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Planta

, Volume 243, Issue 1, pp 97–114 | Cite as

Salt intolerance in Arabidopsis: shoot and root sodium toxicity, and inhibition by sodium-plus-potassium overaccumulation

  • Rocío Álvarez-Aragón
  • Rosario Haro
  • Begoña Benito
  • Alonso Rodríguez-Navarro
Original Article

Abstract

Main conclusion

Arabidopsis plants in NaCl suffering half growth inhibition do not suffer osmotic stress and seldom shoot Na + toxicity; overaccumulation of Na + plus K + might trigger the inhibition.

It is widely assumed that salinity inhibits plant growth by osmotic stress and shoot Na+ toxicity. This study aims to examine the growth inhibition of Arabidopsis thaliana by NaCl concentrations that allow the completion of the life cycle. Unaffected Col-0 wild-type plants were used to define nontoxic Na+ contents; Na+ toxicities in shoots and roots were analyzed in hkt1 and sos1 mutants, respectively. The growth inhibition of Col-0 plants at 40 mM Na+ was mild and equivalent to that produced by 8 and 4 mM Na+ in hkt1 and sos1 plants, respectively. Therefore, these mutants allowed to study the toxicity of Na+ in the absence of an osmotic challenge. Col-0 and Ts-1 accessions showed very different Na+ contents but similar growth inhibitions; Ts-1 plants showed very high leaf Na+ contents but no symptoms of Na+ toxicity. Ak-1, C24, and Fei-0 plants were highly affected by NaCl showing evident symptoms of shoot Na+ toxicity. Increasing K+ in isotonic NaCl/KCl combinations dramatically decreased the Na+ content in all Arabidopsis accessions and eliminated the signs of Na+ toxicity in most of them but did not relieve growth inhibition. This suggested that the dominant inhibition in these conditions was either osmotic or of an ionic nature unspecific for Na+ or K+. Col-0 and Ts-1 plants growing in sorbitol showed a clear osmotic stress characterized by a notable decrease of their water content, but this response did not occur in NaCl. Overaccumulation of Na+ plus K+ might trigger growth reduction in NaCl-treated plants.

Keywords

Arabidopsis Osmotic inhibition Salt tolerance Sodium toxicity 

Notes

Acknowledgments

We thank Carlos Alonso-Blanco, Rhonda Meyer, and José Manuel Pardo for kindly providing seeds of the Arabidopsis accession, and gl1, hkt1-4, and sos1-1 mutants. This work was supported by the Spanish Ministerio de Economía y Competitividad, Grant number AGL2012-36174 and fellowship to RA-A.

Supplementary material

425_2015_2400_MOESM1_ESM.pdf (512 kb)
Supplementary material 1 (PDF 512 kb)

