**3.1 Potassium deficiency and its effects on plants**

Potassium is the second (after nitrogen) most abundant mineral element in plants [2]. It is the main cation (K+ ) in plant cells [77] and is essential for plant growth and adaptation to the environment [78]. In contrast to nitrogen, potassium is not involved in metabolism and remains in ionic form to execute its specific functions in plant cells [79]. Potassium is associated with or directly involved in several physiological processes supporting plant growth and development—photosynthesis, protein and starch biosynthesis; transport of sugars and nutrients; and stomatal closure [77, 80]. Moreover, K+ was shown to be essential in the activation of 50–60 key enzymes, involved in critical metabolic processes [81, 82], including photosynthesis, oxidative metabolism and protein synthesis [2]. Thus, this cation might be involved in the regulation of metabolite patterns and their relative abundances in higher plants [83].

As mentioned above, the lack of potassium might suppress various enzymatic activities [81, 82], but this can occur only when potassium cytosolic contents decrease due to prolonged K deficiency [81]. Hence, cytosolic K<sup>+</sup> homeostasis is crucial for the central cell metabolism [84], plant growth and adaptation to the environment and must, therefore, be finely controlled [78]. In addition, K+ plays a crucial role in the establishment of cell turgor and osmoregulation, neutralization/ scavenging of anions (e.g. those of organic and inorganic acids), control of cytosolic pH, ion homeostasis and electrical membrane potential [77, 78, 83, 85].

Potassium availability in soil is the main factor, affecting supply of terrestrial plants with this element. Indeed, although potassium is the seventh most abundant element in the Earth crust [86], only a small part of the whole soil potassium pool is present in a form readily available for plants, whereas most of the soil potassium constitutes hardly soluble minerals [87]. Thus, due to the low rates of their solubilization, the concentration of biologically available K<sup>+</sup> in soil solution is rather low and varies between 0.1 and 1.0 mmol/L [82, 88]. Moreover, due to a rapid local depletion at the root surface, in reality these values can be even lower, and supply of the plant with potassium is highly dependent on the rates of its liberation from minerals and transport in soil solution [89]. Both rates are typically relatively slow: growing plants can deplete soil solution to yield potassium concentrations between 1 and 2 μmol/L. On the other hand, this might result in enhancement of potassium release and mobilization in soil [89]. Obviously, the amounts of soil water (i.e. soil water contents) essentially affect the gradients of potassium concentrations on the root surface. Thus, diffusion of K+ is essentially restricted in dry soil but is significantly increased upon re-supplementation of soil with water [89].

According to the available literature data, under sufficient nutritional supply, the average potassium contents in the most of the plant species vary between 4 and 8% (w/w) in dry matter [84]. However, for multiple other species, the optimal potassium contents are essentially lower and lie in the range of 0.5–2.0% (w/w) [80]. Thus, a comparative study of potassium contents in 14 hydroponically grown plant species (1 mmol/L K+ in the nutritional solution) revealed potassium contents in the range of 153–274 mmol/kg fresh weight with a drop to 15–53 mmol/kg under a 1000-fold lower potassium supply (1 μmol/L) [90].

In most arable fields, potassium deficiency becomes a limiting factor for sustainable plant growth and development [91]. Therefore, the effects of potassium deficiency on crop plants are intensively studied under hydroponic conditions, which allow reliable defining precise potassium concentrations in nutrient solutions [92]. These experiments revealed the major visual symptoms of potassium deficiency as brown scorching and curling of leaf tips, as well as interveinal chlorosis caused by early chlorophyll degradation induced by ROS generation [92]. At the metabolic level, potassium deficit leads to the accumulation of carbohydrates (mainly sucrose) in leaves [8]. Most likely, this disaccharide plays the role of an osmoprotector, maintaining cell turgor under stressed conditions in plants [6], although some researchers attribute this effect to the enhancement of sucrose export from K+ deficient leaves [8]. Importantly, in contrast to the conditions of nitrogen deprivation, potassium starvation does not result in any increase of root biomass in terms of an acclimation response to the restriction of potassium supply.

