Skip to main content
SpringerLink
Log in

Comparisons in functions of HKT1;5 transporters between Hordeum marinum and Hordeum vulgare in responses to salt stress

  • Original Paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Sea barley (Hordeum marinum) is more salt tolerant than barley (Hordeum vulgare). In our previous study, H. marinum accession H559 showed the superior salt tolerance and K+/Na+ homeostasis than barley cultivar Golden Promise under 400 mM NaCl. However, the molecular mechanism underlying the difference of salt tolerance between the two species remains to be revealed. Here, we characterized a homolog of HvHKT1;5 transporter in sea barley, HmHKT1;5, and compared their functions in salt tolerance. Like HvHKT1;5, HmHKT1;5 also encodes a plasma membrane protein, which is mainly expressed in roots. The expression of both genes was induced by salt stress, but HmHKT1;5 had less increase than HvHKT1;5. When expressed in Xenopus laevis oocytes, both HmHKT1;5 and HvHKT1;5 were permeable to only Na+, but the transport affinity of HmHKT1;5 was lower than that of HvHKT1;5. Moreover, when each of the two genes was introduced into rice cv. Nipponbare, both the HvHKT1;5 and HmHKT1;5 transgenic lines showed greater Na+ uptake than the wild-types, resulting in enhancement of salt stress sensitivity. Besides, the introduction of HvHKT1;5 also increased Na+ translocation from roots to shoots in rice, while the introduction of HmHKT1;5 did not. The results indicate that HvHKT1;5 is involved in Na+ uptake and translocation from roots to shoots and HmHKT1;5 is only involved in Na+ uptake, and the uptake ability of HmHKT1;5 for Na+ is much weaker than that of HvHKT1;5. These findings partially reveal the reasons why H. marinum has higher salt tolerance than H. vulgare.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alamri SA, Barrettlennard EG, Teakle NL, Colmer TD (2013) Improvement of salt and waterlogging tolerance in wheat: comparative physiology of Hordeum marinum-Triticum aestivum amphiploids with their H. marinum and wheat parents. Funct Plant Biol 40:1168–1178

    Article  CAS  PubMed  Google Scholar 

  • Ali A, Raddatz N, Aman R, Kim S, Park HC, Jan M, Baek D, Khan IU, Oh DH, Lee SY, Bressan RA, Lee KW, Maggio A, Pardo JM, Bohnert HJ, Yun DJ (2016) A single amino-acid substitution in the sodium transporter HKT1 associated with plant salt tolerance. Plant Physiol 171:2112–2126

    Article  PubMed  PubMed Central  Google Scholar 

  • Byrt CS, Platten JD, Spielmeyer W, James RA, Lagudah ES, Dennis ES, Tester M, Munns R (2007) HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol 143:1918–1928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byrt CS, Xu B, Krishnan M, Lightfoot DJ, Athman A, Jacobs AK, Watson-Haigh NS, Plett D, Munns R, Tester M, Gilliham M (2014) The Na+ transporter, TaHKT1;5-D, limits shoot Na+ accumulation in bread wheat. Plant J 80:516–526

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davenport RJ, Munoz-Mayor A, Jha D, Essah PA, Rus A, Tester M (2007) The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant, Cell Environ 30:497–507

    Article  CAS  Google Scholar 

  • Garthwaite AJ, Bothmer RV, Colmer TD (2005) Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl− into the shoots. J Exp Bot 56:2365–2378

    Article  CAS  PubMed  Google Scholar 

  • Gorham J, Jones RGW, Bristol A (1990) Partial characterization of the trait for enhanced K+-Na+ discrimination in the D genome of wheat. Planta 180:590–597

    Article  CAS  PubMed  Google Scholar 

  • Grefen C, Chen Z, Honsbein A, Donald N, Hills A, Blatt MR (2010) A novel motif essential for SNARE interaction with the K+ channel KCl and channel gating in Arabidopsis. Plant Cell 22:3076–3092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hauser F, Horie T (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant, Cell Environ 33:552–565

    Article  CAS  Google Scholar 

  • Herbert JK, Mark WS, Lasse MS, Dev TB (2008) Non-reciprocal interactions between K+ and Na+ ions in barley (Hordeum vulgare L.). J Exp Bot 59:2793–2801

