Rewired phenolic metabolism and improved saccharification efficiency of a Zea mays cinnamyl alcohol dehydrogenase 2 (zmcad2) mutant.
bm1
CAD
brown midrib
field-grown
lignin
maize
metabolomics
phenolic profiling
pre-treatment
saccharification
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
revised:
24
11
2020
received:
16
09
2020
accepted:
26
11
2020
pubmed:
2
12
2020
medline:
29
7
2021
entrez:
1
12
2020
Statut:
ppublish
Résumé
Lignocellulosic biomass is an abundant byproduct from cereal crops that can potentially be valorized as a feedstock to produce biomaterials. Zea mays CINNAMYL ALCOHOL DEHYDROGENASE 2 (ZmCAD2) is involved in lignification, and is a promising target to improve the cellulose-to-glucose conversion of maize stover. Here, we analyzed a field-grown zmcad2 Mutator transposon insertional mutant. Zmcad2 mutant plants had an 18% lower Klason lignin content, whereas their cellulose content was similar to that of control lines. The lignin in zmcad2 mutants contained increased levels of hydroxycinnamaldehydes, i.e. the substrates of ZmCAD2, ferulic acid and tricin. Ferulates decorating hemicelluloses were not altered. Phenolic profiling further revealed that hydroxycinnamaldehydes are partly converted into (dihydro)ferulic acid and sinapic acid and their derivatives in zmcad2 mutants. Syringyl lactic acid hexoside, a metabolic sink in CAD-deficient dicot trees, appeared not to be a sink in zmcad2 maize. The enzymatic cellulose-to-glucose conversion efficiency was determined after 10 different thermochemical pre-treatments. Zmcad2 yielded significantly higher conversions compared with controls for almost every pre-treatment. However, the relative increase in glucose yields after alkaline pre-treatment was not higher than the relative increase when no pre-treatment was applied, suggesting that the positive effect of the incorporation of hydroxycinnamaldehydes was leveled off by the negative effect of reduced p-coumarate levels in the cell wall. Taken together, our results reveal how phenolic metabolism is affected in CAD-deficient maize, and further support mutating CAD genes in cereal crops as a promising strategy to improve lignocellulosic biomass for sugar-platform biorefineries.
Substances chimiques
Lignin
9005-53-2
Alcohol Oxidoreductases
EC 1.1.-
cinnamyl alcohol dehydrogenase
EC 1.1.1.195
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1240-1257Informations de copyright
© 2020 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Aden, A., Ruth, M., Ibsen, K., Jechura, J., Neeves, K., Sheehan, J., Wallace, B., Montague, L., Slayton, A. and Lukas, J. (2002) Lignocellulosic biomass to ethanol process design and economics utilizing co-current dilute acid prehydrolysis and enzymatic hydrolysis for corn stover. National Renewable Energy Laboratory Technical Report NREL/TP-510-32438 (http://www.nrel.gov/docs/fy02osti/32438.pdf).
Anderson, N.A., Tobimatsu, Y., Ciesielski, P.N., Ximenes, E., Ralph, J., Donohoe, B.S., Ladisch, M. and Chapple, C. (2015) Manipulation of guaiacyl and syringyl monomer biosynthesis in an Arabidopsis cinnamyl alcohol dehydrogenase mutant results in atypical lignin biosynthesis and modified cell wall structure. Plant Cell, 27, 2195-2209.
Barrière, Y., Chavigneau, H., Delaunay, S., Courtial, A., Bosio, M., Lassagne, H., Derory, J., Lapierre, C., Méchin, V. and Tatout, C. (2013) Different mutations in the ZmCAD2 gene underlie the maize brown-midrib1 (bm1) phenotype with similar effects on lignin characteristics and have potential interest for bioenergy production. Maydica, 58, 6-20.
Barrière, Y., Méchin, V., Lafarguette, F., Manicacci, D., Guillon, F., Wang, H., Lauressergues, D., Pichon, M., Bosio, M. and Tatout, C. (2009) Toward the discovery of maize cell wall genes involved in silage maize quality and capacity to biofuel production. Maydica, 54, 161-198.
Barrière, Y., Ralph, J., Méchin, V., Guillaumie, S., Grabber, J.H., Argillier, O., Chabbert, B. and Lapierre, C. (2004) Genetic and molecular basis of grass cell wall biosynthesis and degradability. II. Lessons from brown-midrib mutants. C. R. Biol. 327, 847-860.
