Abstract
Lignin is a heterogenous phenolic polymer that plays crucial roles in the development and physiology of vascular plants. However, it needs to be removed from cellulose by toxic and energy-requiring processes for the production of high-quality paper. Therefore, a major biotechnological challenge is to obtain transgenic trees with modified lignin to improve the quality of wood for paper making. Here, we review the results obtained by alterating the expression of genes of the monolignol biosynthesis pathway in trees and the effect of these modifications on the lignin polymer and on pulping. The data reported show that lignin engineering is a promising strategy to improve wood quality for the pulp and paper industry.
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Axegård, P., B. Jacobson, S. Ljunggren & N.O. Nilvebrant, 1992. Bleaching of kraft pulps - A research perspective. Papier 46: V16–V25.
Allina, S.M., A. Pri-Hadash, D.A. Theilmann, B.E. Ellis & C.J. Douglas, 1998. 4-Coumarate:coenzyme A ligase in hybrid poplar. Plant Physiol 116: 743–754.
Baucher, M., B. Monties, M. Van Montagu & W. Boerjan, 1998. Biosynthesis and genetic engineering of lignin. Crit Rev Plant Sci 17: 125–197.
Baucher, M., B. Chabbert, G. Pilate, J. Van Doorsselaere, M.-T. Tollier, M. Petit-Conil, D. Cornu, B. Monties, M. Van Montagu, D. Inzé, L. Jouanin & W. Boerjan, 1996. Red xylem and higher lignin extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar (Populus tremula _ P. alba). Plant Physiol 112: 1479–1490.
Bierman, C.J., 1993. Essentials of Pulping and Papermaking. Academic Press, San Diego.
Bugos, R.C., V.L.C. Chiang & W.H. Campbell, 1991. cDNA cloning, sequence analysis and seasonal expression of lignin-bispecific caffeic acid/5-hydroxyferulic acid O-methyltransferase of aspen. Plant Mol Biol 17: 1203–1215.
Butland, S.L., M.L. Chow & B.E. Ellis, 1998. A diverse family of phenylalanine ammonia-lyase genes expressed in pine trees and cell cultures. Plant Mol Biol 37: 15–24.
Chabbert, B., M.T. Tollier, B. Monties, Y. Barrière & O. Argillier, 1994. Biological variability in lignification of maize: expression of the brown midrib bm2 mutation. J Sci Food Agric 64: 455–460.
Chapple, C.C.S., T. Vogt, B.E. Ellis & C.R. Somerville, 1992. An Arabidopsis mutant defective in the general phenylpropanoid pathway. Plant Cell 4: 1413–1424.
Chen, C., H. Meyermans, J. Van Doorsselaere, M. Van Montagu & W. Boerjan, 1998. A gene encoding caffeoyl coenzyme A 3-O-methyltransferase (CCoAOMT) from Populus trichocarpa (Accession No. AJ223621) (PGR98–104). Plant Physiol 117: 719.
Chen, C., W. Ardiles-Diaz, M. Van Montagu & W. Boerjan, 1999. A poplar gene for caffeoyl-coenzyme A 3-O-methyltransferase (Accession No. AJ223620) (PGR99–085). Plant Physiol 120: 635.
Chen, C., H. Meyermans, B. Burggraeve, R.M. De Rycke, K. Inoue, V. De Vleesschauwer, M. Steenackers, M.C. Van Montagu, G.J. Engler & W.A. Boerjan, 2000. Cell-specific and conditional expression of caffeoyl-CoA O-methyltransferase in poplar. Plant Physiol 123: 853–867.
Chiang, V.L., R.J. Puumala, H. Takeuchi & R.E. Eckert, 1988. Comparison of softwood and hardwood kraft pulping. Tappi J 71: 173–176.
Christensen, J.C., M. Baucher, A.P. O'Connell, M. Van Montagu & W. Boerjan, 2000. Control of lignin biosynthesis. In: S.M. Jain & S.C. Minocha (Eds.), Molecular Biology of Woody Plants, Volume 1, (Forestry Sciences, Vol. 64), pp. 227–267. Kluwer Academic Publishers, Dordrecht.
