Genetic Engineering of Wood Formation

Expression of bacterial IAA-biosynthetic genes in hybrid aspen (Populus tremula x P. tremuloides)
  • Hannele Tuominen
  • Olof Olsson
  • Björn Sundberg
Part of the Forestry Sciences book series (FOSC, volume 64)


Not many years after its discovery, the plant hormone indole-3-acetic acid (IAA) was demonstrated to activate cambial growth when applied to sunflower hypocotyls (Snow, 1935). In subsequent studies it was shown that IAA is involved in the control of several aspects of secondary growth, in particular the maintenance of the vascular cambium, the production of the secondary xylem, and the regulation of xylem cell morphology (Savidge, 1983; Aloni, 1987; Little and Savidge, 1987; Lachaud, 1989; Little and Pharis, 1995). However, the exact role of IAA in controlling these processes is still controversial.


Secondary Xylem Adventitious Root Formation Cambial Activity Hybrid Aspen Cambial Zone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Ainley, W. M., McNeil, K. J., Hill, J. W., Lingle, W. L., Simpson, R. B., Brenner, M. L., Nagao, R. T. and Key, J. L. (1993) Regulatable endogenous production of cytokinins up to ‘toxic’ levels in transgenic plants and plant tissues. Plant Mol. Biol. 22, 13–23.PubMedGoogle Scholar
  2. Aloni, R. (1980) Role of auxin and sucrose in the differentiation of sieve and tracheary elements in plant tissue cultures. Planta 150, 255–263.Google Scholar
  3. Aloni, R. (1987) Differentiation of vascular tissues. Ann. Rev. Plant Physiol. 38, 179–204.Google Scholar
  4. Aloni, R. and Zimmermann, M. H. (1983) The control of vessel size and density along the plant axis. A new hypothesis. Differentiation 24, 203–208.Google Scholar
  5. Balatinecz, J. J. and Farrar, J. L. (1966) Pattern of renewed cambial activity in relation to exogenous auxin in detached woody shoots. Can. J. Bot. 44, 1108–1110.Google Scholar
  6. Benfey, P. N., Ren, L. and Chua, N.-H. (1989) The CaMV 35S enhancer contains at least two domains which can confer different developmental and tissue-specific expression patterns. EMBO J 8, 2195–2202.PubMedGoogle Scholar
  7. Bennett, M. J., Marchant, A., Green, H. G., May, S. T., Ward, S. P., Millner, P. A., Walker, A. R., Schulz, B. and Feldmann, K. A. (1996). Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273, 948–950.PubMedGoogle Scholar
  8. Blakesley, D. (1994). Auxin metabolism and adventitious root initiation. In Biology of Adventitious Root Formation. (eds. Davis, T. D. and Haissig, B. E.), pp. 143–154. New York: Plenum Press.Google Scholar
  9. Brown, A. B. and Cormack, R. G. H. (1937) Stimulation of cambial activity, locally in the region of application and at a distance in relation to a wound, by means of heteroauxin. Can. J Res. Sect. C 15, 433–441.Google Scholar
  10. Brummel, D. A. and Hall, J. L. (1987) Rapid cellular responses to auxin and the regulation of growth. Plant, Cell Env. 10, 523–543.Google Scholar
  11. Callos, J. D. and Medford, J. 1. (1994) Organ positions and pattern formation in the shoot. Plant J 6, 1–7.Google Scholar
  12. Campbell, M. M. and Sederoff, R. R. (1996) Variation in lignin content and composition. Mechanisms of control and implications for the genetic improvement of plants. Plant Physiol. 110, 3–13.PubMedGoogle Scholar
  13. Catald, C., Ostin, A., Chamarro, J., Sandberg, G. and Crozier, A. (1992). Metabolism of indole-3-acetic acid by pericarp discs from immature and mature tomato (Lycopersicon esculentum Mill.). Plant Physiol. 100, 1457–1463.Google Scholar
  14. Cernak, A., Lincoln, C., Lammer, D. and Estelle, M. (1997). The SARI gene of Arabidopsis acts downstrean of the AXRI gene in auxin response. Development 124, 1583–1591.Google Scholar
  15. Chen, R., Hilson, P., Sedbrook, J., Rosen, E., Caspar, T. and Masson, P. H. (1998). The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc. Natl. Acad. Sci. USA 95, 15112–15117.PubMedGoogle Scholar
