Journal of Experimental Botany

JXB Advance Access originally published online on December 19, 2005
Journal of Experimental Botany 2006 57(2):425-436; doi:10.1093/jxb/erj034

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RESEARCH PAPER

Plant responses to potassium deficiencies: a role for potassium transport proteins

M. K. Ashley, M. Grant and A. Grabov^*

Division of Biology, Imperial College London, Wye Campus, Wye, Ashford TN25 5AH, Kent, UK

^* To whom correspondence should be addressed. E-mail: a.grabov{at}imperial.ac.uk

Received 7 July 2005; Accepted 27 October 2005

	Abstract

Top Abstract Potassium availability and... Mechanisms of potassium... Plant responses to low... References

 
The availability of potassium to the plant is highly variable, due to complex soil dynamics, which are strongly influenced by root–soil interactions. A low plant potassium status triggers expression of high affinity K⁺ transporters, up-regulates some K⁺ channels, and activates signalling cascades, some of which are similar to those involved in wounding and other stress responses. The molecules that signal low K⁺ status in plants include reactive oxygen species and phytohormones, such as auxin, ethylene and jasmonic acid. Apart from up-regulation of transport proteins and adjustment of metabolic processes, potassium deprivation triggers developmental responses in roots. All these acclimation strategies enable plants to survive and compete for nutrients in a dynamic environment with a variable availability of potassium.

Key words: Acclimation, mineral nutrition, plant plasticity, potassium, potassium deficiencies

	Potassium availability and nutrient dynamics in the rhizosphere

Top Abstract Potassium availability and... Mechanisms of potassium... Plant responses to low... References

 
Potassium is one of the major nutrients, essential for plant growth and development. Although concentrations of K⁺ in soil solution ([K⁺]_o) are in the range of only 0.1–6 mM (Adams, 1971), plants accumulate large quantities of this element, which constitutes between 2% and 10% of plant dry weight (Leigh and Wyn Jones, 1984; Tisdale et al., 1993). Concentrations of K⁺ in the cytosol are maintained in a narrow range, around 100 mM, which is optimal for the function of cytosolic enzymes. Vacuolar content is more variable, depending on potassium availability and tissue type, and is commonly found to be in the range of 20–200 mM (Leigh and Wyn Jones, 1984; Walker et al., 1996).

Potassium is the fourth most abundant mineral, constituting about 2.5% of the lithosphere. However, actual soil concentrations of this mineral vary widely, ranging from 0.04 to 3% (Sparks and Huang, 1985). In accordance with its availability to plants, soil potassium is ascribed to four different pools: (i) soil solution, (ii) exchangeable K, (iii) fixed K, and (iv) lattice K (Syers, 1998). As plants can only acquire K⁺ from solution, its availability is dependent upon the nutrient dynamics as well as on total K content. The exchange of potassium between different pools in soil is strongly dependent upon the concentration of other macronutrients in the soil solution, for example, nitrate (Yanai et al., 1996). The release of exchangeable K is often slower than the rate of K⁺ acquisition by plants (Sparks and Huang, 1985) and, consequently, K⁺ content in some soils is very low (Pretty and Stangel, 1985; Johnston, 2005). Plant potassium status may further deteriorate in the presence of high levels of other monovalent cations such as Na⁺ and that interfere with potassium uptake (Spalding et al., 1999; Qi and Spalding, 2004; Rus et al., 2004).

Apart from long-term deprivation, plant roots can experience transient shortages of potassium because of spatial heterogeneity and temporal variations in the availability of this nutrient. The main sources of soil heterogeneity are often plant roots themselves, the K⁺ transport activity of which creates zones with elevated or reduced nutrient content.

Contact between a root and nutrient may occur because of (i) root growth into the area where a nutrient is located, and (ii) transport of a nutrient to the root surface through the soil (Jungk and Claassen, 1997). The first process, termed ‘root interception’, constitutes less than 1–2% of total K⁺ uptake because of rapid removal of K⁺ at the root surface (Barber, 1985; Rosolem et al., 2003). The second process, K⁺ translocation through the soil to the root surface, is facilitated by diffusion and mass flow (Barber, 1962). Diffusion is the dominant mechanism of K⁺ delivery to the root surface (Seiffert et al., 1995) and constitutes up to 96% of total soil K⁺ transport (Oliveira et al., 2004). Therefore, K⁺ depletion around the root is the most frequently observed phenomenon associated with plant-evoked soil potassium perturbations. If nutrient delivery by diffusion is always associated with the reduction of K⁺ content in the areas adjacent to the root surface, mass flow may, conversely, result in K⁺ accumulation around the root if transpiration is high (Vetterlein and Jahn, 2004).

Experimentally, development of a depletion profile around individual maize root segments has been demonstrated using ⁸⁶Rb as a potassium tracer (Jungk and Claassen, 1997). These data are consistent with results obtained by Yamaguchi and Tanaka (1990), who demonstrated that roots compete for potassium if half the distance between them is less than 4 mm. Similar results were obtained with flat mats of maize (Zea mays L.), rape (Brassica napus L.), and rice (Oryza sativa L.) roots (Jungk and Claassen, 1997; Hylander et al., 1999; Vetterlein and Jahn, 2004).

