The Molecular Mechanism of Potassium Absorption, Transport, and Utilization in Rice

Potassium is essential for plant growth and development and stress adaptation. The maintenance of potassium homeostasis involves a series of potassium channels and transporters, which promote the movement of potassium ions (K+) across cell membranes and exhibit complex expression patterns and regulatory mechanisms. Rice is a major food crop in China. The low utilization rate of potassium fertilizer limits the yield and quality of rice. Elucidating the molecular mechanisms of potassium absorption, transport, and utilization is critical in improving potassium utilization efficiency in rice. Although some K+ transporter genes have been identified from rice, research on the regulatory network is still in its infancy. Therefore, this review summarizes the relevant information on K+ channels and transporters in rice, covering the absorption of K+ in the roots, transport to the shoots, the regulation pathways, the relationship between K+ and the salt tolerance of rice, and the synergistic regulation of potassium, nitrogen, and phosphorus signals. The related research on rice potassium nutrition has been comprehensively reviewed, the existing research foundation and the bottleneck problems to be solved in this field have been clarified, and the follow-up key research directions have been pointed out to provide a theoretical framework for the cultivation of potassium-efficient rice.


Introduction
Potassium (K) is the most abundant cation in plant cells, accounting for 2-10% of plant dry weight [1,2].Potassium is essential for plant growth and development as it regulates enzyme activity, photosynthetic efficiency, and osmotic stress response [3].Furthermore, potassium promotes the development of plant sink organs, and the supply of carbon assimilates in sink tissues, thereby increasing crop yield [4,5].Potassium also plays a role in plant root growth and development, stomatal movement, and reactive oxygen species (ROS) metabolism [6].Studies have demonstrated that sufficient potassium promotes plant resistance to diseases (including rice blast) [7].Potassium ions (K + ) have high fluidity in plants, allowing them to travel vast distances through the xylem and phloem and swiftly transition from old to new leaf tissues.These processes are primarily driven through K + channels or potassium transporters on the plasma membrane [8,9].Potassium deficiency on cultivated land in China results in a low potassium utilization rate, limiting the sustainable development of agricultural production [10].Therefore, the urgent need to improve K + utilization efficiency in plants is pegged on in-depth research of the molecular mechanism of plant response to K + deficiency.Plants respond to variations in external K + concentration.As a signal molecule, K + is delivered to the cytoplasm via K + channels or potassium transporters, and the complex regulatory network maintains K + homeostasis in cells, boosting the adaptability to potassium deficiency.As a result, elucidating the molecular regulatory mechanisms of K + channels and potassium transporters has traditionally been the research focus in this field.
Five families (shaker-type K + channel, TPK-type K + channel, HKT transporter, CPA reverse transporter, and KUP/HAK/KT transporter) have been revealed to be involved in K + transport in plants, with shaker-type K + channels and KUP/HAK/KT transporters being particularly significant [11][12][13].Current research on K + channels and potassium transporters primarily focuses on the model plant Arabidopsis thaliana, with limited reports in rice.The present review systematically describes and summarizes the biological functions and regulatory networks of K + channels and transporters in rice and provides a theoretical basis for cultivating novel potassium-efficient rice cultivars.

