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Coordination of AtHKT1;1 and AtSOS1 facilitates Na+ and K+ homeostasis in Arabidopsis thaliana under salt stress

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Abstract

Reducing Na+ accumulation and maintaining K+ stability in plant is one of the key strategies for improving salt tolerance. AtHKT1;1 and AtSOS1 are not only the salt tolerance determinants themselves, but also mediate K+ uptake and transport indirectly. To assess the contribution of AtHKT1;1 and AtSOS1 to Na+ homeostasis and K+ nutrition in plant, net Na+ and K+ uptake rate, Na+ and K+ distributions in Arabidopsis thaliana wild type (WT), hkt1;1 mutant (athkt1;1) and sos1 mutant (atsos1) were investigated. Results showed that under 2.5 mM K+ plus 25 or 100 mM NaCl, athkt1;1 shoot concurrently accumulated more Na+ and less K+ than did WT shoot, suggesting that AtHKT1;1 was critical for controlling Na+ and K+ distribution in plant; while atsos1 root accumulated more Na+ and absorbed lower K+ than did WT root, implying that AtSOS1 was determiner of Na+ excretion and K+ acquisition. Under 0.01 mM K+, athkt1;1 absorbed lower Na+ than did WT with 100 mM NaCl, suggesting that AtHKT1;1 is involved in Na+ uptake in roots; while atsos1 shoot accumulated less Na+ than did WT shoot no matter with 25 or 100 mM NaCl, implying that AtSOS1 played a key role in controlling long-distance Na+ transport from root to shoot. We present a model in which coordination of AtHKT1;1 and AtSOS1 facilitates Na+ and K+ homeostasis in A. thaliana under salt stress: under the normal K+, the major function of AtHKT1;1 is Na+ unloading and AtSOS1 is mainly involved in Na+ exclusion, whereas under the low K+, AtHKT1;1 may play a dominant role in Na+ uptake and AtSOS1 may be mainly involved in Na+ loading into the xylem.

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References

  • Berthomieu P, Conéjéro G, Nublat A, Brackenbury WJ, Lambert C, Savio C, Uozumi N, Oiki S, Yamada K, Cellier F, Gosti F, Simonneau T, Eassah PA, Tester M, Véry AA, Sentenac H, Casse F (2003) Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J 22:2004–2014

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Davenport RJ, Muñoz-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  PubMed  CAS  Google Scholar 

  • Epstein E (1998) How calcium enhances plant salt tolerance. Science 280:1906–1907

    Article  PubMed  CAS  Google Scholar 

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319

    Article  PubMed  CAS  Google Scholar 

  • Flowers TJ, Hajibagheri MA (2001) Salinity tolerance in Hordeum vulgare: ion concentrations in root cells of cultivars differing in salt tolerance. Plant Soil 231:1–9

    Article  CAS  Google Scholar 

  • Flowers TJ, Läuchli A (1983) Sodium versus potassium: substitution and compartmentation. Enc plant physiol 158:651–681

    Google Scholar 

  • Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferrière N, Thibaud JB, 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

    Article  PubMed  CAS  Google Scholar 

  • Gong JM, Waner DA, Horie T, Li SL, Horie R, Abid KB, Schroeder JI (2004) Microarray-based rapid cloning of an ion accumulation deletion mutant in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:15404–15409

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Guo Q, Wang P, Ma Q, Zhang JL, Bao AK, Wang SM (2012) Selective transport capacity for K+ over Na+ is linked to the expression levels of PtSOS1 in halophyte Puccinellia tenuiflora. Functional Plant Biol 39:1047–1057

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Horie T, Costa A, Kim TH, Han MJ, Horie R, Leung HY, Miyao A, Hirochika H, An G, Schroeder JI (2007) Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J 26:3003–3014

    Article  PubMed  CAS  PubMed Central  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  PubMed  CAS  PubMed Central  Google Scholar 

  • Leigh RA, Wyn Jones RG (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 

  • Liu K, Li L, Luan S (2006) Intracellular K+ sensing of SKOR, a Shaker-type K+ channel from Arabidopsis. Plant J 46:260–268

    Article  PubMed  CAS  Google Scholar 

  • Mäser P, Eckelman B, Vaidyanathan R, Horie T, Fairbairn DJ, Kubo M, Yamagamid M, Yamaguchie K, Nishimurae M, Uozumic N, Robertsonf W, Sussmanf MR, Schroedera JI (2002) 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, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJM, Sanders D, Harper JF, Tchieu J, Gribakov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001). Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667

    Article  PubMed  PubMed Central  Google Scholar 

  • Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiol 109:735–742

    PubMed  CAS  PubMed Central  Google Scholar 

  • Oh DH, Lee SY, Bressan RA, Yun DJ, Bohnert HJ (2010) Intracellular consequences of SOS1 deficiency during salt stress. J Exp Bot 61:1205–1213

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Qi Z, Spalding EP (2004) Protection of plasma membrane K+ transport by the salt overly sensitive1 Na+-H+ antiporter during salinity stress. Plant Physiol 136:2548–2555

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee B, Matsumoto TK, Koiwa H, Zhu JK, Bressan RA, Hasegawa PM (2001) AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc Natl Acad Sci 98:14150–14155

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Shabala S, Cuin TA, Pang JY, Percey W, Chen ZH, Conn S, Eing C, Wegner LH (2010) Xylem ionic relations and salinity tolerance in barley. Plant J 61:839–853

    Article  PubMed  CAS  Google Scholar 

  • Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sunarpi Horie T, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938

    Article  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Véry AA, Sentenac H (2003) Molecular mechanisms and regulation of K+ transport in higher plants. Annu Rev Plant Biol 54:575–603

    Article  PubMed  Google Scholar 

  • ai]Wang SM, Zhang JL, Flowers TJ (2007) Low-affinity Na+ uptake in the halophyte Suaeda maritima. Plant Physiol 145:559–571

    Article  Google Scholar 

  • Wang CM, Zhang JL, Liu XS, Li Z, Wu GQ, Cai JY, Flowers TJ, Wang SM (2009) Puccinellia tenuiflora maintains a low Na+ level under salinity by limiting unidirectional Na+ influx resulting in a high selectivity for K+ over Na+. Plant Cell Environ 32:486–496

    Article  PubMed  CAS  Google Scholar 

  • Wegner LH, De Boer AH (1997) Properties of two outward rectifying channels in root xylem parenchyma cells suggest a role in K+ homeostasis and long-distance signaling. Plant Physiol 115:170–1719

    Google Scholar 

  • Wegner LH, Raschke K (1994) Ion channels in the xylem parenchyma of barley roots. Plant Physiol 105:799–813

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wu SJ, Ding L, Zhu JK (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8:617–627

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang HM, Kim MS, Sun Y, Dowd SE, Shi HZ, Paré PW (2008) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant-Microbe Interact 21:737–744

    Article  PubMed  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann S, Sentenac H (1992) Plant ion channels: from molecular structures to physiological functions. Curr Opin Plant Biol 2:477–482

    Article  Google Scholar 

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Correspondence to Suo-Min Wang.

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Wang, Q., Guan, C. & Wang, SM. Coordination of AtHKT1;1 and AtSOS1 facilitates Na+ and K+ homeostasis in Arabidopsis thaliana under salt stress. J. Plant Biol. 57, 282–290 (2014). https://doi.org/10.1007/s12374-014-0222-y

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