#### **3.2 Regulation of K<sup>+</sup> transport systems and mobilization of vacuolar K+ pools in plant responses to potassium deficiency**

As was unambiguously proven by various analytical techniques, potassium is unequally distributed between different cell compartments, strongly dominating in cytosol and vacuole [80]. Thereby, cytosol and vacuole act as the major depots of potassium in plant cells [93]. This fact is essential for understanding the role of the ion homeostasis system in the mechanisms, underlying cell responses to potassium deficiency. Thus, in barley, the concentrations (activities) of K+ in cytosol of both root and leaf cells measured with triple-barrelled microelectrodes (recording K<sup>+</sup> activity, pH and membrane potential) typically lie in the range of 100–200 mmol/L [93, 94]. Other methods, like K<sup>+</sup> efflux analysis, X-ray microanalysis or application of fluorescent dyes (reviewed by Britto and Kronzucker [95]) showed a larger range of values (30–320 mmol/L) which was probably due to a strong variation in the supply of potassium in cited experiments. Importantly, in cytosol, K+ cannot be replaced by other cations, for example, Na<sup>+</sup> [78], that is, it is a specific cytosolic cation. In contrast to the cytosolic pool, the concentration of vacuolar potassium can vary between 10 and 500 mmol/L (i.e. 50-fold), depending on the plant species, cell type and potassium availability in soil [2, 80]. For example, in most glycophytes, it is ranging from approximately 120 mmol/L in root cell vacuoles [93] to 230 mmol/L in the vacuoles of leaf mesophyll cells [94]. In contrast to the cytosol, vacuolar K+ can be, at least to some extent, replaced by other osmotica (i.e. sucrose, Na<sup>+</sup> or Mg2+) [70, 96]. Vacuolar potassium contents are in a good agreement with the K+ concentrations in the apoplast, which vary between 10 and 200 mmol/L, sometimes reaching up to 500 mmol/L [83, 97].

The responses of vacuolar and cytosolic K<sup>+</sup> pools to potassium deficiency were intensively studied since the 1980s, when the depletion of vacuolar K+ , accompanied by the accumulation of replacing cations (Na+ and Mg2+) in the vacuole, was proposed to be the earliest response of the plant cell to potassium starvation [80]. Remarkably, these alterations were not accompanied with significant changes in cytosolic potassium levels, that is, K<sup>+</sup> -dependent processes in cytosol remain mostly unaffected. Further, it was proposed that the vacuolar potassium pool can be depleted only to a certain minimal value (10–20 mmol/L) [80]. However, subsequent determination of potassium contents in barley, relying on the measurements with triple-barrelled microelectrodes and a 14-day exposure of plants to 2 μmol/L K+ in nutrient solution, revealed quite different responses of the vacuolar and cytosolic potassium pools in two types of root cells [93]. On the one hand, potassium concentrations (expressed as activities) demonstrated a concerted

**69**

*Ion Homeostasis Response to Nutrient-Deficiency Stress in Plants*

cortical cells (from 83 to only 67 mmol/L) [93, 98].

vacuole to the cytosol which might rely on a 1:1 H+

of K+

mal cells [93].

two decades [77, 78, 84, 99–104].

and (iii) high-affinity K+

*Arabidopsis thaliana* K+

transporter 1 (AKT1), K+

to fast and fine adjustments in K+

channel, which prevents AKT1-mediated K+

high-affinity K+

whereas stellar K+

(GORK) K+

of K+

key K+

soil K+

the phloem K+

sources to sinks [78].

K+

to explain this phenomenon in cells severely depleted in K+

influx into the cytosol via the high-affinity K<sup>+</sup>

explained by higher potassium losses via outward-rectifying K+

elements of the potassium transport network were identified as K<sup>+</sup>

families of plant potassium transport systems are (i) Shaker K+

represented by voltage-gated channels; (ii) the tandem-pore K+

uptake/K+

and mediate potassium release [78, 99, 103]. Finally, *Arabidopsis* K+

transporters [103]. Among the Shaker K+

channel 1 (AtKC1) are K+

Thus, in Arabidopsis, seven major families of K+

/K+

existence of an active transport mechanism for the translocation of K<sup>+</sup>

decrease in the vacuole and cytosol from 122 to 124 mmol/L to 10 and 18 mmol/L, respectively. On the other hand, cytosolic concentrations in general showed less of a decline, more pronounced, however, in epidermal (from 81 to 45 mmol/L) than the

Thermodynamic calculations of the cellular potassium homeostasis, performed

to take into account that cortical cells might have a higher capacity for the activation

It is well known that cytosolic potassium homeostasis relies on the activities of multiple transport mechanisms, localized in cellular and organelle membranes [75]. The sophisticated network of potassium transport systems, involved in potassium absorption by roots, transport to shoots and further allocation within organs and cells, is the result of millions years of evolution of terrestrial plants [84]. Multiple

transporters and their regulators, comprehensively characterized during the last

prising in total 75 genes, are known [78, 84]. The most studied and well-characterized

