Phytochemistry Reviews

, Volume 3, Issue 1–2, pp 29–60 | Cite as

Lignins: Natural polymers from oxidative coupling of 4-hydroxyphenyl- propanoids

  • John Ralph
  • Knut Lundquist
  • Gösta Brunow
  • Fachuang Lu
  • Hoon Kim
  • Paul F. Schatz
  • Jane M. Marita
  • Ronald D. Hatfield
  • Sally A. Ralph
  • Jørgen Holst Christensen
  • Wout Boerjan

Abstract

Lignins are complex natural polymers resulting from oxidative coupling of, primarily, 4-hydroxyphenylpropanoids. An understanding of their nature is evolving as a result of detailed structural studies, recently aided by the availability of lignin-biosynthetic-pathway mutants and transgenics. The currently accepted theory is that the lignin polymer is formed by combinatorial-like phenolic coupling reactions, via radicals generated by peroxidase-H2O2, under simple chemical control where monolignols react endwise with the growing polymer. As a result, the actual structure of the lignin macromolecule is not absolutely defined or determined. The ``randomness'' of linkage generation (which is not truly statistically random but governed, as is any chemical reaction, by the supply of reactants, the matrix, etc.) and the astronomical number of possible isomers of even a simple polymer structure, suggest a low probability of two lignin macromolecules being identical. A recent challenge to the currently accepted theory of chemically controlled lignification, attempting to bring lignin into line with more organized biopolymers such as proteins, is logically inconsistent with the most basic details of lignin structure. Lignins may derive in part from monomers and conjugates other than the three primary monolignols (p-coumaryl, coniferyl, and sinapyl alcohols). The plasticity of the combinatorial polymerization reactions allows monomer substitution and significant variations in final structure which, in many cases, the plant appears to tolerate. As such, lignification is seen as a marvelously evolved process allowing plants considerable flexibility in dealing with various environmental stresses, and conferring on them a striking ability to remain viable even when humans or nature alter ``required'' lignin-biosynthetic-pathway genes/enzymes. The malleability offers significant opportunities to engineer the structures of lignins beyond the limits explored to date.

Abbreviations: 4CL – 4-coumarate:CoA ligase; C3H –p-coumarate 3-hydroxylase; HCT –p-hydroxycinnamoyl-CoA: quinate shikimate p-hydroxycinnamoyltransferase; CCoAOMT – caffeoyl-CoA O-methyltransferase; CCR – cinnamoyl-CoA reductase; F5H – ferulate 5-hydroxylase; CAld5H – coniferaldehyde 5-hydroxylase; COMT – caffeic acid O-methyltransferase; AldOMT – (5-hydroxyconifer)aldehyde O-methyltransferase; CAD – cinnamyl alcohol dehydrogenase; NMR – nuclear magnetic resonance (spectroscopy); DFRC – derivatization followed by reductive cleavage; TIZ – tosylation, iodination, zinc (a DFRC method); DHP – dehydrogenation polymer.

biosynthesis inter-unit linkage lignification lignin model monolignol mutant optical activity oxidative coupling peroxidase polymerization transgenic 

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References

  1. Adler E (1977) Lignin chemistry - past, present and future. Wood Sci. Technol. 11(3): 169–218.Google Scholar
  2. Adler E, Björkquist KJ & Häggroth S (1948) Über die Ursache der Farbreaktionen des Holzes. Acta Chem. Scand. 2: 93–94.Google Scholar
  3. Akiyama T, Nawawi DS, Matsumoto Y & Meshitsuka G (2003) Ratio of erythro and threo forms of β-O-4 structures in different wood species. In: Proceedings of the Twelfth International Symposium on Wood and Pulping Chemistry. Vol 1 (pp. 285–288). Madison, Wisconsin, USA. U. Wisconsin-Madison Press.Google Scholar
  4. Akiyama T, Magara K, Matsumoto Y, Meshitsuka G, Ishizu A & Lundquist K (2000) Proof of the presence of racemic forms of arylglycerol-β-aryl ether structure in lignin: studies on the stereo structure of lignin by ozonation. J. Wood Sci. 46(5): 414–415.Google Scholar
  5. Amaya I, Botella MA, de la Calle M, Medina MI, Heredia A, Bressan RA, Hasegawa PM, Quesada MA & Valpuesta V (1999) Improved germination under osmotic stress of tobacco plants overexpressing a cell wall peroxidase. Febs Letters 457(1): 80–84.Google Scholar
  6. Ämmälahti E, Brunow G, Bardet M, Robert D & Kilpeläinen I (1998) Identification of side-chain structures in a poplar lignin using three-dimensional HMQC-HOHAHA NMR spectroscopy. J. Agric. Food Chem. 46(12): 5113–5117.Google Scholar
  7. Anterola AM & Lewis NG (2002) Trends in lignin modification: a comprehensive analysis of the effects of genetic manipula-tions/ mutations on lignification and vascular integrity. Phytochemistry 61(3): 221–294.Google Scholar
  8. Aoyama W, Sasaki S, Matsumura S, Mitsunaga T, Hirai H, Tsutsumi Y & Nishida T (2002) Sinapyl alcohol-specific peroxidase isoenzyme catalyzes the formation of the dehydrogenative polymer from sinapyl alcohol. Mokuzai Gakkaishi 48: 497–504.Google Scholar
  9. Argyropoulos DS, Jurasek L, Kristofova L, Xia ZC, Sun YJ & Palus E (2002) Abundance and reactivity of dibenzodioxocins in softwood lignin. J. Agric. Food Chem. 50(4): 658–666.Google Scholar
  10. Bardet M, Robert D, Lundquist K & von Unge S (1998) Distribution of erythro and threo forms of different types of β-O-4 structures in aspen lignin by carbon-13 NMR using the 2D INADEQUATE experiment. Magn. Reson. Chem. 36(8): 597–600.Google Scholar
  11. Baucher M, Monties B, Van Montagu M & Boerjan W (1998) Bio-synthesis and genetic engineering of lignin. Crit. Rev. in Plant Sci. 17(2): 125–197.Google Scholar
  12. Baucher M, Halpin C, Petit-Conil M & Boerjan W (2003) Lignin: Genetic engineering and impact on pulping. Critical Reviews in Biochemistry and Molecular Biology 38(4): 305–350.Google Scholar
  13. Baucher M, Chabbert B, Pilate G, VanDoorsselaere J, Tollier MT, Petit-Conil M, Cornu D, Monties B, Van Montagu M, Inze D, Jouanin L & Boerjan W (1996) Red xylem and higher lignin.54 extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar. Plant Physiol. 112(4): 1479–1490.Google Scholar
  14. Björkman A (1957) Studies on finely divided wood. Part 5. The effect of milling. Sven. Papperstidn. 60: 329–335.Google Scholar
  15. Boerjan W, Ralph J & Baucher M (2003) Lignin Biosynthesis. Ann. Rev. Plant Biol. 54: 519–549.Google Scholar
  16. Boudet AM (2000) Lignins and lignification: Selected issues. Plant Physiol. Biochem. 38(1–2): 81–96.Google Scholar
  17. Boudet AM, Lapierre C & Grima-Pettenati J (1995) Biochemistry and molecular biology of lignification. New Phytol. 129(2): 203–236.Google Scholar
  18. Brunow G (2001) Methods to Reveal the Structure of Lignin. In: Hofrichter M & Steinbüchel A, <nt >(ed) </nt >, Lignin, Humic Substances and Coal, Vol 1 (pp. 89–116). Wiley-VHC, Weinheim.Google Scholar
  19. Brunow G & Lundquist K (1980) Comparison of a synthetic de-hydrogenation polymer of coniferyl alcohol with milled wood lignin from spruce, using 1 H NMR nuclear magnetic resonance spectroscopy. Paperi jaa Puu 62(11): 669–670.Google Scholar
