Phenolic profiling of caffeic acid O-methyltransferase-deficient poplar reveals novel benzodioxane oligolignols

Plant Physiology

Volumn 136, Issue 4, 2004, Pages 4023-4036

  Morreel, Kris ^a   Ralph, John ^b   Lu, Fachuang ^b   Goeminne, Geert ^a   Busson, Roger ^c   Herdewijn, Piet ^c   Goeman, Jan L ^d   Van Der Eycken, Johan ^d   Boerjan, Wout ^a   Messens, Eric ^a  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC COMPOUNDS; CARBOXYLIC ACIDS; CATALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE; TISSUE;

CAFFEIC ACID O-METHYLTRANSFERASE (COMT); MONOLIGONOL; PHENOLIC FRACTION; XYLEM TISSUES;

ENZYMES;

AROMATIC COMPOUNDS; CAFFEIC ACID; CATALYSTS; ENZYMES; LIQUID CHROMATOGRAPHY; NUCLEAR MAGNETIC RESONANCE; PLANT TISSUES; SINAPALDEHYDE;

POPULUS;

ALCOHOL DERIVATIVE; CAFFEATE O METHYLTRANSFERASE; CAFFEATE O-METHYLTRANSFERASE; CINNAMIC ACID DERIVATIVE; LIGNAN; LIGNIN; METHYLTRANSFERASE; PHENOL DERIVATIVE;

ARTICLE; ASPEN; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; TRANSGENIC PLANT;

ALCOHOLS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CINNAMATES; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; LIGNANS; LIGNIN; MASS SPECTROMETRY; METHYLTRANSFERASES; MOLECULAR STRUCTURE; PHENOLS; PLANTS, GENETICALLY MODIFIED; POPULUS;

EID: 16644396152     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.104.049312     Document Type: Article

References (57)