  16. Cleland, R. E. (1995) Auxin and cell elongation. In Plant Hormones Physiology, Biochemistry and Molecular Biology. (ed. Davies, P. J. ), pp. 214–227. Dordrecht: Academic Publishers.Google Scholar
  17. Cline, M. G. (1994) The role of hormones in apical dominance. New approaches to an old problem in plant development. Physiol. Plant. 90, 230–237.Google Scholar
  18. DeMaggio, A. E. (1966) Phloem differentiation: induced stimulation by gibberellic acid. Science 152, 370–372.PubMedGoogle Scholar
  19. Benne, M. P. (1972) A comparison of root-and shoot-wood development in conifer seedlings. Ann. Bot. 36, 579–587.Google Scholar
  20. Denne, M. P. and Wilson, J. E. (1977). Some quantitative effects of indoleacetic acid on the wood production and tracheid dimensions of Picea. Planta 134, 223–228.Google Scholar
  21. Digby, J. and Wareing, P. F. (1966). The effect of applied growth hormones on cambial division and the differentiation of the cambial derivatives. Ann. Bot. 30, 539–548.Google Scholar
  22. Dodd, R. S. and Fox, P. (1990). Kinetics of tracheid differentiation in Douglas-fir. Ann. Bot. 65, 649–657.Google Scholar
  23. Holey, D. and Leyton, L. (1968) Effects of growth regulating substances and water potential on the development of secondary xylem in Fraxinus. New Phytol. 67, 579–594.Google Scholar
  24. Edlund, A., Eklöf, S., Sundberg, B., Moritz, T. and Sandberg, G. (1995) A microscale technique for gas chromatography-mass spectrometry measurements of picogram amounts of indole-3-acetic acid in plant tissues. Plant Physiol. 108, 1043–1047.PubMedGoogle Scholar
  25. Eklöf, S. (1996) Auxin-cytokinin interactions in transgenic plants expressing the A. tumefaciens ipt, iaaM and iaaHgenes. Ph.D. thesis. Acta Universitatis Agriculturae Sueciae Silvestria 15, Umed.Google Scholar
  26. Eklöf, S., Astot, C., Blackwell, J., Moritz, T., Olsson, O., and Sandberg, G. (1997) Auxin-cytokinin interactions in wild-type and transgenic tobacco. Plant Cell Physiol. 38, 225–235.Google Scholar
  27. Evans, M. L. (1984) Functions of hormones at the cellular level of organization. In Hormonal regulation of development II. Encyclopedia of Plant Physiology. NS. Vol. 10. (ed. Scott, T. K. ), pp. 23–62. Berlin: Springer Verlag.Google Scholar
  28. Ewers, F. W. and Aloni, R. (1985) Effects of applied auxin and gibberellin on phloem and xylem production in needle leaves of Pinus. Bot. Gaz. 146, 466–471.Google Scholar
  29. Field, R. J. and Peel, A. J. (1971) The metabolism and radial movement of growth regulators and herbicides in willow stems. New Phytol. 70, 743–749.Google Scholar
  30. Fraser, D. A. (1949) Production of spring wood with ß-indole acetic acid (heteroauxin). Nature 164, 542.PubMedGoogle Scholar
  31. Gälweiler, L. Guan, C. H., Muller, A., Wisman, E., Mendgen, K., Yephremov, A. and Palme K. (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue, Science 282, 2226–2230.Google Scholar
  32. Guevara-García, A., Mosqueda-Cano, G., Arguello-Astorga, G., Simpson, J. and Herrera-Estrella, L. (1993) Tissue-specific and wound-inducible pattern of expression of the mannopine synthase promoter is determined by the interaction between positive and negative cis-regulatory elements. Plant J. 4, 495–505.PubMedGoogle Scholar
  33. Guilley, H., Dudley, R. K., Jonand, G., Balazs, E. and Richards, K. E. (1982) Transcription of cauliflower mosaic virus DNA; detection of promoter sequences and characterization of transcripts. Cell 30, 763–773.PubMedGoogle Scholar
  34. Hake, S., Char, B. R., Chuck, G., Foster, T., Long, J. and Jackson, D. (1995). Homeobox genes in the functioning of plant meristems. Philos. Trans. R. Soc. Lond. (B) 350, 45–51.Google Scholar
  35. Hanson, J. B. and Trewavas, A. J. (1982) Regulation of plant cell growth: the changing perpective. New Phytol. 90, 1–18.Google Scholar
  36. Hawkins, S., Samaj, J., Lauvergeat, V., Boudet, A. and Grima-Pettenati, J. (1997) Cinnamyl alcohol dehydrogenase: identification of new sites of promoter activity in transgenic poplar. Plant Physiol. 113, 321–325.PubMedGoogle Scholar
