Structural Characterization of Lignin from Maize ( Zea mays L.) Fibers: Evidence for Diferuloylputrescine Incorporated into the Lignin Polymer in Maize Kernels

del Rio, Jose C.; Rencoret, Jorge; Gutierrez, Ana; Kim, Hoon; Ralph, John

doi:10.1021/acs.jafc.8b00880

Structural Characterization of Lignin from Maize ( Zea mays L.) Fibers: Evidence for Diferuloylputrescine Incorporated into the Lignin Polymer in Maize Kernels

Journal Article · Wed Apr 11 00:00:00 EDT 2018 · Journal of Agricultural and Food Chemistry

DOI:https://doi.org/10.1021/acs.jafc.8b00880· OSTI ID:1459411

^[1]; ^[2]; ^[2]; ^[3]; ^[3]

Inst. de Recursos Naturales y Agrobiologia de Sevilla (IRNAS), CSIC, Seville (Spain); Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS)
Inst. de Recursos Naturales y Agrobiologia de Sevilla (IRNAS), CSIC, Seville (Spain)
Univ. of Wisconsin, Madison, WI (United States). Wisconsin Energy Inst., Dept. of Energy Great Lakes Bioenergy Research Center; Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry

The structure of the phenolic polymer in maize grain fibers, with 5.5% Klason lignin content, has been studied. For this, the milled wood lignin (MWL) and dioxane lignin (DL) preparations were isolated and analyzed. The data indicated that the lignin in maize fibers was syringyl rich, mostly involved in β-aryl ether, resinol, and phenylcoumaran substructures. 2D NMR and derivatization followed by reductive cleavage (DFRC) also revealed the occurrence of associated ferulates together with trace amounts of p-coumarates acylating the γ-OH of lignin side chains, predominantly on S-lignin units. More interesting was the occurrence of diferuloylputrescine, a ferulic acid amide, which was identified by 2D NMR and comparison with a synthesized standard, that was apparently incorporated into this lignin. A phenylcoumaran structure involving a diferuloylputrescine coupled through 8–5' linkages to another diferuloylputrescine (or to a ferulate or a guaiacyl lignin unit) was found, providing compelling evidence for its participation in radical coupling reactions. The occurrence of diferuloylputrescine in cell walls of maize kernels and other cereal grains appears to have been missed in previous works, perhaps due to the alkaline hydrolysis commonly used for composition studies.

View Accepted Manuscript (DOE)

Research Organization:: Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Contributing Organization:: NMR facilities of the General Research Services of the University of Seville (SGI-CITIUS)

Grant/Contract Number:: FC02-07ER64494; SC0018409

OSTI ID:: 1459411

Journal Information:: Journal of Agricultural and Food Chemistry, Journal Name: Journal of Agricultural and Food Chemistry Journal Issue: 17 Vol. 66; ISSN 0021-8561

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (47)

