Designer lignins: Harnessing the plasticity of lignification

Current Opinion in Biotechnology

Volumn 37, Issue , 2016, Pages 190-200

  Mottiar, Yaseen ^a   Vanholme, Ruben ^b,c   Boerjan, Wout ^b,c   Ralph, John ^d,e   Mansfield, Shawn D ^a,d  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b GHENT UNIVERSITY   (Belgium)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d USA   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY;

BIOMASS PROCESSING; DEGRADABILITY; DEGREE OF POLYMERISATION; LIGNIN BIOSYNTHESIS; OVERALL EFFICIENCY; PLANT ENGINEERING; POLYMER BACKBONES; SECONDARY CELL WALL;

LIGNIN;

LIGNIN; CARBOHYDRATE;

ARABIDOPSIS; BIOMASS; BIOSYNTHESIS; BRACHYPODIUM; CELL WALL; CROSS LINKING; HYDROPHOBICITY; LIGNIFICATION; METABOLIC ENGINEERING; NONHUMAN; PLANT CELL; POLYMERIZATION; PRIORITY JOURNAL; REVIEW; ANIMAL; CARBOHYDRATE METABOLISM; CHEMICAL PHENOMENA; CHEMISTRY; METABOLISM; PLANT;

BIOMASS; LIGNIFICATION; LIGNINS; PLASTICITY; POLYMERIZATION;

ANIMALS; CARBOHYDRATE METABOLISM; CARBOHYDRATES; CELL WALL; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIGNIN; PLANTS;

EID: 84956707535     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2015.10.009     Document Type: Review

References (52)

