Advertisement

Lignin manipulation for fibre improvement

  • Jennifer Stephens
  • Claire Halpin

Abstract

For centuries plant fibres have been used in a number of commercial areas including textiles, construction, paper and pulp, reinforced composites, and as biomass for energy production. These fibres come from a whole host of crops ranging from cotton, jute and flax for textiles; wood crops such as poplar, eucalyptus and conifers for paper and pulp; and cereal crops such as maize, sorghum and barley to provide straw, bedding and animal fodder. In more recent years the popularity of fibre crops in some of these areas has been superseded by synthetic fibres such as those made from plastic or glass. Environmentally, these synthetic fibres are non-renewable and continue to accumulate as sources of pollution. The impact of this pollution has led to a renewed interest in the use of plant fibres as a sustainable commodity for the future.

Keywords

Caffeic Acid Lignin Content Secondary Cell Wall Kraft Pulp Lignin Biosynthesis 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abbott JC, Barakate A, Pinçon G, Legrand M, Lapierre C, Mila I, Schuch W, Halpin C (2002) Simultaneous suppression of multiple genes by single transgenes. Down-regulation of three unrelated lignin biosynthetic genes in tobacco. Plant Physiol. 128:844–853PubMedCrossRefGoogle Scholar
  2. Atanassova R, Favet N, Martz F, Chabbert B, Tollier MT, Monties B, Fritig B, Legrand M (1995) Altered lignin composition in transgenic tobacco expressing O-methyltransferase sequences in sense and antisense orientation. Plant J. 8:465–477CrossRefGoogle Scholar
  3. Barriere Y, Guillet C, Goffner D, Pichon M (2003) Genetic variation and breeding strategies for improved cell wall digestibility in annual forage crops. A review. Anim. Res. 52:193–228Google Scholar
  4. Barriere Y, Ralph J, Mechin V, Guillaumie S, Grabber JH, Argillier O, Chabbert B, Lapierre C (2004) Genetic and molecular basis of grass cell wall biosynthesis and degradability. II. Lessons from brown-midrib mutants. C.R. Biol. 327:847–860PubMedCrossRefGoogle Scholar
  5. Baucher M, Chabbert B, Pilate G, Van Doorsselaere 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 extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar. Plant Physiol. 112:1479–1490PubMedGoogle Scholar
  6. Baucher M, Petit-Conil M, Boerjan W (2003) Lignin: genetic engineering and impact on pulping. Crit. Rev. Biochem. Mol. 38:305–350CrossRefGoogle Scholar
  7. Bernard-Vailhe MA, Migne C, Cornu A, Maillot MP, Grenet E, Besle JM, Atanassova R, Martz F, Legrand M (1996) Effect of modification of the O-methyltransferase activity on cell wall composition, ultrastructure and degradability of transgenic tobacco. J. Sci. Food Agric. 72:385–391CrossRefGoogle Scholar
  8. Bernard-Vailhe MA, Besle JM, Maillot MP, Cornu A, Halpin C, Knight M. (1998). Effect of down-regulation of cinnamyl alcohol dehydrogenase on cell wall composition and on degradability of tobacco stems. J. Sci. Food Agric. 76:505–514CrossRefGoogle Scholar
  9. Blee KA, Choi JW, O’Connell AP, Schuch W, Lewis NG, Bolwell GP (2003) A lignin-specific peroxidase in tobacco whose antisense suppression leads to vascular tissue modification. Phytochem. 64:163–176CrossRefGoogle Scholar
