Abstract
A chimeric CaHAK1–LeHAK5 transporter with only 15 amino acids of CaHAK1 in the N-terminus mediates high-affinity K+ uptake in yeast cells. Kinetic and expression analyses strongly suggest that LeHAK5 mediates a significant proportion of the high-affinity K+ uptake shown by K+-starved tomato (Solanum lycopersicum) plants. The development of high-affinity K+ uptake, putatively mediated by LeHAK5, was correlated with increased LeHAK5 mRNA levels and a more negative electrical potential difference across the plasma membrane of root epidermal and cortical cells. However, this increase in high-affinity K+ uptake was not correlated with the root K+ content. Thus, (i) growth conditions that result in a hyperpolarized root plasma membrane potential, such as K+ starvation or growth in the presence of NH4 +, but which do not decrease the K+ content, lead to increased LeHAK5 expression; (ii) the presence of NaCl in the growth solution, which prevents the hyperpolarization induced by K+ starvation, also prevents LeHAK5 expression. Moreover, once the gene is induced, depolarization of the plasma membrane potential then produces a decrease in the LeHAK5 mRNA. On the basis of these results, we propose that the plant membrane electrical potential plays a role in the regulation of the expression of this gene encoding a high-affinity K+ transporter.
Similar content being viewed by others
References
Ahn SJ, Shin R, Schachtman DP (2004) Expression of KT/KUP genes in Arabidopsis and the role of root hairs in K+ uptake. Plant Physiol 134:1135–1145. doi:10.1104/pp.103.034660
Amtmann A, Armengaud P, Volkov V (2004) Potassium nutrition and salt stress. In: Blatt MR (ed) Membrane transport in plants. Blackwell, Oxford, pp 293–339
Amtmann A, Hammond JP, Armengaud P et al (2006) Nutrient sensing and signalling in plants: potassium and phosphorus. In: Callow JA (ed) Adv Bot Res. Academic Press, London, pp 209–257
Armengaud P, Breitling R, Amtmann A (2004) The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 136:2556–2576. doi:10.1104/pp.104.046482
Ayling SM (1993) The effect of ammonium-ions on membrane-potential and anion flux in roots of barley and tomato. Plant Cell Environ 16:297–303. doi:10.1111/j.1365-3040.1993.tb00872.x
Bañuelos MA, Garciadeblas B, Cubero B et al (2002) Inventory and functional characterization of the HAK potassium transporters of rice. Plant Physiol 130:784–795. doi:10.1104/pp.007781
Britto DT, Siddiqi MY, Glass ADM et al (2001) Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci USA 98:4255–4258. doi:10.1073/pnas.061034698
Bunelli JP, Pall ML (1993) A series of yeast shuttle vectors for expression of cDNAs and other DNA-sequences. Yeast 9:1299–1308. doi:10.1002/yea.320091203
Carden DE, Walker DJ, Flowers TJ et al (2003) Single-cell measurements of the contributions of cytosolic Na+ and K+ to salt tolerance. Plant Physiol 131:676–683. doi:10.1104/pp.011445
Coombs HV, Miller AJ, Sanders D (1994) Disruptive effects of protein on performance of liquid membrane-based ion-selective microelectrodes. AJP—Cell Physiol 267:C1027–C1035
Epstein E, Rains DW, Elzam OE (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc Natl Acad Sci USA 49:684–692. doi:10.1073/pnas.49.5.684
Gierth M, Maser P, Schroeder JI (2005) The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiol 137:1105–1114. doi:10.1104/pp.104.057216
Glass A (1978) The regulation of K+ influx into intact roots of barley (Hordeum vulgare (L.) cv. Conquest) by internal K+. Can J Bot 56:1759–1764. doi:10.1139/b78-209
Glass ADM, Dunlop J (1978) Influence of potassium content on kinetics of potassium influx into excised ryegrass and barley roots. Planta 141:117–119. doi:10.1007/BF00387753
Glass ADM, Shaff JE, Kochian LV (1992) Studies of the uptake of nitrate in barley: IV. Electrophysiology. Plant Physiol 99:456–463
Haro R, Sainz L, Rubio F et al (1999) Cloning of two genes encoding potassium transporters in Neurospora crassa and expression of the corresponding cDNAs in Saccharomyces cerevisiae. Mol Microbiol 31:511–520. doi:10.1046/j.1365-2958.1999.01192.x
Hartje S, Zimmermann S, Klonus D et al (2000) Functional characterisation of LKT1, a K+ uptake channel from tomato root hairs, and comparison with the closely related potato inwardly rectifying K+ channel SKT1 after expression in Xenopus oocytes. Planta 210:723–731. doi:10.1007/s004250050673
Hasegawa PM, Bressan RA, Zhu JK et al (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499. doi:10.1146/annurev.arplant.51.1.463
Hirsch RE, Lewis BD, Spalding EP et al (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280:918–921. doi:10.1126/science.280.5365.918
Kochian LV, Lucas WJ (1988) Potassium transport in roots. Adv Bot Res 15:93–178. doi:10.1016/S0065-2296(08)60045-2
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. doi:10.1006/meth.2001.1262
