Abstract
Uptake and xylem loading of organic sulfur and nitrogen were analyzed in detached mycorrhizal (Laccaria laccata L.) roots of pedunculate oak (Quercus robur L.) seedlings using radiolabeled reduced glutathione (GSH) and glutamine (Gln) for transport analyses. The experiments showed for the first time that GSH is taken up by plant roots from the nutrient solution and is partially allocated to the shoot. Apparently, GSH produced during mineralization processes in the soil can be used by plant roots as a sulfur source. GSH uptake into the roots showed biphasic kinetics within the concentration range studied (0–500 μM) with maximum transport velocities (v max) and substrate affinities (K m) that were similar to the kinetics of Gln uptake. GSH uptake kinetics were also in the same range as previously reported for sulfate uptake by mycorrhizal roots of pedunculate oak. It may therefore be assumed that GSH and sulfate uptake can be of comparable significance for sulfur nutrition, provided both sulfur sources are available at similar concentrations at the sites of uptake. Xylem loading of GSH and Gln showed monophasic transport kinetics with v max significantly lower than observed for the two respective uptake systems and, as indicated by the K m-values, a substrate affinity between the high and the low affinity uptake systems. The possible nature of the transport systems for GSH and Gln is discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abuzinadah RA and Read DJ 1989 The role of proteins in the nitrigen nutrition of ectomycorrhizal plants IV. The utilization of peptides in birch (Betula pendula L.) infected with different ectomycorrhizal fungi. New Phytol. 112, 55–60.
Bajwa R and Read DJ 1985 The biology of mycorrhizae in the Ericaceae. IX. Peptides as nitrogen sources for the ericoid endophyte and for mycorrhizal and non-mycorrhizal plants. New Phytol 101, 459–467.
Bergmann L and Rennenberg H 1993 Glutathione metabolism in plants. In Sulfur Nutrition and sulfur Assimilation in Higher Plants. Eds. LJ de Kok, I Stulen, H Rennenberg and C Brunold, W Rauser. pp 109–123. SPB Acad Publ, The Hague.
Chalot M and Brun A 1998 Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol Rev 22, 21–44.
Dengler A and Röhrig E 1980 Waldbau auf ökologischer Grundlage. Erster Band: Der Wald als Vegetationstyp und seine Bedeutung für den Menschen. Verlag Paul Parey, Hamburg.
Ellenberg H 1986 Vegetation Mitteleuropas mit den Alpen. Verlag Eugen Ulmer, Stuttgart.
Epron D, Dreyer E and Breda N 1992 Photosynthesis of oak trees (Quercus petraea (Matt.) Lieb.) during drought under field conditions: diurnal course of net COxx2 assimilation and photochemical efficiency of photosystem II. Plant Cell Environ. 15, 809–820.
Foyer CH and Rennenberg H 2000 Regulation of glutathione synthesis and its role in abiotic and biotic stress defense. In Sulfur Nutrition and Sulfur Assimilation in Higher Plants: molecular, biochemical and physiological aspects. Eds. C Brunold, H Rennenberg, LJ De Kok, I Stulen I and JC Davidian. pp 127–153.
Paul Haupt, Bern, Switzerland. Geßler A, Schneider S, von Sengbusch D, Weber P, Hanemann U, Huber C, Rothe A, Kreutzer K and Rennenberg H 1998a Field and laboratory experiments on net uptake of nitrate and ammonium by roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytol. 138, 275–285.
Geßler A, Schneider S, Weber P, Hanemann U and Rennenberg H 1998b Soluble N compounds in trees exposed to high loads of N: a comparison between the roots of Norway spruce (Picea abies (L.) Karst) and beech (Fagus sylvatica) trees grown under field conditions. New Phytol. 138, 385–399.
Hanes CS 1932 Studies of plant analyses. I. The effect of starch concentration upon the velocity of hydrolysis by amylase of germinated barley. Biochem. J. 26, 1406–1421.
Herschbach C and Rennenberg H 1991 Influence of glutathione (GSH) on sulfate influx, xylem loading, and exudation in excised tobacco roots. J. Exp. Bot. 42, 1021–1029.
Herschbach C and Rennenberg H 1997 Sulfur nutrition of conifers and deciduous trees. In Trees-Contributions to Modern Tree Physiology. Eds. H Rennenberg, W Eschrich and H Ziegler. pp 293–311. Backhuys, Leiden, The Netherlands.
Herschbach C and Rennenberg H 2001 Sulfur nutrition of deciduous trees. Naturwissenschaften 88, 25–36.
