Effects of Long-Term, Free-Air Ozone Fumigation on the Cytokinin Content of Mature Beech Trees

Abstract

We present the results of a study of the effects of chronic exposure to elevated ozone on the cytokinins of mature beech trees. Methods for analysing the cytokinin (CK) content of beech (Fagus sylvatica) were developed using seven enzyme-linked immunosorbent assays (ELISAs). Samples taken during 2003 and 2004 from 10 mature beech trees in Kranzberg forest, 5 trees exposed to twice ambient ozone (2 × O₃) by free-air fumigation and 5 control trees (1 × O₃), were analysed. In 2003 and 2004 the cytokinin content of leaf samples followed a similar seasonal pattern. In leaf samples, the content of aromatic types was equal to that of the isoprenoid types. In root samples, the level of aromatic types was no different from leaves, but that of the isoprenoid types was much higher. Leaf and phloem cytokinin contents for 2 × O₃ trees were lower than for 1 × O₃ at almost all sampling times. The effect of ozone was greater for leaves in the sun crown than for leaves in the shade crown. By contrast, the root and xylem contents of cytokinin for 2 × O₃ trees were greatly elevated over the values for 1 × O₃ trees early in the growing season. We propose that O₃-associated CK destruction in leaves reduces CK-mediated root growth suppression. The resulting increases in root growth and ectomycorrhiza, reported by other groups in the Kranzberg forest project, are likely to be responsible for the increased CK export in xylem, although O₃-associated CK destruction in the leaves appears to nullify this increase.