Variations in soil density may also affect potassium availability. Soil compaction is associated with higher volumetric water content and therefore tends to facilitate K⁺ transport to the root surface (Kuchenbuch et al., 1986). However, the dense soil may also cause a reduction in the root length and so the higher bulk density does not necessarily result in increased K⁺ accumulation (Seiffert et al., 1995).

The spatial heterogeneities in K⁺ distribution encountered by a root are often superimposed with temporal variations in K⁺ availability, caused by continuously changing soil moisture content. In dry soils, bulk K⁺ content is normally higher, but mass flow and diffusion are restricted (Seiffert et al., 1995; Vetterlein and Jahn, 2004; Kuchenbuch et al., 1986). The negative effects of drought on K⁺ transport in soil are likely to be more significant than increases in [K⁺]_o and therefore these environmental conditions lead to reduced availability of the nutrient (Kuchenbuch et al., 1986; Seiffert et al., 1995; Liebersbach et al., 2004).

	Mechanisms of potassium acquisition

Top Abstract Potassium availability and... Mechanisms of potassium... Plant responses to low... References

 
Following Epstein's pioneering work, the potassium transport system in plants is considered to consist of low- and high-affinity components (Epstein et al., 1961). At the molecular level, these components are conventionally attributed to the activities of channels and transporters, respectively (Maathuis and Sanders, 1994, 1997). Recent findings indicate that functions of the K⁺ transport proteins are quite diverse and, at least in terms of affinity to K⁺, the boundaries between transporters and channels are not clearly defined (Fu and Luan, 1998; Hirsch et al., 1998; Spalding et al., 1999). Channel-mediated transport has been studied in great detail because of the availability of advanced electrophysiological techniques, and the relative ease of expression in heterologous systems. Less information is available on transporters, which are characterized by a lower rate of K⁺ transport.

Channels
Shaker-type channels:
The Shaker-type K⁺ channels KAT1 (Anderson et al., 1992) and AKT1 (Sentenac et al., 1992) were the first K⁺ transporting proteins cloned from plants. Both AKT1 and KAT1 are activated by a more negative membrane potential and are highly selective for potassium. Of these two channels, only AKT1 is expressed in roots and involved directly in arabidopsis (Arabidopsis thaliana (L.) Heynh.) mineral nutrition (Lagarde et al., 1996; Hirsch et al., 1998). Several AKT1 orthologues have been identified in other plant species, for example, SKT1 in potato (Solanum tuberosum L.; Zimmermann et al., 1998), LKT1 in tomato (Lycopersicon esculentum Mill.; Hartje et al., 2000), MKT1 in common ice plant (Mesembryanthemum crystallinum L.; Su et al., 2001), TaAKT1 in wheat (Triticum aestivum L.; Buschmann et al., 2000), and OsAKT1 in rice (Oryza sativa; Golldack et al., 2003).

Physiological characterization of the akt1 knockout (KO) indicated that AKT1 mediates an -insensitive component of the K⁺ uptake system in arabidopsis roots. Surprisingly, this channel facilitates transport within a very broad range of [K⁺]_o including µM concentrations (Hirsch et al., 1998; Spalding et al., 1999). KAT1 is a guard cell-specific channel and is likely to mediate K⁺ fluxes for turgor-dependent regulation of the stomatal aperture (Nakamura et al., 1995). This KAT1 function is probably redundant (Szyroki et al., 2001).

The product of another member of the Shaker gene family, ATKC1, does not form functional ion channels when expressed in a heterologous system, but disruption of this protein affects the biophysical characteristics of the AKT1-mediated inward current in the root hairs (Dreyer et al., 1997; Reintanz et al., 2002). Based on this observation, it has been proposed that ATKC1 and AKT1 are parts of a heteromeric functional channel protein (Reintanz et al., 2002). This hypothesis is supported by two-hybrid testing, confirming a physical interaction between ATKC1 and AKT1 (Pilot et al., 2003).

The GORK member of the Shaker family in arabidopsis is activated by depolarization and is likely to be responsible for a K⁺ efflux during stomatal closure (Ache et al., 2000). The inhibition of GORK by an acidic pH is similar to the earlier reported effect of pH on the guard cell outward rectifier (Blatt and Armstrong, 1993; Grabov and Blatt, 1997). In root hairs, GORK facilitates membrane depolarization and K⁺ release in response to external stimuli (Ivashikina et al., 2001). Similarly to the outward rectifier from broad bean (Vicia faba L.) guard cells (Blatt and Gradmann, 1997), gating of the GORK channel is K⁺-sensitive. Because of this property of the channel, it may function as a potassium sensor (Ache et al., 2000; Ivashikina et al., 2001).