  10. Blount JW, Korth KL, Masoud SA, Rasmussen S, Lamb C, Dixon RA (2000) Altering expression of cinnamic acid 4-hydroxylase in transgenic plants provides evidence for a feedback loop at the entry point into the phenylpropanoid pathway. Plant Physiol. 122:107–116PubMedCrossRefGoogle Scholar
  11. Boerjan W, Ralph J, Baucher M (2003) Lignin Biosynthesis. Annu. Rev. Plant Biol. 54:519–546PubMedCrossRefGoogle Scholar
  12. Bout S, Vermerris W (2003) A candidate-gene approach to clone the sorghum brown midrib gene caffeic acid O-methyltransferase. Mol. Genet. Genomics 269:205–214PubMedGoogle Scholar
  13. Campbell MM, Sederoff RR (1996) Variation in lignin content and composition. Mechanisms of control and implications for the genetic improvement of plants. Plant Physiol. 110:3–13PubMedGoogle Scholar
  14. Chabannes M, Barakate A, Lapierre C, Marit JM, Ralph J, Pean M, Danoun S, Halpin C, Grima-Pettenati J, Boudet AM (2001a) Strong decrease in lignin content without significant alteration of plant development is induced by simultaneous down-regulation of cinnamoyl CoA reductase (CCR) and cinnamyl alcohol dehydrogenase (CAD) in tobacco plants. Plant J. 28:257–270CrossRefGoogle Scholar
  15. Chabannes M, Ruel K, Yoshinaga A, Chabbert B, Jauneau A, Joseleau JP, Boudet AM (2001b) In situ analysis of lignins in transgenic tobacco reveals a differential impact of individual transformations on the spatial patterns of lignin deposition at the cellular and subcellular levels. Plant J. 28:271–282CrossRefGoogle Scholar
  16. Cherney JH, Axtell JD, Hassen MM, Anliker KS (1988) Forage quality characterization of a chemically induced brown-midrib mutant in pearl millet. Crop Sci. 28:783–787CrossRefGoogle Scholar
  17. Cherney JH, Cherney DJR, Akin DE, Axtell JD (1991) Potential of brown-midrib, low lignin mutants for improving forage quality. Adv. Agron. 46:157–198CrossRefGoogle Scholar
  18. Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: The basic concepts. Euphytica 142:169–196CrossRefGoogle Scholar
  19. Davin LB, Wang HB, Crowell AL, Bedgar DL, Martin DM, Sarkanen S, Lewis NG (1997). Stereoselective bimolecular phenoxy radical coupling by an auxiliary (dirigent) protein without an active center. Science 275:362–366PubMedCrossRefGoogle Scholar
  20. Dharmawardhana DP, Ellis BE, Carlson JE (1999) cDNA cloning and heterologous expression of coniferin beta-glucosidase. Plant Mol. Biol. 40:365–372PubMedCrossRefGoogle Scholar
  21. Ebskamp MJM (2002) Engineering flax and hemp for an alternative to cotton. Trends Biotechnol. 20:229–230PubMedCrossRefGoogle Scholar
  22. Franke R, Hemm MR, Denault JW, Ruegger MO, Humphreys JM, Chapple C (2002) Changes in secondary metabolism and deposition of an unusual lignin in the refs mutant of Arabidopsis. Plant J. 30:47–59PubMedCrossRefGoogle Scholar
  23. Fritz JO, Cantrell RP, Lechtenberg VL, Axtell JD, Hertel JM (1981) Brown midrib mutants in sudangrass and grain sorghum. Crop Sci. 21:706–709CrossRefGoogle Scholar
  24. Goujon T, Ferret V, Mila I, Pollet B, Ruel K, Burlat V, Joseleau JP, Barriere Y, Lapierre C, Jouanin L (2003) Down-regulation of the AtCCRl gene in Arabidoipsis thaliana: effects on phenotype, lignins and cell wall degradability. Plants 217:218–228Google Scholar