Baucher, M., Bernard-Vailhé, M.A., Chabbert, B., Besle, J.-M., Opsomer, C., Van Montagu, M. and Botterman, J. (1999) Down-regulation of cinnamyl alcohol dehydrogenase in transgenic alfalfa (Medicago sativa L.) and the effect on lignin composition and digestibility. Plant Mol. Biol. 39, 437-447.
Baucher, M., Chabbert, B., Pilate, G. et al. (1996) Red xylem and higher lignin extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar. Plant Physiol. 112, 1479-1490.
Bernard Vailhé, M.A., Besle, J.M., Maillot, M.P., Cornu, A., Halpin, C. and 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, 505-514.
Boerjan, W., Ralph, J. and Baucher, M. (2003) Lignin biosynthesis. Annu. Rev. Plant Biol. 54, 519-546.
Bouvier d’Yvoire, M., Bouchabke-Coussa, O., Voorend, W. et al. (2013) Disrupting the cinnamyl alcohol dehydrogenase 1 gene (BdCAD1) leads to altered lignification and improved saccharification in Brachypodium distachyon. Plant J. 73, 496-508.
Carroll, A. and Somerville, C. (2009) Cellulosic biofuels. Annu. Rev. Plant Biol. 60, 165-182.
Chabannes, M., Barakate, A., Lapierre, C., Marita, J.M., Ralph, J., Pean, M., Danoun, S., Halpin, C., Grima-Pettenati, J. and Boudet, A.M. (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.
Chen, F. and Dixon, R.A. (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat. Biotechnol. 25, 759-761.
Chen, L., Auh, C.K., Dowling, P., Bell, J., Chen, F., Hopkins, A., Dixon, R.A. and Wang, Z.Y. (2003) Improved forage digestibility of tall fescue (Festuca arundinacea) by transgenic down-regulation of cinnamyl alcohol dehydrogenase. Plant Biotechnol. J. 1, 437-449.
Chen, W., VanOpdorp, N., Fitzl, D., Tewari, J., Friedemann, P., Greene, T., Thompson, S., Kumpatla, S. and Zheng, P. (2012) Transposon insertion in a cinnamyl alcohol dehydrogenase gene is responsible for a brown midrib1 mutation in maize. Plant Mol. Biol. 80, 289-297.
Coleman, H.D., Samuels, A.L., Guy, R.D. and Mansfield, S.D. (2008) Perturbed lignification impacts tree growth in hybrid poplar-A function of sink strength, vascular integrity, and photosynthetic assimilation. Plant Physiol. 148, 1229-1237.
Dauwe, R., Morreel, K., Goeminne, G. et al. (2007) Molecular phenotyping of lignin-modified tobacco reveals associated changes in cell-wall metabolism, primary metabolism, stress metabolism and photorespiration. Plant J. 52, 263-285.
de Lyra Soriano Saleme, M., Cesarino, I. and Vargas, L. et al. (2017) Silencing CAFFEOYL SHIKIMATE ESTERASE affects lignification and improves saccharification in poplar. Plant Physiol. 175, 1040-1057.
De Meester, B., de Vries, L., Özparpucu, M. et al. (2018) Vessel-specific reintroduction of CINNAMOYL-COA REDUCTASE1 (CCR1) in dwarfed ccr1 mutants restores vessel and xylary fiber integrity and increases biomass. Plant Physiol. 176, 611-633.
del Río, J.C., Rencoret, J., Prinsen, P., Martínez, Á.T., Ralph, J. and Gutiérrez, A. (2012) Structural characterization of wheat straw lignin as revealed by analytical pyrolysis, 2D-NMR, and reductive cleavage methods. J. Agric. Food Chem. 60, 5922-5935.
Eloy, N.B., Voorend, W., Lan, W. et al. (2017) Silencing CHALCONE SYNTHASE in maize impedes the incorporation of tricin into lignin and increases lignin content. Plant Physiol. 173, 998-1016.
Elumalai, S., Tobimatsu, Y., Grabber, J.H., Pan, X. and Ralph, J. (2012) Epigallocatechin gallate incorporation into lignin enhances the alkaline delignification and enzymatic saccharification of cell walls. Biotechnol. Biofuels. 5, 59.
Emrani, N., Harloff, H.-J., Gudi, O., Kopisch-Obuch, F. and Jung, C. (2015) Reduction in sinapine content in rapeseed (Brassica napus L.) by induced mutations in sinapine biosynthesis genes. Mol. Breeding, 35, 37.