  37. Ilejnowicz, A. and Tomaszewski, M. (1969) Growth regulators and wood formation in Pinus silvestris. Physiol. Plant. 22, 984–992.Google Scholar
  38. Hertel, R. (1995) Auxin binding protein 1 is a red herring. J Exp. Bot. 46, 461–462.Google Scholar
  39. Hohn, T., Richards, K. and Lebeuvier, G. (1982) Cauliflower mosaic virus on its way to becoming a useful plant vector. Curr. Top. Microbiol. Immunol. 96, 194–236.PubMedGoogle Scholar
  40. Holder, N. (1979) Positional information and pattern formation in plant morphogenesis and a mechanism for the involvement of plant hormones. J Theor. Biol. 77, 195–212.PubMedGoogle Scholar
  41. Jefferson, R. A., Kavanagh, T. A. and Bevan, M. W. (1987). GUS fusions: ß-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6, 3901–3907.PubMedGoogle Scholar
  42. Jenkins, P. A. (1974). Influence of applied indoleacetic acid and abscisic acid on xylem cell dimensions in Pinus radiata D. Don. In Mechanisms of regulation of plant growth. (eds. Bieleski, R. L., Ferguson, A. R. and Cresswell, M. M. ), pp. 737–742. Wellington: Wellington Roy. Soc.Google Scholar
  43. Jones, A. M., Im, K-H., Savka, M. A., Wu, M-J., DeWitt, N. G., Shillito, R. and Binns, A. N. (1998) Auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1. Science 282, 1114–1117.PubMedGoogle Scholar
  44. Kakimoto, T. (1996) CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274, 982–985.PubMedGoogle Scholar
  45. Kalev, N. and Aloni, R. (1998) Role of auxin and gibberellin in regenerative differentiation of tracheids in Pinus pinea seedlings. New Phytol. 138, 461–468.Google Scholar
  46. Klee, H. J., Horsch, R. B., Hinchee, M. A., Hein, M. B. and Hoffman, N. L. (1987) The effects of overproduction of two Agrobacterium tumefaciens T-DNA auxin biosynthetic gene products in transgenic petunia plants. Genes Dev. 1, 86–96.Google Scholar
  47. Klee, H. J. and Romano, C. P. (1994). The roles of phytohormones in development as studied in transgenic plants. Crit. Rev. Plant Sci. 13, 311–324.Google Scholar
  48. Klee, H. J. and Lanahan, M. B. (1995) Transgenic plants in hormone biology. In Plant Hormones Physiology, Biochemistry and Molecular Biology. (ed. Davies, P. J. ), pp. 340–353. Dordrecht: Kluwer Academic Publishers.Google Scholar
  49. Kutshera, U. (1994) The current status of the acid-growth hypothesis. New Phytol. 126, 549–569.Google Scholar
  50. Lachaud, S. (1983) Xylogénese chez les Dictoylédones arborescentes. IV. Influence des bourgeons, de l’acide ß-indolylacétique et de l’acide gibberellique sur la réactivation cambial et la xylogénèse dans les jeunes tiges de Hêtre. Can. J Bot. 61, 1768–1774.Google Scholar
  51. Lachaud, S. (1989) Participation of auxin and abscisic acid in the regulation of seasonal variations in cambial activity and xylogenesis. Trees 3, 125–137.Google Scholar
  52. Lachaud, S. and Bonnemain, J. L. (1984) Seasonal variations in the polar transport pathways and retention sites of [3H]indole-3-acetic acid in young branches of Fagus sylvatica L. Planta 161, 207–215.Google Scholar
  53. Langridge, W. H. R., Fitzgerald, K. J., Koncz, C., Schell, J. and Szalay, A. A. (1989) Dual promoter of Agrobacterium tumefaciens mannopine synthase genes is regulated by plant growth hormones. Proc. Natl. Acad. Sci. USA 86, 3219–3223.PubMedGoogle Scholar
  54. Larson, P. R. (1960) A physiological consideration of the springwood summerwood transition in red pine. Forest Sei. 6, 110–122.Google Scholar
  55. Larson, P. R. (1962) Auxin gradients and the regulation of cambial activity. In Tree Growth. (ed. Kozlowski, T. T. ), pp. 97–117. New York: The Ronald Press Company.Google Scholar
  56. Larson, P. R. (1994) The vascular cambium. Berlin: Springer-Verlag.Google Scholar
  57. Lev-Yadun, S. and Aloni, R. (1995) Differentiation of the ray system in woody plants. Bot. Rev. 61, 49–88.Google Scholar