Another Shaker-type channel in arabidopsis, SKOR, is expressed in the root pericycle and stelar parenchyma cells, and is likely to be involved in xylem loading because the homozygous KO skor-1 displays a lower rate of K⁺ translocation from roots to shoots. In accordance with this function, SKOR is activated by membrane depolarization and provides a pathway for K⁺ efflux (Gaymard et al., 1998). It has been demonstrated that SKOR and GORK physically interact and form a functional, heteromeric, outwardly rectifying channel (Dreyer et al., 2004).

AKT2 and AKT3 are differentially initiated transcripts from a single gene (At4g22200). As based on the promoter reporter experiments (AKT2) and in situ hybridization (AKT3) this gene is predominantly expressed in phloem and xylem parenchyma (Marten et al., 1999; Lacombe et al., 2000). Low-level expression of AKT2 was also detected in the leaf lamina (Lacombe et al., 2000). The products of AKT2/AKT3 expression in Xenopus (Xenopus laevis) oocytes and COS cells are characterized as weakly rectifying potassium channels. These properties of AKT2/AKT3 enable bi-directional K⁺ transport, which may be involved in phloem loading and/or unloading (Marten et al., 1999; Lacombe et al., 2000; Deeken et al., 2002). AKT2 has been shown to interact physically with AKT1 and AtKC1 (Pilot et al., 2003).

Two pore channels:
Two-pore channels were cloned first from arabidopsis (AtKCO1 for K⁺ channel, Ca²⁺-activated, outward rectifying 1; Czempinski et al., 1997) and more recently from the rain tree (Samanea saman (Jacq.) Merr.; SPOCK1;, Moshelion et al., 2002) and potato (StKCO1; StKCO1ß; Czempinski et al., 2002). It has recently been demonstrated that some members of the family, for example, AtKCO4 do not function as outward rectifiers and, therefore the family was renamed TPK (Tandem-Pore K⁺, Becker et al., 2004). Among the members of the KCO/TPK family in arabidopsis, AtKCO1 and AtKCO6 demonstrated the strongest expression in roots and leaves (Schonknecht et al., 2002), while AtKCO1-GUS (ß-glucuronidase) expression was detected in mitotically active tissues (Czempinski et al., 2002). The recently characterized member of the family, AtTPK4 (AtKCO4), is expressed predominantly in pollen (Becker et al., 2004). At the subcellular level, AtKCO1 is localized to the vacuolar membrane (Czempinski et al., 2002). By contrast, AtTPK4 functions in the plasma membrane and it is likely that it plays a role in potassium homeostasis and membrane potential regulation in the growing pollen tube (Becker et al., 2004).

Cyclic nucleotide-gated channels:
The structure of cyclic nucleotide-gated channels (CNGC) is similar to that of Shaker-type channels. In contrast to animal CNGC, domains binding cyclic nucleotide (CN) and calmodulin (CaM) overlap in plants (Köhler et al., 1999; Arazi et al., 2000; Köhler and Neuhaus, 2000), enabling cross-talk between CaM and CN signalling (Arazi et al., 2000). Arabidosis AtCNGC1 and AtCNGC4 (HLM1) display equal permeability for Na⁺ and K⁺ (Hua et al., 2003; Balague et al., 2003; Bridges et al., 2005). Remarkably, another member of the family, AtCNGC2, characterized by a unique Ala-Asn-Asp selectivity filter was highly selective for K⁺ over Na⁺ (Leng et al., 2002; Hua et al., 2003). Because of its high K⁺ permeability and the appreciable expression in roots (Talke et al., 2003), AtCNGC2 may be directly involved in K⁺ uptake.

Transporters
HKT family:
Wheat HKT1, which facilitates K⁺/Na⁺ symport, was the first K⁺ transporter to be cloned from plants (Schachtman and Schroeder, 1994; Rubio et al., 1995). Because wheat plants expressing antisense HKT1 DNA were more salt-tolerant than the wild type, it has been concluded that the HKT1 transporter is primarily involved in Na⁺ transport (Laurie et al., 2002). HKT1 orthologues have been isolated from a variety of species (see Horie and Schroeder, 2004, for a recent review). In contrast to the rice genome, which has 9 HKT1 orthologues (Garciadeblas et al., 2003), only one gene related to this transporter has been found in arabidopsis (Maser et al., 2001). Interestingly, the hkt1 mutation in arabidopsis suppresses NaCl hypersensitivity in sos1-1, sos2-1, and sos3-1 mutants (Rus et al., 2001, 2004). Overexpression of AtHKT1 in sos3-1 plants augmented both Na⁺ sensitivity and K⁺ deficiency phenotypes when plants were grown at low [K⁺]_o (Rus et al., 2004). Although it was suggested that AtHKT1 is involved in Na⁺ uptake (Rus et al., 2001), the expression pattern, as well as analysis of salt tolerance and Na⁺ accumulation, in athkt1 mutants indicate that this transporter facilitates Na⁺ recirculation from shoots to roots via the phloem (Maser et al., 2002; Berthomieu et al., 2003).

