root k + acquisition in plants: the arabidopsis thaliana model

Root K+ Acquisition in Plants: The Arabidopsis thalianaModelFernando Aleman, Manuel Nieves-Cordones, Vicente Martınez and Francisco Rubio*Centro de Edafologıa y Biologıa Aplicada del Segura-CSIC, Campus de Espinardo, 30100 Murcia, Spain*Corresponding author: E-mail, [email protected]; 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 iswidely used as a fertilizer to increase crop production. Thus,the identification of the systems involved in K+ acquisitionby plants has always been a research goal as it may eventu-ally produce molecular tools to enhance crop productivityfurther. This review is focused on the recent findings on thesystems involved in K+ acquisition. From Epstein’s pioneer-ing work>40 years ago, K+ uptake was considered to consistof a high- and a low-affinity component. The subsequentmolecular 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 ofthese genes and the proteins that they encode have alsobeen gained in recent studies. A demonstration of the roleof the two main K+ uptake systems at the root, AtHKA5 andAKT1, 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 externalconcentrations <10 mM. Between 10 and 200 mM bothAtHAK5 and AKT1 contribute to K+ acquisition. At externalconcentrations >500 mM, AtHAK5 is not relevant andAKT1’s contribution to K+ uptake becomes more important.At 10 mM K+, unidentified systems may provide sufficientK+ 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 isinvolved in many and important physiological processes.Growth is one of the processes where K+ has one of the mostimportant roles. Rapid cell expansion relies on the high mobilityof K+, which acts as an osmoticum, to drive growth, a role thatcan be substituted by a few other inorganic ions. When cell

expansion is over, less mobile osmotica such as sugars, organicacids and compatible solutes are accumulated (Amtmann et al.2006).

K+ is also important for enzyme activation, movements,charge neutralization, transcription and post-translationalmodification (Maathuis 2009), having a great impact on cellmetabolism (Amtmann and Armengaud 2009). It also playsan important role in transport of solutes through thephloem. For example, it is required for sucrose movementfrom 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 andamino 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 Karley2010). 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 andKirkby 2010, Wang and Wu 2010), as K+ deficiency inducesreactive oxygen species (ROS) and jasmonic acid (JA), involvedin tolerance to diseases and pests, as well as ethylene and auxinproduction. Therefore, optimization of K+ nutritional status isimportant 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 from1999 to 2005 and it was predicted to have increased by 12% inthe last decade. Although there are K+ reserves for thousandsof years of agriculture, profitable production, especially inmarginal lands, relies on the increase in the efficient use ofK+ and other nutrients.

It is generally accepted that the typical K+ concentration insoils varies between 0.1 and 1 mM (Maathuis 2009). However,large areas of cultivated land are K+ deficient (Rengel andDamon 2008, Romheld and Kirkby 2010). In addition, inad-equate nutrient recycling leads to nutrient deficiency, especiallyof K+ because nitrogen and phosphorus are added as fertilizersto the same level as they are removed by crops, but the same is

Plant Cell Physiol. 52(9): 1603–1612 (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: [email protected]

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not true for K+. Nutrient deficiencies appear worldwide, and indeveloping countries fertilizers may not be affordable. Indeveloped countries, the increase in the cost of fertilizers andthe need to reduce environmental damage because of abusivefertilizer inputs lead to the use of more efficient cultivars andgenotypes for sustainable, low-input agriculture. In addition,developed countries pay a lot of attention to the use of cropresidues 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 futuredue to global warming, negatively affect K+ nutrition (Romheldand Kirkby 2010, Nieves-Cordones et al. 2011). Among thesestresses, salt stress is one of the most important. Salt stress iscomposed of two main effects: the osmotic and the ionic effect.The latter involves toxicity because of high concentrations ofCl� and Na+. Most importantly, Na+ has been shown to induceK+ deficiency (Botella et al. 1997, Kronzucker et al. 2008,Aleman et al. 2009a) and an increase in K+ in the soil can beused to ameliorate Na+ toxicity (J. S. Rubio et al. 2010).Therefore, to increase crop salt tolerance, it is important notonly to reduce Na+ accumulation within plant tissues, but alsoto increase the K+/Na+ ratio (Shabala and Cuin 2008, J. S. Rubioet 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 withspecial emphasis on the model plant Arabidopsis thaliana. Sincethe identification of the first two plant K+ uptake systems in1992 (Anderson et al. 1992, Sentenac et al. 1992) a largenumber of plant genes for K+ transport have been identified(Maser et al. 2001, Ward et al. 2009). A clear demonstration ofthe physiological role of two of them, HAK5 (or HAK1, for otherspecies) and AKT1, in root K+ uptake has only been possiblewith studies performed in the model plant Arabidopsis, whichare described in the following sections.