  58. Leyser, H. M. O., Lincoln, C. A., Timpte, C., Lammer, D., Turner, J. and Estelle, M. (1993) Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme El. Nature 364, 161–164.Google Scholar
  59. Little, C. H. A. and Bonga, J. M. (1974) Rest in cambium of Abies balsamea. Can. J Bot. 52, 1723–1730Google Scholar
  60. Little, C. H. A. and Wareing, P. F. (1981) Control of cambial activity and dormancy in Picea sitchensis by indol-3-ylacetic and abscisic acid. Can. J. Bot. 59, 1480–1493.Google Scholar
  61. Little, C. H. A. and Savidge, R. A. (1987) The role of plant growth regulators in forest tree cambial growth. Plant Growth Regul. 6, 137–169.Google Scholar
  62. Little, C. H. A. and Sundberg, B. (1991) Tracheid production in response to indole-3-acetic acid varies with internode age in Pinus sylvestres sterns. Trees 5, 101–106.Google Scholar
  63. Little, C. H. A. and Pharis, R. P. (1995) Hormonal control of radial and longitudinal growth in the tree stem. In Plant Stems: Physiology and Functional Morphology. (ed. Gartner, B. L. ), pp. 281–319. San Diego, CA: Academic Press.Google Scholar
  64. Loopstra, C. A. and Sederoff, R. R. (1995) Xylem-specific gene expression in loblolly pine. Plant Mol. Biol. 27, 277–291.PubMedGoogle Scholar
  65. Luschnig, C., Gaxiola, R. A., Grisafi, P. and Fink, G. R. (1998). EIRI, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12, 2175–2187.Google Scholar
  66. Medford, J. I., Horgan, R., EI-Sawi, Z. and Klee, H. J. (1989) Alterations of endogenous cytokinins in transgenic plants using a chimeric isopentenyl transferase gene. Plant Cell 1, 403–413.PubMedGoogle Scholar
  67. Mittler, R. and Lam, E. (1995) In situ detection of nDNA fragmentation during the differentiation of tracheary elements in higher plants. Plant Physiol. 108, 489–493.PubMedGoogle Scholar
  68. Moritz, T. and Olsen, J. E. (1995) Comparison between high-resolution selected ion monitoring, selected reaction monitoring, and four-sector tandem mass spectrometry in quantitative analysis of gibberellins in milligram amounts of plant tissue. Anal. Chem. 67, 1711–1716.Google Scholar
  69. Morris, D. A. and Thomas, A. G. (1978) A microautoradiographic study of auxin transport in the stem of intact pea seedlings. J. Exp. Bot. 29, 147–157.Google Scholar
  70. Morris, D. A. and Small, D. K. (1990) Auxin transport and the regulation of petiole abscission in cotton (Gossypium hirsutum L.): A comparison of IAA and phenylacetic acid. Plant Growth Regul. 9, 201–214.Google Scholar
  71. Müller, A., Guan, C., Gälweiler, L., Tänzler, P., Huijser, P., Marchant, A., Parry, G., Bennett, M., Wisman, E. and Palme K (1998) AIPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17, 6903–6911.Google Scholar
  72. Nagata, T., Okada, K., Kawazu, T. and Takebe, I. (1987) Cauliflower mosaic virus 35S promoter directs S phase specific expression in plant cells. Mol. Gen. Genet. 207, 242–244.Google Scholar
  73. Napier, R. M. and Venis, M. A. (1995) Auxin action and auxin-binding proteins. New Phytol. 129, 167–201.Google Scholar
  74. Nilsson, O., Aldén, T., Sitbon, F., Little, C. H. A., Chalupa, V., Sandberg, G. and Olsson, O. (1992) Spatialpattern of cauliflower mosaic virus 35S promoter-luciferase expression in transgenic hybrid aspen trees monitored by enzymatic assay and non-destructive imaging. Transgenic Res. 1, 209–220.Google Scholar
  75. Nilsson, O., Little, C. H. A., Sandberg, G. and Olsson, O. (1996) Expression of two heterologous promoters, Agrobacterium rhizogenes roiC 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.PubMedGoogle Scholar
  76. Nilsson, O., Tuominen, H., Sundbrg, B. and Olsson, O. (1997) The Agrobacterium rhizogenes rolB and roiC promoters are expressed in pericycie cells competent to serve as root initials in transgenic hybrid aspen. Physiologia Plantarum 100, 456–462.Google Scholar
  77. Odell, J. T., Nagy, F. and Chua, N-H. (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313, 810–812.PubMedGoogle Scholar
