Plant Molecular Biology

, Volume 47, Issue 1–2, pp 239–274 | Cite as

Unravelling cell wall formation in the woody dicot stem

  • Ewa J. Mellerowicz
  • Marie Baucher
  • Björn Sundberg
  • Wout Boerjan


Populus is presented as a model system for the study of wood formation (xylogenesis). The formation of wood (secondary xylem) is an ordered developmental process involving cell division, cell expansion, secondary wall deposition, lignification and programmed cell death. Because wood is formed in a variable environment and subject to developmental control, xylem cells are produced that differ in size, shape, cell wall structure, texture and composition. Hormones mediate some of the variability observed and control the process of xylogenesis. High-resolution analysis of auxin distribution across cambial region tissues, combined with the analysis of transgenic plants with modified auxin distribution, suggests that auxin provides positional information for the exit of cells from the meristem and probably also for the duration of cell expansion. Poplar sequencing projects have provided access to genes involved in cell wall formation. Genes involved in the biosynthesis of the carbohydrate skeleton of the cell wall are briefly reviewed. Most progress has been made in characterizing pectin methyl esterases that modify pectins in the cambial region. Specific expression patterns have also been found for expansins, xyloglucan endotransglycosylases and cellulose synthases, pointing to their role in wood cell wall formation and modification. Finally, by studying transgenic plants modified in various steps of the monolignol biosynthetic pathway and by localizing the expression of various enzymes, new insight into the lignin biosynthesis in planta has been gained.

expressed sequence tag hybrid aspen Populus vascular cambium wood formation xylem cell wall 


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  1. Abe, H., Funada, R., Imaizumi, H., Ohtani, J. and Fukazawa, K. 1995. Dynamic changes in the arrangement of cortical microtubules in conifer tracheids during differentiation. Planta 197: 418–421.Google Scholar
  2. Abe, H., Funada, R., Ohtani, J. and Fukazawa, K. 1997. Changes in the arrangement of cellulose microfibrils associated with the cessation of cell expansion in tracheids. Trees 11: 328–332.Google Scholar
  3. Abel, S., Nguyen, M.D., Chow, W. and Theologis, A. 1995. ASC4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. Structural characterization, expression in Escherichia coli, and expression characteristics in response to auxin. J. Biol. Chem. 270: 19093–19099.Google Scholar
  4. Allina, S.M., Pri-Hadash, A., Theilmann, D.A., Ellis, B.E. and Douglas, C.J. 1998. 4-Coumarate:coenzyme A ligase in hybrid poplar. Plant Physiol. 116: 743–754.Google Scholar
  5. Allona, I., Quinn, M., Shoop, E., Swope, K., St. Cyr, S., Carlis, J., Riedl, J., Retzel, E., Campbell, M.M., Sederoff, R. and Whetten, R.W. 1998. Analysis of xylem formation in pine by cDNA sequencing. Proc. Natl. Acad. Sci. USA 95: 9693–9698.Google Scholar
  6. Aloni, R. 1979. Role of auxin and gibberellin in differentiation of primary phloem fibers. Plant Physiol. 63: 609–614.Google Scholar
  7. Aloni, R. 1991. Wood formation in deciduous hardwood trees. In: A.S. Raghavendra (Ed.) Physiology of Trees, John Wiley, New York, pp. 175–197.Google Scholar
  8. Aloni, R., Tollier, M.T. and Monties, B. 1990. The role of auxin and gibberellin in controlling lignin formation in primary phloem fibers and in xylem of Coleus blumei stems. Plant Physiol. 94: 1743–1747.Google Scholar
  9. Araki, N., Fujita, M., Saiki, H. and Harada, H. 1982. Transition of the fiber wall structure from normal wood to tension wood in Robinia pseudoacacia L. and Populus euroamericana Guinier. Mokuzai Gakkaishi 28: 267–273.Google Scholar
  10. Arioli, T., Peng, L.C., Betzner, A.S., Burn, J., Wittke, W., Herth, W., Camilleri, C., Höfte, H., Plazinski, J., Birch, R., Cork, A., Glover, J., Redmond, J. and Williamson, R.E. 1998. Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279: 717–720.Google Scholar
  11. Awano, T., Takabe, K. and Fujita, M. 1998. Localization of glucuronoxylans in Japanese beech visualized by immunogold labeling. Protoplasma 202: 213–222.Google Scholar
  12. Awano, T., Takabe, K., Fujita, M. and Daniel, G. 2000. Deposition of glucuronoxylans on the secondary cell wall of Japanese beech as observed by immune-scanning electron microscopy. Protoplasma 212: 72–79.Google Scholar
  13. Baba, K.-i., Adachi, K., Take, T., Yokoyama, T., Itho, T., and Nakamura, T. 1995. Induction of tension wood in GA3-treated branches of the weeping type of Japanese cherry, Prunus spachiana. Plant Cell Physiol. 36: 983–988.Google Scholar
  14. Baïer, M., Goldberg, R., Catesson, A.-M., Liberman, M., Bouchemal, N., Michon, V. and Hervé du Penhoat, C. 1994. Pectin changes in samples containing poplar cambium and inner bark in relation to the seasonal cycle. Planta 193: 446–454.Google Scholar
  15. Bailey, I.W. 1954. Contributions to plant anatomy. Chronanica Botanica, Waltham, MA.Google Scholar
  16. Baima, S., Nobili, F., Sessa, G., Lucchetti, S., Ruberti, I. and Morelli, G. 1995. The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121: 4171–4182.Google Scholar
  17. Barnett, J.R. 1992. Reactivation of the cambium in Aesculus hipocastanum L.: a transmission electron microscope study. Ann. Bot. 70: 169–177.Google Scholar
  18. Barnett, J.R. 1995. Ultrastructural factors affecting xylem differentiation. In: M. Iqbal (Ed.) The Cambial Derivatives (Handbuch der Pflanzenanatomie, Band IX, Teil 4: Spezieller Teil), Borntraeger, Berlin, pp. 107–130.Google Scholar
  19. Barnett, J.R. and Harris, J.M. 1975. Early stages of bordered pit formation in radiata pine. Wood Sci. Technol. 9: 233–241.Google Scholar
  20. Bate, N.J., Orr, J., Ni, W., Meromi, A., Nadler-Hassar, T., Doerner, P.W., Dixon, R.A., Lamb, C.J. and Elkind, Y. 1994. Quantitative relationship between phenylalanine ammonia-lyase levels and phenylpropanoid accumulation in transgenic tobacco identifies a rate-determining step in natural product synthesis. Proc. Natl. Acad. Sci. USA 91: 7608–7612.Google Scholar
  21. Baucher, M., Chabbert, B., Pilate, G., Van Doorsselaere, J., Tollier, M.-T., Petit-Conil, M., Cornu, D., Monties, B., Van Mon-tagu, M., Inzé, D., Jouanin, L. and Boerjan, W. 1996. Red xylem and higher lignin extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar). Plant Physiol. 112: 1479–1490.Google Scholar
  22. Baucher, M., Monties, B., Van Montagu, M. and Boerjan, W. 1998. Biosynthesis and genetic engineering of lignin. Crit. Rev. Plant Sci. 17: 125–197.Google Scholar
  23. Baucher, M., Bernard-Vailhé, M.A., Chabbert, B., Besle, J.-M., Opsomer, C., Van Montagu, M. and Botterman, J. 1999. Down-regulation of cinnamyl alcohol dehydrogenase in transgenic alfalfa (Medicago sativa L.) and the impact on lignin composition and digestibility. Plant Mol. Biol. 39: 437–447.Google Scholar
  24. Bell-Lelong, D.A., Cusumano, J.C., Meyer, K. and Chapple, C. 1997. Cinnamate-4-hydroxylase expression in Arabidopsis. Plant Physiol. 113: 729–738.Google Scholar
  25. Benayoun, J. 1983. A cytochemical study of cell wall hydrolysis in the secondary xylem of poplar (Populus italica Moench). Ann. Bot. 52: 189–200.Google Scholar
  26. Benayoun, J., Catesson, A.M. and Czaninski, Y. 1981. A cytochemical study of differentiation and breakdown of vessel end walls. Ann. Bot. 47: 687–698.Google Scholar
  27. Benjavongkulchai, E. and Spencer, M.S. 1986. Purification and characterization of barley aleurone xylanase. Planta 169: 415–419.Google Scholar
  28. Bentum, A.L.K., Côté, W.A. Jr., Day, A.C. and Timell, T.E. 1969. Distibution of lignin in normal and tension wood. Wood Sci. Technol. 3: 218–231.Google Scholar
  29. Bih, F.Y., Wu, S.S.H., Ratnayake, C., Walling, L.L., Nothnagel, E.A. and Huang, A.H.C. 1999. The predominant protein on the surface of maize pollen is an endoxylanase synthesized by a tapetum mRNA with a long 5′ leader. J. Biol. Chem. 274: 22884–22894.Google Scholar
  30. Bisset, I.J.W. and Dadswell, H.E. 1950. The variation in cell length within one growth ring of certain angiosperms and gymnosperms. Aust. For. 14: 17–29.Google Scholar
  31. Blount, J.W., Korth, K.L., Masoud, S.A., Rasmussen, S., Lamb, C. and Dixon, R.A. 2000. Altering expression of cinnamic acid 4-hydroxylase in transgenic plants provides evidence for a feedback loop at the entry point into the phenylpropanoid pathway. Plant Physiol. 122: 107–116.Google Scholar
  32. Bolwell, G.P. 1993. Dynamic aspects of the plant extracellular matrix. Int. Rev. Cytol. 146: 261–324.Google Scholar
  33. Bolwell, G.P. and Northcote, D.H. 1981. Control of hemicellulose and pectin synthesis during differentiation of vascular tissue in bean (Phaseolus vulgaris) callus and in bean hypocotyls. Planta 152: 225–233.Google Scholar