  20. Brunow G & Wallin H (1981) Studies concerning the preparation of synthetic lignin. In: Proceedings of the Ekman-Days 1981, International Symposium on Wood and Pulping Chemistry. Vol 4 (pp. 125–127). Stockholm, Sweden. SPCI (Svenska Pappers-och Cellulosaingeniörsföreningen, The Swedish Association of Pulp and Paper Engineers), Stockholm, Sweden.Google Scholar
  21. Brunow G & Lundquist K (1991) On the acid-catalyzed alkylation of lignins. Holzforschung 45(1): 37–40.Google Scholar
  22. Brunow G, Sipilä J & Mäkelä T (1989) On the mechanism of formation of non-cyclic benzyl ethers during lignin biosynthesis. Part 1: The reactivity of β–0–4 quinone methides with phenols and alcohols. Holzforschung 43(1): 55–59.Google Scholar
  23. Brunow G, Lundquist K & Gellerstedt G (1999) Lignin. In: Sjöström E & Alén R, <nt >(ed) </nt >, Analytical Methods in Wood Chemistry, Pulping, and Papermaking, (pp. 77–124). Springer-Verlag, Germany.Google Scholar
  24. Brunow G, Karlsson O, Lundquist K & Sipilä J (1993) On the distri-bution of the diastereomers of the structural elements in lignins: the steric course of reactions mimicking lignin biosynthesis. Wood Sci. Technol. 27(4): 281–286.Google Scholar
  25. Brunow G, Sipilä J, Syrjänen K, Karhunen P, Setälä H & Rummakko P (1995) Oxidative coupling of phenols and the biosynthesis of lignin. In: Proceedings of the Eighth International Symposium on Wood and Pulping Chemistry. Vol I (pp. 33–35). Helsinki, Finland. KCL (Oy Keskuslaboratorio - Centrallaboratoriuum ab), Espoo, Finland.Google Scholar
  26. Bunzel M, Ralph J, Funk C & Steinhart H (2003) Isolation and identification of a ferulic acid dehydrotrimer from saponified maize bran insoluble fiber. European Food Research and Technology 217(2): 128–133.Google Scholar
  27. Carnachan SM & Harris PJ (2000) Ferulic acid is bound to the primary cell walls of all gymnosperm families. Biochemical Systematics and Ecology 28: 865–879.Google Scholar
  28. Carpin S, Crevecoeur M, de Meyer M, Simon P, Greppin H & Penel C (2001) Identification of a Ca2+-pectate binding site on an apoplastic peroxidase. Plant Cell 13(3): 511–520.Google Scholar
  29. Carpita NC & Gibeaut DM (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): 1–30.Google Scholar
  30. Chang H-M, Cowling EB, Brown W, Adler E & Miksche G (1975) Comparative studies on cellulolytic enzyme lignin and milled wood lignin of sweetgum and spruce. Holzforschung 29(5): 153–159.Google Scholar
  31. Cherney JH, Cherney DJR, Akin DE & Axtell JD (1991) Poten-tial of brown-midrib, low-lignin mutants for improving forage quality. Adv. Agron 46: 157–198.Google Scholar
  32. Christensen JH, Bauw G, Welinder KG, Van Montagu M & Boerjan W (1998) Purification and characterization of peroxidases cor-related with lignification in poplar xylem. Plant Physiol. 118(1): 125–135.Google Scholar
  33. Christensen JH, Baucher M, O'Connell AP, Van Montagu M & Boerjan W (2000a) Control of lignin biosynthesis. In: Jain SM & Minocha SC, <nt >(ed) </nt >, Molecular Biology of Woody Plants, Vol 1 (Forestry Sciences, Vol. 64) (pp. 227–237). Kluwer Academic Publishers, Dordrecht.Google Scholar
  34. Christensen JH, Overney O, Bauw G, Simon P, Van Montagu M & Boerjan W (2000b) Expression of poplar xylem peroxidases in tobacco leaves, insect cells, and transgenic poplars. Plant Peroxidase Newslett. 14: 49–53.Google Scholar
  35. Christensen JH, Overney S, Rohde A, Diaz WA, Bauw G, Simon P, Van Montagu M & Boerjan W (2001) The syringaldazine-oxidizing peroxidase PXP 3–4 from poplar xylem: cDNA isol-ation, characterization and expression. Plant Mol. Biol. 47(5): 581–593.Google Scholar
  36. Davin LB & Lewis NG (2000) Dirigent proteins and dirigent sites explain the mystery of specificity of radical precursor coupling in lignan and lignin biosynthesis. Plant Physiol. 123(2): 453–461.Google Scholar
  37. Davin LB, Wang H-B, Crowell AL, Bedgar DL, Martin DM, Sarkanen S & Lewis NG (1997) Stereoselective biomolecu-lar phenoxy radical coupling by an auxiliary (dirigent) protein without an active center. Science 275: 362–366.Google Scholar
  38. Dixon RA, Chen F, Guo DJ & Parvathi K (2001) The biosynthesis of monolignols: a "metabolic grid", or independent pathways to guaiacyl and syringyl units? Phytochemistry 57(7): 1069–1084.Google Scholar
  39. Donaldson LA (1994) Mechanical constraints on lignin deposition during lignification. Wood Sci. Technol. 28(2): 111–118.Google Scholar
  40. Donaldson LA (2001) Lignification and lignin topochemistry - an ultrastructural view. Phytochemistry 57(6): 859–873.Google Scholar
  41. Ede RM & Brunow G (1992) Application of two-dimensional homo-and heteronuclear correlation NMR spectroscopy to wood lignin structure determination. J. Org. Chem. 57(5): 1477–1480.Google Scholar
  42. Ede RM, Brunow G, Simola LK & Lemmetyinen J (1990) Two-dimensional proton-proton chemical shift correlation and J-resolved NMR studies on isolated and synthetic lignins. Holzforschung 44(2): 95–101.Google Scholar
  43. Ede RM, Ralph J, Torr KM & Dawson BSW (1996) A 2D NMR investigation of the heterogeneity of distribution of diarylpro-pane structures in extracted Pinus radiata lignins. Holzforschung 50(2): 161–164.Google Scholar
  44. Egea C, Ahmed AS, Candela M & Candela ME (2001) Elicitation of peroxidase activity and lignin biosynthesis in pepper suspension cells by Phytophthora capsici. J. Plant Physiol. 158(2): 151–158.Google Scholar
  45. El Mansouri I, Mercado JA, Santiago-Domenech N, Pliego-Alfaro F, Valpuesta V & Quesada MA (1999) Biochemical and phenotypical characterization of transgenic tomato plants overexpressing a basic peroxidase. Physiologia Plantarum 106(4): 355–362.Google Scholar
  46. Elfstrand M, Sitbon F, Lapierre C, Bottin A & von Arnold S (2002) Altered lignin structure and resistance to pathogens in spi 2-expressing tobacco plants. Planta 214(5): 708–716.Google Scholar
  47. Elfstrand M, Fossdal CG, Sitbon F, Olsson O, Lonneborg A & von Arnold S (2001) Overexpression of the endogenous peroxidase-like gene spi 2 in transgenic Norway spruce plants results in increased total peroxidase activity and reduced growth. Plant Cell Rep. 20(7): 596–603.Google Scholar
  48. Erdtman H (1933) Dehydrierungen in der Coniferylreihe. II. Dehydrodi-isoeugenol. Annalen 503: 283–294.Google Scholar
  49. Erdtman H (1957) Outstanding problems in lignin chemistry. Ind. Eng. Chem. 49(9): 1385–1386.Google Scholar
  50. Faix O (1986) Investigation of lignin polymer models (DHPs) by FTIR spectroscopy. Holzforschung 40(5): 273–280.Google Scholar
  51. Faix O & Beinhoff O (1988) FTIR spectra of milled wood lign-ins and lignin polymer models (DHPs) with enhanced resolu-tion obtained by deconvolution. J. Wood Chem. Technol. 8(4): 505–522.Google Scholar
  52. Fournand D, Cathala B & Lapierre C (2003) Initial steps of the peroxidase-catalyzed polymerization of coniferyl alcohol and/or sinapyl aldehyde: capillary zone electrophoresis study of pH effect. Phytochemistry 62(2): 139–146.Google Scholar
  53. Franke R, Hemm MR, Denault JW, Ruegger MO, Humphreys JM & Chapple C (2002) Changes in secondary metabolism and de-position of an unusual lignin in the ref8 mutant of Arabidopsis. Plant J. 30(1): 47–59.Google Scholar
  54. Freudenberg K (1956) Beiträge zur Erforschung des Lignins. Angew. Chem. 68(16): 508–512.Google Scholar