They are activated by membrane hyperpolarization and mediate potassium uptake,

AKT2/3 is a weakly rectifying channel, switching from an inwardly rectifying to a non-rectifying state, mediating both potassium uptake and release depending on the local potassium electrochemical gradient [99, 103]. The Shaker channels are present in all plant organs [102] and ubiquitously expressed in various tissues. Being the main contributors in the potassium membrane fluxes [100, 101], they give access

 between distinct plant sections and cellular compartments to match plant demands under challenging environmental conditions [84]. AKT1, expressed predominantly in root epidermal cells [88], has been identified in Arabidopsis as a

hairs [106], is thought to be rather a regulatory subunit that does not form an own functional channel but interacts with AKT1 to form a functional heterotetrameric

tions [107]. It was shown that SKOR mediates the transfer of potassium to xylem sap for further transport to shoots [78]. Analogously, AKT2 substantially contributes to

channel protein, involved in potassium uptake under low (nearly 10 μmol/L)

concentration [105]. The AtKC1, expressed in root cortex, epidermis and root

loading and unloading for long-distance potassium transport from

mostly associated with root cortical cells [16]. This might result in a higher ability of cortical cells to maintain a suitable potassium cytosolic concentration under nutrient starvation conditions. On the other hand, the observed difference can be

:K+

, clearly indicated the

symport [93]. One also needs

transporter HKT1, which is

from the

channels in epider-

channels,

channels and transporters, com-

transporter (KUP/HAK/KT) family of

transport in plant cells and for the redistribution

loss under potassium starvation condi-

Arabidopsis transporters 1 and 2 (KAT1, KAT2) and

outward-rectifying (SKOR) and guard cell outward-rectifying

channels form Kout channels activated by membrane depolarization

channel family,

channels, Arabidopsis

inwardly rectifying (Kin) channels.

(TPK) channels;

transporter

*DOI: http://dx.doi.org/10.5772/intechopen.89398*

*Cell Growth*

**3.2 Regulation of K<sup>+</sup>**

[93, 94]. Other methods, like K<sup>+</sup>

replaced by other cations, for example, Na<sup>+</sup>

reaching up to 500 mmol/L [83, 97].

in cytosolic potassium levels, that is, K<sup>+</sup>

The responses of vacuolar and cytosolic K<sup>+</sup>

nied by the accumulation of replacing cations (Na+

In most arable fields, potassium deficiency becomes a limiting factor for sustainable plant growth and development [91]. Therefore, the effects of potassium deficiency on crop plants are intensively studied under hydroponic conditions, which allow reliable defining precise potassium concentrations in nutrient solutions [92]. These experiments revealed the major visual symptoms of potassium deficiency as brown scorching and curling of leaf tips, as well as interveinal chlorosis caused by early chlorophyll degradation induced by ROS generation [92]. At the metabolic level, potassium deficit leads to the accumulation of carbohydrates (mainly sucrose) in leaves [8]. Most likely, this disaccharide plays the role of an osmoprotector, maintaining cell turgor under stressed conditions in plants [6], although some researchers attribute this effect to the enhancement of sucrose export from K+

deficient leaves [8]. Importantly, in contrast to the conditions of nitrogen deprivation, potassium starvation does not result in any increase of root biomass in terms

As was unambiguously proven by various analytical techniques, potassium is unequally distributed between different cell compartments, strongly dominating in cytosol and vacuole [80]. Thereby, cytosol and vacuole act as the major depots of potassium in plant cells [93]. This fact is essential for understanding the role of the ion homeostasis system in the mechanisms, underlying cell responses to potassium

root and leaf cells measured with triple-barrelled microelectrodes (recording K+ activity, pH and membrane potential) typically lie in the range of 100–200 mmol/L

tion of fluorescent dyes (reviewed by Britto and Kronzucker [95]) showed a larger range of values (30–320 mmol/L) which was probably due to a strong variation in

ion. In contrast to the cytosolic pool, the concentration of vacuolar potassium can vary between 10 and 500 mmol/L (i.e. 50-fold), depending on the plant species, cell type and potassium availability in soil [2, 80]. For example, in most glycophytes, it is ranging from approximately 120 mmol/L in root cell vacuoles [93] to 230 mmol/L in the vacuoles of leaf mesophyll cells [94]. In contrast to the cytosol, vacuolar

can be, at least to some extent, replaced by other osmotica (i.e. sucrose, Na+

Mg2+) [70, 96]. Vacuolar potassium contents are in a good agreement with the K+ concentrations in the apoplast, which vary between 10 and 200 mmol/L, sometimes

