Root K+ Acquisition in Plants: The Arabidopsis thaliana

Model

Mini Review
Fernando Aleman, Manuel Nieves-Cordones, Vicente Martnez and Francisco Rubio*
Centro de Edafologa y Biologa Aplicada del Segura-CSIC, Campus de Espinardo, 30100 Murcia, Spain
*Corresponding author: E-mail, frubio@cebas.csic.es; Fax, +34-968-396213
(Received May 31, 2011; Accepted July 12, 2011)

K+ is an essential macronutrient required by plants to com-
plete their life cycle. It fulfills important functions and it is
widely used as a fertilizer to increase crop production. Thus,
the identification of the systems involved in K+ acquisition
by plants has always been a research goal as it may eventu-
ally produce molecular tools to enhance crop productivity
further. This review is focused on the recent findings on the
systems involved in K+ acquisition. From Epsteins pioneer-
expansion is over, less mobile osmotica such as sugars, organic
acids and compatible solutes are accumulated (Amtmann et al.
2006).
K+ is also important for enzyme activation, movements,
charge neutralization, transcription and post-translational
modification (Maathuis 2009), having a great impact on cell
metabolism (Amtmann and Armengaud 2009). It also plays
an important role in transport of solutes through the

Downloaded from http://pcp.oxfordjournals.org/ by guest on October 2, 2013

ing work >40 years ago, K+ uptake was considered to consist
of a high- and a low-affinity component. The subsequent
molecular approaches identified genes encoding K+ trans-
port systems which could be involved in the first step of K+
uptake at the plant root. Insights into the regulation of
these genes and the proteins that they encode have also
been gained in recent studies. A demonstration of the role
of the two main K+ uptake systems at the root, AtHKA5 and
AKT1, has been possible with the study of Arabidopsis thali-
ana T-DNA insertion lines that knock out these genes.
AtHAK5 was revealed as the only uptake system at external
concentrations <10 mM. Between 10 and 200 mM both
AtHAK5 and AKT1 contribute to K+ acquisition. At external
concentrations >500 mM, AtHAK5 is not relevant and
AKT1s contribution to K+ uptake becomes more important.
At 10 mM K+, unidentified systems may provide sufficient
K+ uptake for plant growth.
Keywords: Arabidopsis  Nutrition  Potassium  Salinity 
Uptake.
Abbreviations: CNGC, cyclic nucleotide-gated channel; JA,
jasmonic acid; ROS, reactive oxygen species
Introduction
Potassium is an essential macronutrient for plants, and is
involved in many and important physiological processes.
Growth is one of the processes where K+ has one of the most
important roles. Rapid cell expansion relies on the high mobility
of K+, which acts as an osmoticum, to drive growth, a role that
can be substituted by a few other inorganic ions. When cell
phloem. For example, it is required for sucrose movement
from shoot to root and to the sink tissues such as fruits
(White and Karley 2010). Increasing K+ increases photosynthe-
sis, and more effective translocation of photoassimilates and
amino N compounds into reproductive organs via phloem.
On the other hand, K+ deficiency leads to a decline in photo-
synthesis due to sucrose accumulation in leaves (Mengel et al.
2001, Deeken et al. 2002, Hermans et al. 2006, White and Karley
2010). Therefore, K+ has a great impact on fruit quality
(Romheld and Kirkby 2010) and consequently on crop prod-
uctivity. It also plays a role in stress signaling (Romheld and
Kirkby 2010, Wang and Wu 2010), as K+ deficiency induces
reactive oxygen species (ROS) and jasmonic acid (JA), involved
in tolerance to diseases and pests, as well as ethylene and auxin
production. Therefore, optimization of K+ nutritional status is
important to reduce the negative effects of stress conditions,
not only abiotic but also biotic stresses (Amtmann et al. 2008,
Troufflard et al. 2010).
Global K+ consumption has increased 4.4% per year from
1999 to 2005 and it was predicted to have increased by 12% in
the last decade. Although there are K+ reserves for thousands
of years of agriculture, profitable production, especially in
marginal lands, relies on the increase in the efficient use of
K+ and other nutrients.
It is generally accepted that the typical K+ concentration in
soils varies between 0.1 and 1 mM (Maathuis 2009). However,
large areas of cultivated land are K+ deficient (Rengel and
Damon 2008, Romheld and Kirkby 2010). In addition, inad-
equate nutrient recycling leads to nutrient deficiency, especially
of K+ because nitrogen and phosphorus are added as fertilizers
to the same level as they are removed by crops, but the same is

Plant Cell Physiol. 52(9): 16031612 (2011) doi:10.1093/pcp/pcr096, available online at www.pcp.oxfordjournals.org
! The Author 2011. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
All rights reserved. For permissions, please email: journals.permissions@oup.com

