Advertisement

Xylem Development in Trees: From Cambial Divisions to Mature Wood Cells

  • Jörg FrommEmail author
Chapter
Part of the Plant Cell Monographs book series (CELLMONO, volume 20)

Abstract

As one of the major parts of the biosphere, trees will play a significant role in the near future because of an increasing demand for wood as the most important natural raw material. Wood is generated by the vascular cambium and enables water transportation as well as providing mechanical support to the tree. Furthermore, it is the main renewable source for paper, buildings, furniture, boards and fuel. In recent decades intriguing developments in cell, molecular and structural biology have led to an integrated view of wood formation, from its start in the cambium by cell division, via cell expansion and cell wall thickening, to programmed cell death. These complex processes involve the interaction of both exogenous factors, such as photoperiod and temperature, and endogenous regulators, such as phytohormones. In addition, the coordinated expression of the numerous genes implicated in the biosynthesis of the major wood components—cellulose, hemicelluloses and lignin—drives the ordered development of wood. The huge amount of literature in the different fields of wood formation cannot be reviewed here in detail; rather, the aim of this chapter is to give a brief overview of the essential steps leading to mature wood cells, with an emphasis on current progress obtained by modern techniques which have increased our understanding of wood formation.

Keywords

Secondary Wall Cellulose Microfibril Wood Formation Vessel Element Cambial Activity 
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.

References

  1. Abbe LB, Crafts AS (1939) Phloem of white pine and other coniferous species. Bot Gaz 100:695–722Google Scholar
  2. Ache P, Fromm J, Hedrich R (2010) Potassium-dependent wood formation in poplar: seasonal aspects and environmental limitations. Plant Biol 12:259–267PubMedGoogle Scholar
  3. Allona I, Quinn M, Shoop E, Swope K, St. Cyr S, Carlis J, Riedl J, Retzel E, Campbell MM, Sederoff R, Whetten RW (1998) Analysis of xylem formation in pine by cDNA sequencing. Proc Natl Acad Sci USA 95:9693–9698PubMedGoogle Scholar
  4. Alves ES, Angyalossy-Alfonso V (2000) Ecological trends in the wood anatomy of some Brazilian species. 1. Growth rings and vessels. IAWA J 21:3–30Google Scholar
  5. Arend M, Fromm J (2000) Seasonal variation in the K, Ca and P content and distribution of plasma membrane H+-ATPase in the cambium of Populus trichocarpa. In: Savidge RA, Barnett JR, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers, Oxford, pp 67–70Google Scholar
  6. Arend M, Fromm J (2003) Ultrastructural changes in cambial cell derivatives during xylem differentiation in poplar. Plant Biol 5:255–264Google Scholar
  7. Arend M, Fromm J (2004) Die Rolle von Kalium und H+-ATPasen bei der Holzbildung. AFZ-DerWald 19:1032–1033Google Scholar
  8. Arend M, Weisenseel MH, Brummer M, Osswald W, Fromm J (2002) Seasonal changes of plasma membrane H+-ATPase and endogenous ion current during cambial growth in poplar plants. Plant Phys 129:1651–1663Google Scholar
  9. Arend M, Monshausen G, Wind C, Weisenseel MH, Fromm J (2004) Effect of potassium deficiency on the plasma membrane H+-ATPase of the wood ray parenchyma in poplar. Plant Cell Environ 27:1288–1296Google Scholar
  10. Arend M, Stinzing A, Wind C, Langer K, Latz A, Ache P, Fromm J, Hedrich R (2005) Polar-localised poplar K+ channel capable of controlling electrical properties of wood-forming cells. Planta 223:140–148PubMedGoogle Scholar
  11. Arend M, Muninger M, Fromm J (2008) Unique occurrence of pectin-like fibrillar cell wall deposits in xylem fibres of poplar. Plant Biol 10:763–770PubMedGoogle Scholar
  12. Arend M, Schnitzler J-P, Ehlting B, Hänsch R, Lange T, Rennenberg H, Himmelbach A, Grill E, Fromm J (2009) Expression of the Arabidopsis mutant abi1 gene alters abscisic acid sensitivity, stomatal development, and growth morphology in gray poplars. Plant Phys 151:2110–2119Google Scholar
  13. Aspeborg H, Schrader J, Coutinho PM, Stam M, Kallas Å, Nilsson P, Denman S, Amini B, Sterky F, Master E et al (2005) Carbohydrate-active enzymes involved in the secondary cell wall biogenesis in hybrid aspen. Plant Physiol 137:983–997PubMedGoogle Scholar
  14. Avci U, Earl Petzold H, Ismail IO, Beers EP, Haigler CH (2008) Cysteine proteases XCP1 and XCP2 aid micro-autolysis within the intact central vacuole during xylogenesis in Arabidopsis roots. Plant J 56:303–315PubMedGoogle Scholar
  15. Avery GS, Burkholder PR, Creighton HB (1937) Production and distribution of growth hormone in shoots of Aesculus and Malus, and its probable role in stimulating cambial activity. Am J Bot 24:51–58Google Scholar
  16. Awano T, Takabe K, Fujita M, Daniel G (2000) Deposition of glucuronoxylans on the secondary cell wall of Japanese beech as observed by immune-scanning electron microscopy. Protoplasma 212:72–79Google Scholar