1. Sarkanen K.V., Ludwig C.H. Lignins: Occurrence, Formation, Structure and Reactions 1971, Wiley-Interscience.
2. Baucher M., Halpin C., Petit-Conil M., Boerjan W. Lignin: Genetic engineering and impact on pulping. Crit Rev Biochem Mol Biol 2003, 38:305-350.
3. Zeng Y., Zhao S., Yang S., Ding S-Y. Lignin plays a negative role in the biochemical process for producing lignocellulosic biofuels. Curr Opin Biotechnol 2014, 27:38-45.
4. Besle J-M., Cornu A., Jouany J-P. Roles of structural phenylpropanoids in forage cell wall digestion. J Sci Food Agric 1994, 64:171-190.
5. Boerjan W., Ralph J., Baucher M. Lignin biosynthesis. Ann Rev Plant Biol 2003, 54:519-546.
6. Ros-Barceló A., Gómez-Ros L.V., Ferrer M.A., Hernández J.A. The apoplastic antioxidant enzymatic system in the wood-forming tissues of trees. Trees-Struct Funct 2006, 20:145-156.
7. Ralph J., Lundquist K., Brunow G., Lu F., Kim H., Schatz P.F., Marita J.M., Hatfield R.D., Ralph S.A., Christensen J.H., Boerjan W. Lignins: natural polymers from oxidative coupling of 4-hydroxyphenylpropanoids. Phytochem Rev 2004, 3:29-60.
8. Vanholme R., Morreel K., Ralph J., Boerjan W. Lignin engineering. Curr Opin Plant Biol 2008, 11:278-285.
9. Eudes A., Liang Y., Mitra P., Loqué D. Lignin bioengineering. Curr Opin Biotechnol 2014, 26:189-198.
10. Vermerris W., Abril A. Enhancing cellulose utilization for fuels and chemicals by genetic modification of plant cell wall architecture. Curr Opin Biotechnol 2015, 32:104-112.
11. Wagner A., Tobimatsu Y., Phillips L., Flint H., Geddes B., Lu F., Ralph J. Syringyl lignin production in conifers: proof of concept in a Pine tracheary element system. Proc Natl Acad Sci USA 2015, 112:6218-6223.
12. Coleman H.D., Park J-Y., Nair R., Chapple C., Mansfield S.D. RNAi-mediated suppression of p-coumaroyl-CoA 3'-hydroxylase in hybrid poplar impacts lignin deposition and soluble secondary metabolism. Proc Natl Acad Sci 2008, 105:4501-4506.
13. Cass C.L., Peraldi A., Dowd P.F., Mottiar Y., Santoro N., Karlen S.D., Bukhman Y., Foster C.E., Thrower N., Bruno L.C., et al. Effects of PHENYLALANINE AMMONIA LYASE (PAL) knockdown on cell wall composition, biomass digestibility, and biotic and abiotic stress responses in Brachypodium. J Exp Bot 2015, 66:4317-4335.
14. Marita J.M., Ralph J., Hatfield R.D., Chapple C. NMR characterization of lignins in Arabidopsis altered in the activity of ferulate-5-hydroxylase. Proc Natl Acad Sci USA 1999, 96:12328-12332.
15. Mansfield S.D., Kang K.Y., Chapple C. Designed for deconstruction - poplar trees altered in cell wall lignification improve the efficacy of bioethanol production. New Phytol 2012, 194:91-101.
16. Leplé J-C., Dauwe R., Morreel K., Storme V., Lapierre C., Pollet B., Naumann A., Kang K-Y., Kim H., Ruel K., et al. Downregulation of Cinnamoyl-Coenzyme A Reductase in Poplar: multiple-level phenotyping reveals effects on cell wall polymer metabolism and structure. Plant Cell 2007, 19:3669-3691.
17. Ralph J., MacKay J.J., Hatfield R.D., O'Malley D.M., Whetten R.W., Sederoff R.R. Abnormal lignin in a loblolly pine mutant. Science 1997, 277:235-239.
18. Zhao Q., Tobimatsu Y., Zhou R., Pattathil S., Gallego-Giraldo L., Fu C., Jackson L.A., Hahn M.G., Kim H., Chen F., et al. Loss of function of Cinnamyl Alcohol Dehydrogenase 1 causes accumulation of an unconventional lignin and a temperature-sensitive growth defect in Medicago truncatula. Proc Natl Acad Sci USA 2013, 110:13660-13665.
19. Marita J.M., Ralph J., Lapierre C., Jouanin L., Boerjan W. NMR characterization of lignins from transgenic poplars with suppressed caffeic acid O-methyltransferase activity. J Chem Soc Perkin Trans 2001, 1:2939-2945.
20. Wagner A., Tobimatsu Y., Phillips L., Flint H., Torr K., Donaldson L., Piers L., Ralph J. CCoAOMT suppression modifies lignin composition in Pinus radiata. Plant J 2011, 67:119-129.
21. Chen F., Tobimatsu Y., Havkin-Frenkel D., Dixon R.A., Ralph J. A polymer of caffeyl alcohol in plant seeds. Proc Natl Acad Sci USA 2012, 109:1772-1777.
22. Chen F., Tobimatsu Y., Jackson L., Nakashima J., Ralph J., Dixon R.A. Novel seed coat lignins in the Cactaceae: structure, distribution and implications for the evolution of lignin diversity. Plant J 2013, 73:201-211.
23. Ralph J. Hydroxycinnamates in lignification. Phytochem Rev 2010, 9:65-83.
24. Ralph J. What makes a good monolignol substitute?. The Science and Lore of the Plant Cell Wall Biosynthesis, Structure and Function 2006, 285-293. Universal Publishers (BrownWalker Press). T. Hayashi (Ed.).
25. Ralph J., Bunzel M., Marita J.M., Hatfield R.D., Lu F., Kim H., Schatz P.F., Grabber J.H., Steinhart H. Peroxidase-dependent cross-linking reactions of p-hydroxycinnamates in plant cell walls. Phytochem Rev 2004, 3:79-96.
26. Du X.Y., Pérez-Boada M., Fernández C., Rencoret J., del Río J.C., Jiménez-Barbero J., Li J.B., Gutiérrez A., Martínez A.T. Analysis of lignin-carbohydrate and lignin-lignin linkages after hydrolase treatment of xylan-lignin, glucomannan-lignin and glucan-lignin complexes from spruce wood. Planta 2014, 239:1079-1090.
27. Cong F., Diehl B.G., Hill J.L., Brown N.R., Tien M. Covalent bond formation between amino acids and lignin: cross-coupling between proteins and lignin. Phytochemistry 2013, 96:449-456.