Herschbach C, van der Zalm E, Schneider A, Jouanin L, De Kok L and Rennenberg H 2000 Regulation of sulphur nutrition in wildtype and transgenic poplar overexpressing γ-glutamylcysteine synthetase in the cytosol as affected by atmospheric Hxx2S. Plant Physiol. 124, 461–473.
Kielland K 1994 Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75, 2373–2383.
Kreuzwieser J and Rennenberg H 1998 Sulphate uptake and xylem loading of mycorrhizal beech roots. New Phytol. 140, 319–329.
Kreuzwieser J, Herschbach C, Stulen I, Wiersema P, Vaalburg W and Rennenberg H 1997 Interactions of ammonium with nitrate transport processes of non-mycorrhizal beech (Fagus sylvatica L.) roots. J. Exp. Bot. 48, 1431–1438.
Kreuzwieser J, Stulen I, Wiersema P, Vaalburg W and Rennenberg H 2000 Nitrate transport processes in Fagus-Laccaria-Mycorrhizae. Plant Soil 220, 107–117.
Lineweaver H and Burk D 1934 The determination of enzyme dissociation constants. J. Am. Chem. Soc. 56, 658–666
Lipson D and Näsholm T 2001 The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128, 305–316.
Miettinen KJ 1959 Assimilation of amino acids in higher plants. In Symposium of the Society of Experimental Biology 13. pp 210–230. Academic Press, New York.
Miyake T, Hazu T, Yoshida S, Kanayama M, Tomochika K, Shinoda S and Ono B 1998 Glutathione transport systems of the budding yeast Saccharomyces cerevisiae. Biosci Biotechnol Biochem 62, 1858–1864.
Moser M 1958a Die künstliche Mykorrhizaimpfung an Forstpflanzen. Forstwiss. Cbl. 77, 32–40.
Moser M 1958b Die künstliche Mykorrhizaimpfung an Forstpflanzen. II. Die Torfstreukultur von Mykorrhizaspilzen. Forstwiss. Cbl. 77, 273–278.
Murashige T and Skoog F 1962 A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol. Plant 15, 473–497.
Nehls U, Kleber R, Wiese J and Hampp R 1999 Isolation and characterization of a general amino acid permease from the ectomycorrhizal fungus Amanita muscaria. New Phytol. 144, 343–349.
Rennenberg H 1999 The significance of ectomycorrhizal fungi for sulfur nutrition of trees. Plant Soil 215, 115–122.
Rennenberg H 2001 Glutathione-an ancient metabolite with modern tasks. In Significance of Glutathione in Plant Adaptation to the Environment. Eds. D Grill, M Tausz and LJ de Kok. pp 1–11. Kluwer, Dordrecht.
Rennenberg H, Schneider S and Weber P 1996 Analysis of uptake and allocation of nitrogen and sulphur by trees in the field. J. Exp. Bot. 47, 1491–1498.
Schneider A, Martini N and Rennenberg H 1992 Reduced glutathione (GSH) transport into cultured tobacco cells. Plant Physiol. Biochem. 30, 29–38.
Schneider S, Geßler A, Weber P, von Sengbusch D, Hanemann U and Rennenberg H 1996 Soluble nitrogen compounds in trees exposed to high loads of nitrogen: a comparison of spruce (Picea abies L.) and beech (Fagus sylvatica L.) grown under field conditions. New Phytol 134, 103–114.
Seegmüller S 1999 Der Einfluss von Mykorrhizen, atmosphärischem Kohlendioxid und Wassermangel auf das Wachtum und die Schwefel-und Stickstoffversorgung der Stieleiche (Quercus robur L.). Schriftenreihe der Professur für Baumphysiologie, Bd. 8. Dr. Wigbert Maraun, Frankfurt, Germany.
Stribley DP and Read DJ 1980 The biology of mycorrhizae in the Ericaceae: VII. The relationship between mycorrhizal infection and the capacity to utilize simple and complex organic nitrogen sources. New Phytol. 86, 365–371.
Virtanen AI and Linkola H 1946 Organic nitrogen compounds as nitrogen nutrition for higher plants. Nature 157, 515.
Wallenda T and Read DJ 1999 Kinetics of amino acid uptake by ectomycorrhizal roots. Plant Cell Environ 22, 179–187.
Zhao F and McGrath SP 1994 Extractable sulphate and organic sulphur in soils and their availability to plants. Plant Soil 164, 243–250.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Seegmüller, S., Rennenberg, H. Transport of organic sulfur and nitrogen in the roots of young mycorrhizal pedunculate oak trees (Quercus robur L.). Plant and Soil 242, 291–297 (2002). https://doi.org/10.1023/A:1016290324076
Issue Date:
DOI: https://doi.org/10.1023/A:1016290324076