  55. Freudenberg K & Neish AC (1968) Constitution and Biosynthesis of Lignin. Springer-Verlag, Berlin-Heidelberg-New York.Google Scholar
  56. Fukagawa N, Meshitsuka G & Ishizu A (1991) A two dimensional NMR study of birch milled wood lignin. J. Wood Chem. Technol. 11(3): 373–396.Google Scholar
  57. Fukushima K & Terashima N (1991) Heterogeneity in formation of lignin. Part XV: Formation and structure of lignin in compres-sion wood of Pinus thunbergii studied by microautoradiography. Wood Sci. Technol. 25: 371–381.Google Scholar
  58. Gagnaire D & Robert D (1978) Carbon-13 NMR study of a poly-mer model of lignin, DHP, carbon-13 selectively labeled at the benzylic positions. In: Proceedings of the Proc. Eur. Conf. NMR Macromol. (pp. 517–519). Rome, Italy. Lerici, Rome, Italy.Google Scholar
  59. Gang DR, Costa MA, Fujita M, Dinkova-Kostova AT, Wang HB, Burlat V, Martin W, Sarkanen S, Davin LB & Lewis NG (1999) Regiochemical control of monolignol radical coupling: a new paradigm for lignin and lignan biosynthesis. Chem. Biol. 6(3): 143–151.Google Scholar
  60. Gellerstedt G & Zhang L (1991) Reactive lignin structures in high yield pulping. Part 1. Structures of the 1,2-diarylpropane-1,3-diol type. Nord. Pulp Pap. Res. J. 6(3): 136–139.Google Scholar
  61. Gould RF <nt >(ed.) </nt > (1966) Lignin Structure and Reactions. Advances in Chemistry Series, Vol 59. Amer. Chem. Soc., Washington, DC.Google Scholar
  62. Grabber JH, Hatfield RD & Ralph J (1998) Diferulate cross-links impede the enzymatic degradation of nonlignified maize walls. J. Sci. Food Agric. 77(2): 193–200.Google Scholar
  63. Grabber JH, Ralph J & Hatfield RD (2002) Model studies of ferulate-coniferyl alcohol cross-product formation in primary maize walls: implications for lignification in grasses. J. Agric. Food Chem. 50(21): 6008–6016.Google Scholar
  64. Grabber JH, Ralph J, Hatfield RD & Quideau S (1997) p-Hydroxyphenyl, guaiacyl, and syringyl lignins have similar inhibitory effects on wall degradability. J. Agric. Food Chem. 45(7): 2530–2532.Google Scholar
  65. Grabber JH, Ralph J, Lapierre C & Barrière Y (2004) Genetic and molecular basis of grass cell wall biosynthesis and degradability. I. Components and structure of cell walls in grasses. Comptes Rend. Biologies 327(5): 455–465.Google Scholar
  66. Guan SY, Mylnar J & Sarkanen S (1997) Dehydrogenative polymerization of coniferyl alcohol on macromolecular lignin templates. Phytochemistry 45(5): 911–918.Google Scholar
  67. Guo DG, Chen F, Wheeler J, Winder J, Selman S, Peterson M & Dixon RA (2001) Improvement of in-rumen digestib-ility of alfalfa forage by genetic manipulation of lignin O-methyltransferases. Transgenic Res. 10(5): 457–464.Google Scholar
  68. Halpin C, Knight ME, Foxon GA, Campbell MM, Boudet A-M, Boon JJ, Chabbert B, Tollier M-T & Schuch W (1994) Manipulation of lignin quality by downregulation of cinnamyl alcohol dehydrogenase. Plant J. 6(3): 339–350.Google Scholar
  69. Harkin JM (1967) Lignin - a natural polymeric product of phenol oxidation. In: Taylor WI & Battersby AR, <nt >(ed) </nt >, Oxidative Coupling of Phenols, (pp. 243–321). Marcel Dekker, New York.Google Scholar
  70. Harkin JM (1973) Lignin. In: Butler GW, <nt >(ed) </nt >, Chemistry and Bio-chemistry of Herbage, Vol 1 (pp. 323–373). Academic Press, London.Google Scholar
  71. Hatfield RD & Vermerris W(2001) Lignin Formation in Plants. The Dilemma of Linkage Specificity. Plant Physiol. 126(4): 1351–1357.Google Scholar
  72. Hergert HL (1977) Secondary lignification in conifer trees. In: Arthur JC, <nt >(ed) </nt >, Cellulose Chemistry and Technology, Vol 48, Amer. Chem. Soc. Symp. Ser. (pp. 227–243). American Chem. Soc., Washington, DC.Google Scholar
  73. Hertzberg M, Aspeborg H, Schrader J, Andersson A, Erlandsson R, Blomqvist K, Bhalerao R, Uhlen M, Teeri TT, Lundeberg J, Sundberg B, Nilsson P & Sandberg G (2001) A transcriptional roadmap to wood formation. Proc. Natl. Acad. Sci. USA 98(25): 14732–14737.Google Scholar
  74. Higuchi T (1980) Biochemistry of Lignification. Wood Res. 66: 1–16.Google Scholar
  75. Higuchi T (1990) Lignin biochemistry: biosynthesis and biodegradation. Wood Sci. Technol. 24(1): 23–63.Google Scholar
  76. Higuchi T (2003) Pathways for monolignol biosynthesis via metabolic grids: coniferyl aldehyde 5-hydroxylase, a possible key enzyme in angiosperm syringyl lignin biosynthesis. Proc. Japan Acad. Series B-Physical and Biological Sciences 79(8): 227–236.Google Scholar
  77. Higuchi T & Nakatsubo F (1980) Synthesis and biodegradation of oligolignols. Kem. - Kemi 7(9): 481–488.Google Scholar
  78. Higuchi T, Ito T, Umezawa T, Hibino T & Shibata D (1994) Red-brown color of lignified tissues of transgenic plants with antisense CAD gene: Wine-red lignin from coniferyl aldehyde. J. Biotechnol. 37(2): 151–158.Google Scholar
  79. Hori K & Meshitsuka G (2000) Structural heterogeneity of hard-wood lignin: Characteristics of end-wise lignin fraction. In: Glasser WG, Northey RA & Schultz TP, <nt >(ed) </nt >, Lignin: Historical, Biological, and Materials Perspectives, Vol 742, Amer. Chem. Soc. Symp. Ser. (pp. 172–185). American Chemical Society, Washington, DC.Google Scholar
  80. Huh GH, Yun BW, Lee HS, Jo JK & Kwak SS (1998) Overproduction of sweet potato peroxidases in transgenic tobacco plants. Phytochemistry 47(5): 695–700.Google Scholar
  81. Humphreys JM & Chapple C (2002) Rewriting the lignin roadmap. Curr. Opin. Plant Biol. (5): 224–229.Google Scholar
  82. Humphreys JM, Hemm MR & Chapple C (1999) Ferulate 5-hydroxylase from Arabidopsis is a multifunctional cytochrome P450-dependent monooxygenase catalyzing parallel hydroxylations in phenylpropanoid metabolism. Proc. Natl. Acad. Sci. USA 96(18): 10045–10050.Google Scholar
  83. Huntley SK, Ellis D, Gilbert M, Chapple C & Mansfield SD (2003) Significant increases in pulping efficiency in C4H-F5H-transformed poplars: Improved chemical savings and reduced environmental toxins. J. Agric. Food Chem. 51(21): 6178–6183.Google Scholar
  84. Hwang BH & Sakakibara A (1981) Hydrogenolysis of protolignin. XVIII. Isolation of a new dimeric compound with a heterocycle Involving α, α-diether. Holzforschung 35(6): 297–300.Google Scholar
  85. Ikeda T, Holtman K, Kadla JF, Chang HM & Jameel H (2002) Studies on the effect of ball milling on lignin structure using a modified DFRC method. J. Agric. Food Chem. 50(1): 129–135.Google Scholar
  86. Jacquet G, Pollet B, Lapierre C, Francesch C, Rolando C & Faix O (1997) Thioacidolysis of enzymatic dehydrogenation polymers from p-hydroxyphenyl, guaiacyl, and syringyl precursors. Holzforschung 51(4): 349–354.Google Scholar
  87. Jouanin L, Goujon T, de Nadaï V, Martin M-T, Mila I, Vallet C, Pollet B, Yoshinaga A, Chabbert B, Petit-Conil M & Lapierre C (2000) Lignification in transgenic poplars with extremely reduced caffeic acid O-methyltransferase activity. Plant Physiol. 123(4): 1363–1373.Google Scholar
  88. Jurasek L (1996) Morphology of computer-modeled lignin structure: Fractal dimensions, orientation and porosity. J. Pulp Paper Sci. 22(10): J376–J380.Google Scholar