De Melis, L.E., F. Brugliera, S. Pongracic & T.W. Stevenson, 1998a. Isolation of a Eucalyptus globulus cDNA clone encoding cinnamyl alcohol dehydrogenase (Accession No. AF038561) (PGR98–032). Plant Physiol 116: 1191.
DeMelis, L.E., F. Brugliera, S. Pongracic & T.W. Stevenson, 1998b. Isolation of a Eucalyptus globulus cDNA encoding caffeoylcoenzyme A 3-O methyltransferase (Accession No. AF046122) (PGR98–098). Plant Physiol 117: 718.
De Melis, L.E., P.H. Whiteman & T.W. Stevenson, 1999. Isolation and characterisation of a cDNA clone encoding cinnamyl alcohol dehydrogenase in Eucalyptus globulus Labill. Plant Sci 143: 173–182.
Dumas, B., J. Van Doorsselaere, J. Gielen, M. Legrand, B. Fritig, M. VanMontagu & D. Inzé, 1992. Nucleotide sequence of a complementary DNA encoding O-methyltransferase from poplar. Plant Physiol 98: 796–797.
Feuillet, C., V. Lauvergeat, C. Deswarte, G. Pilate, A. Boudet & J. Grima-Pettenati, 1995. Tissue-and cell-specific expression of a cinnamyl alcohol dehydrogenase promoter in transgenic poplar plants. Plant Mol Biol 27: 651–667.
Franke, R., C.M. McMichael, K. Meyer, A.M. Shirley, J.C. Cusumano & C. Chapple, 2000. Modified lignin in tobacco and poplar plants over-expressing the Arabidopsis gene encoding ferulate 5-hydroxylase. Plant J 22: 223–234.
Galliano, H., M. Cabané, C. Eckerskorn, F. Lottspeich, H. Sandermann Jr & D. Ernst, 1993. Molecular cloning, sequence analysis and elicitor-/ozone-induced accumulation of cinnamyl alcohol dehydrogenase from Norway spruce (Picea abies L.). Plant Mol Biol 23: 145–156.
Garcia-Mas, J., R. Messeguer, P. Arus & P. Puigdomenech, 1995. The caffeic acid O-methyltransferase from Prunus amygdalus (GenBank X83217) (PGR95–006). Plant Physiol 108: 1341.
Ge, L. & V.L. Chiang, 1996. A full-length cDNA encoding transcinnamate 4-hydroxylase from developing xylem of Populus tremuloides (Accession number U47293). Plant Physiol 112: 861.
Grand, C., 1984. Ferulic acid 5-hydroxylase: a new cytochrome P-450-dependent enzyme from higher plant microsomes involved in lignin synthesis. FEBS Lett 169: 7–11.
Grimmig, B., R.E. Kneusel, K.T. Junghanns & U. Matern, 1999. Expression of bifunctional caffeoyl-CoA 3-O-methyltransferase in stress compensation and lignification. Plant Biol 1: 299–310.
Grima-Pettenati, J., C. Feuillet, D. Goffner, G. Borderies & A.M. Boudet, 1993. Molecular cloning and expression of a Eucalyptus gunnii cDNA clone encoding cinnamyl alcohol dehydrogenase. Plant Mol Biol 21: 1085–1095.
Hayakawa, T., K. Nanto, S. Kawai, Y. Katayama & N. Morohoshi, 1996. Molecular cloning and tissue-specific expression of two genes that encode caffeic acid O-methyltransferases from Populus kitakamiensis. Plant Sci 113: 157–165.
Hibino, T., J.-Q. Chen, D. Shibata & T. Higuchi, 1994. Nucleotide sequence of a Eucalyptus botryoides gene encoding cinnamyl alcohol dehydrogenase. Plant Physiol 104: 305–306.
Higuchi, T., 1985. Biosynthesis of lignin. In: T. Higuchi (Ed.), Biosynthesis and Biodegradation of Wood Components, pp. 141–160. Academic Press, Orlando.
Higuchi, T., 1990. Lignin biochemistry: biosynthesis and biodegradation. Wood Sci Technol 24: 23–63.
Higuchi, T., T. Ito, T. Umezawa, T. Hibino & D. Shibata, 1994. Red-brown color of lignified tissues of transgenic plants with antisense CAD gene: wine-red lignin from coniferyl aldehyde. J Biotechnol 37: 151–158.