  25. Guillet-Claude C, Birolleau-Touchard C, Manicacci D, Fourmann M, Barraud S, Carret V, Martinant JP, Barriere Y (2004) Genetic diversity associated with variation in silage corn digestibility for three O-methyltransferase genes involved in lignin biosynthesis. Theor. Appl. Genet. 110:126–135PubMedCrossRefGoogle Scholar
  26. Guo D, Chen F, Inoue K, Blount JW, Dixon RA (2001a) Downregulation of caffeic acid 3-O-methyltransferase and caffeoyl CoA 3-O-methyltransferase in transgenic alfalfa: impact on lignin structure and implications for the biosynthesis of G and S lignin. Plant Cell 13:73–88CrossRefGoogle Scholar
  27. Guo D, Chen F, Wheeler J, Winder J, Selman S, Peterson M, Dixon RA (2001b) Improvement of in-rumen digestibility of alfalfa forage by genetic manipulation of lignin O-methyltransferases. Transgenic Res. 10:457–464CrossRefGoogle Scholar
  28. Halpin C (2004) Investigating and manipulating lignin biosynthesis in the post-genomic era. Adv. Bot. Res. 41:63–106CrossRefGoogle Scholar
  29. Halpin C, Holt K, Chojecki J, Oliver D, Chabbert B, Monties B, Edwards K, Barakate A, Foxon GA (1998) Brown-midrib maize (bml) – a mutation affecting the cinnamyl alcohol dehydrogenase gene. Plant J. 14:545–553PubMedCrossRefGoogle Scholar
  30. Halpin C, Boerjan W (2003) Stacking Transgenes in Forest Trees. Trends Plant Sci. 8, 363–365PubMedCrossRefGoogle Scholar
  31. Hepworth DG, Vincent JFV (1998) The mechanical properties of xylem tissue from tobacco plants (Nicotiana tabacum ‘Samsun’). Ann. Bot. 81: 75–759Google Scholar
  32. Hepworth DG, Vincent JFV (1999) The growth response of the stems of genetically modified tobacco plants (Nicotiana tabacum ‘Samsun’) to flexural stimulation. Ann. Bot. 83: 39–43CrossRefGoogle Scholar
  33. 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. U.S.A. 98:14732–14737PubMedCrossRefGoogle Scholar
  34. 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. 37:151–158CrossRefGoogle Scholar
  35. Hoffmann L, Besseau S, Geoffroy P, Ritzenthaler C, Meyer D, Lapierre C, Pollet B, Legrand M (2004) Silencing of Hydroxycinnamoyl-Coenzyme A Shikimate/Quinate Hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell 16:1446–1465PubMedCrossRefGoogle Scholar
  36. Hu WJ, Harding SA, Lung J, Popko JL, Ralph J, Stokke DD, Tsai CJ, Chian VL (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees Nat. Biotechnol. 17:808–812CrossRefGoogle Scholar
  37. Humphreys JM, Hemm MR, Chapple C (1999) New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cytochrome P450-dependent monooxygenase. Proc. Natl. Acad. Sci. U.S.A. 96:10045–10050PubMedCrossRefGoogle Scholar
  38. 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. Agr. Food Chem. 51:6178–6183CrossRefGoogle Scholar
  39. Inoue K, Sewalt VJH, Balance GM, Ni W, Sturzer C, Dixon RA (1998) Developmental expression and substrate specificities of alfalfa caffeic acid 3-O-methyltransferase and caffeoyl coenzyme A 3-O-methyltransferase in relation to lignification. Plant Physiol. 117:761–770PubMedCrossRefGoogle Scholar
  40. James C 2005 Global Status of Commercialized Biotech/GM Crops: 2005. ISAAA Briefs No. 34. ISAAA: Ithaca, NYGoogle Scholar
  41. Jones L, Ennos AR, Turner SR (2001) Cloning and characterization of irregular xylem4 (irx4): a severely lignin-deficient mutant of Arabidopsis. Plant J. 26:205–216PubMedCrossRefGoogle Scholar
  42. Jouanin L, Goujon T, De Nadai V, Martin MT, Mila I, Vallet C, Pollet B, Yoshi-naga A, Chabbert B, Petit-Conil M, Lapierre C (2000) Lignification in transgenie poplars with extremely reduced caffeic acid O-methyltransferase activity. Plant Physiol. 123:1363–1373PubMedCrossRefGoogle Scholar
