Potassium Deficiency and Hormone Signalling in Plants

ABSTRACT

Potassium (K or K⁺) is a vital macronutrient that influences numerous physiological processes related to plant physiology and development. Recently, there is a growing focus on enhancing K⁺‐use efficiency (KUE) to ensure optimal plant growth, especially in K⁺ deficient soils. Most approaches are centred on targeting genes associated with K⁺ sensing, signalling and other pathways related to plant hormones. However, despite progress, the success stories for generating high KUE crops are still limited. In view of this, the present review highlights the role of hormonal signalling in regulating K⁺ deficiency‐induced responses in plants. We integrate shreds of evidence of how these K⁺‐hormone signalling crosstalk modulate root‐system architecture, K⁺ uptake and stress resilience. Furthermore, a meta‐analysis‐based assessment of different hormones highlighted the central role of jasmonic acid and abscisic acid in mediating K⁺ deficiency‐induced changes at the transcriptional level. The present review offers novel insights into K⁺‐hormone crosstalk that can be used as a framework for advancing KUE research and addressing challenges towards global food security.

Summary statement

This review highlights the role of hormonal signalling in regulating K⁺ deficiency‐induced responses in plants. It also offers novel insights into K⁺‐hormone crosstalk that can be used as a framework for advancing KUE research and addressing challenges towards global food security.

1. Introduction

Potassium (K⁺) is an essential macronutrient that comprises up to 10% of the total dry weight of plants (Leigh and Wyn Jones ¹⁹⁸⁴). It plays a pivotal role in various physiological processes, including water uptake, transpiration, enzyme activation and photosynthesis (Y. Wang and Wu ²⁰¹⁷). The K⁺ status of the soils is generally maintained through fertiliser supplementation and air deposition. However, it gets continuously removed via open burning, leaching erosion and harvested crop removal, which makes the soil K⁺ deficient (Figure 1A; White et al. ²⁰²¹). Besides, K⁺ minerals may also be adsorbed to organic matter or trapped in crystal structures, making them unavailable for plant uptake (Pahuja et al. 2023), further magnifying the problem of K⁺ deficiency in the soil. Plants have evolved a range of morphological/physiological adaptations of the rhizosphere processes and root traits, including root plasticity, root length and root hairs to optimise K⁺ uptake under varying soil conditions. These adaptations respond to differences in soil profile distribution, K⁺ mobility, K⁺ availability and bioavailability (Figure 1B; White et al. ²⁰²¹). Despite these strategies, the areas under K⁺ deficiency are still rising, which is a global food security concern with substantial implications for agricultural productivity. As per an estimate, ~20% of the world's agricultural soil is K⁺ deficient, with maximum contribution from regions like East Asia, Latin America, Southeast Asia and sub‐Saharan Africa (Brownlie et al. 2024). One of the biggest challenges to mitigate soil K⁺‐deficiency is the limited reserves for K⁺‐fertilisers such as muriate of potash (KCl) and sulphate of potash (K₂SO₄), which are typically present in countries like Canada, Belarus and Russia (U.S. Geological Survey ²⁰²⁴). Therefore, a heavy import dependency on potash fertilisers causes an economic burden to other countries. Furthermore, the 15‐year (2007–2021) global cereal production data have highlighted the disproportionate gain compared with the consumption of K⁺‐fertiliser, except Zea mays (maize), indicating the excessive use of K⁺ fertiliser (Figure 1C; Table S1; FAO ²⁰²², ²⁰²³). The excessive application of K⁺ fertilisers can disrupt soil nutrient balance, causing deficiencies in calcium (Ca²⁺) and magnesium (Mg²⁺) (Pantha et al. 2023). Besides, it may lead to soil acidification, reducing fertility and harming plant growth (Y. Lu, Cong, et al. ²⁰²²). In addition, the run‐off and leaching of unused K⁺ fertiliser contribute to water pollution, eutrophication, groundwater contamination and soil degradation. Therefore, developing high K⁺‐use‐efficient (KUE) crops will reduce the import cost to support food security from the limited agricultural lands and avoid environmental degradation.

Figure 1.

Potassium (K⁺) availability in soil and K⁺ fertiliser usage by the crops. (A) Methods of K⁺ acquisition and removal from soil. (B) The root traits and rhizosphere processes influencing the acquisition of K⁺ from soil. (C) Fifteen‐year worldwide cereal production and K⁺ fertiliser consumption (FAO ²⁰²², ²⁰²³).

The physiological and molecular effects of K⁺ deficiency in plants have been well‐investigated. Briefly, K⁺ deficiency‐induced imbalance in cellular turgor pressure leads to decreased water uptake and transpiration efficiency (Srivastava et al. 2020; Amtmann and Srivastava ²⁰²³). It also impacts photosynthesis due to the necessity of K⁺ for maintaining a pH gradient across thylakoids, adenosine diphosphate ribosylation factor synthesis and for stomatal opening and closing. Due to the importance of K⁺ for voltage and osmotic gradients, cellular and long‐distance nutrient transport is impaired under K⁺ deficiency, leading to wider nutritional deficiencies. Since K⁺ is a cofactor for various enzymes, its deficiency can affect important metabolic processes like nitrogen (N) assimilation and protein synthesis, resulting in stunted growth and poor plant vigour (Armengaud et al. 2009). Moreover, K⁺ also influences the size and quality of fruits and seed viability. For instance, external K⁺ application has been found to increase fruit quality along with the enhanced nutrient content in tomato leaves (Çolpan et al. 2013). Likewise, intensive K⁺ sprays boost the quality of cherry fruits of Prunus avium L. (Sweet cherry) by making them firmer and reducing fruit cracking (Bustamante et al. 2021). Therefore, K⁺ deficiency during these stages can result in abnormal fruit development, reduced seed set and poor yield. In addition, K⁺ plays a very significant role in enhancing plant resistance to diseases and tolerance to various environmental stresses, such as drought, salinity and temperature extremes (Pandey and Mahiwal ^2020a; Amtmann and Srivastava ²⁰²³).

Mitigating K⁺ deficiency stress in plants can be achieved through various approaches, including agronomic amendments, the use of microorganisms and integrated soil‐nutrient management (ISNM). Agronomic amendments such as the application of K⁺‐rich fertilisers, organic matter and biochar can enhance soil K⁺ availability and improve nutrient balance. In addition, the use of microorganisms, such as K⁺‐solubilising bacteria (KSB) and fungi, can help release K⁺ from insoluble soil forms, making it more accessible to plants. KSB are particularly effective in this regard (Wu et al. 2023). ISNM combines various approaches to make an effective ‘package‐of‐practice’ for mitigating K⁺ deficiency and promoting sustainable agriculture. Furthermore, to have an efficient ISNM along with the reduced use of chemical fertilisers, the development of KUE crop through genetic modifications of the key gene(s) related to K⁺‐uptake, sensing or signalling has been a focus of research (Sathee et al. 2022). The classical studies focussed on the use of high‐affinity K⁺‐channels like ARABIDOPSIS K⁺ TRANSPORTER 1 (AKT1) and HIGH‐AFFINITY K⁺ transporter (HAK) 5 and their molecular regulators associated with the Calcineurin‐B‐Like (CBL) and CBL‐interacting protein kinase (CIPK) signalling pathways (Gierth et al. 2005; Ródenas et al. ²⁰²¹; Ródenas and Vert ²⁰²¹). In addition, the gene pool of extremophiles like Eutrema salsugineum has been utilised for finding suitable targets for promoting K⁺ uptake and increasing grain yield under K⁺ deficient conditions (Zhou et al. 2020). Exploring natural genetic variations has also facilitated the identification of genes that link K⁺ sensing and root architecture for increasing the surface area available for K⁺ absorption (Kellermeier et al. 2013; Kellermeier et al. ²⁰¹⁴). Although significant progress has been made in identifying target gene(s) for enhancing K⁺‐uptake in plants, the development of KUE is still challenging. There has been limited success, especially under realistic field conditions. This is mainly due to the complexity of gene regulatory networks involved in K⁺ transport, sensing and signalling. These networks make it difficult to achieve desired changes in K⁺ accumulation without imposing any growth penalty and/or compromising tolerance towards co‐existing stress factors. With this background, the present review summarises the recent advances in canonical K⁺ deficiency‐induced signalling in plants. The emerging crosstalk between the K⁺ deficiency and hormone signalling has been highlighted through the meta‐analysis of publicly available transcriptome datasets, with the emphasis on prioritising gene(s) crosstalk for developing high‐KUE plants.

