1. Introduction
Most cultivable crops experience one or more abiotic stress(es) of some type throughout their growth stages. Thus, increasing plant resilience in response to abiotic stress is a great challenge in the effort to improve food production by 70% to feed the increasing population by the year 2050 [
1]. Abiotic stress hampers plant productivity by altering plant growth patterns and physiological responses [
2,
3]. The combination of different stresses that affect crops has become more common; for example, the occurrence of drought and high temperature is the most common [
4], while in arid and semi-arid regions, salinity and high temperature stresses are imposed at the same time. High light and high temperature stress, drought and salinity, or high temperature, occur simultaneously under current conditions. Due to the complex nature of this stress, plants are more adversely affected, and hence, research on plant stress tolerance is constantly changing and being updated with the new forms of stresses [
1,
3]. These complex stresses cause changes in cropping patterns, crop cultural practices, and sometimes, the extinction of plant species. Since the beginning of agriculture, a range of cultural practices has been developed through continuous trial and error processes. Among the cultivation practices, the use of fertilizers and organic amendments are the oldest methods for improving plant productivity. However, as a chemical fertilizer, potassium (K) has been used on crop field since the nineteenth century [
5].
The role of K in the plant developmental process is well known. The upregulation of the K status decreases reactive oxygen species (ROS) generation in plants. Potassium reduces the activity of nicotinamide adenine dinucleotide phosphate (NADPH) oxidases and retains the photosynthetic electron transport activity, which helps to reduce ROS. Potassium deficiencies can decrease the photosynthetic CO
2 fixation and the transport and utilization of assimilates [
6]. Membrane and chlorophyll (chl) degradation are favored in K-deficient plants. The regulation of K is associated with the activity of the enzymes involved in ROS detoxification [
5]. Potassium triggers the activation of the adenosine triphosphate (ATP) synthase enzyme. The plasma membrane-bound H
+-ATPase is influenced by the K content [
7]. Potassium-deficient plants have been reported to be light-sensitive, and thus they exhibit chlorotic and necrotic symptoms [
5]. Potassium was reported to decrease different stress effects in plants such as drought, chilling, and high light intensity [
6]. A combined high temperature and drought tolerance induced by potassium was reported [
8]. The role of K as a nutrient has been recognized for a long time. However, its arrays of biological functions in plant physiological processes have still not been fully explored. In recent years, the correlation between phytohormones and K has been studied [
9]; phytohormones interact with one another and other signaling molecules, which regulate biochemical processes and metabolism, exerting physiological responses in relation to almost all the features of plant growth and development and enhancing stress tolerance. Auxin-regulated genes regulate proteins that affect the transcriptional repressors of stress responses in plants [
10]. Abscisic acid (ABA) influences the expression of genes that modulate complex stress-responsive regulatory networks [
11]. The roles of other different hormones including cytokinin [
12], ethylene and jasmonic acids (JA; [
13]), gibberellic acid (GA; [
14]), and salicylic acid (SA; [
15]) have been documented for their ability to confer abiotic stress tolerance. However, the complex process that occurs in response to abiotic stress tolerance is still under investigation. This is a comprehensive review articulating the biological function of K in plants and its role in plant adaptations to abiotic stresses.
