicle trafficking to the plasma
membrane (Grefen et al., 2010).
A cross-talk between several nutrient deficiencies has also
been reported at different levels, suggesting that there is a gen-
eral response from the plant to nutrient deprivation. As with K+ ,
ROS is also a common signal of NO3 − , Pi and SO4 2− depriva-
tion (Schachtman and Shin, 2007; Shin et al., 2005), and both K+
and NO3 − deficiencies induce hyperpolarization of the root cell
membrane potential (Amtmann et al., 2006; Glass et al., 1992).
In Arabidopsis, Pi, N (Shin et al., 2005) and Mn (Wei Yang et al.,
2008) deprivation also increase AtHAK5 mRNA levels, and in tomato
plants, LeHAK5 mRNA levels are increased by Pi and Fe deficien-
cies, in addition to the increase with K+ deprivation (Wang et al.,
2002). Resupplying NO3 − after deprivation down regulates LeHAK5
(Wang et al., 2001). Indeed, K+ and NO3 − signaling pathways share
a common protein kinase, CIPK23, which phosphorylates both the
K+ channel AKT1 and the NO3 − transceptor, CHL1 (Ho et al., 2009;
Xu et al., 2006), and transcriptomic studies have shown that K+
 M. Nieves-Cordones et al. / Journal of Plant Physiology 171 (2014) 688–695
deprivation also induces the expression of genes related to NO3 −
transport and metabolism (Armengaud et al., 2004).
An important abiotic stress that impairs K+ nutrition is salin-
ity. Due to the chemical similarities between K+ and Na+ (see also
Benito et al., 2014), the latter may displace the former from the
K+ -requiring enzymes, including transport systems, so inhibiting
their function. The high amounts of Na+ under salt conditions may
also induce K+ deficiency by other means (Alemán et al., 2009b;
Botella et al., 1997; Cuin et al., 2003). High Na+ concentrations lead
to a strong depolarization of root cells, which could directly affect
low-K+ signaling, suppressing the first steps of low-K+ perception,
so repressing the expression of genes encoding high-affinity K+
transporters, (Alemán et al., 2009a; Nieves-Cordones et al., 2008,
2007, 2010; Volkov and Amtmann, 2006). Furthermore, the strong
membrane depolarization caused by high Na+ makes K+ uptake
thermodynamically more difficult and it also favors K+ efflux via
depolarization-activated outward-rectifying K+ channels (Shabala
et al., 2006). As a result K+ influx is impaired and efflux increased,
resulting in a decrease of plant K+ (see also Demidchik, 2014).
Specific features in plant K+ nutrition in relation to other
organisms
Unlike animals, plants are sessile organisms that remain pos-
itioned within the same habitat throughout their entire life cycle.
Consequently, their ability to cope with changes in K+ availabil-
ity (as well as with all other mineral nutrients and water) will
have a considerable effect on their performance and survival. It
is worth noting that only a small percentage of the total K+ of
the soil exists in a form available for plant uptake; the remain-
der is combined with other elements and organic matter (see also
Zörb et al., 2014). Furthermore, in contrast to other nutrients such
as NO3 − , K+ is relatively immobile in the soil solution, limiting
its availability to a small cylinder of soil surrounding each root
(Marschner, 2012). Plants as well as fungi explore significantly
larger soil areas by extending their roots or hyphae in order to
reach nutrient-rich patches. In addition, they have evolved effi-
cient molecular mechanisms to acquire K+ from the often very low
concentrations found in soils (Maathuis, 2009; Rodríguez-Navarro,
2000). Although fungi are phylogenetically closer to animals, plants
and fungi share many aspects of K+ nutrition. The outstanding con-
centrative capacity of K+ that is exhibited by plants, is also found in
fungi, and in both, is achieved by the establishment of a very neg-
ative plasma membrane potential (more negative than −200 mV
in some cases) driven by the H+ -ATPases, as well as by the pres-
ence of highly K+ -selective transport systems (Fig. 2). In contrast
to plant and fungi cells, most animal cells are surrounded by suf-
ficient K+ concentrations so a steep electrochemical gradient is
unnecessary for absorbing this cation (Heitzmann and Warth, 2008;
Rodríguez-Navarro, 2000). In fact, animal cells show plasma mem-
brane electric potential values around 75 mV (negative inside),
which result from the operation the Na+ -K+ ATPase and K+ chan-
nels. The movement of solutes against their concentration gradient
is mediated by Na+ exchangers, rather than by H+ exchangers as
in plant and fungi cells. Animal and cell-walled eukaryotic cells
are therefore facing very different conditions for K+ absorption
and they show mechanistic differences in this process. However,
they do show some important similarities, which are discussed
below.