  34. Bolwell, G.P. and Northcote, D.H. 1983. Induction by growth factors of polysaccharide synthases in bean cell suspension cultures. Biochem. J. 210: 509–515.Google Scholar
  35. Bolwell, G.P., Dalessandro, G. and Northcote, D.H. 1985. Decrease of polygalacturonic acid synthase during xylem differentiation in sycamore. Phytochemistry 24: 699–702.Google Scholar
  36. Bonin, C.P., Potter, I., Vanzin, G.F. and Reiter, W.-D. 1997. The MUR1 gene of Arabidopsis thaliana encodes an isoform of GDP-D-mannose-4,6-dehydratase, catalyzing the first step in the de novo synthesis of GDP-L-fucose. Proc. Natl. Acad. Sci. USA 94: 2085–2090.Google Scholar
  37. Boudet, A.-M. 2000. Lignin and lignification: selected issues. Plant Physiol. Biochem. 38: 81–96.Google Scholar
  38. Boyce, S.G. and Kaeiser, M. 1961. Environmental and genetic variability in the length of fibers of eastern cottonwood. TAPPI 44: 363–366.Google Scholar
  39. Bradshaw, H.D. Jr. and Stettler, R.F. 1993. Molecular genetics of growth and development in Populus. I. Triploidy in hybrid poplars. Theor. Appl. Genet. 86: 301–307.Google Scholar
  40. Bradshaw, H.D. Jr., Villar, M., Watson, B.D., Otto, K.G., Stewart, S. and Stettler, R.F. 1994. Molecular genetics of growth and development in Populus. III. A genetic linkage map of a hybrid poplar composed of RFLP, STS, and RAPD markers. Theor. Appl. Genet. 89: 167–178.Google Scholar
  41. Bragina, T.V., Martinovitch, L.I., Rodionova, N.A., Bezborodov, A.M., and Grineva, G.M. 1999. Effects of stress induced by total submergence on cellulase and xylanase activities in adventitious roots of maize. Appl. Biochem. Microbiol. 35: 407–410.Google Scholar
  42. Brett, C.T. 2000. Cellulose microfibrils in plants: biosynthesis, deposition, and integration into the cell wall. Int. Rev. Cytol. 199: 161–199.Google Scholar
  43. Brett, C.T. and Waldron, K.W. 1996. Physiology and Biochemistry of Plant Cell Walls. Chapman and Hall, London.Google Scholar
  44. Butterfield, B.G. 1995. Vessel element differentiation. In: M. Iqbal (Ed.) The Cambial Derivatives (Handbuch der Pflanzenanatomie, Band IX, Teil 4: Spezieller Teil), Borntraeger, Berlin, pp. 93–106.Google Scholar
  45. 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.Google Scholar
  46. Carpita, N.C. and Gibeaut, D.M. 1993. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 3: 1–30.Google Scholar
  47. Catesson, A.-M. 1964. Origine, fonctionnement et variations cytologiques saisonnières du cambium de l'Acer pseudoplatanus L. (Acéracées). Ann. Sci. Nat. Bot. (12ème série) 5: 229–498.Google Scholar
  48. Catesson, A.-M. 1989. Specific characters of vessel primary walls during the early stages of wood differentiation. Biol. Cell 67: 221–226.Google Scholar
  49. Catesson, A.-M. 1990. Cambial cytology and biochemistry. In: M. Iqbal (Ed.) The Vascular Cambium (Research Studies in Botany and Related Applied Fields, vol. 7), Research Studies Press, Taunton, USA, pp. 63–112.Google Scholar
  50. Catesson, A.M. and Roland, J.C. 1981. Sequential changes associated with cell wall formation and fusion in the vascular cambium. IAWA Bull. 2: 151–162.Google Scholar
  51. Catesson, A.M., Funada, R., Robertbaby, D., Quinetszely, M., Chuba, J. and Goldberg R. 1994. Biochemical and cytochemical cell-wall changes across the cambial zone. IAWA J. 15: 91–101.Google Scholar
  52. Cervera, M.-T., Storme, V., Ivens, B., Gusmão, J., Liu, B.H., Hostyn, V., Van Slycken, J., Van Montagu, M., Boerjan, W. 2001. Dense genetic linkage maps of three Populus species (Populus deltoides, P. nigra and P. trichocarpa) based on Amplified Fragment Length Polymorphism and Microsatellite Markers. Genetics 158: 787–809.Google Scholar
  53. Chaffey, N., Barnett, J. and Barlow, P. 1997a.Endomembranes, cytoskeleton, and cell walls: aspects of the ultrastructure of the vascular cambium of taproots of Aesculus hippocastanum L. (Hippocastanaceae). Int. J. Plant Sci. 158: 97–109.Google Scholar
  54. Chaffey, N., Barlow, P. and Barnett, J. 1997b. Cortical microtubules rearrange during differentiation of vascular cambial derivatives, microfilaments do not. Trees Struct. Funct. 11: 333–341.Google Scholar
  55. Chaffey, N.J., Barlow, P.W. and Barnett, J.R. 1998. A seasonal cycle of cell wall structure is accompanied by a cyclical rearrangement of cortical microtubules in fusiform cambial cells within taproots of Aesculus hippocastanum (Hippocastanaceae). New Phytol. 139: 623–635.Google Scholar
  56. Chaffey, N., Barnett, J. and Barlow, P. 1999. A cytoskeletal basis for wood formation in angiosperm trees: the involvement of cortical microtubules. Planta 208: 19–30.Google Scholar
  57. Chalmers, M.J. and Gaskell, S.J. 2000. Advances in mass spectrometry for proteome analysis. Curr. Opin. Biotechnol. 11: 384–390.Google Scholar
  58. Chapple, C.C.S., Vogt, T., Ellis, B.E. and Somerville, C.R. 1992. An Arabidopsis mutant defective in the general phenylpropanoid pathway. Plant Cell 4: 1413–1424.Google Scholar
  59. Chen, F., Yasuda, S. and Fukushima, K. 1999. Evidence for a novel biosynthetic pathway that regulates the ratio of syringyl to guaiacyl residues in lignin in the differentiating xylem of Magnolia kobus DC. Planta 207: 597–603.Google Scholar
  60. Chen, C., Meyermans, H., Burggraeve, B., De Rycke, R.M., Inoue, K., De Vleesschauwer, V., Steenackers, M., Van Montagu, M.C., Engler, G.J. and Boerjan, W.A. 2000. Cell-specific and conditional expression of caffeoyl-CoA O-methyltransferase in poplar. Plant Physiol. 123: 853–867.Google Scholar
  61. Christensen, J.H., Bauw, G., Welinder, K.G., Van Montagu, M. and Boerjan, W. 1998. Purification and characterization of peroxidases correlated with lignification in poplar xylem. Plant Physiol. 118: 125–135.Google Scholar
  62. Christensen, J.C., Baucher, M., O'Connell, A.P., Van Montagu, M. and Boerjan, W. 2000. Control of lignin biosynthesis. In: S.M. Jain and S.C. Minocha (Eds.) Molecular Biology of Woody Plants, vol. 1 (Forestry Sciences, vol. 64), Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 227–267.Google Scholar
  63. Cosgrove, D.J. 1997. Assembly and enlargement of the primary cell wall in plants. Annu. Rev. Cell Dev. Biol. 13: 171–201.Google Scholar
  64. Cosgrove, D.J. 2000. Expansive growth of plant cell walls. Plant Physiol. Biochem. 38: 109–124.Google Scholar
  65. Côté, W.A. 1977. Wood ultrastructure in relation to chemical composition. In: F.A. Loewus and V.C. Runeckles (Eds.) The Structure, Biosynthesis, and Degradation of Wood (Recent Advances in Phytochemistry, vol. 11), Plenum, New York, pp. 1–44.Google Scholar
  66. Couchy, I., Minic, Z., Laporte, J., Brown, S. and Satiat-Jeunemaitre, B. 1998. Immunodetection of Rho-like plant proteins with Rac1 and Cdc42Hs antibodies. J. Exp. Bot. 49: 1647–1659.Google Scholar
  67. Dalessandro, G. and Northcote, D.H. 1977. Changes in enzymatic activities of nucleoside diphosphate sugar interconversions during differentiation of cambium to xylem in sycamore and poplar. Biochem. J. 162: 267–279.Google Scholar
  68. Darley, C.P., Forrester, A.M. and McQueen-Mason, S.J. 2001. The molecular basis of plant cell wall extension. Plant Mol. Biol. 47: 171–187.Google Scholar
  69. Dean, J.F.D., LaFayette, P.R., Rugh, C., Tristram, A.H., Hoopes, J.T., Eriksson, K.-E.L. and Merckle, S.A. 1998. Laccases associate with lignifying vascular tissues. In: N.G. Lewis and S. Sarkanen (Eds) Lignin and Lignan Biosynthesis (ACS Symposium Series, vol. 697), American Chemical Society, Washington, DC, pp. 96–108.Google Scholar
  70. del Campillo, E. 1999. Multiple endo-1,4–D-glucanase (cellulase) genes in Arabidopsis. Curr. Top. Dev. Biol. 46: 39–61.Google Scholar
  71. Delmer, D.P., Pear, J.R., Andrawis, A. and Stalker, D.M. 1995. Genes encoding small GTP-binding proteins analogous to mammalian rac are preferentially expressed in developing cotton fibers. Mol. Gen. Genet. 248: 43–51.Google Scholar
  72. Dhillon, S.S. 1987. DNA in tree species. In: J.M. Bonga and D.J. Durzan (Eds.) Cell and Tissue Culture in Forestry, vol. 1, Martinus Nijhoff, Dordrecht, Netherlands, pp. 298–313.Google Scholar
  73. Dhugga, K.S., Tiwari, S.C. and Ray, P.M. 1997. A reversibly glycosylated polypeptide (RGP1) possibly involved in plant cell wall synthesis: purification, gene cloning, and trans-Golgi localization. Proc. Natl. Acad. Sci. USA 94: 7679–7684.Google Scholar
  74. 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
  75. Dodd, R.S. and Fox, P. 1990. Kinetics of tracheid differentiation in Douglas-fir. Ann. Bot. 65: 649–657.Google Scholar
  76. Domingo, C., Roberts, K., Stacey, N.J., Connerton, I., Ruíz-Teran, F. and McCann, M.C. 1998. A pectate lyase from Zinnia elegans is auxin inducible. Plant J. 13: 17–28.Google Scholar
