Acta Physiologiae Plantarum

, Volume 36, Issue 3, pp 687–698 | Cite as

Root apoplastic transport and water relations cannot account for differences in Cl transport and Cl/NO3 interactions of two grapevine rootstocks differing in salt tolerance

Original Paper


Grapevine is moderately sensitive to salinity and accumulation of toxic levels of Cl in leaves is the major reason for salt-induced symptoms. In this study, apoplastic Cl uptake and transport mechanism(s) were investigated in two grapevine (Vitis sp.) rootstock hybrids differing in salt tolerance; 1103 Paulsen (salt tolerant) and K 51–40 (salt sensitive). Increased external salinity caused high Cl accumulation in shoots of the salt sensitive K 51–40 in comparison to Paulsen. Measurement of 15NO3 net fluxes under high salinity showed that by increasing external Cl concentrations K 51–40 roots showed reduced NO3 accumulation. This was associated with increased accumulation of Cl. In comparison to Paulsen, K 51–40 showed reduced NO3/Cl root selectivity with increased salinity, but Paulsen had lower selectivity over the whole salinity range (0–45 mM). To examine if root hydraulic and permeability characterisations accounted for differences between varieties, the root pressure probe was used on excised roots. This showed that the osmotic Lpr was significantly smaller than hydrostatic Lpr, but no obvious difference was observed between the rootstocks. The reflection coefficient (σ) values (0.48–0.59) were the same for both rootstocks, and root anatomical studies showed no obvious difference in apoplastic barriers of the main and lateral roots. Comparing the uptake of Cl with an apoplastic tracer, PTS (3-hydroxy-5,8,10-pyrentrisulphonic acid), showed that there was no correlation between Cl and PTS transport. These results indicated that bypass flow of salts to the xylem is the same for both rootstocks (0.77 ± 0.2 and 1.05 ± 0.12 %) and hence pointed to differences in membrane transport to explain difference in Cl transport to the shoot.