Root K+ absorption

Potassium acquisition from the soil solution takes placethrough epidermal and cortical cells of the roots. The lipidbilayer of cell membranes is not permeable to ions, water andmost of the polar molecules, and K+ enters the root symplastthrough K+-specific transport proteins located in themembrane.

The kinetics of root K+ uptake were described>40 years agoin barley (Epstein et al. 1963). K+ uptake exhibited biphasickinetics in response to increasing external K+ concentrationswith a high- and a low-affinity component. Consideringenergetic limitations, it has been traditionally proposed thathigh-affinity K+ uptake is an active process mediated byH+/K+ symporters, and low-affinity, passive uptake is mediatedby channels (Maathuis and Sanders 1996, Rodrıguez-Navarro2000).

Identification of root K+ uptake systems

The identification of the molecular entities that mediate K+

uptake began with the functional expression of plant cDNAsin heterologous systems such as yeast, Xenopus laevis oocytes orinsect cells (Sentenac et al. 1992, Schachtman and Schroeder1994, Santa-Marıa et al. 1997, Zimmermann et al. 1998).The contribution of each of these transport systems to rootK+ uptake was established from indirect evidence. Theexpression pattern of their encoding genes, their tissue andintracellular localization and their K+ transport properties inheterologous systems, together with the data on cytoplasmicK+ concentrations and membrane potentials of epidermal andcortical root cells, allowed a general model for their function tobe depicted. According to this model, low-affinity K+ uptakecould be mediated by inward-rectifier Shaker K+ channels suchas the Arabidopsis AKT1, whose gene is expressed mainly inroot epidermal cells (Lagarde et al. 1996). These types ofchannels mediate sustained K+ uptake compatible withlow-affinity K+ uptake and are sufficient to promote plantgrowth (Schroeder et al. 1994). High-affinity K+ uptake couldbe mediated by transporters of the TRK-HKT family such as thewheat TaHKT1 (Schachtman and Schroeder 1994) or theKT/HAK/KUP family such as the barley HvHAK1(Santa-Marıa et al. 1997). The physiological relevance ofTRK-HKT transporters for high-affinity root K+ uptake is notyet clear. Some HKT transporters, such as TaHKT1, mediatehigh-affinity Na+-coupled K+-uptake (Rubio et al. 1995) andare 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 landplants, and it is probably mediated by HKT transporters inrice and species in the Triticeae and Aveneae tribes of thePoaceae family (Haro et al. 2010). The only HKT transporterof Arabidopsis, AtHKT1 (Uozumi et al. 2000), is related to boththe control of Na+ accumulation in the root and retrieval ofNa+ from the xylem (Sunarpi et al. 2005, Davenport et al.2007). On the other hand, HAK1-type transporters of theKT/HAK/KUP family show high affinity for K+, low discrimin-ation between K+ and Rb+, inhibition by NH+

4 , and they areencoded by genes that are induced in roots upon K+ starvation(Rodrıguez-Navarro and Rubio 2006). All these characteristicsare in agreement with the high-affinity K+ uptake observed inplant roots (Epstein et al. 1963, Glass and Dunlop 1978), whichstrongly suggests that HAK1-type transporters are majorcontributors to high-affinity K+ uptake. Their transport mech-anism has not been fully demonstrated yet, but it is probablythe same as the predicted K+–H+ symporter mediatinghigh-affinity K+ uptake, as has been shown for the homologousNcHAK1 of Neurospora crassa (Rodriguez-Navarro et al. 1986,Haro et al. 1999). Importantly, high-affinity K+ uptake coupledto H+ has been described in Arabidopsis root protoplasts(Maathuis and Sanders 1994a) and in barley roots (Walkeret al. 1996).