  77. Eklund, L. and Little, C.H.A. 1996. Laterally applied Etherel causes local increases in radial growth and indole-3-acetic acid concentration in Abies balsamea shoots. Tree Physiol. 16: 509–513.Google Scholar
  78. Elkind, Y., Edwards, R., Mavandad, M., Hedrick, S.A., Ribak, O., Dixon, R.A. and Lamb, C.J. 1990. Abnormal plant development and down-regulation of phenylpropanoid biosynthesis in transgenic tobacco containing a heterologous phenylalanine ammonia-lyase gene. Proc. Natl. Acad. Sci. USA 87: 9057–9061.Google Scholar
  79. Eriksson, M.E., Israelsson, M., Olsson, O. and Moritz, T. 2000. Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nature Biotechnol. 18: 784–788.Google Scholar
  80. Ermel, F.F., Follet-Gueye, M.-L., Cibert, C., Vian, B., Morvan, C., Catesson, A.-M. and Goldberg, R. 2000. Differential localization of arabinan and galactan side chains of rhamnogalacturonan 1 in cambial derivatives. Planta 210: 732–740.Google Scholar
  81. Evert, R.F. and Kozlowski, T.T. 1967. Effect of isolation of bark on cambial activity and development of xylem and phloem in trembling aspen. Am. J. Bot. 54: 1045–1054.Google Scholar
  82. Evert, R.F., Kozlowski, T.T. and Davis, J.D. 1972. Influence of phloem blockage on cambial growth of sugar maple. Am. J. Bot. 59: 632–641.Google Scholar
  83. Faik, A., Bar-Peled, M., DeRocher, A.E., Zeng, W., Perrin, R.M., Wilkerson, C., Raikhel, N.V. and Keegstra, K. 2000. Biochemical characterization and molecular cloning of an α-1,2-fucosyltransferase that catalyzes the last step of cell wall xyloglucan biosynthesis in pea. J. Biol. Chem. 275: 15082–15089.Google Scholar
  84. Fagard, M., Desnos, T., Desprez, T., Goubet, F., Refregier, G., Mouille, G., McCann, M., Rayon, C., Vernhettes, S. and Höfte, H. 2001. PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of arabidopsis. Plant Cell 12: 2409–2423.Google Scholar
  85. Fergus, B.J. and Goring, D.A.I. 1970. The location of guaiacyl and syringyl lignins in birch xylem tissue. Holzforschung 24: 113–117.Google Scholar
  86. Feuillet, C., Lauvergeat, V., Deswarte, C., Pilate, G., Boudet, A. and Grima-Pettenati, J. 1995. Tissue-and cell-specific expression of a cinnamyl alcohol dehydrogenase promoter in transgenic poplar plants. Plant Mol. Biol. 27: 651–667.Google Scholar
  87. Follet-Gueye, M.L., Ermel, F.F., Vian, B., Catesson, A.M. and Goldberg, R. 2000. In: R. Savidge, J. Barnett and R. Napier (Eds) Cell and Molecular Biology of Wood Formation, BIOS Scientific Publications, Oxford, pp. 289–294.Google Scholar
  88. Franke, R., McMichael, C.M., Meyer, K., Shirley, A.M., Cusumano, J.C. and Chapple, C. 2000. Modified lignin in tobacco and poplar plants over-expressing the Arabidopsis gene encoding ferulate 5-hydroxylase. Plant J. 22: 223–234.Google Scholar
  89. Frewen, B.E., Chen, T.H.H., Howe, G.T., Davis, J., Rohde, A., Boerjan, W. and Bradshaw, H.D. Jr. 2000. Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus. Genetics 154: 837–845.Google Scholar
  90. Fujii, T., Harada, H. and Saiki H. 1979. The layered structure of ray parenchyma secondary wall in the wood of 49 Jananese angiosperm species. Mokuzai Gakkaishi 25: 251–257.Google Scholar
  91. Fujii, T., Harada, H. and Saiki, H. 1981. Ultrastructure of ‘amorphous layer’ in xylem parenchyma cell wall of angiosperm species. Mokuzai Gakkaishi 27: 149–156.Google Scholar
  92. Fujino, T. and Itoh, T. 1998. Changes in the three dimensional architecture of the cell wall during lignification of xylem cells in Eucalyptus tereticornis. Holzforschung 52: 111–116.Google Scholar
  93. Fujita, M., Sakai, H. and Harada, H. 1974. Electron microscopy of microtubules and cellulose microfibrils in secondary wall formation of poplar tension wood. Mokuzai Gakkaishi 20: 147–156.Google Scholar
  94. Fukuda, H. 1992. Tracheary element formation as a model system of cell differentiation. Int. Rev. Cytol. 136: 289–332.Google Scholar
  95. Fukuda, H. 1997. Tracheary element differentiation. Plant Cell 9: 1147–1156.Google Scholar
  96. Fukuda, H. and Komamine, A. 1980. Direct evidence for cytodifferentiation to tracheary elements without intervening mitosis in a culture of single cells isolated from the mesophyll of Zinnia elegans. Plant Physiol. 65: 61–64.Google Scholar
  97. Fukuda, T. and Terashima, N. 1988. Heterogeneity in formation of lignin XII. Deposition of chemical components during the formation of cell walls of black pine and poplar. Makuzai Gakkaishi 34: 604–608.Google Scholar
  98. Funada, R. 2000. Control of wood structure. In: P. Nick (Ed.) Plant Microtubules, Springer-Verlag, Berlin, pp. 51–82.Google Scholar
  99. Funada, R. and Catesson, A.M. 1991. Partial cell-wall lysis and the resumption of meristematic activity in Fraxinus excelsior cambium. IAWA Bull. 12: 439–444.Google Scholar
  100. Gahan, P.B. 1988. Xylem and phloem differentiation in perspective. In: L.W. Roberts, P.B. Gahan and R. Aloni (Eds.) Vascular Differentiation and Plant Growth Regulators, Springer-Verlag, Berlin, pp. 1–21.Google Scholar
  101. Gang, D.R., Kasahara, H., Xia, Z.-Q., Vander Mijnsbrugge, K., Bauw, G., Boerjan, W., Van Montagu, M., Davin, L.B. and Lewis, N.G. 1999. Evolution of plant defense mechanisms. Relationships of phenylcoumaran benzylic ether reductases to pinoresinol-lariciresinol and isoflavone reductases. J. Biol. Chem. 274: 7516–7527.Google Scholar
  102. Ge, H. 2000. UPA, a universal protein array system for quantitative detection of protein-protein, protein-DNA, protein-RNA and protein-ligand interactions. Nucl. Acids Res. 28: e3.Google Scholar
  103. Gibeaut, D.M. 2000. Nucleotide sugars and glycosyltransferases for synthesis of cell wall matrix polysaccharides. Plant Physiol. Biochem. 38: 69–80.Google Scholar
  104. Goldberg, R., Catesson, A.-M. and Czaninski, Y. 1983. Some properties of syringaldazine oxidase, a peroxidase specifically involved in the lignification processes. Z. Pflanzenphysiol. 110: 267–279.Google Scholar
  105. Goosen-de Rao, L., Bakhuizen, R., van Spronsen, P. and Libbenga, K.R. 1984. The presence of extended phragmosomes containing cytoskeletal elements in fusiform cambial cells of Fraxinus excelsior L. Protoplasma 122: 145–152.Google Scholar
  106. Goring, D.A.I. and Timell, T.E. 1962. Molecular weight of native celluloses. TAPPI 45: 454–460.Google Scholar
  107. Gorshkova, T.A., Chemikosova, S.B., Lozovaya, V.V. and Carpita, N.C. 1997. Turnover of galactans and other cell wall polysaccharides during development of flax plants. Plant Physiol. 114: 723–729.Google Scholar
  108. Goto, M., Takabe, K. and Abe, I. 1998. Histochemistry and UV-microspectrometry of cell walls of untreated and ammonia-treated barley straw. Can. J. Plant Sci. 78: 437–443.Google Scholar
  109. Gregory, A.C.E., O'Connell, A.P. and Bolwell, G.P. 1998. Xylans. Biotechnol. Genet. Eng. Rev. 15: 439–455.Google Scholar
  110. Gregory, R.A. 1971. Cambial activity in Alaskan white spruce. Am. J. Bot. 58: 160–171.Google Scholar
  111. Grima-Pettenati, J. and Goffner, D. 1999. Lignin genetic engineering revisited. FEBS Lett. 145: 51–65.Google Scholar
  112. Grimmig, B., Kneusel, R.E., Junghanns, K.T. and Matern, U. 1999. Expression of bifunctional caffeoyl-CoA 3-O-methyltransferase in stress compensation and lignification. Plant Biol. 1: 299–310.Google Scholar
  113. Guglielmino, N., Liberman, M., Jauneau, A., Vian, B., Catesson, A.M. and Goldberg, R. 1997a. Pectin immunolocalization and calcium visualization in differentiating derivatives from poplar cambium. Protoplasma 199: 151–160.Google Scholar
  114. Guglielmino, N., Liberman, M., Catesson, A.M., Mareck, A., Prat, R., Mutaftschiev, S. and Goldberg, R. 1997b. Pectin methylesterases from poplar cambium and inner bark: localization, properties and seasonal changes. Planta 202: 70–75.Google Scholar
  115. Hafren, J., Daniel, G. and Westmark, U. 2000. The distribution of acidic and esterified pectin in cambium, developing xylem and mature xylem of Pinus sylvestris. IAWA J. 21: 157–168.Google Scholar
  116. Haigler, C.H. and Brown, R.M. Jr. 1986. Transport of rosettes from the Golgi apparatus to the plasma membrane in isolated mesophyll cells of Zinnia elegans during differentiation to tracheary elements in suspension culture. Protoplasma 134: 111–120.Google Scholar
  117. Haigler, C.H., Ivanova-Datcheva, M., Hogan, P.S., Salnikov, V.V., Hwang, S., Martin, L.K. and Delmer, D.P. 2001. Carbon partitioning to cellulose synthesis. Plant Mol. Biol., this issue.Google Scholar
  118. Halpin, C., Knight, M.E., Foxon, G.A., Campbell, M.M., Boudet, A.M., Boon, J.J., Chabbert, B., Tollier, M.-T. and Schuch, W. 1994. Manipulation of lignin quality by downregulation of cinnamyl alcohol dehydrogenase. Plant J. 6: 339–350.Google Scholar
  119. Han, K.-H., Gordon, M.P. and Strauss, S.H. 1997. High-frequency transformation of cottonwoods (genus Populus) byAgrobacterium rhizogenes. Can. J. For. Res. 27: 464–470.Google Scholar