    Article  CAS  Google Scholar 

  • Horie T, Hauser F, Schroeder JI (2009) HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci 14:660–668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang S, Spielmeyer W, Lagudah ES, Munns R (2008) Comparative mapping of HKT genes in wheat, barley, and rice, key determinants of Na+ transport, and salt tolerance. J Exp Bot 59:927–937

    Article  CAS  PubMed  Google Scholar 

  • Huang L, Kuang LH, Li X, Wu LY, Wu DZ, Zhang GP (2018) Metabolomic and transcriptomic analyses reveal the reasons why Hordeum marinum has higher salt tolerance than Hordeum vulgare. Environ Exp Bot 156:48–61

    Article  CAS  Google Scholar 

  • Islam S, Malik A, Islam A, Colmer T (2007) Salt tolerance in a Hordeum marinum-Triticum aestivum amphiploid, and its parents. J Exp Bot 58:1219–1229

    Article  CAS  PubMed  Google Scholar 

  • James RA, Blake C, Byrt CS, Munns R (2011) Major genes for Na+ exclusion, Nax1 and Nax2 (wheat HKT1;4 and HKT1;5), decrease Na+ accumulation in bread wheat leaves under saline and waterlogged conditions. J Exp Bot 62:2939–2947

    Article  CAS  PubMed  Google Scholar 

  • Jang IC, Nahm BH, Kim JK (1999) Subcellular targeting of green fluorescent protein to plastids in transgenic rice plants provides a high-level expression system. Mol Breed 5:453–461

    Article  CAS  Google Scholar 

  • Kobayashi NI, Yamaji N, Yamamoto H, Okubo K, Ueno H, Costa A, Tanoi K, Matsumura H, Fujii-Kashino M, Horiuchi T, Nayef MA, Shabala S, An G, Ma JF, Horie T (2017) OsHKT1;5 mediates Na+ exclusion in the vasculature to protect leaf blades and reproductive tissues from salt toxicity in rice. Plant J 91:657–670

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Zhang C, Wei C, Wang M, Liu X, Yu F, Xue Q, Tu J (2016) The RING finger ubiquitin E3 ligase OsHTAS enhances heat tolerance by promoting H2O2-induced stomatal closure in rice. Plant Physiol 170:429

    Article  CAS  PubMed  Google Scholar 

  • Maršálová L, Vítámvás P, Hynek R, Prášil IT, Kosová K (2016) Proteomic response of Hordeum vulgare cv. Tadmor and Hordeum marinum to salinity stress: similarities and differences between a glycophyte and a halophyte. Front Plant Sci 7:1154

    Article  PubMed  PubMed Central  Google Scholar 

  • Mäser P, Eckelman B, Vaidyanathan R, Horie T, Fairbairn DJ, Kubo M, Yamagami M, Yamaguchi K, Nishimura M, Uozumi N, Robertson W, Sussman MR, Schroeder JI (2002a) Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett 531:157–161

    Article  PubMed  Google Scholar 

  • Mäser P, Hosoo Y, Goshima S, Horie T, Eckelman B, Yamada K, Yoshida K, Bakker EP, Shinmyo A, Oiki S, Schroeder JI, Uozumi N (2002b) Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per-subunit HKT transporters from plants. Proc Natl Acad Sci USA 99:6428–6433

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Matz MV, Fradkov AF, Labas YA, Savitsky AP, Zaraisky AG, Markelov ML, Lukyanov SA (1999) Fluorescent proteins from nonbioluminescent Anthozoa species. Nat Biotechnol 17:969–973

    Article  CAS  PubMed  Google Scholar 

  • Mian A, Oomen RJ, Isayenkov S, Sentenac H, Maathuis FJ, Véry AA (2011) Over-expression of an Na+- and K+-permeable HKT transporter in barley improves salt tolerance. Plant J 68:468–479

    Article  CAS  PubMed  Google Scholar 

  • Møller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Coates JC, Haseloff J, Tester M (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21:2163–2178

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Munns R, James R, Islam A, Colmer T (2011) Hordeum marinum-wheat amphiploids maintain higher leaf K+:Na+ and suffer less leaf injury than wheat parents in saline conditions. Plant Soil 348:365–377

    Article  CAS  Google Scholar 

  • Munns R, James RA, Xu B, Athman A, Conn SJ, Jordans C, Byrt CS, Hare RA, Tyerman SD, Tester M, Plett D, Gilliham M (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotechnol 30:360–364