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Transcriptional regulation of root K+

transport systems

The expression of AKT1 does not respond to the externalsupply 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 expressionin a long-term study (Kaddour et al. 2009), while othersreported no change with shorter NaCl treatments (Maathuiset al. 2003, Pilot et al. 2003). In addition, changes in AKT1expression when plants are treated with hormones have beendescribed (Pilot et al. 2003). Exposure to the cytokininbenzyladenine and to the synthetic auxin 2,4 D decreased theexpression levels of AKT1 and its regulatory subunit AtKC1.However, the study showed that the AKT1 transcript was theleast sensitive to the tested hormones, and SKOR, which isidentified 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 notimportant for its regulation.

In contrast to AKT1, the changes in expression of HAK1-typegenes by the external supply of K+ constitute an importantpart of their regulation. K+ starvation greatly increasesthe mRNA levels of HAK1-type genes (Santa-Marıa et al.1997, Wang et al. 2002, Ahn et al. 2004, Armengaud et al.2004, Martınez-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-Cordoneset al. 2008). Because of the distinct response of the HAK1-type genes to K+, they have been suggested to be useful toolsfor the study of K+ sensing at the root level (Amtmann et al.2006).

Many studies have further deepened our knowledge of theregulation of HAK1-type genes, showing a much more complexregulation than expected (Fig. 1). Apoplastic K+ concentrationand membrane potential have been proposed to be the firststeps 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 thetonoplast (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 membranepotential, which appears within just a few minutes after thedecrease in external K+ (Maathuis and Sanders 1993, Wang andWu 2010). Recently, an important role for the membranepotential has been suggested for the regulation of HAK1-typegenes. In tomato plants, LeHAK5 expression levels in root cellscorrelated with their steady-state plasma membrane potentialsbut not with their cytoplasmic K+ concentrations nor with theK+ concentrations of the external solution (Nieves-Cordoneset al. 2008). The recorded plasma membrane potentials andLeHAK5 expression were importantly affected by long-termchanges in the composition of the growth solution. Forinstance, 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 ethylene–ROS signal that leads toAtHAK5 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 CBL1–CIPK23 complex. AKT1 function is activated by CIPK23-mediated phosphorylation andinactivated by AIP1-mediated dephosphorylation. AKT1 activity is also regulated by interaction with the AtKC1 subunit and the syntaxin SYP121.


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hyperpolarized the membrane potential, increased LeHAK5mRNA levels. The presence of Na+ in K+-starved plantsdepolarized the plasma membrane potential and repressedLeHAK5. In addition, short-term exposure of K+-starved rootsto depolarizing agents such as CCCP or vanadate decreasedLeHAK5 expression. Further results support the idea thatthe membrane potential may be regulating the expression ofHAK1-type genes. Arabidopsis akt1 knock-out lines showhyperpolarization of root cells (Spalding et al. 1999) andAtHAK5 up-regulation (Qi et al. 2008, Rubio et al. 2008).NO�3 deprivation has been shown to hyperpolarize root mem-brane potentials (Meharg and Blatt 1995) and to producean increase in AtHAK5 mRNA levels (Shin et al. 2005).Moreover, NO�3 addition to NO�3 -deprived plants depolarizesthe root membrane potential (Glass et al. 1992, Meharg andBlatt 1995) and represses LeHAK5 expression (Wang et al.2001). Furthermore, Pi (Shin et al. 2005) or Mn (WeiYang et al. 2008) deprivation also increase AtHAK5 expression.All of the above suggest that HAK1-type genes respond toa general nutrient deprivation. It is possible that the signalcascades involved in the response to the low availability of anutrient share some of their elements, an attractive hypothesisthat needs to be further investigated (Schachtman andShin 2007).