2. Canonical K⁺ Deficiency Induced Signalling Pathways

Most of the plants maintain the cytosolic K⁺ concentration at approximately 100 mM, although a typical K⁺ concentration at the root surface is in the range of 0.1–1 mM (Y. Lu, Yu, et al. ²⁰²²; Pahuja et al. ²⁰²³). K⁺ deficiency is initially sensed by root cells which further enhances the H⁺‐ATPases activity leading to membrane hyperpolarization (Pahuja et al. 2023). There are two major strategies to maintain higher cytosolic K⁺ levels, especially under K⁺ deficient conditions: K⁺ acquisition from the soil and K⁺ remobilisation from the vacuolar reserves (Figure 2). For K⁺ acquisition, plants rely on the activation of the K⁺ inward rectifying channel AKT1 and a high‐affinity transporter, HAK5, through the CBL1/9‐CIPK23 signalling module (Figure 2; Table 1; Gierth et al. ²⁰⁰⁵; Ródenas and Vert ²⁰²¹). Conversely, various phosphatases negatively regulate CBLs‐CIPKs complexes via dephosphorylation (K. L. Li et al. ²⁰²³). For instance, ARABIDOPSIS PROTEIN PHOSPHATASE 2C1 (PP2C1) dephosphorylates CIPK9 while AKT1‐Interacting PP2C1 (AIP1) dephosphorylates AKT1, thereby maintaining homoeostasis under K⁺ sufficient conditions (Figure 2; A. Singh et al. ²⁰¹⁸; K. L. Li et al. ²⁰²³). The RNAi lines of osakt1 are sensitive to low K⁺ conditions and exhibit symptoms similar to the atakt1 mutant (J. Li et al. ²⁰¹⁴), suggesting that the function of the CBL1‐CIPK23‐AKT1 module is conserved in rice. In Arabidopsis thaliana (Arabidopsis), AKT1 activity is modulated through the formation of a heteromeric complex with the non‐functional subunit K⁺ Channel 1 (KC1), and this process has been shown to be important in limiting the K⁺ leakage from root cells (Duby et al. 2008). Although a homologue of AtKC1 is not found in the Oryza sativa (rice) genome (Fuchs et al. 2005), OsAKT1 alone can limit the K⁺ leakage under K⁺ deficient conditions (J. Li et al. ²⁰¹⁴). Recent structural studies of AtKC1 also support the inhibition of AKT1 activity by the inhibitory domain or I‐domain of AtKC1 (Table 1; Zheng et al. ²⁰²⁴).

Figure 2.

Potassium signal transduction in plants under K⁺ starvation. K⁺ deficiency in plants is sensed by KSN, leading to hyperpolarisation of the membrane. It further leads to activation of the Ca²⁺ channel, resulting in increased Ca²⁺ concentration in the cytoplasm. Low K⁺ also leads to ROS accumulation via RIC, activating the Ca²⁺ channels. These Ca²⁺ bursts activate SGN1/3 via phosphorylation and CIF peptides. This induces RBOHs peroxidases responsible for ROS generation. RBOHD/F‐induced ROS is involved in Casparian strip formation and suberin deposition, while ROS produced via RBOHC/D is responsible for HAK5 upregulation. In addition, ROS facilitates RICR, leading to an increase in cytosolic Ca²⁺. This spike in ([Ca²⁺]_cyt) generates Ca²⁺ signatures, further activating CBL‐CIPKs complexes. At the plasma membrane, AKT1, AKT2 and HAK5 are activated via (CBL1/9‐CIPK23), (CBL4‐CIPK6) and (CBL1/9‐CIPK1/9/23) complexes, respectively. Activation of AKTs and HAKs is responsible for increasing the K⁺ uptake. AKT1 also interacts with KC1 to limit the K⁺ leakage from the roots. This expression of AKT1 and HAK5 is also enhanced by the binding of WRKY6 and MYB77 to their respective promoter. Simultaneously, TPCs and TPKs, the transporters present in the tonoplast, are also activated via CIPK3/9/23/26, thus participating in K⁺ efflux. These CBLs‐CIPKs complexes inhibit the TORC pathway via phosphorylation. Under higher K⁺ conditions, TORC reciprocally inhibits the CBL‐CIPKs‐dependent K⁺ deficiency response. Furthermore, phosphatases and PA are involved in maintaining the K⁺ homoeostasis in the cell. Under normal conditions, AIP1 and PP2C1 negatively regulate AKT1 and CIPK9, respectively. In addition, another transcription factor, ARF2, negatively regulates the HAK5 expression. Apart from these, other transporters, including KUP7, SKOR and NRT, are involved in loading K⁺ into the xylem tissue, which is then unloaded into leaf tissue for further root‐shoot‐translocation of K⁺ in plants. (Potassium, K⁺; K⁺ SENSING NICHE, KSN; Calcium, Ca²⁺; Reactive Oxygen Species, ROS; SCHENGEN1/3, SGN1/3; RARE INDUCIBLE COLD, RIC; RESPIRATORY BURST OXIDASE HOMOLOGUE, RBOH; CASPARIAN STRIP INTEGRITY FACTOR, CIF; ROS INDUCED Ca²⁺ RELEASE, RICR; CALCINEURIN B‐LIKE PROTEINS, CBLs; CBL‐INTERACTING PROTEIN KINASES, CIPKs; ARABIDOPSIS K⁺ TRANSPORTER, AKT1; HIGH‐AFFINITY K⁺ TRANSPORTER 5, HAK5; K⁺ CHANNEL 1, KC1; STELAR K⁺ OUTWARD RECTIFIER, SKOR; TANDEM PORE K⁺ CHANNEL, TPK; TWO PORE CHANNEL, TPC; NITRATE TRANSPORTER, NRT; K⁺‐UPTAKE PERMEASE, KUP; MYELOBLASTOSIS ONCOGENE Transcription Factor, MYB; AUXIN RESPONSE FACTOR 2, ARF2; LETHAL WITH SEC THIRTEEN 8, LST8; TARGET OF RAPAMYCIN COMPLEX, TOR; REGULATORY ASSOCIATED PROTEIN OF TOR, RAPTOR; Cytosolic Ca²⁺ ([Ca²⁺]_cyt). [Color figure can be viewed at wileyonlinelibrary.com]

Table 1.

Physiological role of potassium (K⁺) transporters in Arabidopsis.