  78. Pharis, R. P., Yeh, F. C. and Dancik, B. P. (1991) Superior growth potential in trees: what is its basis, and can it be tested for at an early age? Can. J For. Res. 21, 368–374.Google Scholar
  79. Pomponi, M., Spanò, L., Sabbadini, M. G. and Costantino, P. (1983) Restriction endonuclease mapping of the root-inducing plasmid of Agrobacterium rhizogenes 1855. Plasmid 10, 119–129.PubMedGoogle Scholar
  80. Regan, S., Bourquin, V., Tuominen, H. and Sundberg, B. (1999) Accurate and high resolution in situ hybridization analysis of gene expression in secondary stern tissues. SubmittedGoogle Scholar
  81. Ribnicky, D. M., Ilic, N., Cohen, J. D. and Cooke, T. J. (1996) The effects of exogenous auxins on endogenous indole-3-acetic acid metabolism. Plant Physiol. 112, 549–558.PubMedGoogle Scholar
  82. Ridoutt, B. G. and Sands, R. (1994) Quantification of the processes of secondary xylem fibre development in Eucalyptus globulus at two height levels. IAWA J 15, 417–424.Google Scholar
  83. Ridoutt, B. G., Pharis, R. P. and Sands, R. (1996) Fibre length and gibberellins Al and A20 are decreased in Eucalyptus globulus by acylcyclohexanedione injected into the stem. Physiol. Plant. 96, 559–566.Google Scholar
  84. Rinne, P., Tuominen, H. and Sundberg, B. (1993) Growth patterns and endogenous indole-3-acetic acid concentrations in current-year coppice shoots and seedlings of two Betula species. Physiol. Plant. 88, 403–412.Google Scholar
  85. Riov, J. and Bangerth, F. (1992) Metabolism of auxin in tomato fruit tissue. Plant Physiol. 100, 1396–1402.PubMedGoogle Scholar
  86. Robards, A. W., Davidson, E. and Kidwai, P. (1969) Short-term effects of some chemicals on cambial activity. J Exp. Bot. 20, 912–920.Google Scholar
  87. Roberts, L. W., Gahan, P. B. and Aloni, R. (1988) Vascular Differentiation and Plant Growth Regulators. Berlin, Heidelberg: Springer Verlag.Google Scholar
  88. Romano, C. P., Hein, M. B. and Klee, H. J. (1991) Inactivation of auxin in tobacco transformed with the indoleacetic acid-lysine synthetase gene of Pseudomonas savastanoi. Genes Dev. 5, 438–446.Google Scholar
  89. Romano, C. P., Cooper, M. L. and Klee, H. J. (1993) Uncoupling auxin and ethylene effects in transgenic tobacco and Arabidopsis plants. Plant Cell 5, 181–189.PubMedGoogle Scholar
  90. Romano, C. P., Robson, P. R. H., Smith, H., Estelle, M. and Klee, H. (1995) Transgene-mediated auxin overproduction in Arabidopsis: hypocotyl elongation phenotype and interactions with the hy6–1 hypocotyl elongation and axr auxin-resistant mutants. Plant Mol. Biol. 27, 1071–1083.PubMedGoogle Scholar
  91. Savidge, R. A. (1983) The role of plant hormones in higher plant cellular differentiation. II. Experiments with the vascular cambium, and sclereid and tracheid differentiation in the pine, Pinus contorta. Histochem. J 15, 447–466.Google Scholar
  92. Savidge, R. A. and Wareing, P. F. (1984) Seasonal cambial activity and xylem development in Pinus contorta in relation to endogenous indol-3-yl-acetic and (S)-abscisic acid levels. Can. J For. Res. 14, 676–682.Google Scholar
  93. Savidge, R. A., Heald, J. K. and Wareing, P. F. (1982) Non-uniform distribution and seasonal variation of endogenous indol-3y1-acetic acid in the cambial region of Pinus contorta Dougl. Planta 155, 89–92.Google Scholar
  94. Schaller, G. E. and Bleecker, A. B. (1995) Ethylene-binding sites generated in yeast expressing the Arabidopsis ETRI gene. Science 270, 1809–1811.PubMedGoogle Scholar
  95. Schröder, G., Waffenschmidt, S., Weiler, E. W. and Schröder, J. (1984) The T-region of Ti plasmids codes for an enzyme synthesizing indole-3-acetic acid. Eur. J. Biochem. 138, 387–391.PubMedGoogle Scholar
  96. Scurfield, G. (1962) Effects of gibberellic acid on woody perennials with special reference to species of Eucalyptus. Forest Sci. 8, 168–179.Google Scholar
  97. Sheldrake, A. R. (1971) Auxin in the cambium and its differentiating derivatives. J. Exp. Bot. 22, 735–740.Google Scholar
