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Licensed Unlicensed Requires Authentication Published by De Gruyter December 4, 2006

Influence of overexpression of a gibberellin 20-oxidase gene on the kinetics of xylem cell development in hybrid poplar (Populus tremula L. and P. tremuloides Michx.)

  • Oliver Dünisch , Matthias Fladung , Satoshi Nakaba , Yoko Watanabe and Ryo Funada
From the journal Holzforschung

Abstract

Gibberellins (GAs) are important regulators of shoot growth in trees. We studied the kinetics of xylem formation in hybrid poplar (Populus tremula L.×P. tremuloides Michx.) in which the key regulatory gene gibberellin acid 20 oxidase (GA20-oxidase) isolated from Arabidopsis is overexpressed. Increments in the height and radius of shoots were registered by high-resolution laser measurements. The anatomical and chemical structure of mature xylem cells was studied by light electron microscopy and UV spectrophotometry. Transgenic plants showed an increase in height growth, but a lower speed of cell elongation during primary growth compared to wild-type plants. During the first year of growth, transgenic plants showed a higher radius increment, an increase in the period of cell expansion of vessels and fibres and their final size, and a higher lignin content of the compound middle lamella between fibres compared to wild-type plants. In contrast, during the third year of growth, only a slight increase in the period of cell expansion of fibre cells was observed in transgenic compared to wild-type plants. Analyses of GA20-oxidase expression in leaves and shoots of 6-month- and 3-year-old plants of three different independent transgenic lines revealed a decrease in its expression only in shoots but not in leaves of the 3-year-old plants. The results indicate that overexpression of the GA20-oxidase gene in young shoots of transgenic poplar predominately affects cell expansion, while no GA20-oxidase expression was observed in shoots of 3-year-old transgenic plants, resulting in wild-type xylem cell development.

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Corresponding author. Institute for Wood Biology and Wood Preservation, Federal Research Centre for Forestry and Forest Products, Leuschnerstr. 91, D-21031 Hamburg, Germany Phone: +49-40-73962460

References

Barnett, J.R. (1992) Reactivation of the cambium in Aesculus hippocastanum L.: A transmission electron microscope study. Ann. Bot.70:169–177.Search in Google Scholar

Biemelt, S., Tschiersch H., Sonnewald, U. (2004) Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol.135:254–265.10.1104/pp.103.036988Search in Google Scholar PubMed PubMed Central

Caño-Delgado, A.I., Metzlaff, K., Bevan, M. (2000) The eli1 mutation reveals a link between cell expansion and secondary wall formation in Arabidopsis thaliana. Development127:3395–3405.10.1242/dev.127.15.3395Search in Google Scholar PubMed

Caño-Delgado, A.I., Penfield, S, Smith, C., Catley M., Bevan, M. (2003) Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana. Plant J.34:351–362.10.1046/j.1365-313X.2003.01729.xSearch in Google Scholar PubMed

Catesson, A.M. (1989) Specific characters of vessel primary walls during early stages of wood differentiation. Biol. Cell67:221–226.10.1111/j.1768-322X.1989.tb00865.xSearch in Google Scholar

Catesson, A.M. (1994) Cambial ultrastructure and biochemistry: Changes in relation to vascular tissue differentiation and the seasonal cycle. Int. J. Plant Sci.155:251–261.10.1086/297165Search in Google Scholar

Cheliak, W.M., Rogers, D.L. (1990) Integrating biotechnology into tree improvement program. Can. J. For. Res.20:452–463.10.1139/x90-062Search in Google Scholar

Confalonieri, M., Balestrazzi, A., Bisoffi, S., Carbonera, D. (2003) In vitro culture and genetic engineering of Populus spp.: Synergy for forest tree improvement. Plant Cell Tissue Organ Culture72:109–138.10.1023/A:1022265504775Search in Google Scholar

Dodd, R.S., Fox, P. (1990) Kinetics of tracheid differentiation in Douglas fir. Ann. Bot.65:649–657.10.1093/oxfordjournals.aob.a087983Search in Google Scholar

Down, R.E., Ford, L, Bedford, S.J., Gatehouse, L.N., Newell, C., Gatehouse, J.-R., Gatehouse, A.M.R. (2001) Influence of plant development and environment on transgene expression in potato and consequences for insect resistance. Transgenic Res.10:223–236.10.1023/A:1016612912999Search in Google Scholar

Doyle, J.J., Doyle, J.L. (1987) A rapid DNA isolation procedure from small quantities of fresh leaf tissues. Phytochem. Bull.19:11–15.Search in Google Scholar

Dünisch, O., Bauch, J. (1994) Influence of soil substrate and drought on wood formation of spruce (Picea abies [L.] Karst.) under controlled conditions. Holzforschung48:447–457.Search in Google Scholar