  89. Jurasek L (1998a) Experimenting with virtual lignins. In: Lewis NG & Sarkanen S, <nt >(ed) </nt >, Lignin and Lignan Biosynthesis, Vol 697, Amer. Chem. Soc. Symp. Ser. (pp. 276–293). American Chemical Society, Washington, DC.Google Scholar
  90. Jurasek L (1998b) Molecular modelling of fibre walls. J. Pulp Paper Sci. 24(7): 209–212.Google Scholar
  91. Karhunen P, Rummakko P, Sipilä J, Brunow G & Kilpeläinen I (1995a) The formation of dibenzodioxocin structures by oxidative coupling. A model reaction for lignin biosynthesis. Tetrahedron Lett. 36(25): 4501–4504.Google Scholar
  92. Karhunen P, Rummakko P, Sipilä J, Brunow G & Kilpeläinen I (1995b) Dibenzodioxocins; a novel type of linkage in softwood lignins. Tetrahedron Lett. 36(1): 169–170.Google Scholar
  93. Katahira R, Ujihara M & Nakatsubo F (2003) A novel selective cleavage method for β-O-4 substructure in lignins named TIZ method. I. Degradation of guaiacyl and syringyl models. J. Wood Chem. Technol. 23(1): 71–87.Google Scholar
  94. Katayama T, Davin LB, Chu A & Lewis NG (1993) Novel benzylic ether reductions in lignan biogenesis in Forsythia intermedia. Phytochemistry 33(3): 581–591.Google Scholar
  95. Katayama Y & Fukuzumi T (1978) Enzymic synthesis of three lignin-related dimers by an improved peroxidase-hydrogen peroxide system. Mokuzai Gakkaishi 24(9): 664–667.Google Scholar
  96. Kawaoka A, Matsunaga E, Endo S, Kondo S, Yoshida K, Shinmyo A & Ebinuma H (2003) Ectopic expression of a horseradish peroxidase enhances growth rate and increases oxidative stress resistance in hybrid aspen. Plant Physiol. 132(3): 1177–1185.Google Scholar
  97. Kawaoka A, Kawamoto T, Moriki H, Murakami A, Murakami K, Yoshida K, Sekine M, Takano M & Shinmyo A (1994) Growth-stimulation of tobacco plant introduced the horseradish-peroxidase gene Prxc1a. J. Ferment. Bioeng. 78(1): 49–53.Google Scholar
  98. Kilpeläinen I, Ämmälahti E, Brunow G & Robert D (1994a) Application of three-dimensional HMQC-HOHAHA NMR spectroscopy to wood lignin, a natural polymer. Tetrahedron Lett. 35(49): 9267–9270.Google Scholar
  99. Kilpeläinen I, Sipilä J, Brunow G, Lundquist K & Ede RM (1994b) Application of two-dimensional NMR spectroscopy to wood lignin determination; Identification of some minor structural units of hard-and softwood lignins. J. Agric. Food Chem. 42(12): 2790–2794.Google Scholar
  100. Kim H, Ralph J, Yahiaoui N, Pean M & Boudet A-M (2000) Cross-coupling of hydroxycinnamyl aldehydes into lignins. Org. Lett. 2(15): 2197–2200.Google Scholar
  101. Kim H, Ralph J, Lu F, Pilate G, Leplé JC, Pollet B & Lapierre C (2002) Identification of the structure and origin of thioacidolysis marker compounds for cinnamyl alcohol dehydrogenase deficiency in angiosperms. J. Biol. Chem. 277(49): 47412–47419.Google Scholar
  102. Kim H, Ralph J, Lu F, Ralph SA, Boudet A-M, MacKay JJ, Se-deroff RR, Ito T, Kawai S, Ohashi H & Higuchi T (2003) NMR Analysis of Lignins in CAD-deficient Plants. Part 1. Incorporation of hydroxycinnamaldehydes and hydroxybenzaldehydes into lignins. Org. Biomol. Chem. 1: 158–281.Google Scholar
  103. Kondo T, Mizuno K & Kato T (1987) Some characteristics of forage plant lignin. Japan Agricultural Research Quarterly 21(1): 47–52.Google Scholar
  104. Kristensen BK, Brandt J, Bojsen K, Thordal-Christensen H, Kerby KB, Collinge DB, Mikkelsen JD & Rasmussen SK (1997) Expression of a defence-related intercellular barley peroxidase in transgenic tobacco. Plant Sci. 122(2): 173–182.Google Scholar
  105. Kukkola EM, Haakana K, Koutaniemi S, H. TT, Brunow G, Saranpää P, Kilpeläinen I, Ruel K & Fagerstedt KV (2001) Localization of dibenzodioxocin structure in lignifying Norway spruce xylem by immunogold labeling. In: Proceedings of the 8th International Conference on Biotechnology in the Pulp and Paper Industry, Pre-symposium on Recent Advances in Lignin Biodegradation and Biosynthesis. Vol 1 (pp. 68–69). Viikki Biocenter, University of Helsinki, Finland. U. Helsinki Press.Google Scholar
  106. Lagrimini LM, Gingas V FF & Rothstein S LT (1997a) Characterization of antisense transformed plants deficient in the tobacco anionic peroxidase. Plant Physiol. 114(4): 1187–1196.Google Scholar
  107. Lagrimini LM, Vaughn J, Erb WA & Miller SA (1993) Peroxidase overproduction in tomato: Wound-induced polyphenol deposition and disease resistance. Hortscience 28(3): 218–221.Google Scholar
  108. Lagrimini LM, Joly RJ, Dunlap JR & Liu TTY (1997b) The consequence of peroxidase overexpression in transgenic plants on root growth and development. Plant Mol. Biol. 33(5): 887–895.Google Scholar
  109. Landucci LL & Ralph SA (2001) Reaction of p-hydroxycinnamyl alcohols with transition metal salts. IV. Tailored syntheses of β-O-4 trimers. J. Wood Chem. Technol. 21(1): 31–52.Google Scholar
  110. Landucci LL, Deka GC & Roy DN (1992) A 13C NMR study of milled wood lignins from hybrid Salix Clones. Holzforschung 46(6): 505–511.Google Scholar
  111. Lapierre C & Lundquist K (1999) Investigations of low molecular weight and high molecular weight lignin fractions. Nord. Pulp Pap. Res. J. 14(2): 158–162, 170.Google Scholar
  112. Lapierre C, Lallemand JY & Monties B (1982) Evidence of poplar lignin heterogeneity by combination of carbon-13 and proton NMR spectroscopy. Holzforschung 36(6): 275–282.Google Scholar
  113. Lapierre C, Tollier MT & Monties B (1988) A new type of constitutive unit in lignins from the corn bm3 mutant. C. R. Acad. Sci., Ser. 3 307(13): 723–728.Google Scholar
  114. Lapierre C, Pollet B, Monties B & Rolando C (1991) Thioacidolysis of spruce lignin: gas chromatography-mass spectroscopy analysis of the main dimers recovered after Raney nickel desulfurization. Holzforschung 45(1): 61–68.Google Scholar
  115. Lapierre C, Pollet B, MacKay JJ & Sederoff RR (2000) Lignin structure in a mutant pine deficient in cinnamyl alcohol dehydrogenase. J. Agric. Food Chem. 48(6): 2326–2331.Google Scholar
  116. Lapierre C, Kim H, Lu F, Marita JM, Mila I, Pollet B & Ralph J (2001) Marker compounds for enzyme deficiencies in the lignin biosynthetic pathway. In: Proceedings of the 11th Internat. Symp. Wood and Pulping Chemistry. Vol II (pp. 23–26). Nice, France. Association Technique de l'Industrie Papetière (ATIP), Paris.Google Scholar
  117. Lapierre C, Pilate G, Pollet B, Mila I, Leplé JC, Jouanin L, Kim H & Ralph J (2004) Signatures of cinnamyl alcohol dehydrogenase deficiency in poplar lignins. Phytochemistry 65(3): 313–321.Google Scholar
  118. Lapierre C, Pollet B, Petit-Conil M, Toval G, Romero J, Pilate G, Leple JC, Boerjan W, Ferret V, De Nadai V & Jouanin L (1999) Structural alterations of lignins in transgenic poplars with depressed cinnamyl alcohol dehydrogenase or caffeic acid O-methyltransferase activity have an opposite impact on the efficiency of industrial kraft pulping. Plant Physiol. 119(1): 153–163.Google Scholar
  119. Lewis NG (1999) A 20th century roller coaster ride: a short account of lignification. Current Opin. Plant Biol. 2(2): 153–162.Google Scholar
  120. Lewis NG & Davin LB (1998) The biochemical control of monolignol coupling and structure during lignan and lignin biosynthesis. In: Lewis NG & Sarkanen S, <nt >(ed) </nt >, Lignin and Lignan Biosynthesis, Vol 697, Amer. Chem. Soc. Symp. Ser. (pp. 334–361). Amer. Chem. Soc., Washington, DC.Google Scholar
