Introduction

Potassium is a macronutrient that may constitute up to 10% of plant dry weight [1]. It is a major inorganic cation in the plant cytoplasm, essential for activity of various enzymes, including those participating in primary metabolism [2]. It contributes significantly to turgor regulation, which is important for many plant processes, such as stomatal function [3,4], cell volume growth [5,6,7], existence of cytoplasm-plasma membrane-cell wall continuum [8], and plant movements [9]. To fulfil the diverse developmental and physiological functions of K⁺ in plants, broad spectrum of K+ transporters and channels evolved to orchestrate K⁺ transport [10,11,12,13].

Root system growth and development relies on K⁺ at various levels. Protein synthesis and enzyme activity of root cells need adequate cytoplasmic K⁺ levels to maintain the cytoplasmic pH [14] and the anionic charge of proteins [15]. Cell expansion in the elongation zone requires turgor pressure, which builds up via osmotically active substances, including K⁺ [16,17]. In the root maturation zone, root hairs grow apically via the action of K⁺ fluxes [18,19,20]. K⁺ affects R:S ratio (root to shoot biomass partitioning) via phloem transport [21,22]. Moreover, adaptive changes of root system architecture (RSA) and root hair coverage evolved in plants to enhance K⁺ uptake in potassium limiting conditions [10,23].

Soil K⁺ bioavailability is often low (especially in acidic soils) and limited mostly to the topsoil as most of soil potassium is incorporated in minerals [24,25]. K⁺ limitation is thus a common problem affecting agricultural production [25,26]. Plants engage high-affinity K⁺ transporters, modulate K⁺ channel transport properties [27,28,29,30], and change root system architecture (RSA) to cope with K⁺ deficiency [31]. Some growth responses to low K⁺ provide functional adjustments of the root system to enhance K⁺ acquisition efficiency. Sensing local K⁺ availability in rhizosphere triggers local root growth [32], but preferential branching to K⁺ rich patches seems to be mild compared to N or P local response [33,34]. K⁺ limitation negatively impacts root elongation and the number of first order lateral roots [35,36,37], but the response varies among species, cultivars, ecotypes, and even root types [35,38]. Suppressed cell volume growth or limited phloem delivery of assimilates to belowground organs may participate in root growth inhibition [21,22]. K⁺ scarcity also increases plant susceptibility to biotic and abiotic stresses [26,39].

Potassium and Root Cell Expansion

The crucial role of osmotically active K⁺ cation in turgor-driven cell expansion is well known (see e.g., [5,17,40]). Two voltage-dependent, inward-rectifying Shaker K⁺ channels, KAT1 and KAT2 (K⁺ CHANNEL IN ARABIDOPSIS THALIANA1, 2), and K⁺ transporter KT2/KUP2/SHY3 (K⁺ TRANSPORT2/K⁺ UPTAKE2/SHORT HYPOCOTYL3) were shown to participate in auxin-induced cell expansion in the hypocotyls and leaves of Arabidopsis thaliana [6,7,41]. Kup2/6/8 triple mutants display significantly larger leaf epidermal cells, which indicates the involvement of these KT/HAK/KUP (K⁺ TRANSPORT/HIGH-AFFINITY K⁺/K⁺ UPTAKE) transporters in K⁺ efflux and modulation of volume growth [6]. KT2/KUP2/SHY3 expression is not limited to the shoot. It is expressed in the root tip [7] and might, therefore, be involved in root cell expansion the same way as in the shoot.

KAT1 functions mostly in the shoot, including in the guard cells [42]; expression of KAT1 in roots is weak [41]. However, similar Shaker K⁺ channel KC1 (K⁺ RECTIFYING CHANNEL1) is active in roots. KC1 is predominantly expressed in root hairs and the endodermis, and modulates root hair K+ uptake [43]. KC1 is a silent regulatory subunit of the heterotetrameric channel AKT1 (ARABIDOPSIS K+ TRANSPORTER1), an inward-rectifying K⁺ channel of the Shaker family. AKT1 plays a dominant role in root K⁺ uptake over a broad range of K⁺ external concentrations [44,45,46]. The assembly of the AKT1/KC1 heterotetramer is triggered by low external K⁺ availability and modifies AKT1 transport properties so that it prevents K+ leakage under these circumstances [29,47]. AKT1 is involved in root hair elongation, but the mechanism is not clear yet [19].

Moreover, a direct link exists between secretion and K⁺ channel activity. SNARE (SOLUBLE NSF ATTACHMENT PROTEIN RECEPTOR; NSF-N-ETHYLMALEIMIDE-SENSITIVE FACTOR) protein SYP121 (SYNTAXIN OF PLANT121), a component of exocytosis regulation machinery controlling vesicle fusion with the target membrane [48], regulates trafficking of K⁺ channel KAT1 and its distribution within plasma membrane subdomains [49]. Moreover, SYP121 directly interacts with the voltage-sensing domain of KAT1 and KC1 channels via FxRF motif and shifts their voltage-driven gating [50,51,52,53]. The SYP121 binding affects the stability of the KAT1 channel in open or closed states and promotes its activity [54]. Binding of SYP121 to KC1 enhances secretion in feedback, highlighting the interplay between exocytosis and K⁺ transport [52,53]. In contrast, binding of the R-SNARE protein VAMP721 (VESICLE-ASSOCIATED MEMBRANE PROTEIN721) to KC1 or KAT1 suppresses their activities [55].