S. no.	K+ transporter	Physiological role	References
1	AKT1 and AKT2	Facilitate K+ uptake under normal K+ concentrations	Gierth et al. (2005)
2	HAK5	Stimulates the K+ uptake under extremely low K+ conditions	Ródenas and Vert (2021)
3	KC1	Refrain from the K+ leakage from root cells during K+ starvation	Duby et al. (2008) and Zheng et al. (2024)
4	TPK1	Activates K+ efflux into the cytoplasm from vacuoles	Y. Wang, Chen, et al. (2021)
5	TPC1	Activates K+ efflux into the cytoplasm	Y. Wang, Chen, et al. (2021)
6	SKOR	Facilitates the long‐distance K+ transport from root‐to‐shoots	Pahuja et al. (2023)
7	KUP7	Stimulates the K+ uptake and translocation in roots	Han et al. (2016)
8	KUP9	K+ and auxin transport from ER to cytoplasm under K+ deficiency	M. L. Zhang et al. (2020)
9	H+‐ATPases	Initiates K+ deficiency sensing by membrane hyperpolarisation	Pahuja et al. (2023)
10	NRT	Loading of K+ into xylem for root to shoot translocation	Pahuja et al. (2023)

Abbreviations: AKT, ARABIDOPSIS K⁺ TRANSPORTER; HAK, HIGH AFFINITY K⁺ TRANSPORTER; K⁺, potassium; KC1, K⁺ CHANNEL; KUP, K⁺ UPTAKE PERMEASE; NRT, NITRATE TRANSPORTER; SKOR, SELAR K⁺ OUTWARD RECTIFIER; TPC1, TWO‐PORE CHANNELS; TPK, TANDEM‐PORE K⁺ CHANNEL.

AKT2, a weakly rectifying member of the plant Shaker family, contributes to K⁺ permeability in mesophyll cells of Arabidopsis (Tian et al. 2021; Y. N. Huang et al. ²⁰²¹). Its activation requires phosphorylation by the CBL4‐CIPK6 complex, which modulates its activity at the plasma membrane (Held et al. 2011). Interestingly, another report suggested the role of AKT2 in generating a K⁺ gradient in vascular tissues, which is further utilised as a source of energy for phloem (re)loading. AKT2 can be switched into a non‐rectifying channel via phosphorylation of two serine residues (S210 and S329), which allows a rapid efflux of K⁺ from the sieve element/companion (Sandmann et al. 2011). The essential role of AKT2 in regulating long‐distance K⁺ transport and phloem loading was also demonstrated through single and double mutant analyses of AKT1 and AKT2 in Arabidopsis, where AKT2 deficiency impaired K⁺ translocation and led to growth defects (Dennison et al. 2001). OsAKT2 regulates the translocation of sucrose and K⁺ from young to old leaves in rice. The osakt2 knockout mutants have lower K⁺ concentrations in phloem sap, preventing shoot‐to‐root K⁺ redistribution. OsAKT2 enhances salt tolerance by limiting root Na⁺ uptake, contributing to Na⁺/K⁺ homoeostasis in plants (Tian et al. 2021). Various transcription factors (TFs) also participate in the regulation of K⁺ uptake under K⁺ deficiency. WRKY6, for instance, acts upstream of AKT1 and positively regulates its expression (Niu et al. 2024).

At the vacuolar membrane, TWO‐PORE CHANNEL 1 (TPC1), TANDEM‐PORE K⁺ channel 1 (TPK1) facilitate K⁺ remobilisation under K⁺‐limited conditions, contributing to processes such as stomatal movement and seed germination (Table 1; Y. Wang, Chen, et al. ²⁰²¹). The CBL2/3‐CIPKs pathway is a primary complex for K⁺ remobilisation under low K⁺ conditions. In agreement with this, the cbl2cbl3 double mutants also showed impeded K⁺ remobilisation from vacuoles, though their K⁺ uptake was normal (Tang et al. 2012). Moreover, recent studies have revealed that upon K⁺ starvation, activation of vacuolar‐localised CBL2/3 occurs before and is required for the complete activation of plasma membrane‐localised CBL1/9 signal transduction. In addition, CIPK9/23 kinases were found to phosphorylate CBL1/9/2/3 under low‐K⁺ stress in Arabidopsis (K. L. Li et al. ²⁰²³). Under high K⁺ conditions, the TARGET OF RAPAMYCIN COMPLEX (TORC) comprising REGULATORY ASSOCIATED PROTEIN OF TOR (RAPTOR) and LETHAL WITH SEC THIRTEEN PROTEIN 8 (LST8) functions to shut down CBL‐CIPK‐dependent low‐K⁺ responses in Arabidopsis. Herein, a CBL2/3‐CIPK9 module phosphorylates RAPTOR and thereby inactivates TORC under K⁺ deficient conditions (Figure 2; K. L. Li et al. ²⁰²³; Bheri et al. ²⁰²⁴).

Apart from the Shaker family K⁺ channels, members of the K⁺ uptake permease (KUP)/HAK/KT family are engaged in high‐affinity K⁺ uptake under low micromolar (µM) concentrations of K⁺ (< 10 µM K⁺; Table 1; Gierth et al. ²⁰⁰⁵; Pyo et al. ²⁰¹⁰). For example, in Arabidopsis, KUP7 is involved in K⁺ uptake and loading into the xylem sap. The kup7 mutants show impaired K⁺ uptake and reduced xylem loading under low K⁺ conditions (Han et al. 2016). Interestingly, KUP9 transports both auxin and K⁺ from the endoplasmic reticulum lumen to the cytoplasm, maintaining root growth and meristem activity under low K⁺ stress (M. L. Zhang et al. ²⁰²⁰). Besides KUP7, STELAR K⁺ OUTWARD RECTIFIER (SKOR) and NITRATE TRANSPORTER (NRT) also regulate the K⁺ loading into the xylem sap (Pahuja et al. 2023). Furthermore, HAK5, which interacts with CIPK1 and CIPK9 in heterologous yeast systems (Figure 2; Lara et al. ²⁰²⁰), illustrates the fine‐tuning of root K⁺ uptake via CBL‐CIPK regulatory complexes. The rice genome also has a larger HAK gene family than Arabidopsis, suggesting a complex K⁺ uptake and transport mechanism. OsHAK1 and OsHAK5 share a high identity with AtHAK5 (Gupta et al. 2008; T. Yang et al. ²⁰¹⁴). OsHAK5 plays a vital role in K⁺ acquisition and translocation from root to shoot under K⁺ deficit conditions. Overexpression of OsHAK5 led to enhanced net K⁺ influx in roots, whereas oshak5 knockout lines show impaired K⁺ uptake and reduced K⁺ concentration in roots and shoots. OsHAK5 overexpression also improves shoots' K⁺/Na⁺ ratio, aiding in salt stress tolerance (T. Yang et al. ²⁰¹⁴). Other KUP/HAK/KT family members, including HAK1, HAK8, HAK16 and HAK18, also contribute to root K⁺ uptake in rice. Similarly, OsHAK16 is induced in response to K⁺ deficiency or salt stress (Feng et al. 2019).

The OsHAK8 is broadly expressed in the root cells. Growth retardation and a decrease in K⁺ uptake were observed under low K⁺ conditions in oshak8 mutants (X. Wang, Li, et al. ²⁰²¹). OsHAK18 participates in phloem K⁺ loading and redistribution. Its disruption significantly reduces K⁺ concentration and impairs root‐to‐shoot‐to‐root translocation (Shen et al. 2023). Thus, the HAK family genes orchestrate a sophisticated K⁺ uptake, transport and redistribution network, essential for sustaining rice growth and stress resilience under challenging environmental conditions.