Plant Cell Physiol. 52(9): 16031612 (2011) doi:10.1093/pcp/pcr096 ! The Author 2011. 1603
 F. Aleman et al.
not true for K+. Nutrient deficiencies appear worldwide, and in
developing countries fertilizers may not be affordable. In
developed countries, the increase in the cost of fertilizers and
the need to reduce environmental damage because of abusive
fertilizer inputs lead to the use of more efficient cultivars and
genotypes for sustainable, low-input agriculture. In addition,
developed countries pay a lot of attention to the use of crop
residues as biofuels instead of recycling them to the soil
(Romheld and Kirkby 2010).
Environmental conditions have an important effect on K+
nutrition. Abiotic stresses, that will be exacerbated in the future
due to global warming, negatively affect K+ nutrition (Romheld
and Kirkby 2010, Nieves-Cordones et al. 2011). Among these
stresses, salt stress is one of the most important. Salt stress is
composed of two main effects: the osmotic and the ionic effect.
The latter involves toxicity because of high concentrations of
Cl and Na+. Most importantly, Na+ has been shown to induce
K+ deficiency (Botella et al. 1997, Kronzucker et al. 2008,
Aleman et al. 2009a) and an increase in K+ in the soil can be
used to ameliorate Na+ toxicity (J. S. Rubio et al. 2010).
Therefore, to increase crop salt tolerance, it is important not
only to reduce Na+ accumulation within plant tissues, but also
to increase the K+/Na+ ratio (Shabala and Cuin 2008, J. S. Rubio
et al. 2010). This increase in the ratio coupled to a high K+
nutritional status is beneficial for plant growth under salinity.
This review is focused on the recent findings on the molecu-
lar entities involved in K+ acquisition at the plant root with
special emphasis on the model plant Arabidopsis thaliana. Since
the identification of the first two plant K+ uptake systems in
1992 (Anderson et al. 1992, Sentenac et al. 1992) a large
number of plant genes for K+ transport have been identified
(Maser et al. 2001, Ward et al. 2009). A clear demonstration of
the physiological role of two of them, HAK5 (or HAK1, for other
species) and AKT1, in root K+ uptake has only been possible
with studies performed in the model plant Arabidopsis, which
are described in the following sections.
Root K+ absorption
Potassium acquisition from the soil solution takes place
through epidermal and cortical cells of the roots. The lipid
bilayer of cell membranes is not permeable to ions, water and
most of the polar molecules, and K+ enters the root symplast
through K+-specific transport proteins located in the
membrane.
The kinetics of root K+ uptake were described >40 years ago
in barley (Epstein et al. 1963). K+ uptake exhibited biphasic
kinetics in response to increasing external K+ concentrations
with a high- and a low-affinity component. Considering
energetic limitations, it has been traditionally proposed that
high-affinity K+ uptake is an active process mediated by
H+/K+ symporters, and low-affinity, passive uptake is mediated
by channels (Maathuis and Sanders 1996, Rodrguez-Navarro
2000).
1604 Plant Cell Physiol. 52(9): 16031612 (2011) doi:10.1093/pcp/pcr096 ! The Author 2011.
Identification of root K+ uptake systems
The identification of the molecular entities that mediate K+
uptake began with the functional expression of plant cDNAs
in heterologous systems such as yeast, Xenopus laevis oocytes or
insect cells (Sentenac et al. 1992, Schachtman and Schroeder
1994, Santa-Mara et al. 1997, Zimmermann et al. 1998).
The contribution of each of these transport systems to root
K+ uptake was established from indirect evidence. The
expression pattern of their encoding genes, their tissue and
intracellular localization and their K+ transport properties in
heterologous systems, together with the data on cytoplasmic
K+ concentrations and membrane potentials of epidermal and
cortical root cells, allowed a general model for their function to
be depicted. According to this model, low-affinity K+ uptake
could be mediated by inward-rectifier Shaker K+ channels such
as the Arabidopsis AKT1, whose gene is expressed mainly in
root epidermal cells (Lagarde et al. 1996). These types of
channels mediate sustained K+ uptake compatible with
low-affinity K+ uptake and are sufficient to promote plant
growth (Schroeder et al. 1994). High-affinity K+ uptake could
be mediated by transporters of the TRK-HKT family such as the
wheat TaHKT1 (Schachtman and Schroeder 1994) or the
KT/HAK/KUP family such as the barley HvHAK1
(Santa-Mara et al. 1997). The physiological relevance of
TRK-HKT transporters for high-affinity root K+ uptake is not
yet clear. Some HKT transporters, such as TaHKT1, mediate
high-affinity Na+-coupled K+-uptake (Rubio et al. 1995) and
are expressed in the root (Schachtman and Schroeder 1994),
but such a transport mechanism has not yet been demon-
strated in higher plants (Maathuis et al. 1996). In contrast,
high-affinity Na+ uptake may occur in most plant land
plants, and it is probably mediated by HKT transporters in
rice and species in the Triticeae and Aveneae tribes of the
Poaceae family (Haro et al. 2010). The only HKT transporter
of Arabidopsis, AtHKT1 (Uozumi et al. 2000), is related to both
the control of Na+ accumulation in the root and retrieval of
Na+ from the xylem (Sunarpi et al. 2005, Davenport et al.
2007). On the other hand, HAK1-type transporters of the
KT/HAK/KUP family show high affinity for K+, low discrimin-
ation between K+ and Rb+, inhibition by NH+4 , and they are
encoded by genes that are induced in roots upon K+ starvation
(Rodrguez-Navarro and Rubio 2006). All these characteristics
are in agreement with the high-affinity K+ uptake observed in
plant roots (Epstein et al. 1963, Glass and Dunlop 1978), which
strongly suggests that HAK1-type transporters are major
contributors to high-affinity K+ uptake. Their transport mech-
anism has not been fully demonstrated yet, but it is probably
the same as the predicted K+H+ symporter mediating
high-affinity K+ uptake, as has been shown for the homologous
NcHAK1 of Neurospora crassa (Rodriguez-Navarro et al. 1986,
Haro et al. 1999). Importantly, high-affinity K+ uptake coupled
to H+ has been described in Arabidopsis root protoplasts
(Maathuis and Sanders 1994a) and in barley roots (Walker
et al. 1996).
 Systems involved in K+ uptake in Arabidopsis

Transcriptional regulation of root K+
transport systems
The expression of AKT1 does not respond to the external
supply of K+ (Lagarde et al. 1996, Pilot et al. 2003). However,
K+ withdrawal from the growth solution increased the expres-
sion of the homologous TaAKT1 from wheat (Buschmann et al.
2000). Interestingly, NaCl treatment reduced AKT1 expression
in a long-term study (Kaddour et al. 2009), while others
reported no change with shorter NaCl treatments (Maathuis
et al. 2003, Pilot et al. 2003). In addition, changes in AKT1
expression when plants are treated with hormones have been
described (Pilot et al. 2003). Exposure to the cytokinin
benzyladenine and to the synthetic auxin 2,4 D decreased the
expression levels of AKT1 and its regulatory subunit AtKC1.
However, the study showed that the AKT1 transcript was the
least sensitive to the tested hormones, and SKOR, which is
identified as an outward-rectifying K+ channel in Arabidopsis,
was the most sensitive among the Shaker channels studied,
suggesting that the transcriptional modulation of AKT1 is not
important for its regulation.
In contrast to AKT1, the changes in expression of HAK1-type
genes by the external supply of K+ constitute an important
part of their regulation. K+ starvation greatly increases
the mRNA levels of HAK1-type genes (Santa-Mara et al.
1997, Wang et al. 2002, Ahn et al. 2004, Armengaud et al.
2004, Martnez-Cordero et al. 2004, Gierth et al. 2005,
Nieves-Cordones et al. 2007, Aleman et al. 2009b) and K+
resupply rapidly reduces the amount of their mRNA
(Ahn et al. 2004, Armengaud et al. 2004, Nieves-Cordones
et al. 2008). Because of the distinct response of the HAK1-
type genes to K+, they have been suggested to be useful tools
for the study of K+ sensing at the root level (Amtmann et al.
2006).
Many studies have further deepened our knowledge of the
regulation of HAK1-type genes, showing a much more complex
regulation than expected (Fig. 1). Apoplastic K+ concentration
and membrane potential have been proposed to be the first
steps in the signaling pathway for acclimation to low K+
(Amtmann et al. 2006). This is because external K+ concentra-
tions have a relatively small influence on cytoplasmic K+
concentrations, which are efficiently buffered by vacuolar K+
through accumulation or release processes through the
tonoplast (Walker et al. 1996, Walker et al. 1998).
Furthermore, one of the first measured events induced by K+
deficiency is the hyperpolarization of root cell membrane
potential, which appears within just a few minutes after the
decrease in external K+ (Maathuis and Sanders 1993, Wang and
Wu 2010). Recently, an important role for the membrane
potential has been suggested for the regulation of HAK1-type
genes. In tomato plants, LeHAK5 expression levels in root cells
correlated with their steady-state plasma membrane potentials
but not with their cytoplasmic K+ concentrations nor with the
K+ concentrations of the external solution (Nieves-Cordones
et al. 2008). The recorded plasma membrane potentials and
LeHAK5 expression were importantly affected by long-term
changes in the composition of the growth solution. For
instance, the presence of NH+4 or K+ starvation, which

Fig. 1 Low K+ sensing in plant cells. Low K+ induces a plasma membrane hyperpolarization that may constitute one of the first steps in low K+
sensing. The hyperpolarized plasma membrane activates AtHAK5 expression. In addition, low K+ triggers an ethyleneROS signal that leads to
AtHAK5 induction. Low K+ also triggers a Ca2+ signal, probably through the activation of plasma membrane and endomembrane Ca2+ channels,
that leads to activation of AKT1 through the CBL1CIPK23 complex. AKT1 function is activated by CIPK23-mediated phosphorylation and
inactivated by AIP1-mediated dephosphorylation. AKT1 activity is also regulated by interaction with the AtKC1 subunit and the syntaxin SYP121.