References

  1. Achard P, Cheng H, De Grauwe L et al (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94PubMedCrossRefGoogle Scholar
  2. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2007) Molecular biology of the cell, 5th edn. Garland Science, New YorkGoogle Scholar
  3. Alemán F, Nieves-Cordones M, Martínez V, Rubio F (2009) Potassium/sodium steady-state homeostasis in Thelungiella halophila and Arabidopsis thaliana under long-term salinity conditions. Plant Sci 176:768–774CrossRefGoogle Scholar
  4. Algeo TJ, Scheckler SE (1998) Terrestrial-marine teleconnections in the Devonian: links between the evolution of land plants, weathering process, and marine anoxic events. Phil Trans R Soc Lond B 353:113–130CrossRefGoogle Scholar
  5. Amtmann A, Sanders D (1998) Mechanisms of Na+ uptake by plant cells. Adv Bot Res 29:75–112CrossRefGoogle Scholar
  6. Attia H, Arnaud N, Karray N, Lachaâl M (2008) Long-term effects of mild salt stress on growth, ion accumulation and superoxide dismutase expression of Arabidopsis rosette leaves. Physiol Plant 132:293–305PubMedCrossRefGoogle Scholar
  7. Baxter I, Brazelton JN, Yu D et al (2010) A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1;1. PLoS Genet 6(11):e1001193PubMedPubMedCentralCrossRefGoogle Scholar
  8. Benito B, Garciadeblás B, Schreier P, Rodríguez-Navarro A (2004) Novel P-type ATPases mediate high-affinity potassium or sodium uptake in fungi. Eukaryot Cell 3:359–368PubMedPubMedCentralCrossRefGoogle Scholar
  9. Benito B, Garciadeblás B, Pérez-Martín J, Rodríguez-Navarro A (2009) Growth at high pH and sodium and potassium tolerance in media above the cytoplasmic pH depend on ENA ATPases in Ustilago maydis. Eukaryot Cell 8:821–829PubMedPubMedCentralCrossRefGoogle Scholar
  10. Benito B, Gaciadeblás B, Fraile-Escanciano A, Rodríguez-Navarro A (2011) Potassium and sodium uptake in fungi. The transporter diversity in Magnaporthe oryzae. Fungal Genet Biol 48:812–822PubMedCrossRefGoogle Scholar
  11. Benito B, Garciadeblás B, Rodríguez-Navarro A (2012) Hak transporters from Physcomitrella patens and Yarrowia lipolytica mediate sodium uptake. Plant Cell Physiol 53:1117–1123PubMedCrossRefGoogle Scholar
  12. Benlloch M, Ojeda MA, Ramos J, Rodriguez-Navarro A (1994) Salt sensitivity and low discrimination between potassium and sodium in bean plants. Plant Soil 166:117–123CrossRefGoogle Scholar
  13. Bennett TH, Flowers TJ, Bromham L (2013) Repeated evolution of salt-tolerance in grasses. Biol Lett 9:20130029PubMedPubMedCentralCrossRefGoogle Scholar
  14. Berthomieu P, Conéjéro G, Nublat A et al (2003) Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J 22:2004–2014PubMedPubMedCentralCrossRefGoogle Scholar
  15. Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta 1465:140–151PubMedCrossRefGoogle Scholar
  16. Boyer JS (1965) Effects of osmotic water stress on metabolic rates of cotton plants with open stomata. Plant Physiol 40:229–234PubMedPubMedCentralCrossRefGoogle Scholar
  17. Cheeseman JM (2013) The integration of activity in saline environments: problems and perspectives. Funct Plant Biol 40:759–774Google Scholar
  18. Clouse SD, Langford M (1996) Brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111:671–678PubMedPubMedCentralCrossRefGoogle Scholar
  19. 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 Arabidosis. Plant Cell Environ 30:497–507PubMedCrossRefGoogle Scholar
  20. Díaz-López L, Gimeno V, Lidón V, Simón I, Martínez V, García-Sánchez F (2012) The tolerance of Jatropha curcas seedlings to NaCl: an ecophysiological analysis. Plant Physiol Biochem 54:34–42PubMedCrossRefGoogle Scholar
  21. Dolferus R (2014) To grow or not to grow: a stressful decision for plants. Plant Sci 229:247–261PubMedCrossRefGoogle Scholar
  22. Evans HJ, Sorger G (1966) Role of mineral elements with emphasis on the univalent cations. Annu Rev Plant Physiol 17:47–76CrossRefGoogle Scholar
  23. Farquharson KL (2009) Targeted overexpression of a sodium transporter in the root stele increases salinity tolerance. Plant Cell 21:1875PubMedPubMedCentralCrossRefGoogle Scholar
  24. Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319PubMedCrossRefGoogle Scholar
  25. Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol 37:604–612CrossRefGoogle Scholar
  26. Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot-London 115:419–431CrossRefGoogle Scholar
  27. Handa S, Bressan RA, Handa AK, Carpita NC, Hasegawa PM (1983) Solutes contributing to osmotic adjustment in cultured plant cells adapted to water stress. Plant Physiol 73:834–843PubMedPubMedCentralCrossRefGoogle Scholar
  28. Haro R, Bañuelos MA, Rodríguez-Navarro A (2010) High-affinity sodium uptake in land plants. Plant Cell Physiol 51:68–79PubMedCrossRefGoogle Scholar
  29. Hasegawa PM (2013) Sodium (Na+) homeostasis and salt tolerance of plants. Environ Exp Bot 92:19–31CrossRefGoogle Scholar
