Biologia plantarum 2016, 60:695-705 | DOI: 10.1007/s10535-016-0634-2

Tracing root permeability: comparison of tracer methods

E. Pecková1, E. Tylová1, A. Soukup1,*
1 Department of Experimental Plant Biology, Faculty of Natural Sciences, Charles University in Prague, Prague, Czech Republic

Root epidermis and apoplastic barriers (endodermis and exodermis) are the critical root structures involved in setting up plant-soil interface by regulating free apoplastic movement of solutes within root tissues. Probing root apoplast permeability with "apoplastic tracers" presents one of scarce tools available for detection of "apoplastic leakage" sites and evaluation of their role in overall root uptake of water, nutrients, or pollutants. Although the tracers are used for many decades, there is still not an ideal apoplastic tracer and flawless procedure with straightforward interpretation. In this article, we present our experience with the most frequently used tracers representing various types of chemicals with different characteristics. We examine their behaviour, characteristics, and limitations. Here, we show that results gained with an apoplastic tracer assay technique are reliable but depend on many parameters-chemical properties of a selected tracer, plant species, cell wall properties, exposure time, or sample processing.

Keywords: apoplast; berberine; endodermis; exodermis; ferrous ions; PAS reaction; propidium iodide; PTS
Subjects: root permeability; apoplast; endodermis; berberine; propidium iodide; PAS reaction; Casparian bands; tobacco; rice; maize
Species: Nicotiana tabacum; Oryza sativa; Zea mays

Received: October 22, 2015; Revised: February 1, 2016; Accepted: March 31, 2016; Published: December 1, 2016Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Pecková, E., Tylová, E., & Soukup, A. (2016). Tracing root permeability: comparison of tracer methods. Biologia plantarum, 60(4), 695-705. doi: 10.1007/s10535-016-0634-2.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)