  121. Lewis NG & Sarkanen S <nt >(ed) </nt > (1998) Lignin and Lignan Biosyn-thesis. Amer. Chem. Soc. Symp. Ser., Vol 697. Amer. Chem. Soc., Washington, DC.Google Scholar
  122. Lewis NG, Davin LB & Sarkanen S (1998a) Lignin and lignan biosynthesis: distinctions and reconciliations. In: Lewis NG & Sarkanen S, <nt >(ed) </nt >, Lignin and Lignan Biosynthesis, Vol 697, Amer. Chem. Soc. Symp. Ser. (pp. 1–27). Amer. Chem. Soc., Washington, DC.Google Scholar
  123. Lewis NG, Davin LB & Sarkanen S (1999) The nature and function of lignins. In: Barton DHR & Nakanishi K, <nt >(ed) </nt >, Comprehensive Natural Products Chemistry, Vol 3 (pp. 617–745). Elsevier.Google Scholar
  124. Lewis NG, Newman J, Just G & Ripmeister J (1987) Determination of bonding patterns of carbon-13 specifically enriched dehydrogenatively polymerized lignin in solution and solid state. Macromolecules 20(8): 1752–1756.Google Scholar
  125. Lewis NG, Jiao Y, Kasahara H, Fujita M, Bedgar DL & Davin LB (1998b) The 'abnormal' lignins: a rediscovery of non-structural infusions? In: Proceedings of the Third Tannin Conference. Bend, Oregon (USA).Google Scholar
  126. Li L, Popko JL, Umezawa T & Chiang VL (2000) 5-Hydroxyconiferyl aldehyde modulates enzymatic methylation for syringyl monolignol formation, a new view of monolignol biosynthesis in angiosperms. J. Biol. Chem. 275(9): 6537–6545.Google Scholar
  127. Li L, Cheng XF, Leshkevich J, Umezawa T, Harding SA & Chiang VL (2001) The last step of syringyl monolignol biosynthesis in angiosperms is regulated by a novel gene encoding sinapyl alcohol dehydrogenase. Plant Cell 13(7): 1567–1585.Google Scholar
  128. Li L, Zhou Y, Cheng X, Sun J, Marita JM, Ralph J & Chiang VL (2003a) Combinatorial modification of multiple lignin traits in trees through multigene cotransformation. Proc. Nat. Acad. Sci. 100(8): 4939–4944.Google Scholar
  129. Li S & Lundquist K (2001) Analysis of hydroxyl groups in lignins by 1 H NMR spectrometry. Nord. Pulp Pap. Res. J. 16(1): 63–67.Google Scholar
  130. Li S, Lundquist K & Stenhagen G (1996) Studies on the formation of 1-(4-hydroxy-3,5-dimethoxyphenyl)-2-(4-hydroxy-3-methoxyphenyl)-1-propanone and 2-(4-hydroxy-3,5-dimethox-yphenyl)-1-(4-hydroxy-3-methoxyphenyl)-1-propanone on acid treatment of birch lignin. Holzforschung 50: 253–257.Google Scholar
  131. Li S, Iliefski T, Lundquist K & Wallis AFA (1997) Reassignment of relative stereochemistry at C-7 and C-8 in arylcoumaran neolignans. Phytochemistry 46(5): 929–934.Google Scholar
  132. Li YH, Kajita S, Kawai S, Katayama Y & Morohoshi N (2003b) Down-regulation of an anionic peroxidase in transgenic aspen and its effect on lignin characteristics. J. Plant Res. 116(3): 175–182.Google Scholar
  133. Lin SY & Dence CW (1992) Methods in Lignin Chemistry. Springer-Verlag, Heidelberg.Google Scholar
  134. Lu F & Ralph J (1997) The DFRC method for lignin analysis. Part 1. A new method for β-aryl ether cleavage: lignin model studies. J. Agric. Food Chem. 45(12): 4655–4660.Google Scholar
  135. Lu F & Ralph J (2002) Preliminary evidence for sinapyl acetate as a lignin monomer in kenaf. J. Chem. Soc., Chem. Commun. (1): 90–91.Google Scholar
  136. Lu F & Ralph J (2003) Non-degradative dissolution and acetylation of ball-milled plant cell walls; high-resolution solution-state NMR. Plant J. 35(4): 535–544.Google Scholar
  137. Lu F & Ralph J (2004) Why do COMT-deficient plants pulp inefficiently? Holzforschung: submitted.Google Scholar
  138. Lu F, Ralph J, Morreel K & Boerjan W (2004) Preparation and relevance of a cross-coupling product between sinapyl alcohol and sinapyl p-hydroxybenzoate. Org. Biomol. Chem.: submitted.Google Scholar
  139. Lu F, Ralph J, Marita JM, Lapierre C, Jouanin L & Boerjan W (2003) Sequencing around 5-hydroxyconiferyl alcohol-derived units in COMT-deficient lignins. In: Proceedings of the Twelfth International Symposium on Wood and Pulping Chemistry. Vol 3 (pp. 115–118). Madison, Wisconsin, USA. U. Wisconsin-Madison Press.Google Scholar
  140. Lundquist K (1970) Acid degradation of lignin. II. Separation and identification of low-molecular weight phenols. Acta Chem. Scand. 24(3): 889–907.Google Scholar
  141. Lundquist K (1973) Acid degradation of lignin. Part VIII. Low molecular weight phenols from acidolysis of birch lignin. Acta Chem. Scand. 27(7): 2597–2606.Google Scholar
  142. Lundquist K (1987) On the occurrence of β-1 structures in lignins. J. Wood Chem. Technol. 7(2): 179–185.Google Scholar
  143. Lundquist K (1992a) Acidolysis. In: Lin SY & Dence CW, <nt >(ed) </nt >, Methods in Lignin Chemistry, (pp. 287–300). Springer-Verlag, Heidelberg.Google Scholar
  144. Lundquist K (1992b) Isolation and purification: Wood. In: Lin SY & Dence CW, <nt >(ed) </nt >, Methods in Lignin Chemistry, (pp. 65–70). Springer-Verlag, Heidelberg.Google Scholar
  145. Lundquist K (1992c) 1 H NMR spectral studies of lignins. Results regarding the occurrence of β-5 structures, β-β-structures, non-cyclic benzyl aryl ethers, carbonyl groups and phenolic groups. Nord. Pulp Pap. Res. J. 7(1): 4–8, 16.Google Scholar
  146. Lundquist K & Miksche GE (1965) Nachweis eines neuen Verknüp-fungsprinzips von Guajacylpropaneinheiten im Fichtenlignin. Tetrahedron Lett. (25): 2131–2136.Google Scholar
  147. Lundquist K & Stomberg R (1988) On the occurrence of structural elements of the lignan type ( β-β structures) in lignins. The crystal structures of (+)-pinoresinol and ( ±)-trans-3,4-divanillyltetrahydrofuran. Holzforschung 42(6): 375–384.Google Scholar
  148. Lundquist K & Stern K (1989) Analysis of lignins by 1 H NMR spectroscopy. Nord. Pulp Pap. Res. J. 4: 210–213.Google Scholar
  149. Lundquist K, Ohlsson B & Simonson R (1977) Isolation of lignin by means of liquid-liquid extraction. Sven. Paperstidn. 80: 143–144.Google Scholar
  150. Lundquist K, Miksche GE, Ericsson L & Berndtson L (1967) Über das Vorkommen von Glyceraldehyd-2-arylätherstrukturen im Lignin (On the occurrence of glyceraldehyde 2-aryl ethers in lignin). Tetrahedron Lett. (46): 4587–4591.Google Scholar
  151. Lundquist K, Langer V, Li S & Stomberg R (2003) Lignin stereochemistry and its biosynthetic implications. In: Proceedings of the Twelfth International Symposium on Wood and Pulping Chemistry. Vol 1 (pp. 239–244). Madison, Wisconsin, USA. U. Wisconsin-Madison Press.Google Scholar
  152. Mackay J, Omalley D & Sederoff R (1995) Effect of a null mutation at the Cad (cinnamyl alcohol-dehydrogenase) locus on lignin biosynthesis in Loblolly pine. Plant Physiol. 108(2): 49 Suppl.Google Scholar
  153. MacKay JJ, Dimmel DR & Boon JJ (2001) Pyrolysis MS characterization of wood from CAD-deficient pine. J. Wood Chem. Technol. 21: 19–29.Google Scholar
  154. Mäder M (1992) Compartmentation of peroxidase isoenzymes in plant cells. In: Penel C, Gaspar T & Greppin H, <nt >(ed) </nt >, Plant Peroxidases 1980–1990, Topics and Detailed Literature on Molecular, Biochemical and Physiological Aspects, (pp. 37–46). Université de Genève, Genève, Switzerland.Google Scholar
  155. Marita J, Ralph J, Hatfield RD & Chapple C (1999) NMR characterization of lignins in Arabidopsis altered in the activity of ferulate-5-hydroxylase. Proc. Natl. Acad. Sci. USA 96(22): 12328–12332.Google Scholar