Signalling molecules such as reactive oxygen species (ROS), Ca²⁺ and phosphatidic acid (PA) also play key roles in the molecular responses to K⁺ deficiency in plants. For instance, ROS‐induced Ca²⁺ release (RICR) is responsible for the transcriptional activation of HAK (Figure 2; Kim et al. ²⁰¹⁰; F. Wang et al. ²⁰²⁰). The expression analysis also linked ROS to K⁺ deficiency, with differential regulation of genes encoding K⁺ transporters and Respiratory Burst Oxidase Homologue (RBOHs; Shin and Schachtman ²⁰⁰⁴; Shin et al. ²⁰⁰⁵). The attenuated expression of these genes in rbohc mutants highlights the importance of RBOHC in mediating the K⁺ deficiency responses (Shin and Schachtman 2004; Shin et al. ²⁰⁰⁵). RBOHC, also known as ROOT HAIR DEFICIENT 2, is vital for root hair formation and development, suggesting that root hairs act as sensors for K⁺ deficiency due to their direct soil contact (Parker et al. 2000; Tarkowski et al. ²⁰²³). Furthermore, in Arabidopsis, a peroxidase RARE COLD INDUCIBLE 3 (RCI3) contributes to ROS production and induces HAK5 expression under K⁺ deficiency, with its secretion to the apoplast suggesting the role of apoplastic ROS during low K⁺ stress (Kim et al. 2010). In addition, RBOHC and RBOHD are involved in ROS generation downstream of a Casparian strip integrity factor 2 (CIF2) peptide‐receptor‐like kinase complex, that is, LOW K⁺ SENSING 4 (LKS4)/SCHENGEN (SGN) 1 and SGN3 complex, which induces the HAK5 for enhanced K⁺ uptake (Figure 2; Fujita et al. ²⁰²⁰; Y. Wang, Mostafa, et al. ²⁰²¹). Likewise, PA also exhibits transient increases under K⁺ deficiency (Testerink and Munnik 2005). This signalling lipid is involved in plant stress responses, directly binding and inhibiting K⁺ channels such as K⁺ CHANNEL Β‐SUBUNIT 1 (KAB1) and the shaker‐like channel AKT2 (McLoughlin et al. ²⁰¹³; Shen et al. ²⁰²⁰). In Arabidopsis, phospholipase dα1 (pldα1) mutants grown under high Mg²⁺ show reduced K⁺ content, which can be rescued by external K⁺ supplementation. This highlights PLDα1 role in generating PA, which influences K⁺ deficiency responses. Besides this, the downregulation of CIPK9 and HAK5 in pldα1 seedlings under high Mg²⁺ stress suggests a link between K⁺ and Mg²⁺ responses in Arabidopsis, with CIPK9 integrating these stress responses by regulating PA turnover via PLDα1 (Pandey et al. 2007; Nieves‐Cordones et al. ²⁰¹⁰; Mogami et al. ²⁰¹⁵; Tang et al. ²⁰¹⁵; Kocourková et al. ²⁰²⁰). Taken together, the interconnected molecular insights highlight the orchestrating plant responses to K⁺ deficiency, offering targets for improving nutrient stress tolerance.

3. Hormonal Regulation of K⁺ Deficiency Induced Responses

Extensive studies have unveiled the intricate hormone signalling networks under various abiotic stresses, including nutrient deficiencies (Waadt et al. 2022). For example, abscisic acid (ABA) has received significant attention due to its central role in modulating plant responses to salt and drought stress by regulating stomatal closure, osmotic adjustment and stress‐responsive gene expression (Y. Zhang et al. ²⁰²³). Similarly, jasmonic acid (JA) has emerged as a pivotal player in plant defence against biotic attacks as well as various abiotic stresses, including salt and heavy metals (Y. Wang, Yu, et al. ²⁰²¹). Besides, the crosstalk between JA and ABA signalling pathways has been shown to integrate responses to K⁺ deficiency with those under water stress (Savchenko et al. 2014). In view of this, we provide state‐of‐the‐art information for different hormone signalling pathways in mediating plant responses under K⁺ deficient conditions.

3.1. JA

The first evidence for the involvement of JA under K⁺ deficiency responses came from transcriptomics data, where K⁺ deprivation was seen to bring about differential expression of JA‐associated genes (Armengaud et al. 2004). Subsequent studies confirmed that JA levels increase under K⁺ starvation (S. Cao et al. ²⁰⁰⁶; Troufflard et al. ²⁰¹⁰). The K⁺ deficiency‐induced rise in cytosolic Ca²⁺ ([Ca²⁺]_cyt) along with ROS, activates JA biosynthesis through enzymes such as LIPOXYGENASE (LOX), ALLENE OXIDE SYNTHASE (AOS), ALLENE OXIDE CYCLASE (AOC) and 12‐OXOPHYTODIENOIC ACID REDUCTASE 3 (X. Wang et al. ²⁰¹⁹, Tarkowski et al. ²⁰²³). JA is then conjugated by jasmonate resistant 1 to form bioactive ligands, which activate gene expression via the CORONATINE‐INSENSITIVE 1 (COI1) ‐JASMONATE ZIM‐DOMAIN (JAZ) co‐receptor complex (X. Wang et al. ²⁰¹⁹). This forms a positive feedback loop with the ubiquitin‐ligase complexes (SCF^COI1)‐JAZ regulatory module, enhancing stress responses (Figure 3; Wasternack and Hause ²⁰¹³).

Figure 3.

Potassium (K⁺) deficiency‐stress signalling and hormones crosstalk. K⁺ deficiency is sensed by ARABIDOPSIS K⁺ TRANSPORTER 1 (AKT1) leading to a release of calcium (Ca²⁺) signatures. CBL INTERACTING PROTEIN KINASE 23 (CIPK23), on interaction with CALCINEURIN B‐LIKE (CBL1/CBL9) proteins, phosphorylates both AKT and HIGH‐AFFINITY K⁺ TRANSPORTER 5 (HAK5). The Ca²⁺ signalling also leads to the expression of Jasmonic Acid (JA) biosynthesis genes. JA binds to the CORONATINE‐INSENSITIVE 1 (COI1) to activate further genes like HAK5. COI1 ‐JASMONATE ZIM‐DOMAIN (JAZ) forms a positive feedback regulation of JA. JA‐responsive JAZ9 also regulates root growth under K⁺ deficiency conditions. CIPK25, which is responsive in K⁺ deficiency conditions under low oxygen, acts as a hub to integrate auxin and cytokinin (CK) signalling to regulate root meristem development. CK also acts upstream of ZINC FINGER PROTEIN 5 (ZFP5) to regulate root growth via ETHYLENE INSENSITIVE 2 (EIN2). It is also involved in ROS response and inhibition of HAK5 under K⁺ deficiency conditions. In addition, the hormone ethylene (ET) is involved in ROS response, root proliferation and elongation and regulates the expression of HAK5 directly or via RAP2.11. ET regulates stomatal closure by ETR1/EIN2 in response to K⁺ deficiency under water stress conditions. ABA influences K⁺ deficiency‐induced ROS production parallel to or in conjunction with ET and CK. Another hormone, gibberellic acid (GA), that is negatively regulated under K⁺ deficiency conditions, interacts with JA to form a negative feedback loop for precise and targeted response by degradation of DELLA or JAZ protein by GA or JA, thereby releasing the respective genes from repression. (LOX: LIPOXYGENASE; AOS: ALLENE OXIDE SYNTHASE; AOC: ALLENE OXIDE CYCLASE; OPDA: OPDA REDUCTASE3; JAR1: JASMONATE RESISTANT 1; ETR1: ETHYLENE RECEPTOR 1; RCI3: RARE COLD INDUCIBLE 3; RBOH: RESPIRATORY BURST OXIDASE HOMOLOGUE; ETO1: ET OVERPRODUCER 1; GL2: GLABRA2.) [Color figure can be viewed at wileyonlinelibrary.com]