proposed to be the earliest response of the plant cell to potassium starvation [80]. Remarkably, these alterations were not accompanied with significant changes

in nutrient solution, revealed quite different responses of the vacuolar

mostly unaffected. Further, it was proposed that the vacuolar potassium pool can be depleted only to a certain minimal value (10–20 mmol/L) [80]. However, subsequent determination of potassium contents in barley, relying on the measurements with triple-barrelled microelectrodes and a 14-day exposure of plants to

and cytosolic potassium pools in two types of root cells [93]. On the one hand, potassium concentrations (expressed as activities) demonstrated a concerted

intensively studied since the 1980s, when the depletion of vacuolar K+

the supply of potassium in cited experiments. Importantly, in cytosol, K+

 **transport systems and mobilization of vacuolar K+**

efflux analysis, X-ray microanalysis or applica-

[78], that is, it is a specific cytosolic cat-

pools to potassium deficiency were


and Mg2+) in the vacuole, was

of an acclimation response to the restriction of potassium supply.

deficiency. Thus, in barley, the concentrations (activities) of K+

**in plant responses to potassium deficiency**


 **pools** 

cannot be

or

, accompa-

in cytosol of both

**68**

2 μmol/L K+

K+

decrease in the vacuole and cytosol from 122 to 124 mmol/L to 10 and 18 mmol/L, respectively. On the other hand, cytosolic concentrations in general showed less of a decline, more pronounced, however, in epidermal (from 81 to 45 mmol/L) than the cortical cells (from 83 to only 67 mmol/L) [93, 98].

Thermodynamic calculations of the cellular potassium homeostasis, performed to explain this phenomenon in cells severely depleted in K+ , clearly indicated the existence of an active transport mechanism for the translocation of K<sup>+</sup> from the vacuole to the cytosol which might rely on a 1:1 H+ :K+ symport [93]. One also needs to take into account that cortical cells might have a higher capacity for the activation of K+ influx into the cytosol via the high-affinity K<sup>+</sup> transporter HKT1, which is mostly associated with root cortical cells [16]. This might result in a higher ability of cortical cells to maintain a suitable potassium cytosolic concentration under nutrient starvation conditions. On the other hand, the observed difference can be explained by higher potassium losses via outward-rectifying K+ channels in epidermal cells [93].

It is well known that cytosolic potassium homeostasis relies on the activities of multiple transport mechanisms, localized in cellular and organelle membranes [75]. The sophisticated network of potassium transport systems, involved in potassium absorption by roots, transport to shoots and further allocation within organs and cells, is the result of millions years of evolution of terrestrial plants [84]. Multiple elements of the potassium transport network were identified as K<sup>+</sup> channels, transporters and their regulators, comprehensively characterized during the last two decades [77, 78, 84, 99–104].

Thus, in Arabidopsis, seven major families of K+ channels and transporters, comprising in total 75 genes, are known [78, 84]. The most studied and well-characterized families of plant potassium transport systems are (i) Shaker K+ channel family, represented by voltage-gated channels; (ii) the tandem-pore K+ (TPK) channels; and (iii) high-affinity K+ /K+ uptake/K+ transporter (KUP/HAK/KT) family of high-affinity K+ transporters [103]. Among the Shaker K+ channels, Arabidopsis K+ transporter 1 (AKT1), K+ Arabidopsis transporters 1 and 2 (KAT1, KAT2) and *Arabidopsis thaliana* K+ channel 1 (AtKC1) are K+ inwardly rectifying (Kin) channels. They are activated by membrane hyperpolarization and mediate potassium uptake, whereas stellar K+ outward-rectifying (SKOR) and guard cell outward-rectifying (GORK) K+ channels form Kout channels activated by membrane depolarization and mediate potassium release [78, 99, 103]. Finally, *Arabidopsis* K+ transporter AKT2/3 is a weakly rectifying channel, switching from an inwardly rectifying to a non-rectifying state, mediating both potassium uptake and release depending on the local potassium electrochemical gradient [99, 103]. The Shaker channels are present in all plant organs [102] and ubiquitously expressed in various tissues. Being the main contributors in the potassium membrane fluxes [100, 101], they give access to fast and fine adjustments in K+ transport in plant cells and for the redistribution of K+ between distinct plant sections and cellular compartments to match plant demands under challenging environmental conditions [84]. AKT1, expressed predominantly in root epidermal cells [88], has been identified in Arabidopsis as a key K+ channel protein, involved in potassium uptake under low (nearly 10 μmol/L) soil K+ concentration [105]. The AtKC1, expressed in root cortex, epidermis and root hairs [106], is thought to be rather a regulatory subunit that does not form an own functional channel but interacts with AKT1 to form a functional heterotetrameric channel, which prevents AKT1-mediated K+ loss under potassium starvation conditions [107]. It was shown that SKOR mediates the transfer of potassium to xylem sap for further transport to shoots [78]. Analogously, AKT2 substantially contributes to the phloem K+ loading and unloading for long-distance potassium transport from sources to sinks [78].