  156. Marita JM, Vermerris W, Ralph J & Hatfield RD (2003a) Variations in the cell wall composition of maize brown midrib mutants. J. Agric. Food Chem. 51(5): 1313–1321.Google Scholar
  157. Marita JM, Ralph J, Lapierre C, Jouanin L & Boerjan W (2001) NMR characterization of lignins from transgenic poplars with suppressed caffeic acid O-methyltransferase activity. J. Chem. Soc., Perkin Trans. 1 (22): 2939–2945.Google Scholar
  158. Marita JM, Ralph J, Hatfield RD, Guo D, Chen F & Dixon RA (2003b) Structural and compositional modifications in lignin of transgenic alfalfa down-regulated in caffeic acid 3-O-methyltransferase and caffeoyl coenzyme A 3-O-methyltransferase. Phytochemistry 62(1): 53–65.Google Scholar
  159. Matsumoto Y, Ishizu A & Nakano J (1981) Estimation of glyceraldehyde-2-aryl ether type structure in lignin by the use of ozonolysis. Mokuzai Gakkaishi 27(10): 750–751.Google Scholar
  160. McIntyre CL, Bettenay HM & Manners JM(1996) Strategies for the suppression of peroxidase gene expression in tobacco. II. In vivo suppression of peroxidase activity in transgenic tobacco using ribozyme and antisense constructs. Transgenic Res. 5(4): 263–270.Google Scholar
  161. Meyer K, Shirley AM, Cusumano JC, Bell-Lelong DA & 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(12): 6619–6623.Google Scholar
  162. Meyermans H, Morreel K, Lapierre C, Pollet B, De Bruyn A, Busson R, Herdewijn P, Devreese B, Van Beeumen J, Marita JM, Ralph J, Chen C, Burggraeve B, Van Montagu M, Messens E & Boerjan W (2000) Modifications 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(47): 36899–36909.Google Scholar
  163. Monties B & Lapierre C (1981) Donnés récentes sur l'hétérogénéite de la lignine. Physiologie Végétale 19(3): 327–348.Google Scholar
  164. Monties BL (1989) Lignins. In: Harborne J, <nt >(ed) </nt >, Methods in Plant Biochemistry, Vol 1 (pp. 113–157). Academic Press, London.Google Scholar
  165. Morreel K, Ralph J, Kim H, Lu F, Goeminne G, Ralph SA, Messens E & Boerjan W (2004) Targeted phenolic profiling of oligolignols from lignifying poplar xylem. submitted.Google Scholar
  166. Müsel G, Schindler T, Bergfeld R, Ruel K, Jacquet G, Lapierre C, Speth V & Schopfer P (1997) Structure and distribution of lignin in primary and secondary cell walls of maize coleoptiles analyzed by chemical and immunological probes. Planta 201(2): 146–159.Google Scholar
  167. Nakano J, Ishizu A & Migata N (1961) Studies on lignin. XXXII. Ester groups of lignin. Tappi 44(1): 30–32.Google Scholar
  168. Nimz H (1974) Beech lignin - Proposal of a constitutional scheme. Angew. Chem., Int. Ed. 13(5): 313–321.Google Scholar
  169. Nimz H & Lüdemann H-D (1974) 13 C-Kernresonanzspektren von Ligninen, 5. Oligomere Ligninmodellsubstanzen. Makromol. Chem. 175: 2577–2583.Google Scholar
  170. Nimz HH, Robert D, Faix O & Nemr M (1981) Carbon-13 NMR spectra of lignins, 8. Structural differences between lignins of hardwoods, softwoods, grasses and compression wood. Holzforschung 35(1): 16–26.Google Scholar
  171. Obst JR (1983) Kinetics of alkaline cleavage of β-aryl ether bonds in lignin models: significance to delignification. Holzforschung 37(1): 23–28.Google Scholar
  172. Obst JR & Kirk TK (1988) Isolation of lignin. Methods Enzymol. 161(Biomass, Pt. B): 3–12.Google Scholar
  173. Önnerud H & Gellerstedt G (2003) Inhomogeneities in the chemical structure of hardwood lignins. Holzforschung 57(3): 255–265.Google Scholar
  174. Osakabe K, Tsao CC, Li L, Popko JL, Umezawa T, Carraway DT, Smeltzer RH, Joshi CP & Chiang VL (1999) Coniferyl al-dehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms. Proc. Natl. Acad. Sci. USA 96: 8955–8960.Google Scholar
  175. Otter T & Polle A (1997) Characterisation of acidic and basic apoplastic peroxidases from needles of Norway spruce (Picea abies, L, Karsten) with respect to lignifying substrates. Plant Cell Physiol. 38(5): 595–602.Google Scholar
  176. Patten AM, Anterola AM, Chung B-Y, Davin LB & Lewis NG (2003) Confocal microscopy and laser excision microdissection/ chemical analyses of Arabidopsis lignifying xylem and interfascicular fibers genetically altered in lignin monomer composition: evidence for differential control of monolignol polymerization. In: Proceedings of the 14th International Conference on Arabidopsis Research. Vol 1 (pp. Poster No. 68). Madison, WI, USA. Wisconsin Union Conference Services, Madison, WI, USA.Google Scholar
  177. Peng J, Lu F & Ralph J (1998) The DFRC method for lignin analysis. Part 4. Lignin dimers isolated from DFRC-degraded loblolly pine wood. J. Agric. Food Chem. 46(2): 553–560.Google Scholar
  178. Pilate G, Guiney E, Holt K, Petit-Conil M, Lapierre C, Leple JC, Pollet B, Mila I, Webster EA, Marstorp HG, Hopkins DW, Jouanin L, Boerjan W, Schuch W, Cornu D & Halpin C (2002) Field and pulping performances of transgenic trees with altered lignification. Nature Biotechnol. 20(6): 607–612.Google Scholar
  179. Quiroga M, Guerrero C, Botella MA, Ros Barceló A, Amaya I, Medina MI, Alonso FJ, de Forchetti SM, Tigier H & Valpuesta V (2000) A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiol. 122(4): 1119–1127.Google Scholar
  180. Ralph J (1993) 1H NMR of acetylated β-ether/ β-ether lignin model trimers. Magn. Reson. Chem. 31(4): 357–363.Google Scholar
  181. Ralph J (1996) An unusual lignin from Kenaf. J. Nat. Prod. 59(4): 341–342.Google Scholar
  182. Ralph J (1997) Recent advances in characterizing 'non-traditional' lignins and lignin-polysaccharide cross-linking. In: Proceedings of the 9th International Symposium on Wood and Pulping Chemistry. Vol 1 (pp. 1–7, paper PL2). Montreal, Quebec. CPPA (Canadian Pulp and Paper Association), Montreal, Quebec.Google Scholar
  183. Ralph J (2001) Poplar Lignin Models, available from http://www.dfrc.ars.usda.gov/LigninModels.html, US Dairy Forage Research Center: Madison.Google Scholar
  184. Ralph J & Grabber JH (1996) Dimeric β-ether thioacid-olysis products resulting from incomplete ether cleavage. Holzforschung 50(5): 425–428.Google Scholar
  185. Ralph J, Grabber JH & Hatfield RD (1995) Lignin-ferulate cross-links in grasses: active incorporation of ferulate polysaccharide esters into ryegrass lignins. Carbohydr. Res. 275(1): 167–178.Google Scholar
  186. Ralph J, Peng J & Lu F (1998a) Isochroman structures in lignin: a new β-1 pathway. Tetrahedron Lett. 39(28): 4963–4964.Google Scholar
  187. Ralph J, Quideau S, Grabber JH & Hatfield RD (1994a) Identification and synthesis of new ferulic acid dehydrodimers present in grass cell walls. J. Chem. Soc., Perkin Trans. 1 (23): 3485–3498.Google Scholar
  188. Ralph J, Peng J, Lu F & Hatfield RD (1999a) Are lignins optically active? J. Agric. Food Chem. 47(8): 2991–2996.Google Scholar
  189. Ralph J, Kim H, Peng J & Lu F (1999b) Arylpropane-1,3-diols in lignins from normal and CAD-deficient pines. Org. Lett. 1(2): 323–326.Google Scholar
  190. Ralph J, Hatfield RD, Quideau S, Helm RF, Grabber JH & Jung H-JG (1994b) Pathway of p-coumaric acid incorporation into maize lignin as revealed by NMR. J. Amer. Chem. Soc. 116(21): 9448–9456.Google Scholar