JA biosynthesis also influences primary root growth under K⁺ deficiency, likely by modulating K⁺ transporters and root system architecture (RSA; N. Singh and Pandey ²⁰²⁰; Deepika et al. ²⁰²²). The JA signalling repressor JAZ9 is a key regulator of K⁺ deficiency responses. OsJAZ9 overexpression enhances K⁺ deficiency tolerance by modulating K⁺ transporters and RSA (A. P. Singh et al. ²⁰¹⁸, ²⁰²⁰). The JA‐COI1‐JAZ module also regulates stress responses, K⁺ uptake and defence mechanisms by activating stress‐responsive genes (Xie et al. 1998; Staswick and Tiryaki ²⁰⁰⁴). JAZ9 also promotes root growth, increasing surface area for K⁺ absorption and paralleling responses mediated by ethylene (ET) and auxin (Xu et al. 2020). This highlights JA's broader role beyond KUE, contributing to abiotic stress resilience (Table 2). In addition to JAZ9, AOS from Triticum aestivum (wheat) enhances K⁺ deficiency tolerance in rice (Fan et al. 2023). JA enhances HAK5 expression via GCC and TGACG motif binding (Figure 3; Shikha et al. ²⁰²³). These findings suggest that JA‐K⁺ crosstalk plays a critical role in plant responses to nutrient stress.

Table 2.

Manipulation of hormone pathway genes for tolerance against potassium (K⁺) deficiency and other abiotic stresses.

Gene	Interaction type	Hormone	Transgenic plant	Type	Phenotype under stress	Phenotypic alteration under stress	Stress	Reference
AtCIPK25	−Ve	Auxin	Arabidopsis thaliana (Thale Cress)	M	S	Reduced chlorophyll content, reduced stalk height and delay in bolting under energy‐limiting conditions	K+ def. and Anoxia	Tagliani et al. (2020)
AtIPT1,3,5,7	+Ve	CK	Arabidopsis thaliana (Thale Cress)	M	T	Enhanced root growth, more ROS accumulation	K+ def.	Nam et al. (2012)
AtIPT3			Arabidopsis thaliana (Thale Cress)	OX	S	Root growth suppressed	K+ def.	Nam et al. (2012)
GhIPT: GhSAG12			Gossypium hirsutum (Cotton)	EX	T	Enhanced stress tolerance, promotion of seed germination under stress, increased antioxidant enzyme activity, less ROS accumulation	Salt	Shan et al. (2019)
Bean P(SARK): Agrobacterium IPT			Gossypium hirsutum (Cotton)		T	More root and shoot biomass, flower dropping reduced, higher chlorophyll content and higher photosynthetic rates	Water def.	Kuppu et al. (2013)
AtZFP5			Arabidopsis thaliana (Thale Cress)	M	S	Short root hair	K+ def.	L. Huang et al. (2020)
AtEIN2	+Ve	ET	Arabidopsis thaliana (Thale Cress)	M	S	Increased ABA sensitivity	K+ def	Y. Wang et al. (2007)
AtEIN2					S		Salt
AtEIN2					S		Osmotic
TaAOS	+Ve	JA	Oryza sativa (rice)	OX	T	Increase dry weight	K+ def.	G. Li et al. (2017)
OsAOS				M	S	Low dry weight
OsAOS				M	S	High arsenic in grains, high root‐to‐shoot translocation of arsenic	Arsenic	Fan et al. (2023)
OsJAZ9	+Ve	JA	Oryza sativa (rice)	OX	T	High dry weight, increased root number, shorter seminal roots	K+ def.	Singh et al. (2020)
				M	S	Low dry weight, longer seminal roots	K+ def.
				OX	T	Enhanced ABA and JA, reduced leaf width & stomatal density, low leaf transpiration	Water def	A. P. Singh et al. (2021)
				M	S		Salt	Wu et al. (2015)
AtUNC93	+Ve	ABA	Arabidopsis thaliana (Thale Cress)	OX	T	Large phenotype, tolerant to abiotic stress, decreased ABA sensitivity	K+ def. Salt Drought High temp	Xiang et al. (2018)
				M	S	Dwarf phenotype, sensitive to abiotic stress, increased ABA sensitivity

Abbreviations: ABA, abscisic acid; AOS, ALLENE OXIDE SYNTHASE; EIN, ETHYLENE INSENSITIVE 2; CIPK25, CALCINEURIN B‐LIKE PROTEIN‐INTERACTING PROTEIN KINASES 25; CK, cytokinin; def, deficiency; ET, ethylene; EX, ectopic expression; IPT, ISOPENTENYL TRANSFERASES; JA, jasmonic acid; JAZ9, JASMONATE‐ZIM DOMAIN PROTEIN 9; M, mutant; OX, overexpression; S, sensitive; T, tolerant; UNC93, UNCOORDINATED PROTEIN 93; ZFP5, ZINC FINGER PROTEIN 5.

JA‐dependent immune responses influence fungal susceptibility based on K⁺ availability (Davis et al. 2018). However, the relationship between K⁺ homoeostasis and defence remains unclear. Some studies suggest that JA, glucosinolates and secondary metabolites enhance disease resistance under K⁺ deficiency, indicating a negative correlation between K⁺ content and disease resistance (Amtmann et al. 2008; Davis et al. ²⁰¹⁸). Conversely, other findings suggest a positive correlation, as K⁺ supports metabolic processes crucial for plant defence (Holzmueller et al. 2007; Sarwar ²⁰¹²; Pandey and Mahiwal ^2020b). Notably, stem borer resistance may depend on salicylate and serotonin, suggesting that K⁺ deficiency's impact on pest susceptibility varies by defence pathway JA versus salicylic acid (SA)‐mediated resistance (H. Lu et al. ²⁰¹⁸). Furthermore, JA accumulation is linked to K⁺ deficiency‐induced leaf senescence, a function distinct from its role in defence (He et al. 2002; S. Cao et al. ²⁰⁰⁶).

3.2. ABA

ABA is known to be a master regulator of stomatal closure and has long been thought to influence K⁺ deficiency responses. This is because the ABA‐mediated stomatal closure leads to minimised water loss, which may help to sustain cellular functions during K⁺ scarcity (Figure 3; Peuke et al. ²⁰⁰²; Kim et al. ²⁰⁰⁹). It is known that K⁺ deprivation inhibits stomatal closure in an ET‐dependent manner under water stress (Benlloch‐Gonzalez et al. ²⁰¹⁰). Therefore, ABA accumulation may counteract the process, but it is unknown if the time‐course dynamics of both these hormones would support this possibility (Benlloch‐Gonzalez et al. ²⁰¹⁰). Moreover, since the expression of the peroxidase RCI3 is modulated by ABA, it is also conceived to influence K⁺ deficiency‐induced ROS production. This effect could occur either in parallel with or potentially in conjunction with ET and/or CK signalling, as both hormones are involved in plant stress responses and could modulate ROS production pathways (Figure 3; Kim et al. ²⁰¹⁰). ABA produced in the Arabidopsis roots upon K⁺ deprivation is involved in suberin deposition that helps in the adaptation of root cells to nutrient deficiency (Barberon et al. 2016). Therefore, ABA signalling is important to finetune the K⁺ deficiency response along with conferring abiotic stress resilience.