Expression Patterns of K + Channels and Transporters in Rice
The structure of shaker-type K + channel proteins in plants and Drosophila is highly similar [14].Plant shaker-type K + channels are classified into inward K + , outward K + , and weak rectifier K + channels based on voltage dependency and K + transmembrane movement direction [15].The Arabidopsis genome contains nine shaker-type K + channels, of which AtAKT1 is the earliest cloned, mainly expressed in root hairs and the root endodermis [16,17].AtAKT2 is mainly expressed in the phloem and xylem of the shoot [18].AtSKOR and AtGORK are mainly expressed in vascular tissues of Arabidopsis roots [19].AtKAT1, AtKAT2 and AtKAT3 are mainly expressed in guard cells [20].The rice genome contains seven shaker-type K + channels, with them being most expressed in the shoots [21][22][23] (Table 1).The inward K + channel OsAKT1 is primarily expressed in the roots, mediating K + absorption [21,22].OsAKT2 is mainly expressed in mature leaves, sheaths, internodes, and glumes [23].The outward K + channel OsSKOR is primarily expressed in the vascular tissues of rice roots, flowers, and seed shields, whereas OsGORK is expressed in various rice tissues but is most abundant in flowers [24,25].OsKAT1 expression is nearly undetectable in rice roots and stems, but the expression levels of OsKAT2 and OsKAT3 are higher in leaves and sheaths [26].Although the expression patterns of shaker-type K + channels in Arabidopsis and rice are similar, their functions in participating in biotic and abiotic stress responses are different [7,22,27].
Six TPK family genes were found in Arabidopsis thaliana.Among them, AtTPK1 was highly expressed in the root tip, vascular tissue, and pollen, AtTPK3 was mainly expressed in the root tip and pollen, AtTPK4 was highly expressed in pollen, and AtTPK5 and AtKCO3 were expressed in the vascular tissue [28].Rice contains two members of the TPK family, OsTPKa and OsTPKb, which are expressed in nearly all tissues [29] (Table 1).
There are 13 HAK/KUP/KT family members in Arabidopsis thaliana.AtKUP2 is highly expressed in flowers.AtKUP3 and AtKUP4 are highly expressed in developing siliques.AtKUP5, AtKUP6, AtKUP7, AtKUP8, AtKUP10, and AtKUP12 are expressed in roots and leaves.AtKUP11 has a higher expression level in the reproductive growth stage [30].AtHAK5 is the most widely studied in this family, and its expression level in roots is higher [31][32][33].HAK/KUP/KT is the largest K + transporter family in rice, with 27 members [34] (Table 1).Rice HAK family members, including OsHAK1, OsHAK5, Os-HAK7, OsHAK8, OsHAK12, OsHAK16, and OsHAK18, have higher expression levels in roots [34][35][36][37][38][39][40][41][42][43][44] (Table 1).OsHAK5 is expressed in numerous rice tissues, with higher expression levels in the epidermis, vascular tissue, and mesophyll cells of the root system [38].OsHAK21 is highly expressed in the roots and leaves of seedlings, as well as in the vascular bundles of anthers and leaf sheaths [45].OsHAK26 is primarily expressed in rice anthers and seed coats [46].The response of AtHAK5 and OsHAK5 to low potassium stress was similar [32,33], and both were induced by high salt [34,39], indicating that both genes may be involved in the maintenance of low potassium homeostasis and salt stress response.Plant HKT transporters mediate K + transport, Na + transport, and Na + -K + co-transport.There is only one specific Na + transporter gene AtHKT1;1 in Arabidopsis, which is mainly expressed in the vascular system of the roots and leaves [47].The rice genome contains eight OsHKT genes (Table 1).OsHKT1;1 is primarily expressed in the leaf phloem [48].OsHKT1;3 is highly expressed in the rice shoot [49].OsHKT1;4 is primarily expressed in leaf sheaths [50].OsHKT1;5 is highly expressed in rice roots [51].OsHKT2;1 is expressed in the cortex, endodermis, and the vascular bundle sheath of roots [52].OsHKT2;4 is expressed in all rice tissues [53] (Table 1).The HKT1 family genes in rice are expressed in roots and shoots, which is similar to the expression pattern of AtHKT1;1 in Arabidopsis.However, the HKT2 family gene OsHKT2;1 in rice is induced by low potassium and participates in the absorption of Na + in roots [52], indicating that HKT family genes are involved in the regulation of Na + /K + homeostasis in plants.
The NHX transporters are Na + /H + antiporters located on the vacuolar membrane.They have been studied in Arabidopsis thaliana in depth and have eight members.Among them, AtNHX1 and AtNHX2 have high homology and are mainly expressed in roots, shoots, and seedlings.The expression levels of AtNHX3, AtNHX4, and AtNHX6 in roots and shoots are low [54].There are five members in rice; OsNHX1 and OsNHX2 exhibit higher transcription levels in rice panicles and flag leaf sheaths.OsNHX5 is significantly expressed in flag leaves [55] (Table 1).The expression of NHX family genes in Arabidopsis and rice was significantly induced by high salt, indicating that they were involved in the salt stress response of plants.The specific functions will be elaborated upon in the subsequent chapters.
The temporal and spatial expression patterns of the above K + channel and transporter family members and their responses to external potassium concentrations were significantly different, indicating that they have unique and diverse functions in the maintenance of potassium homeostasis and plant growth and development in rice.The biological functions and regulatory mechanisms of related genes will be described in detail from the aspects of root K + absorption, root K + transport, K + transport to the shoot, and K + distribution in various organs.