Salinity Cl transport Grapevine PTS Pressure probe Apoplastic pathway 


  1. Azaizeh H, Steudle E (1991) Effects of salinity on water transport of excised maize (Zea mays L.) roots. Plant Physiol 97:1136–1145PubMedCentralPubMedCrossRefGoogle Scholar
  2. Bernstein L (1975) Effects of salinity and sodicity on plant growth. Annu Rev Phytopathol 13:295–312CrossRefGoogle Scholar
  3. Bramley H, Turner NC, Turner DW, Tyerman SD (2007) Comparison between gradient-dependent hydraulic conductivities of roots using the root pressure probe: the role of pressure propagation and implications for the relative roles of parallel radial pathways. Plant Cell Environ 30:861–874PubMedCrossRefGoogle Scholar
  4. Brundrett MC, Enstone DE, Peterson CA (1988) A berberine-aniline blue fluorescent staining procedure for suberin, lignin and callose in plant tissue. Protoplasma 146:133–142CrossRefGoogle Scholar
  5. Cataldo DA, Haroon M, Schrader LE, Young VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6(1):71–80CrossRefGoogle Scholar
  6. Cramer GR, Ergül A, Grimplet J, Tillett RL, Tattersall EAR, Bohlman MC, Vincent D, Sonderegger J, Evans J, Osborne G, Quilici D, Schlauch KA, David A, Schooley DA, Cushman JC (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomics 7:111–134PubMedCrossRefGoogle Scholar
  7. Downton WJS (1977) Photosynthesis in salt-stressed grapevines. Aust J Plant Physiol 4:183–192CrossRefGoogle Scholar
  8. Downton WJS (1985) Growth and mineral composition of the Sultana grapevine as influenced by salinity and rootstock. Aust J Agric Res 36:425–439CrossRefGoogle Scholar
  9. Downton WJS, Millhouse J (1983) Turgor maintenance during salt stress prevents loss of variable fluorescence in grapevine leaves. Plant Sci Lett 31:1–7CrossRefGoogle Scholar
  10. Fisarakis I, Nikolaou N, Tsikalas P, Therios I, Stavarakas D (2004) Effect of salinity and rootstock on concentration of potassium, calcium, magnesium, phosphorus and nitrate-nitrogen in Thompson seedless grapevine. J Plant Nutr 27(12):2117–2134CrossRefGoogle Scholar
  11. Fiscus EL (1975) The interaction between osmotic and pressure induced water flow in plant roots. Plant Physiol 55:917–922PubMedCentralPubMedCrossRefGoogle Scholar
  12. Flowers TJ, Yeo AR (1992) Solute transport in plants. Chapman and Hall, New YorkCrossRefGoogle Scholar
  13. Frota JNE, Tucker TC (1987) Absorption rates of ammonium and nitrate by red kidney beans under salt and water stress. Soil Sci Soc Am J 42:753–756CrossRefGoogle Scholar
  14. Garcia M, Charbaji T (1993) Effect of sodium chloride salinity on cation equilibria in grapevine. J Plant Nutr 16(11):2225–2237CrossRefGoogle Scholar
  15. Garcia A, Rizzo CA, UD-Din J, Bartos SL, Senadhira D, Flowers TJ, Yeo AR (1997) Sodium and potassium transport to the xylem are inherited independently in rice, and the mechanism of sodium:potassium selectivity differs between rice and wheat. Plant Cell Environ 20:1167–1174CrossRefGoogle Scholar
  16. Gloser V, Zwieniecki MA, Orians C, Holbrook NM (2007) Dynamic changes in root hydraulic properties in response to nitrate availability. J Exp Bot 58:2409–2415PubMedCrossRefGoogle Scholar
  17. Gorska A, Zwieniecka A, Holbrook NM, Zwieniecki MA (2008a) Nitrate induction of root hydraulic conductivity in maize is not correlated with aquaporin expression. Planta 228:989–998PubMedCrossRefGoogle Scholar
  18. Gorska A, Ye Q, Holbrook NM, Zwieniecki MA (2008b) Nitrate control of root hydraulic properties in plants: translating local information to whole plant response. Plant Physiol 148:1159–1167PubMedCentralPubMedCrossRefGoogle Scholar
  19. Gratten SR, Grieve CM (1994) Mineral nutrient acquisition and response by plants grown in saline environment. In: Pessarakli M (ed) Handbook of plant and crop stress. Marcel Dekker Inc., New York, pp 203–226Google Scholar
  20. Greenway H (1965) Salt tolerance and crop production: a comprehensive approach. Annu Rev Phytopathol 25:271–291Google Scholar
  21. Hanson PJ, Succof EI, Markhart AH (1985) Quantifying apoplastic flux through red pine root systems using trisodium, 3-hydroxy-5,8,10-pyrenetrisulfonate. Plant Physiol 77:21–24PubMedCentralPubMedCrossRefGoogle Scholar
  22. Hardie WJ, Crimai RM (2000) Grapevine rootstocks. In: Coombe BG, Dry PR (eds) Viticulture volume 1 resources, chapter 8. Winetitles, London, pp 154–176Google Scholar
  23. Jaenicke H, Lips HS, Ullrich WR (1996) Growth, ion distribution, potassium and nitrate uptake of Leucaena leucocephala and effects of NaCl. Plant Physiol Biochem 34(5):743–751Google Scholar
  24. Kafkafi U, Valoras N, Letey J (1982) Chloride interaction with nitrate and phosphate nutrition in tomato (Lycopersicon esculentum L.). J Plant Nutr 5(12):1369–1385CrossRefGoogle Scholar
  25. Kamaluddin M, Zwiazek JJ (2001) Metabolic inhibition of root water flow in red-osier dogwood (Cornus stolonifera) seedlings. J Exp Bot 52:739–745PubMedGoogle Scholar
  26. Karahara I, Ikeda A, Kondo T, Uetake Y (2004) Development of the Casparian strip in primary roots of maize under salt stress. Planta 219:41–47PubMedCrossRefGoogle Scholar
  27. Knipfer T, Das D, Steudle E (2007) During measurements of root hydraulics with pressure probes, the contribution of unstirred layers is minimized in the pressure relaxation mode: comparison with pressure clamp and high-pressure flowmeter. Plant Cell Environ 30:845–860PubMedCrossRefGoogle Scholar
  28. Lauchli PJC (1976) Apoplastic transport in tissue. In: Luttge U, Pitman MG (eds) Encyclopedia of plant physiology. New series, vol 2B. Springer, Berlin, pp 3–33Google Scholar