3.3. Ethylene

The role of gaseous hormone ET in regulating K⁺ deficiency was discovered almost two decades ago (Shin and Schachtman 2004; Jung et al. ²⁰⁰⁹). ET accumulates in K⁺‐deprived seedlings and is involved in inhibiting primary and lateral root growth and root hair elongation (Shin and Schachtman 2004). In addition, ET acts upstream of ROS production under low K⁺ in Arabidopsis roots and partially influences HAK5 expression (Jung et al. 2009). Analysis of ROS production in et‐insensitive (ein) mutants and HAK5 expression studies with ET biosynthesis inhibitors have also shown the existence of ET‐independent ROS production and induction of HAK5 expression pathways, suggesting that multiple parallel pathways work to control these events (Jung et al. 2009). In addition, the ET‐responsive TF, RAP2.11, is involved in ROS production and regulation of HAK5 expression (Figure 3; Kim et al. ²⁰¹²). Along with altering ROS levels, this protein also regulates HAK5 expression by directly binding to its promoter, showing that ET might also induce HAK5 expression independent of ROS production. It has also been suggested that RAP2.11 may mediate a positive feedback loop between ET and ROS production, thus amplifying the signal in response to the stress (Kim et al. 2012). ET also transcriptionally activates the expression of RBOH protein in other stress conditions (C. Y. Yang and Hong ²⁰¹⁵).

Recently, in Arabidopsis, GLABRA2 (GL2) was shown to bind to the gene ET Overproducer 1 (ETO1), regulating ET and root growth under K⁺‐deficient conditions (Cheng et al. 2024). The GL2‐ETO1 module was also shown to regulate genes like Lotus japonicus Roothairless‐like 3 (LRL3), Root Hair Defective 6‐like 4 (RSL4) and Short Hypocotyl Under Blue 1 (SHB1). The gene RSL4 encodes a TF, LRL3 is associated with root hair growth and epidermal cell differentiation, and SHB1 is associated with nutritional regulation (Cheng et al. 2024).

3.4. Cytokinin (CK)

CKs are crucial for cell division and differentiation. K⁺ deficiency generally results in reduced CK levels in roots and increased levels in shoots, which suggests a reallocation of resources towards root growth to enhance K⁺ uptake. A significant decrease in the bioactive CK levels was reported in both the roots and shoots of K⁺‐deprived seedlings, which, in turn, reduces cell division in roots to conserve energy during stress conditions (Takei et al. 2002; Nam et al. ²⁰¹²). CK also controls the growth of primary, lateral roots and root hairs, possibly by modulating ROS levels in the root and transducing signal through the CK receptors, ARABIDOPSIS HISTIDINE KINASE (AHK) 2 and AHK3 (Nam et al. 2012). The CK content is also negatively correlated with ROS levels and HAK5 expression, placing CKs upstream of ROS production (Figure 3; Nam et al. ²⁰¹²). The ISOPENTENYL TRANSFERASES (IPTs) are key enzymes in CK biosynthesis. Under K⁺ deficiency, ipt1,3,5,7 mutants showed an increase in Arabidopsis root growth, but the IPT3 overexpression lines showed the opposite phenotype, suggesting that CKs negatively regulate tolerance to K⁺ deficiency (Table 2; Nam et al. ²⁰¹²). Furthermore, CK‐regulated ZINC FINGER PROTEIN 5 (ZFP5) controls the EIN2 transcription, mediating root hair elongation under, as shown by a short root hair phenotype under K⁺ deficiency (L. Huang et al. ²⁰²⁰). Studies have shown that CK induces ZFP5; thus, it mediates ET and CK to regulate root hair development (An et al. 2012). Furthermore, it is known that expression of SHORT HYPOCOTYL 2 (SHY2) is regulated by CK‐activated Arabidopsis response regulator (ARR1), resulting in auxin response factor (ARF) repression and thereby downregulation of auxin transporting PIN‐FORMED (PIN) proteins (Ioio et al. 2008; Mockaitis and Estelle ²⁰⁰⁸). It is not yet known if the CK levels have any effect on the ET‐induced ROS production or if ET and CK form parallel pathways towards the same end. Hence, it will also be interesting to determine if there is any crosstalk between auxins and CKs and/or ET and CK to control the process of root growth under K⁺ deprivation.

3.5. Auxin

The initial evidence about the auxin involvement in K⁺ deficiency came from the correlation of effects of ammonium (NH₄ ⁺) with K⁺ deficiency, where some auxin‐insensitive mutants were also insensitive to NH₄ ⁺‐mediated root growth inhibition during K⁺ deficiency (Y. Cao et al. ¹⁹⁹³). However, the K⁺ transporter, TINY ROOT HAIR 1 (TRH1)/KUP4, also mediates auxin transport under K⁺ deficiency (Vicente‐Agullo et al. ²⁰⁰⁴). There was a ‘distortion’ in root DR5:GUS expression under K⁺ deprivation, correlating it with the agravitropic behaviour of seedlings observed in K⁺ deficient media, which may be an adaptive response to scout for K⁺‐rich patches in the soil (Vicente‐Agullo et al. ²⁰⁰⁴; Rigas et al. ²⁰¹³). Auxin's role in low K⁺ stress responses includes changes like RSA modification that are dominantly controlled by its signalling (Overvoorde et al. 2010).

Auxin also plays a major role in determining the primary root growth in K⁺ deficient conditions. K⁺ deficiency disrupts the auxin gradient in primary root tip and lateral root founder cells through degradation or internalisation of PIN proteins, specifically PIN1, leading to root growth inhibition (Y. Wang and Wu ²⁰¹⁷; Shahzad et al. ²⁰²⁰). The decrease in primary root tip auxin concentration is accompanied by an increase in the maturation zone, suggesting a disturbed acropetal transport of auxin (Y. Wang and Wu ²⁰¹⁷). Lateral root growth is controlled by pathways mediated by NRT1.1, a nitrate‐cum‐auxin transporter and AKT1 (both regulated by the common upstream kinase, CIPK23; Figure 3). Thus, it was proposed that auxin may act as a node connecting this regulatory response and that AKT1 may be involved in auxin recycling at the lateral root tip (Kellermeier et al. 2014; J. Li et al. ²⁰¹⁷). Moreover, CIPK25 modulates the K⁺ uptake via AKT1 under K⁺ deficiency and hypoxia (Figure 3; Tagliani et al. ²⁰²⁰).

While the attenuation of the root‐tip auxin gradient provided the initial clue, the underlying mechanisms still remain elusive. Low K⁺ arrests meristem growth by affecting cell division in the quiescent centre, along with a reduction in cell numbers in all zones of the root, a process that depends on KUP9 (Y. Wang and Wu ²⁰¹⁷; M. L. Zhang et al. ²⁰²⁰). KUP9 mediates direct auxin transport similar to other K⁺ transporters like KUP4/TRH1, and transports K⁺ only in the presence of auxin (Rigas et al. 2001; M. L. Zhang et al. ²⁰²⁰).

MYELOBLASTOSIS 77 (MYB77) enhances the HAK5 expression under low K⁺ conditions in an auxin‐independent manner, suggesting its dual role in high‐affinity K⁺ uptake and auxin‐induced root growth regulation (Feng et al. 2021). The reduction in auxin concentration may be influenced by secondary Ca²⁺ signalling that peak around 24 h post‐stress (Behera et al. 2017). Since ET also controls primary root growth and HAK5 expression via RAP2.11 under K⁺ deficiency (Kim et al. 2012), some hormonal cross‐talks may fine‐tune ET‐auxin‐mediated root growth under K⁺‐limited conditions. However, ET‐dependent auxin production inhibits root growth by reducing cell length in the primary root without affecting meristem activity, which is opposite to what is observed under K⁺ starvation (M. L. Zhang et al. ²⁰²⁰). Thus, auxins‐ET‐CK‐dependent intricate networks might play an important role in regulating K⁺ deficiency‐induced signalling. These findings further add a layer of complexity to the hormonal crosstalk of auxin, ET, JA, and CK to regulate root growth under K⁺ deficient conditions.