  191. Ralph J, MacKay JJ, Hatfield RD, O'Malley DM, Whetten RW & Sederoff RR (1997) Abnormal lignin in a loblolly pine mutant. Science 277: 235–239.Google Scholar
  192. Ralph J, Hatfield RD, Grabber JH, Jung HG, Quideau S & Helm RF (1998b) Cell wall cross-linking in grasses by ferulates and diferulates. In: Lewis NG & Sarkanen S, <nt >(ed) </nt >, Lignin and Lignan Biosynthesis, Vol 697, Amer. Chem. Soc. Symp. Ser. (pp. 209–236). American Chemical Society, Washington, DC.Google Scholar
  193. Ralph J, Hatfield RD, Piquemal J, Yahiaoui N, Pean M, Lapierre C & Boudet A-M (1998c) NMR characterization of altered lignins extracted from tobacco plants down-regulated for lignification enzymes cinnamyl-alcohol dehydrogenase and cinnamoyl-CoA reductase. Proc. Nat. Acad. Sci. 95(22): 12803–12808.Google Scholar
  194. Ralph J, Lapierre C, Lu F, Marita JM, Pilate G, Van Doors-selaere J, Boerjan W & Jouanin L (2001a) NMR evidence for benzodioxane structures resulting from incorporation of 5-hydroxyconiferyl alcohol into lignins of O-methyl-transferase-deficient poplars. J. Agric. Food Chem. 49(1): 86–91.Google Scholar
  195. Ralph J, Marita J, Lu F, Hatfield RD, Lapierre C, Ralph SA, Vermerris W, Boerjan W & Jouanin L (2001b) 5-Hydroxyconiferyl alcohol as a monolignol in COMT-deficient angiosperms. In: Proceedings of the 11th Internat. Symp. Wood and Pulping Chemistry. Vol II (pp. 27–30). Nice, France. Association Technique de l'Industrie Papetière (ATIP), Paris.Google Scholar
  196. Ralph J, Bunzel M, Marita JM, Hatfield RD, Lu F, Kim H, Schatz PF, Grabber JH & Steinhart H (2004) Peroxidase-dependent cross-linking reactions of p-hydroxycinnamates in plant cell walls. Phytochem. Reviews: 3: 79–96.Google Scholar
  197. Ralph J, Bunzel M, Marita JM, Hatfield RD, Lu F, Kim H, Grabber JH, Ralph SA, Jimenez-Monteon G & Steinhart H (2000) Diferulates analysis: new diferulates and disinapates in insoluble cereal fibre. Polyphénols Actualités (19): 13–17.Google Scholar
  198. Ralph J, Marita JM, Ralph SA, Hatfield RD, Lu F, Ede RM, Peng J, Quideau S, Helm RF, Grabber JH, Kim H, Jimenez-Monteon G, Zhang Y, Jung H-JG, Landucci LL, MacKay JJ, Sederoff RR, Chapple C & Boudet AM(1999c) Solution-state NMR of lignins. In: Argyropoulos DS & Rials T, <nt >(ed) </nt >, Advances in Lignocellulosics Characterization, (pp. 55–108). TAPPI Press, Atlanta, GA.Google Scholar
  199. Ralph J, Lapierre C, Marita J, Kim H, Lu F, Hatfield RD, Ralph SA, Chapple C, Franke R, Hemm MR, Van Doorsselaere J, Sederoff RR, O'Malley DM, Scott JT, MacKay JJ, Yahiaoui N, Boudet A-M, Pean M, Pilate G, Jouanin L & Boerjan W (2001c) Elucidation of new structures in lignins of CAD-and COMT-deficient plants by NMR. Phytochemistry 57(6): 993–1003.Google Scholar
  200. Ray H, Douches DS & Hammerschmidt R (1998) Transformation of potato with cucumber peroxidase: expression and disease response. Physiol. Mol. Plant Path. 53(2): 93–103.Google Scholar
  201. Robert DR & Brunow G (1984) Quantitative estimation of hydroxyl groups in milled wood lignin from spruce and in a dehydrogenation polymer from coniferyl alcohol using carbon-13 NMR spectroscopy. Holzforschung 38(2): 85–90.Google Scholar
  202. Rolando C, Monties B & Lapierre C (1992) Thioacidolysis. In: Dence CW & Lin SY, <nt >(ed) </nt >, Methods in Lignin Chemistry, (pp. 334–349). Springer-Verlag, Berlin-Heidelberg.Google Scholar
  203. Ros Barceló A, Pedreño MA, Munoz R & Sabater F (1989) Physiological Significance of the Binding of Acidic Isoperoxidases to Cell-Walls of Lupin. Physiologia Plantarum 75(2): 267–274.Google Scholar
  204. Rouau X, Cheynier V, Surget A, Gloux D, Barron C, Meuded E, Louis-Montero J & Criton M (2003) A dehydrodimer of ferulic acid from maize bran. Phytochemistry 63: 899–903.Google Scholar
  205. Rouhi AM (2001) Only facts will end the lignin war. Chem. Eng. News (April 2): 52–56.Google Scholar
  206. Sakakibara A (1980) A structural model of softwood lignin. Wood Sci. Technol. 14(2): 89–100.Google Scholar
  207. Sakakibara A (1991) Chemistry of lignin. In: Hon DN-S & Shiraishi N, <nt >(ed) </nt >, Wood and Cellulosic Chemistry, (pp. 113–175). Marcel Dekker, New York.Google Scholar
  208. Sakakibara A, Sasaya T, Miki K & Takahashi H (1987) Lignans and Brauns' lignins from softwoods. Holzforschung 41(1): 1–11.Google Scholar
  209. Sakihama Y, Cohen MF, Grace SC & Yamasaki H (2002) Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology 177(1): 67–80.Google Scholar
  210. Sarkanen KV (1971) Precursors and their polymerization. In: Sarkanen KV & Ludwig CH, <nt >(ed) </nt >, Lignins, Occurrence, Formation, Structure and Reactions, (pp. 95–163). Wiley-Interscience, New York.Google Scholar
  211. Sarkanen KV & Ludwig CH (1971) Lignins, Occurrence, Formation, Structure and Reactions. Wiley-Interscience, New York.Google Scholar
  212. Sarkanen KV & Hergert HL (1971) Classification and Distribution. In: Sarkanen KV & Ludwig CH, <nt >(ed) </nt >, Lignins. Occurrence, Formation, Structure and Reactions, (pp. 43–94). Wiley-Interscience, New York.Google Scholar
  213. Sarkanen S (1998) Template polymerization in lignin biosynthesis. In: Lewis NG & Sarkanen S, <nt >(ed) </nt >, Lignin and Lignan Biosyn-thesis, Vol 697, Amer. Chem. Soc. Symp. Ser. (pp. 194–208). Amer. Chem. Soc., Washington, DC.Google Scholar
  214. Sasaki S, Nishida T, Tsutsumi Y & Kondo R (2004) Lignin de-hydrogenative polymerization mechanism: a poplar cell wall peroxidase directly oxidizes polymer lignin and produces in vitro dehydrogenative polymer rich in β-O-4 linkage. FEBS Lett. 562(pp1–3): 197–201.Google Scholar
  215. Sato Y, Sugiyama M, Gorecki RJ, Fukuda H & Komamine A (1993) Interrelationship between lignin deposition and the activities of peroxidase isoenzymes in differentiating tracheary elements of Zinnia - Analysis using L-α-aminooxy-β-phenylpropionic acid and 2-aminoindan-2-phosphonic acid. Planta 189(4): 584–589.Google Scholar
  216. Schmidt Michael WI, Knicker H, Hatcher Patrick G & Koegel Knabner I (1997) Does ultrasonic dispersion and homogeniza-tion by ball milling change the chemical structure of organic matter in geochemical samples?-a CPMAS 13 C NMR study with lignin. Org. Geochem. 26: 7–8.Google Scholar
  217. Schreiber SL (1999) Using synthesis to explain life's unsolved mysteries. Chem. Eng. News (July 26): 43–45.Google Scholar
  218. Sederoff R & Chang HM (1991) Lignin biosynthesis. In: Lewin M & Goldstein IS, <nt >(ed) </nt >, Wood structure and composition, (pp. 263–285). Marcel Dekker, New York.Google Scholar
  219. Sederoff RR, MacKay JJ, Ralph J & Hatfield RD (1999) Unexpected variation in lignin. Current Opin. Plant Biol. 2(2): 145–152.Google Scholar
  220. Setälä H, Pajunen A, Rummakko P, Sipilä J & Brunow G (1999) A novel type of spiro compound formed by oxidative cross-coupling of methyl sinapate with a syringyl lignin model com-pound. A model system for the β-1 pathway in lignin biosynthesis. J. Chem. Soc., Perkin Trans. 1 (4): 461–464.Google Scholar
  221. Sherf BA, Bajar AM & Kolattukudy PE (1993) Abolition of an Inducible Highly Anionic Peroxidase-Activity in Transgenic Tomato. Plant Physiol. 101(1): 201–208.Google Scholar