  17. Baba K, Karlberg A, Schmidt J, Schrader J, Hvidsten TR, Bako L, Bhalerao RP (2011) Activity-dormancy transition in the cambial meristem involves stage-specific modulation of auxin response in hybrid aspen. Proc Nat Acad Sci USA 108:3418–3423PubMedGoogle Scholar
  18. Baier M, Goldberg R, Catesson A-M, Liberman M, Bouchemal N, Michon V, Herve du Penhoat C (1994) Pectin changes in samples containing poplar cambium and inner bark in relation to the seasonal cycle. Planta 193:446–454Google Scholar
  19. Bannan MW (1955) The vascular cambium and radial growth in Thuja occidentalis L. Can J Bot 33:113–138Google Scholar
  20. Baskin TI (2001) On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215:150–171PubMedGoogle Scholar
  21. Baumann MJ, Eklof JM, Michel G, Kallas AM, Teeri TT, Czjzek M, Brumer H (2007) Structural evidence for the evolution of xyloglucanase activity from xyloglucan endotransglycosylases: biological implications for cell wall metabolism. Plant Cell 19:1947–1963PubMedGoogle Scholar
  22. Begum S, Nakaba S, Oribe Y, Kubo T, Funada R (2007) Induction of cambial reactivation by localized heating in a deciduous hardwood hybrid poplar (Populus sieboldii × P. grandidentata). Ann Bot 100:439–447PubMedGoogle Scholar
  23. Begum S, Nakaba S, Oribe Y, Kubo T, Funada R (2010) Changes in the localization and levels of starch and lipids in cambium and phloem during cambial reactivation by artificial heating of main stems of Cryptomeria japonica trees. Ann Bot 106:885–895PubMedGoogle Scholar
  24. Bertaud F, Holmbom B (2004) Chemical composition of earlywood and latewood in Norway spruce heartwood, sapwood and transition zone wood. Wood Sci Tech 38:245–256Google Scholar
  25. Bhaudari S, Fujino T, Thammanagowda S, Zhang DY, Xu FY, Joshi CP (2006) Xylem-specific and tension stress-responsive coexpression of KORRIGAN endoglucanase and three secondary wall-associated cellulose synthase genes in aspen trees. Planta 224:828–837Google Scholar
  26. Bishopp A, Lehesranta S, Vatén A, Help H, El-Showk S, Scheres B, Helariutta K, Mähönen AP, Sakakibara H, Helariutta Y (2011) Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr Biol 21:927–932PubMedGoogle Scholar
  27. Bissett IJW, Dadswell HE (1950) The variation in cell length within one growth ring of certain angiosperms and gymnosperms. Aust For 14:17–29Google Scholar
  28. Björklund S, Antti H, Uddestrand I, Moritz T, Sundberg B (2007) Cross-talk between gibberellin and auxin in development of Populus wood: gibberellin stimulate polar auxin transport and has a common transcriptome with auxin. Plant J 52:499–511PubMedGoogle Scholar
  29. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54(1):519–546PubMedGoogle Scholar
  30. Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043PubMedGoogle Scholar
  31. Bollhöner B, Prestele J, Tuominen H (2012) Xylem cell death: emerging understanding of regulation and function. J Exp Bot 63(3):1081–1094PubMedGoogle Scholar
  32. Brett CT (2000) Cellulose microfibrils in plants: biosynthesis, deposition, and integration into the cell wall. Int Rev Cytol 199:161–199PubMedGoogle Scholar
  33. Brett C, Waldron K (1990) Physiology and biochemistry of plant cell walls. Unwin Hyman, LondonGoogle Scholar
  34. Brienen RJW, Zuidema PA (2005) Relating tree growth to rainfall in Bolivian rain forests: a test for six species using tree ring analysis. Oecologia 146:1–12PubMedGoogle Scholar
  35. Catesson A-M (1989) Specific characters of vessel primary walls during the early stages of wood differentiation. Biol Cell 67:221–226Google Scholar
  36. Catesson A-M (1990) Cambial cytology and biochemistry. In: Iqbal M (ed) The vascular cambium, vol 7, Research studies in botany and related applied fields. Research Studies Press, Taunton, MA, pp 63–112Google Scholar
  37. Catesson A-M (1994) Cambial ultrastructure and biochemistry: changes in relation to vascular tissue differentiation and the seasonal cycle. Int J Plant Sci 155:251–261Google Scholar
  38. Catesson A-M, Roland JC (1981) Sequential changes associated with cell wall formation and fusion in the vascular cambium. IAWA Bull 2:151–162Google Scholar
  39. Catesson A-M, Funada R, Robertbaby D, Quinetszely M, Chuba J, Goldberg R (1994) Biochemical and cytochemical cell-wall changes across the cambial zone. IAWA J 15:91–101Google Scholar
  40. Chaffey N (1999) Cambium: old challenges – new opportunities. Trees 13:138–151Google Scholar
  41. Chaffey NF, Barnett JR, Barlow PW (1998) A cycle of microtubule rearrangement accompanies the seasonal cycle of wall thickening within the vascular cambium of Aesculus hippocastanum L. taproots. New Phytol 139:623–635Google Scholar
  42. Chaffey N, Barnett J, Barlow P (1999) A cytoskeletal basis for wood formation in angiosperm trees: the involvement of cortical microtubules. Planta 208:19–30Google Scholar
  43. Chaffey N, Cholewa E, Regan S, Sundberg B (2002) Secondary xylem development in Arabidopsis: a model for wood formation. Physiol Plant 114:594–600PubMedGoogle Scholar