K + Absorption in Rice Roots
Plant roots have the most direct touch with the soil and are responsible for the majority of nutrient absorption.As a result, the roots first perceive changes in the external K + concentration.The absorption of water and other nutrients from the soil by Arabidopsis occurs first through the epidermal, cortical, and endodermal cells of the root system and then into the vascular tissue [56].Low potassium can promote the formation of Casparian strips in the endodermis of the roots [57][58][59].As an important physical barrier, the Casparian strip controls the entry of water and nutrients into the stele through the endodermis cells [60].The expression of AtCIPK25 was significantly induced in the root endodermis under anaerobic conditions.AtCIPK25 regulates potassium homeostasis and enhances stress resistance under hypoxic conditions by interacting with AtAKT1 [61].
In addition to the direct effect of root architecture on K + uptake by plants, the K + absorption system also plays an important role.Plants have two distinct K + absorption systems: the low-affinity potassium system is primarily involved when the K + concentration exceeds 1.0 mM, whereas the high-affinity potassium system functions when the external K + concentration is less than 0.2 mM [62,63].In general, the high-affinity potassium transport system belongs to the active absorption process of reverse chemical gradient and energy consumption, which is primarily mediated by potassium transporters, whereas the low-affinity potassium transport system belongs to the passive absorption process, which is primarily achieved by potassium channels [64].Mounting research has established that plants respond to variations in external K + concentrations via these two differing affinity potassium absorption systems [65].
Shaker-type K + channels and KUP/HAK/KT transporters in higher plants are critical for root K + uptake (Figure 1).AtAKT1 is the first cloned shaker-type K + channel in Arabidopsis, and it mediates K + uptake by the roots [66].OsAKT1 is the rice homolog of AtAKT1 and belongs to the inward K + channel located on the plasma membrane, and being primarily expressed in the roots, mediates K + absorption in rice roots [21].The decrease in K + absorption and content in the osakt1 rice mutant leads to the sensitivity of the mutant to low potassium and the inhibition of growth and development [21].Overexpression of OsAKT1 increases rice tolerance to osmotic and drought stress by boosting K + absorption, increasing K + accumulation in the roots, and decreasing the Na + /K + ratio [22].
transport system belongs to the active absorption process of reverse chemical gradient and energy consumption, which is primarily mediated by potassium transporters, whereas the low-affinity potassium transport system belongs to the passive absorption process, which is primarily achieved by potassium channels [64].Mounting research has established that plants respond to variations in external K + concentrations via these two differing affinity potassium absorption systems [65].
Shaker-type K + channels and KUP/HAK/KT transporters in higher plants are critical for root K + uptake (Figure 1).AtAKT1 is the first cloned shaker-type K + channel in Arabidopsis, and it mediates K + uptake by the roots [66].OsAKT1 is the rice homolog of AtAKT1 and belongs to the inward K + channel located on the plasma membrane, and being primarily expressed in the roots, mediates K + absorption in rice roots [21].The decrease in K + absorption and content in the osakt1 rice mutant leads to the sensitivity of the mutant to low potassium and the inhibition of growth and development [21].Overexpression of OsAKT1 increases rice tolerance to osmotic and drought stress by boosting K + absorption, increasing K + accumulation in the roots, and decreasing the Na + /K + ratio [22].K + uptake in plant roots is facilitated by particular KUP/HAK/KT transporters.The KUP/HAK/KT family genes in Arabidopsis affect the growth of root hairs, and AtKUP4 is involved in the absorption of K + by the roots [30].The high-affinity K + transporter OsHAK1 is primarily expressed in the epidermis and vascular cells of the root system.Potassium deficiency stimulates K + absorption in the root system and significantly induces OsHAK1 K + uptake in plant roots is facilitated by particular KUP/HAK/KT transporters.The KUP/HAK/KT family genes in Arabidopsis affect the growth of root hairs, and AtKUP4 is involved in the absorption of K + by the roots [30].The high-affinity K + transporter OsHAK1 is primarily expressed in the epidermis and vascular cells of the root system.Potassium deficiency stimulates K + absorption in the root system and significantly induces OsHAK1 expression [37].OsHAK5 is highly expressed in the root epidermis and stele.OsHAK5 contributes to root K + uptake under low-potassium conditions, and OsHAK5 overexpression significantly increases K + uptake and transport [38].OsHAK21 promotes K + absorption and salt tolerance in germinated rice seeds under salt stress [45].In addition, OsHAK8 and OsHAK16 are highly expressed in rice roots and are critical in the absorption and transport of K + [41,43].AtAKT1 and AtHAK5 play a dominant role in root K + uptake in Arabidopsis.AtHAK5 is the only transporter that mediates K + uptake in the roots at very low external K concentrations (<20 µM) [32,33].However, under low-potassium stress, OsHAK1, OsHAK5, OsHAK8, OsHAK16, and OsHAK21 in rice are involved in high-affinity K + uptake; thus, the following questions arise: which transporter plays a leading role?How do these transporters synergistically regulate K + uptake in rice roots?Further research is still needed.
Similar to other higher plants, rice also has two different types of potassium absorption systems.The inward shaker-type K + channels mainly mediate low-affinity potassium absorption, while the KUP/HAK/KT family is mainly involved in high-affinity potassium absorption in the roots, but this distinction is not absolute.For example, OsHAK1 is also involved in root potassium absorption under 1 mM K + conditions.Future research can focus on how rice roots perceive changes in external K + concentration and accurately regulate the division and collaboration of K + channels and transporters through signal transduction.The optimization of core functional genes or the exploration of excellent allelic variations can maximize the range of external K + concentration that can be absorbed by the roots and improve the utilization efficiency of soil potassium.

K + Transport from Rice Roots to Shoots
K + absorbed by plant roots is transferred to the shoots via xylem K + channels and K + transporters [67].The outward K + channel AtSKOR in Arabidopsis mediates K + transport from the xylem to the shoots [68].Nitrate transporter AtNRT1.5 may indirectly affect K + transport from the roots to shoots through AtSKOR [69].The Arabidopsis K + transporter AtKUP7 is also involved in the transport of K + in the xylem, affecting the long-distance transport of K + [70].OsGORK plays a crucial role in stomatal movement and K + loading in the xylem in rice.The K + transported from roots to shoots through the xylem is decreased in the osgork mutant, as is the K + level in shoots (25% decrease) [25].Some KUP/HAK/KT transporters also participate in K + transport to the shoots (Figure 1).OsHAK5, OsHAK8, and OsHAK16 promote K + transport from the roots to shoots under K-deficient conditions [38,41,43].Furthermore, OsHAK21 is highly expressed in xylem parenchyma and endodermis cells, indicating that OsHAK21 potentially plays a role in K + delivery to the shoots [45].Low potassium promotes the expression of low-affinity nitrate transporter OsNPF2.4 in the leaves, in addition to K + channels and K + transporters.The K + content of the osnpf2.4mutant increases in a high NO −  3 environment, which indirectly influences K + reuse in the roots and stems, indicating that OsNPF2.4 may mediate the transport and utilization of K + to the shoots [71].AtSKOR and AtKUP7 in Arabidopsis are involved in the long-distance transport of K + , while the specific function of OsSKOR in rice has not been reported in detail and needs to be further identified.
To date, only a few K + channels and transporters have been identified in rice that have the function of transporting K + to the shoots.The long-distance transport of K + is the premise of K accumulation in the shoots of rice.It is the basis for the normal growth of plants and improvement of low potassium tolerance.Therefore, in the future, new functional genes involved in K + transport to the shoots of rice can be further explored, which is conducive to further improving the molecular mechanism of rice response to low-potassium stress.