1. Akabori S, Tsuchiya S (1990) The preparation of crown ethers containing dicinnamoyl groups and their complexing abilities. Bull Chem Soc Jpn 63: 1623-1628
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: 465-477
3. Baucher M, Halpin C, Petit-Conil M, Boerjan W (2003) Lignin: genetic engineering and impact on pulping. Crit Rev Biochem Mol Biol 38: 305-350
4. Birks JS, Kanowski PJ (1993) Analysis of resin compositional data. Silvae Genet 42: 340-350
5. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54: 519-546
6. Chabannes M, Barakate A, Lapierre C, Marita JM, Ralph J, Pean M, Danoun S, Halpin C, Grima-Pettenati J, Boudet AM (2001) 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: 257-270
7. Chen C, Meyermans H, Burggraeve B, De Rycke RM, Inoue K, De Vleesschauwer V, Steenackers M, Van Montagu MC, Engler GJ, Boerjan WA (2000) Cell-specific and conditional expression of caffeoylCoA O-methyltransferase in poplar. Plant Physiol 123: 853-867
8. Chen F, Duran AL, Blount JW, Sumner LW, Dixon RA (2003) Profiling phenolic metabolites in transgenic alfalfa modified in lignin biosynthesis. Phytochemistry 64: 1013-1021
9. Chen F, Kota P, Blount JW, Dixon RA (2001) Chemical syntheses of caffeoyl and 5-OH coniferyl aldehydes and alcohols and determination of lignin O-methyltransferase activities in dicot and monocot species. Phytochemistry 58: 1035-1042
10. Daubresse N, Francesch C, Mhamdi F, Rolando C (1994) A mild synthesis of coumaryl, coniferyl, sinapyl aldehydes and alcohols. Synthesis 1994: 369-371
11. Davin LB, Wang H-B, 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: 362-366
12. Dixon RA (2004) Phytoestrogens. Annu Rev Plant Biol 55: 225-261
13. Goujon T, Sibout R, Pollet B, Maba B, Nussaume L, Bechtold N, Lu F, Ralph J, Mila I, Barrière Y, et al (2003) A new Arabidopsis thaliana mutant deficient in the expression of O-methyltransferase impacts lignins and sinapoyl esters. Plant Mol Biol 51: 973-989
14. Guo D, Chen F, Inoue K, Blount JW, Dixon RA (2001) Downregulation of caffeic acid 3-O-methyltransferase and caffeoyl CoA 3-O-methyltransferase in transgenic alfalfa: impacts on lignin structure and implications for the biosynthesis of G and S lignin. Plant Cell 13: 73-88
15. Hatfield R, Vermerris IV (2001) Lignin formation in plants. The dilemma of linkage specificity. Plant Physiol 126: 1351-1357
16. 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 USA 96: 10045-10050
17. Inoue K, Parvathi K, Dixon RA (2000) Substrate preferences of caffeic acid/5-hydroxyferulic acid 3/5-O-methyltransferases in developing stems of alfalfa (Medicago sativa). Arch Biochem Biophys 375: 175-182
18. Inoue K, Sewalt VJH, Ballance GM, Ni W, Stürzer 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: 761-770
19. Ishikawa T, Seki M, Nishigaya K, Miura Y, Seki H, Chen I-S, Ishii H (1995) Studies on the chemical constituents of Xanthoxylum nitidum (Roxb.) D. C. (Fagara nitida Roxb.) III. The chemical constituents of wood. Chem Pharm Bull 43: 2014-2018
20. Jouanin L, Goujon T, de Nadaï V, Martin M-T, Mila I, Vallet C, Pollet B, Yoshinaga A, Chabbert B, Petit-Conil M, et al (2000) Lignification in transgenic poplars with extremely reduced caffeic acid O-methyltransferase activity. Plant Physiol 123: 1363-1373
21. Kim H, Ralph J, Lu F, Ralph SA, Boudet A-M, MacKay JJ, Sederoff RR, Ito T, Kawai S, Ohashi H, et al (2003) NMR analysis of lignins in CAD-deficient plants. Part 1. Incorporation of hydroxycinnamaldehydes and hydroxybenzaldehydes into lignin. Org Biomol Chem 1: 268-281
22. Kim H, Ralph J, Yahiaoui N, Pean M, Boudet A-M (2000) Cross-coupling of hydroxycinnamyl aldehydes into lignins. Org Lett 2: 2197-2200
23. Lapierre C, Tollier MT, Monties B (1988) A new type of constitutive unit in lignins from the corn bm3 mutant. C R Acad Sei Ser III Sei Vie 307; 723-728
24. Lapierre C, Pollet B, Petit-Conil M, Toval G, Romero J, Pilate G, Leplé J-C, Boerjan W, Ferret V, De Nadai V, et al (1999) Structural alterations of lignins in transgenic poplars with depressed cinnamyl alcohol dehydrogenase or caffeic acid O-methyltransferase activity have opposite impact on the efficiency of industrial Kraft pulping. Plant Physiol 119: 153-163
25. Lewis NG (1999) A 20th century roller coaster ride: a short account of lignification. Curr Opin Plant Biol 2: 153-162
26. Lewis NG, Davin LB (1999) Lignans: biosynthesis and function. In U Sankawa, ed, Comprehensive Natural Products Chemistry, Vol 1: Polyketides and Other Secondary Metabolites Including Fatty Acids and Their Derivatives. Elsevier Science, Amsterdam, pp 639-712
27. 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: 1567-1585
28. 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: 6537-6545
29. Lu F, Ralph J (1998) Facile synthesis of 4-hydroxycinnamyl p-coumarates. J Agric Food Chem 46: 2911-2913
30. Lu F, Ralph J, Morreel K, Messens E, Boerjan W (2004) Preparation and relevance of a cross-coupling product between sinapyl alcohol and sinapyl p-hydroxybenzoate. Org Biomol Chem 2: 2888-2890
31. Marita JM, Ralph J, Hatfield RD, Guo D, Chen F, Dixon RA (2003a) 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: 53-65
32. Marita JM, Vermerris W, Ralph J, Hatfield RD (2003b) Variations in the cell wall composition of maize brown midrib mutants. J Agric Food Chem 51: 1313-1321
33. Matsui N, Chen F, Yasuda S, Fukushima K (2000) Conversion of guaiacyl to syringyl moieties on the cinnamyl alcohol pathway during the biosynthesis of lignin in angiosperms. Planta 210: 831-835