3. Potassium Uptake, Transport, and Assimilation in Plants
The potassium reserve in soil is very high and accounts for nearly 2.1–2.3% of the earth’s crust [
17,
18]. Therefore, soil K reserves are generally large [
17]. Plants uptake K as cation (K
+) and many sources of K are available in soils or provided as fertilizers, including potassium chloride (KCl), potassium nitrate (KNO
3), potassium sulfate (K
2SO
4), and potassium carbonate (K
2CO
3). Among these forms, KCl, or muriate of potash, is the most inexpensive and most frequently used for agronomic crops, with some exceptions [
19]. Other forms such as K
2SO
4 and KNO
3 are used for some crops that are sensitive to chloride (Cl
−), although they are expensive. For example, KCl causes leaf burn in tobacco due to its chloride ions [
20]. However, the availability of K
+ from soil or fertilizers depends on the soil texture, soil moisture content, pH, and some other factors. Apart from the common and soluble forms of K compounds, some forms such as K silicate minerals are also available in some soils. The availability of these compounds is very low, and in these cases, some microbes (especially bacteria and fungi) assist in solubilizing K and converting it into soluble forms through acidification, chelation, and exchange reactions [
21]. As a macronutrient, K is mostly applied as a basal dose to the soil. In some cases (e.g., sandy soil), K is applied as a foliar spray [
22]. Foliar application is also very effective under waterlogged conditions [
23]. However, the effectiveness of the foliar spray is dependent on the absorption capacity by and penetration into leaves; therefore, it can only partially compensate for insufficient uptake by the roots. Moreover, the efficacy of foliar application also requires a sufficient leaf area [
24].
Apart from the factors detailed above, the capacity of plant species to take up K
+ is another factor that controls K release from the soil minerals or applied fertilizers. To facilitate K
+ uptake from the outer environment and transport it to different cellular compartments, many proteins are present in the cell, primarily in the membrane. These proteins are often called transporters and channels. Based on their affinity for K
+, K
+ transport components can be classified as high-affinity components (transporters), which are active at a low concentration of external K
+, and low-affinity components (channels), which are active at a higher concentration, usually at more than 0.3 mM external K
+ [
25]. Advances in molecular approaches and tools have led to the identification of some low-affinity and high-affinity transporters in different plant species including barley (
Hordeum vulgare L.), rice (
Oryza sativa L.)
, and capsicum (
Capsicum annuum L.) [
26]. A yeast mutant lacking the ability to take up K
+ could grow only when the mutant was transformed with cDNA from barley. This study led to the identification of the high-affinity K transporter HvHAK1, which is homologous to the
Escherichia coli and
Schwanniomyces occidentalis HAK1 K
+ transporter [
27]. To support the low-affinity transport mechanism as an inward rectifying K
+ channel, a high-affinity potassium transporters (HKT) has been proposed [
26]. An
Arabidopsis mutant lacking the
HKT1 gene (which was screened from a T-DNA insertion line) was able to grow in a 1 mM KCl solution without experiencing growth reduction. However, at 100 μM KCl, the mutant showed significant growth reduction, indicating
HKT1 channel involvement in K
+ uptake from the low K solution [
28]. In
Arabidopsis, 75 genes encode the proteins that facilitate K
+ uptake and transport. These genes can be roughly categorized into seven categories viz. shaker-type K
+ channels (nine genes), two-pore K
+ channels (six genes), putative K
+/H
+ antiporters (six genes), KUP/HAK/KT transporters (13 genes), HKT transporters (one gene), cyclic-nucleotide gate channels (20 genes), and glutamate receptors [
29]. The Shaker-type K
+ channels were further classified into three groups. These types are an inward-rectifying channel, which facilitates K
+ uptake and is activated upon hyperpolarization; outward-rectifying channels, which mediate K
+ efflux and are activated upon membrane depolarization; and weakly rectifying channels, which can function in both K
+ influx and K
+ efflux, and they are activated by membrane hyperpolarization [
25]. The channels and transporters encoded by different genes are different with respect to structure and function [
25].
