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Genome-wide analysis and identification of HAK potassium transporter gene family in maize (Zea mays L.)

Molecular Biology Reports volume 39, pages 8465–8473 (2012)Cite this article

Abstract

The high-affinity K+ (HAK) transporter gene family constitutes the largest family that functions as potassium transporter in plant and is important for various cellular processes of plant life. In spite of their physiological importance, systematic analyses of ZmHAK genes have not yet been investigated. In this paper, we indicated the isolation and characterization of ZmHAK genes in whole-genome wide by using bioinformatics methods. A total of 27 members (ZmHAK1–ZmHAK27) of this family were identified in maize genome. ZmHAK genes were distributed in all the maize 10 chromosomes. These genes expanded in the maize genome partly due to tandem and segmental duplication events. Multiple alignment and motif display results revealed major maize ZmHAK proteins share all the three conserved domains. Phylogenetic analysis indicated ZmHAK family can be divided into six subfamilies. Putative cis-elements involved in Ca2+ response, abiotic stress adaption, light and circadian rhythms regulation and seed development were observed in the promoters of ZmHAK genes. Expression data mining suggested maize ZmHAK genes have temporal and spatial expression pattern. In all, these results will provide molecular insights into the potassium transporter research in maize.

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Abbreviations

GA3 :

Gibberellin

HAK:

High-affinity K+

NAA:

Naphthaleneacetic acid

ORF:

Open reading frame

KCO:

K+ channel openers

KT:

Cytokinin

References

  1. Glass ADM (1983) Regulation of ion-transport. Annu Rev Plant Physiol 34:311–326

    Article  CAS  Google Scholar 

  2. Schroeder JI, Ward JM, Gassmann W (1994) Perspectives in the physiology and structure of inward rectifying K+ channels in higher-plants: biophysical implications for K+ uptake. Annu Rev Biophys Biomol Struct 23:441–471. doi:10.1146/annurev.bb.23.060194.002301

    Article  PubMed  CAS  Google Scholar 

  3. Maathuis FJ, Sanders D (1999) Plasma membrane transport in context: making sense out of complexity. Curr Opin Plant Biol 2:236–243. doi:10.1016/S1369-5266(99)80041-7

    Article  PubMed  CAS  Google Scholar 

  4. Santa-Maria GE, Rubio F, Dubcovsky J, Rodriguez-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. doi:10.1105/tpc.9.12.2281

    PubMed  CAS  Google Scholar 

  5. Gierth M, Mäser P, Schroeder JI (2005) The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiol 137:1105–1114. doi:10.1104/pp.104.057216

    Article  PubMed  CAS  Google Scholar 

  6. Ashley MK, Grant M, Grabov A (2006) Plant responses to potassium deficiencies: a role for potassium transport proteins. J Exp Bot 57:425–436. doi:10.1093/jxb/erj034

    Article  PubMed  CAS  Google Scholar 

  7. Zimmerman S, Sentenac H (1999) Plant ion channel: from molecular structures to physiological functions. Curr Opin Plant Biol 2:477–482. doi:10.1016/S1369-5266(99)00020-5

    Article  Google Scholar 

  8. Véry AA, Sentenac H (2003) Molecular mechanisms and regulation of K+ transport in higher plants. Annu Rev Plant Biol 54:575–603. doi:10.1146/annurev.plant.54.031902.134831

    Article  PubMed  Google Scholar 

  9. Maathuis FJM, Sanders D (1997) Regulation of K+ absorption in plant root cells by external K+: interplay of different K+ transporters. J Exp Bot 48:451–458. doi:10.1093/jxb/48.Special_Issue.451

    Article  PubMed  CAS  Google Scholar 

  10. Maathuis FJM, Sanders D (1994) Mechanism of high-affinity potassium uptake in roots of Arabidopsis thaliana. Proc Natl Acad Sci USA 91:9272–9276

    Article  PubMed  CAS  Google Scholar 

  11. Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667. doi:10.1104/pp.126.4.1646

    Article  PubMed  Google Scholar 

  12. Gupta M, Qiu X, Wang L, Xie W, Zhang C, Xiong LZ, Lian XM, Zhang QF (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. doi:10.1007/s00438-008-0377-7

    Article  PubMed  CAS  Google Scholar 

  13. Ahn SJ, Shin R, Schachtman DP (2004) Expression of KT/KUP genes in Arabidopsis and the role of root hairs K+ uptake. Plant Physiol 134:1135–1145. doi:10.1104/pp.103.034660

    Article  PubMed  CAS  Google Scholar 

  14. Epstein W, Kim BS (1971) Potassium transport loci in Escherichia coli K-12. J Bacteriol 108:639–644

    PubMed  CAS  Google Scholar 

  15. Martínez-Cordero M, 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

    Article  PubMed  Google Scholar 

  16. Quintero FJ, Blatt MR (1997) A new family of K+ transporters from Arabidopsis that are conserved across phyla. FEBS Lett 415:206–211. doi:10.1016/S0014-5793(97)01125-3