The biological roles of the plant TPK K+ -selective channels are much less understood than those of the Shakers [78]. The representatives of the TPK family differ by their intracellular localization, while TPK4 is targeted to the plasma membrane; the other family members—TPK1, 2, 3 and 5—are located in organelle membranes [108]. Among them, due to its high selectivity, TPK1 appears to be mostly involved in the response to K+ deficiency [109]. This protein is ubiquitously expressed in the tonoplast of guard and mesophyll cells and seems to impact on the vacuolar release of K+ and on intracellular K<sup>+</sup> homeostasis [110].

The high-affinity K<sup>+</sup> transporters from the KUP/HAK/KT family are directly involved in maintaining the constant influx of K+ in plant roots under severe potassium deficiency [78, 102]. The best characterized transporters of this group are AtHAK5 from Arabidopsis and its homologs in other species, which are assumed to be involved in K<sup>+</sup> uptake from very dilute potassium soil solutions, in co-transport with protons [103, 111, 112]. Besides this, AtKUP1 is described as a dual-affinity transporter in the plasma membrane of root cells and assumed to be essential in K+ uptake [113], whereas AtKUP 2, 4, 6 and 8 are supposed to mediate K+ efflux in root cells [78]. Similarly to HAK5, its homologs in other plant species (rice, barley, pepper, tomato) are highly up-regulated by potassium starvation [103]. It is generally recognized that HAK5 and AKT1 are the two main players in K+ uptake from the soils, characterized with potassium shortage [102, 114, 115]. Indeed, the studies with T-DNA insertion lines clearly demonstrated that AtHAK5 is the only system mediating K+ uptake at external potassium concentrations below 10 μmol/L [116], whereas both AtHAK5 and AKT1 systems contribute to K+ absorption, when potassium concentrations are in the range of 10–200 μmol/L [117]. In particular, the uptake of K+ in AtHAK5 AKT1 double mutant plants under potassium starvation conditions was reduced by 85% in comparison to the wild-type plants [115].

KUPs are found in plasma membrane and organelle membranes, and, in addition to K+ uptake from soil, they are involved in K+ homeostasis, long-distance K<sup>+</sup> transport, cell elongation, response to osmotic stress and even in the regulation of auxin transport [111]. Recently AtKUP7 in Arabidopsis roots was shown to contribute to K+ uptake and K+ efflux to the xylem especially under limited access to potassium [118]. The schematic view of the mechanisms behind the plant responses to potassium deficiency is shown in **Figure 2**. Less studied are high-affinity K+ and Na<sup>+</sup> transporters from the HKT family. These proteins are expressed exclusively in the tonoplast. However, K+ -transporting members of the family seem to be present only in monocots [104]. This family is poorly characterized with regard to posttranslational regulation, although some of its representatives are definitely involved in the control of K+ homeostasis [78, 119].

Recently, elucidation of the mechanisms underlying the regulation of potassium transport in response to potassium starvation stress became a new focus of research, especially those acting both on the transcription and post-transcription levels [77, 102]. Various signaling cascades, enhancing transport of K+ , triggered by potassium starvation, might rely on reactive oxygen species, phytohormones, calcium and phosphatidic acid [8, 77]. Among the mentioned regulatory pathways, involved in the response to potassium deficiency, due to its spatial and temporal specificity, calcium signaling seems to be the most important one [77, 120]. In response to K<sup>+</sup> deprivation, the intracellular calcium levels change that affects peptide calcium sensors CBL1 and CBL9, localized in the plasma membrane (PM) [102]. The affected peptides interact with the cytoplasm-localized protein kinase CIPK23, and the formed complex is recruited to the root cell plasma membrane where it activates the AKT1 channel protein via phosphorylation [77, 121, 122] that results in enhancement of AKT1-mediated root uptake of K+ . Besides, AtKC1 as a channel regulatory subunit interacts with AtAKT1, forming an AtAKT1-AtKC1