Plant Cell Physiol. 52(9): 16031612 (2011) doi:10.1093/pcp/pcr096 ! The Author 2011. 1605
 F. Aleman et al.
hyperpolarized the membrane potential, increased LeHAK5
mRNA levels. The presence of Na+ in K+-starved plants
depolarized the plasma membrane potential and repressed
LeHAK5. In addition, short-term exposure of K+-starved roots
to depolarizing agents such as CCCP or vanadate decreased
LeHAK5 expression. Further results support the idea that
the membrane potential may be regulating the expression of
HAK1-type genes. Arabidopsis akt1 knock-out lines show
hyperpolarization of root cells (Spalding et al. 1999) and
AtHAK5 up-regulation (Qi et al. 2008, Rubio et al. 2008).
NO3 deprivation has been shown to hyperpolarize root mem-
brane potentials (Meharg and Blatt 1995) and to produce
an increase in AtHAK5 mRNA levels (Shin et al. 2005).
Moreover, NO3 addition to NO3 -deprived plants depolarizes
the root membrane potential (Glass et al. 1992, Meharg and
Blatt 1995) and represses LeHAK5 expression (Wang et al.
2001). Furthermore, Pi (Shin et al. 2005) or Mn (Wei
Yang et al. 2008) deprivation also increase AtHAK5 expression.
All of the above suggest that HAK1-type genes respond to
a general nutrient deprivation. It is possible that the signal
cascades involved in the response to the low availability of a
nutrient share some of their elements, an attractive hypothesis
that needs to be further investigated (Schachtman and
Shin 2007).
Adding more complexity to the regulation of HAK1-type
genes, it has been shown that the addition of some metabolites,
such as sucrose, increases root AtHAK5 expression in the dark
but much less in the light (Lejay et al. 2008), suggesting a role
for photosynthesis in its regulation.
Finding a physiological explanation for the induction of
HAK1 genes by conditions not related to K+ deficiency, such
as NO3 or Pi deprivation or sucrose addition, is difficult at
present. It can be speculated that the important role of K+ in
maintaining xylem and phloem function and therefore in the
movement of nutrients and photoassimilates within the plant
(Marschner 1995, White and Karley 2010) is behind this appar-
ent cross-talk. Remarkably, it has recently been shown that the
Shaker K+ channel AKT2, mainly expressed in the phloem
tissue, switches on a potassium battery that efficiently assists
the plasma membrane H+-ATPase in energizing transmem-
brane transport processes (Gajdanowicz et al. 2011). K+ gradi-
ents are proposed to serve as decentralized energy storage in
this study, which could bring together photosynthesis and
transport of photoassimilates with K+ homeostasis and
AtHAK5 expression.
Another important factor affecting the expression of these
genes seems to be the presence of salinity because, as stated
above, high Na+ concentrations depolarize the plasma mem-
brane potential and repress HAK1-type gene expression.
This was illustrated by the decrease of LeHAK5
(Nieves-Cordones et al. 2007, Nieves-Cordones et al. 2008),
AtHAK5 (Nieves-Cordones et al. 2010) and ThHAK5 (Aleman
et al. 2009b) transcripts when plants were starved of K+ in the
presence of Na+. Importantly, salinity decreased the levels of
ThHAK5 mRNA in the close relative of Arabidopsis, Tellungiella
1606 Plant Cell Physiol. 52(9): 16031612 (2011) doi:10.1093/pcp/pcr096 ! The Author 2011.
halophila, to a lesser extent than those of AtHAK5 transcripts in
the glycophyte. Interestingly, it has been described that root
cells of T. halophila maintain a more negative membrane
potential than Arabidopsis after a 100 mM NaCl treatment
(Volkov and Amtmann 2006). Other examples of differential
gene regulation between salt-sensitive and salt-tolerant species
have been described. In the halophyte Messembryanthemum
crystallinum, HAK genes of group II are expressed and some are
up-regulated in the presence of salinity (Su et al. 2002).
The SOS1 gene, encoding a plasma membrane Na+H+ anti-
porter, is more strongly induced by salt in shoots and expressed
to a higher degree in unstressed roots of T. halophila than in
Arabidopsis (Kant et al. 2006). Therefore, a difference between
salt-sensitive and salt-tolerant species may reside in the differ-
ential regulation of the genes encoding K+ or Na+ transporters
and channels, key players in K+/Na+ homeostasis and plant salt
tolerance. In addition, differences in protein functionality
also occur, as has been observed for ion channels of T. halophila
and Arabidopsis (Volkov and Amtmann 2006, Wang et al.
2006).
In addition to the membrane potential, important elements
of the regulation of HAK1-type genes are ROS and hormones.
ROS and ethylene increase when plants are deprived of K+,
ethylene acting upstream of ROS production (Shin and
Schachtman 2004, Jung et al. 2009). In parallel, AtHAK5 expres-
sion has been shown to be dependent on ethylene and ROS
signaling because mutants affected in ethylene or ROS
pathways, such as the ethylene insensitive2-1 mutant (ein2-1)
or an NADPH oxidase null mutant (rhd2), showed altered
AtHAK5 expression patterns. In addition, ethylene- or EIN2-in-
dependent pathways may also be controlling AtAHK5
expression, and the role of ROS in low K+ signaling seems to
be mediated by the RCI3A peroxidase (Kim et al. 2010).
Interestingly, as well as K+, N and Pi deprivation have been
shown to increase H2O2 (Shin et al. 2005), suggesting that
ROS, together with membrane potential, may be one of the
common pieces in the signaling cascades of low nutrient
sensing. JA may also be participating in low K+ sensing as
up-regulation of the genes controlling the first three steps of
JA biosynthesis has been observed in K+-deprived plants
(Armengaud et al. 2004).
Post-transcriptional regulation of root K+
transport systems
The only report in which the regulation of HAK1-type trans-
porters at the protein level was discussed revealed that the
HvHAK1-mediated Rb+ uptake in Saccharomyces cerevisiae
was modulated by the yeast HAL4/5 kinases and the PPZ1
phosphatase (Fulgenzi et al. 2008). Both types of enzymes
seemed to regulate HvHAK1 activity negatively in K+-starved
yeast cells. Intriguingly, S. cerevisiae does not have homologs of
the HAK K+ transporters, and the observed regulation has to be
further clarified.
 Systems involved in K+ uptake in Arabidopsis