    Article  PubMed  CAS  Google Scholar 

  17. Fu H-H, Luan S (1998) AtKUP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell 10:63–74. doi:10.1105/tpc.10.1.63

    PubMed  CAS  Google Scholar 

  18. Kim EJ, Kwak JM, Uozumi N, Schroeder JI (1998) AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell 10:51–62. doi:10.1105/tpc.10.1.51

    PubMed  CAS  Google Scholar 

  19. 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

    Article  PubMed  CAS  Google Scholar 

  20. 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. doi:10.1016/j.plantsci.2006.09.003

    Article  CAS  Google Scholar 

  21. 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 Interact 17:789–797. doi:10.1094/MPMI.2004.17.7.789

    Article  PubMed  CAS  Google Scholar 

  22. 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. doi:10.1093/jxb/erl091

    Article  PubMed  CAS  Google Scholar 

  23. 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. doi:10.1023/A:1019951023362

    Article  PubMed  CAS  Google Scholar 

  24. Baňuelos MA, Garciadeblas B, Cubero B, Rodríguez-Navarro A (2002) Inventory and functional characterization of the HAK potassium transporters of rice. Plant Physiol 130:784–795. doi:10.1104/pp.007781

    Article  PubMed  Google Scholar 

  25. Qi Z, Hampton CR, Shin R, Barkla BJ, White PJ, Schachtman DP (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

    Article  PubMed  CAS  Google Scholar 

  26. Rubio F, Santa-María GE, Rodríguez-Navarro A (2000) Cloning of Arabidopsis and barley cDNA sencoding HAK potassium transporters in root and shoot cells. Physiol Plant 109:34–43. doi:10.1034/j.1399-3054.2000.100106.x

    Article  CAS  Google Scholar 

  27. Su H, Golldack D, Zhao CS, 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. doi:10.1104/pp.001149

    Article  PubMed  CAS  Google Scholar 

  28. Elumalai RP, Nagpal P, Reed JW (2002) A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell 14:119–131. doi:10.1105/tpc.010322

    Article  PubMed  CAS  Google Scholar 

  29. Rigas S, Debrosses G, Haralampidis K, Vicente-Agullo F, Feldmann KA, Grabov A, Dolan L, Hatzopoulos P (2001) TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13:139–151. doi:10.1105/tpc.13.1.139

    PubMed  CAS  Google Scholar 

  30. Vicente-Agullo F, Rigas S, Desbrosses G, Dolan L, Hatzopoulos P, Grabov A (2004) Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. Plant J 40:523–535. doi:10.1111/j.1365-313X.2004.02230.x

    Article  PubMed  CAS  Google Scholar 

  31. Maathuis FJM (2006) The role of monovalent cation transporters in plant responses to salinity. J Exp Bot 57:1137–1147. doi:10.1093/jxb/erj001

    Article  PubMed  CAS  Google Scholar 

  32. Takahashi R, Nishio T, Ichizen N, Takano T (2007) 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. doi:10.1007/s00299-007-0364-1

    Article  PubMed  CAS  Google Scholar 

  33. Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326(5956):1112–1115. doi:10.1126/science.1178534

    Article  PubMed  CAS  Google Scholar 

  34. Yang ZF, Gao QS, Sun CS, Li WJ, Gu SL, Xu CW (2009) Molecular evolution and functional divergence of HAK potassium transporter gene family in rice (Oryza sativa L.). J Genet Genomics 36:161–172. doi:10.1016/S1673-8527(08)60103-4

    Article  PubMed  CAS  Google Scholar 

  35. Sonnhammer EL, Eddy SR, Durbin R (1997) Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 28:405–420

    Article  PubMed  CAS  Google Scholar 

  36. Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29(8):1023–1026. doi:10.1360/yc-007-1023

    PubMed  CAS  Google Scholar 

  37. Bailey TL, Boden M, Buske FA et al (2009) MEME SUITE: tools for motif discovery and searching. Nucl Acids Res 37:202–208. doi:10.1093/nar/gkp335

    Article  Google Scholar 

  38. Larkin MA, Blackshields G, Brown NP et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948. doi:10.1093/bioinformatics/btm404

    Google Scholar 

  39. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599. doi:10.1093/molbev/msm092

    Article  PubMed  CAS  Google Scholar 

  40. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucl Acids Res 27(1):297–300. doi:10.1093/nar/27.1.297

    Article  PubMed  CAS  Google Scholar 

  41. Wang YJ, Deng DX, Bian YL, Lv YP, Xie Q (2010) Genome-wide analysis of primary auxin-responsive Aux/IAA gene family in maize (Zea mays. L.). Mol Biol Rep 37:3991–4001. doi:10.1007/s11033-010-0058-6