KT/KUP/HAK family:
The genes of this family are homologous to bacterial KUP (TrkD) potassium transporters. The KUP transporter from E. coli is characterized by a mid-range (0.37 mM) K_M for K⁺ and a similar affinity for Rb⁺ and Cs⁺ (Bossemeyer et al., 1989). There are indications that KUP-mediated transport of potassium in bacteria is coupled to transport of H⁺ (Zakharyan and Trchounian, 2001). Plant KUP transporters were first identified and cloned from arabidopsis (Quintero and Blatt, 1997; Fu and Luan, 1998; Kim et al., 1998) and barley (Hordeum vulgare L.; Santa-Maria et al., 1997). As different groups designated different acronyms such as KT, KUP and HAK to these transporters, they are commonly known as KT/KUP/HAK family.

Barley HvHAK1 is characterized by a K_M=27 µM (Santa-Maria et al., 1997) and probably represents a component of the high affinity K⁺ transport system observed by Epstein et al. (1961). This transporter is assigned to the so-called cluster I, along with, AtHAK5 and OsHAK1, the closest related HvHAK1 orthologues in arabidopsis and rice, respectively (Banuelos et al., 2002; Rubio et al., 2000). Notably, AtHAK5 has been demonstrated to mediate high affinity K⁺ transport in arabidopsis (Gierth et al., 2005). Other arabidopsis genes in cluster I include AtHAK7, AtKT5, and AtKUP12.

The barley transporter HvHAK2 belongs to cluster II and facilitates low affinity transport with a K_M5 mM (Rubio et al., 2000; Senn et al., 2001). Arabidopsis HvHAK2 orthologues include AtKT1/KUP1, AtKT2/KUP2, AtKT3/KUP4, AtKT4/KUP3, AtHAK6, and AtHAK8. The affinity of arabidopsis transporters to K⁺ is less clearly defined. Depending on the expression system, AtKUP1 was referred to as a dual- (Fu and Luan, 1998) or high (Kim et al., 1998) affinity transporter. AtKUP2 was more effective than AtKUP1 in rescuing the growth of E. coli (TK2463) and yeast (W3) strains defective in K uptake transporters (Quintero and Blatt, 1997; Kim et al., 1998).

Transformation with AtKT3/AtKUP4 cDNA enabled growth of the M398 strain of yeast (Saccharomyces cerevisiae) carrying the trk1 mutation on media containing as little as 0.2 mM K⁺, but failed to rescue CY162 (trk1/trk2) lethality at low [K⁺] (Rigas et al., 2001). Disruption of this gene in the trh1 (tiny root hair 1) mutant arrested root hair elongation, caused a reduction in the rate of Rb⁺ uptake (Rigas et al., 2001) and affected root gravitropic behaviour (Vicente-Agullo et al., 2004; Grabov et al., 2005). It was unlikely that the trh1 developmental phenotypes were due to cell potassium shortage, because defects in root gravitropic behaviour and root hair development were observed in external [K⁺]_o as high as 20 mM, while defects in transport were observed across µM ranges of [K⁺]_o. Lower external potassium did not affect root hair growth, but surprisingly, attenuated the root bending phenotype in trh1 and rendered WT roots weakly agravitropic (Vicente-Agullo et al., 2004). Although the root hair phenotype and agravitropic root bending are both due to the defects in epidermal cell development, no promoter–reporter pTRH1-GUS expression was detected in the root epidermis. Instead, the highest level of the promoter–reporter construct expression was observed in the root cap. The latter findings indicated that there were non-cell autonomous effects of the trh1 mutation on epidermal cell development (Vicente-Agullo et al., 2004). Expression patterns of the construct containing a GUS reporter gene cloned under the synthetic auxin responsive element DR5 (DR5-GUS; Ulmasov et al., 1997) and experiments with radiolabelled auxin transport in the trh1 root segments as well as in TRH1 expressing yeast suggested that this transporter is also required for auxin transport (Vicente-Agullo et al., 2004). Therefore, the defects in epidermal development in the trh1 mutant are most likely due to the alteration of auxin fluxes and not because of a reduction in K⁺ supply.

A point mutation in the AtKT2/KUP2 gene also resulted in developmental defects. The cognate mutant was designated shy3-1 (short hypocotyl 3-1) and is characterized by reduced cell size (Elumalai et al., 2002). Although AtKT2/KUP2 does transport potassium (Quintero and Blatt, 1997; Kim et al., 1998), the shy phenotype was probably not due to the potassium deficiency because the single base shy3-1 mutation had no effect on the K⁺ transport properties of the protein, as assessed in E. coli T2463 cells. Moreover, the rate of ⁸⁶Rb⁺ uptake by shy3-1 tissues was not significantly different from the wild type and the total K⁺ accumulation in the shy3-1 seedlings was only marginally lower (Elumalai et al., 2002).