  29. Lawton JR, Todd A, Naidoo DK (1981) Preliminary investigations into the structure of the roots of the mangroves, Avicennia marina and Bruguiera gymnorrhiza, in relation to ion uptake. New Phytol 88:713–722CrossRefGoogle Scholar
  30. Mahajan TS, Sonar KR (1980) Effect of NaCl and Na2SO4 on dry matter accumulation and uptake of N, P and K by wheat. J Maharashtra Agric Univ 15:110–112Google Scholar
  31. Miklos E, Zs Szegletes, Erdei L (2000) Nitrate and chloride transport interaction in grapevine. Acta Horticult 526:249–254Google Scholar
  32. Miyamoto N, Steudle E, Hirasawa T, Lafitte R (2001) Hydraulic conductivity of rice roots. J Exp Bot 52:1835–1846PubMedCrossRefGoogle Scholar
  33. Moon GJ, Clough BF, Peterson CA, Allaway WG (1986) Apoplastic and symplastic pathways in Avicennia marina (Forsk.) roots revealed by fluorescent dyes. Aust J Plant Physiol 13:637–648CrossRefGoogle Scholar
  34. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  35. Nicholas P (1997) Rootstock characteristics. Aust Grapegrower Winemak 400:30Google Scholar
  36. Palfi G (1965) The effect of sodium salts on the nitrogen, phosphorus, potassium, sodium and amino acid content of rice shoots. Plant Soil 22:127–135CrossRefGoogle Scholar
  37. Passioura JB (1988) Water transport in and to the root. Annu Rev Plant Physiol Plant Mol Biol 39:245–265CrossRefGoogle Scholar
  38. Pessarakli M, Tucker TC (1985) Uptake of nitrogen-15 by cotton under salt stress. Soil Sci Soc Am J 49:149–152CrossRefGoogle Scholar
  39. Pitman MG (1982) Transport across plant roots. Quart Rev Biophys 15:481–554CrossRefGoogle Scholar
  40. Prior LD, Grieve AM, Slavich PG, Culls BR (1992) Sodium chloride and soil texture interactions in irrigated field grown Sultana grapevines. 2. Plant mineral content, growth and physiology. Aust J Agric Res 43:1067–1083CrossRefGoogle Scholar
  41. Sanderson J (1983) Water uptake by different regions of the barley root. Pathways of radial flow in relation to development of the endodermis. J Exp Bot 34:240–253CrossRefGoogle Scholar
  42. Steudle E (1993) Pressure probe techniques: basic principles and application to studies of water and solute relations at the cell, tissue and organ level. In: Smith JAC, Griffith H (eds) Water deficits: plant responses from cell to community. Bios Scientific Publishers, Oxford, pp 5–36Google Scholar
  43. Steudle E (2000) Water transport by plant roots: an integration of views. Plant Soil 226:45–56CrossRefGoogle Scholar
  44. Steudle E, Frensch J (1996) Water transport in plants: role of the apoplast. Plant Soil 187:67–79CrossRefGoogle Scholar
  45. Steudle E, Jeschke W (1983) Water transport in barley roots. Planta 158(3):237–248PubMedCrossRefGoogle Scholar
  46. Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788Google Scholar
  47. Stevens RM, Harvey G, Partington DL, Coomb BG (1999) Irrigation of grapevines with saline water at different growth stages. 1. Effects on soil, vegetative growth and yield. Aust J Agric Res 50:343–355CrossRefGoogle Scholar
  48. Teakle NL, Tyerman SD (2010) Mechanisms of Cl-transport contributing to salt tolerance. Plant Cell Environ 33(4):566–589PubMedCrossRefGoogle Scholar
  49. Tyerman SD, Findlay GP (1989) Current-voltage curves of single Cl channels which coexist with two types ofK+ channel in the tonoplast of Chara corallina. J Exp Bot 40:105–117CrossRefGoogle Scholar
  50. Vesk PA, Ashford AE, Markovina AL, Allaway WG (2000) Apoplastic barriers and their significance in the exodermis and sheath of Eucalyptus pilularisPisolithus ectomycorrhizas. New Phytol 145:333–346CrossRefGoogle Scholar
  51. Walker RR, Blackmore DH, Clingeleffer PR, Correl RL (2002) Rootstock effects on salt tolerance of irrigated field-grown grapevines (Vitis vinifera L. cv. Sultana). 1-Yield and vigor inter-relationships. Aust J Grape Wine Res 8:3–14CrossRefGoogle Scholar
  52. Walker RR, Blackmore DH, Clingelffer PR, Correl R (2004) Rootstock effects on salt tolerance of irrigated field-grown grapevines (Vitis vinifera L. cv. Sultana) 2. Ion concentrations in leaves and juice. Aust J Grape Wine Res 10(2):90–99Google Scholar
  53. White PJ, Broadley MR (2001) Chloride in soils and its uptake and movement within the plant: a review. Ann Bot 88:967–988CrossRefGoogle Scholar
  54. Yeo AR, Yeo ME, Flowers TJ (1987) The contribution of an apoplastic pathway to sodium uptake by rice roots in saline conditions. J Exp Bot 38:1141–1153CrossRefGoogle Scholar
  55. Yeo AR, Flowers SA, Rao G, Welfare K, Senanayake N, Flowers TJ (1999) Silicon reduces sodium uptake in rice (Oryza sativa L.) in saline conditions and this is accounted for by a reduction in the transpirational bypass flow. Plant, Cell and Environ 22:559–565CrossRefGoogle Scholar
  56. Zeier J, Schreiber L (1998) Comparative investigation of primary and tertiary endodermal cell walls isolated from the roots of five monocotyledonous species: chemical composition in relation to fine structure. Planta 206:349–361CrossRefGoogle Scholar
  57. Zimmermann HM, Steudle E (1998) Apoplastic transport across young maize roots: effect of the exodermis. Planta 206:7–19CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2013

Authors and Affiliations

  1. 1.Biology Department, Faculty of SciencesUrmia UniversityUrmiaIran
  2. 2.School of Agriculture, Food and WineUniversity of AdelaideAdelaideAustralia

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