34. Maury S, Geoffroy P, Legrand M (1999) Tobacco O-methyltransferases involved in phenylpropanoid metabolism. The different caffeoylcoenzyme A/5-hydroxyferuloyl-coenzyme A 3/5-O-methyltransferase and caffeic acid/5-hydroxyferulic acid 3/5-O-methyltransferase classes have distinct substrate specificities and expression patterns. Plant Physiol 121: 215-223
35. Meng H, Campbell WH (1998) Substrate profiles and expression of caffeoyl coenzyme A and caffeic acid O-methyltransferases in secondary xylem of aspen during seasonal development. Plant Mol Biol 38: 513-520
36. Meyermans H, Morreel K, Lapierre C, Pollet B, De Bruyn A, Busson R, Herdewijn P, Devreese B, Van Beeumen J, Marita JM, et al (2000) Modification in lignin and accumulation of phenolic glucosides in poplar xylem upon down-regulation of caffeoyl-coenzyme A O-methyltransferase, an enzyme involved in lignin biosynthesis. J Biol Chem 275: 36899-36909
37. Morreel K, Ralph J, Kim H, Lu F, Goeminne G, Ralph SA, Messens E, Boerjan W (2004) Profiling of oligolignols reveals monolignol coupling conditions in lignifying poplar xylem. Plant Physiol 136: 3537-3549
38. Neter J, Kutner MH, Nachtsheim CJ, Wasserman W (1996) Applied Linear Statistical Models, Ed 4. WCB/McGraw-Hill, Boston
39. Nilsson O, Little CHA, Sandberg G, Olsson O (1996) Expression of two heterologous promoters, Agrobacterium rhizogenes rolC and cauliflower mosaic virus 35S, in the stem of transgenic hybrid aspen plants during the annual cycle of growth and dormancy. Plant Mol Biol 31: 887-895
40. Osakabe K, Tsao CC, Li L, Popko JL, Umezawa T, Carraway DT, Smeltzer RH, Joshi CP, Chiang VL (1999) Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms. Proc Natl Acad Sci USA 96: 8955-8960
41. Parvathi K, Chen F, Guo D, Blount DW, Dixon RA (2001) Substrate preferences of O-methyltransferases in alfalfa suggest new pathways for 3-O-methylation of monolignols. Plant J 25: 193-202
42. Piquemal J, Chamayou S, Nadaud I, Beckert M, Barrière Y, Mila I, Lapierre C, Rigau J, Puigdomenech P, Jauneau A, et al (2002) Down-regulation of caffeic acid O-methyltransferase in maize revisited using a transgenic approach. Plant Physiol 130: 1675-1685
43. Ralph J, Helm RF, Quideau S, Halfield RD (1992) Lignin - feruloyl ester cross-links in grasses. Part 1. Incorporation of feruloyl esters into coniferyl alcohol dehydrogenation polymers. J Chem Soc Perkin Trans I 1: 2961-2969
44. Ralph SA, Landucci LL, Ralph J (2004a) NMR database of lignin and cell wall model compounds. U.S. Dairy Forage Research Center, U.S. Department of Agriculture-Agricultural Research Service. http://www. dfrc.ars.usda.gov/ software.html (November 15, 2004)
45. Ralph J, Lapierre C, Lu F, Marita JM, Pilate G, Van Doorsselaere J, Boerjan W, Jouanin L (2001a) NMR evidence for benzodioxane structures resulting from incorporation of 5-hydroxyconiferyl alcohol into lignins of O-methyltransferase-deficient poplars. J Agric Food Chem 49: 86-91
46. Ralph J, Lapierre C, Marita JM, Kim H, Lu F, Hatfield RD, Ralph S, Chapple C, Franke R, Hemm MR, et al (2001b) Elucidation of new structures in lignins of CAD- and COMT-deficient plants by NMR. Phytochemistry 57: 993-1003
47. Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz FF, Marita JM, Hatfield RD, Ralph SA, Christensen JH, et al (2004b) Lignins: natural polymers from oxidalive coupling of 4-hydroxyphenylpropanoids. Phytochem Rev 3: 29-60
48. Ranocha P, Chabannes M, Chamayou S, Danoun S, Jauneau A, Boudet A-M, Goffner D (2002) Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar. Plant Physiol 129: 145-155
49. She XG, Qi SH, Gu WX, Pan XF (1998) Study of the total synthesis of neolignans(I): synthesis of the methyl ethers of americanin A and americanol A. J Chem Res S 1998: 436-437
50. Sousa EP, Silva AMS, Pinto MMM, Pedro MM, Cerqueira FAM, Nascimento MSJ (2002) Isomeric kielcorins and dihydroxyxanthones: synthesis, structure elucidation, and inhibitory activities of growth of human cancer cell lines and on the proliferation of human lymphocytes in vitro. Helv Chim Acta 85: 2862-2876
51. Tsai C-J, Popko JL, Mielke MR, Hu W-J, Podila GK, Chiang VL (1998) Suppression of O-methyltransferase gene by homologous sense transgene in quaking aspen causes red-brown wood phenotypes. Plant Physiol 117: 101-112
52. Umezawa T (2004) Diversity of lignan biosynthesis. Phytochemistry Rev (in press)
53. Van Doorsselaere J, Baucher M, Chognot E, Chabbert B, Tollier M-T, Petit-Conil M, Leplé J-C, Pilate G, Cornu D, Monties B, et al (1995) A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic acid O-methyltransferase activity. Plant J 8: 855-864
54. Van Doorsselaere J, Dumas B, Baucher M, Fritig B, Legrand M, Van Montagu M, Inzé D (1993) One-step purification and characterization of a lignin-specific O-methyltransferase from poplar. Gene 133: 213-217
55. Vignols F, Rigau J, Torres MA, Capellades M, Puigdomènech P (1995) The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. Plant Cell 7: 407-416
56. Zhong R, Morrison WH III, Himmelsbach DS, Poole FL II, Ye Z-H (2000) Essential role of caffeoyl coenzyme A O-methyltransferase in lignin biosynthesis in woody poplar plants. Plant Physiol 124: 563-577
57. Zubiela C, Kota P, Ferrer J-L, Dixon RA, Noel JP (2002) Structural basis for the modulation of lignin monomer methylation by caffeic acid/5- hydroxyferulic acid 3/5-O-methyltransferase. Plant Cell 14: 1265-1277