  43. Jung HJG, Ni W, Chapple CCS, Meyer K (1999) Impact of lignin composition on cell-wall degradability in an Arabidopsis mutant. J. Sci. Food Agr. 79:922–928CrossRefGoogle Scholar
  44. Kajita S, Hishiyama S, Tomimura Y, Katayama Y, Omori S (1997) Structural characterization of modified lignin in transgenic tobacco plants in which the activity of 4-Coumarate:Coenzyme A Ligase is depressed. Plant Physiol. 114:871–879PubMedGoogle Scholar
  45. Kajita S, Ishifuji M, Ougiya H, Hara S, Kawabata H, Morohoshi N, Katayama Y (2002) Improvement in pulping and bleaching properties of xylem from transgenic tobacco plants. J. Sci. Food Agric. 82:1216–1223CrossRefGoogle Scholar
  46. Kirst M, Myburg AA, De Leon JPG, Kirst ME, Scott J, Sederoff R (2004) Coordinated genetic regulation of growth and lignin revealed by quantitative trait locus analysis of cDNA microarray data in an interspecific backcross of Eucalyptus. Plant Physiol. 135:2368–2378PubMedCrossRefGoogle Scholar
  47. Koopmann E, Logemann E, Hahlbrock K (1999) Regulation and functional expression of cinnamate 4-hydroxylase from parsley. Plant Physiol. 119:49–55PubMedCrossRefGoogle Scholar
  48. Lagrimini LM, Gingas V, Finger F, Rothstein S, Liu TTY (1997a) Characterization of antisense transformed plants deficient in the tobacco anionic peroxidase. Plant Physiol. 114:1187–1196Google Scholar
  49. 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: 887–895CrossRefGoogle Scholar
  50. Lapierre C, Tollier MT, Monties B (1988) Occurrence of additional monomeric units in the lignins from internodes of a brown-midrib mutant of maize BM3. CR. Acad. Sci. III-Vie 307:723–728Google Scholar
  51. Lapierre C, Pollet B, Petit-Conil M, Toval G, Romero J, Pilate G, Leple JC, Boer Jan 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. 119:153–163PubMedCrossRefGoogle Scholar
  52. Lauer J, Coors J (1997) Brown midrib corn. Wisconsin Crop Manager 4:16–18Google Scholar
  53. Li L, Zhou Y, Cheng X, Sun J, Marit JM, Ralph J, Chiang V (2003a) Combinatorial modification of multiple lignin traits in trees through multigene cotransformation. Proc. Natl. Acad. Sci. U.S.A. 100:4939–4944CrossRefGoogle Scholar
  54. 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. 116:175–182CrossRefGoogle Scholar
  55. Lim EK, Li Y, Parr A, Jackson R, Ashford DA, Bowles DJ (2001). Identification of glucosyltransferase genes involved in sinapate metabolism and lignin synthesis in Arabidopsis. J. Biol. Chem. 276: 4344–4349PubMedCrossRefGoogle Scholar
  56. Lim EK, Jackson RG, Bowles DJ (2005) Identification and characterisation of Arabidopsis glycosyltransferases capable of glucosylating coniferyl aldehyde and sinapyl aldehyde. FEBS Lett. 579: 2802–2806PubMedCrossRefGoogle Scholar
  57. MacKay J, Presnell T, Jameel H, Taneda H, O’Malley D, Sederoff R (1999) Modified lignin and delignification with a CAD-deficient loblolly pine. Holzforschung 53:403–410CrossRefGoogle Scholar
  58. Marita JM, 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. U.S.A. 96:12328–12332PubMedCrossRefGoogle Scholar