**71**

impact on K+

**Figure 2.**

*response to K<sup>+</sup>*

*stomata guard cells.*

*metabolism in plants. K<sup>+</sup>*

*However, in contrast to the NO3*

*serve as the most prominent indicators of K+*

the regulation of putative outward K+

*Ion Homeostasis Response to Nutrient-Deficiency Stress in Plants*

heterotetrameric channel [123]. The regulatory subunit modulates the activity of AtAKT1 together with AtCIPK23 in a synergistic way, coordinating AtAKT1 mediated low-potassium stress responses [123, 124]. Another proposed mechanism relies on the calcium sensor CBL4, acting together with the protein kinase CIPK6,

*shoots to roots and therefore does not influence root growth and branching. In source leaves, remobilization of K+ results in suppression of photosynthesis, inter-veinal chlorosis and tip browning of leaves. Scorching and curling* 

*well as distribution between root cells, translocation from root to shoot and from source to sink leaves, control of* 

AKT2 in Arabidopsis [125]. Thereby, CBL4 mediates translocation from the endo-

to the younger leaves under the conditions of potassium deficiency [126, 127]. It was also proposed that the AtCBL1/AtCIPK23 complex can phosphorylate the AtHAK5 transporter, which belongs to the KUP/HAK/KT family and expressed mainly in roots

seems to be more important for the adaptive response to potassium deficiency than

There are indications that the calcium sensors CBL3 and CIPK9 work together and

homeostasis under low (100 μmol/L) potassium nutritional stress via

 *deficiency in soil triggers metabolic adjustment in plant tissues to maintain cell turgor.* 

*<sup>−</sup> deficiency response, this adjustment does not affect the carbon flow from* 

 *deficiency. (B) The major transport systems, involved in plant* 

 *uptake, accumulation and remobilization in root cell, as* 

channels, localized in tonoplast [97]. However,

channel

transporters

reallocation from older

 *deficiency on carbon* 

modulating activity and PM localization of the weak inward-rectifying K<sup>+</sup>

[128]. However, in contrast to AKT1, transcriptional regulation of the K+

plasmic reticulum membrane to PM and enhances AKT2 activity.

other authors assume that CIPK9 is more likely involved in K+

*Schematic view of plant responses to potassium deficiency. (A) The effect of K+*

 *deficiency, that is, contributing in K+*

*DOI: http://dx.doi.org/10.5772/intechopen.89398*

*Ion Homeostasis Response to Nutrient-Deficiency Stress in Plants DOI: http://dx.doi.org/10.5772/intechopen.89398*

#### **Figure 2.**

*Cell Growth*

of K+

K+

in the response to K+

be involved in K<sup>+</sup>

system mediating K+

uptake of K+

tion to K+

tribute to K+

Na<sup>+</sup>

and on intracellular K<sup>+</sup>

The high-affinity K<sup>+</sup>

The biological roles of the plant TPK K+

involved in maintaining the constant influx of K+

stood than those of the Shakers [78]. The representatives of the TPK family differ by their intracellular localization, while TPK4 is targeted to the plasma membrane; the other family members—TPK1, 2, 3 and 5—are located in organelle membranes [108]. Among them, due to its high selectivity, TPK1 appears to be mostly involved

tonoplast of guard and mesophyll cells and seems to impact on the vacuolar release

homeostasis [110].

sium deficiency [78, 102]. The best characterized transporters of this group are AtHAK5 from Arabidopsis and its homologs in other species, which are assumed to

with protons [103, 111, 112]. Besides this, AtKUP1 is described as a dual-affinity transporter in the plasma membrane of root cells and assumed to be essential in

uptake [113], whereas AtKUP 2, 4, 6 and 8 are supposed to mediate K+

[116], whereas both AtHAK5 and AKT1 systems contribute to K+

uptake from soil, they are involved in K+

homeostasis [78, 119].

results in enhancement of AKT1-mediated root uptake of K+

levels [77, 102]. Various signaling cascades, enhancing transport of K+

uptake and K+

the tonoplast. However, K+

in the control of K+

response to K<sup>+</sup>

in root cells [78]. Similarly to HAK5, its homologs in other plant species (rice, barley, pepper, tomato) are highly up-regulated by potassium starvation [103]. It is generally recognized that HAK5 and AKT1 are the two main players in K+

from the soils, characterized with potassium shortage [102, 114, 115]. Indeed, the studies with T-DNA insertion lines clearly demonstrated that AtHAK5 is the only

potassium concentrations are in the range of 10–200 μmol/L [117]. In particular, the