  120. Han, K.-H., Meilan, R., Ma, C. and Strauss, S.H. 2000. An Agrobacterium tumefaciens transformation protocol effective on a variety of cottonwood hybrids (genus Populus). Plant Cell Rep. 19: 315–320.Google Scholar
  121. Harada, H. and Côté, W.A. Jr. 1985. Structure of wood. In: T. Higuchi (Ed.) Biosynthesis and Biodegradation of Wood Components, Academic Press, Orlando, FL, pp. 1–44.Google Scholar
  122. Hauch, S. and Magel, E. 1998. Extractable activities and protein content of sucrose-phosphate synthase, sucrose synthase and neutral invertase in trunk tissues of Robinia pseudoacacia L. are related to cambial wood production and heartwood formation. Planta 207: 266–274.Google Scholar
  123. 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.Google Scholar
  124. Hayashi, T. 1989. Xyloglucans in the primary cell wall. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40: 139–168.Google Scholar
  125. He, L. and Terashima, N. 1991. Formation and structure of lignin in monocotyledons. IV. Deposition process and structural diversity of the lignin in the cell wall of sugarcane and rice plants studied by ultraviolet microscopic spectroscopy. Holzforschung 45: 191–198.Google Scholar
  126. Hejnowicz, A. and Hejnowicz, Z. 1958. Variation of length of vessel members and fibres in the trunk of Populus tremula L. Acta Soc. Bot. Pol. 27: 131–159.Google Scholar
  127. Hertzberg, M., Sievertzon, M., Aspeborg, H., Nilsson, P., Sandberg, G. and Lundeberg, J. 2001. cDNA microarray analysis of small plant tissue samples using a cDNA tag target amplification protocol. Plant J., in press.Google Scholar
  128. Hibino, T., Takabe, K., Kawazu, T., Shibata, D. and Higuchi, T. 1995. Increase of cinnamaldehyde groups in lignin of transgenic tobacco plants carrying an antisense gene for cinnamyl alcohol dehydrogenase. Biosci. Biotech. Biochem. 59: 929–931.Google Scholar
  129. Holland, N., Holland, D., Helentjaris, T., Dhugga, K.S., Xoconostle-Cazares, B. and Delmer, D.P. 2000. A comparative analysis of the plant cellulose synthase (Cesa) gene family. Plant Physiol. 123: 1313–1323.Google Scholar
  130. Hrazdina, G. 1992. Compartmentation in aromatic metabolism. In: H.A. Stafford and R.K. Ibrahim (Eds.) Phenolic Metabolism in Plants (Recent Advances in Phytochemistry, vol. 26), Plenum New York, pp. 1–23.Google Scholar
  131. Hu, W.-J., Kawaoka, A., Tsai, C.-J., Lung, J., Osakabe, K., Ebinuma, H. and Chiang, V.L. 1998. Compartmentalized expression of two structurally and functionally distinct 4-coumarate:CoA ligase genes in aspen (Populus tremuloides). Proc. Natl. Acad. Sci. USA 95: 5407–5412.Google Scholar
  132. Hu, W.-J., Harding, S.A., Lung, J., Popko, J.L., Ralph, J., Stokke, D.D., Tsai, C.-J. and Chiang, V.L. 1999. Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nature Biotechnol. 17: 808–812.Google Scholar
  133. Humphreys, J.M., Hemm, M.R. and Chapple, C. 1999. New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cytochrome P450-dependent monooxygenase. Proc. Natl. Acad. Sci. USA 96: 10045–10050.Google Scholar
  134. Im, K.-H., Cosgrove, D.J. and Jones, A.M. 2000. Subcellular localization of expansin mRNA in xylem cells. Plant Physiol. 123: 463–470.Google Scholar
  135. Imai, T. and Terashima, N. 1992. Determination of the distribution and reaction of polysaccharides in wood cell-walls by the isotope tracer technique III. Visualisation of the deposition and distribution of galacturanan in the cell walls of magnolia (Magnolia kobus DC.) xylem by microautoradiography. Mokuzai Gakkaishi 38: 475–481.Google Scholar
  136. Ingold, E., Sugiyama, M. and Komamine, A. 1988. Secondary cell wall formation: changes in cell wall constituents during the differentiation of isolated mesophyll cells of Zinnia elegans to tracheary elements. Plant Cell Physiol. 29: 295–303.Google Scholar
  137. Inoue, K., Sewalt, V.J.H., Ballance, G.M., Ni, W., Stürzer, C. and Dixon, R.A. 1998. Developmental expression and substrate specificities of alfalfa caffeic acid 3-O-methyltransferase and caffeoyl coenzyme A 3-O-methyltransferase in relation to lignification. Plant Physiol. 11: 761–770.Google Scholar
  138. Iqbal, M. and Ghouse, A.H.M. 1990. Cambial concept and organisation. In: M. Iqbal (Ed.) The Vascular Cambium (Research Studies in Botany and Related Applied Fields, vol. 7), Research Studies Press, Taunton, USA, pp. 1–36.Google Scholar
  139. Jones, J.K.N., Purves, C.B. and Timell, T.E. 1961. Constitution of a 4-O-methylglucuronoxylan from the wood of trembling aspen (Populus tremuloides Michx.). Can. J. Chem. 39: 1059–1066.Google Scholar
  140. Jones, L., Seymour, G.B. and Knox, J.P. 1997. Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (14)–D-galactan. Plant Physiol.113: 1405–1412.Google Scholar
  141. Joseleau, J.-P. and Ruel, K. 1997. Study of lignification by non-invasive techniques in growing maize internodes. An investigation by Fourier transform infrared cross-polarization-magic angle spinning 13C-nuclear magnetic resonance spectroscopy and immunocytochemical transmission electron microscopy. Plant Physiol. 114: 1123–1133.Google Scholar
  142. Jouanin, L., Goujon, T., de Nadaï, V., Martin, M.-T., Mila, I., Vallet, C., Pollet, B., Yoshinaga, A., Chabbert, B., Petit-Conil, M. and Lapierre, C. 2000. Lignification in transgenic poplars with extremely reduced caffeic acid O-methyltransferase activity. Plant Physiol. 123: 1363–1373.Google Scholar
  143. Jung, H.-J.G., Ni, W., Chapple, C.C.S. and Meyer, K. 1999. Impact of lignin composition on cell-wall degradability in an Arabidopsis mutant. J. Sci. Food Agric. 79: 922–928.Google Scholar
  144. Kaeiser, M. 1955. Frequency and distribution of gelatinous fibers in eastern cottonwood. Am. J. Bot. 42: 331–334.Google Scholar
  145. Kaeiser M. 1964. Vascular cambial initials in Eastern cottonwood in relation to mature wood cells derived from them. Trans. Ill. Acad. Sci. 57: 182–184.Google Scholar
  146. Kaeiser, M. and Stewart, K.D. 1955. Fiber size in Populus deltoides Marsh in relation to lean of trunk and position in trunk. Bull. Torrey Bot. Club 82: 57–61.Google Scholar
  147. Kakegawa, K., Edashige, Y. and Ishii, T. 2000. Metabolism of cell wall polysaccharides in cell suspension cultures of Populus alba in relation to cell growth. Physiol. Plant. 108: 420–425.Google Scholar
  148. Kawamata, S., Shimoharai, K., Imura, Y., Ozaki, M., Ichinose, Y., Shiraishi, T., Kunoh, H. and Yamada, T. 1997. Temporal and spatial pattern of expression of the pea phenylalanine ammonialyase gene1 promoter in transgenic tobacco. Plant Cell Physiol. 38: 792–803.Google Scholar
  149. Kawaoka, A., Kaothien, P., Yoshida, K., Endo, S., Yamada, K. and Ebinuma, H. 2000. Functional analysis of tobacco LIM protein Ntlim1 involved in lignin biosynthesis. Plant J. 22: 289–301.Google Scholar
  150. Kim, M.-S., Klopfenstein, N.B. and Chun, Y.W. 1997. Agrobacterium-mediated transformation of Populus species. In: N.B. Klopfenstein, Y.W. Chun, M.-S. Kim and M.R. Ahuja (Eds.) Micropropagation, Genetic Engineering, and Molecular Biology of Populus (General Technical Report RM-GTR-297), Rocky Mountain Forest and Range Experiment Station,Fort Collins, USA, pp. 51–59.Google Scholar
  151. Kim, H., Ralph, J., Yahiaoui, N., Pean, M. and Boudet, A.-M. 2000. Cross-coupling of hydroxycinnamyl aldehydes into lignins. Org. Lett. 2: 2197–2200.Google Scholar
  152. Kimura, S., Laosinchai, W., Itoh, T., Cui, X., Linder, C.R. and Brown, R.M. Jr. 1999. Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. Plant Cell 11: 2075–2085.Google Scholar
  153. Klee, H.J., Horsch, R.B., Hinchee, M.A., Hein, M.B., and Hoffmann, 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
  154. Klekowski, E.J. and Godfrey, P.J. 1989. Ageing and mutation in plants. Nature 340: 389–391.Google Scholar
  155. Klopfenstein, N.B., Chun, Y.W., Kim, M.-S. and Ahuja, M.R. 1997. Micropropagation, Genetic Engineering, and Molecular Biology of Populus (General Technical Report RM-GTR-297), Rocky Mountain Forest and Range Experiment Station, Fort Collins, USA.Google Scholar
  156. Knox, J.P. 1997. The use of antibodies to study the architecture and developmental regulation of plant cell walls. Int. Rev. Cytol. 171: 79–120.Google Scholar
  157. Knox, J.P., Linstead, P.J., King, J., Cooper, C. and Roberts, K. 1990. Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta 181: 512–521.Google Scholar
  158. Koopmann, E., Logemann, E. and Hahlbrock, K. 1999. Regulation and functional expression of cinnamate 4-hydroxylase from parsley. Plant Physiol. 119: 49–55.Google Scholar
  159. Kroll, R.E., Ritter, D.C., Gertjejansen, R.O. and Au, K.C. 1992. Anatomical and physical properties of balsam poplar (Populus balsamifera L.) in Minnesota. Wood Fiber Sci. 24: 13–24.Google Scholar
  160. Lagrimini, L.M. 1991. Wound-induced deposition of polyphenols in transgenic plants overexpressing peroxidase. Plant Physiol. 96: 577–583.Google Scholar