  98. Sheriff, D. W. (1983) Control by indole-3-acetic acid of wood production in Pinus radiata D. Don segments in culture. Aust. J Plant Physiol. 10, 131–135.Google Scholar
  99. Sitbon, F., Little, C. H. A., Olsson, O. and Sandberg, G. (1992a). Correlation between the expression of T-DNA IAA biosynthetic genes from developmentally regulated promoters and the distribution of IAA in different organs of transgenic tobacco. Physiol. Plant. 85, 679–688.Google Scholar
  100. Sitbon, F., Hennion, S., Sundberg, B., Little, C. H. A., Olsson, O. and Sandberg, G. (19926). Transgenic tobacco plants coexpressing the Agrobacterium tumefaciens iaaM and iaaH genes display altered growth and indoleacetic acid metabolism. Plant Physiol. 99, 1062–1069.Google Scholar
  101. Sitbon, F., Östin, A., Sundberg, B., Olsson, O. and Sandberg, G. (1993a). Conjugation of indole-3-acetic acid (IAA) in wild-type and IAA-overproducing transgenic tobacco plants, and identification of the main conjugates by frit-fast atom bombardment liquid chromatography-mass spectrometry. Plant Physiol. 101, 313–320.PubMedGoogle Scholar
  102. Sitbon, F., Edlund, A., Gardeström, P., Olsson, O. and Sandberg, G. (1993b). Compartmentation of indole-3acetic acid metabolism in protoplasts isolated from leaves of wild-type and IAA-overproducing transgenic tobacco plants. Planta 191, 274–279.Google Scholar
  103. Sitbon, F., Dargeviciute, A. and Perrot-Rechenmann, C. (1996) Expression of auxin-inducible genes in relation to endogenous indoleacetic acid (IAA) levels in wild-type and IAA-overproducing transgenic tobacco plants. Physiol. Plant. 98, 677–684.Google Scholar
  104. Sitbon, F., Hennion, S., Little, C. H. A. and Sundberg, B. (1999) Enhanced ethylene production and peroxidase activity in IAA-overproducing transgenic tobacco plants is associated with increased lignin content and altered lignin composition. Plant Science 141, 165–173.Google Scholar
  105. Snow, R. (1935) Activation of cambial growth by pure hormones. New Phytol, 34, 347–360.Google Scholar
  106. Spam), L., Pomponi, M., Costantino, P. S., Slogteren, G. M. S. and Tempé, J. (1982) Identification of T-DNA in the root-inducing plasmid of the agropine type Agrobacterium rhizogenes 1855. Plant Mol. Biol. 1, 291–300.Google Scholar
  107. Steeves, T. A. and Sussex, I. M. (1989) Patterns in Plant Development. Cambridge: Cambridge University Press.Google Scholar
  108. Stitt, M. (1995) The use of transgenic plants to study the regulation of plant carbohydrate metabolism. Aust. J. Plant Physiol. 22, 635–646.Google Scholar
  109. Sundberg, B. (1990) Influence of extraction solvent (buffer, methanol, acetone) and time on the quantification of indole-3-acetic acid in plants. Physiol. Plant. 78, 293–297.Google Scholar
  110. Sundberg, B. and Little, C. H. A. (1990) Tracheid production in response to changes in the internal level of indole-3-acetic acid in 1-year-old shoots of Scots pine. Plant Physiol. 94, 1721–1727.PubMedGoogle Scholar
  111. Sundberg, B. and Uggla, C. (1998) Origin and dynamics of indoleacetic acid under polar transport in Pinus sylvestris. Physiologia Plantarum 104, 22–29.Google Scholar
  112. Sundberg, B., Little, C.H.A. and Cui, K. (1990) Distribution of indole-3-acetic acid and the occurrence of its alkali-labile conjugates in the extraxylary region of Pinus sylvestris stems. Plant Physiol. 93, 1295–1302.PubMedGoogle Scholar
  113. Sundberg, B., Tuominen, H. and Little, C. H. A. (1994) Effects of the indole-3-acetic acid (IAA) transport inhibitors N-1-naphthylphthalamic acid and morphactin on endogenous IAA dynamics in relation to compression wood formation in I-year-old Pinus sylvestris (L.) shoots. Plant Physiol. 106, 469–476.PubMedGoogle Scholar
  114. Swan, H. S. D. (1958) The influence of gibberellic acid on the growth and development of hybrid poplar. Woodland Res. Index Pulp Paper Res. Inst. Can. No. 105 Google Scholar
  115. Söding, H. (1940) Weitere Untersuchungen Ober die Wuchsstoffregulation der Kambiumtätigkeit. Zeitschrift fur Botanik 36, 113–141.Google Scholar