  30. Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499PubMedCrossRefGoogle Scholar
  31. 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 33:552–565PubMedCrossRefGoogle Scholar
  32. Heyser JW, Nabors MW (1981a) Growth, water content, and solute accumulation of two tobacco cell lines cultured on sodium chloride, dextran, and polyethylene glycol. Plant Physiol 68:1454–1459PubMedPubMedCentralCrossRefGoogle Scholar
  33. Heyser JW, Nabors MW (1981b) Osmotic adjustment of cultured tobacco cells (Nicotiana tabacum var. Samsum) grown on sodium chloride. Plant Physiol 67:720–727PubMedPubMedCentralCrossRefGoogle Scholar
  34. Horie T, Sugawara M, Okunou K, Nakayama H, Schroeder JI, Shinmyo A, Yoshida K (2008) Functions of HKT transporters in sodium transport in roots and in protecting leaves from salinity stress. Plant Biotechnol 25:233–239CrossRefGoogle Scholar
  35. Horie T, Hauser F, Schroeder JI (2009) HKT transporter-mediated salinity resistance mechanism in Arabidopsis and monocot plants. Trends Plant Sci 14:660–668PubMedPubMedCentralCrossRefGoogle Scholar
  36. Jha D, Shirley N, Tester M, Roy SJ (2010) Variation in salinity tolerance and shoot sodium accumulation in Arabidopsis ecotypes linked to differences in the natural expression levels of transporters involved in sodium transport. Plant Cell Environ 33:793–804PubMedGoogle Scholar
  37. Kaddour R, M’rah S, Karray-Bouraoui N, Lambert C, Berthomieu P, Lahaâl M (2010) Physiological and molecular characterization of salt response of Arabidopsis thaliana NOK2 ecotype. Acta Physiol Plant 32:503–510CrossRefGoogle Scholar
  38. Katori T, Ikeda A, Iuchi S et al (2010) Dissecting the genetic control of natural variation in salt tolerance of Arabidopsis thaliana accessions. J Exp Bot 61:1125–1138PubMedPubMedCentralCrossRefGoogle Scholar
  39. Kinraide TB (1999) Interactions among Ca2+, Na+ and K+ in salinity toxicity: quantitative resolution of multiple toxic and ameliorative effects. J Exp Bot 50:1495–1505CrossRefGoogle Scholar
  40. Kronzucker HJ, Coskun D, Schulze LM, Wong JR, Britto DT (2013) Sodium as nutrient and toxicant. Plant Soil 369:1–23CrossRefGoogle Scholar
  41. Labidi N, Lachaâl M, Chibani F, Grignon C, Hajji M (2002) Variability of the response to sodium chloride of eight ecotypes of Arabidopsis thaliana. J Plant Nut 25:2627–2638CrossRefGoogle Scholar
  42. Lauter DJ, Meiri A, Shuali M (1988) Isoosmotic regulation of cotton and peanut at saline concentrations of K and Na. Plant Physiol 87:911–916PubMedPubMedCentralCrossRefGoogle Scholar
  43. Liu J, Zhu J-K (1997) An Arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proc Natl Acad Sci USA 94:14960–14964PubMedPubMedCentralCrossRefGoogle Scholar
  44. Liu T-Y, Chang C-Y, Chiou T-J (2009) The long-distance signaling of mineral macronutrients. Curr Opin Plant Biol 12:312–319PubMedCrossRefGoogle Scholar
  45. Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133CrossRefGoogle Scholar
  46. Maggio A, Miyazaki S, Veronese P et al (2002) Does proline accumulation play an active role in stress-induced growth reduction? Plant J 31:699–712PubMedCrossRefGoogle Scholar
  47. Maggio A, Raimondi G, Martino A, Pascale SD (2007) Salt stress response in tomato beyond the salinity tolerance threshold. Environ Exp Bot 59:276–282CrossRefGoogle Scholar
  48. Mäser P, Eckelman B, Vaidyanathan R et al (2002) Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett 531:157–161PubMedCrossRefGoogle Scholar
  49. Moller IS, Tester M (2007) Salinity tolerance of Arabidospsis: a good model for cereals? Trends Plant Sci 12:534–540PubMedCrossRefGoogle Scholar
  50. Moller IS, Gilliham M, Jha D et al (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21:2163–2178PubMedPubMedCentralCrossRefGoogle Scholar
  51. Morgan JM (1984) Osmoregulation and water stress in higher plants. Annu Rev Plant Physiol 35:299–319CrossRefGoogle Scholar
  52. Munns R (1993) Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant Cell Environ 16:15–24CrossRefGoogle Scholar
  53. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250PubMedCrossRefGoogle Scholar
  54. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  55. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–479CrossRefGoogle Scholar
  56. Pardo JM, Quintero FJ (2002) Plants and sodium ions: keeping company with the enemy. Genome Biol 3:1017.1011–1017.1013Google Scholar
  57. Plett D, Safwat G, Moller IS et al (2010) Improved salinity tolerance of rice through cell type-specific expression of AtHKT1;1. PLoS ONE 5(9):e12571PubMedPubMedCentralCrossRefGoogle Scholar
  58. Qiu QS, Barkla BJ, Vera-Estrella R, Zhu JK, Schumaker KS (2003) Na+/H+ exchange activity in the plasma membrane of Arabidopsis. Plant Physiol 132:1041–1052PubMedPubMedCentralCrossRefGoogle Scholar