The major regulation of AKT1 is at the protein level (Fig. 1).
By analyzing Arabidopsis mutants sensitive to low K+ stress,
the protein kinase CIPK23 (for CBL-Interacting Protein Kinase
23) was found to be required for the activation of AKT1
(Xu et al. 2006). Furthermore, two calcineurin B-like proteins,
CBL1 and CBL9, interact with and activate CIPK23. Activation
of the CBLs depends on Ca2+, as demonstrated by patchclamp
recordings (Li et al. 2006), suggesting that low K+ triggers
a Ca2+ signal at the root level that leads to AKT1 activation
(Luan et al. 2009). Additionally, the Arabidopsis mutant
cipk23 also exhibits an impaired growth phenotype at low K+
concentrations in the presence of NH+4 (Cheong et al.
2007), demonstrating the importance of this signaling pathway
in K+ nutrition. Furthermore a 2C-type protein phosphatase
AIP1 physically interacts with and inactivates AKT1 (Lee et al.
2007).
Because functional Shaker channels are formed by tetra-
mers, AKT1 activity may also be regulated by interaction
with other a-subunits, giving rise to heterotetrameric proteins
which increase the diversity of their function (Very and
Sentenac 2003, Lebaudy et al. 2007). In particular, AKT1 is
regulated by AtKC1, whose gene is strongly expressed in
roots (Reintanz et al. 2002), and up-regulated by K+ starvation
(Shin and Schachtman 2004) and by salt stress in the shoots
(Pilot et al. 2003). When AtKC1 is co-expressed with AKT1 in
heterologous systems, a shift in the activation threshold
towards more negative values is observed (Duby et al. 2008,
Geiger et al. 2009), probably preventing AKT1 from mediating
K+ efflux. Recently, it has been shown that AtKC1 forms a
ternary complex with AKT1 and the syntaxin SYP121. syp121
mutants show a phenotype that resembles that of akt1 mu-
tants, demonstrating the importance of SYP121 for AKT1 func-
tion, probably by promoting gating of the channel (Honsbein
et al. 2009).
Physiological relevance of AtHAK5 and
AtAKT1
As mentioned above, the physiological relevance of HAK1-type
transporters and AKT1-type channels in root K+ uptake was
first established by indirect evidence. A clear demonstration of
their relative contribution to K+ uptake has recently been
possible by employing T-DNA insertion mutants and selective
inhibitors in the model plant Arabidopsis (Hirsch et al. 1998,
Spalding et al. 1999, Gierth et al. 2005, Qi et al. 2008,
Rubio et al. 2008, Nieves-Cordones et al. 2010, Pyo et al.
2010, Rubio et al. 2010a). The complete sequencing of
the Arabidopsis genome, the highly efficient methods of
Agrobacterium-mediated transformation together with the
short life cycle of Arabidopsis have enabled multiple
approaches to study gene function. Public libraries of T-DNA
insertion lines for most genes are now available (Alonso et al.
2003) and characterization of these lines has become one of
the standards in studying the role of a gene in plant physiology.
The studies with T-DNA insertion lines show that AtHAK5 is
the only system mediating K+ uptake at external concentra-
tions <10 mM (Qi et al. 2008, Nieves-Cordones et al. 2010,
Rubio et al. 2010b) (Fig. 2). Thus, it is likely that AtHAK5 me-
diates the K+/H+ symport suggested by in vivo measurements
(Maathuis and Sanders 1994b). At higher concentrations,
K+ uptake also takes place through AKT1, and between
10 and 200 mM both AtHAK5 and AKT1 systems contribute
to K+ acquisition (Rubio et al. 2010a). In fact, it has been
reported that the athak5 line does not show a growth-deficient
phenotype in agar plates containing 30 mM K+ (Pyo et al. 2010),
suggesting that the lack of AtHAK5 may be fully compensated
by AKT1. That a channel mediates K+ uptake at such low
concentrations may be surprising; however, the recorded
membrane potentials in root cells are sufficiently negative to

[K+]ext (mM)
0.001
Stele Casparian strip NH4+

H+ 0.01
K+ HAK5
ATP
H+
ADP
0.1
K+ AKT1

Ba2+ 1

K+ ?
10
+ +
Fig. 2 Root K acquisition in A. thaliana roots. AtHAK5 is the only system mediating K uptake at external concentrations <10 mM, probably by
a K+H+ symporter. At higher concentrations, K+ uptake also takes place through the AKT1 channel, and between 10 and 200 mM both the
AtHAK5 and AKT1 systems contribute to K+ acquisition. At external concentrations >500 mM, AKT1 is the only system mediating K+ uptake.
AtHAK5 mediates the NH+4 -sensitive component of K+ uptake and AtAKT1 the Ba2+-sensitive component. In the absence of AtHAK5 and
AtAKT1, unknown systems (?) mediate K+ uptake sufficient for plant growth at concentrations >1 mM.

Plant Cell Physiol. 52(9): 16031612 (2011) doi:10.1093/pcp/pcr096 ! The Author 2011. 1607
 F. Aleman et al.
allow this process (Spalding et al. 1999). At external concentra-
tions >500 mM, AtHAK5 is not relevant and the contribution of
AKT1 to K+ uptake becomes more important. Thus, the atakt1
line grows at a lower rate than the wild type and the athak5
line at a similar rate to the wild type at 500 mM external K+
(Rubio et al. 2010a).
The definitive demonstration of the aforementioned results
was obtained by studying a double mutant athak5, atakt1
(Pyo et al. 2010, Rubio et al. 2010a). This double mutant
displayed no Rb+ uptake at concentrations <100 mM, demon-
strating that AtHAK5 and AKT1 were the only systems operat-
ing in the high-affinity range of concentrations. Similar results
were obtained when one of these two systems was impaired
either by selective inhibitors or by gene disruption, confirming
that AtHAK5 and AKT1 mediated the NH+4 - and Ba2+ sensitive
components of K+ uptake, respectively (Spalding et al. 1999,
Santa-Mara et al. 2000, Rubio et al. 2008, Rubio et al. 2010a).
These two inhibitors may be used in other plant species, where
mutants are not available, to study the contribution to K+
uptake of AtHAK5 and AtAKT1 homologs (Nieves-Cordones
et al. 2007, Rubio et al. 2010b).
Above 100 mM K+, other as yet unidentified systems seem to
be involved in K+ uptake in the athak5, atakt1 plants. This
uptake is not sufficient at 0.5 mM K+, because athak5, atakt1
plants displayed lower K+ uptake, biomass and internal K+
concentrations than wild-type plants. Since only the plants
possessing functional AKT1 were similar to wild-type plants,
it could be deduced that AKT1 is the most important system
at this concentration. At 10 mM K+, the unidentified systems
provided sufficient K+ uptake because no deficient phenotype
was observed in athak5, atakt1 double mutants (Rubio et al.
2010a).
Candidate systems that could mediate the K+ uptake
observed in the athak5, atakt1 double mutants could belong
to the CHX family (Zhao et al. 2008), the non-selective channel
regulated by the cyclic nucleotide-gated channels
(CNGCs) family (Li et al. 2005, Demidchik and Maathuis
2007, Kaplan et al. 2007) or to the glutamate receptor-like
channel family (GLR) (Dietrich et al. 2010, White and Karley
2010).
Within the CHX family, AtCHX13 has been suggested as a
possible pathway for root K+ uptake because of its low Km for
K+ (136 mM) when functionally expressed in yeast (Zhao et al.
2008). However, its high sensitivity to Cs+ and Na+ makes the
important contribution of AtCHX13 to K+ acquisition unlikely,
because root K+ uptake does not show such a high sensitivity to
those inhibitors (Rubio et al. 2010b). In addition, a K+ uptake
system with a 136 mM Km for K+ is not observed in the athak5,
atakt1 double mutant (Rubio et al. 2010a), and AtCHX13
expression in roots is restricted to the root tip under low
K+ conditions, which makes it difficult to reconcile with root
K+ uptake allowing growth of the athak5, atakt1 mutant at
high external K+.
With regard to CNGCs, AtCNGC10 transports both K+ and
+
Na and partially rescues an Arabidopsis akt1 mutant line
1608 Plant Cell Physiol. 52(9): 16031612 (2011) doi:10.1093/pcp/pcr096 ! The Author 2011.
(Kaplan et al. 2007). Results obtained with antisense lines of
this channel, which displayed lower AtCNGC10 expression than
wild-type plants, indicated a role in Na+/K+ homeostasis in
roots (Guo et al. 2008). Similar results were obtained for
AtCNGC3. A null mutation in this channel altered both
short-term Na+ influx and K+ uptake at high external K+ con-
ditions, also suggesting a role in non-selective monovalent
cation uptake at the plasma membrane level (Gobert et al.
2006).
Finally, GLR channels could also be considered for root
K+ uptake since several members are expressed in the roots
and, together with CNGCs, are thought to constitute
voltage-independent cation channels in planta (White and
Karley 2010). GLRs allow, like CNGCs, non-selective transport
of ions, including K+, into root cells. However, cytosolic Ca2+
homeostasis and signaling seem to be the major roles of these
channels (Demidchik and Maathuis 2007).
Future perspectives
According to the above, more efforts are needed to increase the
K+ uptake capacities of crops. One way to obtain plants with
improved traits related to K+ uptake is to exploit natural
variability. Responses to environmental conditions depend on
numerous genes and are typically controlled by quantitative
trait loci (QTLs). The identification of variants with improved
stress responses and/or vigor requires phenotypic/genetic
screenings capable of distinguishing between plants with
different behavior. Many examples can be found in the litera-
ture regarding K+ homeostasis, especially under salt stress, and
natural variants with improved performance (Zhu 2001,
Ren 2005, Huang et al. 2006, Rus et al. 2006, Byrt et al. 2007,
Aleman et al. 2009b). Nevertheless, genome sequencing of
natural accessions will reveal sequence variability and will
permit a faster and easier identification of new interesting
varieties.
On the other hand, recent advances in the identification of
molecular entities involved in K+ uptake and its regulation, like
those described in the present review, have opened up a new
group of biotechnological targets to be considered. Now it is
possible to modify the entity of interest directly in a manner
that improves plant responses. This concept can be put into
practice by following two strategies: (i) altering the amount of
the protein (quantity) or (ii) improving its activity (quality).
As regards the first strategy, transformation of plants with a
modified promoter sequence upstream of the gene of interest
would allow changes in the mRNA pool. Strong constitutive
promoters could be used, but cell-specific inducible promoters
may be more efficient. The latter provided better results than
constitutive overexpression when used with AtHKT1 and salt
tolerance in Arabidopsis (Moller et al. 2009). Different gene
regulation of tolerant counterparts could also provide an alter-
native to drive gene expression with fewer side effects.
The different expression patterns of the genes encoding the