KUPs are found in plasma membrane and organelle membranes, and, in addi-

transport, cell elongation, response to osmotic stress and even in the regulation of auxin transport [111]. Recently AtKUP7 in Arabidopsis roots was shown to con-

potassium [118]. The schematic view of the mechanisms behind the plant responses to potassium deficiency is shown in **Figure 2**. Less studied are high-affinity K+

transporters from the HKT family. These proteins are expressed exclusively in

only in monocots [104]. This family is poorly characterized with regard to posttranslational regulation, although some of its representatives are definitely involved

Recently, elucidation of the mechanisms underlying the regulation of potassium transport in response to potassium starvation stress became a new focus of research, especially those acting both on the transcription and post-transcription

by potassium starvation, might rely on reactive oxygen species, phytohormones, calcium and phosphatidic acid [8, 77]. Among the mentioned regulatory pathways, involved in the response to potassium deficiency, due to its spatial and temporal specificity, calcium signaling seems to be the most important one [77, 120]. In

peptide calcium sensors CBL1 and CBL9, localized in the plasma membrane (PM) [102]. The affected peptides interact with the cytoplasm-localized protein kinase CIPK23, and the formed complex is recruited to the root cell plasma membrane where it activates the AKT1 channel protein via phosphorylation [77, 121, 122] that

a channel regulatory subunit interacts with AtAKT1, forming an AtAKT1-AtKC1

deprivation, the intracellular calcium levels change that affects

conditions was reduced by 85% in comparison to the wild-type plants [115].

in AtHAK5 AKT1 double mutant plants under potassium starvation

deficiency [109]. This protein is ubiquitously expressed in the

transporters from the KUP/HAK/KT family are directly

uptake at external potassium concentrations below 10 μmol/L

efflux to the xylem especially under limited access to


uptake from very dilute potassium soil solutions, in co-transport


in plant roots under severe potas-

homeostasis, long-distance K<sup>+</sup>

efflux

absorption, when

uptake

and

, triggered

. Besides, AtKC1 as

**70**

*Schematic view of plant responses to potassium deficiency. (A) The effect of K+ deficiency on carbon metabolism in plants. K<sup>+</sup> deficiency in soil triggers metabolic adjustment in plant tissues to maintain cell turgor. However, in contrast to the NO3 <sup>−</sup> deficiency response, this adjustment does not affect the carbon flow from shoots to roots and therefore does not influence root growth and branching. In source leaves, remobilization of K+ results in suppression of photosynthesis, inter-veinal chlorosis and tip browning of leaves. Scorching and curling serve as the most prominent indicators of K+ deficiency. (B) The major transport systems, involved in plant response to K<sup>+</sup> deficiency, that is, contributing in K+ uptake, accumulation and remobilization in root cell, as well as distribution between root cells, translocation from root to shoot and from source to sink leaves, control of stomata guard cells.*

heterotetrameric channel [123]. The regulatory subunit modulates the activity of AtAKT1 together with AtCIPK23 in a synergistic way, coordinating AtAKT1 mediated low-potassium stress responses [123, 124]. Another proposed mechanism relies on the calcium sensor CBL4, acting together with the protein kinase CIPK6, modulating activity and PM localization of the weak inward-rectifying K<sup>+</sup> channel AKT2 in Arabidopsis [125]. Thereby, CBL4 mediates translocation from the endoplasmic reticulum membrane to PM and enhances AKT2 activity.

There are indications that the calcium sensors CBL3 and CIPK9 work together and impact on K+ homeostasis under low (100 μmol/L) potassium nutritional stress via the regulation of putative outward K+ channels, localized in tonoplast [97]. However, other authors assume that CIPK9 is more likely involved in K+ reallocation from older to the younger leaves under the conditions of potassium deficiency [126, 127]. It was also proposed that the AtCBL1/AtCIPK23 complex can phosphorylate the AtHAK5 transporter, which belongs to the KUP/HAK/KT family and expressed mainly in roots [128]. However, in contrast to AKT1, transcriptional regulation of the K+ transporters seems to be more important for the adaptive response to potassium deficiency than

post-translational modification of K+ channels [102, 129, 130]. Potassium starvation was shown to increase the abundance of HAK transcripts in a wide variety of plants, including barley, rice, *Arabidopsis thaliana*, *Solanum lycopersicum* and some others [19]. Thereby, the mRNA levels of HAK1-type genes were most remarkably increased [17, 105, 129]. The mechanisms, underlying expressional regulation of the HAK1-type genes might rely on alterations of membrane potential, as well as to reactive oxygen species (ROS) and to hormone-mediated signaling [105]. Recently, it was shown that transcription of AtHAK5 in *A. thaliana* roots can be induced by low-potassium nutritional stress via the transcription factor RAP2.11 that directly binds to the promoter region of *AtHAK5* and may be involved in the low-potassium signaling pathway [88]. The HAK/KUP/KT transporters were proposed to act as K+ -H+ symporters in the tonoplast and might mobilize K+ from the vacuole under potassium deficiency conditions [131]. Indeed, in *Arabidopsis thaliana*, OsHAK10 and five members of the KUP family have been found to be localized in the tonoplast [19] that supports the above functional assumption.