Eudes, A., Liang, Y., Mitra, P. and Loqué, D. (2014) Lignin bioengineering. Curr. Opin. Biotechnol. 26, 189-198.
Eyster, W.H. (1926) chromosome VIII in maize. Science, 64, 22.
Fornalé, S., Capellades, M., Encina, A. et al. (2012) Altered lignin biosynthesis improves cellulosic bioethanol production in transgenic maize plants down-regulated for cinnamyl alcohol dehydrogenase. Mol. Plant, 5, 817-830.
Fornalé, S., Rencoret, J., García-Calvo, L., Encina, A., Rigau, J., Gutiérrez, A., del Río, J.C. and Caparros-Ruiz, D. (2017) Changes in cell wall polymers and degradability in maize mutants lacking 3´-and 5´-O-methyltransferases involved in lignin biosynthesis. Plant Cell Physiol. 58, 240-255.
Freudenberg, K. (1959) Biosynthesis and constitution of lignin. Nature, 183, 1152-1155.
Fu, C., Xiao, X., Xi, Y., Ge, Y., Chen, F., Bouton, J., Dixon, R.A. and Wang, Z.-Y. (2011) Downregulation of cinnamyl alcohol dehydrogenase (CAD) leads to improved saccharification efficiency in switchgrass. BioEnergy Res. 4, 153-164.
Gómez, L.D., Vanholme, R., Bird, S., Goeminne, G., Trindade, L.M., Polikarpov, I., Simister, R., Morreel, K., Boerjan, W. and McQueen-Mason, S.J. (2014) Side by side comparison of chemical compounds generated by aqueous pretreatments of maize stover. Miscanthus and sugarcane bagasse. BioEnergy Res. 7, 1466-1480.
Grabber, J.H., Hatfield, R.D., Lu, F. and Ralph, J. (2008) Coniferyl ferulate incorporation into lignin enhances the alkaline delignification and enzymatic degradation of cell walls. Biomacromol, 9, 2510-2516.
Grabber, J.H., Schatz, P.F., Kim, H., Lu, F. and Ralph, J. (2010) Identifying new lignin bioengineering targets: 1. Monolignol-substitute impacts on lignin formation and cell wall fermentability. BMC Plant Biol. 10, 114.
Hake, S. and Ross-Ibarra, J. (2015) The natural history of model organisms: genetic, evolutionary and plant breeding insights from the domestication of maize, eLife 4, e05861.
Halpin, C. (2019) Lignin engineering to improve saccharification and digestibility in grasses. Curr. Opin. Biotechnol. 56, 223-229.
Halpin, C., Holt, K., Chojecki, J., Oliver, D., Chabbert, B., Monties, B., Edwards, K., Barakate, A. and Foxon, G.A. (1998) Brown-midrib maize (bm1) - a mutation affecting the cinnamyl alcohol dehydrogenase gene. Plant J. 14, 545-553.
Halpin, C., Knight, M.E., Foxon, G.A., Campbell, M.M., Boudet, A.M., Boon, J.J., Chabbert, B., Tollier, M.-T. and Schuch, W. (1994) Manipulation of lignin quality by down-regulation of cinnamyl alcohol-dehydrogenase. Plant J. 6, 339-350.
Hatfield, R., Ralph, J. and Grabber, J.H. (2008) A potential role for sinapyl p-coumarate as a radical transfer mechanism in grass lignin formation. Planta, 228, 919-928.
Hatfield, R.D., Marita, J.M., Frost, K., Grabber, J., Ralph, J., Lu, F. and Kim, H. (2009) Grass lignin acylation: p-coumaroyl transferase activity and cell wall characteristics of C3 and C4 grasses. Planta, 229, 1253-1267.
Holtman, K.M., Chang, H.-M., Jameel, H. and Kadla, J.F. (2006) Quantitative 13C NMR characterization of milled wood lignins isolated by different milling techniques. J. Wood Chem. Technol. 26, 21-34.
Ibdah, M., Berim, A., Martens, S., Valderrama, A.L.H., Palmieri, L., Lewinsohn, E. and Gang, D.R. (2014) Identification and cloning of an NADPH-dependent hydroxycinnamoyl-CoA double bond reductase involved in dihydrochalcone formation in Malus × domestica Borkh. Phytochemistry, 107, 24-31.