The challenge of root cells is to absorb enough K+ , often from
diluted solutions, to keep cytosolic K+ at optimal levels and vac-
uoles filled with sufficient K+ to maintain turgor pressure and
growth (for vacuolar K+ transporters see Hamamoto and Uozumi,
2014; Pottosin and Dobrovinskaya, 2014). The Arabidopsis channels
AKT1/AtKC1 (Geiger et al., 2009; Honsbein et al., 2009; Reintanz
et al., 2002), involved in sustained K+ influx in the root are known
691
as plant Shaker channels due to their sequence homology with
the animal Shaker Kv K+ channels (Sentenac et al., 1992; Sharma
et al., 2013; Véry and Sentenac, 2003). These plant channels, as with
the animal counterparts, are tetrameric structures whose subunits
are often encoded by different genes (Lebaudy et al., 2008). Each
plant Shaker subunit possesses 6 transmembrane domains (6TM
structure) with a voltage sensor (segment 4), a pore loop between
segments 5 and 6 and cytosolic N- and C-termini (Lebaudy et al.,
2007). These features are shared by animal Shaker Kv subunits and
also by the members of the other big group of animal voltage-
dependent 6TM K+ channels, the KCNH superfamily (HCN, EAG,
ELK channels; Pilot et al., 2003). Indeed, the plant Shaker subunit
structure is closer to that of the KCNH superfamily, rather than that
of Shaker Kv subunits, with both types of channels having a short
N-terminus and a long C-terminus where a cyclic-nucleotide bind-
ing domain is located (Pilot et al., 2003). It is worth noting that K+
inward-rectification, as exhibited by many plant Shaker channels,
is only carried out in animal cells by the HCN channels (Craven and
Zagotta, 2006). Nonetheless, despite the subunit structure similar-
ity between plant Shaker and KCNH channels, plant counterparts
exhibit the canonical amino acid sequence GYGD of the K+ selec-
tivity filter and discriminate extremely well K+ over Na+ . The basis
for this discrimination relies on the precise spatial arrangement
of these four residues that allows the efficient coordination of K+
ions over others such as Na+ (Doyle et al., 1998; see also Benito
et al.), making plant Shaker channels highly selective for K+ . In con-
trast, the members of the KCNH superfamily lack the last residue
of such a motif and so poorly discriminate K+ over Na+ . Conversely,
the GYGD sequence located in the selectivity filter is common to
Shaker Kv channels (Long et al., 2005), denoting high selectivity for
K+ .
Most Arabidopsis Shaker subunits are able to form homote-
trameric channels at the plasma membrane of heterologous
systems, giving rise to functional K+ channels (Lebaudy et al., 2007).
However this is not the case of AtKC1, which does not produce any
K+ conductance in heterologous systems such as Xenopus oocytes,
yeast or tobacco protoplast; it is thus considered to be a silent sub-
unit (Dreyer et al., 1997; Wang et al., 2010; Duby et al., 2008). This
silent behavior seems to be due to its retention in the endoplasmic
reticulum as observed in tobacco protoplasts. After co-expression
with other Shaker subunits, such as AKT1, AtKC1 assemblies into
heterotetrameric channels that traffic to the plasma membrane and
mediate K+ currents (Duby et al., 2008; Jeanguenin et al., 2011).
The mechanisms by which this silent subunit fails to form func-
tional channels but is able to co-assemble with other subunits
may depend on interactions of its C-terminus, as described for the
carrot homologue, KDC1 (Naso et al., 2009). Interestingly, this con-
ditional targeting to the plasma membrane is also observed in some
Shaker Kv subunits (subfamilies Kv6, Kv8 and Kv11; Bocksteins and
Snyders, 2012; Ottschytsch et al., 2005).