  161. Lagrimini, L.M., Bradford, S. and Rothstein, S. 1990. Peroxidase-induced wilting in transgenic tobacco plants. Plant Cell 2: 7–18.Google Scholar
  162. Lapierre, C., Pollet, B., Petit-Conil, M., Toval, G., Romero, J., Pilate, G., Leplé, J.-C., Boerjan, W., Ferret, V., De Nadai, V. and Jouanin, L. 1999. Structural alterations of lignins in transgenic poplars with depressed cinnamyl alcohol dehydrogenase or caffeic acid O-methyltransferase activity have opposite impact on the efficiency of industrial Kraft pulping. Plant Physiol. 119: 153–163.Google Scholar
  163. Larson, P.R. 1969. Wood formation and the concept of wood quality. Yale Univ. Sch. Forestry Bull. 74: 1–54.Google Scholar
  164. Larson, P.R. 1994. The Vascular Cambium. Springer-Verlag, Berlin.Google Scholar
  165. Li, L., Osakabe, Y., Joshi, C.P. and Chiang, V.L. 1999. Secondary xylem-specific expression of caffeoyl-coenzyme A 3-O-methyltransferase plays an important role in the methylation pathway associated with lignin biosynthesis in loblolly pine. Plant Mol. Biol. 40: 555–565.Google Scholar
  166. Li, L., Popko, J.L., Umezawa, T. and Chiang, V.L. 2000. 5-Hydroxyconiferyl aldehyde modulates enzymatic methylation for syringyl monolignol formation, a new view of monolignol biosynthesis in angiosperms. J. Biol. Chem. 275: 6537–6545.Google Scholar
  167. Liese, W. and Ammer, U. 1958. Investigation on the length of wood fibers in poplars. Holzforschung 11: 69–174.Google Scholar
  168. Little, C.H.A. and Pharis, R.P. 1995. Hormonal control of radial and longitudinal growth in the tree stem. In: B.L. Gartner(Ed.) Plant Stems: Physiology and Functional Morphology (Physiological Ecology Series), Academic Press, San Diego, CA, pp. 281–319.Google Scholar
  169. 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
  170. Loewus, F.A. and Murthy, P.P.N. 2000. myo-Inositol metabolism in plants. Plant Sci. 150: 1–19.Google Scholar
  171. MacKay, J.J., O Malley, D.M., Presnell, T., Booker, F.L., Campbell, M.M., Whetten, R.W. and Sederoff, R.R. 1997. Inheritance, gene expression, and lignin characterization in a mutant pine deficient in cinnamyl alcohol dehydrogenase. Proc. Natl. Acad. Sci. USA 94: 8255–8260.Google Scholar
  172. Marita, J.M., Ralph, J., Hatfield, R.D. and Chapple, C. 1999. NMR characterization of lignins in Arabidopsis altered in the activity of ferulate 5-hydroxylase. Proc. Natl. Acad. Sci. USA 96: 12328–12332.Google Scholar
  173. Martz, F., Maury, S., Pinçon, G. and Legrand, M. 1998. cDNA cloning, substrate specificity and expression study of tobacco caffeoyl-CoA 3-O-methyltransferase, a lignin biosynthetic enzyme. Plant Mol. Biol. 36: 427–437.Google Scholar
  174. Matsui, N., Chen, F., Yasuda, S. and Fukushima, K. 2000. Conversion of guaiacyl to syringyl moieties on the cinnamyl alcohol pathway during the biosynthesis of lignin in angiosperms. Planta 210: 831–835.Google Scholar
  175. Matsumoto, T., Sakai, F. and Hayashi, T. 1997. A xyloglucan-specific endo-1,4-β-glucanase isolated from auxin-treated pea stems. Plant Physiol. 114: 661–667.Google Scholar
  176. Maury, S., Geoffroy, P. and Legrand, M. 1999. Tobacco O-methyltransferases involved in phenylpropanoid metabolism. The different caffeoyl-coenzyme A/5-hydroxyferuloyl-coenzyme A 3/5-O-methyltransferase and caffeic acid/5-hydroxyferulic acid 3/5-O-methyltransferase classes have distinct substrate specificities and expression patterns. Plant Physiol. 121: 215–223.Google Scholar
  177. McCann, M.C. and Roberts, K. 1994. Changes in cell-wall architecture during cell elongation. J. Exp. Bot. 45: 1683–1691.Google Scholar
  178. McDougall, G.J., Morrison, I.M., Stewart, D., Weyers, J.D.B. and Hillman, J.R. 1993. Plant fibres: botany, chemistry and processing for industrial use. J. Sci. Food Agric. 62: 1–20.Google Scholar
  179. McQueen-Mason, S. 1997. Plant cell walls and the control of growth. Biochem. Soc. Trans. 25: 204–214.Google Scholar
  180. Mellerowicz, E.J., Coleman, W.K., Riding, R.T. and Little, C.H.A. 1992. Periodicity of cambial activity in Abies balsamea.I.Effects of temperature and photoperiod on cambial dormancy and frost hardiness. Physiol. Plant. 85: 515–525.Google Scholar
  181. Mellerowicz, E.J., Blomqvist, K., Bourquin, V., Brumer, H., Christiernin, M., Denman, S., Djerbi, S., Eklund, M., Gray-Mitsumine, M., Kallas, Å., Lehtiö, J., Raza, S., Regan, S., Rudsander, U., Sundberg, B. and Teeri, T.T. 2000. Cell wall enzyme discovery using high throughput sequencing and in-depth expression analysis in poplar wood forming tissues. Proceedings of the Symposium on Friendly and Emerging Technologies for a Sustainable Pulp and Paper Industry, Taiwan Research Institute, Taipei, Taiwan, 25–27 April 2000.Google Scholar
  182. Meng, H. and Campbell, W.H. 1998. Substrate profiles and expression of caffeoyl coenzyme A and caffeic acid O-methyltransferases in secondary xylem of aspen during seasonal development. Plant Mol. Biol. 38: 513–520.Google Scholar
  183. Meyer, K., Shirley, A.M., Cusumano, J.C., Bell-Lelong, D.A. and Chapple, C. 1998. Lignin monomer composition is determined by the expression of a cytochrome P450-dependent monooxygenase in Arabidopsis. Proc. Natl. Acad. Sci. USA 95: 6619–6623.Google Scholar
  184. Meyermans, H., Morreel, K., Lapierre, C., Pollet, B., De Bruyn, A., Busson, R., Herdewijn, P., Devreese, B., Van Beeumen, J., Marita, J.M., Ralph, J., Chen, C., Burggraeve, B., Van Montagu, M., Messens, E. and Boerjan, W. 2000. Modification in lignin and accumulation of phenolic glucosides in poplar xylem upon down-regulation of caffeoyl-coenzyme A O-methyltransferase, an enzyme involved in lignin biosynthesis. J. Biol. Chem. 275: 36899–36909.Google Scholar
  185. Micheli, F., Sundberg, B., Goldberg, R. and Richard, L. 2000a. Radial distribution pattern of pectin methylesterases across the cambial region of hybrid aspen at activity and dormancy. Plant Physiol. 124: 191–199.Google Scholar
  186. Micheli, F., Bordenave, M. and Richard, L. 2000b. Pectin methylesterases: possible marker for cambial derivative differentiation. In: R. Savidge, J. Barnett and R. Napier (Eds) Cell and Molecular Biology of Wood Formation, BIOS Scientific Publications, Oxford, pp. 295–304.Google Scholar
  187. Milioni, D., Sado, P-E., Stacey, N. J., Domingo, C., Roberts, K. and McCann, M.C. 2001 Differential expression of cell-wall-related genes during formation of tracheary elements in the Zinnia mesophyll cell system. Plant Mol. Biol., this issue.Google Scholar
  188. Miller, A.R. and Roberts, L.W. 1984. Ethylene biosynthesis and xylogenesis in Lactuca explants cultured in vitro in the presence of auxin and cytokinin: the effect of ethylene precursors and inhibitors. J. Exp. Bot. 35: 691–698.Google Scholar
  189. Monties, B. 1998. Novel structures and properties of lignins in relation to their natural and induced variability in ecotypes, mutants and transgenic plants. Polymer Degrad. Stabil. 59: 53–64.Google Scholar
  190. Moritz, T. and Sundberg, B. 1996. Endogenous cytokinins in the vascular cambial regions of Pinus sylvestris during activity and dormancy. Physiol. Plant. 98: 693–698.Google Scholar
  191. Mueller, S.C. and Brown, R.M. Jr. 1980. Evidence for an in-tramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants. J. Cell. Biol. 84: 315–326.Google Scholar
  192. Murakami, Y., Funada, R., Sano, Y. and Ohtani, J. 1999. The differentiation of contact cells and isolation cells in the xylem ray parenchyma of Populus maximowiczii. Ann. Bot. 84: 429–435.Google Scholar
  193. Nakashima, J., Awano, T., Takabe, K., Fujita, M. and Saiki, H. 1997. Immunocytochemical localization of phenylalanine ammonia-lyase and cinnamyl alcohol dehydrogenase in differentiating tracheary elements derived from Zinnia mesophyll cells. Plant Cell Physiol. 38: 113–123.Google Scholar
  194. Nishitani, K. 1997. The role of endoxyloglucan transferase in the organization of plant cell walls. Int. Rev. Cytol. 173: 157–206.Google Scholar
  195. Nishitani, K. 1998. Construction and restructuring of the cellulose-xyloglucan framework in the apoplast as mediated by the xyloglucan-related protein family: a hypothetical scheme. J. Plant Res. 111: 159–166.Google Scholar
  196. Nobushi, T. and Fujitta, M. 1972. Cytological structure of differentiating tension wood fibres of Populus euroamericana. Mokuzai Gakkaishi 18: 137–144.Google Scholar
  197. Norberg, P.H. and Meier, H. 1966. Physical and chemical properties of the gelatinous layer in tension wood fibers of aspen (Populus tremula L.). Holzforschung 20: 174–178.Google Scholar
  198. Northcote, D.H. 1972. Chemistry of the plant cell wall. Annu. Rev. Plant Physiol. 23: 113–132.Google Scholar