Cell wall cross-linking by ferulates and diferulates in grasses Hatfield, Ronald D.; Ralph, John; Grabber, John H. Journal of the Science of Food and Agriculture, Vol. 79, Issue 3 https://doi.org/10.1002/(SICI)1097-0010(19990301)79:3<403::AID-JSFA263>3.0.CO;2-0	journal	March 1999
Lignification: are Lignins Biosynthesized via simple Combinatorial Chemistry or via Proteinaceous Control and Template Replication? Ralph, John; Brunow, Gösta; Harris, Philip J. Recent Advances in Polyphenol Research, Vol. 1 https://doi.org/10.1002/9781444302400.ch2	book	July 2008
Chemical Pulping Advantages of Zip-lignin Hybrid Poplar Zhou, Shengfei; Runge, Troy; Karlen, Steven D. ChemSusChem, Vol. 10, Issue 18 https://doi.org/10.1002/cssc.201701317	journal	August 2017
Utilisation of corn ( Zea mays ) bran and corn fiber in the production of food components: Applications of corn co-products Rose, Devin J.; Inglett, George E.; Liu, Sean X. Journal of the Science of Food and Agriculture, Vol. 90, Issue 6 https://doi.org/10.1002/jsfa.3915	journal	March 2010
Isolation of terrestribisamide from Peltophorum pterocarpum (DC.) Baker ex. K. Heyne and its antimicrobial, antioxidant, and cytotoxic activities Karunai Raj, M.; Balachandran, C.; Duraipandiyan, V. Medicinal Chemistry Research, Vol. 22, Issue 8 https://doi.org/10.1007/s00044-012-0393-3	journal	December 2012
Ferulate–coniferyl alcohol cross-coupled products formed by radical coupling reactions Zhang, Aiping; Lu, Fachuang; Sun, Runcang Planta, Vol. 229, Issue 5 https://doi.org/10.1007/s00425-009-0894-6	journal	February 2009
Hydroxycinnamates in lignification Ralph, John Phytochemistry Reviews, Vol. 9, Issue 1, p. 65-83 https://doi.org/10.1007/s11101-009-9141-9	journal	August 2009
Diferuloylputrescine and p-coumaroyl-feruloylputrescine, abundant polyamine conjugates in lipid extracts of maize kernels Moreau, Robert A.; Nuñez, Alberto; Singh, Vijay Lipids, Vol. 36, Issue 8 https://doi.org/10.1007/s11745-001-0793-6	journal	August 2001
Corn Fiber: Structure, Composition, and Response to Enzymes for Fermentable Sugars and Coproducts Akin, Danny E.; Rigsby, Luanne L. Applied Biochemistry and Biotechnology, Vol. 144, Issue 1 https://doi.org/10.1007/s12010-007-0053-0	journal	July 2007
Lignin-ferulate cross-links in grasses: active incorporation of ferulate polysaccharide esters into ryegrass lignins Ralph, John; Grabber, John H.; Hatfield, Ronald D. Carbohydrate Research, Vol. 275, Issue 1, p. 167-178 https://doi.org/10.1016/0008-6215(95)00237-N	journal	September 1995
Thermally assisted hydrolysis and alkylation as a novel pyrolytic approach for the structural characterization of natural biopolymers and geomacromolecules del Rio, J. C.; Martin, F.; Gonzalez-Vila, F. J. TrAC Trends in Analytical Chemistry, Vol. 15, Issue 2 https://doi.org/10.1016/0165-9936(96)80763-1	journal	February 1996
Alkaline extraction and characterisation of heteroxylans from maize bran Chanliaud, E.; Saulnier, L.; Thibault, J. -F. Journal of Cereal Science, Vol. 21, Issue 2 https://doi.org/10.1016/0733-5210(95)90035-7	journal	January 1995
Metabolism of tyramine and feruloyltyramine in TMV inoculated leaves of Nicotiana tabacum Negrel, Jonathan; Jeandet, Philippe Phytochemistry, Vol. 26, Issue 8 https://doi.org/10.1016/S0031-9422(00)84681-6	journal	January 1987
The phenolic fraction of maize bran: evidence for lignin-heteroxylan association Lapierre, Catherine; Pollet, Brigitte; Ralet, Marie-Christine Phytochemistry, Vol. 57, Issue 5 https://doi.org/10.1016/S0031-9422(01)00104-2	journal	July 2001
Ether-linked ferulic acid amides in natural and wound periderms of potato tuber Negrel, Jonathan; Pollet, Brigitte; Lapierre, Catherine Phytochemistry, Vol. 43, Issue 6 https://doi.org/10.1016/S0031-9422(96)00500-6	journal	December 1996
Designer lignins: harnessing the plasticity of lignification Mottiar, Yaseen; Vanholme, Ruben; Boerjan, Wout Current Opinion in Biotechnology, Vol. 37 https://doi.org/10.1016/j.copbio.2015.10.009	journal	February 2016
Film-forming polymers from distillers’ grains: structural and material properties Xiang, Zhouyang; Watson, Jamison; Tobimatsu, Yuki Industrial Crops and Products, Vol. 59 https://doi.org/10.1016/j.indcrop.2014.05.023	journal	August 2014
Composition of non-woody plant lignins and cinnamic acids by Py-GC/MS, Py/TMAH and FT-IR del Río, José C.; Gutiérrez, Ana; Rodríguez, Isabel M. Journal of Analytical and Applied Pyrolysis, Vol. 79, Issue 1-2 https://doi.org/10.1016/j.jaap.2006.09.003	journal	May 2007
Lignin engineering Vanholme, R.; Morreel, K.; Ralph, J. Current Opinion in Plant Biology, Vol. 11, Issue 3, p. 278-285 https://doi.org/10.1016/j.pbi.2008.03.005	journal	June 2008
Corn fiber as a raw material for hemicellulose and ethanol production Gáspár, Melinda; Kálmán, Gergely; Réczey, Kati Process Biochemistry, Vol. 42, Issue 7 https://doi.org/10.1016/j.procbio.2007.04.003	journal	July 2007
Structural elucidation of new ferulic acid-containing phenolic dimers and trimers isolated from maize bran Bunzel, Mirko; Ralph, John; Funk, Carola Tetrahedron Letters, Vol. 46, Issue 35 https://doi.org/10.1016/j.tetlet.2005.06.140	journal	August 2005
Characterization and Elimination of Undesirable Protein Residues in Plant Cell Wall Materials for Enhancing Lignin Analysis by Solution-State Nuclear Magnetic Resonance Spectroscopy Kim, Hoon; Padmakshan, Dharshana; Li, Yanding Biomacromolecules, Vol. 18, Issue 12 https://doi.org/10.1021/acs.biomac.7b01223	journal	November 2017
Variability in Lignin Composition and Structure in Cell Walls of Different Parts of Macaúba ( Acrocomia aculeata ) Palm Fruit Rencoret, Jorge; Kim, Hoon; Evaristo, Anderson B. Journal of Agricultural and Food Chemistry, Vol. 66, Issue 1 https://doi.org/10.1021/acs.jafc.7b04638	journal	December 2017