K + Transport in Rice Leaves
K + is transported to different tissues and organs following absorption by plant roots for effective utilization via the in vivo transport system.The shaker-type K + channel AtAKT2 in Arabidopsis is a weak rectifier K + channel that primarily mediates K + loading or unloading in the phloem, allowing for long-distance transport in plants [72,73].OsAKT2 is the rice homolog of AtAKT2 and belongs to the weak rectifier K + channel family.OsAKT2 disruption decreases the K + content in phloem sap, indicating that OsAKT2 plays a crucial role in the phloem loading process of K + [23] (Figure 1).The osakt2 mutant had higher K + accumulation in the old leaves than the wild type (WT) but decreased K + accumulation in the young leaves, indicating that OsAKT2 mediates K + redistribution from the old to the young leaves [23].The AKT2 gene in Arabidopsis and rice has similar functions and plays a role in the phloem loading of K + .OsAKT2 in rice is also involved in the redistribution of K + and improves the utilization efficiency of K + , which is beneficial to improving rice yield and quality.

K + Transport in Rice Guard Cells
The stoma is a critical location in plant leaves for water vapor exchange and CO 2 acquisition.The number, density, and opening and closing of stomata are crucial indicators of plant drought stress response, and K + channels and K + transporters in rice guard cells can regulate stomatal opening [74].Guard cells in Arabidopsis thaliana have elevated expression levels of the inward shaker-type K + channels AtKAT1 and AtKAT2 and the outward K + channel AtGORK; these channels regulate stomatal opening and closing by mediating K + transmembrane influx and efflux [75,76].The shaker-type K + channels, OsKAT2, and OsKAT3 in rice are primarily expressed in guard cells, and the OsKAT2 influx-type K + channel activity is comparable to that of Arabidopsis AtKAT1 [26].There is no typical K + channel activity despite the strong homology between OsKAT3 and OsKAT2.The possibility of restoring the channel activity of OsKAT3 by removing its C-terminal domain indicates that the C-terminal region functions as a regulatory domain suppressing channel activity [26].OsGORK is expressed in both the guard and subsidiary guard cells of rice stomata and encodes a slowly activated and outwardly rectifying K + channel.The loss of OsGORK function decreases K + efflux from guard cells, slows stomatal closure, and increases the rate of water loss [25].

K + Transport during Rice Pollen Development
Pollen development, a crucial aspect of plant sexual reproduction, also significantly affects yield [77]. K + stimulates cell expansion, hydrates tissues, creates swelling pressure, and accelerates the formation of pollen tubes [78,79].The inward K + channel AtSPIK is expressed explicitly in Arabidopsis pollen, inhibiting the pollen germination and pollen tube growth of atspik mutants [80,81].The plasma membrane contains the shaker-type K + channel ZmKZM1 in maize and OsAKT1.2 in rice, which regulates pollen development, pollen tube growth, and rupture [82,83] (Figure 1).Arabidopsis AtTPK4 regulates K + homeostasis and pollen tube growth [84].While the functions of OsTPKa and OsTPKb in rice in response to salt stress have been documented, their potential regulatory role in pollen development is unclear [85].OsHAK1 is involved in K + distribution in rice floral organs.The loss of OsHAK1 function leads to decreased pollen viability and fertility [37].OsHAK5 is involved in acquiring K + by pollen grains in rice [46].OsHAK26, found in the Golgi apparatus, is involved in the formation of pollen walls and is critical for pollen development and fertility [46].The interaction of rice receptor-like kinase OsRUPO (ruptured pollen tube) with OsHAK1, OsHAK19, and OsHAK20 mediates the growth and integrity of pollen tubes by maintaining K + homeostasis [86].
The mobility of K + is conducive to its transfer in various organs of rice.K + channels and transporters are involved in the redistribution of K + in rice.At present, most studies focus on revealing the function of K + transporters in an independent organ (such as guard cells and pollen), while there are few studies on the movement or redistribution of K + between multiple tissues or organs.The movement of K + from senescent tissue to newborn tissue can meet the basic growth needs of plants and promote the improvement of low potassium tolerance and potassium utilization efficiency.However, there is a lack of analysis of related functional genes and regulatory networks.Follow-up studies can further explore this and provide feasible solutions for potassium-efficient rice breeding.