Ishii, T. (1991) Isolation and characterization of a diferuloyl arabinoxylan hexasaccharide from bamboo shoot cell-walls. Carbohydr. Res. 219, 15-22.
Jørgensen, H., Kristensen, J.B. and Felby, C. (2007) Enzymatic conversion of lignocellulose into fermentable sugars: challenges and opportunities. Biofuels Bioprod. Biorefin. 1, 119-134.
Jung, H.-J.-G. (2003) Maize stem tissues: ferulate deposition in developing internode cell walls. Phytochemistry, 63, 543-549.
Karlen, S.D., Zhang, C., Peck, M.L. et al. (2016) Monolignol ferulate conjugates are naturally incorporated into plant lignins. Sci. Adv. 2, e1600393.
Kim, H., Padmakshan, D., Li, Y.D., Rencoret, J., Hatfield, R.D. and Ralph, J. (2017) Characterization and elimination of undesirable protein residues in plant cell wall materials for enhancing lignin analysis by solution-state nuclear magnetic resonance spectroscopy. Biomacromol, 18, 4184-4195.
Kim, H. and Ralph, J. (2010) Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6/pyridine-d5. Org. Biomol. Chem. 8, 576-591.
Kim, H., Ralph, J. and Akiyama, T. (2008) Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6. BioEnergy Res. 1, 56-66.
Kim, H., Ralph, J., Lu, F., Pilate, G., Leplé, J.-C., Pollet, B. and Lapierre, C. (2002) Identification of the structure and origin of thioacidolysis marker compounds for cinnamyl alcohol dehydrogenase deficiency in angiosperms. J. Biol. Chem. 277, 47412-47419.
Končitíková, R., Vigouroux, A., Kopečná, M., Andree, T., Bartoš, J., Šebela, M., Moréra, S. and Kopečný, D. (2015) Role and structural characterization of plant aldehyde dehydrogenases from family 2 and family 7. Biochem J. 468, 109-123.
Koshiba, T., Murakami, S., Hattori, T., Mukai, M., Takahashi, A., Miyao, A., Hirochika, H., Suzuki, S., Sakamoto, M. and Umezawa, T. (2013) CAD2 deficiency causes both brown midrib and gold hull and internode phenotypes in Oryza sativa L. cv. Nipponbare. Plant Biotechnol. 30, 365-373.
Kuc, J. and Nelson, O.E. (1964) The abnormal lignins produced by the brown-midrib mutants of maize: I. the brown-midrib-1 mutant. Arch. Biochem. Biophys. 105, 103-113.
Lan, W., Lu, F., Regner, M., Zhu, Y., Rencoret, J., Ralph, S.A., Zakai, U.I., Morreel, K., Boerjan, W. and Ralph, J. (2015) Tricin, a flavonoid monomer in monocot lignification. Plant Physiol. 167, 1284-1295.
Lan, W., Morreel, K., Lu, F., Rencoret, J., del Río, J.C., Voorend, W., Vermerris, W., Boerjan, W. and Ralph, J. (2016) Maize tricin-oligolignol metabolites and their implications for monocot lignification. Plant Physiol. 171, 810-820.
Lapierre, C. (2010) Determing lignin structure by chemical degradations. In Lignin and Lignans. (Heitner, C., Dimmel, D.R. and Schmidt, J.A., eds). Boca Raton, FL: CRC Press, pp. 11-48.
Lapierre, C., Pilate, G., Pollet, B., Mila, I., Leplé, J.-C., Jouanin, L., Kim, H. and Ralph, J. (2004) Signatures of cinnamyl alcohol dehydrogenase deficiency in poplar lignins. Phytochemistry, 65, 313-321.
Lapierre, C., Pollet, B., Petit-Conil, M. et al. (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, 153-164.
Lapierre, C., Voxeur, A., Karlen, S.D., Helm, R.F. and Ralph, J. (2018) Evaluation of feruloylated and p-coumaroylated arabinosyl units in grass arabinoxylans by acidolysis in dioxane/methanol. J. Agric. Food Chem. 66, 5418-5424.
Leplé, J.-C., Dauwe, R., Morreel, K. et al. (2007) Downregulation of cinnamoyl-coenzyme A reductase in poplar: multiple-level phenotyping reveals effects on cell wall polymer metabolism and structure. Plant Cell, 19, 3669-3691.
Li, H.-Q., Jiang, W., Jia, J.-X. and Xu, J. (2014) pH pre-corrected liquid hot water pretreatment on corn stover with high hemicellulose recovery and low inhibitors formation. Bioresour. Technol. 153, 292-299.
