From hidden to visual K deficiency in plants: Integration of subcellular K⁺ distribution and photosynthetic performance

Abstract

The earliest occurrence of chlorosis at the tips of the oldest leaves is widely recognized as a reliable indicator for diagnosing potassium (K) deficiency and determining the need for K fertilizer. However, hidden K deficiency, typically associated with a decrease in individual leaf photosynthetic area, precedes the onset of visible yellowing symptoms. These concealed symptoms pose challenges for the early diagnosis of K deprivation in plants. The two distinct stages of deficiency exhibit different photosynthetic performances, which are speculated to be closely linked to the subcellular K⁺ distribution. This minireview focuses on investigating K⁺ dynamics across subcellular compartments, along with the involvement of functional transporter proteins and ion channels during K deficiency. We propose potential mechanisms by which subcellular K⁺ regulates photosynthetic capacity under both hidden and visual K deficiency conditions, which sheds new light on the diagnosis of K deficiency. Additionally, future research prospects and areas deserving further investigation are also outlined.

Keywords

Hidden K deficiency / Leaf photosynthesis / Leaf photosynthetic area / Subcellular K⁺ distribution / Visual K deficiency

Abbreviations

Not applicable.

Availability of data and materials

Not applicable.

Authors’ contributions

All authors contributed to the review. The first draft of the manuscript was predominantly written by H.G. with assistance of all authors. Z.L., T.R., and J.L. revised the first draft and all the authors approved the final manuscript.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This study was supported by the National Natural Science Foundation of China (32072680), the National Key Research and Development Program of China (2022YFD2301405), the China Agriculture Research System of MOF and MARA (CARS-12), and Fundamental Research Funds for the Central Universities (2662020ZHPY005).

References

[1] Adams, E., Shin, R., 2014. Transport, signaling, and homeostasis of potassium and sodium in plants. J. Integr. Plant Biol. 56, 231-249.

[2] Allen, J., 2002. Photosynthesis of ATP-electrons, proton pumps, rotors, and poise. Cell 110, 273-276.

[3] Amtmann, A., Troufflard, S., Armengaud, P., 2008. The effect of potassium nutrition on pest and disease resistance in plants. Physiol. Plant. 133, 682-691.

[4] Andrés, Z., Pérez-Hormaeche, J., Leidi, E.O., Schlücking, K., Steinhorst, L., McLachlan, D.H., Schumacher, K., Hetherington, A.M., Kudla, J., Cubero, B., Pardo, J.M., 2014. Control of vacuolar dynamics and regulation of stomatal aperture by tonoplast potassium uptake. Proc. Natl. Acad. Sci. U. S. A. 111, E1806-E1814.

[5] Aranda-Sicilia, M.N., Aboukila, A., Armbruster, U., Cagnac, O., Schumann, T., Kunz, H., Jahns, P., Rodríguez-Rosales, M.P., Sze, H., Venema, K., 2016. Envelope K⁺/H⁺ antiporters AtKEA1 and AtKEA 2 function in plastid development. Plant Physiol. 172, 441-449.

[6] Aranda-Sicilia, M.N., Sánchez-Romero, M.E., Rodríguez-Rosales, M.P., Venema, K., 2021. Plastidial transporters KEA1 and KEA 2 at the inner envelope membrane adjust stromal pH in the dark. New Phytol. 229, 2080-2090.

[7] Armbruster, U., Carrillo, L.R., Venema, K., Pavlovic, L., Schmidtmann, E., Kornfeld, A., Jahns, P., Berry, J.A., Kramer, D.M., Jonikas, M.C., 2014. Ion antiport accelerates photosynthetic acclimation in fluctuating light environments. Nat. Commun. 5, 5439.

[8] Armengaud, P., Sulpice, R., Miller, A.J., Stitt, M., Amtmann, A., Gibon, Y., 2009. Multilevel analysis of primary metabolism provides new insights into the role of potassium nutrition for glycolysis and nitrogen assimilation in Arabidopsis roots. Plant Physiol. 150, 772-785.

[9] Bak, G., Lee, E., Lee, Y., Kato, M., Segami, S., Sze, H., Maeshima, M., Hwang, J., Lee, Y., 2013. Rapid structural changes and acidification of guard cell vacuoles during stomatal closure require phosphatidylinositol 3,5-bisphosphate. Plant Cell 25, 2202-2216.