Regulation of K + Channels and Transporters
Arabidopsis primarily regulates the expression or activity of downstream functional genes or proteins at the transcriptional and post-transcriptional levels in response to low potassium stress, hence regulating the absorption, transport, and redistribution of K + in plants.The CBL-CIPK complex plays a role in the post-transcriptional regulation of K + channels: AtCBL1/9 interacts with AtCIPK23 and recruits it to the plasma membrane.AtCIPK23 phosphorylates AtAKT1 on the plasma membrane, and this phosphorylation increases in potassium-deficient plants, allowing them to absorb more K + from the environment [87,88] (Figure 2A).The AtCBL4-AtCIPK6 complex plays a role in AtAKT2 regulation, recruiting it from the cytoplasm to the plasma membrane and increasing the AtAKT2-mediated potassium current [73].The AtCBL2/3-AtCIPK3/9/23/26 complex promotes K + efflux from vacuoles to the cytoplasm by activating the potassium channel TPK on vacuoles [89] (Figure 2A).Although post-transcriptional regulation of KT/KUP/HAK transporters has been documented, including AtHAK5 activation of AtCBL1-AtCIPK23 phosphorylation [90], further research has established that potassium transporters are primarily regulated at the transcriptional level; multiple transcription factors, including AtRAP2.11,AtDDF2, AtJLO, AtTFII_A, AtbHLH121, AtARF2 and AtMYB77, regulate AtHAK5 expression [91,92] (Figure 2A).The low-potassium phosphorylation of AtARF2 can alleviate its transcriptional inhibition of AtHAK5, while AtMYB77 can increase AtHAK5 expression by binding to the AtHAK5 promoter, increasing plant high-affinity potassium absorption and low potassium tolerance [93,94].AtMYB59 is a positive transcription regulator of AtNRT1.5.The transcription and protein levels of AtMYB59 are reduced, and AtNRT1.5 expression is suppressed under low-potassium stress, resulting in a blockage of K + transport from Arabidopsis roots to the crown [95].In addition, yeast one-hybrid experiments in wheat and maize revealed that TaNAC71 interacted with the TaHAK1 promoter, while ZmRAP2.11and ZmARF2 interacted with the ZmHAK1 promoter [96,97].

Regulation of K + Channels and Transporters
Arabidopsis primarily regulates the expression or activity of downstream functional genes or proteins at the transcriptional and post-transcriptional levels in response to low potassium stress, hence regulating the absorption, transport, and redistribution of K + in plants.The CBL-CIPK complex plays a role in the post-transcriptional regulation of K + channels: AtCBL1/9 interacts with AtCIPK23 and recruits it to the plasma membrane.AtCIPK23 phosphorylates AtAKT1 on the plasma membrane, and this phosphorylation increases in potassium-deficient plants, allowing them to absorb more K + from the environment [87,88] (Figure 2A).The AtCBL4-AtCIPK6 complex plays a role in AtAKT2 regulation, recruiting it from the cytoplasm to the plasma membrane and increasing the AtAKT2-mediated potassium current [73].The AtCBL2/3-AtCIPK3/9/23/26 complex promotes K + efflux from vacuoles to the cytoplasm by activating the potassium channel TPK on vacuoles [89] (Figure 2A).Although post-transcriptional regulation of KT/KUP/HAK transporters has been documented, including AtHAK5 activation of AtCBL1-AtCIPK23 phosphorylation [90], further research has established that potassium transporters are primarily regulated at the transcriptional level; multiple transcription factors, including AtRAP2.11,AtDDF2, AtJLO, AtTFII_A, AtbHLH121, AtARF2 and AtMYB77, regulate AtHAK5 expression [91,92] (Figure 2A).The low-potassium phosphorylation of AtARF2 can alleviate its transcriptional inhibition of AtHAK5, while AtMYB77 can increase AtHAK5 expression by binding to the AtHAK5 promoter, increasing plant high-affinity potassium absorption and low potassium tolerance [93,94].AtMYB59 is a positive transcription regulator of AtNRT1.5.The transcription and protein levels of AtMYB59 are reduced, and AtNRT1.5 expression is suppressed under low-potassium stress, resulting in a blockage of K + transport from Arabidopsis roots to the crown [95].In addition, yeast onehybrid experiments in wheat and maize revealed that TaNAC71 interacted with the TaHAK1 promoter, while ZmRAP2.11and ZmARF2 interacted with the ZmHAK1 promoter [96,97].Until recently, the molecular regulation pathway of potassium nutrition in rice has been mainly reported at the post-transcriptional level: OsCBL1-OsCIPK23 regulates the activity of OsAKT1 and OsAKT2 [21,98].OsHAK21 interacts with the OsCYB5-2 protein to stabilize OsHAK21-mediated K + uptake and to maintain intracellular K + /Na + balance [99] (Figure 2B).Transcriptional regulation is solely reported in the potassium transporter HKT.HKT proteins are classified into two categories based on the amino acid differences and transport characteristics in their first pore domain.Class I members (HKT1) are Na + transporters, while class II members (HKT2) are Na + /K + co-transporters [100].Previous research has focused on the transcriptional regulation of OsHKT1: OsSUVH7, OsBAG4, and OsMYB106 to form a transcriptional complex to activate OsHKT1;5 expression under salt stress [101].OsMYBc binds to the OsHKT1;1 promoter and regulates Na + accumulation in the shoots [48,102] (Figure 2B).
In rice, only two post-translational regulation pathways of potassium nutrition, OsCBL1-OsCIPK23-OsAKT1/OsAKT2 and OsHAK21-OsCYB5-2, have been found, and only the transcriptional regulation mechanisms of Na + transporter genes OsHKT1;1, OsHKT1;5 and OsHKT2;1 have been clarified.The fine regulation of potassium nutrition at the transcriptional level in rice and its relationship with low-potassium stress tolerance have not been reported.Therefore, it is of great significance to further explore the key components of the rice potassium nutrition regulation pathway at the transcriptional level and analyze its molecular mechanism to improve the regulatory network of rice in response to low potassium.