Cross-Linking of Maize Walls by Ferulate Dimerization and Incorporation into Lignin Grabber, John H.; Ralph, John; Hatfield, Ronald D. Journal of Agricultural and Food Chemistry, Vol. 48, Issue 12, p. 6106-6113 https://doi.org/10.1021/jf0006978	journal	December 2000
Model Studies of Ferulate−Coniferyl Alcohol Cross-Product Formation in Primary Maize Walls: Implications for Lignification in Grasses Grabber, John H.; Ralph, John; Hatfield, Ronald D. Journal of Agricultural and Food Chemistry, Vol. 50, Issue 21, p. 6008-6016 https://doi.org/10.1021/jf0205312	journal	October 2002
Sinapate Dehydrodimers and Sinapate−Ferulate Heterodimers in Cereal Dietary Fiber Bunzel, Mirko; Ralph, John; Kim, Hoon Journal of Agricultural and Food Chemistry, Vol. 51, Issue 5 https://doi.org/10.1021/jf020910v	journal	February 2003
Lignins and Ferulate−Coniferyl Alcohol Cross-Coupling Products in Cereal Grains Bunzel, Mirko; Ralph, John; Lu, Fachuang Journal of Agricultural and Food Chemistry, Vol. 52, Issue 21 https://doi.org/10.1021/jf040204p	journal	October 2004
Structural Identification of Dehydrotriferulic and Dehydrotetraferulic Acids Isolated from Insoluble Maize Bran Fiber Bunzel, Mirko; Ralph, John; Brüning, Philipp Journal of Agricultural and Food Chemistry, Vol. 54, Issue 17 https://doi.org/10.1021/jf061196a	journal	August 2006
Structural Characterization of Wheat Straw Lignin as Revealed by Analytical Pyrolysis, 2D-NMR, and Reductive Cleavage Methods del Río, José C.; Rencoret, Jorge; Prinsen, Pepijn Journal of Agricultural and Food Chemistry, Vol. 60, Issue 23 https://doi.org/10.1021/jf301002n	journal	December 2011
Derivatization Followed by Reductive Cleavage (DFRC Method), a New Method for Lignin Analysis: Protocol for Analysis of DFRC Monomers Lu, Fachuang; Ralph, John Journal of Agricultural and Food Chemistry, Vol. 45, Issue 7 https://doi.org/10.1021/jf970258h	journal	July 1997
Online Structural Elucidation of Alkaloids and Other Constituents in Crude Extracts and Cultured Cells of Nandina domestica by Combination of LC-MS/MS, LC-NMR, and LC-CD Analyses Iwasa, Kinuko; Takahashi, Teturo; Nishiyama, Yumi Journal of Natural Products, Vol. 71, Issue 8 https://doi.org/10.1021/np8001496	journal	August 2008
Isolation and characterization of new lignin streams derived from extractive-ammonia (EA) pretreatment da Costa Sousa, Leonardo; Foston, Marcus; Bokade, Vijay Green Chemistry, Vol. 18, Issue 15 https://doi.org/10.1039/C6GC00298F	journal	January 2016
Lignin–ferulate cross-links in grasses. Part 4.1–3 Incorporation of 5–5-coupled dehydrodiferulate into synthetic lignin Quideau, Stéphane; Ralph, John Journal of the Chemical Society, Perkin Transactions 1, Issue 16 https://doi.org/10.1039/a701808h	journal	January 1997
Identification and synthesis of new ferulic acid dehydrodimers present in grass cell walls Ralph, John; Quideau, St�phane; Grabber, John H. Journal of the Chemical Society, Perkin Transactions 1, Issue 23 https://doi.org/10.1039/p19940003485	journal	January 1994
NMR characterization of altered lignins extracted from tobacco plants down-regulated for lignification enzymes cinnamylalcohol dehydrogenase and cinnamoyl-CoA reductase Ralph, J.; Hatfield, R. D.; Piquemal, J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 22 https://doi.org/10.1073/pnas.95.22.12803	journal	October 1998
Environmental Stresses of Field Growth Allow Cinnamyl Alcohol Dehydrogenase-Deficient Nicotiana attenuata Plants to Compensate for their Structural Deficiencies Kaur, Harleen; Shaker, Kamel; Heinzel, Nicolas Plant Physiology, Vol. 159, Issue 4 https://doi.org/10.1104/pp.112.196717	journal	May 2012
Tricin, a Flavonoid Monomer in Monocot Lignification Lan, Wu; Lu, Fachuang; Regner, Matthew Plant Physiology, Vol. 167, Issue 4 https://doi.org/10.1104/pp.114.253757	journal	February 2015
Maize Tricin-Oligolignol Metabolites and their Implications for Monocot Lignification Lan, Wu; Morreel, Kris; Lu, Fachuang Plant Physiology https://doi.org/10.1104/pp.16.02012	journal	April 2016
Hydroxystilbenes Are Monomers in Palm Fruit Endocarp Lignins Carlos del Río, José; Rencoret, Jorge; Gutiérrez, Ana Plant Physiology, Vol. 174, Issue 4 https://doi.org/10.1104/pp.17.00362	journal	June 2017
Metabolic engineering of novel lignin in biomass crops Vanholme, Ruben; Morreel, Kris; Darrah, Chiarina New Phytologist, Vol. 196, Issue 4 https://doi.org/10.1111/j.1469-8137.2012.04337.x	journal	October 2012
Monolignol Ferulate Transferase Introduces Chemically Labile Linkages into the Lignin Backbone Wilkerson, C. G.; Mansfield, S. D.; Lu, F. Science, Vol. 344, Issue 6179, p. 90-93 https://doi.org/10.1126/science.1250161	journal	April 2014
Phenylamides in plants Edreva, A. M.; Velikova, V. B.; Tsonev, T. D. Russian Journal of Plant Physiology, Vol. 54, Issue 3 https://doi.org/10.1134/S1021443707030016	journal	May 2007
Hydroxycinnamic acid amide metabolism: physiology and biochemistry Facchini, Peter J.; Hagel, Jillian; Zulak, Katherine G. Canadian Journal of Botany, Vol. 80, Issue 6 https://doi.org/10.1139/b02-065	journal	June 2002
Identifying new lignin bioengineering targets: 1. Monolignol-substitute impacts on lignin formation and cell wall fermentability Grabber, John H.; Schatz, Paul F.; Kim, Hoon BMC Plant Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2229-10-114	journal	January 2010
Genetic manipulation of putrescine biosynthesis reprograms the cellular transcriptome and the metabolome Page, Andrew F.; Cseke, Leland J.; Minocha, Rakesh BMC Plant Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12870-016-0796-2	journal	May 2016
Impact of lignin polymer backbone esters on ionic liquid pretreatment of poplar Kim, Kwang Ho; Dutta, Tanmoy; Ralph, John Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0784-2	journal	April 2017
Developing Pericarp of Maize: A Model to Study Arabinoxylan Synthesis and Feruloylation Chateigner-Boutin, Anne-Laure; Ordaz-Ortiz, José J.; Alvarado, Camille Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01476	journal	September 2016