  44. Chiang VL (2006) Monolignol biosynthesis and genetic engineering of lignin in trees, a review. Environ Chem Lett 4(3):143–146Google Scholar
  45. Clark A, Daniels RF, Jordan L (2006) Juvenile/mature wood transition in loblolly pine as defined by annual ring specific gravity, proportion of latewood, and microfibril angle. Wood Fiber Sci 38:292–299Google Scholar
  46. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6(11):850–861PubMedGoogle Scholar
  47. Courtois-Moreau CL, Pesquet E, Sjodin A, Muniz L, Bollhöner B, Kaneda M, Samuels L, Jansson S, Tuominen H (2009) A unique program for cell death in xylem fibers of Populus stem. Plant J 58:260–274PubMedGoogle Scholar
  48. Del Campillo E (1999) Multiple endo-1,4-D-glucanase (cellulase) genes in Arabidopsis. Curr Top Dev Biol 46:39–61PubMedGoogle Scholar
  49. Djerbi S, Aspeborg H, Nilsson P, Sundberg B, Mellerowicz E, Blomqvist K, Teeri TT (2004) Identification and expression analysis of genes encoding putative cellulose synthases (CesA) in the hybrid aspen, Populus tremula (L.) × P. tremuloides (Michx.). Cellulose 11:301–312Google Scholar
  50. Djerbi S, Lindskog M, Arvestad L, Sterky F, Teeri TT (2005) The genome sequence of black cottonwood (Populus trichocarpa) reveals 18 conserved cellulose synthase (CesA) genes. Planta 221:739–746PubMedGoogle Scholar
  51. Donaldson L (2007) Cellulose microfibril aggregates and their size variation with cell wall type. Wood Sci Technol 41:443–460Google Scholar
  52. Druart N, Johansson A, Baba K, Schrader J, Sjödin A, Bhalerao RR, Resman L, Trygg J, Moritz T, Bhalerao RP (2007) Environmental and hormonal regulation of the activity-dormancy cycle in the cambial meristem involves stage-specific modulation of transcriptional and metabolic networks. Plant J 50:557–573PubMedGoogle Scholar
  53. Endo S, Pesquet E, Tashiro G, Kuriyama H, Goffner D, Fukuda H, Demura T (2008) Transient transformation and RNA silencing in Zinnia tracheary element differentiating cell cultures. Plant J 53:864–875PubMedGoogle Scholar
  54. Eriksson ME, Israelsson M, Olsson O, Moritz T (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat Biotechnol 18:784–788PubMedGoogle Scholar
  55. Ermel FF, Follet-Gueye M-L, Cibert C, Vian B, Morvan C, Catesson A-M, Goldberg R (2000) Differential localization of arabinan and galactan side chains of rhamnogalacturonan 1 in cambial derivatives. Planta 210:732–740PubMedGoogle Scholar
  56. Espinosa-Ruiz A, Saxena S, Schmidt J, Mellerowicz E, Miskolczi P, Bako L, Bhalerao R (2004) Differential stage-specific regulation of cyclin-dependent kinases during cambial dormancy in hybrid aspen. Plant J 38:603–615PubMedGoogle Scholar
  57. Farrar JJ, Evert RF (1997) Seasonal changes in the ultrastructure of the vascular cambium of Robinia pseudoacacia. Trees 11:191–202Google Scholar
  58. Fernandes AN, Thomas LH, Altaner CM, Callow P, Forsyth VT, Apperley DC, Kennedy CJ, Jarvis MC (2011) Nanostructure of cellulose microfibrils in spruce wood. Proc Natl Acad Sci USA 108:E1195–E1203PubMedGoogle Scholar
  59. Fisher K, Turner S (2007) PXY, a receptor–like kinase essential for maintaining polarity during plant vascular-tissue development. Curr Biol 17:1061–1066PubMedGoogle Scholar
  60. Follet-Gueye ML, Verdus MC, Demarty M, Thellier M, Ripoll C (1998) Cambium pre-activation in beech correlates with a strong temporary increase of calcium in cambium and phloem but not in xylem cells. Cell Calcium 24(3):205–211PubMedGoogle Scholar
  61. Follet-Gueye ML, Ermel FF, Vian B, Catesson A-M, Goldberg R (2000) Pectin remodeling during cambial derivative differentiation. In: Savidge RA, Barnett JR, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers, Oxford, pp 289–294Google Scholar
  62. Foucart C, Paux E, Ladouce N, San-Clemente H, Grima-Pettenati J, Sivadon P (2006) Transcript profiling of a xylem vs phloem cDNA subtractive library identifies new genes expressed during xylogenesis in Eucalyptus. New Phytol 170:739–752PubMedGoogle Scholar
  63. Fromm J (1997) Hormonal physiology of wood growth in willow (Salix viminalis L.): effects of spermine and abscisic acid. Wood Sci Technol 31:119–130Google Scholar
  64. Fromm J (2010) Wood formation of trees in relation to potassium and calcium nutrition. Tree Phys 30:1140–1147Google Scholar
  65. Fromm J, Hedrich R (2007) The role of potassium in wood formation of poplar. In: Sattelmacher B, Horst WJ (eds) The Apoplast of higher plants: compartment of storage, transport and reactions. Springer, New York, pp 137–149Google Scholar
  66. Fromm J, Sautter I, Matthies D, Kremer J, Schumacher P, Ganter C (2001) Xylem water content and wood density in spruce and oak trees detected by high-resolution computed tomography. Plant Phys 127:416–425Google Scholar
  67. Fromm J, Rockel B, Lautner S, Windeisen E, Wanner G (2003) Lignin distribution in wood cell walls determined by TEM and backscattered SEM techniques. J Struct Biol 143:77–84PubMedGoogle Scholar
  68. Fuchs M, Ehlers K, Will T, van Bel AJE (2010a) Immunolocalization indicates plasmodesmal trafficking of storage proteins during cambial reactivation in Populus nigra. Ann Bot 106:385–394PubMedGoogle Scholar