KEA transporters:
KEA is the least studied class of plant transporters. The gene family consists of six members in arabidopsis and was identified through homology to bacterial K⁺/H⁺ antiporters (Maser et al., 2001).

CHX transporters:
In arabidopsis, 38 genes encode proteins homologous to mammalian and bacterial Na⁺/H⁺ exchangers (Maser et al., 2001). 28 of these genes form the Monovalent Cation:Proton Antiporter-2 (CPA2) family, which is also known as CHX (Cation/H⁺ eXchanger). Surprisingly, a member of the family AtCHX17 is involved in K⁺ acquisition and homeostasis rather than Na⁺ transport (Cellier et al., 2004). In accordance with this function, AtCHX17 is expressed in the cortex and epidermis of the mature root.

	Plant responses to low potassium status

Top Abstract Potassium availability and... Mechanisms of potassium... Plant responses to low... References

 
Physiological plasticity and regulation of K⁺ transport proteins in response to K⁺ deficiencies
Regulation of transporters:
Potassium starvation is known to activate K⁺ uptake in plants (Siddiqi and Glass, 1987; Fernando et al., 1990; Shin and Schachtman, 2004). This activation has been conventionally associated with induction of expression of high affinity transporters, and was considered a major mechanism of adaptation to K⁺ starvation.

Indeed, in several independent studies it has been demonstrated that transcription of the AtHAK5 transporter is activated in arabidopsis in response to K⁺ deprivation (Ahn et al., 2004; Armengaud et al., 2004; Hampton et al., 2004; Shin and Schachtman, 2004; Gierth et al., 2005). In some experiments, AtHAK5 was rapidly and transiently activated by potassium starvation at 6 h after onset of the K⁺ deprivation (Shin and Schachtman, 2004), while in others the transcript abundance was significantly increased only after 48 h growth in K⁺-free media, and then remained high over at least the next 5 d (Gierth et al., 2005). Elevated transcription of AtHAK5 was down-regulated by K⁺ re-supply (Armengaud et al., 2004; Gierth et al., 2005). Interestingly, in contrast to the above-cited works, Rubio and coauthors observed a decrease of AtHAK5 transcripts in K⁺-depleted roots (Rubio et al., 2000). One important difference in experimental conditions in which these contrasting outcomes were obtained is the composition of nutrient media. The decrease in AtHAK5 transcript abundance was observed in -rich MS media, when K⁺ was substituted with (Rubio et al., 2000), while activation of the AtHAK5 transcription in roots was found in -free media (Ahn et al., 2004; Armengaud et al., 2004; Gierth et al., 2005). The discrepancy between the results obtained in different media raises an interesting question about the selectivity of a K⁺ sensing system and possible interference of in signalling of K⁺ status.

Analysis of Rb⁺ uptake in K⁺-starved wild type and Athak5 knockouts indicated that the cognate AtHAK5 transporter operates within a high affinity range of concentrations with K_M =14 µM (Gierth et al., 2005). This agrees closely with the K⁺ affinity of the transporter expressed in yeast (K_M=13 µM; Rubio et al., 2000). In accordance with its function in K⁺ uptake, AtHAK5 expression in plants is localized to the epidermis of main and lateral roots, and the stele of main roots (Gierth et al., 2005). Activation of this high affinity transporter in response to K⁺ deprivation is probably a common feature shared between plant families. To date it has been demonstrated that AtHAK5 orthologues are induced by low external potassium in barley (HvHAK1; Santa-Maria et al., 1997), tomato (LeHAK5; Wang et al., 2002), and rice (OsHAK1; Banuelos et al., 2002). However, the significance of AtHAK5 activation for plant mineral nutrition at low [K⁺] has yet to be demonstrated. It is likely that some other KT/KUP/HAK transporters may complement AtHAK5 function, at least under some experimental conditions. Activation of AtKUP3 expression, for instance, has been shown in roots of plants grown for 2–3 weeks on solidified K⁺-depleted media (Kim et al., 1998). Interestingly, these growth conditions lead to a decrease in AtKUP2 transcript abundance (Kim et al., 1998). AtKUP12, another member of the KT/KUP/HAK family, may also play role in acclimation to mineral deficiencies as it was down-regulated in shoots after K⁺ re-supply (Armengaud et al., 2004).

Among the members of the KEA potassium transporter family, KEA5 has been shown to be transiently induced after 6 h of K⁺ deprivation (Shin and Schachtman, 2004). As localization of this transporter and its role in K⁺ transport is not known, it is difficult to assess the contribution of KEA5 in plant acclimation to potassium deficiencies.

Transcription of AtCHX17, the member of the CHX family involved in K⁺ acquisition and homeostasis was induced by K⁺ starvation in arabidopsis (Cellier et al., 2004).