  59. Maury S, Geoffroy P, Legrand M (1999) Tobacco O-methyltransferases involved in phenylpropanoid metabolism. The different caffeoyl-coenzyme A/5-hydroxyferuloyl-coenzyme A 3/5-O-methyltransferase and caffeic acid/5-hydroxyferulic acid 3/5-O-methyltransferase classes have distinct substrate specificities and expression patterns. Plant Physiol. 121:215–223PubMedCrossRefGoogle Scholar
  60. Meyer K, Cusumano JC, Somerville C, Chapple CS (1996) Ferulate-5-hydroxylase from Arabidopsis thaliana defines a new family of cytochrome P450-dependent monooxygenases. Proc. Natl. Acad. Sci. U.S.A. 93:6869–6874PubMedCrossRefGoogle Scholar
  61. O’Connell A, Holt K, Piquemal J, Grima-Pettenati J, Boudet A, Pollet B, Lapierre C, Petit-Conil M, Schuch W, Halpin C (2002) Improved paper pulp from plants with suppressed cinnamoyl-CoA reductase or cinnamyl alcohol dehydrogenase. Transgenic Res. 11:495–503PubMedCrossRefGoogle Scholar
  62. Pedersen JF, Vogel KP, Funnell DL (2005) Impact of reduced lignin on plant fitness. Crop Sci. 45:812–819CrossRefGoogle Scholar
  63. Pilate G, Guiney E, Holt K, Petit-Conil M, Lapierre C, Leplé JC, Pollet B, Mila I, Webster EA, Marstorp HG, Hopkins DW, Jouanin L, Boerjan W, Shuch W, Cornu D, Halpin C (2002) Field and pulping performances of transgenic trees with altered lignification. Nat. Biotechnol. 20:606–612CrossRefGoogle Scholar
  64. Pinçon G, Maury S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2001a) Repression of O-methyltransferase genes in transgenic tobacco affects lignin synthesis and plant growth. Phytochemistry 57:1167–1176CrossRefGoogle Scholar
  65. Pinçon G, Chabannes M, Lapierre C, Pollet B, Ruel K, Joseleau JP, Boudet AM, Legrand M (2001b) Simultaneous down-regulation of caffeic/5-hydroxy ferulic acid-O-methyltransferase I and cinnamoyl-coenzyme A reductase in the progeny from a cross between tobacco lines homozygous for each transgene. Consequences for plant development and lignin synthesis. Plant Physiol. 126:145–155CrossRefGoogle Scholar
  66. Piquemal J, Lapierre C, Myton K, O’Connell A, Schuch W, Grima-Pettenati J, Boudet AM (1998) Down-regulation of Cinnamoyl-CoA Reductase induces significant changes of lignin profiles in transgenic tobacco plants. Plant J. 13:71–83CrossRefGoogle Scholar
  67. Porter KS, Axtell JD, Lechtenberg VL, Colenbrander VF (1978) Phenotype, fiber composition, and in vitro dry matter disappearance of chemically induced brown midrib (bmr) mutants of sorghum. Crop Sci. 18:205–208CrossRefGoogle Scholar
  68. Raes J, Rohde A, Christensen JH, Van de Peer Y, Boerjan W (2003) Genomewide characterization of the lignification toolbox in Arabidopsis. Plant Physiol. 133:1051–1071PubMedCrossRefGoogle Scholar
  69. Ralph J, Hatfield RD, Piquemal J, Yahiaoui N, Pean M, Lapierre C, Boudet AM (1998) NMR characterization of altered lignins extracted from tobacco plants down-regulated for lignification enzymes cinnamyl-alcohol dehydrogenase and cinnamoyl-CoA reductase. Proc. Natl. Acad. Sci. U.S.A. 95:12803–12808PubMedCrossRefGoogle Scholar
  70. Ralph J, Akiyama T, Kim H, Lu FC, Schatz PF, Marita JM, Ralph SA, Reddy MSS, Chen F, Dixon RA (2006) Effects of coumarate 3-hydroxylase down-regulation on lignin structure. J. Biol. Chem. 281:8843–8853PubMedCrossRefGoogle Scholar
  71. Ranalli P, Venturi G (2004) Hemp as a raw material for industrial applications. Euphytica 140:1–6CrossRefGoogle Scholar