Madrid R, Gómez MJ, Ramos J et al (1998) Ectopic potassium uptake in trk1 trk2 mutants of Saccharomyces cerevisiae correlates with a highly hyperpolarized membrane potential. J Biol Chem 273:14838–14844. doi:10.1074/jbc.273.24.14838
Marschner H (1995) Mineral nutrition of higher plants. Springer, New York
Martínez-Cordero MA, Martínez V, Rubio F (2004) Cloning and functional characterization of the high-affinity K+ transporter HAK1 of pepper. Plant Mol Biol 56:413–421. doi:10.1007/s11103-004-3845-4
Martinez-Cordero MA, Martinez V, Rubio F (2005) High-affinity K+ uptake in pepper plants. J Exp Bot 56:1553–1562. doi:10.1093/jxb/eri150
Nieves-Cordones M, Martinez-Cordero MA, Martinez V et al (2007) An NH4 +-sensitive component dominates high-affinity K+ uptake in tomato plants. Plant Sci 172:273–280. doi:10.1016/j.plantsci.2006.09.003
Qi Z, Hampton CR, Shin R et al (2008) The high affinity K+ transporter AtHAK5 plays a physiological role in planta at very low K+ concentrations and provides a caesium uptake pathway in Arabidopsis. J Exp Bot 59:595–607. doi:10.1093/jxb/erm330
Rodríguez-Navarro A (2000) Potassium transport in fungi and plants. Biochim Biophys Acta 1469:1–30
Rodríguez-Navarro A, Ramos J (1984) Dual system for potassium transport in Saccharomyces cerevisiae. J Bacteriol 159:940–945
Rodríguez-Navarro A, Rubio F (2006) High-affinity potassium and sodium transport systems in plants. J Exp Bot 57:1149–1160. doi:10.1093/jxb/erj068
Rubio F, Santa-Maria GE, Rodríguez-Navarro A (2000) Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Physiol Plant 109:34–43. doi:10.1034/j.1399-3054.2000.100106.x
Santa-María GE, Rubio F, Dubcovsky J et al (1997) The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell 9:2281–2289
Schaller A, Frasson D (2001) Induction of wound response gene expression in tomato leaves by ionophores. Planta 212:431–435. doi:10.1007/s004250000413
Shabala S, Demidchik V, Shabala L et al (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665. doi:10.1104/pp.106.082388
Sherman F (1991) Getting started with yeast. Methods Enzymol 194:3–21. doi:10.1016/0076-6879(91)94004-V
Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832. doi:10.1073/pnas.0401707101
Spalding EP, Hirsch RE, Lewis DR et al (1999) Potassium uptake supporting plant growth in the absence of AKT1 channel activity: inhibition by ammonium and stimulation by sodium. J Gen Physiol 113:909–918. doi:10.1085/jgp.113.6.909
Stankovic B, Davies E (1998) The wound response in tomato involves rapid growth and electrical responses, systemically up-regulated transcription of proteinase inhibitor and calmodulin and down-regulated translation. Plant Cell Physiol 39:268–274
Ullrich CI, Novacky AJ (1990) Extra- and intracellular pH and membrane potential changes induced by K+, Cl−, H2PO4 −, and NO3 − uptake and fusicoccin in root hairs of Limnobium stoloniferum. Plant Physiol 94:1561–1567
Vian A, Henry-Vian C, Schantz R et al (1996) Is membrane potential involved in calmodulin gene expression after external stimulation in plants? FEBS Lett 380:93–96. doi:10.1016/0014-5793(96)00015-4
Walker DJ, Smith SJ, Miller AJ (1995) Simultaneous measurement of intracellular pH and K+ or NO3 − in barley root cells using triple-barreled, ion-selective microelectrodes. Plant Physiol 108:743–751
Walker DJ, Black CR, Miller AJ (1998) The role of cytosolic potassium and pH in the growth of barley roots. Plant Physiol 118:957–964. doi:10.1104/pp.118.3.957
Wang TB (1998) Rapid up-regulation of HKT1, a high-affinity potassium transporter gene, in roots of barley and wheat following withdrawal of potassium. Plant Physiol 118:651–659. doi:10.1104/pp.118.2.651
Wang MY, Glass ADM, Shaff JE et al (1994) Ammonium uptake by rice roots. 3. Electrophysiology. Plant Physiol 104:899–906
Wang YH, Garvin DF, Kochian LV (2001) Nitrate-induced genes in tomato roots. Array analysis reveals novel genes that may play a role in nitrogen nutrition. Plant Physiol 127:345–359. doi:10.1104/pp.127.1.345
Wang YH, Garvin DF, Kochian LV (2002) Rapid induction of regulatory and transporter genes in response to phosphorus, potassium, and iron deficiencies in tomato roots. Evidence for cross talk and root/rhizosphere-mediated signals. Plant Physiol 130:1361–1370. doi:10.1104/pp.008854
Acknowledgments
This research was funded by grant AGL-2006-01135 from the Ministerio de Educación y Ciencia awarded to F.R., an F.P.U. fellowship from the Ministerio de Educación y Ciencia awarded to M.N.-C. and an I3P pre-doctoral fellowship from the CSIC awarded to F. A. Rothamsted Research is grant-aided by the Biotechnology and Biological Sciences Research Council (BBSRC) of the UK.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nieves-Cordones, M., Miller, A.J., Alemán, F. et al. A putative role for the plasma membrane potential in the control of the expression of the gene encoding the tomato high-affinity potassium transporter HAK5. Plant Mol Biol 68, 521–532 (2008). https://doi.org/10.1007/s11103-008-9388-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-008-9388-3