Li, M., Heckwolf, M., Crowe, J.D., Williams, D.L., Magee, T.D., Kaeppler, S.M., de Leon, N. and Hodge, D.B. (2015) Cell-wall properties contributing to improved deconstruction by alkaline pre-treatment and enzymatic hydrolysis in diverse maize (Zea mays L.) lines. J. Exp. Bot. 66, 4305-4315.
Lu, F. and Ralph, J. (1999) Detection and determination of p-coumaroylated units in lignins. J. Agric. Food Chem. 47, 1988-1992.
MacAdam, J.W. and Grabber, J.H. (2002) Relationship of growth cessation with the formation of diferulate cross-links and p-coumaroylated lignins in tall fescue leaf blades. Planta, 215, 785-793.
Mansell, R.L., Gross, G.G., Stöckigt, J., Franke, H. and Zenk, M.H. (1974) Purification and properties of cinnamyl alcohol dehydrogenase from higher plants involved in lignin biosynthesis. Phytochemistry, 13, 2427-2435.
Mansfield, S.D., Kim, H., Lu, F. and Ralph, J. (2012) Whole plant cell wall characterization using solution-state 2D NMR. Nat. Protoc. 7, 1579-1589.
Mansfield, S.D., Mooney, C. and Saddler, J.N. (1999) Substrate and enzyme characteristics that limit cellulose hydrolysis. Biotechnol. Prog. 15, 804-816.
Marita, J.M., Hatfield, R.D., Rancour, D.M. and Frost, K.E. (2014) Identification and suppression of the p-Coumaroyl CoA:hydroxycinnamyl alcohol transferase in Zea mays L. Plant J. 78, 850-864.
Marita, J.M., Vermerris, W., Ralph, J. and Hatfield, R.D. (2003) Variations in the cell wall composition of maize brown midrib mutants. J. Agric. Food Chem. 51, 1313-1321.
Martin, A.F., Tobimatsu, Y., Kusumi, R., Matsumoto, N., Miyamoto, T., Lam, P.Y., Yamamura, M., Koshiba, T., Sakamoto, M. and Umezawa, T. (2019) Altered lignocellulose chemical structure and molecular assembly in CINNAMYL ALCOHOL DEHYDROGENASE-deficient rice. Sci. Rep. 9, 17153.
Mechin, V., Argillier, O., Menanteau, V., Barriere, Y., Mila, I., Pollet, B. and Lapierre, C. (2000) Relationship of cell wall composition to in vitro cell wall digestibility of maize inbred line stems. J. Sci. Food Agric. 80, 574-580.
Mir Derikvand, M., Berrio Sierra, J., Ruel, K., Pollet, B., Do, C.-T., Thévenin, J., Buffard, D., Jouanin, L. and Lapierre, C. (2008) Redirection of the phenylpropanoid pathway to feruloyl malate in Arabidopsis mutants deficient for cinnamoyl-CoA reductase 1. Planta, 227, 943-956.
Mittasch, J., Böttcher, C., Frolov, A., Strack, D. and Milkowski, C. (2013) Reprogramming the phenylpropanoid metabolism in seeds of oilseed rape by suppressing the orthologs of REDUCED EPIDERMAL FLUORESCENCE. Plant Physiol. 161, 1656-1669.
Morreel, K., Dima, O., Kim, H. et al. (2010a) Mass spectrometry-based sequencing of lignin oligomers. Plant Physiol. 153, 1464-1478.
Morreel, K., Kim, H., Lu, F. et al. (2010b) Mass spectrometry-based fragmentation as an identification tool in lignomics. Anal. Chem. 82, 8095-8105.
Morreel, K., Saeys, Y., Dima, O., Lu, F., Van de Peer, Y., Vanholme, R., Ralph, J., Vanholme, B. and Boerjan, W. (2014) Systematic structural characterization of metabolites in Arabidopsis via candidate substrate-product pair networks. Plant Cell, 26, 929-945.
Morrison, T.A., Kessler, J.R., Hatfield, R.D. and Buxton, D.R. (1994) Activity of two lignin biosynthesis enzymes during development of a maize internode. J. Sci. Food Agric. 65, 133-139.