Thus, numerous studies in the field of K<sup>+</sup> membrane transport and intracellular potassium distribution in plants with regard to the changes in the availability of potassium in the environment indicate that the mechanisms supporting ion homeostasis of the plant cell might be involved in plant responses to potassium deficiency to ensure stress adaptation.

### **4. Conclusion**

Nutrient deficiency, including moderate or severe shortages of NO3 <sup>−</sup> and K<sup>+</sup> in soils, represents a serious challenge to modern agriculture, negatively affecting plant productivity and crop yields. Fortunately, plants possess an array of finely tuned mechanisms of nutritional stress adjustment and maintenance of cell ion homeostasis. Hence, the plant response to nitrate and potassium deficiency relies both on transcriptional and post-transcriptional regulation of high-affinity NO3 <sup>−</sup> and K<sup>+</sup> membrane transport mechanisms, impacting on the increase of abundance and activity of transporters. Importantly, this includes not only an increase in the activity of root ion carriers but also mobilization of NO3 <sup>−</sup> and K<sup>+</sup> from their storage vacuolar pools and subsequent redistribution to the metabolic cytosolic pool. In general, these data indicate that the ion homeostasis system plays an important role in plant cell responses to nutrient deficiency. Since these responses depend on plant taxonomy and duration of K<sup>+</sup> or NO3 <sup>−</sup> shortage, these studies need to be extended to a broad selection of crop plants. To characterize the adaptive potential of these plants, various exposure times need to be addressed.

Currently, proteomics and metabolomics studies, aiming to improve stress tolerance in crop plants, became mainstream in the study of K+ or NO3 <sup>−</sup> starvation. The use of these techniques in research on nutrient stresses seems to be promising. Indeed, these approaches deliver valuable information about the accumulation of important secondary metabolites in plants under different types of environmental stresses.

#### **Acknowledgements**

This work was supported by the Russian Science Foundation (project number 17-16-01042) and the EU through EFRE with the state of Saxony-Anhalt (Agrochemical Institute Piesteritz, IB grant no. ZS/2016/04/78153).

**73**

*Ion Homeostasis Response to Nutrient-Deficiency Stress in Plants*

AtAKT *Arabidopsis thaliana* Arabidopsis K+

AtCLCa *Arabidopsis thaliana* chloride channel a AtHAK *Arabidopsis thaliana* high-affinity K<sup>+</sup>

CIPK calcineurin B-like-interacting protein kinase

Arabidopsis transporter

NAR nitrate transporter-activating protein

NRT/NPF nitrate transporter/peptide transporter

SLAC/SLAH slow anion channel-associated homologs

/K+

transporter

channel

uptake/K+

transporter

outward-rectifying K+

channel

transporter

uptake transporter family

channel

transporter family

transporter family

channels



transporter family

*DOI: http://dx.doi.org/10.5772/intechopen.89398*

AtKC *Arabidopsis thaliana* K+

AtKUP *Arabidopsis thaliana* K+

CLC chloride channel family

Km Michaelis-Menten constant

OsHAK *Oryza sativa* high-affinity K+

T-DNA transfer deoxyribonucleic acid

GORK guard cell outward-rectifying K+

CBL calcineurin B-like

HAK/KUP/KT high-affinity K<sup>+</sup>

HKT high-affinity K+

K potassium

N nitrogen

<sup>−</sup> nitrate NR nitrate reductase NRT nitrate transporter

P phosphorous PM plasma membrane RNA ribonucleic acid ROS reactive oxygen species

TPK tandem-pore K+

V-ATPase the vacuolar H+

V-PPase the vacuolar H+

SKOR stelar K+

KAT K+

NO3

AKT Arabidopsis K<sup>+</sup>

**Abbreviations**

*Ion Homeostasis Response to Nutrient-Deficiency Stress in Plants DOI: http://dx.doi.org/10.5772/intechopen.89398*