  69. Fuchs M, van Bel AJE, Ehlers K (2010b) Season-associated modifications in symplasmic organization of the cambium in Populus nigra. Ann Bot 105:375–387PubMedGoogle Scholar
  70. Fujino T, Itoh T (1998) Changes in the three dimensional architecture of the cell wall during lignifications of xylem cells in Eucalyptus tereticornis. Holzforschung 52:111–116Google Scholar
  71. Fukuda H (1996) Xylogenesis: initiation, progression and cell death. Annu Rev Plant Physiol Plant Mol Biol 47:299–325PubMedGoogle Scholar
  72. Fukuda H (1997) Tracheary element differentiation. Plant Cell 9:1147–1156PubMedGoogle Scholar
  73. Fukuda H (2004) Signals that control plant vascular cell differentiation. Nat Rev 5:379–391Google Scholar
  74. Funada R, Catesson A-M (1991) Partial cell wall lysis and the resumption of meristematic activity in Fraxinus excelsior cambium. IAWA Bull ns 12:439–444Google Scholar
  75. Funada R, Abe H, Furusawa O, Imaizumi H, Fukuzawa K, Ohtani J (1997) The orientation and localization of cortical microtubules in differentiating conifer tracheids during cell expansion. Plant Cell Physiol 38(2):210–212Google Scholar
  76. Funada R, Kubo T, Tabuchi M, Sugiyama T, Fushitani M (2001) Seasonal variations in endogenous indole-3-acetic acid and abscisic acid in the cambial region of Pinus densiflora Sieb. Et Zucc. stems in relation to earlywood-latewood transition and cessation of tracheid production. Holzforschung 55:128–134Google Scholar
  77. Geisler-Lee J, Geisler M, Coutinho PM, Segerman B, Nishikubo N, Takahashi J, Aspeborg H, Djerbi S, Master E, Andersson-Gunnerås S et al (2006) Poplar carbohydrate-active enzymes (CAZymes). Gene identification and expression analyses. Plant Physiol 140:946–962PubMedGoogle Scholar
  78. Ghouse AKM, Hashmi S (1983) Periodicity of cambium and of the formation of xylem and phloem in Mimusops elengi L., an evergreen member of tropical India. Flora 173:479–487Google Scholar
  79. Gion JM, Carouché A, Deweer S, Bedon F, Pichavant F, Charpentier JP, Baillères H, Rozenberg P, Carocha V, Ognouabi N et al (2011) Comprehensive genetic dissection of wood properties in a widely-grown tropical tree: Eucalyptus. BMC Genomics 12:301PubMedGoogle Scholar
  80. González-Martínez SC, Wheeler NC, Ersoz E, Nelson CD, Neale DB (2006) Association genetics in Pinus taeda L. I. Wood property traits. Genetics 175:399–409PubMedGoogle Scholar
  81. Goué N, Lesage-Descauses M-C, Mellerowicz EJ, Magel E, Label P, Sundberg B (2008) Microgenomic analysis reveals cell type-specific gene expression patterns between ray and fusiform initials within the cambial meristem of Populus. New Phytol 180:45–56PubMedGoogle Scholar
  82. Gregory RA (1971) Cambial activity in Alaskan white spruce. Am J Bot 58:160–171Google Scholar
  83. Gregory ACE, O’Connell AP, Bolwell GP (1998) Xylans. Biotechnol Genet Eng Rev 15:439–455Google Scholar
  84. Groover A, Jones AM (1999) Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol 119:375–384PubMedGoogle Scholar
  85. Groover A, DeWitt N, Heidel A, Jones A (1997) Programmed cell death of plant tracheary elements differentiating in vitro. Protoplasma 196:197–211Google Scholar
  86. Haigler CH, Brown RM 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 134:111–120Google Scholar
  87. Harada H, Coté WA Jr (1985) Structure of wood. In: Biosynthesis and biodegradation of wood components. Academic, Orlando, FL, pp 1–44Google Scholar
  88. Heath IB (1974) A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. J Theor Biol 48:445–449PubMedGoogle Scholar
  89. Heide O (1993) Daylength and thermal time responses of bud burst during dormancy release in some northern deciduous trees. Physiol Plant 88:531–540Google Scholar
  90. Hejnowicz A, Hejnowicz Z (1958) Variation of length of vessel members and fibres in the trunk of Populus tremula L. Acta Soc Bot Pol 27:131–159Google Scholar
  91. Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M, Sawa S, Ohashi-Ito K, Matsubayashi Y, Fukuda H (2008) Non-cell autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci USA 105:15208–15213PubMedGoogle Scholar
  92. Hoenicka H, Lautner S, Klingberg A, Koch G, El-Sherif F, Lehnhardt D, Zhang B, Burgert I, Odermatt J, Melzer S, Fromm J, Fladung M (2012) Influence of over-expression of the FLOWERING PROMOTING FACTOR 1 gene (FPF1) from Arabidopsis on wood formation in hybrid poplar (Populus tremula L. × P. tremuloides Michx.). Planta 235:359–373PubMedGoogle Scholar
  93. Holland N, Holland D, Helentjaris T, Dhugga KS, Xoconostle-Cazares B, Delmer DP (2000) A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Phys 123:1313–1323Google Scholar
  94. Hoson T (1991) Structure and function of plant cell walls: immunological approaches. Int Rev Cytol 130:233–268Google Scholar
  95. Hou H-W, Zhou Y-T, Mwange K-N, Li W-F, He X-Q, Cui K-M (2006) ABP1 expression regulated by IAA and ABA is associated with the cambium periodicity in Eucommia ulmoides Oliv. J Exp Bot 57(14):3857–3867PubMedGoogle Scholar
