Skip to main content
Log in

Functional analysis of a high-affinity potassium transporter PaHAK1 from Phytolacca acinosa by overexpression in eukaryotes

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

KUP/HAK/KT transporters mainly play a role of K+ uptake in plants. PaHAK1 was a previously isolated KUP/HAK/KT transporter gene from a high K+ plant Phytolacca acinosa Roxb. In this study, we want to identify the function of PaHAK1.

Methods

PaHAK1 was overexpressed in eukaryotes including Arabidopsis, rice, and yeast. The growth and K+ uptake of transgenic lines in media of low K+ concentration were investigated.

Results

We found that PaHAK1 rescued the growth phenotype of athak5 seedlings which was hard to grow in the media of 10 μM K+. Faster depletion from diluted K solutions was detected for transgenic than for WT plants. Moreover, PaHAK1 confers the growth of K+ uptake deletion yeast mutant on AP media containing 50 μM of K+.

Conclusions

Taken together, these results suggest an important role for PaHAK1 transporter on K+ uptake.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amrutha RN, Sekhar PN, Varshney RK, Kishor PK (2007) Genome-wide analysis and identification of genes related to potassium transporter families in rice (Oryza sativa L.). Plant Sci 172:708–721

    Article  CAS  Google Scholar 

  • Amtmann A, Blatt MR (2009) Regulation of macronutrient transport. New Phytol 181:35–52

    Article  PubMed  CAS  Google Scholar 

  • Anschutz U, Becker D, Shabala S (2014) Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment. J Plant Physiol 171:670–687

    Article  PubMed  CAS  Google Scholar 

  • Bañuelos MA, Garciadeblas B, Cubero B, Rodrı́guez-Navarro A (2002) Inventory and functional characterization of the HAK potassium transporters of rice. Plant Physiol 130:784–795

    Article  PubMed  PubMed Central  Google Scholar 

  • Benito B, Haro R, Amtmann A, Cuin TA, Dreyer I (2014) The twins K+ and Na+ in plants. J Plant Physiol 171:723–731

    Article  PubMed  CAS  Google Scholar 

  • Bose J, Rodrigo-Moreno A, Lai D, Xie Y, Shen W, Shabala S (2015) Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Ann Bot 115:481–494

    Article  PubMed  Google Scholar 

  • Bregante M, Yang Y, Formentin E, Carpaneto A, Schroeder JI, Gambale F, Schiavo FL, Costa A (2008) KDC1, a carrot shaker-like potassium channel, reveals its role as a silent regulatory subunit when expressed in plant cells. Plant Mol Biol 66:61–72

    Article  PubMed  CAS  Google Scholar 

  • Brunelli JP, Pall ML (1993) A series of yeast/Escherichia coli λ expression vectors designed for directional cloning of cDNAs and cre/lox-mediated plasmid excision. Yeast 9:1309–1318

    Article  PubMed  CAS  Google Scholar 

  • Cellier F, Conéjéro G, Ricaud L, Luu DT, Lepetit M, Gosti F, Casse F (2004) Characterization of AtCHX17, a member of the cation/H+ exchangers, CHX family, from Arabidopsis thaliana suggests a role in K+ homeostasis. Plant J 39:834–846

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou M, Palmgren MG, Newman IA (2007) Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiol 145:1714–1725

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Corratgé-Faillie C, Jabnoune M, Zimmermann S, Véry A-A, Fizames C, Sentenac H (2010) Potassium and sodium transport in non-animal cells: the Trk/Ktr/HKT transporter family. Cell Mol Life Sci 67:2511–2532

    Article  PubMed  CAS  Google Scholar 

  • Coskun D, Britto DT, Li M, Oh S, Kronzucker HJ (2013) Capacity and plasticity of potassium channels and high-affinity transporters in roots of barley and Arabidopsis. Plant Physiol 162:496–511