Mosier, N., Hendrickson, R., Brewer, M., Ho, N., Sedlak, M., Dreshel, R., Welch, G., Dien, B., Aden, A. and Ladisch, M. (2005a) Industrial scale-up of pH-controlled liquid hot water pretreatment of corn fiber for fuel ethanol production. Appl. Biochem. Biotechnol. 125, 77-97.
Mosier, N., Wyman, C., Dale, B., Elander, R., Lee, Y.Y., Holtzapple, M. and Ladisch, M. (2005b) Features of promising technologies for pretreatment of lignocellulosic biomass. Biores. Technol. 96, 673-686.
Nair, R.B., Bastress, K.L., Ruegger, M.O., Denault, J.W. and Chapple, C. (2004) The Arabidopsis thaliana REDUCED EPIDERMAL FLUORESCENCE1 gene encodes an aldehyde dehydrogenase involved in ferulic acid and sinapic acid biosynthesis. Plant Cell, 16, 544-554.
Ostos Garrido, F.J. Pistón, F., Gómez, L.D. and McQueen-Mason, S.J. (2018) Biomass recalcitrance in barley, wheat and triticale straw: correlation of biomass quality with classic agronomical traits. PLoS One, 13, e0205880.
Oyarce, P., De Meester, B., Fonseca, F. et al. (2019) Introducing curcumin biosynthesis in Arabidopsis enhances lignocellulosic biomass processing. Nat. Plants, 5, 225-237.
Porter, K.S., Axtell, J.D., Lechtenberg, V.L. and Colenbrander, V.F. (1978) Phenotype, fiber composition, and in-vitro dry-matter disappearance of chemically-induced brown midrib (bmr) mutants of sorghum. Crop Sci. 18, 205-208.
Provan, G.J., Scobbie, L. and Chesson, A. (1997) Characterisation of lignin from CAD and OMT deficient Bm mutants of maize. J. Sci. Food Agric. 73, 133-142.
Pillonel, C., Mulder, M.M., Boon, J.J., Forster, B. and Binder, A. (1991) Involvement of cinnamyl-alcohol dehydrogenase in the control of lignin formation in Sorghum bicolor L, Moench. Planta, 185, 538-544.
Ralph, J. (2010) Hydroxycinnamates in lignification. Phytochem. Rev. 9, 65-83.
Ralph, J., Hatfield, R.D., Quideau, S., Helm, R.F., Grabber, J.H. and Jung, H.-J.-G. (1994) Pathway of p-coumaric acid incorporation into maize lignin as revealed by NMR. J. Am. Chem. Soc. 116, 9448-9456.
Ralph, J., Kim, H., Lu, F., Grabber, J.H., Leplé, J.-C., Berrio-Sierra, J., Mir Derikvand, M., Jouanin, L., Boerjan, W. and Lapierre, C. (2008) Identification of the structure and origin of a thioacidolysis marker compound for ferulic acid incorporation into angiosperm lignins (and an indicator for cinnamoyl CoA reductase deficiency). Plant J. 53, 368-379.
Ralph, J., Lapierre, C. and Boerjan, W. (2019) Lignin structure and its engineering. Curr. Opin. Biotechnol. 56, 240-249.
Ralph, J., Lapierre, C., Marita, J.M. et al. (2001) Elucidation of new structures in lignins of CAD- and COMT-deficient plants by NMR. Phytochemistry, 57, 993-1003.
Ralph, J., MacKay, J.J., Hatfield, R.D., O’Malley, D.M., Whetten, R.W. and Sederoff, R.R. (1997) Abnormal lignin in a loblolly pine mutant. Science, 277, 235-239.
Saathoff, A.J., Sarath, G., Chow, E.K., Dien, B.S. and Tobias, C.M. (2011) Downregulation of cinnamyl alcohol dehydrogenase in switchgrass by RNA silencing results in enhanced glucose release after cellulase treatment. PLoS One, 6, e16416.
Saballos, A., Vermerris, W., Rivera, L. and Ejeta, G. (2008) Allelic association, chemical characterization and saccharification properties of brown midrib mutants of sorghum (Sorghum bicolor (L.) Moench). Bioenergy Res. 2, 198-204.
Saballos, A., Ejeta, G., Sanchez, E., Kang, C. and Vermerris, W. (2009) A genomewide analysis of the cinnamyl alcohol dehydrogenase family in sorghum (Sorghum bicolor (L.) Moench) identifies SbCAD2 as the Brown midrib6 gene. Genetics, 181, 783-795.