    • Open full article

    References

    1. Aloni, R., Enstone, D.E., Peterson, C.A.: Indirect evidence for bulk water flow in root cortical cell walls of three dicotyledonous species. - Planta 207: 1-7, 1998. Go to original source...
    2. Armstrong, J., Armstrong, W.: Rice and Phragmites: effects of organic acids on growth, root permeability, and radial oxygen loss to the rhizosphere. - Amer. J. Bot. 88: 1359-1370, 2001. Go to original source...
    3. Armstrong, W., Cousins, D., Armstrong, J., Turner, D., Beckett, P.: Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis. - Ann. Bot. 86: 687-703, 2000. Go to original source...
    4. Barnabas, A.D.: Casparian band-like structures in the root hypodermis of some aquatic angiosperms. - Aquat. Bot. 55: 217-225, 1996. Go to original source...
    5. Bederska, M., Borucki, W., Znojek, E.: Movement of fluorescent dyes Lucifer Yellow (LYCH) and carboxyfluorescein (CF) in Medicago truncatula Gaertn. roots and root nodules. - Symbiosis 58: 183-190, 2012. Go to original source...
    6. Bramley, H., Turner, N.C., Turner, D.W., Tyerman, S.D.: Comparison between gradient-dependent hydraulic conductivities of roots using the root pressure probe: the role of pressure propagations and implications for the relative roles of parallel radial pathways. - Plant Cell Environ. 30: 861-874, 2007. Go to original source...
    7. Brundrett, M.C., Enstone, D.E., Peterson, C.A.: A berberineaniline blue fluorescent staining procedure for suberin, lignin, and callose in plant tissue. - Protoplasma 146: 133-142, 1988. Go to original source...
    8. Brundrett, M.C., Kendrick, B., Peterson, C.A.: Efficient lipid staining in plant material with Sudan Red 7B or Fluoral Yellow 088 in polyethylene glycol-glycerol. - Biotech. Histochem. 66: 111-116, 1991. Go to original source...
    9. Canny, M.: Transfusion tissue of pine needles as a site of retrieval of solutes from the transpiration stream. - New Phytol. 125: 227-232, 1993. Go to original source...
    10. Canny, M., Huang C.: Rates of diffusion into roots of maize. - New Phytol. 126: 11-19, 1994. Go to original source...
    11. Chaney, W., Kozlowski, T.: Patterns of water movement in intact and excised stems of Fraxinus americana and Acer saccharum seedlings. - Ann. Bot. 41: 1093-1100, 1977. Go to original source...
    12. Cholewa, E., Peterson, C.A.: Detecting exodermal Casparian bands in vivo and fluid-phase endocytosis in onion (Allium cepa L.) roots. - Can. J. Bot. 79: 30-37, 2001. Go to original source...
    13. Colmer, T.: Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. - Plant Cell Environ. 26: 17-36, 2003. Go to original source...
    14. De Lavison, R.: [About the penetration of some salts into the living plants. The role of endodermis.] - Rev. gen. Bot. 22: 225-241, 1910. [In French]
    15. Degenhardt, B., Gimmler, H.: Cell wall adaptations to multiple environmental stresses in maize roots. - J. exp. Bot. 51: 595-603, 2000. Go to original source...
    16. Enstone, D.E., Peterson, C.A.: The apoplastic permeability of root apices. - Can. J. Bot. 70: 1502-1512, 1992. Go to original source...
    17. Enstone, D.E., Peterson, C.A., Ma, F.: Root endodermis and exodermis: structure, function, and responses to the environment. - J. Plant Growth Regul. 21: 335-351, 2003.
    18. Epel, B.L., Bandurski, R.S.: Apoplastic domains and subdomains in the shoots of etiolated corn seedlings. - Physiol. Plant. 79: 599-603, 1990. Go to original source...
    19. Esau, K.: Plant Anatomy. - John Wiley & Sons, New York 1953.
    20. Faiyue, B., Al-Azzawi, M.J., Flowers, T.J.: The role of lateral roots in bypass flow in rice (Oryza sativa L.). - Plant Cell Environ. 33: 702-716, 2010.
    21. Geldner, N.: The endodermis. - Annu. Rev. Plant Biol. 64: 531-558, 2013. Go to original source...
    22. Gierth, M., Stelzer, R., Lehmann, H.: An analytical microscopical study on the role of the exodermis in apoplastic Rb+ (K+) transport in barley roots. - Plant Soil 207: 209-218, 1999.
    23. Hoagland, D.R., Arnon, D.I.: The water-culture method for growing plants without soil. - Circular California Agr. Exp. Sta. 347: 32, 1950.
    24. Hose, E., Clarkson, D., Steudle, E., Schreiber, L., Hartung, W.: The exodermis: a variable apoplastic barrier. - J. exp. Bot. 52: 2245-2264, 2001. Go to original source...