In roots, the K
+ uptake from the media is primarily mediated by two proteins, AKT1 and HAK5, because these two proteins are expressed in the roots of
Arabidopsis [
30] and rice [
31,
32]. The loss of function mutants
hak5 or
akt1 were able to survive at 100 μM KCl solution, but the double
hak5 akt1 mutant failed to survive at the same concentration, indicating that AKT1 and HAK5 are high-affinity transporters that mediate sufficient K
+ uptake for plant growth [
30]. In rice, Os-AKT1 mediated K
+ uptake as regulated by a complex of two proteins, calcineurin B-like protein1 (Os-CBL1) and CBL-interacting protein kinase23 (CIPK23) [
31]. For long-distance transport, K
+ transport from the root cortex to the xylem was mediated by outward-rectifying channels (
Figure 1). Experimental evidence showed that a mutant lacking the stellar outward rectifying K
+ channel (SKOR channel) reduces the K
+ content in the shoots by 50% and reduces the K
+ content in the xylem sap. Stomatal closure or opening depends on the K
+ concentration in the guard cell, where inward channel KAT1 and KAT2 mediate K
+ uptake into the cell and outward rectifying K
+ channel, and the guard cell's outward rectifying K
+ channel (GORK channel) mediates K
+ release to close the stomata [
33]. In the case of K
+, voltage-dependent K
+ channel (TPK1TPK2, TPK3, and TPK5) and vacuolar Na
+, K
+/H
+ antiporters such as NHX1 and NHX2 are present in the tonoplast to facilitate K
+ influx and efflux in the vacuole [
34,
35,
36].
6. Role of Potassium in the Detoxification of Reactive Oxygen Species
One of the common consequences of abiotic stress is the overproduction of ROS such as singlet oxygen (
1O
2), superoxides (O
2•−), H
2O
2 and hydroxyl radicals (OH
•) [
166], alkoxy radicals (RO
•), peroxy radicals (ROO
•), and organic hydroperoxides (ROOH) [
167,
168]. Inside plant cells, low concentrations of ROS act as a signaling molecule to protect plants from stresses, while higher concentrations of ROS enhance the lipid peroxidation, oxidation of proteins, inhibition of enzyme activities, and activation of the programmed cell death (PCD) pathway, ultimately leading to cell death [
169]. During photosynthetic electron transport and membrane-bound NADPH oxidase reactions, the formation of ROS in plant cells is increased due to K deficiency. Hence, it was suggested that the exogenous use of K could decrease ROS formation by maintaining the plant photosynthetic electron transport and diminishing the action of NADPH oxidase ([
6];
Table 5;
Figure 3).
Plants that are exposed to environmental stresses such as drought show enhanced K requirements, and furthermore, they show increased oxidative damage to cells by inducing the formation of ROS, especially during photosynthesis [
9]. At the time of drought stress, CO
2 fixation is limited in plants, and it impacts the stomata regulation, transfer of light into chemical energy and translocation of photosynthates from source to sink (
Figure 3; [
170,
171]). Due to the impairment of photosynthetic CO
2 fixation, plant molecular O
2 is activated and ROS production is increased within the plant cell [
6,
9,
172], which causes the degradation of the photosynthetic pigment and cellular membranes. Sangakkara et al. [
173] found a positive role for K by reducing ROS formation and increasing the net photosynthesis rate under water-stressed conditions in mung bean (
V. radiata) and the cowpea (
V. unguiculata). Egilla et al. [
113] observed that adequate K
+ availability to China rose (
Hibiscus rosa-sinensis L.) under drought stress reduced the inhibition of photosynthesis by mitigating ROS formation. Likewise, Milford and Johnston [
174] suggested that K plays a vital role in stomatal opening and closing and in the transpiration and photosynthesis of plant cells. Raza et al. [
81] experimented with
T. aestivum under drought conditions and found that an application of 1.5% K decreased the ROS formation and improved the transpiration and photosynthesis rates. Thus, it was suggested that an adequate supply of K under drought conditions improved the photosynthetic CO
2 fixation and the export of photosynthates from source to sink organs and prevented photosynthetic electron transport to O
2. As a result, the formation of ROS was reduced [
6,
9].