Relationship between Potassium and Salt Stress Response in Rice
Intracellular K + /Na + equilibrium is a crucial indicator of salt tolerance when plants are subjected to salt stress [103].High Na + concentration competes with K + for cell entry, disrupting K + /Na + equilibrium.In this view, maintaining a low Na + concentration and normal K + /Na + balance is critical for salt stress resistance [104][105][106][107]. Increased K + uptake in high-salt environments can enhance plant salt tolerance [108,109].In addition, salt stress can also induce an increase in endogenous NO in plants, promote the ion exchange of Na + /H + , and the accumulation of K + in roots and leaves, thereby improving the salt tolerance of plants [110].
HKT transporters are crucial in plant K + /Na + transport and salt stress response [111].Under salt stress, the athkt1;1 Arabidopsis mutant accumulated excessive Na + and leaf chlorosis [112].AtHKT1;1 protected the leaves from salt stress damage by mediating the removal of Na + from the xylem [113].Rice OsHKT1;1 plays a role in regulating Na + content and reducing Na + toxicity in leaves.The oshkt1;1 mutant is hypersensitive to salt stress, accumulates more Na + in vivo, and inhibits plant growth [48].OsHKT1;4 is responsible for Na + unloading in the xylem, mediates Na + transport in the shoots, promotes Na + excretion from the leaves, and improves the salt tolerance of rice during reproductive development [50] (Figure 3).OsHKT1;5 is primarily expressed in parenchyma cells around the xylem of rice.OsHKT1;5 reflows excessive Na + from the shoots to the roots through xylem unloading under salt stress, lowering Na + toxicity and improving salt tolerance in rice [51].OsHKT2;1 promotes root Na + absorption under K + -deficient conditions, and Na + temporarily substitutes K + to support plant growth [49,52].The OsPRR73 protein can bind to the promoter of OsHKT2;1, inhibit OsHKT2;1 transcription by recruiting histone deacetylase HDAC10, decrease Na + absorption in a specific time, and regulate the salt tolerance of rice by regulating Na + homeostasis and ROS levels [114].AtHKT1;1 in Arabidopsis and OsHKT1;1, OsHKT1;4, and OsHKT1;5 in rice belong to the class I HKT transporter family, which have high similarity in preventing excessive accumulation of Na + in the leaves and enhancing plant salt tolerance by increasing the K + /Na + ratio [51,115] (Figure 3).
HAK transporters also exert crucial functions in plant response to salt stress (Figure 3).Overexpression of OsHAK1 and OsHAK5 enhances rice tolerance to salt stress by promoting K + uptake and transport and maintaining K + /Na + equilibrium [36,39].OsHAK12 mediates Na + transport from the roots to shoots to improve salt tolerance under salt stress [42], while OsHAK18 enhances salt tolerance by mediating Na + redistribution from the shoots to roots [44].OsHAK21 promotes the absorption of K + and Na + during rice seed germination, induces the expression of abscisic acid (ABA) signaling pathway genes, increases ABA biosynthesis, and inhibits ROS accumulation, consequently enhancing salt tolerance during seed germination [45].OsHAK20 and OsHAK13 were identified as critical quantitative trait loci (QTLs) related to salt tolerance during the seedling and flowering stages, respectively, using high-resolution genetic maps.These two genes can be utilized as molecular markers in marker-assisted selection to develop highly resistant rice [116].HAK transporters also exert crucial functions in plant response to salt stress (Figure 3).Overexpression of OsHAK1 and OsHAK5 enhances rice tolerance to salt stress by promoting K + uptake and transport and maintaining K + /Na + equilibrium [36,39].OsHAK12 mediates Na + transport from the roots to shoots to improve salt tolerance under salt stress [42], while OsHAK18 enhances salt tolerance by mediating Na + redistribution from the shoots to roots [44].OsHAK21 promotes the absorption of K + and Na + during rice seed germination, induces the expression of abscisic acid (ABA) signaling pathway genes, increases ABA biosynthesis, and inhibits ROS accumulation, consequently enhancing salt tolerance during seed germination [45].OsHAK20 and OsHAK13 were identified as critical quantitative trait loci (QTLs) related to salt tolerance during the seedling and flowering stages, respectively, using high-resolution genetic maps.These two genes can be utilized as molecular markers in marker-assisted selection to develop highly resistant rice [116].
In addition, other K + channels and transporters are involved in the regulation of Na + /K + homeostasis under salt stress (Figure 3): OsKAT1 overexpression improves rice salt tolerance by increasing intracellular K + content [117].The vacuolar Na + /H + antiporter NHX family genes play an important role in plant salt stress response.Under high-salt conditions, AtNHX1 overexpression plants have a stronger ability to maintain intracellular K + homeostasis, thereby improving salt tolerance [118].Under salt stress, K + accumulation decreased and Na + content increased in the leaves of nhx1 nhx2 mutants, indicating that AtNHX1 and AtNHX2 may be involved in the maintenance of Na + /K + homeostasis [119].In addition, the nhx5 nhx6 mutant was also sensitive to salt stress [120].AtNHX7/AtSOS1 located on the plasma membrane is regulated by the phosphorylation of the upstream AtSOS2-AtSOS3 complex [121] and actively transports Na + to expel Na + from the roots [122].Under high-salt conditions, the expression of AtCycC1;1 was inhibited, while the expression of AtWRKY75 was activated, resulting in increased recruitment of the AtSOS1 promoter by RNAP II, which promoted the expression of AtSOS1 and enhanced salt tolerance [123] (Figure 3A).OsNHX1 and OsNHX2 are induced by salt stress in rice, and the accumulation of Na + and K + in the cytoplasm is regulated by vacuolar compartmentation.Overexpression of OsNHX1 significantly improves the salt tolerance of rice [109,111].In rice, OsSOS3 also interacts with OsSOS2 and phosphorylates the OsSOS2 protein, thereby activating OsSOS1 on the plasma membrane, resulting in Na + efflux from cells and maintaining the Na + /K + balance in cells [124] (Figure 3B).K + channels and transporters in Arabidopsis and rice maintain intracellular K + /Na + homeostasis and normal turgor pressure by regulating the K + /Na + ratio in vivo, prevent cells In addition, other K + channels and transporters are involved in the regulation of Na + /K + homeostasis under salt stress (Figure 3): OsKAT1 overexpression improves rice salt tolerance by increasing intracellular K + content [117].The vacuolar Na + /H + antiporter NHX family genes play an important role in plant salt stress response.Under high-salt conditions, AtNHX1 overexpression plants have a stronger ability to maintain intracellular K + homeostasis, thereby improving salt tolerance [118].Under salt stress, K + accumulation decreased and Na + content increased in the leaves of nhx1 nhx2 mutants, indicating that AtNHX1 and AtNHX2 may be involved in the maintenance of Na + /K + homeostasis [119].In addition, the nhx5 nhx6 mutant was also sensitive to salt stress [120].AtNHX7/AtSOS1 located on the plasma membrane is regulated by the phosphorylation of the upstream AtSOS2-AtSOS3 complex [121] and actively transports Na + to expel Na + from the roots [122].Under high-salt conditions, the expression of AtCycC1;1 was inhibited, while the expression of AtWRKY75 was activated, resulting in increased recruitment of the AtSOS1 promoter by RNAP II, which promoted the expression of AtSOS1 and enhanced salt tolerance [123] (Figure 3A).OsNHX1 and OsNHX2 are induced by salt stress in rice, and the accumulation of Na + and K + in the cytoplasm is regulated by vacuolar compartmentation.Overexpression of OsNHX1 significantly improves the salt tolerance of rice [109,111].In rice, OsSOS3 also interacts with OsSOS2 and phosphorylates the OsSOS2 protein, thereby activating OsSOS1 on the plasma membrane, resulting in Na + efflux from cells and maintaining the Na + /K + balance in cells [124] (Figure 3B).K + channels and transporters in Arabidopsis and rice maintain intracellular K + /Na + homeostasis and normal turgor pressure by regulating the K + /Na + ratio in vivo, prevent cells from being subjected to ion toxicity and oxidative damage, and coordinate the dynamic balance between growth and development and salt stress adaptation.