  96. Ingold E, Sugiyama M, 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 29:295–303Google Scholar
  97. Ito J, Fukuda H (2002) ZEN1 is a key enzyme in the degradation of nuclear DNA during programmed cell death of tracheary elements. Plant Cell 14:3201–3211PubMedGoogle Scholar
  98. Jarvis M (2003) Chemistry: cellulose stacks up. Nature 426:611–612PubMedGoogle Scholar
  99. Jenkins PA, Shepherd KR (1974) Seasonal changes in levels of indoleacetic acid and abscisic acid in stem tissues of Pinus radiata. N Z J For Sci 4:511–519Google Scholar
  100. Jordan L, He R, Hall DB, Clark A, Daniels RF (2006) Variation in loblolly pine cross-sectional microfibril angle with tree height and physiographic region. Wood Fiber Sci 38:390–398Google Scholar
  101. Keegstra K, Raikhel N (2001) Plant glycosyltransferases. Curr Opin Plant Biol 4:219–224PubMedGoogle Scholar
  102. Kenada M, Rensing KH, Wong JCT, Banno B, Mansfield SD, Samuels AL (2008) Tracking monolignols during wood development in lodgepole pine. Plant Phys 147:1750–1760Google Scholar
  103. Kerr AJ, Goring DAI (1975) The ultrastructural arrangement of the wood cell wall. Cellulose Chem Technol 9:563–573Google Scholar
  104. Ko JH, Prassinos C, Keathley D, Han KH (2011) Novel aspects of transcriptional regulation in the winter survival and maintenance mechanism of poplar. Tree Phys 31:208–225Google Scholar
  105. Kroll RE, Ritter DC, Gertjejansen RO, Au KC (1992) Anatomical and physical properties of balsam poplar (Populus balsamifera L.) in Minnesota. Wood Fiber Sci 24:13–24Google Scholar
  106. Kuriyama H (1999) Loss of tonoplast integrity programmed in tracheary element differentiation. Plant Physiol 121:763–774PubMedGoogle Scholar
  107. Lachaud S (1989) Participation of auxin and abscisic acid in the regulation of seasonal variations in cambial activity and xylogenesis. Trees 3:125–137Google Scholar
  108. Lang GA (1987) Dormancy: a new universal terminology. Hort Sci 22:817–820Google Scholar
  109. Langer K, Ache P, Geiger D, Stinzing A, Arend M, Wind C, Regan S, Fromm J, Hedrich R (2002) Poplar potassium transporters capable of controlling K+ homeostasis and K+-dependent xylogenesis. Plant J 32:997–1009PubMedGoogle Scholar
  110. Larisch C, Dittrich M, Wildhagen H, Lautner S, Fromm J, Polle A, Hedrich R, Rennenberg H, Müller T, Ache P (2012) Poplar wood rays are involved in seasonal remodeling of tree physiology. Plant Physiol 160(3):1515–1529PubMedGoogle Scholar
  111. Larson PR (1994) The cambium: development and structure. Springer, BerlinGoogle Scholar
  112. Lautner S, Zollfrank C, Fromm J (2012) Microfibril angle distribution of poplar tension wood. IAWA J 33(4):431–439Google Scholar
  113. Lavigne MB, Little CHA, Riding RT (2004) Changes in stem respiration rate during cambial reactivation can be used to refine estimates of growth and maintenance respiration. New Phytol 162:81–93Google Scholar
  114. Lee C, Teng Q, Zhong R, Ye ZH (2011) Molecular dissection of xylan biosynthesis during wood formation in poplar. Mol Plant 4:730–747PubMedGoogle Scholar
  115. Li X, Wu HX, Southerton SG (2011) Transcriptome profiling of Pinus radiata juvenile wood with contrasting stiffness identifies putative candidate genes involved in microfibril orientation and cell wall mechanics. BMC Genomics 12:480–496PubMedGoogle Scholar
  116. Little CHA, Bonga JM (1974) Rest in the cambium of Abies balsamea. Can J Bot 52:1723–1730Google Scholar
  117. Little CHA, Savidge RA (1987) The role of plant growth regulators in forest tree cambial growth. Plant Growth Regul 6:137–169Google Scholar
  118. Love J, Björklund S, Vahala J, Hertzberg M, Kangasjärvi J, Sundberg B (2009) Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus. Proc Natl Acad Sci USA 106:5984–5989PubMedGoogle Scholar
  119. Magel EA, Monties B, Drouet A, Jay-Allemand C, Ziegler H (1995) Heartwood formation: biosynthesis of heartwood extractives and “secondary” lignifications. In: Sandermann H Jr, Bonnet-Masimbert M (eds) Eurosilva – contribution to forest tree physiology. INRA, Versailles, pp 35–56Google Scholar
  120. Mansfield SD, Iliadis L, Avramidis S (2007) Neural network prediction of bending strength and stiffness in western hemlock (Tsuga heterophylla Raf.). Holzforschung 61:707–716Google Scholar
  121. Matsumoto T, Sakai F, Hayashi T (1997) A xyloglucan-specific endo-1,4-ß-glucanase isolated from auxin-treated pea stems. Plant Phys 114:661–667Google Scholar
  122. Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Václavíková K, Miyawaki K, Kakimoto T (2008) Cytokinins are central regulators of cambial activity. Proc Natl Acad Sci USA 105:20027–20031PubMedGoogle Scholar
  123. Mauriat M, Moritz T (2009) Analyses of GA20ox-and GID1-over-expressing aspen suggest that gibberellins play two distinct roles in wood formation. Plant J 58:989–1003PubMedGoogle Scholar
  124. McQueen-Mason S (1997) Plant cell walls and the control of growth. Biochem Soc Trans 25:204–214PubMedGoogle Scholar