Under saline conditions, low K increased the toxicity of Na
+ in plant tissue. Thus, the K
+/Na
+ ratio decreased and led to ROS formation, which affects the stomatal closure and inhibits the plant’s photosynthesis activity, and it increases oxidative damage [
175]. The higher production of ROS due to severe salinity leads to cellular membrane damage. Programmed cell death occurs as a result of K
+ leaks from the plant cells due to the activation of K
+ efflux channels [
176]. The external use of K in a saline growing medium was involved in improving salt tolerance through reduced ROS formation in
T. aestivum [
177],
Z. mays [
178], and
O. sativa [
179]. The application of K enhanced the antioxidant enzyme activities such as those of superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD) in zinger (
Zingiber officinale Roscoe) [
180], which reduced the ROS formation in plant cells. Zheng et al. [
181] suggested that applying a suitable amount of KNO
3 detoxified the ROS through increased SOD, CAT, and POD enzyme activities in
T. aestivum under salt stress. Jan et al. [
182] reported that the SOD, CAT, and ascorbate peroxidase (APX) enzyme activities were enhanced, and applying K under salt stress thus detoxified the ROS.
On the other hand, NADPH-oxidizing enzymes reduce O
2 to O
2− by using NADPH as an electron donor ([
6];
Figure 3). Moreover, the NADPH oxidase activity was substantially enhanced under K deficiency, increasing the NADPH-dependent O
2− production. Cakmak [
6] found that K deficiency increased the NADPH oxidase activity in the cytosol of
P. vulgaris roots, with a corresponding increase in the NADPH-dependent O
2− generation, but exogenous K decreased the NADPH oxidase activity. Potassium deficiency is most likely the primary reason for the increased NADPH oxidase and NADPH-dependent ROS formation through the generation of ABA. Peuke et al. [
184] experimented with castor (
Ricinus communis) and found that K deficiency increased the biosynthesis of ABA in roots and increased the translocation of ABA from the roots to the shoots. Moreover, ABA has likewise appeared to be effective at increasing the accumulation of H
2O
2 and O
2− in plant roots [
185,
186], but this point needs to be verified in future studies. It is clear that an improvement in the K status maintains the photosynthetic electron transport and inhibits the NADPH oxidase activities, which reduce ROS formation in plants.
7. Interaction of Potassium with Other Biomolecules
Potassium is called the policeman nutrient; it plays an important role in the growth, development, and yield as well as the metabolism of plants. It also has some interactive regulatory functions with other biomolecules [
5,
9]. Therefore, K deficiency leads to dysfunction in numerous physiological and biochemical processes; for example, in the water balance, enzyme activity, and charge balance, in addition to tolerance to biotic and abiotic stresses [
187]. Potassium is also essential for the function and performance of many plant enzymes; at least 60 enzymes require K as a cofactor for activation [
188]. These enzymes regulate the vital metabolic mechanisms in arable plants [
38,
189]. To increase substrate attraction, K binds with the specific binding site of inactive enzymes, resulting in their activation, and these enzymes were involved in various metabolic and physiological mechanisms. Several studies have suggested that the activity of nitrate reductase (NR), RuBisCO, starch synthase, sucrose phosphate synthase, β-amylase, invertase, phosphofructokinase, and pyruvate kinase greatly depends on the K sufficiency of plants [
190,
191].
Among the biomolecules, carbohydrates have a greater interactive relation with K. When plants obtain enough K, they synthesize large biomolecules; for example, cellulose, starch, protein, etc. As a result, the number of small molecules such as free sugars, amino acids, organic acids, and amides are reduced in the cell while the concentration of phenols increases, and these compounds aid in plant resistance [
192] and increase the plant response to abiotic stress [
193]. Carbohydrates, mostly in terms of hexose content, are decreased in leaves due to a sufficient K supply, which was transported to another plant organ due to better phloem activity. On the other hand, K deficiency resulted in the decreased activity of pyruvate kinase and/or increased invertase activity that reduces the concentration of starch in leaves because of the inhibition of starch synthase [
60].