  59. Quesada V, García-Martínez S, Piqueras P, Ponce MR, Micol JL (2002) Genetic architecture of NaCl tolerance in Arabidopsis. Plant Physiol 130:951–963PubMedPubMedCentralCrossRefGoogle Scholar
  60. Rahnama A, James RA, Poustini K, Munns R (2010) Stomatal conductance as a screen for osmotic stress tolerance in durum wheat growing in saline soil. Funct Plant Biol 37:255–263CrossRefGoogle Scholar
  61. Rajendran K, Tester M, Roy SJ (2009) Quantifying the three main components of salinity tolerance in cereals. Plant Cell Environ 32:237–249PubMedCrossRefGoogle Scholar
  62. Robinson SP, Downton WJS, Millhouse JA (1983) Photosynthesis and ion content of leaves and isolated chloroplasts of salt-treated spinach. Plant Physiol 73:238–242PubMedPubMedCentralCrossRefGoogle Scholar
  63. Rodríguez-Navarro A, Rubio F (2006) High-affinity potassium and sodium transport systems in plants J Exp Bot 57:1149–1160Google Scholar
  64. Ronchi A, Farina G, Gozzo F, Tonelli C (1997) Effects of a triazolic fungicide on maize plant metabolism: modifications of transcript abundance in resistance-related pathways. Plant Sci 130:51–62CrossRefGoogle Scholar
  65. Roy SJ, Negrao S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotech 26:115–124PubMedCrossRefGoogle Scholar
  66. Rozema J, Schat H (2013) Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture. Environ Exp Bot 92:83–95CrossRefGoogle Scholar
  67. Rus A, Lee BH, Munoz-Mayor A et al (2004) AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiol 136:2500–2511PubMedPubMedCentralCrossRefGoogle Scholar
  68. Rus A, Baxter I, Muthukumar B, Gustin J, Lahner B, Yakubova E, Salt DE (2006) Natural variants of AtHKT1 enhance Na+ accumulation in two wild populations of Arabidopsis. PLoS Genet 2(12):e210PubMedPubMedCentralCrossRefGoogle Scholar
  69. Salim M (1989) Effects of salinity and relative humidity on growth and ionic relations of plants. New Phytol 113:13–20CrossRefGoogle Scholar
  70. Schulze LM, Britto DT, Li M, Kronzucker HJ (2012) A pharmacological analysis of high-affinity sodium transport in barley (Hordeum vulgare L.): a 24Na+/42K+ study. J Exp Bot 63:2479–2489PubMedPubMedCentralCrossRefGoogle Scholar
  71. Shabala S, Cuin TA (2007) Potassium transport and plant salt tolerance. Physiol Plant 133:651–669CrossRefGoogle Scholar
  72. Shalhevet J, Hsiao TC (1986) Salinity and drought. A comparison of their effects on osmotic adjustment, assimilation, transpiration and growth. Irrig Sci 7:249–264CrossRefGoogle Scholar
  73. Shelden MC, Roessner U, Sharp RE, Tester M, Bacic A (2013) Genetic variation in the root growth response of barley genotypes to salinity stress. Funct Plant Biol 40:516–530CrossRefGoogle Scholar
  74. Shi H, Ishitani M, Kim C, Zhu J-K (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901PubMedPubMedCentralCrossRefGoogle Scholar
  75. Shi H, Quintero FJ, Pardo JM, Zhu J-K (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477PubMedPubMedCentralCrossRefGoogle Scholar
  76. Slayter RO (1961) Effects of several osmotic substrates on the water relationships of tomato. Aust J Biol Sci 14:519–540Google Scholar
  77. Sparks E, Wachsman G, Benfey PN (2013) Spatiotemporal signalling in plant development. Nature Rev Genet 14:631–644PubMedCrossRefGoogle Scholar
  78. Steinbach HB (1962) The prevalence of K. Perspect Biol Med 69:2015–2026Google Scholar
  79. Sunarpi Horie T, Motoda J et al (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938PubMedCrossRefGoogle Scholar
  80. Teakle NL, Tyerman SD (2010) Mechanisms of Cl transport contributing to salt tolerance. Plant Cell Environ 33:566–589PubMedCrossRefGoogle Scholar
  81. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527PubMedPubMedCentralCrossRefGoogle Scholar
  82. Van Oosten MJ, Sharkhuu A, Batelli G, Bressan RA, Maggio A (2013) The Arabidopsis thaliana mutant air1 implicates SOS3 in the regulation of anthocynins under salt stress. Plant Mol Biol 83:405–415PubMedCrossRefGoogle Scholar
  83. Wu S-J, Ding L, Zhu J-K (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8:617–627PubMedPubMedCentralCrossRefGoogle Scholar
  84. Zhang Z, Zhang S, Zhang Y et al (2011) Arabidopsis floral initiator SKB1 confers high salt tolerance by regulating transcription and pre-mRNA splicing through altering histone H4R3 and small nuclear ribonucleoprotein LSM4 methylation. Plant Cell 23:396–411PubMedPubMedCentralCrossRefGoogle Scholar
  85. Zhu J-K (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124:941–948PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Rocío Álvarez-Aragón
    • 1
  • Rosario Haro
    • 1
  • Begoña Benito
    • 1
  • Alonso Rodríguez-Navarro
    • 1
  1. 1.Centro de Biotecnología y Genómica de PlantasUniversidad Politécnica de MadridMadridSpain

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