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cuin TA, Betts SA, Chalmandrier R, Shabala S (2008) A root’s ability to retain K+ correlates with salt tolerance in wheat. J Exp Bot 59:2697–2706

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Davies C, Shin R, Liu W, Thomas MR, Schachtman DP (2006) Transporters expressed during grape berry (Vitis vinifera L.) development are associated with an increase in berry size and berry potassium accumulation. J Exp Bot 57:3209–3216

    Article  PubMed  CAS  Google Scholar 

  • Desbrosses G, Kopka C, Ott T, Udvardi MK (2004) Lotus japonicus LjKUP is induced late during nodule development and encodes a potassium transporter of the plasma membrane. Mol Plant Microbe In 17:789–797

    Article  CAS  Google Scholar 

  • Epstein E, Rains D, Elzam O (1963) Resolution of dual mechanisms of potassium absorption by barley roots. P Natl Acad Sci USA 49:684

    Article  CAS  Google Scholar 

  • Fu H-H, Luan S (1998) AtKUP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell 10:63–73

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gajdanowicz P, Michard E, Sandmann M, Rocha M, Corrêa LGG, Ramírez-Aguilar SJ, Gomez-Porras JL, González W, Thibaud J-B, Van Dongen JT (2011) Potassium (K+) gradients serve as a mobile energy source in plant vascular tissues. P Natl Acad Sci USA 108:864–869

    Article  CAS  Google Scholar 

  • Garciadeblas B, Benito B, Rodríguez-Navarro A (2002) Molecular cloning and functional expression in bacteria of the potassium transporters CnHAK1 and CnHAK2 of the seagrass Cymodocea nodosa. Plant Mol Biol 50:623–633

    Article  PubMed  CAS  Google Scholar 

  • Garciadeblas B, Barrero-Gil J, Benito B, Rodríguez-Navarro A (2007) Potassium transport systems in the moss Physcomitrella patens: pphak1 plants reveal the complexity of potassium uptake. Plant J 52:1080–1093

    Article  PubMed  CAS  Google Scholar 

  • Gierth M, Mäser 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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gupta M, Qiu X, Wang L, Xie W, Zhang C, Xiong L, Lian X, Zhang Q (2008) KT/HAK/KUP potassium transporters gene family and their whole-life cycle expression profile in rice (Oryza sativa). Mol Genet Genomics 280:437–452

    Article  PubMed  CAS  Google Scholar 

  • Haro R, Rodrı́guez-Navarro A (2003) Functional analysis of the M2 D helix of the TRK1 potassium transporter of Saccharomyces cerevisiae. BBA-Biomembranes 1613:1–6

    Article  PubMed  CAS  Google Scholar 

  • Haro R, Bañuelos MA, Rodríguez-Navarro A (2010) High-affinity sodium uptake in land plants. Plant Cell Physiol 51:68–79

    Article  PubMed  CAS  Google Scholar 

  • He C, Cui K, Duan A, Zeng Y, Zhang J (2012) Genome-wide and molecular evolution analysis of the Poplar KT/HAK/KUP potassium transporter gene family. Ecol Evol 2:1996–2004

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu D, Dong R, Ge D (1993) Theory and practice of potassium nutrition in plant. Hunan Science and Technology Press, Changsha, pp 242–251

  • Hyun TK, Rim Y, Kim E, Kim JS (2014) Genome-wide and molecular evolution analyses of the KT/HAK/KUP family in tomato (Solanum lycopersicum L.). Genes Genom 36:365–374

    Article  CAS  Google Scholar 

  • Jiang C, Belfield EJ, Cao Y, Smith JAC, Harberd NP (2013) An Arabidopsis soil-salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis. Plant Cell 25:3535–3552

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lagarde D, Basset M, Lepetit M, Conejero G, Gaymard F, Astruc S, Grignon C (1996) Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. Plant J 9:195–203