Sattler, S.E., Saathoff, A.J., Haas, E.J., Palmer, N.A., Funnell-Harris, D.L., Sarath, G. and Pedersen, J.F. (2009) A nonsense mutation in a cinnamyl alcohol dehydrogenase gene is responsible for the sorghum brown midrib6 phenotype. Plant Physiol. 150, 584-595.
Scully, E.D., Gries, T., Funnell-Harris, D.L., Xin, Z., Kovacs, F.A., Vermerris, W. and Sattler, S.E. (2016) Characterization of novel Brown midrib 6 mutations affecting lignin biosynthesis in sorghum. J. Integr. Plant Biol. 58, 136-149.
Shuai, L., Yang, Q., Zhu, J.Y., Lu, F.C., Weimer, P.J., Ralph, J. and Pan, X.J. (2010) Comparative study of SPORL and dilute-acid pretreatments of spruce for cellulosic ethanol production. Bioresour. Technol. 101, 3106-3114.
Sibout, R., Eudes, A., Mouille, G., Pollet, B., Lapierre, C., Jouanin, L. and Séguin, A. (2005) CINNAMYL ALCOHOL DEHYDROGENASE-C and -D are the primary genes involved in lignin biosynthesis in the floral stem of Arabidopsis. Plant Cell, 17, 2059-2076.
Terrett, O.M. and Dupree, P. (2018) Covalent interactions between lignin and hemicelluloses in plant secondary cell walls. Curr. Opin. Biotechnol. 56, 97-104.
Thévenin, J., Pollet, B., Letarnec, B., Saulnier, L., Gissot, L., Maia-Grondard, A., Lapierre, C. and Jouanin, L. (2011) The simultaneous repression of CCR and CAD, two enzymes of the lignin biosynthetic pathway, results in sterility and dwarfism in Arabidopsis thaliana. Mol. Plant, 4, 70-82.
Torres, A.F., Slegers, P.M., Noordam-Boot, C.M.M., Dolstra, O., Vlaswinkel, L., van Boxtel, A.J.B., Visser, R.G.F. and Trindade, L.M. (2016) Maize feedstocks with improved digestibility reduce the costs and environmental impacts of biomass pretreatment and saccharification. Biotechnol. Biofuels, 9, 63.
Trabucco, G.M., Matos, D.A., Lee, S.J., Saathoff, A.J., Priest, H.D., Mockler, T.C., Sarath, G. and Hazen, S.P. (2013) Functional characterization of cinnamyl alcohol dehydrogenase and caffeic acid O-methyltransferase in Brachypodium distachyon. BMC Biotechnol. 13, 61.
Valério, L., Carter, D., Rodrigues, J.C., Tournier, V., Gominho, J., Marque, C., Boudet, A.-M., Maunders, M., Pereira, H. and Teulières, C. (2003) Down regulation of cinnamyl alcohol dehydrogenase, a lignification enzyme, in Eucalyptus camaldulensis. Mol. Breeding, 12, 157-167.
Van Acker, R., Déjardin, A., Desmet, S. et al. (2017) Different routes for conifer- and sinapaldehyde and higher saccharification upon deficiency in the dehydrogenase CAD1. Plant Physiol. 175, 1018-1039.
Van Acker, R., Leplé, J.-C., Aerts, D. et al. (2014) Improved saccharification and ethanol yield from field-grown transgenic poplar deficient in cinnamoyl-CoA reductase. Proc. Natl. Acad. Sci. USA, 111, 845-850.
Van Acker, R., Vanholme, R., Piens, K. and Boerjan, W. (2016) Saccharification protocol for small-scale lignocellulosic biomass samples to test processing of cellulose into glucose. Bio-Protocol, 6, e1701 (http://www.bio-protocol.org/e1701).
Van Acker, R., Vanholme, R., Storme, V., Mortimer, J.C., Dupree, P. and Boerjan, W. (2013) Lignin biosynthesis perturbations affect secondary cell wall composition and saccharification yield in Arabidopsis thaliana. Biotechnol. Biofuels, 6, 46.
van der Weijde, T., Lessa Alvim Kamei, C., Torres, A.F.. et al. (2013) The potential of C4 grasses for cellulosic biofuel production. Front. Plant Sci. 4, 107.
van der Weijde, T., Torres, A.F., Dolstra, O., Dechesne, A., Visser, R.G.F. and Trindade, L.M. (2016) Impact of different lignin fractions on saccharification efficiency in diverse species of the bioenergy crop Miscanthus. Bioenerg. Res. 9, 146-156.