[10] Barragán, V., Leidi, E.O., Andrés, Z., Rubio, L., De Luca, A., Fernández, J.A., Cubero, B., Pardo, J.M., 2012. Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24, 1127-1142.

[11] Bassil, E., Tajima, H., Liang, Y., Ohto, M., Ushijima, K., Nakano, R., Esumi, T., Coku, A., Belmonte, M., Blumwald, E., 2011. The Arabidopsis Na⁺/H⁺ antiporters NHX1 and NHX2 control vacuolar pH and K⁺ homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23, 3482-3497.

[12] Battie-Laclau, P., Laclau, J.P., Beri, C., Mietton, L., Muniz, M.R.A., Arenque, B.C., de Cássia Piccolo, M., Jordan-Meille, L., Bouillet, J.P., Nouvellon, Y., 2014. Photosynthetic and anatomical responses of Eucalyptus grandis leaves to potassium and sodium supply in a field experiment. Plant Cell Environ. 37, 70-81.

[13] Bednarz, C.W., Oosterhuis, D.M., Evans, R.D., 1998. Leaf photosynthesis and carbon isotope discrimination of cotton in response to potassium deficiency. Environ. Exp. Bot. 39, 131-139.

[14] Bose, J., Munns, R., Shabala, S., Gilliham, M., Pogson, B., Tyerman, S.D., 2017. Chloroplast function and ion regulation in plants growing on saline soils: lessons from halophytes. J. Exp. Bot. 68, 3129-3143.

[15] Britto, D.T., Kronzucker, H.J., 2008. Cellular mechanisms of potassium transport in plants. Physiol. Plant. 133, 637-650.

[16] Carraretto, L., Formentin, E., Teardo, E., Checchetto, V., Tomizioli, M., Morosinotto, T., Giacometti, G.M., Finazzi, G., Szabó, I., 2013. A thylakoid-located two-pore K⁺ channel controls photosynthetic light utilization in plants. Science 342, 114-118.

[17] Carraretto, L., Teardo, E., Checchetto, V., Finazzi, G., Uozumi, N., Szabo, I., 2016. Ion channels in plant bioenergetic organelles, chloroplasts and mitochondria: from molecular identification to function. Mol. Plant 9, 371-395.

[18] Chen, B., Fang, J., Piao, S., Ciais, P., Black, T.A., Wang, F., Niu, S., Zeng, Z., Luo, Y., 2024. A meta-analysis highlights globally widespread potassium limitation in terrestrial ecosystems. New Phytol. 241, 154-165.

[19] Correa Galvis, V., Strand, D.D., Messer, M., Thiele, W., Bethmann, S., Hübner, D., Uflewski, M., Kaiser, E., Siemiatkowska, B., Morris, B.A., Tóth, S.Z., Watanabe, M., Brückner, F., Höfgen, R., Jahns, P., Schöttler, M.A., Armbruster, U., 2020. H⁺ transport by K⁺ EXCHANGE ANTIPORTER3 promotes photosynthesis and growth in chloroplast ATP synthase mutants. Plant Physiol. 182, 2126-2142.

[20] Coskun, D., Britto, D.T., Kronzucker, H.J., 2014. The physiology of channel-mediated K⁺ acquisition in roots of higher plants. Physiol. Plant. 151, 305-312.

[21] Cui, J., Tcherkez, G., 2021. Potassium dependency of enzymes in plant primary metabolism. Plant Physiol. Biochem. 166, 522-530.

[22] de Bang, T.C., Husted, S., Laursen, K.H., Persson, D.P., Schjoerring, J.K., 2021. The molecular-physiological functions of mineral macronutrients and their consequences for deficiency symptoms in plants. New Phytol. 229, 2446-2469.

[23] Deeken, R., Geiger, D., Fromm, J., Koroleva, O., Ache, P., Langenfeld-Heyser, R., Sauer, N., May, S.T., Hedrich, R., 2002. Loss of the AKT2/3 potassium channel affects sugar loading into the phloem of Arabidopsis. Planta 216, 334-344.