Regulation of the plant Shaker channels also has plant-specific
characteristics. As described above, in Arabidopsis, AKT1 is phos-
phorylated by the Ca2+ -dependent CIPK23–CBL1/9 complexes,
which firmly control its transport capacity (Li et al., 2006; Xu
et al., 2006). Regulation by CIPK–CBLs complexes, which have
been found in all plant genomes sequenced so far, is exclu-
sive to plants. Although they do represent a variation of the
calmodulin–calcineurin system present in fungi and animals (Luan
et al., 2009), the plant and the animal systems operate differ-
ently. Thus, CBLs are homologous to the B subunit of calcineurin
and both are Ca2+ sensors. But whereas CBLs’ target is a kinase
(CIPKs), the target of calcineurin B is a phosphatase (the A subunit of
Calcineurin; Luan, 2009). CIPKs are most similar to the Sucrose Non-
Fermenting (SNF) protein kinases in yeast and AMP-dependent
kinases (AMPKs) in animals in the kinase domain but they retain
their unique C-terminal regulatory domains (Luan, 2009; Luan
692 M. Nieves-Cordones et al. / Journal of Plant Physiology 171 (2014) 688–695

Fig. 2. Strategies for efficient K+ uptake in model plant and fungal cells. (A) In plants, root cells exhibit a membrane potential (Vm ) that ranges from −60 mV to −200 mV
and is energized by an H+ -ATPase. This electrical component is used to drive K+ through channels and transporters against its concentration gradient. In Arabidopsis root
cells, K+ influx is mediated by non-selective channels, inward-rectifying K+ channels and K+ transporters. It is not clear which proteins form these non-selective channels, but
cyclic-nucleotide gated channels (CNGC) may be good candidates, although other entities may be involved. Inward-rectifying K+ -selective channels are tetrameric structures
that contain AKT1 and AtKC1 Shaker subunits. AKT1 subunits are activated by phosphorylation by the CIPK23–CBL1 complex. In addition, the syntaxin SYP121 also enhances
K+ transport through this channel by interacting with AtKC1 subunits. The K+ transporter HAK5 is likely to mediate active K+ uptake by a H+ :K+ symport. (B) In the fungal
model, Neurospora crassa, a significant Vm , similar to that of plant cells, is developed by the operation of the H+ -ATPase, allowing TRK and HAK proteins to take up K+ from
the external solution. Similarly to plants, fungal HAK transporters are induced under K+ -limiting conditions to complement, in this case, TRK passive K+ transport.

et al., 2002). As described in the previous section, K+ uptake through
AKT1/AtKC1 heterotetramers is also dependent on the interaction
of the syntaxin 121 (SYP121) with the AtKC1 subunit. This interac-
tion leads to increased K+ uptake through the channels (Honsbein
et al., 2009). The regulation of K+ conductance by a syntaxin-K+
channel interaction has been previously described in animal cells
(Leung et al., 2007; Sun et al., 2005). However, this SYP121-AtKC1
interaction does not depend on the SYP121 H3 domain, which is
a coiled-coil region that binds with its cognate SNARE partners or
membrane-spanning ␣-helices, as is the case of animal syntaxins,
but on a motif isolated at the cytosolic N terminus of SYP121 which
seems to be unique to plants (Grefen et al., 2010).
In addition to Ca2+ , cyclic nucleotides (cAMP or cGMP) act as
key second messengers in animal and fungal cells (Berdeaux and
Stewart, 2012; McDonough and Rodriguez, 2012). Besides other
roles in animal cells, these signaling molecules strongly modu-
late ion transport mediated by HCN channels by binding the CNBD
(cyclic nucleotide binding domain) present in their cytosolic C-
terminus (Craven and Zagotta, 2006; Zagotta et al., 2003). In plants,
the role of cyclic nucleotides has been a matter of debate (Newton
and Smith, 2004), but it has been found that they participate as
second messengers that control different processes, including ion
transport (Caballero et al., 2012; Isner et al., 2012; Maathuis and
Sanders, 2001; Maathuis, 2006). Plant Shaker K+ channels, such
as AKT1 and AtKC1, also possess a CNBD within their cytosolic C-
terminus. However, cyclic nucleotides have shown to have little
effect on the K+ currents mediated by these channels (Gaymard
et al., 1996; Hoshi, 1995) and they also lack the key binding
residues in their CNBDs (Zagotta et al., 2003). Therefore, plant
Shaker channels seem not to mediate the aforementioned cyclic
nucleotide-regulated ion transport. Other transport systems, yet
unidentified, may be involved in the ion transport regulated by
cyclic nucleotides in plants.
As described above for Arabidopsis, the transporter AtHAK5 is
the only system that mediates uptake K+ in the root to support
plant growth, at very low K+ concentrations (<10 ␮M; Alemán
et al., 2011). HAK homologues are also found in other kingdoms.