    25. Hosmani, P.S., Kamiya, T., Danku, J., Naseer, S., Geldner, N., Guerinot, M.L., Salt, D.E.: Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root. - Proc. nat. Acad. Sci. USA 110: 14498-14503, 2013. Go to original source...
    26. Knipfer, T., Fricke, W.: Root pressure and a solute reflection coefficient close to unity exclude a purely apoplastic pathway of radial water transport in barley (Hordeum vulgare). - New Phytol. 187: 159-170, 2010. Go to original source...
    27. Krishnamurthy, P., Jyothi-Prakash, P.A., Qin, L., He, J., Lin, Q., Loh, C.S., Kumar, P.P.: Role of root hydrophobic barriers in salt exclusion of a mangrove plant Avicennia officinalis. - Plant Cell Environ. 37: 1656-1671, 2014. Go to original source...
    28. Kroemer, K.: [Rhizodermis, hypodermis and endodermis of angiosperm roots. - Bibl. Bot. 59: 1-160, 1903. [In German]
    29. López-Pérez, L., Fernández-García, N., Olmos, E., Carvajal, M.: The phi thickening in roots of broccoli plants: an acclimation mechanism to salinity? - Int. J. Plant Sci. 168: 1141-1149, 2007. Go to original source...
    30. Meyer, C.J., Peterson, C.A.: Casparian bands occur in the periderm of Pelargonium hortorum stem and root. - Ann. Bot. 107: 591-598, 2011. Go to original source...
    31. Meyer, C.J., Seago, J.L., Jr., Peterson, C.A.: Environmental effects on the maturation of the endodermis and multiseriate exodermis of Iris germanica roots. - Ann. Bot. 103: 687-702, 2009. Go to original source...
    32. Mistrikova, I., Kozinka, V.: Patterns of long-distance movement of water in roots. - In: Loughman, B. (ed.) Structural and Functional Aspects of Transport in Roots. Pp. 165-168. Kluwer Academic Publisher, Dordrecht 1989.
    33. Moon, G., Peterson, C.A., Peterson, R.: Structural, chemical, and permeability changes following wounding in onion roots. - Can. J. Bot. 62: 2253-2259, 1984. Go to original source...
    34. Naseer, S., Lee, Y., Lapierre, C., Franke, R., Nawrath, C., Geldner, N.: Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. - Proc. nat. Acad. Sci. USA. 109: 10101-10106, 2012. Go to original source...
    35. North, G.B., Nobel, P.S.: Hydraulic conductivity of concentric root tissues of Agave deserti Engelm. under wet and drying conditions. - New Phytol. 130: 47-57, 1995. Go to original source...
    36. Ochiai, K., Matoh, T.: Characterization of the Na+ delivery from roots to shoots in rice under saline stress: excessive salt enhances apoplastic transport in rice plants. - Soil Sci. Plant Nutr. 48: 371-378, 2002. Go to original source...
    37. Oparka, K.: Uptake and compartmentation of fluorescent probes by plant cells. - J. exp. Bot. 42: 565-579, 1991. Go to original source...
    38. Opatrný, Z., Opatrná, J.: The specificity of the effect of 2,4-D and NAA of the growth, micromorphology, and occurrence of starch in long-term Nicotiana tabacum L. cell strains. - Biol. Plant. 18: 359-365, 1976. Go to original source...
    39. Pearse, A.: Histochemistry (Theoretical and Applied). - J.A. Churchill, London 1968.
    40. Perumalla, C.J., Peterson, C.A., Enstone, D.E.: A survey of angiosperm species to detect hypodermal Casparian bands. I. Roots with a uniseriate hypodermis and epidermis. - Bot. J. Linn. Soc. 103: 93-112, 1990. Go to original source...
    41. Peterson, C., Edgington, L.: Uptake of the systemic fungicide methyl 2-benzimidazolecarbamate and the fluorescent dye PTS [trisodium, 3-hydroxy-5, 8, 10-pyrenetrisulfonate] by onion roots. - Phytopathology 65: 1254-1259, 1975. Go to original source...
    42. Peterson, C.A., Emanuel, M.E., Humphreys, G.: Pathway of movement of apoplastic fluorescent dye tracers through the endodermis at the site of secondary root formation in corn (Zea mays) and broad bean (Vicia faba). - Can. J. Bot. 59: 618-625, 1981a. Go to original source...
    43. Peterson, C.A., Emanuel, M.E., Weerdenburg, C.A.: The permeability of phi thickenings in apple (Pyrus malus) and geranium (Pelargonium hortorum) roots to an apoplastic fluorescent dye tracer. - Can. J. Bot. 59: 1107-1110, 1981b. Go to original source...
    44. Peterson, C.A., Murrmann, M., Steudle, E.: Location of the major barriers to water and ion movement in young roots of Zea mays L. - Planta 190: 127-136, 1993. Go to original source...
    45. Peterson, C.A., Perumalla, C.J.: A survey of angiosperm species to detect hypodermal Casparian bands. II. Roots with a multiseriate hypodermis or epidermis. - Bot. J. Linn. Soc. 103: 113-125, 1990. Go to original source...