  116. Teeri, T. I-I., Lehväslaiho, H., Franck, M., Uotila, J., Heino, P., Palva, E. T., Van Montagu, M. and Herrera-Estella, L. (1989) Gene fusions to lacZ reveal new expression patterns of chimeric genes in transgenic plants. EMBO J. 8, 343–350.PubMedGoogle Scholar
  117. Thomashow, L. S., Reeves, S. and Thomashow, M. F. (1984) Crown gall oncogenesis: Evidence that a T-DNA gene from the Agrobacterium Ti plasmid pTiA6 encodes an enzyme that catalyzes synthesis of indoleacetic acid. Proc. Natl. Acad. Sci. USA 81, 5071–5075.PubMedGoogle Scholar
  118. Thomashow, M. F., Hugly, S., Buchholz, W. G. and Thomashow, L. S. (1986) Molecular basis for the auxin-independent phenotype of crown gall tumor tissues. Science 231, 616–618.PubMedGoogle Scholar
  119. Trewavas, A. J. (1981) How do plant growth substances act? Plant, Cell Env. 4, 203–228.Google Scholar
  120. Tsurumi, S. and Wada, S. (1980) Metabolism of indole-3-acetic acid and natural occurence of dioxindole-3acetic acid derivatives in Vicia roots. Plant Cell Physiol. 21, 1515–1525.Google Scholar
  121. Tuominen, H. (1997) Secondary xylem formation in transgenic hybrid aspen trees with an altered indole-3acetic acie balance. Ph.D. thesis. Acta Universitatis Agriculturae Sueciae, Silvestria 38, Umeä.Google Scholar
  122. Tuominen, H., Ostin, A., Sandberg, G. and Sundberg, B. (1994) A novel metabolic pathway for Mole-3acetic acid in apical shoots of Populus tremula (L.) x Populus tremuloides (Michx.). Plant Physiol. 106, 1511–1520.PubMedGoogle Scholar
  123. Tuominen, H., Sitbon, F., Jacobsson, C., Sandberg, G., Olsson, O., Sundberg, B. (1995) Altered growth and wood characteristics in transgenic hybrid aspen expressing Agrobacterium tumefaciens T-DNA indoleacetic acid-biosynthetic genes. Plant Physiol. 109, 1179–1189.PubMedGoogle Scholar
  124. Tuominen, H., Puech, L., Fink, S., Sundberg, B. (1997) A radial gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen. Plant Physiology 115, 577–585.PubMedGoogle Scholar
  125. Tuominen H., Regan, S., Puech, L., Fink, S., Olsson, O. and Sundberg, B. (1999) Vascular-specific expression of bacterial indole-3-acetic acid-biosynthetic genes in transgenic Populus visualized by the uidA reporter gene as a co-ordinately expressed control. submittedGoogle Scholar
  126. Uggla, C., Moritz, T., Sandberg, G. and Sundberg, B. (1996) Auxin as a positional signal in pattern formation in plants. Proc. Natl. Acad. Sci. USA 93, 9282–9286.PubMedGoogle Scholar
  127. Uggla, C., Mellerowicz, E. J. and Sundberg, B. (1998) Indole-3-acetic acid controls cambial growth in Scots pine by positional signaling. Plant Physiol. 117, 113–121.PubMedGoogle Scholar
  128. Utsuno, K., Shikanai, T., Yamada, Y. and Hashimoto, T. (1998) AGR, an Agravitropic locus of Arabidopsis thaliana, encodes a novel membrane-protein family member. Plant Cell Physiol. 39, 1111–1118.Google Scholar
  129. Van Onckelen, H., Prinsen, E., Inzé, D., Rüdelsheim, P., Van Lijsebettens, M., Follin, A., Schell, J., Van Montagu, M. and De Greef, J. (1986) Agrobacterium T- DNA gene I codes for tryptophan 2monooxygenase activity in tobacco crown gall cells. FEBS Lett. 198, 357–360.Google Scholar
  130. Van Montagu, M., Herrera-Estella, A. and Wang, K. (1994) Transformation of Plants and Soil Microorganisms. Cambridge: University Press.Google Scholar
  131. Velten, J., Velten, L., Hain, R. and Schell, J. (1984) Isolation of a dual plant promoter fragment from the Ti plasmid of Agrobacterium tumefaciens. EMBO J 3, 2723–2730.Google Scholar
  132. Venis, M. A. (1972) Auxin-induced conjugation systems in peas. Plant Physiol. 49, 24–27.PubMedGoogle Scholar
  133. Wang, Q. (1996) Gibberellins and the control of shoot growth in Scots pine (Pinus sylvestris L.). Ph.D. thesis. The Swedish University of Agricultural Sciences, Umeä.Google Scholar