Vanholme, B., Desmet, T., Ronsse, F., Rabaey, K., Van Breusegem, F., De Mey, M., Soetaert, W. and Boerjan, W. (2013a) Towards a carbon-negative sustainable bio-based economy. Front. Plant Sci. 4, 174.
Vanholme, R., Cesarino, I., Rataj, K. et al. (2013b) Caffeoyl shikimate esterase (CSE) is an enzyme in the lignin biosynthetic pathway in Arabidopsis. Science, 341, 1103-1106.
Vanholme, R., De Meester, B., Ralph, J. and Boerjan, W. (2019) Lignin biosynthesis and its integration into metabolism. Curr. Opin. Biotechnol. 56, 230-239.
Vanholme, R., Demedts, B., Morreel, K., Ralph, J. and Boerjan, W. (2010a) Lignin biosynthesis and structure. Plant Physiol. 153, 895-905.
Vanholme, R., Morreel, K., Darrah, C., Oyarce, P., Grabber, J.H., Ralph, J. and Boerjan, W. (2012a) Metabolic engineering of novel lignin in biomass crops. New Phytol. 196, 978-1000.
Vanholme, R., Morreel, K., Ralph, J. and Boerjan, W. (2008) Lignin engineering. Curr. Opin. Plant Biol. 11, 278-285.
Vanholme, R., Ralph, J., Akiyama, T. et al. (2010b) Engineering traditional monolignols out of lignin by concomitant up-regulation of F5H1 and down-regulation of COMT in Arabidopsis. Plant J. 64, 885-897.
Vanholme, R., Storme, V., Vanholme, B., Sundin, L., Christensen, J.H., Goeminne, G., Halpin, C., Rohde, A., Morreel, K. and Boerjan, W. (2012b) A systems biology view of responses to lignin biosynthesis perturbations in Arabidopsis. Plant Cell, 24, 3506-3529.
Vermaas, J.V., Dixon, R.A., Chen, F., Mansfield, S.D., Boerjan, W., Ralph, J., Crowley, M.F. and Beckham, G.T. (2019) Passive membrane transport of lignin-related compounds. Proc. Natl. Acad. Sci. USA, 116, 23117-23123.
Vermerris, W., Saballos, A., Ejeta, G., Mosier, N.S., Ladisch, M.R. and Carpita, N.C. (2007) Molecular breeding to enhance ethanol production from corn and sorghum stover. Crop Sci. 47, S142-S153.
Voorend, W., Nelissen, H., Vanholme, R., De Vliegher, A., Van Breusegem, F., Boerjan, W., Roldán-Ruiz, I., Muylle, H. and Inzé, D. (2016) Overexpression of GA20-OXIDASE1 impacts plant height, biomass allocation and saccharification efficiency in maize. Plant Biotechnol. J. 14, 997-1007.
Wu, R.L., Remington, D.L., MacKay, J.J., McKeand, S.E. and O’Malley, D.M. (1999) Average effect of a mutation in lignin biosynthesis in loblolly pine. Theor. Appl. Genet 99, 705-710.
Yamamoto, M., Tomiyama, H., Koyama, A. et al. (2020) A century-old mystery unveiled: Sekizaisou is a natural lignin mutant. Plant Physiol. 182, 1821-1828.
Yan, X., Liu, J., Kim, H. et al. (2019) CAD1 and CCR2 protein complex formation in monolignol biosynthesis in Populus trichocarpa. New Phytol. 222, 244-260.
Zeng, Y., Zhao, S., Yang, S. and Ding, S.-Y. (2014) Lignin plays a negative role in the biochemical process for producing lignocellulosic biofuels. Curr. Opin. Biotechnol. 27, 38-45.
Zhang, K., Bhuiya, M.-W., Rencoret Pazo, J., Miao, Y., Kim, H., Ralph, J. and Liu, C.-J. (2012) An engineered monolignol 4-O-methyltransferase depresses lignin biosynthesis and confers novel metabolic capability in Arabidopsis. Plant Cell, 24, 3135-3152.
Zhang, K., Qian, Q., Huang, Z., Wang, Y., Li, M., Hong, L., Zeng, D., Gu, M., Chu, C. and Cheng, Z. (2006) GOLD HULL AND INTERNODE2 encodes a primarily multifunctional cinnamyl-alcohol dehydrogenase in rice. Plant Physiol. 140, 972-983.