Adding more complexity to the regulation of HAK1-typegenes, it has been shown that the addition of some metabolites,such as sucrose, increases root AtHAK5 expression in the darkbut much less in the light (Lejay et al. 2008), suggesting a rolefor photosynthesis in its regulation.

Finding a physiological explanation for the induction ofHAK1 genes by conditions not related to K+ deficiency, suchas NO�3 or Pi deprivation or sucrose addition, is difficult atpresent. It can be speculated that the important role of K+ inmaintaining xylem and phloem function and therefore in themovement 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 theShaker K+ channel AKT2, mainly expressed in the phloemtissue, switches on a ‘potassium battery’ that efficiently assiststhe 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 inthis study, which could bring together photosynthesis andtransport of photoassimilates with K+ homeostasis andAtHAK5 expression.

Another important factor affecting the expression of thesegenes seems to be the presence of salinity because, as statedabove, 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 (Alemanet al. 2009b) transcripts when plants were starved of K+ in thepresence of Na+. Importantly, salinity decreased the levels ofThHAK5 mRNA in the close relative of Arabidopsis, Tellungiella

halophila, to a lesser extent than those of AtHAK5 transcripts inthe glycophyte. Interestingly, it has been described that rootcells of T. halophila maintain a more negative membranepotential than Arabidopsis after a 100 mM NaCl treatment(Volkov and Amtmann 2006). Other examples of differentialgene regulation between salt-sensitive and salt-tolerant specieshave been described. In the halophyte Messembryanthemumcrystallinum, HAK genes of group II are expressed and some areup-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 expressedto a higher degree in unstressed roots of T. halophila than inArabidopsis (Kant et al. 2006). Therefore, a difference betweensalt-sensitive and salt-tolerant species may reside in the differ-ential regulation of the genes encoding K+ or Na+ transportersand channels, key players in K+/Na+ homeostasis and plant salttolerance. In addition, differences in protein functionalityalso occur, as has been observed for ion channels of T. halophilaand Arabidopsis (Volkov and Amtmann 2006, Wang et al.2006).

In addition to the membrane potential, important elementsof 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 andSchachtman 2004, Jung et al. 2009). In parallel, AtHAK5 expres-sion has been shown to be dependent on ethylene and ROSsignaling because mutants affected in ethylene or ROSpathways, such as the ethylene insensitive2-1 mutant (ein2-1)or an NADPH oxidase null mutant (rhd2), showed alteredAtHAK5 expression patterns. In addition, ethylene- or EIN2-in-dependent pathways may also be controlling AtAHK5expression, and the role of ROS in low K+ signaling seems tobe mediated by the RCI3A peroxidase (Kim et al. 2010).Interestingly, as well as K+, N and Pi deprivation have beenshown to increase H2O2 (Shin et al. 2005), suggesting thatROS, together with membrane potential, may be one of thecommon pieces in the signaling cascades of low nutrientsensing. JA may also be participating in low K+ sensing asup-regulation of the genes controlling the first three steps ofJA 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 theHvHAK1-mediated Rb+ uptake in Saccharomyces cerevisiaewas modulated by the yeast HAL4/5 kinases and the PPZ1phosphatase (Fulgenzi et al. 2008). Both types of enzymesseemed to regulate HvHAK1 activity negatively in K+-starvedyeast cells. Intriguingly, S. cerevisiae does not have homologs ofthe HAK K+ transporters, and the observed regulation has to befurther clarified.


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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 Kinase23) 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. Activationof the CBLs depends on Ca2+, as demonstrated by patch–clamprecordings (Li et al. 2006), suggesting that low K+ triggersa Ca2+ signal at the root level that leads to AKT1 activation(Luan et al. 2009). Additionally, the Arabidopsis mutantcipk23 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 pathwayin K+ nutrition. Furthermore a 2C-type protein phosphataseAIP1 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 interactionwith other a-subunits, giving rise to heterotetrameric proteinswhich increase the diversity of their function (Very andSentenac 2003, Lebaudy et al. 2007). In particular, AKT1 isregulated by AtKC1, whose gene is strongly expressed inroots (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 inheterologous systems, a shift in the activation thresholdtowards more negative values is observed (Duby et al. 2008,Geiger et al. 2009), probably preventing AKT1 from mediatingK+ efflux. Recently, it has been shown that AtKC1 forms aternary complex with AKT1 and the syntaxin SYP121. syp121mutants 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 (Honsbeinet al. 2009).