HAK5 transporter of A. thaliana and T. halophila provide
an example (Aleman et al. 2009b).
With respect to the second strategy, selection of mutated
versions of the transporter with better features (low sensitivity
to inhibitors or higher uptake capacity) could be carried out in
heterologous systems such as yeast, plant protoplasts or
Xenopus oocytes before assaying them in the plant. This
could be done in combination with the first strategy as well.
Improved versions of different K+ transport systems have
already been obtained for AtHAK5 (Rubio et al. 2000),
HvHAK1 (Mangano et al. 2008), TaHKT1 (Rubio et al. 1995,
Rubio et al. 1999) and HAK1-type transporters of
Physcomitrella patens (Garciadeblas et al. 2007) that could
yield interesting results in planta.
Finally, modification of regulatory proteins could also pro-
vide improvements regarding protein activity. Enhanced K+
uptake via AKT1 was achieved after overexpression of members
of the CIPKCBL pathway that regulates its transport capacity
(Xu et al. 2006). By using these and/or other strategies, it is
tempting to expect that biotechnological approaches could
give a boost to crop yield in the forthcoming years and
therefore help to compensate for climate change damages.
Funding
This work was funded by Fundacion Seneca of Region de
Murcia, Spain [grant No. 08696/PI/08]; the Ministerio de
Ciencia e Innovacion Spain [grant No. AGL2009-08140].
Acknowledgments
We thank Mario Fon for critically reading the manuscript.
References
Ahn, S.J., Shin, R. and Schachtman, D.P. (2004) Expression of KT/KUP
genes in Arabidopsis and the role of root hairs in K+ uptake.
Plant Physiol. 134: 11351145.
Aleman, F., Nieves-Cordones, M., Martnez, V. and Rubio, F. (2009a)
Potassium/sodium steady-state homeostasis in Thellungiella halo-
phila and Arabidopsis thaliana under long-term salinity conditions.
Plant Sci. 176: 768774.
Aleman, F., Nieves-Cordones, M., Martnez, V. and Rubio, F. (2009b)
Differential regulation of the HAK5 genes encoding the high-affinity
K+ transporters of Thellungiella halophila and Arabidopsis thaliana.
Environ. Exp. Bot. 65: 263269.
Alonso, J., Stepanova, A., Leisse, T., Kim, C., Chen, H., Shinn, P. et al.
(2003) Genome-wide insertional mutagenesis of Arabidopsis thali-
ana. Science 301: 653657.
Amtmann, A. and Armengaud, P. (2009) Effects of N, P, K and S on
metabolism: new knowledge gained from multi-level analysis. Curr.
Opin. Plant Biol. 12: 275283.
Amtmann, A., Hammond, J.P., Armengaud, P., White, P.J. and
Callow, J.A. (2006) Nutrient sensing and signalling in plants: potas-
sium and phosphorus. Adv. Bot. Res. 43: 209257.
Plant Cell Physiol. 52(9): 16031612 (2011) doi:10.1093/pcp/pcr096 ! The Author 2011.
Systems involved in K+ uptake in Arabidopsis
Amtmann, A., Troufflard, S. and Armengaud, P. (2008) The effect of
potassium nutrition on pest and disease resistance in plants.
Physiol. Plant. 133: 682691.
Anderson, J.A., Huprikar, S.S., Kochian, L.V., Lucas, W.J. and Gaber, R.F.
(1992) Functional expression of a probable Arabidopsis thaliana
potassium channel in Saccharomyces cerevisiae. Proc. Natl Acad.
Sci. USA 89: 37363740.
Armengaud, P., Breitling, R. and Amtmann, A. (2004) The
potassium-dependent transcriptome of Arabidopsis reveals a
prominent role of jasmonic acid in nutrient signaling. Plant
Physiol. 136: 25562576.
Botella, M.A., Martinez, V., Pardines, J. and Cerda, A. (1997) Salinity
induced potassium deficiency in maize plants. J. Plant Physiol. 150:
200205.
Buschmann, P.H., Vaidyanathan, R., Gassmann, W. and Schroeder, J.I.
(2000) Enhancement of Na+ uptake currents, time-dependent
inward-rectifying K+ channel currents, and K+ channel transcripts
by K+ starvation in wheat root cells. Plant Physiol. 122: 13871398.
Byrt, C.S., Platten, J.D., Spielmeyer, W., James, R.A., Lagudah, E.S.,
Dennis, E.S. et al. (2007) HKT1;5-like cation transporters linked to
Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol. 143:
19181928.
Cheong, Y.H., Pandey, G.K., Grant, J.J., Batistic, O., Li, L., Kim, B.G. et al.
(2007) Two calcineurin B-like calcium sensors, interacting with pro-
tein kinase CIPK23, regulate leaf transpiration and root potassium
uptake in Arabidopsis. Plant J. 52: 223239.
Davenport, R., Munoz-Mayor, A., Jha, D., Essah, P., Rus, A. and
Tester, M. (2007) The Na+ transporter AtHKT1;1 controls retrieval
of Na+ from the xylem in Arabidopsis. Plant Cell Environ. 30:
497507.
Deeken, R., Geiger, D., Fromm, J., Koroleva, O., Ache, P., Langenfeld-
Heyser, R. et al. (2002) Loss of the AKT2/3 potassium channel af-
fects sugar loading into the phloem of Arabidopsis. Planta 216:
334344.
Demidchik, V. and Maathuis, F. (2007) Physiological roles of nonselec-
tive cation channels in plants: from salt stress to signalling and
development. New Phytol. 175: 387404.
Dietrich, P., Anschutz, U., Kugler, A. and Becker, D. (2010) Physiology
and biophysics of plant ligand-gated ion channels. Plant Biol. 12:
8093.
Duby, G., Hosy, E., Fizames, C., Alcon, C., Costa, A., Sentenac, H. et al.
(2008) AtKC1, a conditionally targeted Shaker-type subunit,
regulates the activity of plant K+ channels. Plant J. 53: 115123.
Epstein, E., Rains, D.W. and Elzam, O.E. (1963) Resolution of dual
mechanisms of potassium absorption by barley roots. Proc. Natl
Acad. Sci. USA 49: 684692.
Fulgenzi, F.R., Peralta, M.L., Mangano, S., Danna, C.H., Vallejo, A.J.,
Puigdomenech, P. et al. (2008) The ionic environment controls
the contribution of the barley HvHAK1 transporter to potassium
acquisition. Plant Physiol. 147: 252262.
Gajdanowicz, P., Michard, E., Sandmann, M., Rocha, M., Correa, L. and
Ramirez Aguilar, S. (2011) Potassium (K+) gradients serve as a
mobile energy source in plant vascular tissues. Proc. Natl Acad.
Sci. USA 108: 864869.
Garciadeblas, B., Barrero-Gil, J., Benito, B. and Rodriguez-Navarro, A.
(2007) Potassium transport systems in the moss Physcomitrella
patens: pphak1 plants reveal the complexity of potassium uptake.
Plant J. 52: 10801093.
Geiger, D., Becker, D., Vosloh, D., Gambale, F., Palme, K., Rehers, M.
et al. (2009) Heteromeric AtKC1/AKT1 channels in Arabidopsis
1609
 F. Aleman et al.
roots facilitate growth under K+ limiting conditions. J. Biol. Chem.
284: 2128821295.
Gierth, M., Maser, P. and Schroeder, J.I. (2005) The potassium trans-
porter AtHAK5 functions in K+ deprivation-induced high-affinity
K+ uptake and AKT1 K+ channel contribution to K+ uptake kinet-
ics in Arabidopsis roots. Plant Physiol. 137: 11051114.
Glass, A.D. and Dunlop, J. (1978) The influence of potassium content