[24] Demmig, B., Gimmler, H., 1983. Properties of the isolated intact chloroplast at cytoplasmic K⁺ concentrations: I. Light-induced cation uptake into intact chloroplasts is driven by an electrical potential difference. Plant Physiol. 73, 169-174.

[25] Deng, K., Wang, W., Feng, L., Yin, H., Xiong, F., Ren, M., 2020. Target of rapamycin regulates potassium uptake in Arabidopsis and potato. Plant Physiol. Biochem. 155, 357-366.

[26] Dreyer, I., Uozumi, N., 2011. Potassium channels in plant cells. FEBS J. 278, 4293-4303.

[27] Gaymard, F., Pilot, G., Lacombe, B., Bouchez, D., Bruneau, D., Boucherez, J., Michaux-Ferriére, N., Thibaud, J., Sentenac, H., 1998. Identification and disruption of a plant shaker-like outward channel involved in K⁺ release into the xylem sap. Cell 94, 647-655.

[28] Gobert, A., Isayenkov, S., Voelker, C., Czempinski, K., Maathuis, F.J.M., 2007. The twopore channel TPK1 gene encodes the vacuolar K⁺ conductance and plays a role in K⁺ homeostasis. Proc. Natl. Acad. Sci. U. S. A. 104, 10726-10731.

[29] Hu, W., Gu, H., Wang, K., Lu, Z., Li, X., Cong, R., Ren, T., Lu, J., 2023. Potassium deficiency stress reduces Rubisco activity in Brassica napus leaves by subcellular acidification decreasing photosynthetic rate. Plant Physiol. Biochem. 201, 107912.

[30] Hu, W., Lu, Z., Meng, F., Li, X., Cong, R., Ren, T., Sharkey, T.D., Lu, J., 2020. The reduction in leaf area precedes that in photosynthesis under potassium deficiency: the importance of leaf anatomy. New Phytol. 227, 1749-1763.

[31] Imtiaz, H., Mir, A.R., Corpas, F.J., Hayat, S., 2023. Impact of potassium starvation on the uptake, transportation, photosynthesis, and abiotic stress tolerance. Plant Growth Regul. 99, 429-448.

[32] Johnson, R., Vishwakarma, K., Hossen, M.S., Kumar, V., Shackira, A.M., Puthur, J.T., Abdi, G., Sarraf, M., Hasanuzzaman, M., 2022. Potassium in plants: Growth regulation, signaling, and environmental stress tolerance. Plant Physiol. Biochem. 172, 56-69.

[33] Jordan-Meille, L., Pellerin, S., 2004. Leaf area establishment of a maize (Zea mays L.) field crop under potassium deficiency. Plant Soil 265, 75-92.

[34] Jordan-Meille, L., Pellerin, S., 2008. Shoot and root growth of hydroponic maize (Zea mays L.) as influenced by K deficiency. Plant Soil 304, 157-168.

[35] Kashtoh, H., Baek, K., 2021. Structural and functional insights into the role of guard cell ion channels in abiotic stress-induced stomatal closure. Plants 10, 2774.

[36] Kim, T., Böhmer, M., Hu, H., Nishimura, N., Schroeder, J.I., 2010. Guard cell signal transduction network: advances in understanding abscisic acid, CO₂, and Ca²⁺ signaling. Annu. Rev. Plant Biol. 61, 561-591.

[37] Kunz, H., Gierth, M., Herdean, A., Satoh-Cruz, M., Kramer, D.M., Spetea, C., Schroeder, J.I., 2014. Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 111, 7480-7485.

[38] Kusaka, M., Kalaji, H.M., Mastalerczuk, G., Dabrowski, P., Kowalczyk, K., 2021. Potassium deficiency impact on the photosynthetic apparatus efficiency of radish. Photosynthetica 59, 127-136.

[39] Latz, A., Becker, D., Hekman, M., Müller, T., Beyhl, D., Marten, I., Eing, C., Fischer, A., Dunkel, M., Bertl, A., Rapp, U.R., Hedrich, R., 2007. TPK1, a Ca²⁺-regulated Arabidopsis vacuole two-pore K⁺ channel is activated by 14-3-3 proteins. Plant J. 52, 449-459.

[40] Leigh, R.A., Wyn Jones, R.G., 1984. A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytol. 97, 1-13.