Physiological relevance of AtHAK5 andAtAKT1

As mentioned above, the physiological relevance of HAK1-typetransporters and AKT1-type channels in root K+ uptake wasfirst established by indirect evidence. A clear demonstration oftheir relative contribution to K+ uptake has recently beenpossible by employing T-DNA insertion mutants and selectiveinhibitors 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 ofthe Arabidopsis genome, the highly efficient methods ofAgrobacterium-mediated transformation together with theshort life cycle of Arabidopsis have enabled multipleapproaches to study gene function. Public libraries of T-DNAinsertion lines for most genes are now available (Alonso et al.2003) and characterization of these lines has become one ofthe standards in studying the role of a gene in plant physiology.

The studies with T-DNA insertion lines show that AtHAK5 isthe 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 between10 and 200 mM both AtHAK5 and AKT1 systems contributeto K+ acquisition (Rubio et al. 2010a). In fact, it has beenreported that the athak5 line does not show a growth-deficientphenotype in agar plates containing 30 mM K+ (Pyo et al. 2010),suggesting that the lack of AtHAK5 may be fully compensatedby AKT1. That a channel mediates K+ uptake at such lowconcentrations may be surprising; however, the recordedmembrane potentials in root cells are sufficiently negative to

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Fig. 2 Root K+ acquisition in A. thaliana roots. AtHAK5 is the only system mediating K+ uptake at external concentrations<10mM, probably bya K+–H+ symporter. At higher concentrations, K+ uptake also takes place through the AKT1 channel, and between 10 and 200 mM both theAtHAK5 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 andAtAKT1, unknown systems (?) mediate K+ uptake sufficient for plant growth at concentrations >1 mM.



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allow this process (Spalding et al. 1999). At external concentra-tions>500 mM, AtHAK5 is not relevant and the contribution ofAKT1 to K+ uptake becomes more important. Thus, the atakt1line grows at a lower rate than the wild type and the athak5line 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 mutantdisplayed 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 resultswere obtained when one of these two systems was impairedeither by selective inhibitors or by gene disruption, confirmingthat AtHAK5 and AKT1 mediated the NH+

4 - and Ba2+ sensitivecomponents of K+ uptake, respectively (Spalding et al. 1999,Santa-Marıa et al. 2000, Rubio et al. 2008, Rubio et al. 2010a).These two inhibitors may be used in other plant species, wheremutants are not available, to study the contribution to K+

uptake of AtHAK5 and AtAKT1 homologs (Nieves-Cordoneset al. 2007, Rubio et al. 2010b).

Above 100 mM K+, other as yet unidentified systems seem tobe involved in K+ uptake in the athak5, atakt1 plants. Thisuptake is not sufficient at 0.5 mM K+, because athak5, atakt1plants displayed lower K+ uptake, biomass and internal K+

concentrations than wild-type plants. Since only the plantspossessing functional AKT1 were similar to wild-type plants,it could be deduced that AKT1 is the most important systemat this concentration. At 10 mM K+, the unidentified systemsprovided sufficient K+ uptake because no deficient phenotypewas observed in athak5, atakt1 double mutants (Rubio et al.2010a).

Candidate systems that could mediate the K+ uptakeobserved in the athak5, atakt1 double mutants could belongto the CHX family (Zhao et al. 2008), the non-selective channelregulated by the cyclic nucleotide-gated channels(CNGCs) family (Li et al. 2005, Demidchik and Maathuis2007, Kaplan et al. 2007) or to the glutamate receptor-likechannel family (GLR) (Dietrich et al. 2010, White and Karley2010).