3.6. Gibberellins (GA)

GA regulate growth processes such as stem elongation and seed germination. K⁺ deficiency typically results in reduced GA levels, leading to stunted growth, which conserves energy and resources during stress. GA interacts with ABA and ET to balance plant growth and stress responses (Achard et al. 2008; Hedden and Sponsel ²⁰¹⁵). Under K⁺ deficiency in Arabidopsis, the accumulation of DELLA proteins causes lateral root growth inhibition, and the phenotype is rescued by GA supplementation (Hetherington et al. 2021). Similarly, in Solanum lycopersicum (tomato), under K⁺ deficiency, the GAs antagonise JAs to regulate root growth (X. Wang et al. ²⁰²³).

3.7. SA

SA is primarily known for its role in pathogen defence, but also responds to nutrient stress. SA also influences the expression and activity of K⁺ transporters, such as HAK/KUP/KT family transporters, which are crucial for maintaining K⁺ homoeostasis under deficient conditions. This regulation helps optimise K⁺ uptake and distribution (Forieri et al. 2017; Guo et al. ²⁰²⁵). In addition, SA interacts with other hormones, such as ABA, ET and JA, to fine‐tune stress responses. These interactions help optimise resource allocation and enhance stress tolerance under K⁺ deficiency (Bari and Jones 2009). K⁺ deficiency increases SA levels, which helps to modulate antioxidant defences and maintain cellular homoeostasis under stress conditions (Khan et al. 2015; Cui et al. ²⁰²¹). SA enhances the expression of antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT) and peroxidases (POX), which help in mitigating oxidative damage (Khan et al. 2015).

Overall, the findings highlight the complexity of hormone‐mediated responses to K⁺ deficiency in plants and offer insights into potential molecular mechanisms governing plant adaptation to nutrient‐limiting conditions in general.

4. Biotechnological Interventions to Improve K⁺ Deficiency Responses in Plants

Considering their universal role in K⁺ uptake, the high‐affinity transporters such as HAK5, 8, 18 and 16 in rice and HAK1‐4A in wheat have been targeted through genetic manipulation for enhancing the K⁺ deficiency tolerance (Table S2; T. Yang et al. ²⁰¹⁴; Feng et al. ²⁰¹⁹; T. Yang et al. ²⁰²⁰; X. Wang, Li, et al. ²⁰²¹; Jing et al. ²⁰²²; Xu et al. ²⁰²²; Shen et al. ²⁰²³). However, the translation potential of these studies under realistic field conditions with a multiple stress regime is yet to be tested. In view of this, targeting the genes related to ‘K⁺‐hormone’ crosstalk could be a viable strategy for simultaneously improving KUE and overall stress tolerance in crops. In recent years, several such genes from the hormone signalling pathways have been either mutated or over‐expressed to enhance plants' tolerance towards K⁺ deficiency and other plant abiotic stresses (Table 2). For instance, OsJAZ9 interacts with a novel interactor of JAZ (OsNINJA) to suppress basic helix‐loop‐helix 62 (OsbHLH062) for regulating JA‐responsive genes under salt stress (Wu et al. 2015). Furthermore, the overexpression of OsJAZ9 in rice leads to improved water‐deficit stress tolerance, higher K⁺ content as osmoticum, and reduced transpiration due to reduced leaf width and stomatal density, while osjaz9 shows a sensitive phenotype under salt stress (Wu et al. 2015; A. P. Singh et al. ²⁰²¹). Similarly, AOS from wheat improved the K⁺ deficiency response in rice. The overexpression of TaAOS in rice resulted in increased K⁺ concentration in leaves and the JA concentration compared to the wild type under low K⁺ conditions. Moreover, the osaos mutants showed decreased dry weights and K⁺ concentrations in leaf and root tissues compared to the wild‐type (G. Li et al. ²⁰¹⁷). Apart from regulating K⁺ deficiency, AOS1 also contributed to limiting the arsenic (As) accumulation in rice grains. The osaos1‐1 and osaos2‐1 rice mutants showed increased sensitivity to both As(V) and As(III). The role of OsAOS1 was to modulate both As‐detoxification as well as allocation, while OsAOS2 contributes only to As‐tolerance, as the osaos1 mutants showed increased As‐accumulation and root‐to‐shoot As‐translocation (Table 2; Fan et al. ²⁰²³).

An ABA signalling component, UNCOORDINATED PROTEIN 93 (AtUNC93) from Arabidopsis has been shown to regulate K⁺ translocation from roots to shoots by modulating ABA signalling (Xiang et al. 2018). The AtUNC93 overexpression lines showed enhanced tolerance to salt, drought and high‐temperature stress and improved responses to K⁺ deficiency, whereas the atunc93 mutant exhibited increased sensitivity to these stresses (Table 2; Xiang et al. ²⁰¹⁸). Furthermore, in Helianthus annuus (sunflower), under combined K⁺ and drought stress, ET production inhibits stomatal closure (Benlloch‐Gonzalez et al. ²⁰¹⁰). ET mediates the regulation of stomatal closure via ET receptor 1 (ETR1) and EIN2 along with hydrogen peroxide (H₂O₂) (Tanaka et al. 2005; Desikan et al. ²⁰⁰⁶). Arabidopsis atein2, shows higher sensitivity to K⁺ deficiency, a significant decrease in shoot fresh weight and leaf chlorophyll content and hypersensitivity to ABA, salt and osmotic stress (Table 2; Y. Wang et al. ²⁰⁰⁷). The ZFP5 regulates the EIN2 transcription, mediating root hair elongation under K⁺ deficiency. The Arabidopsis zfp5 RNAi lines showed a short root hair phenotype under K⁺ deficiency (L. Huang et al. ²⁰²⁰). Similar phenotype was also observed in the case of phosphorus deficiency (Table 2; L. Huang et al. ²⁰²⁰). Studies have shown that CK induces ZFP5; thus, mediating ET and CK to regulate root hair development (An et al. 2012). Further, in the transgenic Gossypium hirsutum (cotton), the overexpression of the IPT led to improved tolerance to salt and drought stresses (Table 2; Kuppu et al. ²⁰¹³; Shan et al. ²⁰¹⁹).

Under K⁺ deficiency and limited oxygen conditions, the CIPK25 modulates the K⁺ uptake via the K⁺ channel AKT1 (Tagliani et al. 2020). The atcipk25 had reduced root growth and showed a short root phenotype (Kumar Meena et al. 2019). In addition, there was a loss in auxin‐responsive promoter activity and auxin transport, and the expression of an Aux/IAA family gene SHY2 and auxin efflux carriers (PIN1 and PIN2) were altered. However, the decreased expression of PIN1 and PIN2 in atcipk25 was restored in combined atcipk25atshy2 mutant lines (Kumar Meena et al. 2019). The atcipk25 mutants were also sensitive to K⁺ deficiency and anoxia (Table 2; Tagliani et al. ²⁰²⁰). The Y2H assay confirms that CIPK25 regulates K⁺ homoeostasis by interacting with the AKT1 K⁺ channel (Tagliani et al. 2020). Therefore, CIPK25 may act as a hub to integrate auxin and CK signalling to regulate root meristem development (Figure 3; Meena et al. ²⁰¹⁸).