    Article  PubMed  CAS  Google Scholar 

  • Leigh R, Wyn Jones R (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

    Article  CAS  Google Scholar 

  • Lin W, Ma L, Su Y, Huang Z, Xiao L (2011) Cloning and expression analysis of high-affinity potassium transporter gene PaHAK1 from Phytolacca acinosa Roxb. Plant Physiol J 47:91–96

    CAS  Google Scholar 

  • Ma L, Su Y, Guo Z, Zhao X, Lin W (2011) Characteristics of K+ uptake in Phytolacca acinosa. J Hunan Agr Univ 37:621–623

    Article  CAS  Google Scholar 

  • Ma T-L, Wu W-H, Wang Y (2012) Transcriptome analysis of rice root responses to potassium deficiency. BMC Plant Biol 12:161

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667

    Article  PubMed  PubMed Central  Google Scholar 

  • Mäser P, Gierth M, Schroeder JI (2002) Molecular mechanisms of potassium and sodium uptake in plants. Plant Soil 247:43–54

    Article  Google Scholar 

  • Mengel K, Kirkby EA, Kosegarten H, Appel T (2001) The soil as a plant nutrient medium: in Principles of Plant Nutrition (5th Edition). Springer International Publishing Press 15–110

  • Nieves-Cordones M, Martínez-Cordero MA, Martínez V, Rubio F (2007) An NH4 +-sensitive component dominates high-affinity K+ uptake in tomato plants. Plant Sci 172:273–280

    Article  CAS  Google Scholar 

  • Nieves-Cordones M, Alemán F, Martínez V, Rubio F (2010) The Arabidopsis thaliana HAK5 K+ transporter is required for plant growth and K+ acquisition from low K+ solutions under saline conditions. Mol Plant 3:326–333

    Article  PubMed  CAS  Google Scholar 

  • Osakabe Y, Arinaga N, Umezawa T, Katsura S, Nagamachi K, Tanaka H, Ohiraki H, Yamada K, Seo SU, Abo M (2013) Osmotic stress responses and plant growth controlled by potassium transporters in Arabidopsis. Plant Cell 25:609–624

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pottosin I, Dobrovinskaya O (2014) Non-selective cation channels in plasma and vacuolar membranes and their contribution to K+ transport. J Plant Physiol 171:732–742

    Article  PubMed  CAS  Google Scholar 

  • Pyo YJ, Gierth M, Schroeder JI, Cho MH (2010) High-affinity K+ transport in Arabidopsis: AtHAK5 and AKT1 are vital for seedling establishment and postgermination growth under low-potassium conditions. Plant Physiol 153:863–875

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Qi Z, Hampton CR, Shin R, Barkla BJ, White PJ, Schachtman DP (2008) The high affinity K+ transporter AtHAK5 plays a physiological role in plants at very low K+ concentrations and provides a caesium uptake pathway in Arabidopsis. J Exp Bot 59:595–607

    Article  PubMed  CAS  Google Scholar 

  • Renkema H, Koopmans A, Hale B, Berkelaar E (2015) Thallium and potassium uptake kinetics and competition differ between durum wheat and canola. Environ Sci Pollut Res Int 22:2166–2174

  • Rodrı́guez-Navarro A (2000) Potassium transport in fungi and plants. BBA-Rev Biomembranes 1469:1–30

    Google Scholar 

  • Rodríguez-Navarro A, Ramos J (1984) Dual system for potassium transport in Saccharomyces cerevisiae. J Bacteriol 159:940–945

    PubMed  PubMed Central  Google Scholar 

  • Römheld V, Kirkby EA (2010) Research on potassium in agriculture: needs and prospects. Plant Soil 335:155–180

    Article  CAS  Google Scholar 

  • Rubio F, Santa-María GE, Rodríguez-Navarro A (2000) Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Physiol Plantarum 109:34–43

    Article  CAS  Google Scholar 

  • Rubio F, Nieves-Cordones M, Alemán F, Martínez V (2008) Relative contribution of AtHAK5 and AtAKT1 to K+ uptake in the high-affinity range of concentrations. Physiol Plantarum 134:598–608