  125. McQueen-Mason SJ, Cosgrove DJ (1995) Expansin mode of action on cell walls (analysis of wall hydrolysis, stress relaxation, and binding). Plant Phys 107(1):87–100Google Scholar
  126. Mellerowicz EJ, Sundberg B (2008) Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties. Curr Opin Plant Biol 11:293–300PubMedGoogle Scholar
  127. Mellerowicz EJ, Baucher M, Sundberg B, Boerjan W (2001) Unravelling cell wall formation in the woody dicot stem. Plant Mol Biol 47:239–274PubMedGoogle Scholar
  128. Moreau C, Aksenov N, Lorenzo M, Segerman B, Funk C, Nilsson P, Jansson S, Tuominen H (2005) A genomic approach to investigate developmental cell death in woody tissues of Populus trees. Genome Biol 6:R34PubMedGoogle Scholar
  129. Moyle R, Schrader J, Stenberg A, Olsson O, Saxena S, Sandberg G, Bhalerao RP (2002) Environmental and auxin regulation of wood formation involves members of the Aux/IAA gene family in hybrid aspen. Plant J 31(6):675–685PubMedGoogle Scholar
  130. Muñiz L, Minguet EG, Singh SK, Pesquet E, Vera-Sirera F, Moreau-Courtois CL, Carbonell J, Blázquez MA, Tuominen H (2008) ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development 135:2573–2582PubMedGoogle Scholar
  131. Murakami Y, Funada R, Sano Y, Ohtani J (1999) The differentiation of contact cells and isolation cells in the xylem ray parenchyma of Populus maximowiczii. Ann Bot 84:429–435Google Scholar
  132. Mutwil M, Debold S, Persson S (2008) Cellulose synthesis: a complex. Curr Opin Plant Biol 11:252–257PubMedGoogle Scholar
  133. Nakaba S, Sano Y, Kubo T, Funada R (2006) The positional distribution of cell death of ray parenchyma in a conifer, Abies sachalinensis. Plant Cell Rep 25:1143–1148PubMedGoogle Scholar
  134. Nicholson RL, Hammerschmidt R (1992) Phenolic compounds and their role in disease resistance. Annu Rev Phytopathol 30:369–389Google Scholar
  135. Nick P (2008) Control of cell axis. In: Nick P (ed) Plant microtubules – development and flexibility. Springer, Berlin, pp 3–46Google Scholar
  136. Nieminen K, Immanen J, Laxell M, Kauppinen L, Tarkowski P, Dolezal K, Tähtiharju S, Elo A, Decourteix M, Ljung K et al (2008) Cytokinin signaling regulates cambial development in poplar. Proc Natl Acad Sci USA 105:20032–20037PubMedGoogle Scholar
  137. Nieminen K, Robischon M, Immanen J, Helariutta Y (2012) Towards optimizing wood development in bioenergy trees. New Phytol 194:46–53PubMedGoogle Scholar
  138. Nilsson J, Karlberg A, Antti H, Lopes-Vernaza M, Mellerowicz E, Perrot-Rechenmann C, Sandberg G, Bhalerao RP (2008) Dissecting the molecular basis of the regulation of wood formation by auxin in hybrid aspen. Plant Cell 20:843–855PubMedGoogle Scholar
  139. Nishikubo N, Awano T, Banasiak A, Bourquin V, Ibatullin F, Funada R, Brumer H, Teeri TT, Hayashi T, Sundberg B, Mellerowicz EJ (2007) Xyloglucan endotransglycosylase (XET) functions in gelatinous layers of tension wood fibers in poplar – a glimpse into the mechanism of the balancing act of trees. Plant Cell Physiol 48:843–855PubMedGoogle Scholar
  140. Oakley RV, Wang YS, Ramakrishna W, Harding SA, Tsai CJ (2007) Differential expansion and expression of α- and β-tubulin gene families in Populus. Plant Physiol 145:961–973PubMedGoogle Scholar
  141. Obara K, Kuriyama H, Fukuda H (2001) Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia. Plant Physiol 125:615–626PubMedGoogle Scholar
  142. Oda H, Fukuda H (2012) Secondary cell wall patterning during xylem differentiation. Curr Opin Plant Biol 15:38–44PubMedGoogle Scholar
  143. Ohashi-Ito K, Oda Y, Fukuda H (2010) Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 22:3461–3473PubMedGoogle Scholar
  144. Ohmiya Y, Samejima M, Shiroishi M, Amano Y, Kanda T, Sakai F, Hayashi T (2000) Evidence that endo-1,4-ß-glucanases act on cellulose in suspension-cultured poplar cells. Plant J 24:147–158PubMedGoogle Scholar
  145. Oribe Y, Funada R, Shibagaki M, Kubo T (2001) Cambial reactivation in the partially heated stem in an evergreen conifer Abies sachalinensis. Planta 212:684–691PubMedGoogle Scholar
  146. Oribe Y, Funada R, Kubo T (2003) Relationships between cambial activity, cell differentiation and the localization of starch in storage tissues around the cambium in locally heated stems of Abies sachalinensis (Schmidt) Masters. Trees 17:185–192Google Scholar
  147. Paredez A, Wright A, Ehrhardt DW (2006a) Microtubule cortical array organization and plant cell morphogenesis. Curr Opin Plant Biol 9:571–578Google Scholar
  148. Paredez AR, Somerville CR, Ehrhardt DW (2006b) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495PubMedGoogle Scholar
  149. Pelloux J, Rustérucci C, Mellerowicz EJ (2007) New insights into pectin methylesterase (PME) structure and function. Trends Plant Sci 12:267–277PubMedGoogle Scholar
  150. Pesquet E, Tuominen H (2011) Ethylene stimulates tracheary element differentiation in Zinnia elegans cell cultures. New Phytol 190:138–149Google Scholar
  151. Pesquet E, Korolev AV, Calder G, Lloyd CW (2010) The microtubule-associated protein AtMAP70-5 regulates secondary wall patterning in Arabidopsis wood cells. Curr Biol 20:744–749PubMedGoogle Scholar