Hu, W.-J., A. Kawaoka, C.-J. Tsai, J. Lung, K. Osakabe, H. Ebinuma & V.L. Chiang, 1998. Compartmentalized expression of two structurally and functionally distinct 4-coumarate:CoA ligase genes in aspen (Populus tremuloides). Proc Natl Acad Sci USA 95: 5407–5412.
Hu, W.-J., S.A. Harding, J. Lung, J.L. Popko, J. Ralph, D.D. Stokke, C.-J. Tsai & V.L. Chiang, 1999. Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nature Biotechnol 17: 808–812.
Humphreys, J.M., M.R. Hemm & C. Chapple, 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.
Inoue, K., V.J.H. Sewalt, G.M. Ballance, W. Ni, C. Stürzer & R.A. Dixon, 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.
Jouanin, L., T. Goujon, V. de Nadaï, M.-T. Martin, I. Mila, C. Vallet, B. Pollet, A. Yoshinaga, B. Chabbert, M. Petit-Conil & C. Lapierre, 2000. Lignification in transgenic poplars with extremely reduced caffeic acid O-methyltransferase activity. Plant Physiol 123: 1363–1373.
Jung, H.-J.G., W. Ni, C.C.S. Chapple & K. Meyer, 1999. Impact of lignin composition on cell-wall degradability in an Arabidopsis mutant. J Sci Food Agric 79: 922–928.
Kawai, S., A. Shiokawa, T. Mori, S. Kajita, Y. Katayama & N. Morohoshi, 1996. Isolation and analysis of cinnamic acid 4-hydroxylase homologous genes from a hybrid aspen, Populus kitakamiensis. Biosci Biotech Biochem 60: 1586–1597.
Kawai, S., Y. Katayama & N. Morohoshi, 1994. Analysis of genes involved in lignin biosynthesis in Populus kitakamiensis. In: N. Morohoshi, R. Sederoff & K. Hata (Eds.), International Wood Biotechnology Symposium, pp. 23–28. Tokyo University of Agriculture and Technology, Tokyo.
Lacombe, E., S. Hawkins, J. Van Doorsselaere, J. Piquemal, D. Goffner, O. Poeydomenge, A.-M. Boudet & J. Grima-Pettenati, 1997. Cinnamoyl CoA reductase, the first committed enzyme of the lignin branch biosynthetic pathway: cloning, expression and phylogenetic relationships. Plant J 11: 429–441.
Lapierre, C., 1993. Application of new methods for the investigation of lignin structure. In: H.G. Jung, D.R. Buxton, R.D. Hatfield & J. Ralph (Eds.), Forage Cell Wall Structure and Digestibility, pp. 133–166. American Society of Agronomy, Madison.
Lapierre, C., B. Pollet, M. Petit-Conil, G. Toval, J. Romero, G. Pilate, J.-C. Leplé, W. Boerjan, V. Ferret, V. De Nadai & L. Jouanin, 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.
Leplé, J.-C., J. Grima-Pettenati, M. Van Montagu & W. Boerjan, 1998. A cDNA encoding cinnamoyl-CoA reductase from Populus trichocarpa (Accession No. AJ224986) (PGR98–121). Plant Physiol 117: 1126.
Li, L., Y. Osakabe, C.P. Joshi & V.L. Chiang, 1999. Secondary xylem-specific expression of caffeoyl-coenzyme A 3-O methyltransferase plays an important role in the methylation pathway associated with lignin biosynthesis in loblolly pine. Plant Mol Biol 40: 555–565.
Li, L., J.L. Popko, T. Umezawa & V.L. Chiang, 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.
MacKay, J.J., W. Liu, R. Whetten, R.R. Sederoff & D.M. O'Malley, 1995. Genetic analysis of cinnamyl alcohol dehydrogenase in loblolly pine: single gene inheritance, molecular characterization and evolution. Mol Gen Genet 247: 537–545.
MacKay, J.J., D.M. O'Malley, T. Presnell, F.L. Booker, M.M. Campbell, R.W. Whetten & R.R. Sederoff, 1997. Inheritance, gene expression, and lignin characterization in a mutant pine deficient in cinnamyl alcohol dehydrogenase. Proc Natl Acad Sci USA 94: 8255–8260.