SNARE-dependent control of K⁺ uptake thus presents not only a regulatory pathway of K⁺ acquisition in plants subjected to K⁺ deficiency [23], but also a mechanism to coordinate membrane expansion and cell wall material exocytosis with K⁺ uptake and generation of turgor pressure to drive cell growth [53,56]. SYP121 also coordinates the trafficking of some plasma membrane localized aquaporins (PIP2-7) and thus fine-tunes the water permeability of the membrane [57].

Potassium and Root Hair Growth

Root hairs are short-lived tubular emergences of rhizodermal cells that serve many important roles in root-soil contact, nutrient uptake, and microbial interactions [58]. Long root hairs are advantageous for K⁺ acquisition under K⁺ shortage, as was shown by comparing different crop species [59] and even rice (Oryza sativa L.) genotypes differing in average length of root hairs [60].

Root hair establishment starts with the determination of trichoblast cell fate orchestrated by the action of transcription and other regulatory factors. It continues with the formation of a bulge in the cell wall and specialized tip growth of the emerging hair. Many aspects of this process, including trichoblast genetic determinants, cell wall loosening, deposition of new cell wall material, Ca2⁺ signaling, cytoskeleton action, pH gradients, and other processes, have been studied and reviewed thoroughly [58,61,62]. The bulge formation and tip growth require turgor pressure generation, and, here, K⁺ comes to the scene as the main osmotically active inorganic ion of the plant cell [62]. Apoplast acidification was shown to activate K+ channels [63] and an acidic environment is typical for bulge outgrowth domains [64].

Among others, the AKT1 channel is present in root hairs and participates in K⁺ uptake [44,45,46]. Surprisingly, akt1 plants exhibit a K⁺-dependent root hair phenotype that is not fully consistent with the proposed role of the AKT1/KC1 channel in triggering root hair growth via K⁺ uptake. Akt1 mutants possess longer root hairs under zero external K⁺ levels but shorter root hairs under very high K⁺ levels. At 100 mM external K⁺ root hairs of akt1 mutants completely fail to even elongate. The authors hypothesized that AKT1 negatively regulates root hair elongation in the absence of K⁺, but is required to sustain root hair tip growth under K⁺ levels above 50 mM [19].

K⁺ transporter mutant trh1 (tiny root hair1) also shows a strong root hair phenotype. Trichoblast cell fate determination pathways are not affected in trh1 plants, but root hairs fail to elongate and remain very short [18,65,66]. TRH1/KUP4 is a member of the KT/HAK/KUP family of K⁺ transporters [30,67,68]. Based on a complementation study in Saccharomyces cerevisiae, TRH1 can mediate high-affinity K⁺ uptake [18], but the trh1 root hair phenotype is insensitive to K⁺ supply [18,19]. It can be rescued by external auxin application [69] or phosphorus deficiency, but not iron deficiency [70]. This observation, together with agravitropic root growth, mis-localization of the PIN1 (PIN-FORMED1) auxin efflux carrier, and auxin over-accumulation in the root tip of trh1 plants, highlights TRH1 function in auxin homeostasis maintenance within root apex as necessary to sustain the growth of root hairs [18,65]. The importance of auxin signaling in root hair growth regulation is evident [71] and supported by root hairs defective phenotypes of other auxin mutants, e.g., tir1 (TRANSPORT INHIBITOR RESPONSE1), an auxin receptor mutant [72]. However, the effect of TRH1 might be also indirect via modification of K⁺ homeostasis in meristematic cells, as discussed below.

TRH1 may act as an auxin efflux carrier involved in shoot to root auxin translocation [69]. In roots, it localizes at plasmalemma in a polarized manner. It co-localizes with PIN1 on the basal side of cells in stele in the elongation zone. In the meristematic zone, the preferential localization is in the rhizodermis and cortex. TRH1 might therefore contribute to both acropetal and basipetal auxin transport within the root apex [65] and coordinate environmental cues, auxin signaling, and root hair development [66]. TRH1 seems to function as a homodimer: its assembly is driven by strong interactions between the C-terminal cytoplasmic domains of each of the TRH1 subunits [66].

It must be mentioned that root hair growth responds to K+ soil status [73], see Figure 1. K⁺ deficiency stimulates root hair growth [59] in an ethylene-dependent manner [36,74]. This response relies significantly, but not completely, on EIN2 (ETHYLENE INSENSITIVE2), a positive regulator of the ethylene pathway [36,75,76]. K⁺ deficient plants increase ethylene levels [77] and ROS (reactive oxygen species) signaling is involved downstream of ethylene [74,78].

Figure 1. Symptoms of K⁺ deprivation in Arabidopsis thaliana: Root systems of 10-day-old in vitro plants on (a) high-K and (b) low-K media show preferential inhibition of the first-order lateral root growth in low-K. Root system branching of 16-day-old in vitro plants on (c) high-K and (d) low-K media with enhanced branching to higher orders in low-K. Root hairs of in vitro plants on (e) high-K and (f) low-K media. Shoots of 16-day-old in vitro plants on (g) high-K and (h) low-K media with symptoms of K+ deficiency on leaves in low-K. Lateral root apex of (i) high-K and (j) low-K plants. High-K medium: 0.2x strength MS (Murashige and Skoog) with 4 mM K+; low-K medium: 0.2x strength MS with 15 μM K⁺. Media were supplemented with 1% agar and 1% sucrose. Scale bars: 1 cm (a–d, g–h); 2 mm (e–f); 100 μm (i–j).