Regulation of channels:
Electrophysiological experiments indicated activation of inwardly rectifying 5 pS K⁺ channels in the arabidopsis root plasma membrane in response to low (100 µM) potassium (Maathuis and Sanders, 1995). These changes in channel activity were parallelled by an increased rate of Rb⁺ uptake in K⁺-starved plants. Hirsch et al. (1998) also demonstrated that the inwardly rectifying AKT1 channel provides a major pathway for potassium acquisition, even if the nutrient is available in the µM range of concentrations. At low [K⁺]_o however, disruption of the AKT1 gene affected plant growth only in media containing (Hirsch et al., 1998; Spalding et al., 1999). The contribution of AKT1 to K⁺ transport from media with 25 and 50 µM concentrations of this cation has been shown in Rb⁺-uptake experiments with K⁺-starved akt1-1 and wild-type plants, but due to the complex uptake kinetics, these results could not be unequivocally extended to the whole µM range of K⁺ concentrations (Gierth et al., 2005).

In arabidopsis, activation of AKT1 by low [K⁺]_o probably occurs post-transcriptionally because neither RNA blot nor microarray experiments revealed an alteration in AKT1 transcription in K⁺-starved plants (Pilot et al., 2003; Maathuis et al., 2003; Hampton et al., 2004). Similarly, no transcriptional activation of AKT1 orthologues was detected in rape (Lagarde et al., 1996). It has been demonstrated that AKT1 can form heteromeric complexes with AtKC1 (Reintanz et al., 2002; Pilot et al., 2003), and the recent discovery that AtKC1 is transiently activated by K⁺ starvation in arabidopsis (Shin and Schachtman, 2004) indicates an intriguing possibility that AKT1 may be activated through an interaction with AtKC1.

K⁺ starvation has also been shown to enhance an inwardly rectifying current across the root cell plasma membrane in wheat. In contrast to arabidopsis, the induced current was associated with increased transcription of TaAKT1 (Buschmann et al., 2000).

Potassium starvation down-regulated transcription of SKOR and AKT2 in arabidopsis (Maathuis et al., 2003; Pilot et al., 2003). As these channels are involved in long-distance transport, it has been suggested that their reduced expression at low [K⁺]_o is required to restrict recirculation of K⁺ between the tissues and organs. Alterations in the long-distance transport of K⁺ may also be important for the communication of potassium status between shoots and roots (Pilot et al., 2003).

The major K⁺-transport proteins involved in K⁺ acquisition, homeostasis, and responses to K⁺ deficiencies in arabidopsis are listed in Table 1.

View this table: [in this window] [in a new window]   Table 1. The major K+ transport proteins putatively involved in responses to potassium deficiencies in arabidopsis roots

 
Signalling cascades regulating responses to potassium deficiencies
Signalling of K⁺ deficiencies in bacteria:
Although plant responses to potassium deficiencies are well documented at the physiological and transcriptional levels, the regulatory mechanisms underlying these changes are still obscure. The K⁺-dependent signalling cascades have been studied in detail in bacterial cells, where it has been demonstrated that K⁺-limiting conditions trigger autophosphorylation of the KdpD sensor kinase and subsequent transfer of a phosphoryl group to the KdpE cytosolic response regulator. Binding of phosphorylated KdpE to the promoter of the kdpFABC operon, triggers expression of the KdpFABC high-affinity transport system (Heermann et al., 2003). No similar signalling cascade has so far been identified in plants, although it is known that histidine kinases regulate a variety of responses in plant cells.

AAA-ATPase-related proteins:
Screening of a mouse macrophage cDNA library for suppression of the trk1 phenotype in the potassium uptake-deficient yeast strain CY162, identified the SKD1 (Suppressor of K⁺ Transport Growth Defect) gene (Perier et al., 1994). SKD1 belongs to the AAA-ATPase family and is involved in membrane transport through endosomes and lysosomes (Fujita et al., 2004). Expression of the ice plant SKD1 orthologue (mcSKD1) has been shown to be induced by salt stress, while in high [K⁺]_o medium transcription of this gene was reduced (Jou et al., 2004). As with its mammalian counterpart, mcSKD1 was able to complement potassium transport deficiency in yeast Trk^– mutants. Elevated expression of the SKD1 orthologue was also observed in tomato plants in response to K or Fe deprivation (Wang et al., 2002). Another gene belonging to the AAA-ATPase class, At1g43910, was up-regulated 6-fold in arabidopsis plants subjected to K⁺ starvation for 7 d (Hampton et al., 2004). The role of the SKD1 protein in membrane trafficking in mammals and yeast implies that its function in plants might be associated with protein sorting/targeting in response to salt stress and K⁺ deficiencies (Jou et al., 2004). This hypothesis, albeit plausible, requires further experimental confirmation.