  72. Ranocha P, Chabannes M, Chamayou S, Danoun S, Jauneau A, Boudet AM, Goffner D (2002) Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar. Plant Physiol. 129:145–155PubMedCrossRefGoogle Scholar
  73. Reddy MSS, Chen F, Shadle G, Jackson L, Aljoe H, Dixon RA (2005) Targeted down-regulation of cytochrome P450 enzymes for forage quality improvement in alfalfa (Medicago saliva L.) Proc. Natl. Acad. Sci. U.S.A. 102:16573–16578PubMedCrossRefGoogle Scholar
  74. Samuels AL, Rensing KH, Douglas CJ, Mansfield SD, Dharmawardhana DP, Ellis BE (2002) Cellular machinery of wood production: differentiation of secondary xylem in Pinus contorta var. latifolia. Planta 216:72–82PubMedCrossRefGoogle Scholar
  75. Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D (2001) CYP98A3 from Arabidopsis thaliana is a 3’-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J. Biol. Chem. 276:36566–36574PubMedCrossRefGoogle Scholar
  76. Sengupta G, Palit P (2004) Characterization of a lignified secondary phloem fibredeficient mutant of jute (Corchorus capsularis). Ann. Bot.-London 93:211–220CrossRefGoogle Scholar
  77. Sewalt VJH, Ni W, Blount JW, Jung HG, Masoud SA, Howles PA, Lamb C, Dixon RA (1997a) Reduced lignin content and altered lignin composition in transgenic tobacco down-regulated in expression of L-phenylalanine ammonia-lyase or cinnamate 4-hydroxylase. Plant Physiol. 115:41–50Google Scholar
  78. Sewalt VJH, Ni WT, Jung HG, Dixon RA (1997b) Lignin impact on fiber degradation: Increased enzymatic digestibility of genetically engineered tobacco (Nicotiana tabacum) stems reduced in lignin content J. Agric. Food Chem. 45:1977–1983CrossRefGoogle Scholar
  79. Thumma BR, Nolan MF, Evans R, Moran GF (2005) Polymorphisms in Cinnamoyl CoA Reductase (CCR) are associated with variation in microfibril angle in Eucalyptus spp. Genetics 171:1257–1265PubMedCrossRefGoogle Scholar
  80. Vermerris W, Boon JJ (2001) Tissue-specific patterns of lignification are disturbed in the brown midrib2 mutant of maize (Zea mays L.) J. Agr. Food Chem. 49:721–728CrossRefGoogle Scholar
  81. Vignols F, Rigau J, Torres MA, Capellades M, Puigdomenech P (1995) The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. Plant Cell 7:407–416PubMedCrossRefGoogle Scholar
  82. Wang HM, Postle R, Kessler RW, Kessler W (2003) Removing pectin and lignin during chemical processing of hemp for textile applications. Text. Res. J. Aug 2003Google Scholar
  83. Wanner LA, Li G, Ware D, Somssich IE, Davis KR (1995) The phenylalanine ammonia-lyase gene family in Arabidopsis thaliana. Plant Mol. Biol. 27:327–338PubMedCrossRefGoogle Scholar
  84. Zhang K, Qian Q, Huang Z, Wang Y, Li M, Hong L, Zeng D, Gu M, Chu C, Cheng Z (2006) Gold hull and internode2 encodes a primarily multifunctional cinnamyl alcohol dehydrogenase in rice. Plant Physiol. 140:972–983PubMedCrossRefGoogle Scholar
  85. Zhong RQ, Morrison WH, Negrel J, Ye ZH (1998) Dual methylation pathways in lignin biosynthesis. Plant Cell 10:2033–2045PubMedCrossRefGoogle Scholar
  86. Zhong RQ, Morrison WH, Himmelsbach DS, Poole FL, Ye ZH (2000) Essential role of caffeoyl coenzyme A O-methyltransferase in lignin biosynthesis in woody poplar plants. Plant Physiol. 124:563–577PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Jennifer Stephens
    • 1
  • Claire Halpin
    • 1
  1. 1.Plant Research Unit, School of Life SciencesUniversity of Dundee at SCRIDundeeUK

Personalised recommendations