  134. Wang, Q., Little, C. H. A., Sheng, C., Odén, P. C. and Pharis, R. P. (1992) Effect of exogenous gibberellin A4i7 on tracheid production, longitudinal growth and the levels of indole-3-acetic acid and gibberellins A4, A7 and A9 in the terminal shoot of Pinus sylvestris seedlings. Physiol. Plant. 86, 202–208.Google Scholar
  135. Wang, Q., Little, C. H. A. and Odén, P. C. (1995) Effect of laterally applied gibberellin A417 on cambial growth and the level of indole-3-acetic acid in Pinus sylvestris shoots. Physiol. Plant. 95, 187–194.Google Scholar
  136. Wang, H., Li, J., Bostock, R. M. and Gilchrist, D. G. (1996) Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8, 375–391.Google Scholar
  137. Wareing, P. F. (1958) Interaction between indole-acetic acid and gibberellic acid in cambial activity. Nature 181, 1744–1745.PubMedGoogle Scholar
  138. Warren Wilson, J. and Warren Wilson, P. M. (1984) Control of tissue patterns in normal development and in regeneration. In Positional controls in plant development. (eds. Barlow, P. W. and Carr, D. J. ), pp. 225–280. Cambridge: Cambridge University Press.Google Scholar
  139. Wetmore, R. H. and Kier, J. P. (1963) Experimental induction of vascular tissues in callus of angiosperms. Am. J. Bot. 50, 418–430.Google Scholar
  140. Whetten, R. and Sederoff, R. (1991) Genetic engineering of wood. Forest Ecol. Manage. 43, 301–316.Google Scholar
  141. Wilson, B. F. and Howard R. A. (1968) A computer model for cambial activity. For. Sci. 14, 77–90.Google Scholar
  142. Wilson, B. F., Wodzicki, T. J. and Zahner, R. (1966) Differentiation of cambial derivatives: proposed terminology. Forest Sci. 12, 438–440.Google Scholar
  143. Wodzicki, T. J. and Zajaczkowski, S. (1974) Effect of auxin on xylem tracheid differentiation in decapitated stems of Pinus sylvestris L. and its interaction with some vitamins and growth regulators. Acta Soc. Bot. Pol. 43, 129–148.Google Scholar
  144. Wodzicki, T. J., Rakowski, K., Starck, Z., Porandowski, J. and Zajaczkowski, S. (1982) Apical control of xylem formation in the pine stem. I. Auxin effects and distribution of assimilates. Acta Soc. Bot. Pol. 51, 187–201.Google Scholar
  145. Wolpert, L. (1994) Positional information and pattern formation in development. Dev. Genetics 15, 485–490.Google Scholar
  146. Wolpert, L. (1996) One hundred years of positional information. Trends Genet. 12, 359–364.PubMedGoogle Scholar
  147. Wolpert, L. and Tickle, C. (1993) Pattern formation and limb morphogenesis. In Molecular Basis of Morphogenesis. (ed. Bernfield, M. ), pp. 207–220. New York: Wiley-Liss.Google Scholar
  148. Yamamoto, F. and Kozlowski, T. T. (1987) Effects of flooding, tilting of stems, and ethrel application on growth, stem anatomy, and ethylene production of Acer platanoides seedlings. Scand. J. For. Res. 2, 141–156.Google Scholar
  149. Yamamoto, F., Angeles, G. and Kozlowski, T. T. (1987) Effect of ethrel on stem anatomy of Ulmus americana seedlings. IAWA Bull. 8, 3–9.Google Scholar
  150. Yang, S. F. and Hoffman, N. E. (1984) Ethylene biosynthesis and its regulation in higher plants. Ann. Rev. Plant Physiol. 35, 155–189.Google Scholar
  151. Zakrzewski, J. (1983) Hormonal control of cambial activity and vessel differentiation in Quercus robur. Physiol. Plant. 57, 537–542.Google Scholar
  152. Zakrzewski, J. (1991) Effect of indole-3-acetic acid (IAA) and sucrose on vessel size and density in isolated stem segments of oak (Quercus robur). Physiol. Plant. 81, 234–238.Google Scholar
  153. Zamski, E. and Wareing, P. F. (1974) Vertical and radial movement of auxin in young sycamore plants. New Phytol. 73, 61–69.Google Scholar
  154. Zobel, B. J. and van Buijtenen, J. P. (1989) Wood variation. Its causes and control. Berlin: Springer-Verlag.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2000

Authors and Affiliations

  • Hannele Tuominen
    • 1
  • Olof Olsson
    • 1
  • Björn Sundberg
    • 1
  1. 1.Department of Forest Genetics and Plant PhysiologySwedish University of Agricultural SciencesUmeåSweden

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