Dünisch, O., Rühmann, O. (2005) Kinetics of cell formation and growth stresses in the secondary xylem of Swietenia mahagoni (L.) Jacq. and Khaya ivorensis A. Chev. (Meliaceae). Wood Sci. Technol.40:49–62.Search in Google Scholar

Dünisch, O., Bauch, J., Müller, M., Greis, O. (1998) Subcellular quantitative determination of K and Ca in phloem, cambium and xylem cells of spruce (Picea abies [L.] Karst.) at the time of earlywood and latewood formation. Holzforschung52:582–588.Search in Google Scholar

Dünisch, O., Schulte, M, Kruse, K. (2003) Cambial growth of Swietenia macrophylla King studied under controlled conditions by high resolution laser measurements. Holzforschung57:196–206.10.1515/HF.2003.029Search in Google Scholar

Eriksson, M.E., Moritz, T. (2002) Daylength and spatial expression of a gibberellin 20-oxidase isolated from hybrid aspen (Populus tremula L.×P. tremuloides Michx.). Planta214:920–930.10.1007/s00425-001-0703-3Search in Google Scholar PubMed

Eriksson, M.E., Israelsson, M., Olsson, O., Moritz, T. (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat. Biotechnol.18:784–788.10.1038/77355Search in Google Scholar PubMed

Farrar, J.J., Evert, R.F. (1997a) Seasonal changes in the ultra-structure of the vascular cambium of Robinia pseudoacacia. Trees11:191–202.10.1007/PL00009667Search in Google Scholar

Farrar, J.J., Evert, R.F. (1997b) Ultrastructure of cell division in fusiform cells of the vascular cambium of Robinia pseudoacacia. Trees11:203–215.10.1007/PL00009668Search in Google Scholar

Fladung, M., Ahuja, M.R. (1995) “Sandwich” method for non-radioactive hybridizations. Biotechniques18:3–5.Search in Google Scholar

Fladung, M., Muhs, H.J., Ahuja, M.R. (1996) Morphological changes observed in transgenic Populus carrying the rolC gene from Agrobacterium rhizogenes. Silvae Genet.45:349–354.Search in Google Scholar

Fladung, M., Kumar, S., Ahuja, M.R. (1997) Genetic transformation of Populus genotypes with different chimeric gene constructs: Transformation efficiency and molecular analysis. Transgenic Res.6:111–121.10.1023/A:1018421620040Search in Google Scholar

Israelsson, M., Eriksson, M.E., Hertzberg, M., Aspeborg, H., Nilsson, P., Moritz, T. (2003) Changes in gene expression in the wood-forming tissue of transgenic hybrid aspen with increased secondary growth. Plant Mol. Biol.52:893–903.10.1023/A:1025097410445Search in Google Scholar

Israelsson, M., Sundberg, B., Moritz, T. (2005) Tissue-specific localization of gibberellins and expression of gibberellin-biosynthetic and signalling genes in wood-forming tissues in aspen. Plant J.44:494–504.10.1111/j.1365-313X.2005.02547.xSearch in Google Scholar PubMed

Kitin, P., Sano, Y., Funada, R. (2003) Three-dimensional imaging and analysis of differentiating secondary xylem by confocal microscopy. IAWA J.24:211–222.10.1163/22941932-90001590Search in Google Scholar

Koch, G., Kleist, G. (2001) Application of scanning UV micro-spectrophotometry to localise lignins and phenolic extractives in plant cell walls. Holzforschung55:563–567.10.1515/HF.2001.091Search in Google Scholar

Kohli A., Griffiths, S., Palacios, N., Twyman, R.M., Vain, P., Laurie, D.A., Christou, P. (1999) Molecular characterization of transforming plasmid rearrangements in transgenic rice reveals a recombination hotspot in the CaMV 35S promoter and confirms the predominance of microhomology mediated recombination. Plant J.17:591–601.10.1046/j.1365-313X.1999.00399.xSearch in Google Scholar

Koncz, C., Martini, N., Szabados, L., Hrouda, M., Bachmair, A., Schell, J. (1994) Specialized vectors for gene tagging and expression studies. In: Plant Molecular Biology Manual, Vol. B2. Eds. Gelvin, S., Schilperoort, B. Kluwer Academic, Dordrecht. pp. 1–22.10.1007/978-94-011-0511-8_4Search in Google Scholar

Langer, K., Ache, P., Geiger, D., Stinzing, A., Arend, M., Wind, S., Regan, S., Fromm, J., Hedrich, R. (2002) Poplar potassium transporters capable of controlling K+ homeostasis and K+-dependent xylogenesis. Plant J.32:997–1009.10.1046/j.1365-313X.2002.01487.xSearch in Google Scholar