    Article  CAS  PubMed  Google Scholar 

  • Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136

    Article  CAS  PubMed  Google Scholar 

  • Pascal MS, Yoshihiro H, Shinobu G, Tomoaki H, Brendan E, Katsuyuki Y (2002) Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per-subunit HKT transporters from plants. Proc Natl Acad Sci USA 99:6428–6433

    Article  CAS  Google Scholar 

  • Platten JD, Cotsaftis O, Berthomieu P, Bohnert H, Davenport RJ, Fairbairn DJ, Horie T, Leigh RA, Lin HX, Luan S, Mäser P, Pantoja O, Rodríguez-Navarro A, Schachtman DP, Schroeder JI, Sentenac H, Uozumi N, Véry AA, Zhu JK, Dennis ES, Tester M (2006) Nomenclature for HKT transporters, key determinants of plant salinity tolerance. Trends Plant Sci 11:372–374

    Article  CAS  PubMed  Google Scholar 

  • Pornsiriwong W, Estavillo GM, Chan KX, Tee EE, Ganguly D, Crisp PA, Phua SY, Zhao C, Qiu J, Park J, Yong MT, Nisar N, Yadav AK, Schwessinger B, Rathjen J, Cazzonelli CI, Wilson PB, Gilliham M, Chen ZH, Pogson BJ (2017) A chloroplast retrograde signal, 3′-phosphoadenosine 5′-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination. Elife 6:e23361

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiu L, Wu DZ, Ali S, Cai SG, Dai F, Jin XL, Wu FB, Zhang GP (2011) Evaluation of salinity tolerance and analysis of allelic function of HvHKT1 and HvHKT2 in Tibetan wild barley. Theor Appl Genet 122:695–703

    Article  CAS  PubMed  Google Scholar 

  • Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146

    Article  CAS  PubMed  Google Scholar 

  • Rodrígueznavarro A, Rubio F (2006) High-affinity potassium and sodium transport systems in plants. J Exp Bot 57:1149–1160

    Article  Google Scholar 

  • Rubio F, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660–1663

    Article  CAS  PubMed  Google Scholar 

  • Rubio F, Schwarz M, Gassmann W, Schroeder JI (1999) Genetic selection of mutations in the high affinity K+ transporter HKT1 that define functions of a loop site for reduced Na+ permeability and increased Na+ tolerance. J Biol Chem 274:6839–6847

    Article  CAS  PubMed  Google Scholar 

  • Seckin B, Turkan I, Sekmen AH, Ozfi̇dan C (2010) The role of antioxidant defense systems at differential salt tolerance of Hordeum marinum Huds. (sea barleygrass) and Hordeum vulgare L. (cultivated barley). Environ Exp Bot 69:76–85

    Article  CAS  Google Scholar 

  • Uozumi N, Kim EJ, Rubio F, Yamaguchi T, Muto S, Tsubota A, Bakker EP, Nakamura T, Schroeder JI (2000) The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopus laevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiol 122:1249–1259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waters S, Gilliham M, Hrmova M (2013) Plant high-affinity potassium (HKT) transporters involved in salinity tolerance: structural insights to probe differences in ion selectivity. Int J Mol Sci 14:7660–7680

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu DZ, Shen QF, Cai SG, Chen ZH, Dai F, Zhang GP (2013) Ionomic responses and correlations between elements and metabolites under salt stress in wild and cultivated barley. Plant Cell Physiol 54:1976–1988

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–444

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by National Natural Science Foundation of China (31620103912, 31771685), China Agriculture Research System (CARS-05) and Jiangsu Collaborative Innovation Centre for Modern Crop Production (JCIC-MCP). We thank Dr. JM Xu (Zhejiang University, China) for elements analysis.

Author information

Authors and Affiliations

  1. Department of Agronomy, Key Laboratory of Crop Germplasm Resource of Zhejiang Province, Zhejiang University, Hangzhou, 310058, China

    Lu Huang, Liuhui Kuang, Liyuan Wu, Dezhi Wu & Guoping Zhang

Authors
  1. Lu Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liuhui Kuang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liyuan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dezhi Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guoping Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dezhi Wu.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 1339 kb)

Supplementary material 2 (XLSX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, L., Kuang, L., Wu, L. et al. Comparisons in functions of HKT1;5 transporters between Hordeum marinum and Hordeum vulgare in responses to salt stress. Plant Growth Regul 89, 309–319 (2019). https://doi.org/10.1007/s10725-019-00538-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-019-00538-7

Keywords

Search

Navigation