Cited By (2)

Lignin biosynthesis: old roads revisited and new roads explored Dixon, Richard A.; Barros, Jaime Open Biology, Vol. 9, Issue 12 https://doi.org/10.1098/rsob.190215	journal	December 2019
Lignin – An underutilized, renewable and valuable material for food industry Tao, Jianming; Li, Sheng; Ye, Fayin Critical Reviews in Food Science and Nutrition, Vol. 60, Issue 12 https://doi.org/10.1080/10408398.2019.1625025	journal	June 2019

Similar Records

Insights of Ethanol Organosolv Pretreatment on Lignin Properties of Broussonetia papyrifera

Journal Article · Mon Sep 10 20:00:00 EDT 2018 · ACS Sustainable Chemistry & Engineering · OSTI ID:1492166

Estimation of Syringyl Units in Wood Lignins by FT-Raman Spectroscopy

Journal Article · Tue Mar 26 20:00:00 EDT 2019 · Journal of Agricultural and Food Chemistry · OSTI ID:1546618

Related Subjects

2D NMR
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
Maize kernels
ferulates
hydroxycinnamoyl amides
lignin monomers

Structural Characterization of Lignin from Maize ( Zea mays L.) Fibers: Evidence for Diferuloylputrescine Incorporated into the Lignin Polymer in Maize Kernels

Citation Formats

References (47)

Cited By (2)

Similar Records

Related Subjects