Jasmonic acid (JA) and related signalling cacades:
Some components of signalling cascades regulating responses to K⁺ deficiencies are similar to those involved in stress responses to wounding and insect and pathogen attacks, in which JA and derivatives have been demonstrated to play a prominent role (Howe, 2004; Pozo et al., 2004; Rayko and Ian, 2004). Iterative group analyses of the arabidopsis transcriptome in K⁺-deprived plants and K⁺-starved plants resupplied with potassium, revealed that genes related to JA metabolism and signalling form the largest group affected by these conditions (Armengaud et al., 2004). A subgroup of genes involved in polyamine metabolism was also included in the group of JA-related genes (Armengaud et al., 2004). Transcripts for Arg decarboxylase, AtADC2, involved in putrescine biosynthesis, were the most strongly induced in this subgroup. In agreement with earlier data (Watson and Malmberg, 1996), no changes in the abundance of the AtADC1 transcript were detected. These results suggest the increases in putrescine content demonstrated in K⁺-starved plants (Watson and Malmberg, 1996) are probably due to the activity of the AtADC2 Arg decarboxylase isoform. Polyamines efficiently block a variety of ion channels (Bruggemann et al., 1998; Dobrovinskaya et al., 1999; Guo and Lu, 2000), including inwardly rectifying AtKAT1 (Liu et al., 2000), but it is not yet clear if these physiological effects of polyamines are important for plant acclimation to stress conditions. One can speculate, however, that reduced permeability of ion channels during potassium deprivation may be required for the reallocation of K⁺ between the different storage pools.

Reactive oxygen species (ROS):
Shin and Schachtman (2004) recently demonstrated that ROS are of primary significance for the regulation of plant responses to K⁺ deprivation. An induction of the high affinity K⁺ transport component by K⁺ deprivation was accompanied by 2-fold increases in H₂O₂ production. The ROS signal is non-redundant and enables activation of the high affinity K⁺ uptake component even in the K⁺-sufficient plants. Expression of the RHD2 gene was up-regulated in K⁺-deficient plants, indicating involvement of this NADPH oxidase (Foreman et al., 2003) in production of H₂O₂ in response to K⁺ deprivation. This has been confirmed in experiments with an rhd2 knockout line, where no induction of HAK5 and KEA5 potassium transporters was observed in K⁺-deprived plants (Shin and Schachtman, 2004).

Ethylene:
Both activation of JA-related genes and ROS production indicate some overlap between the cascades that signal conditions of K⁺-deficiencies, and wounding. These parallels are enhanced by an observation that K⁺ deprivation of arabidopsis plants induces strong expression of genes related to ethylene biosynthesis and signalling and, in addition, an orthologue to a tomato wound-inducible gene, At4g10270 (Shin and Schachtman, 2004). Ethylene, alongside JA is known to play an important role in wounding responses (Devoto and Turner, 2003). The role of ethylene signalling in K⁺ deficiency stress was confirmed by direct measurements of the amount of ethylene released into the atmosphere by K⁺-deficient and K⁺-sufficient plants. In these experiments, K⁺ starvation caused an almost 2-fold increase in production of this phytohormone (Shin and Schachtman, 2004).

Auxin:
Auxin has been shown to control expression of the inwardly rectifying ZMK1 channel in maize (Philippar et al., 1999). The increased abundance of the ZMK1 transcripts after addition of auxin was paralleled by increases in K⁺ channel density, detected electrophysiologically in maize coleoptile protoplasts (Philippar et al., 1999; Thiel and Weise, 1999). The ZMK1 channel, which is highly homologous to arabidopsis AKT1, may play a role in maize mineral nutrition, but this hypothesis has yet to be confirmed experimentally.

Further evidence for a role of auxin-dependent processes in acclimation to K⁺ deficiencies was provided by the demonstration that the CYP79B2 and CYP79B3 genes involved in the Trp-dependent auxin biosynthesis were down-regulated upon K⁺ resupply to K⁺-starved roots (Armengaud et al., 2004).

Misexpression of the auxin-dependent DR5-GUS construct (Ulmasov et al., 1997) indicated auxin accumulation in the central cylinder of the roots of K⁺-deficient plants (Vicente-Agullo et al., 2004). The perturbations in the auxin profile in these experiments are probably due to alterations in auxin transport, resulting from potassium deprivation. The auxin profile of the K⁺-starved plants was reminiscent of those found in trh1 K⁺-sufficient plants in which the TRH1(AtKUP4/AtKT3) potassium transporter was disrupted.

Although the trh1 mutation does affect K⁺ transport under some experimental conditions (Rigas et al., 2001), it has been shown that TRH1 is also required for auxin efflux in root cap cells (Vicente-Agullo et al., 2004). Three putative mechanisms may be associated with TRH1 involvement in the transport of auxin. (i) TRH1 can generate ionic and electrical gradients that favour phytohormone efflux. (ii) Transport of potassium can be directly coupled to transport of phytohormones, similarly to K⁺/Na⁺-coupled transport of neurotransmitters (Kanner et al., 2001). (iii) TRH1 may transport auxin independently of potassium. The plausibility of the hypothesis that a cation transporter may facilitate uncoupled transport of anion is supported by recent data by Kuroda et al. (2004). These authors found that major yeast Trk potassium transporters also function as anion channels (Kuroda et al., 2004).