  199. Northcote, D.H. 1989. Control of plant cell wall biosynthesis: an overview. In: N.G. Lewis, and M.G. Paice (Eds.) Plant Cell Wall Polymers (ACS Symposium Series vol. 399), American Chemical Society, Washington, DC, pp. 1–15.Google Scholar
  200. Northcote, D.H., Davey, R. and Lay, J. 1989. Use of antisera to localize callose, xylan and arabinogalactan in the cell-plate, primary and secondary walls of plant cells. Planta 178: 353–366.Google Scholar
  201. Ohmiya, Y., Samejima, M., Shiroishi, M., Amano, Y., Kanda, T., Sakai, F. and Hayashi, T. 2000. Evidence that endo-1,4-β-glucanases act on cellulose in suspension-cultured poplar cells. Plant J. 24: 147–158.Google Scholar
  202. Ohta, S. 1979. Tension wood from stems of poplar (Populus euroamericana) with various degree of leaning. Mokuzai Gakkaishi 25: 610–614.Google Scholar
  203. Olsson, O. and Little, C.H.A. 2000. Molecular control of the development and function of the vascular cambium. In: S.M. Jain, and S.C. Minocha (Eds.) Molecular Biology of Woody Plants, vol. 1 (Forestry Sciences vol. 64), Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 155–180.Google Scholar
  204. Osakabe, K., Tsao, C.C., Li, L., Popko, J.L., Umezawa, T., Carraway, D.T., Smeltzer, R.H., Joshi, C.P. and Chiang, V.L. 1999. Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms. Proc. Natl. Acad. Sci. USA 96: 8955–8960.Google Scholar
  205. Panshin, A.J. and de Zeeuw, C. 1980. Textbook of Wood Technology. McGraw-Hill, New York.Google Scholar
  206. Parresol, B.R. and Cao, F. 1998. An investigation of crystalline intensity of the wood of poplar clones grown in Jiangsu Province, China. Research Paper, Southern Research Station, USDA Forest Service, No. SRS-11, 7 pp.Google Scholar
  207. Perrin, R.M., DeRocher, A.E., Bar-Peled, M., Zeng, W., Norambuena, L., Orellana, A., Raikhel, N.V. and Keegstra, K. 1999. Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science 284: 1976–1979.Google Scholar
  208. Perri, R., Wilkerson, C. and Keegstra, K. 2001. Golgi enzymes that synthesize plant cell wall polysaccharides: finding and evaluating candidates in the genomic era. Plant Mol. Biol. 47: 109–124.Google Scholar
  209. Phillips, R. and Arnott, S.M. 1983. Studies on induced tracheary element differentiation in cultured tissues of tubers of the Jerusalem artichoke, Helianthus tuberosus. Histochem. J. 15: 427–436.Google Scholar
  210. Piquemal, J., Lapierre, C., Myton, K., O'Connell, A., Schuch, W., Grima-Pettenati, J. and Boudet, A.-M. 1998. Down-regulation in cinnamoyl-CoA reductase induces significant changes of lignin profiles in transgenic tobacco plants. Plant J. 13: 71–83.Google Scholar
  211. Piro, G., Zuppa, A., Dalessandro, G. and Northcote, D.H. 1993. Glucomannan synthesis in pea epicotyls: the mannose and glucose transferases. Planta 190: 206–220.Google Scholar
  212. Plomion, C., Pionneau, C., Brach, J., Costa, P. and Baillères, H. 2000. Compression wood-responsive proteins in developing xylem of maritime pine (Pinus pinaster Ait.). Plant Physiol. 123: 959–969.Google Scholar
  213. Potikha, T.S., Collins, C.C., Johnson, D.I., Delmer, D.P. and Levine, A. 1999. The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol. 119: 849–858.Google Scholar
  214. Prodhan, A.K.M.A., Funada, R., Ohtani, J., Abe, H. and Fukazawa, K. 1995. Orientation of microfibrils and microtubules in developing tension-wood fibres of Japanese ash (Fraxinus mandshurica var. japonica). Planta 196: 577–585.Google Scholar
  215. Puhlmann, J., Bucheli, E., Swain, M.J., Dunning, N., Albersheim, P., Darvill, A.G. and Hahn, M.G. 1994. Generation of monoclonal antibodies against plant cell-wall polysaccharides. I. Characterization of a monoclonal antibody to a terminal α-( 1→2)-linked fucosyl-containing epitope. Plant Physiol. 104: 699–710.Google Scholar
  216. Rajagopal, J., Das, S., Khurana, D.K., Srivastava, P.S. and Lakshmikumaran, M. 1999. Molecular characterization and distribution of a 145-bp tandem repeat family in the genus Populus. Genome 42: 909–918.Google Scholar
  217. Ralph, J., Lapierre, C., Lu, F., Marita, J.M., Van Doorsselaere, J., Pilate, G., Boerjan, W. and Jouanin, L. 2001. NMR evidence for benzodioxane structures resulting from incorporation of 5-hydroxyconiferyl alcohol into lignins of O-methyltransferase-deficient poplars. J. Agric. Food Chem. 49: 86–91.Google Scholar
  218. Ranocha, P., Goffner, D. and Boudet, A.M. 2000. Plant laccases: are they involved in lignification. In: R. Savidge, J. Barnett, and R. Napier (Eds.) Cell and Molecular Biology of Wood Formation, BIOS Scientific Publications, Oxford, pp. 397–410.Google Scholar
  219. Rasmussen, S. and Dixon, R.A. 1999. Transgene-mediated and elicitor-induced perturbation of metabolic channeling at the entry point into the phenylpropanoid pathway. Plant Cell 11: 1537–1551.Google Scholar
  220. Regan, S., Bourquin, V., Tuominen, H., Sundberg, B. 1999. Accurate and high resolution in situ hybridization analysis of gene expression in secondary stem tissues. Plant J. 19: 363–369.Google Scholar
  221. Reis, D., Vian, B. and Roland, J.C. 1994. Cellulose-glucuronoxylans and plant-cell wall structure. Micron 25: 171–187.Google Scholar
  222. Reiter, W.-D. and Vanzin, G. 2001. Molecular genetics of nucleotide sugar interconversion pathways. Plant Mol. Biol., this issue.Google Scholar
  223. Ren, C. and Kermode, A.R. 2000. An increase in pectin methyl esterase activity accompanies dormancy breakage and germination of yellow cedar seeds. Plant Physiol. 124: 231–242.Google Scholar
  224. Richmond, T.A. and Somerville, C.R. 2001. Integrative approaches to determining Csl function. Plant Mol. Biol., this issue.Google Scholar
  225. Riding, R.T. and Little, C.H.A. 1984. Anatomy and histochemistry of Abies balsamea cambial zone cells during the onset and breaking of dormancy. Can. J. Bot. 62: 2571–2579.Google Scholar
  226. Roberts, L.W. 1988. Hormonal aspects of vascular differentiation In: Vascular Differentiation and Plant Growth Regulators, Springer-Verlag, Berlin, pp. 22–38.Google Scholar
  227. Roland, J.C. 1978. Early differences between radial walls and tangential walls of actively growing cambial zone. IAWA Bull. 1978: 7–10.Google Scholar
  228. Saka, S. and Goring, D.A.I. 1985. Localization of lignins in wood cell walls. In: T. Higuchi (Ed.) Biosynthesis and Biodegradation of Wood Components, Academic Press, Orlando, FL, pp. 51–62.Google Scholar
  229. Samaj, J., Hawkins, S., Lauvergeat, V., Grima-Pettenati, J. and Boudet, A. 1998. Immunolocalization of cinnamyl alcohol dehydrogenase 2 (CAD 2) indicates a good correlation with cell-specific activity of CAD 2 promoter in transgenic poplar shoots. Planta 204: 437–443.Google Scholar
  230. Samuels, A.L., Giddings, T.H. Jr and Staehelin, L.A. 1995. Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J. Cell Biol. 130: 1345–1357.Google Scholar
  231. Sauter, J.J. 2000. Photosynthate allocation to the vascular cambium: facts and problems. In: R. Savidge, J. Barnett and R. Napier (Eds) Cell and Molecular Biology of Wood Formation, BIOS Scientific Publications, Oxford, pp. 71–83.Google Scholar
  232. 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
  233. Savidge, R.A. 2000. Biochemistry of seasonal cambial growth and wood formation: an overview of the challenges. In: R. Savidge, J. Barnett and R. Napier (Eds) Cell and Molecular Biology of Wood Formation, BIOS Scientific Publications, Oxford, pp. 1–30.Google Scholar
  234. Saxena, I.M. and Brown, R.M. Jr. 1999. Are the reversibly glycosylated polypeptides implicated in plant cell wall biosynthesis non-processive β-glycosyltransferases? Trends Plant Sci. 4: 6–7.Google Scholar
  235. Sederoff, R.R., MacKay, J.J., Ralph, J. and Hatfield, R.D. 1999. Unexpected variation in lignin. Curr. Opin. Plant Biol. 2: 145–152.Google Scholar
  236. Seitz, B., Klos, C., Wurm, M. and Tenhaken, R. 2000. Matrix polysaccharide precursors in Arabidopsis cell walls are synthesized by alternate pathways with organ-specific expression patterns. Plant J. 21: 537–546.Google Scholar
  237. Sewalt, V.J.H., Ni, W., Blount, J.W., Jung, H.G., Masoud, S.A., Howles, P.A., Lamb, C. and Dixon, R.A. 1997. Reduced lignin content and altered lignin composition in transgenic tobacco down-regulated in expression of L-phenylalanine ammonialyase or cinnamate 4-hydroxylase. Plant Physiol. 115: 41–50.Google Scholar
  238. Shani, Z., Dekel, M., Tsabary, G., Jensen, C.S., Tzfira, T., Goren, R., Altman, A. and Shoseyov, O. 1999. Expression of Arabidopsis thaliana, endo-1,4-β-glucanase (cel1) in transgenic poplar plants. In: A. Altman, M. Ziv, and S. Izhar (Eds.) Plant Biotechnology and In Vitro Biology in the 21st Century Current Plant Science and Biotechnology in Agriculture vol. 36, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 209–212.Google Scholar
  239. Sheen, J., Zhou, L. and Jang, J.-C. 1999. Sugars as signaling molecules. Curr. Opin. Plant Biol. 2: 410–418.Google Scholar