Within the CHX family, AtCHX13 has been suggested as apossible pathway for root K+ uptake because of its low Km forK+ (136mM) when functionally expressed in yeast (Zhao et al.2008). However, its high sensitivity to Cs+ and Na+ makes theimportant contribution of AtCHX13 to K+ acquisition unlikely,because root K+ uptake does not show such a high sensitivity tothose inhibitors (Rubio et al. 2010b). In addition, a K+ uptakesystem with a 136 mM Km for K+ is not observed in the athak5,atakt1 double mutant (Rubio et al. 2010a), and AtCHX13expression in roots is restricted to the root tip under lowK+ conditions, which makes it difficult to reconcile with rootK+ uptake allowing growth of the athak5, atakt1 mutant athigh external K+.

With regard to CNGCs, AtCNGC10 transports both K+ andNa+ and partially rescues an Arabidopsis akt1 mutant line

(Kaplan et al. 2007). Results obtained with antisense lines ofthis channel, which displayed lower AtCNGC10 expression thanwild-type plants, indicated a role in Na+/K+ homeostasis inroots (Guo et al. 2008). Similar results were obtained forAtCNGC3. A null mutation in this channel altered bothshort-term Na+ influx and K+ uptake at high external K+ con-ditions, also suggesting a role in non-selective monovalentcation uptake at the plasma membrane level (Gobert et al.2006).

Finally, GLR channels could also be considered for rootK+ uptake since several members are expressed in the rootsand, together with CNGCs, are thought to constitutevoltage-independent cation channels in planta (White andKarley 2010). GLRs allow, like CNGCs, non-selective transportof ions, including K+, into root cells. However, cytosolic Ca2+

homeostasis and signaling seem to be the major roles of thesechannels (Demidchik and Maathuis 2007).

Future perspectives

According to the above, more efforts are needed to increase theK+ uptake capacities of crops. One way to obtain plants withimproved traits related to K+ uptake is to exploit naturalvariability. Responses to environmental conditions depend onnumerous genes and are typically controlled by quantitativetrait loci (QTLs). The identification of variants with improvedstress responses and/or vigor requires phenotypic/geneticscreenings capable of distinguishing between plants withdifferent behavior. Many examples can be found in the litera-ture regarding K+ homeostasis, especially under salt stress, andnatural 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 ofnatural accessions will reveal sequence variability and willpermit a faster and easier identification of new interestingvarieties.

On the other hand, recent advances in the identification ofmolecular entities involved in K+ uptake and its regulation, likethose described in the present review, have opened up a newgroup of biotechnological targets to be considered. Now it ispossible to modify the entity of interest directly in a mannerthat improves plant responses. This concept can be put intopractice by following two strategies: (i) altering the amount ofthe protein (quantity) or (ii) improving its activity (quality).As regards the first strategy, transformation of plants with amodified promoter sequence upstream of the gene of interestwould allow changes in the mRNA pool. Strong constitutivepromoters could be used, but cell-specific inducible promotersmay be more efficient. The latter provided better results thanconstitutive overexpression when used with AtHKT1 and salttolerance in Arabidopsis (Moller et al. 2009). Different generegulation 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


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HAK5 transporter of A. thaliana and T. halophila providean example (Aleman et al. 2009b).

With respect to the second strategy, selection of mutatedversions of the transporter with better features (low sensitivityto inhibitors or higher uptake capacity) could be carried out inheterologous systems such as yeast, plant protoplasts orXenopus oocytes before assaying them in the plant. Thiscould be done in combination with the first strategy as well.Improved versions of different K+ transport systems havealready 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 ofPhyscomitrella patens (Garciadeblas et al. 2007) that couldyield 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 membersof the CIPK–CBL pathway that regulates its transport capacity(Xu et al. 2006). By using these and/or other strategies, it istempting to expect that biotechnological approaches couldgive a boost to crop yield in the forthcoming years andtherefore help to compensate for climate change damages.

Funding

This work was funded by Fundacion Seneca of Region deMurcia, Spain [grant No. 08696/PI/08]; the Ministerio deCiencia e Innovacion Spain [grant No. AGL2009-08140].

Acknowledgments

We thank Mario Fon for critically reading the manuscript.

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