Potassium has a positive relationship to plant hormone synthesis as well [
194]. When the K concentration in the cell is low, JA and auxin biosynthesis are upregulated [
195], but ethylene synthesis is increased by two-fold in
Arabidopsis when the plant is suffering from K-starvation [
196], and the other biological functions decreased in the roots and xylem sap, leading to sucrose accumulation. Conversely, the cytokinin concentrations in the leaf and the xylem sap decreased when plants obtained sufficient amounts of K [
187,
197]. Ethylene, which is another important plant hormone, assists in the progression of root morphology and stimulates ROS biosynthesis to tolerate a low K condition in
Arabidopsis [
198]. Exogenously applied K and naphthaleneacetic acid (NAA) can interact significantly to increase the growth and yield of
V. radiata [
199]. A similar result was also obtained by applying K and GA to rice [
200] and by applying K and SA to olive trees under salinity [
201]. Increased levels of JA, hydroxy-12-oxo-octadecadienoic acids (HODs), and 12-oxo-phytodienoic acid (OPDA) were obtained under K-starved conditions along with the upregulation of the 13-lipoxygenase (LOX) pathway, indicating the transcript levels of several biosynthetic enzymes with K interactions [
202]. ABA acts as an important signal-mediated factor during the transduction of the sucrose regulation signal. The ABA content in the seed is negatively correlated with the sucrose content, and the ABA/(Indole acetic acid + GA + cytokinin) ratio is influenced by K nutrition in a way that particularly reduces the ABA content, playing a key role in the increase in the sucrose content, which suggested the K interactions with phytohormones [
187].
Polyamines also have a role in a wide range of environmental stresses, and they are involved in various physiological processes. Their concentrations at the cellular level increased under K deficit conditions in oat (
Avena sativa L.) [
203]. When plants face any stress, they accumulate polyamines at a higher concentration. Polyamines have significant interactions with K at the cellular level, and they regulate the plasma membrane K
+ channel of the guard cells, modulating stomatal regulation [
204]. The authors also reported that spermidine, spermine, cadaverine, and putrescine powerfully block the opening and closing of stomata, which provides a link among the stress, the stomatal regulation, and the polyamine level.
8. Potassium-Induced Abiotic Stress Signaling
In a dynamic environment, the K content of the soil may not remain the same over the growing period of a crop. Interestingly, plant roots can sense fluctuations in the K
+ availability. When the K deficiency is sensed by plant roots, a series of events occurs in the plant at the molecular level to cope with this condition. Some signaling components are involved from the signal perception to the adaptive responses (
Figure 4). For example, the Ca
2+ signaling, ROS, microRNA, membrane potential and phytohormones are the signaling components [
25,
52]. Under K-deficient conditions, CIPK23 (a protein kinase) activates the K
+ transporter AKT1 by phosphorylation. The calcium sensors CBL1 and CBL2 regulate the activation of CIPK23 [
205]. Later, low K
+ induces two distinct Ca
2+ signals that are read by CBL1/9, as observed in
A. thaliana [
206]. The CBL1/9 then regulates the AKT1 by activating CBL1/9-CIPK23 complexes [
206]. The overexpression of the type III peroxidase
RCI3 increased the production of ROS as well as the HAK5 expression. However, a mutant lacking this gene exhibited reductions in both ROS production and HAK5 expression, indicating the relationship between the ROS and the low K response [
207]. Potassium channels such as NSCC and GORK are very sensitive to ROS. Under saline conditions, the ROS-mediated activation of NSCC and GORK is the primary reason for the K pool reduction in the cytosol [
29,
208]. A prolonged K deficiency in the cytosol activates different endonucleases and proteases, which in turn causes cell death [
29].
Phytohormones such as ethylene, auxin, cytokinin, and JA are also involved in low K-induced signaling processes. Under K-deficient conditions,
HAK5 transcription is regulated by the upstream signaling molecule ethylene and ROS [
209]. However, the cytokinin content decreases under low K stress to regulate
HAK5 by inducing ROS [
209]. A K
+ transporter in rice has been found to be regulated by JA [
210]. The involvement of microRNAs in plant nutrient homeostasis has been reported in many studies. For example, the gene chip overexpression of
OsmiR399 increased the nutrient contents of the plant, including the contents of K
+. Under nutrient starvation,
OsmiR399 expression increases [
211]. The elucidation of a complex pathway that was induced by K signaling allowed us to engineer the pathway in a way that would ensure the optimum K level in the plant.