  240. 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
  241. Shimizu, Y., Aotsuka, S., Hasegawa, O., Kawada, T., Sakuno, T., Sakai, F. and Hayashi T. 1997. Changes in levels of mRNAs for cell wall-related enzymes in growing cotton fiber cells. Plant Cell Physiol. 38: 375–378.Google Scholar
  242. Simson, B.W. and Timell, T.E. 1978a. Polysaccharides in cambial tissues of Populus tremuloides and Tilia americana. 1. Isolation, fractionation, and chemical composition of the cambial tissues. Cell. Chem. Technol. 12: 39–50.Google Scholar
  243. Simson, B.W. and Timell, T.E. 1978b. Polysaccharides in cambial tissues of Populus tremuloides and Tilia americana. II. Isolation and structure of a xyloglucan. Cell. Chem. Technol. 12: 51–62.Google Scholar
  244. Simson, B.W. and Timell, T.E. 1978c. Polysaccharides in cambial tissues of Populus tremuloides and Tilia americana.IV. 4-O-methylglucuronoxylan and pectin. Cell. Chem. Technol. 12: 79–84.Google Scholar
  245. Simson, B.W. and Timell, T.E. 1978d. Polysaccharides in cambial tissues of Populus tremuloides and Tilia americana. V. Cellulose. Cell. Chem. Technol. 12: 137–141.Google Scholar
  246. Sinnott, E.W. and Bloch, R. 1940. Cytoplasmic behaviour during division of vacuolate plant cells. Proc. Natl. Acad. Sci. USA 26: 223–227.Google Scholar
  247. Sitbon, F., Hennion, S., Sundberg, B., Little, C.H.A., Olsson, O. and Sandberg, G. 1992. 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
  248. 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 Sci. 141: 165–173.Google Scholar
  249. Smith, C.G., Rodgers, M.W., Zimmerlin, A., Ferdinando, D. and Bolwell, G.P. 1994. Tissue and subcellular immunolocalisation of enzymes of lignin synthesis in differentiating and wounded hypocotyl tissue of French beans (Phaseolus vulgaris L.). Planta 192: 155–164.Google Scholar
  250. Sonobe, S., Nakayama, N., Shimmen, T. and Sone, Y. 2000. Intracellular distribution of subcellular organelles revealed by antibody against xyloglucan during cell cycle in tobacco BY-2 cells. Protoplasma 213: 218–227.Google Scholar
  251. Stacey, N.J., Roberts, K., Carpita, N.C., Wells, B. and McCann, M.C. 1995. Dynamic changes in cell surface molecules are very early events in the differentiation of mesophyll cells from Zinnia elegans into tracheary elements. Plant J. 8: 891–906.Google Scholar
  252. Stafford, H.A. 1981. Phenylalanine ammonia-lyase. In: E.E. Conn (Ed.) Secondary Plant Products (The Biochemistry of Plants vol. 7), Academic Press, New York, pp. 117–137.Google Scholar
  253. Sterky, F., Regan, S., Karlsson, J., Hertzberg, M., Rohde, A., Holmberg, A., Amini, B., Bhalerao, R., Larsson, M., Villarroel, R., Van Montagu, M., Sandberg, G., Olsson, O., Teeri, T.T., Boerjan, W., Gustafsson, P., Uhlén, M., Sundberg, B. and Lundeberg, J. 1998a. Gene discovery in the wood-forming tissues of poplar: analysis of 5692 expressed sequence tags. Proc. Natl. Acad. Sci. USA 95: 13330–13335.Google Scholar
  254. Sterky, F., Sievertzon, M. and Kleczkowski, L.A. 1998b. Molecular cloning of a cDNA encoding a cytosolic form of phosphoglu-comutase (Accession No. AF097938) from cambium of poplar (PGR 98–205). Plant Physiol. 118: 1535.Google Scholar
  255. Sultze, R.F. 1957. A study of the developing tissues of aspen wood. TAPPI 40: 985–994.Google Scholar
  256. 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.Google Scholar
  257. Sundberg, B., Uggla, C. and Tuominen H. 2000. Auxin gradients and cambial growth. In: R. Savidge, J. Barnett and R. Napier (Eds.) Cell and Molecular Biology of Wood Formation (SEB Experimental Biology Reviews), BIOS, Oxford, pp. 169–188.Google Scholar
  258. Sussex, I.M., Clutter, M.E. and Goldsmith, M.H.M. 1972. Wound recovery by pith cell redifferentiation: structural changes. Am. J. Bot. 59: 797–804.Google Scholar
  259. Suzuki, K., Ingold, E., Sugiyama, M. and Komamine, A. 1991. Xylan synthase activity in isolated mesophyll cells of Zinnia elegans during differentiation to tracheary elements. Plant Cell Physiol. 32: 303–306.Google Scholar
  260. Takabe, K., Miyauchi, S., Tsunoda, R. and Fukazawa, K. 1992. Distribution of guaiacyl and syringyl lignins in Japanese beech (Fagus crenata): variation within an annual ring. IAWA Bull. 13: 105–112.Google Scholar
  261. Takeda, T., Mitsuishi, Y., Sakai, F. and Hayashi, T. 1996. Xyloglucan endotransglycosylation in suspension-cultured poplar cells. Biosci. Biotech. Biochem. 60: 1950–1955.Google Scholar
  262. Tamagnone, L., Merida, A., Parr, A., Mackay, S., Culianez-Macia, F.A., Roberts, K. and Martin, C. 1998. The AmMYB308 and AmMYB330 transcription factors from Antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. Plant Cell 10: 135–154.Google Scholar
  263. Taylor, J.G. and Haigler, C.H. 1993. Patterned secondary cell-wall assembly in tracheary elements occurs in a self-perpetuating cascade. Acta Bot. Neerl. 42: 153–163.Google Scholar
  264. Taylor, N.G., Scheible, W.-R., Cutler, S., Somerville, C.R. and Turner, S.R. 1999. The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11: 769–779.Google Scholar
  265. Tenhaken, R. and Thulke, O. 1996. Cloning of an enzyme that synthesizes a key nucleotide-sugar precursor of hemicellulose biosynthesis from soybean: UDP-glucose dehydrogenase. Plant Physiol. 112: 1127–1134.Google Scholar
  266. Terashima, N., Okada, M. and Tomimura, Y. 1979. Heterogeneity in formation of lignin. I. Heterogeneous incorporation of p-hydroxybenzoic acid into poplar lignin. Mokuzai Gakkaishi 25: 422–426.Google Scholar
  267. Terashima, N., Fukushima, K., He, L.F. and Takabe, K. 1993. Comprehensive model of the lignified plant cell wall. In: H.G. Jung (Ed.) Forage Cell Wall Structure and Digestibility, ASA-CSSA-SSSA, Madison, WI, pp. 247–270.Google Scholar
  268. Thompson, J.E. and Fry, S.C. 2000. Evidence for covalent linkage between xyloglucan and acidic pectins in suspension-cultured rose cells. Planta 211: 275–286.Google Scholar
  269. Tognolli, M., Overney, S., Penel, C., Greppin, H. and Simon, P. 2000. A genetic and enzymatic survey of Arabidopsis thaliana peroxidases. Plant Peroxidase Newsl. 14: 3–12.Google Scholar
  270. Torki, M., Mandaron, P., Mache, R. and Falconet, D. 2000. Characterization of a ubiquitous expressed gene family encoding polygalacturonase in Arabidopsis thaliana. Gene 242: 427–436.Google Scholar
  271. Torrey, J.G., Fosket, D.E. and Hepler, P.K. 1971. Xylem formation: a paradigm of cytodifferentiation in higher plants. Am. Scient. 59: 338–352.Google Scholar
  272. Tsai, C.-J., Popko, J.L., Mielke, M.R., Hu, W.-J., Podila, G.K. and Chiang, V.L. 1998. Suppression of O-methyltransferase gene by homologous sense transgene in quaking aspen causes red-brown wood phenotypes. Plant Physiol. 117: 101–112.Google Scholar
  273. Tuominen, H., Sitbon, F., Jacobsson, C., Sandberg, G., Olsson, O. and 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.Google Scholar
  274. Tuominen, H., Puech, L., Fink, S. and Sundberg, B. 1997. A radial concentration gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen. Plant Physiol. 115: 577–585.Google Scholar
  275. Tuominen, H., Olsson, O. and Sundberg, B. 2000a. Genetic engineering of wood formation. Expression of bacterial IAA-biosynthetic genes in hybrid aspen (Populus tremula ×P. tremuloides. In: S.M. Jain and S.C. Minocha (Eds.) Molecular Biology of Woody Plants, vol. 1 (Forestry Sciences vol. 64), Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 181–203.Google Scholar
  276. Tuominen, H., Puech, L., Regan, S., Fink, S., Olsson, O. and Sundberg, B. 2000b. Cambial-region-specific expression of the Agrobacterium iaa genes in transgenic aspen visualized by a linked uidA reporter gene. Plant Physiol. 123: 531–541.Google Scholar
  277. Turner, S.R. and Somerville, C.R. 1997. Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9: 689–701.Google Scholar
  278. Turner, S., Taylor, N. and Jones, L. 2001. Mutations of the secondary wall. Plant Mol Biol, this issue.Google Scholar
  279. Tuskan, G., West, D., Bradshaw, H.D., Neale, D., Sewell, M., Wheeler, N., Megraw, B., Jech, K., Wiselogel, A., Evans, R., Elam, C., Davis, M. and Dinus, R. 1999. Two high-throughput techniques for determining wood properties as part of a molecular genetics analysis of hybrid poplar and loblolly pine. Appl. Biochem. Biotech. 77: 55–65.Google Scholar
  280. Uggla, C. and Sundberg, B., 2001. Sampling of cambial region tissues for high resolution analysis. In: N.J. Chaffey (Ed.) Wood formation in Trees: Cell and Molecular Biology Techniques, Harwood Academic Publishers, in press.Google Scholar
  281. 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.Google Scholar
  282. 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.Google Scholar
  283. Uggla, C., Magel, E., Moritz, T. and Sundberg, B. 2001. Function and dynamics of auxin and carbohydrates during early-wood/ latewood transition in Pinus sylvestris. Plant Physiol., in press.Google Scholar