Morphological plasticity and K⁺ availability
Apart from induction of physiological responses, the variations in mineral nutrient availability often evoke some alterations in root architecture. In barley and many other plants, low phosphorus, nitrogen or potassium supply resulted in a reduction of total lateral root length (Drew, 1975). In soils with non-uniform distribution of mineral nutrients, localized extension of lateral roots in barley was triggered in patches rich in phosphate and nitrogen (Drew, 1975). By contrast, K⁺-rich patches in these experiments induced a global response and accelerated the growth of laterals even in those root segments that were exposed to low potassium concentrations. These experimental data indicate that the localized [K⁺]_o increases evoke systemic signals responsible for global lateral root proliferation. The observed pattern of morphological responses may also be associated with the high mobility of K⁺ in the plant body (Hodge, 2004, and references therein).

Similarly to barley (Drew, 1975), potassium deficiencies arrest lateral root development in arabidopsis (Shin and Schachtman, 2004; Armengaud et al., 2004). Increased levels of ethylene may be responsible for the inhibition of lateral root development observed in the K⁺-starved plants (Shin and Schachtman, 2004), but this developmental response was not necessarily accompanied by the activation of genes related to ethylene metabolism and signalling (Armengaud et al., 2004). The fact that auxin is important for the development of lateral roots indicates that this phytohormone may also be involved in signalling of nutrient availability. Experimental data on the role of this phytohormone in nitrogen- and phosphate-dependent root plasticity are, however, rather contradictory (Bates and Lynch, 1996; Zhang et al., 1999; Linkohr et al., 2002).

Growth and development of root hairs is controlled by the availability of phosphate, nitrate, and iron (see Forde and Lorenzo, 2001, for a review), but potassium in physiologically relevant concentrations has no effect on these developmental processes in the epidermis of arabidopsis (Desbrosses et al., 2003).

One important mechanism of acclimation to phosphate deficiencies in common bean (Phaseolus vulgaris L.), soybean (Glycine max (L.) Merr.), and pea (Pisum sativum L.) is associated with reduction of the gravitropic set-point angle (GSA) in basal roots (Bonser et al., 1996). As a result, at low phosphorus availability the root system is more shallow and enables more efficient exploration of upper soil layers, normally containing higher levels of this nutrient. Changes in root gravitropic behaviour were also observed in low potassium media in arabidopsis (Vicente-Agullo et al., 2004; Fig. 1). In these experiments, wild-type arabidopsis plants (Fig. 1A, C) and trh1 mutants (Fig. 1B, D) grown on standard Murashige–Skoog medium for 3 d, were transferred for a further 3 d growth on media containing either 20 (Fig. 1A, B) or 0.1 mM (Fig. 1C, D) of potassium. As the section on the KUP/HAK/KT family indicated, disruption of the TRH1 (AtKUP4/AtKT3) potassium transporter affected root gravitropic behaviour in high potassium concentrations (Fig. 1B). Surprisingly, reduced potassium availability triggered agravitropic root growth in the WT plants. This reaction to the low K⁺ status may be important for mineral acquisition in soils where K⁺ distribution is heterogeneous. The deviation from gravitropic growth, probably enables the root to escape from low [K⁺]_o soil patches and potentiates exploration of areas with higher nutrient content (Vicente-Agullo et al., 2004). In stark contrast to WT, in trh1 mutants, the reduction of external [K⁺]_o attenuated root agravitropic behaviour. This difference in the effects of K⁺ deprivation on the gravitropic behaviour of WT and trh1 roots suggest that the TRH1 potassium transporter plays a pivotal role in these responses and regulates them through K⁺-dependent phytohormone distribution in the root tip (Vicente-Agullo et al., 2004).

View larger version (12K): [in this window] [in a new window]   Fig. 1. Gravitropic behaviour of roots of wild-type and trh1 plants grown on vertical agarose plates containing different concentrations of K+. Wild-type Arabidopsis plants (A, C) and trh1 mutants (B, D) were grown on the standard Murashige–Skoog medium for 3 d, after which they were transferred for a further 3 d growth on media containing either 20 (A, B) or 0.1 mM (C, D) of potassium as described in Vicente-Agullo et al. (2004). The deviation from the gravitropic growth in low [K+] medium may enable the root to escape from low nutrient patches in soil. The TRH1 transporter is pivotal for the K+-dependent gravitropic behaviour because the trh1 mutant displays a different pattern of responses.

 
In conclusion, growing roots continuously experience variations in potassium availability, to which they have to adjust their physiology and growth pattern. In order to optimize their performance as nutrient uptake organs, and to compete for K⁺ uptake in the dynamic and heterogeneous environment, plant roots developed mechanisms of acclimation to the current K⁺ status in the rhizosphere. Moreover, emerging evidence showing changes in expression of transcripts encoding K⁺ transporters and channels in response to ROS and phytohormones, provide the intriguing possibility that K⁺ may play a more specific regulatory role in plant stress responses.

	Acknowledgements

 
The authors thank the Biotechnology and Biological Sciences Research Council and the Society for Experimental Biology for their support.

	References

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