on the kinetics of potassium influx into excised ryegrass and barley
roots. Planta 141: 117119.
Glass, A.D.M., Shaff, J.E. and Kochian, L.V. (1992) Studies of the
uptake of nitrate in barley. 4. Electrophysiology. Plant Physiol. 99:
456463.
Gobert, A., Park, G., Amtmann, A., Sanders, D. and Maathuis, F.J.M.
(2006) Arabidopsis thaliana cyclic nucleotide gated channel 3 forms
a non-selective ion transporter involved in germination and cation
transport. J. Exp. Bot. 57: 791800.
Guo, K., Babourina, O., Christopher, D., Borsics, T. and Rengel, Z. (2008)
The cyclic nucleotide-gated channel, AtCNGC10, influences salt
tolerance in Arabidopsis. Physiol. Plant. 134: 499507.
Haro, R., Banuelos, M.A. and Rodrguez-Navarro, A. (2010)
High-affinity sodium uptake in land plants. Plant Cell Physiol. 51:
6879.
Haro, R., Sainz, L., Rubio, F. and Rodrguez-Navarro, A. (1999) Cloning
of two genes encoding potassium transporters in Neurospora crassa
and expression of the corresponging cDNAs in Saccharomyces
cerevisiae. Mol. Microbiol. 31: 511520.
Hermans, C., Hammond, J.P., White, P.J. and Verbruggen, N. (2006)
How do plants respond to nutrient shortage by biomass allocation?.
Trends Plant Sci. 11: 610617.
Hirsch, R.E., Lewis, B.D., Spalding, E.P. and Sussman, M.R. (1998) A role
for the AKT1 potassium channel in plant nutrition. Science 280:
918921.
Honsbein, A., Sokolovski, S., Grefen, C., Campanoni, P., Pratelli, R.,
Paneque, M. et al. (2009) A tripartite SNARE- K+ channel complex
mediates in channel-dependent K+ nutrition in Arabidopsis. Plant
Cell 21: 28592877.
Huang, S., Spielmeyer, W., Lagudah, E.S., James, R.A., Platten, J.D.,
Dennis, E.S. et al. (2006) A sodium transporter (HKT7) is a candidate
for Nax1, a gene for salt tolerance in durum wheat. Plant Physiol.
142: 17181727.
Jung, J.Y., Shin, R. and Schachtman, D.P. (2009) Ethylene mediates
response and tolerance to potassium deprivation in Arabidopsis.
Plant Cell 21: 607621.
Kaddour, R., Narsi, N., Mrah, S., Berthomieu, P. and Lachaal, M. (2009)
Comparative effect of potassium on K and Na uptake and transport
in two accessions of Arabidopsis thaliana during salinity stress. C.R.
Biol. 332: 784794.
Kant, S., Kant, P., Raveh, E. and Barak, S. (2006) Evidence that
differential gene expression between the halophyte, Thellungiella
halophila, and Arabidopsis thaliana is responsible for higher levels of
the compatible osmolyte proline and tight control of Na+ uptake in
T. halophila. Plant Cell Environ. 29: 12201234.
Kaplan, B., Sherman, T. and Fromm, H. (2007) Cyclic nucleotide-gated
channels in plants. FEBS Lett. 581: 22372246.
Kim, M.J., Ciani, S. and Schachtman, D.P. (2010) A peroxidase contrib-
utes to ROS production during Arabidopsis root response to
potassium deficiency. Mol. Plant 3: 420427.
Kronzucker, H.J., Szczerba, M.W., Schulze, L.M. and Britto, D.T. (2008)
Non-reciprocal interactions between K+ and Na+ ions in barley
(Hordeum vulgare L.). J. Exp. Bot. 59: 27932801.
1610 Plant Cell Physiol. 52(9): 16031612 (2011) doi:10.1093/pcp/pcr096 ! The Author 2011.
Lagarde, D., Basset, M., Lepetit, M., Conejero, G., Gaymard, F., Astruc, S.
et al. (1996) Tissue-specific expression of Arabidopsis AKT1 gene is
consistent with a role in K+ nutrition. Plant J. 9: 195203.
Lebaudy, A., Very, A.A. and Sentenac, H. (2007) K+ channel activity in
plants: genes, regulations and functions. FEBS Lett. 581: 23572366.
Lee, S.C., Lan, W.Z., Kim, B.G., Li, L., Cheong, Y.H., Pandey, G.K. et al.
(2007) A protein phosphorylation/dephosphorylation network
regulates a plant potassium channel. Proc. Natl Acad. Sci. USA
104: 1595915964.
Lejay, L., Wirth, J., Pervent, M., Cross, J.M.-F., Tillard, P. and Gojon, A.
(2008) Oxidative pentose phosphate pathway-dependent sugar
sensing as a mechanism for regulation of root ion transporters by
photosynthesis. Plant Physiol. 146: 20362053.
Li, L., Kim, B.G., Cheong, Y.H., Pandey, G.K. and Luan, S. (2006) A Ca2+
signaling pathway regulates a K+ channel for low-K response in
Arabidopsis. Proc. Natl Acad. Sci. USA 103: 1262512630.
Li, X., Borsics, T., Harrington, H.M. and Christopher, D.A. (2005)
Arabidopsis AtCNGC10 rescues potassium channel mutants of E.
coli, yeast and Arabidopsis and is regulated by calcium/calmodulin
and cyclic GMP in E. coli. Funct. Plant Biol. 32: 643653.
Luan, S., Lan, W. and Chul Lee, S. (2009) Potassium nutrition, sodium
toxicity, and calcium signaling: connections through the CBLCIPK
network. Curr. Opin. Plant Biol. 12: 339346.
Maathuis, F.J.M. (2009) Physiological functions of mineral macronu-
trients. Curr. Opin. Plant Biol. 12: 250258.
Maathuis, F.J.M., Filatov, V., Herzyk, P., Krijger, G.C., Axelsen, K.B.,
Chen, S.X. et al. (2003) Transcriptome analysis of root transporters
reveals participation of multiple gene families in the response to
cation stress. Plant J. 35: 675692.
Maathuis, F.J.M. and Sanders, D. (1993) Energization of potassium
uptake in Arabidopsis thaliana. Planta 191: 302307.
Maathuis, F.J. and Sanders, D. (1994a) Mechanism of high-affinity
potassium uptake in roots of Arabidopsis thaliana. Proc. Natl
Acad. Sci. USA 91: 92729276.
Maathuis, F.J.M. and Sanders, D. (1994b) Mechanisms of high-affinity
potassium uptake in roots of Arabidopsis thaliana. Proc. Natl Acad.
Sci. USA 91: 92729276.
Maathuis, F.J.M. and Sanders, D. (1996) Mechanisms of
potassium absorption by higher plant roots. Physiol. Plant. 96:
158168.
Maathuis, F.J.M., Verlin, D., Smith, F.A., Sanders, D., Fernandez, J.A. and
Walker, N.A. (1996) The physiological relevance of Na+-coupled K+-
transport. Plant Physiol. 112: 16091616.
Mangano, S., Silberstein, S. and Santa-Maria, G.E. (2008) Point muta-
tions in the barley HvHAK1 potassium transporter lead to im-
proved K+-nutrition and enhanced resistance to salt stress. FEBS
Lett. 582: 39223928.
Marschner, H. (1995) In Mineral Nutrition of Higher Plants. Springer,
New York.
Martnez-Cordero, M.A., Martnez, V. and Rubio, F. (2004) Cloning and
functional characterization of the high-affinity K+ transporter
HAK1 of pepper. Plant Mol. Biol. 56: 413421.
Maser, P., Thomine, S., Schroeder, J.I., Ward, J.M., Hirschi, K., Sze, H.
et al. (2001) Phylogenetic relationships within cation transporter
families of Arabidopsis. Plant Physiol. 126: 16461667.
Meharg, A. and Blatt, M. (1995) NO3 transport across the plasma
membrane of Arabidopsis thaliana root hairskinetic control by
pH and membrane voltage. J. Membr. Biol. 145: 4966.
Mengel, K., Kirkby, E.A., Kosegarten, H. and Appel, T. (2001) In
Principles on Plant Nutrition. Kluwer, Dordrecht.