  284. Valster, A.H., Hepler, P.K. and Chernoff, J. 2000. Plant GTPases: the Rhos in bloom. Trends Cell Biol. 10: 141–146.Google Scholar
  285. Vander Mijnsbrugge, K., Meyermans, H., Van Montagu, M., Bauw, G. and Boerjan, W. 2000. Wood formation in poplar: identification, characterization, and seasonal variation of xylem proteins. Planta 210: 589–598.Google Scholar
  286. Van Doorsselaere, J., Baucher, M., Chognot, E., Chabbert, B., Tollier, M.-T., Petit-Conil, M., Leplé, J.-C., Pilate, G., Cornu, D., Monties, B., Van Montagu, M., Inzé, D., Boerjan, W. and Jouanin, L. 1995. A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic acid O-methyltransferase activity. Plant J. 8: 855–864.Google Scholar
  287. Vaughn, K.C., Hoffman, J.C., Hahn, M.G. and Staehelin, L.A. 1996. The herbicide dichlobenil disrupts cell plate formation: immunogold characterization. Protoplasma 194: 117–132.Google Scholar
  288. Vian, B., Roland, J.C., Reis, D. and Mosiniak, M. 1992. Distribution and possible morphogenetic role of the xylans within the secondary vessel wall of linden wood. IAWA Bull. 13: 269–282.Google Scholar
  289. Vietor, R.J., Renard, C.M.G.C., Goldberg, R. and Catesson, A.M. 1995. Cell-wall polysaccharides in growing poplar bark tissue. Int. J. Biol. Micromol. 17: 341–344.Google Scholar
  290. Wang, J. and Hall, R. 1995. Comparison of DNA content and chromosome numbers in species and clones of poplar. Abstract presented at the International Poplar Symposium (Seattle, WA, 20–25 August 1995), p. 93.Google Scholar
  291. Wang, Q., Little, C.H.A. and Oden, P.C. 1997. Control of longitudinal and cambial growth by gibberellins and indole-3-acetic acid in current-year shoots of Pinus sylvestris. Tree Physiol. 17: 715–721.Google Scholar
  292. Warren Wilson, J. and Warren Wilson, P.M. 1984. Control of tissue patterns in normal development and in regeneration. In: P. Barlow and D. Carr (Eds.) Positional Controls in Plant Development. Cambridge University Press, Cambridge, UK, pp. 225–280.Google Scholar
  293. Watanabe, Y., Fukazawa, K., Kojima, Y., Funada, R., Ona, T. and Asada, T. 1997. Histochemical study on heterogeneity of lignin in Eucalyptus species. 1. Effects of polyphenols. Mokuzai Gakkaishi 43: 102–107.Google Scholar
  294. Wenham, M.W. and Cusick, F. 1975. The growth of secondary fibers. New Phytol. 74: 247–261.Google Scholar
  295. Whetten, R.W., MacKay, J.J. and Sederoff, R.R. 1998. Recent advances in understanding lignin biosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 585–609.Google Scholar
  296. Whitmore, F.W. and Zahner, R. 1966. Development of the xylem ring in stems of young red pine trees. Forestry Sci. 12: 198–210.Google Scholar
  297. Whitney, S.E.C., Gothard, M.G.E., Mitchell, J.T. and Gidley, M.J. 1999. Roles of cellulose and xyloglucan in determining the mechanical properties of primary plant cell walls. Plant Physiol. 121: 657–663.Google Scholar
  298. Willats, W.G.T., Marcus, S.E. and Knox, J.P. 1998. Generation of a monoclonal antibody specific to (15)-α-Larabinan. Carbohydrate Res. 308: 149–152.Google Scholar
  299. Willats, W.G.T., Steele-King, C.G., Marcus, S.E. and Knox, J.P. 1999. Side chains of pectic polysaccharides are regulated in relation to cell proliferation and cell differentiation. Plant J. 20: 619–628.Google Scholar
  300. Willats, W.G.T., McCartney, L., Mackie, W. and Knox, J.P. 2001. Pectin: Cell biology and prospects for the functional analysis. Plant Mol. Biol., this issue.Google Scholar
  301. Wilson, B.F. 1964. A model for cell production by the cambium in conifers. In: M.H. Zimmerman (Ed.) The Formation of Wood in Forest Trees, Academic Press, New York, pp. 19–36.Google Scholar
  302. Winter, H. and Huber, S.C. 2000. Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit. Rev. Plant Sci. 19: 31–67.Google Scholar
  303. Wloch, W. and Polap, E. 1994. The intrusive growth of initial cells in re-arrangement of cells in cambium of Tilia cordata Mill. Acta Soc. Bot. Pol. 63: 109–116.Google Scholar
  304. Wojtaszek, P. and Bolwell, G.P. 1995. Secondary cell-wall-specific glycoproteins(s) from French bean hypocotyls. Plant Physiol. 108: 1001–1012.Google Scholar
  305. Wu, L.R. 1998. Genetic mapping of QTLs affecting tree growth and architecture in Populus: implication for ideotype breeding. Theor. Appl. Genet. 96: 447–457.Google Scholar
  306. Wu, R. and Stettler, R.F. 1994. Quantitative genetics of growth and development in Populus. I. A three-generation comparison of tree architecture during the first 2 years of growth. Theor. Appl. Genet. 89: 1046–1054.Google Scholar
  307. Wu, R. and Stettler, R.F. 1997. Quantitative genetics of growth and development in Populus. II. The partitioning of genotype x environment interaction in stem growth. Heredity 78: 124–134.Google Scholar
  308. Wu, R., Bradshaw, H.D. Jr. and Stettler, R.F. 1997. Molecular genetics of growth and development in Populus (Salicaceae). V. Mapping quantitative trait loci affecting leaf variation. Am. J. Bot. 84: 143–153.Google Scholar
  309. Wu, R., Bradshaw, H.D. Jr. and Stettler, R.F. 1998. Developmental quantitative genetics of growth in Populus. Theor. Appl. Genet. 97: 1110–1119.Google Scholar
  310. Wu, L., Joshi, C.P. and Chiang, V.L. 2000. A xylem-specific cellulose synthase gene from aspen (Populus tremuloides) is responsive to mechanical stress. Plant J. 22: 495–502.Google Scholar
  311. Wulff, C., Norambuena, L. and Orellana, A. 2000. GDP-fucose uptake into the Golgi apparatus during xyloglucan biosynthesis requires the activity of a transporter-like protein other than the UDP-glucose transporter. Plant Physiol. 122: 867–877.Google Scholar
  312. Yahiaoui, N., Marque, C., Myton, K.E., Negrel, J. and Boudet, A.M. 1998. Impact of different levels of cinnamyl alcohol dehydrogenase down-regulation on lignins of transgenic tobacco plants. Planta 204: 8–15.Google Scholar
  313. Yang, K.C. 1978. The fine structue of pits in yellow birch (Betula alleghaniensis Britton). IAWA Bull. 1978: 71–77.Google Scholar
  314. Ye, Z.-H. 1997. Association of caffeoyl coenzyme A 3-O-methyltransferase expression with lignifying tissues in several dicot plants. Plant Physiol. 115: 1341–1350.Google Scholar
  315. Yin, T.M., Huang, M.R., Wang, M.X., Zhu, L.H., He, P. and Zhai, W.X. 1999. RAPD linkage mapping in a Populus adenopoda ×P. alba F-1 family. Acta Bot. Sin. 41: 956–961.Google Scholar
  316. Yoshinaga, A., Fujita, M. and Saiki, H. 1993. Compositions of lignin building units and neutral sugars in oak xylem tissue. Mokuzai Gakkaishi 39: 621–627.Google Scholar
  317. Yoshinaga, A., Fujita, M. and Saiki, H. 1997a. Cellular distribution of guaiacyl and syringyl lignins within an annual ring in oak wood. Mokuzai Gakkaishi 43: 384–390.Google Scholar
  318. Yoshinaga„ A., Fujita, M. and Saiki, H. 1997b. Secondary wall thickening and lignification of oak xylem components during latewood formation. Mokuzai Gakkaishi 43: 377–383.Google Scholar
  319. Zablackis, E., York, W.S., Pauly, M., Hantus, S., Reiter, W.-D., Chapple, C.C.S., Albersheim, P. and Darvill, A. 1996. Substitution of L-fucose by L-galactose in cell walls of Arabidopsis mur1. Science 272: 1808–1810.Google Scholar
  320. 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
  321. Zhang, G.F. and Staehelin, L.A. 1992. Functional compartmentation of the Golgi apparatus of plant cells. Immunocytochemical analysis of high-pressure frozen-and freeze-substituted sycamore maple suspension culture cells. Plant Physiol. 99: 1070–1083.Google Scholar
  322. Zheng, Z.-L. and Yang, Z. 2000. The Rop GTPase switch turns on polar growth in pollen. Trends Plant Sci. 5: 298–303.Google Scholar
  323. Zhong, R. and Ye, Z.-H. 1999. IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell 11: 2139–2152.Google Scholar
  324. Zhong, R., Morrison, W.H. III, Negrel, J. and Ye, Z.-H. 1998. Dual methylation pathways in lignin biosynthesis. Plant Cell 10: 2033–2046.Google Scholar
  325. Zhong, R., Ripperger, A. and Ye, Z.-H. 2000. Ectopic deposition of lignin in the pith of stems of two Arabidopsis mutants. Plant Physiol. 123: 59–69.Google Scholar
  326. Zobel, B.J. and van Buijtenen, J.P. 1989. Wood Variation: Its Causes and Control. Springer-Verlag, New York.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Ewa J. Mellerowicz
    • 1
  • Marie Baucher
    • 2
  • Björn Sundberg
    • 1
  • Wout Boerjan
    • 3
  1. 1.Department of Forest Genetics and Plant PhysiologySwedish University of Agricultural SciencesUmeåSweden
  2. 2.Laboratory of Plant BiotechnologyFree University of Brussels (ULB)BrusselsBelgium
  3. 3.Department of Plant Genetics, Flanders Interuniversity Institute for Biotechnology (VIB)Ghent UniversityGentBelgium

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