    46. Peterson, C.A., Peterson R., Robards A.: A correlated histochemical and ultrastructural study of the epidermis and hypodermis of onion roots. - Protoplasma 96: 1-21, 1978. Go to original source...
    47. Ranathunge, K., Kotula, L., Steudle, E., Lafitte, R.: Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores. - J. exp. Bot. 55: 433-447, 2004. Go to original source...
    48. Ranathunge, K., Schreiber, L.: Water and solute permeabilities of Arabidopsis roots in relation to the amount and composition of aliphatic suberin. - J. exp. Bot. 62: 1961-1974, 2011.
    49. Ranathunge, K., Steudle, E., Lafitte, R.: Control of water uptake by rice (Oryza sativa L.): role of the outer part of the root. - Planta 217: 193-205, 2003.
    50. Ranathunge, K., Steudle, E., Lafitte, R.: Blockage of apoplastic bypass-flow of water in rice roots by insoluble salt precipitates analogous to a Pfeffer cell. - Plant Cell Environ. 28: 121-133, 2005a. Go to original source...
    51. Ranathunge, K., Steudle, E., Lafitte, R.: A new precipitation technique provides evidence for the permeability of Casparian bands to ions in young roots of corn (Zea mays L.) and rice (Oryza sativa L.). - Plant Cell Environ. 28: 1450-1462, 2005b. Go to original source...
    52. Redjala, T., Zelko, I., Sterckeman, T., Legué, V., Lux, A.: Relationship between root structure and root cadmium uptake in maize. - Environ. exp. Bot. 71: 241-248, 2011. Go to original source...
    53. Severina, I.I., Muntyan, M.S., Lewis, K., Skulachev, V.P.: Transfer of cationic antibacterial agents berberine, palmatine, and benzalkonium through bimolecular planar phospholipid film and Staphylococcus aureus membrane. - IUBMB Life 52: 321-324, 2001. Go to original source...
    54. Shiono, K., Ogawa, S., Yamazaki, S., Isoda, H., Fujimura, T., Nakazono, M., Colmer, T.D.: Contrasting dynamics of radial O2-loss barrier induction and aerenchyma formation in rice roots of two lengths. - Ann. Bot. 107: 89-99, 2011. Go to original source...
    55. Shiono, K., Yamauchi, T., Yamazaki, S., Mohanty, B., Malik, A.I., Nagamura, Y., Nishizawa, N.K., Tsutsumi, N., Colmer, T.D., Nakazono, M.: Microarray analysis of lasermicrodissected tissues indicates the biosynthesis of suberin in the outer part of roots during formation of a barrier to radial oxygen loss in rice (Oryza sativa). - J. exp. Bot.: 65: 4795-4806, 2014. Go to original source...
    56. Sivaguru, M., Horst, W.J., Eticha, D., Matsumoto, H.: Aluminum inhibits apoplastic flow of high-molecular weight solutes in root apices of Zea mays L. - J. Plant Nutr. Soil Sci. 169: 679-690, 2006. Go to original source...
    57. Skinner, R., Radin, J.: The effect of phosphorus nutrition on water flow through the apoplastic bypass in cotton roots. - J. exp. Bot. 45: 423-428, 1994. Go to original source...
    58. Soukup, A.: Selected simple methods of plant cell wall histochemistry and staining for light microscopy. - In Žárský V., Cvrčková F. (ed.): Plant Cell Morphogenesis. Methods and Protocols. Pp. 25-40. Springer, Berlin - Heidelberg - New York 2014.
    59. Soukup, A., Armstrong, W., Schreiber, L., Franke, R., Votrubova, O.: Apoplastic barriers to radial oxygen loss and solute penetration: a chemical and functional comparison of the exodermis of two wetland species, Phragmites australis and Glyceria maxima. - New Phytol. 173: 264-278, 2007. Go to original source...
    60. Soukup, A., Votrubová, O., Čížková, H.: Development of anatomical structure of roots of Phragmites australis. - New Phytol. 153: 277-287, 2002. Go to original source...
    61. Strugger, S.: [The analysis of transpiration stream in parenchyma by luminescence microscopy. II. The properties of berberinsulfates and their storage by living cells.] - Biol. Zentralbl. 59: 274-288, 1939. [In German]
    62. Varney, G., McCully, M., Canny, M.: Sites of entry of water into the symplast of maize roots. - New Phytol. 125: 733-741, 1993. Go to original source...
    63. Wegner, L.H.: Root pressure and beyond: energetically uphill water transport into xylem vessels? - J. exp. Bot. 65: 381-393, 2014. Go to original source...
    64. Wilson, C., Peterson, C.: Chemical composition of the epidermal, hypodermal, endodermal and intervening cortical cell walls of various plant roots. - Ann. Bot. 51: 759-769, 1983. Go to original source...
    65. Zimmermann, H.M., Steudle, E.: Apoplastic transport across young maize roots: effect of the exodermis. - Planta 206: 7-19, 1998. Go to original source...

    Return to the content