Moller, I.S., Gilliham, M., Jha, D., Mayo, G.M., Roy, S.J., Coates, J.C. et al.
(2009) Shoot Na+ exclusion and increased salinity tolerance
engineered by cell type-specific alteration of Na+ transport in
Arabidopsis. Plant Cell 21: 21632178.
Nieves-Cordones, M., Aleman, F., Martnez, V. and Rubio, F. (2010) The
Arabidopsis thaliana HAK5 K+ transporter is required for plant
growth and K+ acquisition from low K+ solutions under saline
conditions. Mol. Plant 3: 326333.
Nieves-Cordones, M., Aleman, F., Martnez, V. and Rubio, F. (2011) K+
nutrition, K+ uptake and its role in environmental stress in plants.
In Environmental Adaptations and Stress Tolerance in Plants in the
Era of Climate Change. Edited by Parvaiz, A. and Prasad, M. Springer,
Berlin; (in press).
Nieves-Cordones, M., Martinez-Cordero, M.A., Martinez, V. and
Rubio, F. (2007) An NH4+-sensitive component dominates
high-affinity K+ uptake in tomato plants. Plant Sci. 172: 273280.
Nieves-Cordones, M., Miller, A., Aleman, F., Martnez, V. and Rubio, F.
(2008) A putative role for the plasma membrane potential in the
control of the expression of the gene encoding the tomato
high-affinity potassium transporter HAK5. Plant Mol. Biol. 68:
521532.
Pilot, G., Gaymard, F., Mouline, K., Cherel, I. and Sentenac, H. (2003)
Regulated expression of Arabidopsis Shaker K+ channel genes
involved in K+ uptake and distribution in the plant. Plant Mol.
Biol. 51: 773787.
Pyo, Y.J., Gierth, M., Schroeder, J.I. and Cho, M.H. (2010) High-affinity
K+ transport in Arabidopsis: AtHAK5 and AKT1 are vital for
seedling establishment and postgermination growth under
low-potassium conditions. Plant Physiol. 153: 863875.
Qi, Z., Hampton, C.R., Shin, R., Barkla, B.J., White, P.J. and
Schachtman, D.P. (2008) The high affinity K+ transporter AtHAK5
plays a physiological role in planta at very low K+ concentrations
and provides a caesium uptake pathway in Arabidopsis. J. Exp. Bot.
59: 595607.
Reintanz, B., Szyroki, A., Ivashikina, N., Ache, P., Godde, M., Becker, D.
et al. (2002) AtKC1, a silent Arabidopsis potassium channel
alpha-subunit modulates root hair K+ influx. Proc. Natl Acad. Sci.
USA 99: 40794084.
Ren, Z.H. (2005) A rice quantitative trait locus for salt
tolerance encodes a sodium transporter. Nat. Genet. 37:
11411146.
Rengel, Z. and Damon, P.M. (2008) Crops and genotypes differ in
efficiency of potassium uptake and use. Physiol. Plant. 133: 624636.
Rodrguez-Navarro, A. (2000) Potassium transport in fungi and plants.
Biochim. Biophys. Acta 1469: 130.
Rodrguez-Navarro, A., Blatt, M.R. and Slayman, C.L. (1986) A potas-
siumproton symport in Neurospora crassa. J. Gen. Physiol. 87:
649674.
Rodrguez-Navarro, A. and Rubio, F. (2006) High-affinity potassium
and sodium transport systems in plants. J. Exp. Bot. 57: 11491160.
Romheld, V. and Kirkby, E. (2010) Research on potassium in
agriculture: needs and prospects. Plant Soil 335: 155180.
Rubio, F., Aleman, F., Nieves-Cordones, M. and Vicente, M. (2010a)
Studies on Arabidopsis athak5, atakt1 double mutants disclose the
range of concentrations at which AtHAK5, AtAKT1 and unknown
systems mediate K+ uptake. Physiol. Plant. 139: 220228.
Rubio, F., Arevalo, L., Caballero, F., Botella, M.A., Rubio, J.S., Garca-
Sanchez, F. et al. (2010b) Systems involved in K+ uptake from
diluted solutions in pepper plants as revealed by the use of specific
inhibitors. J. Plant Physiol. 167: 14941499.
Plant Cell Physiol. 52(9): 16031612 (2011) doi:10.1093/pcp/pcr096 ! The Author 2011.
Systems involved in K+ uptake in Arabidopsis
Rubio, F., Gassmann, W. and Schroeder, J.I. (1995) Sodium-driven
potassium uptake by the plant potassium transporter HKT1 and
mutations conferring salt tolerance. Science 270: 16601663.
Rubio, F., Nieves-Cordones, M., Aleman, F. and Martnez, V. (2008)
Relative contribution of AtHAK5 and AtAKT1 to K+ uptake in the
high-affinity range of concentrations. Physiol. Plant. 134: 598608.
Rubio, F., Santa-Maria, G.E. and Rodrguez-Navarro, A. (2000) Cloning
of Arabidopsis and barley cDNAs encoding HAK potassium trans-
porters in root and shoot cells. Physiol. Plant. 109: 3443.
Rubio, F., Schwarz, M., Gassmann, W. and Schroeder, J.I. (1999) Genetic
selection of mutations in the high affinity K+ transporter HKT1 that
define functions of a loop site for reduced Na+ permeability and
increased Na+ tolerance. J. Biol. Chem. 274: 68396847.
Rubio, J.S., Garcia-Sanchez, F., Rubio, F., Garcial, A.L. and Martnez, V.
(2010) The importance of K+ in ameliorating the negative effects of
salt stress on the growth of pepper plants. Eur. J. Hort. Sci. 75: 3341.
Rus, A., Baxter, I., Muthukumar, B., Gustin, J., Lahner, B., Yakubova, E.
et al. (2006) Natural variants of AtHKT1 enhance Na+ accumula-
tion in two wild populations of Arabidopsis. PLoS Genet. 2:
19641973.
Santa-Mara, G.E., Danna, C.H. and Czibener, C. (2000) High-affinity
potassium transport in barley roots. Ammonium-sensitive and
-insensitive pathways. Plant Physiol. 123: 297306.
Santa-Mara, G.E., Rubio, F., Dubcovsky, J. and Rodrguez-Navarro, A.
(1997) The HAK1 gene of barley is a member of a large gene family