[41] Li, J., Long, Y., Qi, G., Li, J., Xu, Z., Wu, W., Wang, Y., 2014. The Os-AKT1 channel is critical for K⁺ uptake in rice roots and is modulated by the rice CBL1-CIPK23 complex. Plant Cell 26, 3387-3402.

[42] Li, S., Yang, F., Sun, D., Zhang, Y., Zhang, M., Liu, S., Zhou, P., Shi, C., Zhang, L., Tian, C., 2020. Cryo-EM structure of the hyperpolarization-activated inwardly rectifying potassium channel KAT 1 from Arabidopsis. Cell Res. 30, 1049-1052.

[43] Lu, Z., Ren, T., Pan, Y., Li, X., Cong, R., Lu, J., 2016. Differences on photosynthetic limitations between leaf margins and leaf centers under potassium deficiency for Brassica napus L. Sci. Rep. 6, 21725.

[44] Lu, Z., Xie, K., Pan, Y., Ren, T., Lu, J., Wang, M., Shen, Q., Guo, S., 2019. Potassium mediates coordination of leaf photosynthesis and hydraulic conductance by modifications of leaf anatomy. Plant Cell Environ. 42, 2231-2244.

[45] Luan, S., 2009. The CBL-CIPK network in plant calcium signaling. Trends Plant Sci. 14, 37-42.

[46] MacRobbie, E.A., 1998. Signal transduction and ion channels in guard cells. Philos. Trans. R. Soc. B-Biol. Sci. 353, 1475-1488.

[47] Nieves-Cordones, M., Alemán, F., Martínez, V., Rubio, F., 2014. K⁺ uptake in plant roots. The systems involved, their regulation and parallels in other organisms. J. PlantPhysiol. 171, 688-695.

[48] Nieves-Cordones, M., Lara, A., Ródenas, R., Amo, J., Rivero, R.M., Martínez, V., Rubio, F., 2019. Modulation of K⁺ translocation by AKT1 and AtHAK 5 in Arabidopsis plants. Plant Cell Environ. 42, 2357-2371.

[49] Pan, Y., Lu, Z., Li, X., Cong, R., Ren, T., Lu, J., 2019. Contributions of radiation interception and radiation-use efficiency to biomass decrease due to potassium starvation depend on potassium deficiency intensities. Acta Physiol. Plant. 41, 48.

[50] Paul, M.J., Pellny, T.K., 2003. Carbon metabolite feedback regulation of leaf photosynthesis and development. J. Exp. Bot. 54, 539-547.

[51] Pottosin, I., Shabala, S., 2016. Transport across chloroplast membranes: optimizing photosynthesis for adverse environmental conditions. Mol. Plant 9, 356-370.

[52] Ruban, A.V., 2016. Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol. 170, 1903-1916.

[53] Sánchez-Barrena, M.J., Chaves-Sanjuan, A., Raddatz, N., Mendoza, I., Cortés, A., Gago, F., González-Rubio, J.M., Benavente, J.L., Quintero, F.J., Pardo, J.M., Albert, A., 2020. Recognition and activation of the plant AKT 1 potassium channel by the kinase CIPK23. Plant Physiol. 182, 2143-2153.

[54] Sánchez-McSweeney, A., González-Gordo, S., Aranda-Sicilia, M.N., Rodríguez-Rosales, M.P., Venema, K., Palma, J.M., Corpas, F.J., 2021. Loss of function of the chloroplastmembrane K⁺/H⁺ antiporters AtKEA1 and AtKEA 2 alters theROS andNOmetabolism but promotes drought stress resilience. Plant Physiol. Biochem. 160, 106-119.

[55] Schachtman, D.P., Shin, R., 2007. Nutrient sensing and signaling: NPKS. Annu. Rev. Plant Biol. 58, 47-69.

[56] Schroeder, D., 1978. Structure and weathering of potassium containing minerals. IPI Research Topics. International Potash Institute, Bern, Switzerland, pp. 5-25.

[57] Shimazaki, K., Iino, M., Zeiger, E., 1986. Blue light-dependent proton extrusion by guardcell protoplasts of Vicia faba. Nature 319, 324-326.