Cytokinin - ozone - Fagus sylvatica - shoot-to-root signalling

References

• 1 Andersen C. P., Wilson R., Plocher M., Hogsett W. E.. Carry-over effects of ozone on root growth and carbohydrate concentrations of ponderosa pine seedlings.  Tree Physiology. (1997);  17 805-811
• 2 Aloni R., Langhans M., Aloni E., Dreieicher E., Ullrich C. I.. Root synthesised cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream.  Journal of Experimental Botany. (2005);  56 1535-1544
• 3 Baier M., Kandlbinder A., Golldack D., Dietz K.-J.. Oxidative stress and ozone: perception, signalling and response.  Plant, Cell and Environment. (2005);  28 1012-1020
• 4 Biswal B., Biswal U. C.. Leaf senescence: physiology and molecular biology.  Current Science. (1999);  77 775-782
• 5 Coleman M. D., Dickson R. E., Isebrands J. G., Karnosky D. F.. Root growth and physiology of potted and field-grown trembling aspen exposed to tropospheric ozone.  Tree Physiology. (1996);  16 145-152
• 6 Collier M. D., Huitson S., Hanke D. E.. Altering N nutrition changes the cytokinin content of leaves of woody plants.  Phyton. (2000);  40 13-16
• 7 Collier M. D., Sheppard L. J., Crossley A., Hanke D. E.. Needle cytokinin content as a sensitive bioindicator of N pollution in Sitka spruce.  Plant, Cell and Environment. (2003 a);  26 1929-1939
• 8 Collier M. D., Fotelli M. N., Nahm M., Kopriva S., Rennenberg H., Hanke D. E., Gessler A.. Regulation of nitrogen uptake by Fagus sylvatica on a whole plant level - interactions between cytokinins and soluble N compounds.  Plant, Cell and Environment. (2003 b);  26 1549-1560
• 9 Dent R. M., Hanke D. E.. The effects of pollution on the cytokinin content of Norway spruce needles. Kraigher, H., Batic, F., Hanke, D. E., Agerer, R., and Grill, D., eds. Bioindication of Forest Site Pollution. Ljubljana, Slovenia; Forestry Institute of Slovenia (1995): 89-93
• 10 Fusseder A., Zeigler A.. Metabolism and compartmentation of dihydrozeatin exogenously supplied to suspension cultures of Chenopodium rubrum.  Planta. (1998);  173 104-109
• 11 Gessler A., Schneider S., Weber D., Heneman U., Rennenberg H.. Soluble N compounds in trees exposed to high loads of N: a comparison between the roots of Norway spruce and beech.  New Phytologist. (1998);  138 385-399
• 12 Grayling A., Hanke D. E.. Cytokinins in exudates from leaves and roots of Perilla.  Phytochemistry. (1992);  31 1863-1868
• 13 Grebenc T., Kraigher H.. Changes in the community of ectomycorrhizal fungi and increased fine root number under adult beech trees chronically fumigated with double ambient ozone concentration.  Plant Biology. (2007);  9 279-287
• 14 Haberer K., Grebenc T., Alexou M., Gessler A., Kraigher H., Rennenberg H.. Effects of long-term free-air ozone fumigation on δ¹⁵N and total N in Fagus sylvatica and associated mycorrhizal fungi.  Plant Biology. (2007);  9 242-252
• 15 Holub J., Hanus J., Hanke D. E., Strnad M.. Biological activity of cytokinins derived from ortho- and meta-hydroxybenzyladenine.  Journal of Plant Growth Regulation. (1998);  26 109-115
• 16 Horgan J. M., Wareing P. F.. Cytokinins and the growth responses of seedlings of Betula perdula Roth. and Acer pseudoplatanus L. to nitrogen and phosphorus deficiency.  Journal of Experimental Botany. (1980);  31 525-532
• 32 Jones L. H., Martinkova H., Strnad M., Hanke D. E.. Occurrence of aromatic cytokinins in oil palm (Elaeis guineensis Jacq.).  Journal of Plant Growth Regulation. (1996);  15 39-49
• 17 Kraigher H., Strnad M., Hanke D. E., Batic F.. Cytokiningehalte von Fichtennadeln (Picea abies [L.] Karst) nach Inokulation mit zwei Stämmen des Mykorrhizapilzes Thelephora terrestris (Ehrh.) Fr.  Forstwissenschaftliches Centralblatt. (1993);  112 107-111
• 18 Kraigher H., Hanke D. E.. Cytokinins in Norway spruce seedlings and forest soil pollution.  Phyton. (1996);  36 57-60
• 19 Leitch I. J.. Studies on the bean gall induced by Pontania proxima Lep. on Salix triandra L. PhD Thesis, University of Bristol, UK. (1990)
• 20 Letham D. S., Palni L. M. S.. The biosynthesis and metabolism of cytokinins.  Annual Review of Plant Physiology. (1983);  34 163-197
• 22 Palmer M. V., Horgan R., Wareing P. F.. Cytokinin metabolism in Phaseolus vulgaris L. I. variations in cytokinin levels in leaves of decapitated plants in relation to lateral bud outgrowth.  Journal of Experimantal Botany. (1981);  32 1231-1241
• 23 Rayahu Y. S., Walch-Lui P., Neumann G., Romheld V., von Wiren N., Bangerth F.. Root derived cytokinins as long distance signals for NO₃ ^--induced stimulation of leaf growth.  Journal of Experimental Botany. (2005);  56 1143-1152
• 24 Riefler M., Novak O., Strnad M., Schmülling T.. Arabidopsis cytokinin mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism.  Plant Cell. (2006);  18 40-54
• 25 Scholander P. F., Hammel T., Bradstreet E. D.. Sap pressure in vascular plants.  Science. (1965);  148 339-345
• 26 Stenlid G.. Cytokinins as inhibitors of root growth.  Physiologia Plantarum. (1982);  56 500-506
• 27 Strnad M., Hanus J., Vanek T., Kamínek M., Ballantine J. A., Fussell B., Hanke D. E.. meta-Topolin, a highly active aromatic cytokinin from poplar leaves (Populus × Canadensis Moench., cv Robusta).  Phytochemistry. (1997);  45 213-218
• 28 van Staden J.. Seasonal changes in the cytokinin content of Gingko biloba leaves.  Physiologia Plantarum. (1976);  38 1-5
• 29 van Staden J., Davey J. E.. The synthesis, transport, and metabolism of endogenous cytokinins.  Plant, Cell and Environment. (1979);  2 93-106
• 30 von Schwartzenberg K., Hahn H.. The cytokinin content in needles of Norway spruce (Picea abies [L]. Karst) with different degrees of damage.  Journal of Plant Physiology. (1991);  139 218-223
• 31 Werner H., Fabian P.. Free-air fumigation of mature trees: a novel system for controlled ozone enrichment in grown-up beech and spruce canopies.  Environmental Science and Pollution. (2002);  9 117-121

Guest Editor: R. Matyssek