28. Voelker S.L., Lachenbruch B., Meinzer F.C., Kitin P., Strauss S.H. Transgenic poplars with reduced lignin show impaired xylem conductivity, growth efficiency and survival. Plant Cell Environ 2011, 34:655-668.
29. Bonawitz N.D., Chapple C. Can genetic engineering of lignin deposition be accomplished without an unacceptable yield penalty?. Curr Opin Biotechnol 2013, 24:336-343.
30. Vanholme R., Morreel K., Darrah C., Oyarce P., Grabber J.H., Ralph J., Boerjan W. Metabolic engineering of novel lignin in biomass crops. New Phytol 2012, 196:978-1000.
31. Crestini C., Melone F., Sette M., Saladino R. Milled wood lignin: a linear oligomer. Biomacromolecules 2011, 12:3928-3935.
32. Eudes A., George A., Mukerjee P., Kim J.S., Pollet B., Benke P.I., Yang F., Mitra P., Sun L., Persil-Çetinkol Ö., et al. Biosynthesis and incorporation of side-chain-truncated lignin monomers to reduce lignin polymerization degree and enhance saccharification. Plant Biotech J 2012, 10:609-620.
33. Lapierre C., Rolando C. Thioacidolyses of pre-methylated lignin samples from pine compression and poplar woods. Holzforschung 1988, 42:1-4.
34. Stewart J.J., Akiyama T., Chapple C.C., Ralph J., Mansfield S.D. The effects on lignin structure of overexpression of ferulate 5-hydroxylase in hybrid poplar. Plant Physiol 2009, 150:621-635.
35. Grabber J.H., Ress D., Ralph J. Identifying new lignin bioengineering targets: impact of epicatechin, quercetin glycoside, and gallate derivatives on the lignification and fermentation of maize cell walls. J Agric Food Chem 2012, 60:5152-5160.
36. Carmona C., Langan P., Smith J.C., Petridis L. Why genetic modification of lignin leads to low-recalcitrance biomass. Phys Chem Chem Phys 2015, 17:358-364.
37. Tobimatsu Y., Elumalai S., Grabber J.H., Davidson C.L., Pan X., Ralph J. Hydroxycinnamate conjugates as potential monolignol replacements: in vitro lignification and cell wall studies with rosmarinic acid. ChemSusChem 2012, 5:676-686.
38. Molinari H.B., Pellny T.K., Freeman J., Shewry P.R., Mitchell R.A. Grass cell wall feruloylation: distribution of bound ferulate and candidate gene expression in Brachypodium distachyon. Front Plant Sci 2013, 4:50.
39. Wilkerson C.G., Mansfield S.D., Lu F., Withers S., Park J-Y., Karlen S.D., Gonzales-Vigil E., Padmakshan D., Unda F., Rencoret J., et al. Monolignol ferulate transferase introduces chemically labile linkages into the lignin backbone. Science 2014, 344:90-93.
40. Tsuji Y., Vanholme R., Tobimatsu Y., Ishikawa Y., Foster C.E., Kamimura N., Hishiyama S., Hashimoto S., Shino A., Hara H., et al. Introduction of chemically labile substructures into Arabidopsis lignin through the use of LigD, the Cα-dehydrogenase from Sphingobium sp. strain SYK-6. Plant Biotechnol J 2015, 13:821-832.
41. Liang H.Y., Frost C.J., Wei X.P., Brown N.R., Carlson J.E., Tien M. Improved sugar release from lignocellulosic material by introducing a tyrosine-rich cell wall peptide gene in poplar. Clean-Soil Air Water 2008, 36:662-668.
42. Ragauskas A.J., Beckham G.T., Biddy M.J., Chandra R., Chen F., Davis M.F., Davison B.H., Dixon R.A., Gilna P., Keller M., et al. Lignin valorization: improving lignin processing in the biorefinery. Science 2014, 344:1246843.
43. Lan W., Lu F., Regner M., Zhu Y., Rencoret J., Ralph S.A., Zakai U.I., Morreel K., Boerjan W., Ralph J. Tricin, a flavonoid monomer in monocot lignification. Plant Physiol 2015, 167:1284-1295.
44. Petrik D.L., Karlen S.D., Cass C.L., Padmakshan D., Lu F., Liu S., Le Bris P., Antelme S., Santoro N., Wilkerson C.G., et al. p-Coumaroyl-CoA:Monolignol Transferase (PMT) acts specifically in the lignin biosynthetic pathway in Brachypodium distachyon. Plant J 2014, 77:713-726.
45. Schuetz M., Smith R., Ellis B. Xylem tissue specification, patterning, and differentiation mechanisms. J Exp Bot 2013, 64:11-31.
46. Bonawitz N.D., Kim J.I., Tobimatsu Y., Ciesielski P.N., Anderson N.A., Ximenes E., Maeda J., Ralph J., Donohoe B.S., Ladisch M., et al. Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant. Nature 2014, 509:376-380.
47. Yang F., Mitra P., Zhang L., Prak L., Verhertbruggen Y., Kim J.S., Sun L., Zheng K., Tang K., Auer M., et al. Engineering secondary cell wall deposition in plants. Plant Biotechnol J 2013, 11:325-335.
48. Alejandro S., Lee Y., Tohge T., Sudre D., Osorio S., Park J., Bovet L., Lee Y., Geldner N., Fernie A.R., et al. AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Curr Biol 2012, 22:1207-1212.
49. Lu S., Li Q., Wie H., Chang M-J., Tunlaya-Anukit S., Kim H., Liu J., Song J., Sun Y-H., Yuan L., et al. Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci USA 2013, 110:10848-10853.
50. Zhao Q., Dixon R.A. Altering the cell wall and its impact on plant disease: from forage to bioenergy. Ann Rev Phytopathol 2014, 52:69-91.
51. Petersen P.D., Lau J., Ebert B., Yang F., Verhertbruggen Y., Kim J.S., Varanasi P., Suttangkakul A., Auer M., Loqué D., et al. Engineering of plants with improved properties as biofuels feedstocks by vessel-specific complementation of xylan biosynthesis mutants. Biotechnol Biofuels 2012, 5:84.
52. Tobimatsu Y., Takano T., Kamitakahara H., Nakatsubo F. Studies on the dehydrogenative polymerizations (DHPs) of monolignol β-glycosides: Part 4. Horseradish peroxidase-catalyzed copolymerization of isoconiferin and isosyringin. Holzforschung 2008, 62:495-500.