  152. Prassinos C, Ko JH, Han KH (2005) Transcriptome profiling of vertical stem segments provides insights into the genetic regulation of secondary growth in hybrid aspen trees. Plant Cell Physiol 46:1213–1225PubMedGoogle Scholar
  153. Ragni L, Nieminen K, Pacheco-Villalobos D, Sibout R, Schwechheimer C, Hardtke CS (2011) Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expansion. Plant Cell 23:1322–1336PubMedGoogle Scholar
  154. Ralph J, MacKay JJ, Hatfield RD, O’Malley DM, Whetten RW, Sederoff RR (1997) Abnormal lignin in a loblolly pine. Science 277:235–239PubMedGoogle Scholar
  155. Ranik M, Myburg AA (2006) Six new cellulose synthase genes from Eucalyptus are associated with primary and secondary cell wall biosynthesis. Tree Physiol 26:545–556PubMedGoogle Scholar
  156. Rathgeber CBK, Rossi S, Bontemps JD (2011) Cambial activity related to tree size in a mature silver-fir plantation. Ann Bot 108:429–438PubMedGoogle Scholar
  157. Resman L, Howe G, Jonsen D, Englund M, Druart N, Schrader J, Antti H, Skinner J, Sjodin A, Chen T, Bhalerao RP (2010) Components acting downstream of short day perception regulate differential cessation of cambial activity and associated responses in early and late clones of hybrid poplar. Plant Phys 154:1294–1303Google Scholar
  158. Rinne PLH, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjarvi J, van der Schoot C (2011) Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-beta-glucanases to reopen signal conduits and release dormancy in Populus. Plant Cell 23:130–146PubMedGoogle Scholar
  159. Robards AW, Kidway P (1969) A comparative study of the ultrastructure of resting and active cambium of Salix fragilis L. Planta 84:239–249Google Scholar
  160. Robischon M, Du J, Miura E, Groover A (2011) The Populus class III HD ZIP, popREVOLUTA, influences cambium initiation and patterning of woody stems. Plant Physiol 155:1214–1225PubMedGoogle Scholar
  161. Rohde A, Boerjan W (2001) Insights into bud development and dormancy in poplar. In: Huttunen S, Heikkilä H, Bucher J, Sundberg B, Jarvis P, Matyssek R (eds) Trends in European tree physiology research. Kluwer, The Netherlands, pp 33–52Google Scholar
  162. Ruttink T, Arend M, Morreel K, Strome V, Rombauts S, Fromm J, Bhalerao R, Boerjan W, Rohde A (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19:2370–2390PubMedGoogle Scholar
  163. Sampedro J, Carey RE, Cosgrove DJ (2006) Genome histories clarify evolution of the expansin superfamily: new insights from the poplar genome and pine ESTs. J Plant Res 119:11–21PubMedGoogle Scholar
  164. Schrader J, Baba K, May ST, Palme K, Bennett M, Bhalerao RP (2003) Polar auxin transport in the wood forming tissues of hybrid aspen is under simultaneous control of developmental and environmental signals. Proc Natl Acad Sci USA 100:10096–10101PubMedGoogle Scholar
  165. Schrader J, Moyle R, Bhalerao R, Hertzberg M, Lundeberg J, Nilsson P, Bhalerao RP (2004a) Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 40:173–187PubMedGoogle Scholar
  166. Schrader J, Nilsson J, Mellerowicz E, Berglund A, Nilsson P, Hertzberg M, Sandberg G (2004b) A high-resolution transcript profile across the wood-forming meristem of poplar identifies potential regulators of cambial stem cell identity. Plant Cell 16:2278–2292PubMedGoogle Scholar
  167. Sennerby-Forsse L (1986) Seasonal variation in the ultrastructure of the cambium in young stems of willow (Salix viminalis) in relation to phenology. Plant Physiol 67:529–537Google Scholar
  168. Sexton TR, Henry RJ, Harwood CE, Thomas DS, McManus LJ, Raymond C, Henson M, Shepherd M (2012) Pectin methylesterase genes influence solid wood properties of Eucalyptus pilularis. Plant Physiol 158:531–541PubMedGoogle Scholar
  169. Siedlecka A, Wiklund S, Péronne MA, Micheli F, Lésniewska J, Sethson I, Edlund U, Richard L, Sundberg B, Mellerowicsz EJ (2008) Pectin methyl esterase inhibits intrusive and symplastic cell growth in developing wood cells of Populus. Plant Physiol 146:554–565PubMedGoogle Scholar
  170. Söding H (1937) Wuchsstoff und Kambiumtätigkeit der Bäume. Jahrb Wiss Bot 84:639–670Google Scholar
  171. Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78PubMedGoogle Scholar
  172. 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 TT, Boerjan W, Gustafsson P, Uhlén M, Sundberg B, Lundeberg J (1998) Gene discovery in the wood-forming tissues of poplar: analysis of 5692 expressed sequence tags. Proc Natl Acad Sci USA 95:13330–13335PubMedGoogle Scholar
  173. Sterky F, Bhalerao RR, Unneberg P, Segerman B, Nilsson P, Brunner AM, Campaa LC, Lindvall JJ, Tandre K, Strauss SH, Sundberg B, Gustafsson P, Uhlen M, Bhalerao RP, Nilsson O, Sandberg G, Karlsson J, Lundeberg J, Jansson S (2004) A Populus EST resource for plant functional genomics. Proc Natl Acad Sci USA 101:13951–13956PubMedGoogle Scholar
  174. Steward CM (1966) Excretion and heartwood formation in living trees. Science 153:1068–1074Google Scholar