Although the success in biotechnological studies provided an avenue for improving KUE, the core genetic component(s) of ‘K⁺‐hormone’ crosstalk still remains unclear. To resolve this, we performed a meta‐analysis to understand the relative contribution of different hormone signalling events in regulating K⁺ deficiency responses. The publicly available transcriptome of rice related to K⁺ deficiency (GSE66935; Takehisa et al. ²⁰¹⁵) and various hormone supplementation (GSE39429; Sato et al. ²⁰¹³) were utilised for this purpose. Here, K⁺ deficiency was studied at three different levels viz., 1/4^th, 1/16^th, and 1/64^th of normal K⁺ concentration. The highest overlap in the 1/16^th K⁺ deficiency transcriptome, in terms of differentially expressed genes (DEGs), was observed with JA (53%), followed by ABA (44%), CK (27%), auxin (18%), brassinolide (BL; 13%) and GA (5%; Figure 4A,B). The overlap of JA transcriptome, with 1/4^th, 1/16^th, and 1/64^th K⁺ transcriptome was 49%, 53%, and 53% respectively. However, there were a large number of unique genes also in respective transcriptomes (JA > 8500, K⁺ > 2300; Figure 4B). Furthermore, JA‐modulated transcriptome was compared across different levels of K⁺ deficiencies, and more than 67% of overlapping genes exhibited similar expression patterns (Figure 4C). The analysis of the shared DEGs revealed significant enrichment of JA signalling, emphasising the potential interaction between JA signalling in coordinating plant responses to K⁺ deficiency. The significant enrichment of metal ion transport and homoeostasis was also seen, suggesting compensation for K⁺ deficiency by other metal ions (Figure 4C,D). Furthermore, the genes' enrichment in response to stress, stimulus and wounding implies potential crosstalk with plant responses to K⁺ deficiency (Figure 4C,D). Some of the genes highlighted in the meta‐analysis (Figure 4D; Table S3) like TIFY domain‐containing protein 9 (TIFY9), IPT2, Ca ²⁺ ‐dependent protein kinase 21 (CPK21), Empty pericarp 1 (EMP1) and Late embryogenesis abundant protein 17 (LEA17), are known to be either involved in hormonal pathways or in stress tolerance. Taken together, we propose to prioritise the targeting of these genes related to ‘K⁺‐JA’ crosstalk for optimising the crop performance under challenging field conditions, including those of K⁺ deficiency.

Figure 4.

Similarities between hormonal signalling pathways and potassium (K⁺) deficiency response in rice seedlings. (A) The transcriptional response to supplementation of hormones abscisic acid (ABA), brassinolide (BL), cytokinin (CK), gibberellic acid (GA), auxin (IAA) and jasmonic acid (JA) was compared to different levels of K⁺ deficiency (1/4, 1/16 and 1/64). The maximum overlap of 53% was with JA, with a regression value (R ²) of 0.35 at 1/16^th K⁺ reduction, followed by ABA showing a 45% overlap at 1/64K⁺ reduction. (B) Venn diagram showing the unique DEGs and shared DEGs under K⁺ deficiency and JA hormone supplementation conditions. The total number of overlapping genes, along with the percentage of overlap with the K⁺ transcriptome at different levels of K⁺ deficiency, is provided at the centre. (C) Graphical representation of similar expression tendency amongst the shared DEGs. The greatest similarity of the JA transcriptome was observed with a 1/16^th K⁺ reduction, exhibiting 89% upregulated and 81% downregulated genes in the shared DEGs. (D) Furthermore, the common genes were filtered based on values of |logfc| > 1.5, and protein‐protein enrichment (PPI) was conducted for network construction (gene details in Table S3). The colour in the circle corresponds to the biological process it represents, (E) with top enriched terms further delineated. [Color figure can be viewed at wileyonlinelibrary.com]

5. Conclusions and Way Forward

Plants possess intricate signalling mechanisms to adapt under K⁺ deficiency conditions. The major components that function to restore K⁺ homoeostasis include high‐affinity K⁺ transporters that are majorly regulated through CBL‐CIPKs, ROS and phytohormones, including JA, ABA, ET, CK, auxin, GA and SA. These hormonal networks not only regulate K⁺ uptake and distribution but also modulate RSA, stomatal behaviour, antioxidant defence and crosstalk with other nutrient and stress responses. Considering the K⁺‐hormone crosstalk, many genetic candidates from different hormone signalling pathways have been genetically manipulated to enhance plant tolerance to K⁺ deficiency and general abiotic stress tolerance. However, the success stories under the realistic multi‐stress field scenarios are still limited. Towards this, a meta‐analysis highlighted the significant overlap between K⁺deficiency and JA‐dependent signalling and genes highlighted could be used for future crop improvement programs. Moreover, gene(s) related to ‘K⁺‐JA’ crosstalk could also be prioritised over hormones for genetic manipulation studies, using single and/or multi‐components regulatory hubs like (SCF^COI1)‐JAZ regulatory module for developing high‐KUE crops in future. In addition, the novel quantitative trait loci (QTLs) should be identified for K⁺‐JA crosstalk, which can streamline molecular breeding efforts towards incorporating KUE traits into the existing stress‐tolerant varieties. Such an approach of integrating K⁺ deficiency with other biotic/abiotic stress responses will lead to the development of crops with optimised nutrient‐use‐efficiency and stress resilience. In addition, there has always been a technical challenge in doing phenotyping under realistic field conditions, especially for RSA‐related traits. A concerted research effort is required to quantify root‐system architecture in natural accessions in soils that are naturally deficient in K⁺ and then identify the causal genes/single‐nucleotide polymorphisms using genome‐wide association studies. The genetic factors identified using this approach will better guide marker‐assisted breeding programs as well as genetic engineering programs for developing high‐KUE crops.

Furthermore, nanotechnology is rapidly transforming nutrient delivery systems, including K⁺ fertilisation. The nano‐formulations, such as nano‐K₂SiO₃ and nano‐K₁₈Mo₈O₃₃, have improved K⁺ utilisation efficiency to 80%, enhanced root activity, and increased seed nutritional quality compared to conventional K₂SO₄ fertilisers in Glycine max (soybean), along with soil peroxidase and catalase activity (Q. Wang et al. ²⁰²⁴). Similarly, nano‐K₂SO₄, nano‐NPK and K⁺‐based chitosan or silica composites have shown superior outcomes in crops like Medicago sativa (alfalfa), Beta vulgaris (sugar beet) and maize, reducing nutrient leaching and synchronising delivery with crop demand (El‐Sharkawy et al. ²⁰¹⁷; Kumaraswamy et al. ²⁰²¹; HAMED et al. ²⁰²⁵). Therefore, nano‐based fertilisers can enhance root uptake and reduce K⁺ loss through controlled‐release mechanisms and support antioxidative enzyme activities. Such sustainable agricultural practices must also be optimised alongside genetic advancements. Incorporating crop rotation and cover crops like legumes can enhance soil K⁺ availability naturally, reducing the need for chemical fertilisers. These comprehensive approaches can be used to enhance food security addressing the urgent need for efficient nutrient management in the face of climate change and increasing population pressures.

Conflicts of Interest

The authors declare no conflicts of interest.

Supporting information

Supplementary Table S1: Detailed information of year wise production of cereals and their potassium (K⁺) fertilizer consumption.

Supplementary Table S2: Gene modifications to combat low K⁺ responses in crop plants.

Supplementary Table S3: Annotation of genes for Figure 4.

Mishra, S. , Bisht D., Amtmann A., Srivastava A. K., and Pandey G. K.. 2026. “Potassium Deficiency and Hormone Signalling in Plants.” Plant, Cell & Environment 49: 2935–2951. 10.1111/pce.70165.

Data Availability Statement

Data used in this manuscript are available in Supplementary Tables S1, S2, and S3.