Synergistic Regulation of Potassium and Nitrogen
The coordinated application of nitrogen and potassium fertilizers can increase the yield and quality of crops [125].The nitrate transporter AtNRT1.5/NPF7.3 in Arabidopsis thaliana is an H + /K + antiporter involved in K + xylem loading.The atnrt1.5 mutant lacks K + transport to the shoots [69,126].AtCBL1-AtCIPK23 phosphorylates ammonia transporters AtAMT1;1 and AtAMT1;2 to avoid NH + 4 accumulation under an external high concentration of NH + 4 and low potassium conditions [127].OsNPF2.4promotes NO − 3 absorption and long-distance transport.OsNPF2.4expression in the roots and shoots is regulated under low-potassium conditions, indirectly influencing K + reuse [71].OsNRT2.4 and OsAMT1;3 are implicated in the absorption of NO − 3 and NH + 4 in rice, respectively.Low potassium (-K) inhibits their expression, while low nitrogen (-N) or low nitrogen and low potassium (-N-K) induce their expression, indicating that the two genes play different roles in the response to -N and -K [128][129][130].In addition, -N significantly influences the expression of some HAK transporter genes: -N, -K, and -N-K induce the expression of OsHAK1, particularly in the shoots under -N-K conditions [130].-K promotes the expression of OsHAK5, OsHAK16, and OsHAK17, while -N and -N-K significantly inhibit the expression of the three genes [130].Some OsHAKs transporter genes respond to both -K and -N, indicating that they may be involved in the synergistic regulation of potassium and nitrogen, but the specific signal transduction and regulatory pathways need to be further revealed.