    Article  CAS  Google Scholar 

  • Santa-Maria GE, Rubio F, Dubcovsky J, Rodríguez-Navarro A (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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sparks DL (1987) Potassium dynamics in soils. Adv Soil Sci 6:1–63

  • Su H, Golldack D, Zhao C, Bohnert HJ (2002) The expression of HAK-type K+ transporters is regulated in response to salinity stress in common ice plant. Plant Physiol 129:1482–1493

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Takahashi R, Liu S, Takano T (2007a) Cloning and functional comparison of a high-affinity K+ transporter gene PhaHKT1 of salt-tolerant and salt-sensitive reed plants. J Exp Bot 58:4387–4395

    Article  PubMed  CAS  Google Scholar 

  • Takahashi R, Nishio T, Ichizen N, Takano T (2007b) High-affinity K+ transporter PhaHAK5 is expressed only in salt-sensitive reed plants and shows Na+ permeability under NaCl stress. Plant Cell Rep 26:1673–1679

    Article  PubMed  CAS  Google Scholar 

  • Teakle N, Bazihizina N, Shabala S, Colmer T, Barrett-Lennard E, Rodrigo-Moreno A, Läuchli A (2013) Differential tolerance to combined salinity and O2 deficiency in the halophytic grasses Puccinellia ciliata and Thinopyrum ponticum: the importance of K+ retention in roots. Environ Exp Bot 87:69–78

    Article  CAS  Google Scholar 

  • Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47:969–976

    Article  PubMed  CAS  Google Scholar 

  • Very AA, Nieves-Cordones M, Daly M, Khan I, Fizames C, Sentenac H (2014) Molecular biology of K+ transport across the plant cell membrane: what do we learn from comparison between plant species? J Plant Physiol 171:748–769

    Article  PubMed  CAS  Google Scholar 

  • Walker DJ, Leigh RA, Miller AJ (1996) Potassium homeostasis in vacuolate plant cells. P Natl Acad Sci USA 93:10510–10514

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wang Z, Chen C, Xu Y, Jiang R, Han Y, Xu Z, Chong K (2004) A practical vector for efficient knockdown of gene expression in rice (Oryza sativa L.). Plant Mol Biol Rep 22:409–417

    Article  CAS  Google Scholar 

  • Yang Z, Gao Q, Sun C, Li W, Gu S, Xu C (2009) Molecular evolution and functional divergence of HAK potassium transporter gene family in rice (Oryza sativa L.). J Genet Genomics 36:161–172

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Zhang J, Chen Y, Li R, Wang H, Wei J (2012) Genome-wide analysis and identification of HAK potassium transporter gene family in maize (Zea mays L.). Mol Biol Rep 39:8465–8473

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Cheng NH, Motes CM, Blancaflor EB, Moore M, Gonzales N, Padmanaban S, Sze H, Ward JM, Hirschi KD (2008) AtCHX13 is a plasma membrane K+ transporter. Plant Physiol 148:796–807

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 91317312 and 30900099) and Scientific Research Fund of Hunan Provincial Education Department (Grant Nos. 15K061, 12K061, and 13K065). We thank Professor Myeon Haeng Cho from Yonsei University for the donation of Arabidopsis mutants and Professor Alonso Rodríguez-Navarro from Universidad Politécnica of Madrid for the donation of yeast mutant strain WΔ6. We are also grateful to Prof. Langtao Xiao and Dr. Zhigang Huang who provided some valuable suggestions in this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wanhuang Lin.

Additional information

Responsible Editor: Guillermo Santa Maria.

Yi Su and Weigui Luo contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Su, Y., Luo, W., Zhao, X. et al. Functional analysis of a high-affinity potassium transporter PaHAK1 from Phytolacca acinosa by overexpression in eukaryotes. Plant Soil 397, 63–73 (2015). https://doi.org/10.1007/s11104-015-2601-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-015-2601-7

Keywords

Navigation