Larson, P.R. (1969) Wood formation and the concept of wood quality. Bulletin No. 74. School of Forestry, Yale University.Search in Google Scholar

Little, C.H.A., Savidge R.A. (1987) The role of plant growth regulators in forest tree cambial growth. Plant Growth Regulation6:137–170.10.1007/BF00043953Search in Google Scholar

Logemann, J., Schell, J., Willmitzer, L. (1987) Improved method for the isolation of RNA from plant tissues. Ann. Biochem.163:16–20.10.1016/0003-2697(87)90086-8Search in Google Scholar

Mellerowicz, E.J., Baucher, M., Sundberg, B., Boerjan, W. (2001) Unravelling cell wall formation in the woody dicot stem. Plant Mol. Biol.47:239–274.10.1023/A:1010699919325Search in Google Scholar

Mitscherlich, G., Moll, W., Künstle, E., Maurer, P. (1966) Ertragskundlich-ökologische Untersuchungen im Rein- und Mischbestand. VI. Zuwachsbeginn und -ende, Stärkenänderung und jährlicher Durchmesserzuwachs. Allg. For. Jagdzeitung137:72–91.Search in Google Scholar

Nilsson O., Little, C.H.A., Sandberg, G., Olsson, O. (1996) Expression of two heterologous promoters, Agrobacterium rhizogenes rolC and cauliflower mosaic virus 35S, in the stem of transgenic hybrid aspen plants during the annual cycle of growth and dormancy. Plant Mol. Biol.31:887–895.10.1007/BF00019475Search in Google Scholar

Porsch, P. (1995) Transformation von Solanum tuberosum mit mikrobiellen Genen zur Beeinflussung des CO2-Stoffwechsels. Ph.D. Thesis. University of Cologne.Search in Google Scholar

Sambrook, J., Fritsch, E.F., Maniatis, T. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbour Laboratory Press, New York, 1989.Search in Google Scholar

Smouni, A., Laplaze, L., Bogusz, D., Guermache, F., Auguy, F., Duhoux, E., Franche, C. (2002) The 35S promoter is not constitutively expressed in the transgenic tropical actinorhizal tree Casuarina glauca. Funct. Plant Biol.29:649–656.10.1071/PP01121Search in Google Scholar

Spurr, A.R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. L. Ultrastruct. Res.26:31–43.10.1016/S0022-5320(69)90033-1Search in Google Scholar

Sundberg, B., Uggla, C., Tuominen, H. (2000) Cambial growth and auxin gradients. In: Cell and Molecular Biology of Wood formation. Eds. Savidge, R.A., Barnett, J.R., Napier, R. BIOS Scientific Publishers, Oxford. pp. 160–188.Search in Google Scholar

Takabe, K., Miyauchi, S., Tsunoda, R., Fukazawa, K. (1992) Distribution of guiacyl and syringyl lignins in Japanese beech (Fagus crenata): Variation within an annual ring. IAWA Bull.13:105–112.10.1163/22941932-90000561Search in Google Scholar

van Leeuwen, W., Ruttink, T., Borst-Vrenssen, A.W.M., van der Plas, L.H.W., van der Krol, A.R. (2001) Characterization of position-induced spatial and temporal regulation of transgene promoter activity in plants. J. Exp. Bot.52:949–959.10.1093/jexbot/52.358.949Search in Google Scholar PubMed

Wareing, F.B. (1958) Interaction between indole-acetic acid and gibberellic acid in cambial activity. Nature181:1744–1745.10.1038/1811744a0Search in Google Scholar PubMed

Watanabe, Y., Kojima, Y., Ona, T., Asada, T., Sano, Y., Fukazawa, K., Funada, R. (2004) Histochemical study on heterogeneity of lignin in Eucalyptus species II. The distribution of lignins and polyphenols in the walls of various cell types. IAWA J.25:283–295.Search in Google Scholar

Watanabe, Y., Sano, Y., Asada, T., Funada, R. (2006) Histochemical study of the chemical composition of vestured pits in two species of Eucalyptus. IAWA J.27:33–43.10.1163/22941932-90000135Search in Google Scholar

Wodzicki, T.J., Wodzicki, A.B. (1973) Auxin stimulation of cambial activity in Pinus sylvestris L. II. Dependence on basipedal transport. Physiol. Plant.29:288–292.Search in Google Scholar

Yang, S.H., Loopstra, C.A. (2005) Seasonal variation in gene expression for loblolly pines (Pinus taeda) from different geographical regions. Tree Physiol.25:1063–1073.10.1093/treephys/25.8.1063Search in Google Scholar PubMed

Published Online: 2006-12-04
Published in Print: 2006-11-01

©2006 by Walter de Gruyter Berlin New York

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