Synergistic Regulation of Potassium and Phosphorus
There are limited investigations on the synergistic effect of phosphorus and potassium.The expression of particular transcription factors, MAPK and MAPKK, is rapidly induced following variations in the external potassium or phosphorus concentrations in tomatoes [131].Phosphate transporter OsPHT1;4 is involved in Pi absorption in rice and Pi transport and homeostasis maintenance [132].Low phosphorus (-P), low potassium (-K), and low phosphorus and low potassium (-P-K) were found to significantly induce OsPHT1;4 expression in roots [130].OsPHO1;1 and OsPHO1;3 have the function of phosphorus transport.-P induces the two genes, whereas -K and -P-K inhibit their expression [130].However, the molecular signaling pathways co-regulated by potassium and phosphorus in rice warrant further investigation.

Conclusions and Future Perspectives
The absorption of K + in rice roots and the transport of K + in vivo involves a series of K + channels and transporters.These transporters promote K + movement across cell membranes and exhibit varying expression patterns, subcellular localization, transport affinity, and regulatory mechanisms.Therefore, they serve distinct and diversified functions in rice growth and development and stress adaptability.However, with the research progress on the cloning and functional identification of K + absorption-and transport-related genes, the intricacy of potassium nutrition trait regulation has steadily been recognized.Gene networks regulate all processes from the signal reception, transduction, gene interaction, and expression of functional genes to physiological or morphological changes related to K + transport and distribution, ultimately modifying K + absorption or utilization efficiency.Therefore, potassium nutrition-efficient breeding must be examined from the perspective of the whole signal regulation network.Of note, only the post-transcriptional regulation and modification of potassium channels and transporters have been reported in rice, with no evidence of upstream critical genes in the transcriptional regulation of potassium nutrition.In addition, the AtMYB59-AtNRT1.5 transcriptional regulatory pathway in Arabidopsis is crucial in responding to K + /NO − 3 deficiency and regulating the synergistic transport of potassium and nitrogen.Are there analogous critical genes regulating the synergistic utilization of potassium and nitrogen in rice?Therefore, it is imperative in the future to further investigate new potassium nutrition regulatory genes, reveal the genetic mechanism of maintaining potassium homeostasis in rice, analyze the regulatory network of the synergistic and efficient utilization of potassium, nitrogen, and phosphorus nutrition in rice, and uncover the excellent allelic variation of key functional genes in germplasm resources, explore its utilization value, and provide genetic resources and theoretical support for cultivating new rice varieties with efficient utilization of nutrients.

Figure 1 .
Figure 1.K + channels and transporters involved in K + uptake and transport in Arabidopsis and rice.(A,B) The K + channels or transporters that mediate K + transport in pollen tubes in Arabidopsis (A) or rice (B).(C,D) The K + channels or transporters involved in K + transport from the roots to shoots in Arabidopsis (C) or rice (D).(E,F) The K + channels or transporters involved in root K + uptake in Arabidopsis (E) or rice (F).

Figure 1 .
Figure 1.K + channels and transporters involved in K + uptake and transport in Arabidopsis and rice.(A,B) The K + channels or transporters that mediate K + transport in pollen tubes in Arabidopsis (A) or rice (B).(C,D) The K + channels or transporters involved in K + transport from the roots to shoots in Arabidopsis (C) or rice (D).(E,F) The K + channels or transporters involved in root K + uptake in Arabidopsis (E) or rice (F).

Figure 2 .Figure 2 .
Figure 2. A schematic diagram of the regulatory pathways of K + channels or transporters in Arabidopsis and rice.(A,B) Transcriptional regulation and post-translational regulation pathways of K +Figure 2. A schematic diagram of the regulatory pathways of K + channels or transporters in Arabidopsis and rice.(A,B) Transcriptional regulation and post-translational regulation pathways of K + channels or transporters in Arabidopsis (A) or rice (B)."→" indicates promoting effects."⊥" indicates an inhibitory effect.

Figure 3 .
Figure 3.A schematic diagram of the regulatory pathways of K + channels or transporters involved in salt stress response in Arabidopsis and rice.(A,B) The regulatory pathway of K + channels or transporters involved in salt stress response in Arabidopsis (A) or rice (B)."→" indicates promoting effects."⟂" indicates an inhibitory effect.

Figure 3 .
Figure 3.A schematic diagram of the regulatory pathways of K + channels or transporters involved in salt stress response in Arabidopsis and rice.(A,B) The regulatory pathway of K + channels or transporters involved in salt stress response in Arabidopsis (A) or rice (B)."→" indicates promoting effects."⊥" indicates an inhibitory effect.

Table 1 .
Expression patterns of K + channel and transporter genes in Arabidopsis and rice.