MacKay J., T. Presnell, H. Jameel, H. Taneda, D. O'Malley & R. Sederoff, 1999. Modified lignin and delignification with a CADdeficient loblolly pine. Holzforschung 53: 403–410.
Martz, F., S. Maury, G. Pinçon & M. Legrand, 1998. cDNA cloning, substrate specificity and expression study of tobacco caffeoyl-CoA 3-O-methyltransferase, a lignin biosynthetic enzyme. Plant Mol Biol 36: 427–437.
Maury, S., P. Geoffroy & M. Legrand, 1999. Tobacco O-methyltransferases involved in phenylpropanoid metabolism. The different caffeoyl-coenzyme A/5-hydroxyferuloylcoenzyme 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.
Meng, H. & W.H. Campbell, 1995. Cloning of aspen xylem caffeoyl-CoA 3-O-methyltransferase (GenBank U27116) (PGR95–040). Plant Physiol 108: 1749.
Meng, H. & W.H. Campbell, 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.
Meyer, K., A.M. Shirley, J.C. Cusumano, D.A. Bell-Lelong & C. Chapple, 1998. Lignin monomer composition is determined by the expression of a cytochrome P450-dependent monooxygenase in Arabidopsis. Proc Natl Acad Sci USA 95: 6619–6623.
Meyermans, H., K. Morreel, C. Lapierre, B. Pollet, A. De Bruyn, R. Busson, P. Herdewijn, B. Devreese, J. Van Beeumen, J.M. Marita, J. Ralph, C. Chen, B. Burggraeve, M. Van Montagu, E. Messens & W. Boerjan, 2000. Changes in lignin and in vivo accumulation of phenolic glucosides in poplar xylem upon downregulation of caffeoyl-CoA-O-methyltransferase, an enzyme involved in lignin biosynthesis. J Biol Chem: in press.
Moerschbacher, B.M., U. Noll, L. Gorrichon & H.-J. Reisener, 1990. Specific inhibition of lignification breaks hypersensitive resistance of wheat to stem rust. Plant Physiol 93: 465–470.
Monties, B., 1989. Lignins. In: P.M. Dey & J.B. Harborne (Eds.), Methods in Plant Biochemistry: Plant Phenolics, Vol. 1, pp. 113–157. Academic Press, New York.
Moyle, R., A. Wagner & C. Walter, 1998. Nucleotide sequence of a cinnamyl alcohol dehydrogenase gene (Accession No. AF060491) from Pinus radiata (PGR98–118). Plant Physiol 117: 1125–1127.
Moyle, R., A. Wagner & C. Walter, 1999. Nucleotide sequence of a caffeic acid O-methyltransferase (cOMT) gene (Accession No. AF119225) from Pinus radiata (PGR99–026). Plant Physiol 119: 1147.
Northcote, D.H., 1989. Control of plant cell wall biosynthesis: an overview. In: N.G. Lewis & M.G. Paice (Eds.), Plant Cell Wall Polymers, (ACS Symposium Series, Vol. 399), pp. 1–15. American Chemical Society, Washington, D.C.
O'Malley, D.M., S. Porter & R.R. Sederoff, 1992. Purification, characterization and cloning of cinnamyl alcohol dehydrogenase in loblolly pine (Pinus taeda L.). Plant Physiol 98: 1364–1371.
Osakabe, Y., Y. Ohtsubo, S. Kawai, Y. Katayama & N. Morohoshi, 1995a. Structure and tissue-specific expression of genes for phenylalanine ammonia-lyase from a hybrid aspen, Populus kitakamiensis. Plant Sci 105: 217–226.
Osakabe, Y., K. Osakabe, S. Kawai, Y. Katayama & N. Morohoshi, 1995b. Characterization of the structure and determination of mRNA levels of the phenylalanine ammonia-lyase gene family from Populus kitakamiensis. Plant Mol Biol 28: 1133–1141.
Osakabe, K., C.C. Tsao, L. Li, J.L. Popko, T. Umezawa, D.T. Carraway, R.H. Smeltzer, C.P. Joshi & V.L. Chiang, 1999. Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms. Proc Natl Acad Sci USA 96: 8955–8960.
Petit-Conil, M., C. Lapierre, B. Pollet, I. Mila, H. Meyermans, G. Pilate, J.-C. Leplé, L. Jouanin, W. Boerjan & C. de Choudens, 1999. Impact of lignin engineering on pulping processes of poplar trees. In: Proceedings of the 27th EUCEPA Conference, in press.