  175. Sundberg B, Uggla C (1997) Origin and dynamics of indoleacetic acid under polar transport in Pinus sylvestris. Physiol Plant 104:22–29Google Scholar
  176. Sundberg B, Tuominen H, Little C (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 1-year-old Pinus sylvestris (L) shoots. Plant Physiol 106:469–476PubMedGoogle Scholar
  177. Sundberg B, Uggla C, Tuominen H (2000) Cambial growth and auxin gradients. In: Savidge RA, Barnett JR, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers, Oxford, pp 169–188Google Scholar
  178. Suzuki S, Li LG, Sun Y, Chiang VL (2006) The cellulose synthase gene superfamily and biochemical functions of xylem-specific cellulose synthase-like genes in Populus trichocarpa. Plant Physiol 142:1233–1245PubMedGoogle Scholar
  179. Tanino K (2004) Hormones and endodormancy induction in woody plants. J Crop Improv 10:157–199Google Scholar
  180. Terashima N, Fukushima K, He LF, Takabe K (1993) Comprehensive model of the lignified plant cell wall. In: Jung HG (ed) Forage cell wall structure and digestibility. ASA-CSSA-SSSA, Madison, WI, pp 247–270Google Scholar
  181. 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 109:1179–1189PubMedGoogle Scholar
  182. Tuskan GA et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604PubMedGoogle Scholar
  183. Tyerman SD, Niemietz CM et al (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25(2):173–194PubMedGoogle Scholar
  184. Uggla C, Mellerowicz EJ, Sundberg B (1998) Indole-3-acetic acid controls cambial growth in Scots pine by positional signaling. Plant Physiol 117:113–121PubMedGoogle Scholar
  185. Uggla C, Magel E, Moritz T, Sundberg B (2001) Function and dynamics of auxin and carbohydrates during earlywood/latewood transition in Scots pine. Plant Phys 125(4):2029–2039Google Scholar
  186. Vetter RE, Botosso PC (1989) Remarks on age and growth rate determination of Amazonian trees. IAWA Bull ns 10:133–145Google Scholar
  187. Voelker SL, Lachenbruch B, Meinzer FC, Jourdes M, Ki C, Patten AM, Davin LB, Lewis NG, Tuskan GA, Gunter L, Decker SR, Selig MJ, Sykes R, Himmel ME, Kitin P, Shevchenko O, Strauss SH (2010) Antisense down-regulation of 4CL expression alters lignification, tree growth and saccharification potential of field-grown poplar. Plant Physiol 154:874–886PubMedGoogle Scholar
  188. Wind C, Arend M, Fromm J (2004) Potassium-dependent cambial growth in poplar. Plant Biol 6:30–37PubMedGoogle Scholar
  189. Wodzicki TJ, Wodzicki AB (1980) Seasonal abscisic acid accumulation in stem and cambial region of Pinus sylvestris and its contribution to the hypothesis of a late-wood control system in conifers. Physiol Plant 48:443–447Google Scholar
  190. Worbes M (1985) Structural and other adaptations to long-term flooding by trees in Central Amazonia. Amazoniana 9:459–484Google Scholar
  191. Worbes M (1995) How to measure growth dynamics in tropical trees – a review. IAWA J 16:337–351Google Scholar
  192. Wu L, Joshi CP, Chiang VL (2000) A xylem-specific cellulose synthase gene from aspen (Populus tremuloides) is responsive to mechanical stress. Plant J 22:495–502PubMedGoogle Scholar
  193. Yamaguchi M, Kubo M, Fukuda H, Demura T (2008) Vascular-related NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J 55:652–664PubMedGoogle Scholar
  194. Yamaguchi M, Ohtani M, Mitsuda N, Kubo M, Ohme-Takagi M, Fukuda H, Demura T (2010) VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 22:1249–1263PubMedGoogle Scholar
  195. Yordanov YS, Regan S, Busov V (2010) Members of the LATERAL ORGAN BOUNDARIES DOMAIN transcription factor family are involved in the regulation of secondary growth in Populus. Plant Cell 22:3662–3677PubMedGoogle Scholar
  196. York SW, O’Neill MA (2008) Biochemical control of xylan biosynthesis – which end is up? Curr Opin Plant Biol 11:258–265PubMedGoogle Scholar
  197. Zagórska-Marek B (1995) Morphogenetic waves in cambium and figured wood formation. In: Iqbal M (Hrgs) Encyclopedia of plant anatomy, Band 9, Teil 4, the cambial derivatives. Gebrüder Borntraeger, Berlin, pp 69–69Google Scholar
  198. Zhang J, Elo A, Helariutta Y (2011) Arabidopsis as a model for wood formation. Curr Opin Biotechnol 22:293–299PubMedGoogle Scholar
  199. Zhong R, Ye Z-H (2007) Regulation of cell wall biosynthesis. Curr Opin Plant Biol 10:564–572PubMedGoogle Scholar
  200. Zhong R, Richardson EA, Ye ZH (2007) Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225:1603–1611PubMedGoogle Scholar
  201. Zhong R, Lee C, Ye Z-H (2010) Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Mol Plant 3:1087–1103PubMedGoogle Scholar
  202. Zhong R, McCarthy RL, Lee C, Ye ZH (2011) Dissection of the transcriptional program regulating secondary walls biosynthesis during wood formation in Poplar. Plant Physiol 157:1452–1468PubMedGoogle Scholar
  203. Zhu Z, An F, Feng Y, Li P, Xue L, Mu A, Jiang Z, Kim JM, To TK, Li W et al (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci USA 108:12539–12544PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Institute for Wood BiologyUniversity of HamburgHamburgGermany

Personalised recommendations