  222. Smith DCC (1955) p-Hydroxybenzoates groups in the lignin of Aspen (Populus tremula). J. Chem. Soc.: 2347.Google Scholar
  223. Sudo K & Sakakibara A (1974) Hydrogenolysis of protolignin. XI. Mokuzai Gakkaishi 20(8): 396–401.Google Scholar
  224. Sun RC, Fang JM & Tomkinson J (1999) Fractional isolation and structural characterization of lignins from oil palm trunk and empty fruit bunch fibres. J. Wood Chem. Technol. 19(4): 335–356.Google Scholar
  225. Syrjanen K & Brunow G (1998) Oxidative cross coupling of p-hydroxycinnamic alcohols with dimeric arylglycerol β-aryl ether lignin model compounds. The effect of oxidation potentials. J. Chem. Soc. Perkin Trans. 1 (20): 3425–3429.Google Scholar
  226. Syrjanen K & Brunow G (2000) Regioselectivity in lignin biosynthesis. The influence of dimerization and cross-coupling. J. Chem. Soc. Perkin Trans. 1 (2): 183–187.Google Scholar
  227. Syrjanen K & Brunow G (2001) Regioselectivity in oxidative cross-coupling of phenols. Application to the synthesis of dimeric neolignans. Tetrahedron 57(2): 365–370.Google Scholar
  228. Takahama U (1995) Oxidation of hydroxycinnamic acid and hydroxycinnamyl alcohol derivatives by laccase and peroxidase - interactions among p-hydroxyphenyl, guaiacyl and syringyl groups during the oxidation reactions. Physiologia Plantarum 93(1): 61–68.Google Scholar
  229. Takahama U & Oniki T (1996) Enhancement of peroxidase-dependent oxidation of sinapyl alcohol by esters of 4-coumaric and ferulic acid. In: Obinger C, Burner U, Ebermann R, Penel C & Greppin H, <nt >(ed) </nt >, Plant Peroxidases, Biochemistry and Physiology, (pp. 118–123). Université de Genève, Genève, Switzerland.Google Scholar
  230. Takahama U & Oniki T (1997) A peroxidase/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells. Physiologia Plantarum 101(4): 845–852.Google Scholar
  231. Takahama U, Oniki T & Shimokawa H (1996) A possible mechanism for the oxidation of sinapyl alcohol by peroxidase-dependent reactions in the apoplast: Enhancement of the oxidation by hydroxycinnamic acids and components of the apoplast. Plant Cell Physiol. 37(4): 499–504.Google Scholar
  232. Talas-O?ra? T, Kazan K & Gözükirmizi N (2001) Decreased peroxidase activity in transgenic tobacco and its effect on lignification. Biotechnol. Lett. 23(4): 267–273.Google Scholar
  233. Tanahashi M, Takeuchi H & Higuchi T (1976) Dehydrogenative polymerization of 3,5-disubstituted p-coumaryl alcohols. Wood Res. 61: 44–53.Google Scholar
  234. Terashima N, Fukushima K & Takabe K (1986) Heterogeneity in formation of lignin. VIII. An autoradiographic study on the form-ation of guaiacyl and syringyl lignin in Magnolia kobus DC. Holzforschung 40(Suppl.): 101–105.Google Scholar
  235. Terashima N, Fukushima K, He L-F & Takabe K (1993) Comprehensive model of the lignified plant cell wall. In: Jung HG, Buxton DR, Hatfield RD & Ralph J, <nt >(ed) </nt >, Forage Cell Wall Structure and Digestibility, (pp. 247–270). ASA-CSSA-SSSA, Madison.Google Scholar
  236. Terashima N, Awano T, Takabe K & Yoshida M (2004) Formation of macromolecular lignin in ginkgo xylem cell walls as observed by electron microscopy. Comptes Rend. Biologies 327(6): in press.Google Scholar
  237. Terashima N, Atalla RH, Ralph SA, Landucci LL, Lapierre C & Monties B (1995) New preparations of lignin polymer models under conditions that approximate cell well lignification. I: Synthesis of novel lignin polymer models and their structural characterization by 13 C NMR. Holzforschung 49(6): 521–527.Google Scholar
  238. Thorburn WM (1918) The myth of occam's razor. Mind 27: 345–353.Google Scholar
  239. Timell TE (1982) Recent progress in the chemistry and topochemistry of compression wood. Wood Sci. Technol. 16(2): 83–122.Google Scholar
  240. Tognolli M, Penel C, Greppin H & Simon P (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288(1–2): 129–138.Google Scholar
  241. Tollier MT, Monties B, Lapierre C, Herve du Penhoat C & Rolando C (1986) Inhomogeneity of angiosperm lignin: comparison of the monomeric composition of lignin fractions isolated from different wood species. Holzforschung 40(Suppl.): 75–79.Google Scholar
  242. Tsutsumi Y, Matsui K & Sakai K (1998) Substrate-specific peroxidases in woody angiosperms and gymnosperms participate in regulating the dehydrogenative polymerization of syringyl and guaiacyl type lignins. Holzforschung 52(3): 275–281.Google Scholar
  243. 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 & Jouanin L (1995) A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic acid O-methyltransferase activity. Plant J. 8(6): 855–864.Google Scholar
  244. Welinder KG (1992) Plant peroxidases: structure - function relationships. In: Penel C, Gaspar T & Greppin H, <nt >(ed) </nt >, Plant Peroxidases 1980 - 1990, Topics and Detailed Literature on Molecular, Biochemical and Physiological Aspects, (pp. 1–24). Université de Genève, Genève, Switzerland.Google Scholar
  245. Whetten R & Sederoff R (1995) Lignin Biosynthesis. Plant Cell 7: 1001–1013.Google Scholar
  246. Yasuda S & Sakakibara A (1976) Hydrogenolysis of protolignin in compression wood. II. Mokuzai Gakkaishi 22(11): 606–612.Google Scholar
  247. Yasuda S & Sakakibara A (1977) Hydrogenolysis of protolignin in compression wood. III. Isolation of four dimeric compounds with carbon to carbon linkage. Mokuzai Gakkaishi 23(2): 114–119.Google Scholar
  248. Zablackis E, York WS, Pauly M, Hantus S, Reiter WD, Chapple CCS, Albersheim P & Darvill A (1996) Substitution of L-fucose by L-galactose in cell walls of Arabidopsis mur1. Science 272(5269): 1808–1810.Google Scholar
  249. Zhang L & Gellerstedt G (2001) NMR observation of a new lignin structure, a spiro-dienone. Chem. Commun. (24): 2744–2745.Google Scholar
  250. Zhang L & Gellerstedt G (2004) Observation of a novel β- β-structure in native lignin by high resolution 2D NMR techniques. In: Proceedings of the Eighth European Workshop on Lignocellulosics and Pulp. Riga, Latvia. Latvian State Institute of Wood Chemistry, Riga, Latvia.Google Scholar
  251. Zhang L, Henriksson G & Gellerstedt G (2003) The formation of β - β structures in lignin biosynthesis - are there two different pathways? Org. Biomol. Chem. 1(20): 3621–3624.Google Scholar
  252. Zhang L, Gellerstedt G, Lu F & Ralph J (2004) NMR studies on the occurrence of spiro-dienone structures in lignins. J. Wood Chem. Technol.: submitted.Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • John Ralph
    • 1
    • 2
  • Knut Lundquist
    • 2
  • Gösta Brunow
    • 3
  • Fachuang Lu
    • 1
    • 2
  • Hoon Kim
    • 1
    • 2
  • Paul F. Schatz
    • 1
  • Jane M. Marita
    • 1
  • Ronald D. Hatfield
    • 1
  • Sally A. Ralph
    • 4
  • Jørgen Holst Christensen
    • 5
  • Wout Boerjan
    • 5
  1. 1.U.S. Dairy Forage Research CenterUSDA-Agricultural Research ServiceMadisonU.S.A
  2. 2.Department of ForestryU. Wisconsin-MadisonMadisonU.S.A
  3. 3.Department of ChemistryUniversity of HelsinkiHelsinkiFinland
  4. 4.USDA-Forest ServiceMadisonU.S.A
  5. 5.Department of Plant Systems BiologyFlanders Interuniversity Institute for Biotechnology, Universiteit GentGentBelgium

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