Poeydomenge, O., A.M. Boudet & J. Grima-Pettenati, 1994. A cDNA encoding S-adenosyl-l-methionine:caffeic acid 3-O methyltransferase from Eucalyptus. Plant Physiol 105: 749–750.
Ralph, J., J.J. MacKay, R.D. Hatfield, D.M. O'Malley, R.W. Whetten & R.R. Sederoff, 1997. Abnormal lignin in a loblolly pine mutant. Science 277: 235–239.
Saka, S. & D.A.I. Goring, 1985. Localization of lignins in wood cell walls. In: T. Higuchi (Ed.), Biosynthesis and Biodegradation of Wood Components, pp. 51–62. Academic Press, Orlando.
Subramaniam, R., S. Reinold, E. Molitor & C.J. Douglas, 1993. Structure, inheritance and expression of hybrid poplar (Populus trichocarpa _ Populus deltoides) phenylalanine ammonia-lyase genes. Plant Physiol 102: 71–83.
Tsai, C.-J., G.K. Podila & V.L. Chiang, 1995. Nucleotide sequence of a Populus tremuloides gene encoding bispecific caffeic acid/5-hydroxyferulic acid O-methyltransferase. Plant Physiol 107: 1459.
Tsai, C.-J., J.L. Popko, M.R. Mielke, W.-J. Hu, G.K. Podila & V.L. Chiang, 1998. Suppression of O-methyltransferase gene by homologous sense transgene in quaking aspen causes red-brown wood phenotypes. Plant Physiol 117: 101–112.
Van Doorsselaere, J., M. Baucher, E. Chognot, B. Chabbert, M.-T. Tollier, M. Petit-Conil, J.-C. Leplé, G. Pilate, D. Cornu, B. Monties, M. Van Montagu, D. Inzé, W. Boerjan & L. Jouanin, 1995a. A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic acid O-methyltransferase activity. Plant J 8: 855–864.
Van Doorsselaere, J., M. Baucher, C. Feuillet, A.M. Boudet, M. Van Montagu & D. Inzé, 1995b. Isolation of cinnamyl alcohol dehydrogenase cDNAs from two important economic species: alfalfa and poplar. Demonstration of a high homology of the gene within angiosperms. Plant Physiol Biochem 33: 105–109.
Voo, K.S., R.W. Whetten, D.M. O'Malley & R.R. Sederoff, 1995. 4-Coumarate:coenzyme A ligase from loblolly pine xylem. Plant Physiol 108: 85–97.
Wagner, A., A. Walden & C. Walter, 1996. A cDNA encoding a cinnamyl alcohol dehydrogenase (Accession No. U62394) from Pinus radiata (PGR96–097). Plant Physiol 112: 1397.
Whetten, R.W. & R.R. Sederoff, 1992. Phenylalanine ammonialyase from loblolly pine. Purification of the enzyme and isolation of complementary DNA clones. Plant Physiol 98: 380–386.
Ye, Z.-H., R.E. Kneusel, U. Matern & J.E. Varner, 1994. An alternative methylation pathway in lignin biosynthesis in Zinnia. Plant Cell 6: 1427–1439.
Zhan, X., S. Kawai, A. Mori, Y. Katayama & N. Morohoshi, 1996. Manipulation of lignin synthesis through the introduction of an antisense cinnamic acid 4-hydroxylase gene into tobacco and poplar plants. Abstract presented at the Keystone Symposia on Molecular and Cellular Biology on ‘The extracellular Matrix of Plants: Molecular, Cellular and Developmental Biology’, Tamarron (CO, USA), March 15–21, 1996, p. 22.
Zhang, X.-H. & V.L. Chiang, 1997. Molecular cloning of 4-coumarate:coenzyme A ligase in loblolly pine and the roles of this enzyme in the biosynthesis of lignin in compression wood. Plant Physiol 113: 65–74.
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Chen, C., Baucher, M., Holst Christensen, J. et al. Biotechnology in trees: Towards improved paper pulping by lignin engineering. Euphytica 118, 185–195 (2001). https://doi.org/10.1023/A:1004176714883
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DOI: https://doi.org/10.1023/A:1004176714883