and encodes a high-affinity potassium transporter. Plant Cell 9:
22812289.
Schachtman, D.P. and Schroeder, J.I. (1994) Structure and transport
mechanism of a high-affinity potassium uptake transporter from
higher plants. Nature 370: 655658.
Schachtman, D.P. and Shin, R. (2007) Nutrient sensing and signaling:
NPKS. Annu. Rev. Plant Biol. 58: 4769.
Schroeder, J.I., Ward, J.M. and Gassmann, W. (1994) Perspectives on
the physiology and structure of inward-rectifying K+ channels in
higher plants: biophysical implications for K+ uptake. Annu. Rev.
Biophys. Biomol. Struct. 23: 441471.
Sentenac, H., Bonneaud, N., Minet, M., Lacroute, F., Salmon, J.M.,
Gaymard, F. et al. (1992) Cloning and expression in
yeast of a plant potassium ion transport system. Science 256:
663665.
Shabala, S. and Cuin, T.A. (2008) Potassium transport and plant salt
tolerance. Physiol. Plant. 133: 651669.
Shin, R., Berg, R.H. and Schachtman, D.P. (2005) Reactive oxygen
species and root hairs in Arabidopsis root response to nitrogen,
phosphorus and potassium deficiency. Plant Cell Physiol. 46:
13501357.
Shin, R. and Schachtman, D.P. (2004) Hydrogen peroxide mediates
plant root cell response to nutrient deprivation. Proc. Natl Acad.
Sci. USA 101: 88278832.
Spalding, E.P., Hirsch, R.E., Lewis, D.R., Qi, Z., Sussman, M.R. and
Lewis, B.D. (1999) Potassium uptake supporting plant growth in
the absence of AKT1 channel activity: inhibition by ammonium
and stimulation by sodium. J. Gen. Physiol. 113: 909918.
Su, H., Golldack, D., Zhao, C. and Bohnert, H.J. (2002) The expression of
HAK-type K+ transporters is regulated in response to salinity stress
in common ice plant. Plant Physiol. 129: 14821493.
Sunarpi., Horie, T., Motoda, J., Kubo, M., Yang, H., Yoda, K. et al. (2005)
Enhanced salt tolerance mediated by AtHKT1 transporter-induced
Na+ unloading from xylem vessels to xylem parenchyma cells. Plant
J. 44: 928938.
1611
 F. Aleman et al.
Troufflard, S., Mullen, W., Larson, T., Graham, I., Crozier, A. and
Amtmann, A. (2010) Potassium deficiency induces the biosynthesis
of oxylipins and glucosinolates in Arabidopsis thaliana. BMC Plant
Biol. 10: 172.
Uozumi, N., Kim, E.J., Rubio, F., Yamaguchi, T., Muto, S., Tsuboi, A. et al.
(2000) The Arabidopsis HKT1 gene homolog mediates inward Na+
currents in Xenopus laevis oocytes and Na+ uptake in
Saccharomyces cerevisiae. Plant Physiol. 122: 12491259.
Very, A.A. and Sentenac, H. (2003) Molecular mechanisms and regu-
lation of K+ transport in higher plants. Annu. Rev. Plant. Biol. 54:
575603.
Volkov, V. and Amtmann, A. (2006) Thellungiella halophila, a
salt-tolerant relative of Arabidopsis thaliana, has specific root
ion-channel features supporting K+/Na+ homeostasis under salinity
stress. Plant J. 48: 342353.
Walker, D.J., Black, C.R. and Miller, A.J. (1998) The role of cytosolic
potassium and pH in the growth of barley roots. Plant Physiol. 118:
957964.
Walker, D.J., Leigh, R.A. and Miller, A.J. (1996) Potassium homeostasis
in vacuolate plant cells. Proc. Natl Acad. Sci. USA 93: 1051010514.
Wang, B., Davenport, R.J., Volkov, V. and Amtmann, A. (2006) Low
unidirectional sodium influx into root cells restricts net sodium
accumulation in Thellungiella halophila, a salt-tolerant relative of
Arabidopsis thaliana. J. Exp. Bot. 57: 11611170.
Wang, Y.-H., Garvin, D.F. and Kochian, L.V. (2002) Rapid induction of
regulatory and transporter genes in response to phosphorus, po-
tassium, and iron deficiencies in tomato roots. Evidence for cross
1612 Plant Cell Physiol. 52(9): 16031612 (2011) doi:10.1093/pcp/pcr096 ! The Author 2011.
talk and root/rhizosphere-mediated signals. Plant Physiol. 130:
13611370.
Wang, Y. and Wu, W.-H. (2010) Plant sensing and signaling in response
to K+-deficiency. Mol. Plant 3: 280287.
Wang, Y.H., Garvin, D.F. and Kochian, L.V. (2001) Nitrate-induced
genes in tomato roots. Array analysis reveals novel genes that
may play a role in nitrogen nutrition. Plant Physiol. 127: 345359.
Ward, J.M., Maser, P. and Schroeder, J.I. (2009) Plant ion channels: gene
families, physiology, and functional genomics analyses. Annu.
Rev.Physiol. 71: 5982.
Wei Yang, T.J., Perry, P.J., Ciani, S., Pandian, S. and Schmidt, W. (2008)
Manganese deficiency alters the patterning and development of
root hairs in Arabidopsis. J. Exp. Bot. 59: 34533464.
White, P.J. and Karley, A.J. (2010) Potassium. In Cell Biology of Metals
and Nutrients. Edited by Hell, R. and Mendel, R.-R. pp. 199224.
Springer, Heidelberg.
Xu, J., Li, H.D., Chen, L.Q., Wang, Y., Liu, L.L., He, L. and Wu, W.H. (2006)
A protein kinase, interacting with two calcineurin B-like proteins,
regulates K+ transporter AKT1 in Arabidopsis. Cell 125: 13471360.
Zhao, J., Cheng, N.H., Motes, C.M., Blancaflor, E.B., Moore, M.,
Gonzales, N. et al. (2008) AtCHX13 is a plasma membrane K+
transporter. Plant Physiol. 148: 796807.
Zhu, J.K. (2001) Plant salt tolerance. Trends Plant Sci. 6: 6671.
Zimmermann, S., Talke, I., Ehrhardt, T., Nast, G. and Muller-Rober, B.
(1998) Characterization of SKT1, an inwardly rectifying potassium
channel from potato, by heterologous expression in insect cells.
Plant Physiol. 116: 879890.