For instance, genes encoding HAK/Kup/KT transporters have been
identified in several species of Bacteria, Archaea, Fungi and Amoe-
bozoa and all sequenced plant genomes contain genes coding
for these transporters (Gomez-Porras et al., 2012). In addition to
the homology in sequence, fungal counterparts also participate in
high affinity K+ uptake at the plasma membrane like AtHAK5 and
homologous transporters of other plant species such as the bar-
ley HvHAK1 (Santa-María et al., 1997), the rice OsHAK1 (Bañuelos
et al., 2002), the pepper CaHAK1 (Martínez-Cordero et al., 2004)
or the tomato LeHAK5 (Nieves-Cordones et al., 2007), all belonging
to the phylogenetic group I. This highlights the key contribution
of these transporters toward allowing plants and fungi to sur-
vive in K+ -depleted environments probably due to their, as yet
undemonstrated, ability to mediate active K+ transport into the
cell. This similarity in sequence and function shared between plant
and fungal HAK transporters contrasts with the difference between
plant and fungal Shaker K+ channels. Inward-rectifying Shaker K+
channels are yet to be described in fungi, implying an important dif-
ference in the adaptations of the K+ transport machinery between
these two kingdoms. It appears that fungal Trk transporters, which
belong to the Trk/Ktr/HKT family, mediate K+ uptake at the plasma
membrane in a manner expected of inward-rectifying K+ chan-
nels (Fig. 2; Cabrera et al., 2012; Corratgé-Faillie et al., 2010; Haro
et al., 1999; Rivetta et al., 2013). Interestingly, the basic struc-
ture of the prokaryotic KcsA K+ channel is repeated four times in
 M. Nieves-Cordones et al. / Journal of Plant Physiology 171 (2014) 688–695 693

Fig. 3. Relative contribution of channels and transporters to K+ uptake in Arabidopsis roots as a function of the K+ regime. When the external K+ concentration is high, at a level
of 5 mM for example, the H+ -ATPase sets Vm to values around −90 mV, which is more negative than the K+ diffusion potential (EK = −76 mV). This allows the passive uptake
of K+ through channels. Experimental data point to a major role for non-selective channels at high K+ concentrations over inward-rectifying K+ -selective channels labeled
as the AKT1 complex to denote all the structural (AKT1 and AtKC1) and regulatory (CBL1, CIPK23 and SYP121) proteins (see Figs. 1 and 2). At intermediate K+ concentrations
(1 mM), the membrane potential is still more negative than EK but, to ensure sufficient K+ uptake over other ions, K+ uptake through the AKT1 complex is activated. This
activation occurs because of the more negative Vm values and via the phosphorylation of AKT1 by the CIPK23–CBL1 complex. When the K+ supply is reduced to 0.1 mM
the Vm becomes closer to EK and K+ influx through the AKT1 complex decreases. The H+ :K+ symport activity of HAK5, is up-regulated under a low K+ supply, allowing K+
uptake. When the external K+ concentrations are below 0.01 mM, K+ passive uptake is not possible even though the cell is hyperpolarized, and HAK5-mediated K+ uptake
then becomes the only pathway for K+ entry into the root.

fungal Trk (Durell and Guy, 1999) and plant HKT transporters (Kato
et al., 2001; see also Benito et al., 2014), suggesting that there is a
structural and functional link between fungal Trk transporters and
ancestral K+ channels (Corratgé-Faillie et al., 2010).
With regard to the regulation of AtHAK5, proteins interacting
with this transporter or its plant or fungal homologues involved
in high-affinity K+ uptake are yet to be identified. Recently, new
insights into the regulation of HpHAK1 at the protein level have
been gained in the yeast Hansenula polymorpha (Cabrera et al.,
2012), revealing that HpHAK1 up-regulation by K+ starvation is
dependent on a calcineurin-dependent response.
In conclusion, recent research has provided us with a clearer
picture of how plants, especially Arabidopsis, adapt to main-
tain K+ uptake under different conditions (Fig. 3), but there
are still many issues to be addressed in the forthcoming years.
These include the regulation and the mechanism of transport of
HAK proteins and the translatability of the Arabidopsis model to
other crop species (in this context see Véry et al., 2014). Such
work would enable us to increase K+ use efficiency and improve
plant production according to the economic and climatic sta-
tus.
Acknowledgements
We thank Judit Nieto for her assistance with English. This work
was funded by Grant number AGL2012-33504 from Ministerio de
Economía y Competitividad, Spain.
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