    Article  PubMed  CAS  Google Scholar 

  42. Maher C, Stein L, Ware D (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16:510–519. doi:10.1101/gr.4680506

    Article  PubMed  CAS  Google Scholar 

  43. Nakano M, Nobuta K, Vemaraju K, Tej SS, Skogen JW, Meyers BC (2006) Plant MPSS databases: signature-based transcriptional resources for analyses of mRNA and small RNA. Nucl Acids Res 34:731–735. doi:10.1093/nar/gkj077

    Article  Google Scholar 

  44. Mulder N, Apweiler R (2007) InterPro and InterProScan: tools for protein sequence classification and comparison. Methods Mol Biol 396:59–70

    Article  PubMed  CAS  Google Scholar 

  45. Grabova (2007) Plant KT/KUP/HAK potassium transporters: single family-multiple functions. Ann Bot 99:1035–1041. doi:10.1093/aob/mcm066

    Article  Google Scholar 

  46. Schleyer M, Bakker EP (1993) Nucleotide sequence and 3’-end deletion studies indicate that the K+-uptake protein Kup from Escherichia coli is composed of a hydrophobic core linked to a large and partially essential hydrophilic C terminus. J Bacteriol 175:6925–6931

    PubMed  CAS  Google Scholar 

  47. Baňuelos MA, Klein RD, Alexander-Bowman SJ, Rodríguez-Navarro A (1995) A potassium transporter of the yeast Schwanniomyces occidentalis homologous to the Kup system of Escherichia coli has a high concentrative capacity. EMBO J 14:3021–3027

    PubMed  Google Scholar 

  48. Greiner T, Ramos J, Alvarez MC, Gurnon JR, Kang M, Etten JLV, Moroni A, Thiell G (2011) Functional HAK/KUP/KT-like potassium transporter encoded by chlorella viruses. Plant J 68:977–986. doi:10.1111/j.1365-313X.2011.04748.x

    Article  PubMed  CAS  Google Scholar 

  49. Amrutha RN, Sekhar PN, Varshney RK, Kishor PBK (2007) Genome-wide analysis and identification of genes related to potassium transporter families in rice (Oryza sativa L.). Plant Sci 172:708–721. doi:10.1016/j.plantsci.2006.11.019

    Article  CAS  Google Scholar 

  50. Qiu D, Xiao J, Xie W, Cheng H, Li X, Wang S (2009) Exploring transcriptional signalling mediated by OsWRKY13, a potential regulator of multiple physiological processes in rice. BMC Plant Biol 9:74. doi:10.1186/1471-2229-9-74

    Article  PubMed  Google Scholar 

  51. Vornam B, Gailing O, Derory J, Plomion C, Kremer A, Finkeldey R (2011) Characterisation and natural variation of a dehydrin gene in Quercus petraea (Matt.) Liebl. Plant Biol 13:881–887. doi:10.1111/j.1438-8677.2011.00446.x

    Article  PubMed  CAS  Google Scholar 

  52. Bratić AM, Majić DB, Samardžić JT, Maksimović VR (2009) Functional analysis of the buckwheat metallothionein promoter: tissue specificity pattern and up-regulation under complex stress stimuli. J Plant Physiol 166:996–1000. doi:10.1016/j.jplph.2008.12.002

    Article  PubMed  Google Scholar 

  53. Yazaki J, Shimatani Z, Hashimoto A, Nagata Y, Fujii F, Kojima K, Suzuki K, Taya T, Tonouchi M, Nelson C et al (2004) Transcriptional profiling of genes responsive to abscisic acid and gibberellin in rice: phenotyping and comparative analysis between rice and Arabidopsis. Physiol Genom 17:87–100. doi:10.1152/physiolgenomics.00201.2003

    Article  CAS  Google Scholar 

  54. Guo L, Yu Y, Xia X, Yin W (2010) Identification and functional characterisation of the promoter of the calcium sensor gene CBL1 from the xerophyte Ammopiptanthus mongolicus. BMC Plant Biol 10:18. doi:10.1186/1471-2229-10-18

    Article  PubMed  Google Scholar 

  55. Piechulla B, Merforth N, Rudolph B (1998) Identification of tomato Lhc promoter regions necessary for circadian expression. Plant Mol Biol 38:655–662. doi:10.1023/A:1006094015513

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful to editors and reviewers for their helpful comments. This work was supported partly by the International Science and Technology Cooperation Project (ISTCP) in China (No. 2010DFB33740) and the Beijing Municipal Science and Technology Commission (No. Z111100066111005).

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Authors and Affiliations

  1. Beijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China

    Zhongbao Zhang, Jiewei Zhang, Yajuan Chen, Ruifen Li, Hongzhi Wang & Jianhua Wei

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  1. Zhongbao Zhang
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  2. Jiewei Zhang
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Correspondence to Jianhua Wei.

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Zhang, Z., Zhang, J., Chen, Y. et al. Genome-wide analysis and identification of HAK potassium transporter gene family in maize (Zea mays L.). Mol Biol Rep 39, 8465–8473 (2012). https://doi.org/10.1007/s11033-012-1700-2

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Keywords

  • Maize
  • Potassium transporter
  • Cis-elements
  • Phylogenetic analysis