[58] Shope, J.C., DeWald, D.B., Mott, K.A., 2003. Changes in surface area of intact guard cells are correlated with membrane internalization. Plant Physiol. 133, 1314-1321.

[59] Suelter, C.H., 1970. Enzymes activated by monovalent cations. Science 168, 789-795.

[60] Tanaka, Y., Sano, T., Tamaoki, M., Nakajima, N., Kondo, N., Hasezawa, S., 2005. Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol. 138, 2337-2343.

[61] Tang, R., Zhao, F., Yang, Y., Wang, C., Li, K., Kleist, T.J., Lemaux, P.G., Luan, S., 2020. A calcium signalling network activates vacuolar K⁺ remobilization to enable plant adaptation to low-K environments. Nat. Plants 6, 384-393.

[62] Tao, R., Ding, J., Li, C., Zhu, X., Guo, W., Zhu, M., 2021. Evaluating and screening of agrophysiological indices for salinity stress tolerance in wheat at the seedling stage. Front. Plant Sci. 12, 646175.

[63] Tikhonov, A.N., 2013. pH-dependent regulation of electron transport and ATP synthesis in chloroplasts. Photosynth. Res. 116, 511-534.

[64] Triboulot, M., Pritchard, J., Levy, G., 1997. Effects of potassium deficiency on cell water relations and elongation of tap and lateral roots of maritime pine seedlings. New Phytol. 135, 183-190.

[65] Tsujii, M., Kera, K., Hamamoto, S., Kuromori, T., Shikanai, T., Uozumi, N., 2019. Evidence for potassium transport activity of Arabidopsis KEA1-KEA6. Sci. Rep. 9, 10040.

[66] Walker, D.J., Leigh, R.A., Miller, A.J., 1996. Potassium homeostasis in vacuolate plant cells. Proc. Natl. Acad. Sci. U. S. A. 93, 10510-10514.

[67] Wang, F., Chen, Z., Liu, X., Colmer, T.D., Shabala, L., Salih, A., Zhou, M., Shabala, S., 2016. Revealing the roles of GORK channels and NADPH oxidase in acclimation to hypoxia in Arabidopsis. J. Exp. Bot. 68, 3191-3204.

[68] Wang, Y., Chen, Y.F., Wu, W.H., 2021. Potassium and phosphorus transport and signaling in plants. J. Integr. Plant Biol. 63, 34-52.

[69] Wang, Y., Wu, W., 2010. Plant sensing and signaling in response to K⁺-deficiency. Mol. Plant 3, 280-287.

[70] Wang, Y., Wu, W., 2013. Potassium transport and signaling in higher plants. Annu. Rev. Plant Biol. 64, 451-476.

[71] Weng, X.Y., Zheng, C.J., Xu, H.X., Sun, J.Y., 2007. Characteristics of photosynthesis and functions of the water-water cycle in rice (Oryza sativa) leaves in response to potassium deficiency. Physiol. Plant. 131, 614-621.

[72] Wu, W., Berkowitz, G.A., 1992. Stromal pH and photosynthesis are affected by electroneutral K and H exchange through chloroplast envelope ion channels. Plant Physiol. 98, 666-672.

[73] Yadav, U.P., Ivakov, A., Feil, R., Duan, G.Y., Walther, D., Giavalisco, P., Piques, M., Carillo, P., Hubberten, H., Stitt, M., Lunn, J.E., 2014. The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J. Exp. Bot. 65, 1051-1068.

[74] Yan, J., Ye, X., Song, Y., Ren, T., Wang, C., Li, X., Cong, R., Lu, Z., Lu, J., 2023. Sufficient potassium improves inorganic phosphate-limited photosynthesis in Brassica napus by enhancing metabolic phosphorus fractions and Rubisco activity. Plant J. 113, 416-429.

[75] Yang, T., Feng, H., Zhang, S., Xiao, H., Hu, Q., Chen, G., Xuan, W., Moran, N., Murphy, A., Yu, L., Xu, G., 2020. The potassium transporter OsHAK5 alters rice architecture via ATP-dependent transmembrane auxin fluxes. Plant Commun. 1, 100052.

[76] Zörb, C., Senbayram, M., Peiter, E., 2014. Potassium in agriculture - Status and perspectives. J. Plant Physiol. 171, 656-669.