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Formation of syringyl-rich lignins in maize as influenced by feruloylated xylans and p-coumaroylated monolignols

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Abstract

Grass cell walls are atypical because their xylans are acylated with ferulate and lignins are acylated with p-coumarate. To probe the role and interactions of these p-hydroxycinnamates during lignification, feruloylated primary cell walls isolated from maize cell suspensions were lignified with coniferyl and sinapyl alcohols and with varying levels of p-coumarate esters. Ferulate xylan esters enhanced the formation of wall-bound syringyl lignin more than methyl p-coumarate, however, maximal concentrations of syringyl lignin were only one-third that of guaiacyl lignin. Including sinapyl p-coumarate, the presumed precursor of p-coumaroylated lignins, with monolignols unexpectedly accelerated peroxidase inactivation, interfered with ferulate copolymerization into lignin, and had minimal or adverse effects on cell wall lignification. Free phenolic groups of p-coumarate esters in isolated maize lignin and pith cell walls did not undergo oxidative coupling with each other or with added monolignols. Thus, the extensive formation of syringyl-rich lignins and the functional role of extensive lignin acylation by p-coumarate in grasses remains a mystery.

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Abbreviations

AIP:

2-Aminoindan-2-phosphonic acid

References

  • Bergvinson DJ, Arnason JT, Hamilton RI (1997) Phytochemical changes during recurrent selection for resistance to the European corn borer. Crop Sci 37:1567–1572

    Article  CAS  Google Scholar 

  • Bily AC, Reid LM, Taylor JH, Johnston D, Malouin C, Burt AJ, Bakan B, Regnault-Roger C, Pauls KP, Arnason JT, Philogene BJR (2003) Dehydrodimers of ferulic acid in maize grain pericarp and aleurone: resistance factors to Fusarium graminearum. Phytopathology 93:712–719

    Article  CAS  PubMed  Google Scholar 

  • Bunzel M, Ralph J, Marita JM, Hatfield RD, Steinhart H (2001) Diferulates as structural components in soluble and insoluble cereal dietary fibre. J Sci Food Agric 81:653–660

    Article  CAS  Google Scholar 

  • Casler MD, Jung HJG (1999) Selection and evaluation of smooth bromegrass clones with divergent lignin or etherified ferulic acid concentration. Crop Sci 39:1866–1873

    Article  CAS  Google Scholar 

  • Chesson A, Provan GJ, Russell W, Scobbie L, Chabbert B, Monties B (1997) Characterisation of lignin from parenchyma and sclerenchyma cell walls of the maize internode. J Sci Food Ag 73:10–16

    Article  CAS  Google Scholar 

  • Ferguson LR, Lim IF, Pearson AE, Ralph J, Harris PJ (2003) Bacterial antimutagenesis by hydroxycinnamic acids from plant cell walls. Mutation Research 542:49–58

    PubMed  CAS  Google Scholar 

  • Ferrer MA, Barcelo AR (1994) Inactivation of cell wall acidic peroxidase isoenzymes during the oxidation of coniferyl alcohol in Lupinus. Phytochemistry 36:1161–1163

    Article  CAS  Google Scholar 

  • Funk C, Weber P, Thilker J, Grabber JH, Steinhart H, Bunzel M (2006) Influence of lignification and feruloylation of maize cell walls on the adsorption of heterocyclic aromatic amines. J Ag Food Chem 54:1860–1867

    Article  CAS  Google Scholar 

  • Garcia-Conesa MT, Wilson PD, Plumb GW, Ralph J, Williamson G (1999) Antioxidant properties of 4,4′-dihydroxy-3,3′-dimethoxy-β,β′-bicinnamic acid (8-8-diferulate non-cyclic form). J Sci Food Agric 79:379–384

    Article  CAS  Google Scholar 

  • Gordon AH, Lomax JA, Dalgarno K, Chesson A (1985) Preparation and composition of mesophyll, epidermis and fibre cell walls from perennial ryegrass (Lolium perenne) and Italian ryegrass (Lolium multiflorum). J Sci Food Agric 36:509–519

    Article  CAS  Google Scholar 

  • Grabber JH (2005) How do lignin composition, structure, and cross-linking affect degradability? A review of cell wall model studies. Crop Sci 45:820–831

    Article  CAS  Google Scholar 

  • Grabber JH, Jung GA, Hill RR (1991) Chemical composition of parenchyma and sclerenchyma cell walls isolated from orchardgrass and switchgrass. Crop Sci 31:1058–1065

    Article  CAS  Google Scholar 

  • Grabber JH, Quideau S, Ralph J (1996a) p-Coumaroylated syringyl units in maize lignin; implications for β-ether cleavage by thioacidolysis. Phytochemistry 43:1189–1194

    Article  CAS  Google Scholar 

  • Grabber JH, Ralph J, Hatfield RD, Quideau S, Kuster T, Pell AN (1996b) Dehydrogenation polymer-cell wall complexes as a model for lignified grass walls. J Agric Food Chem 44:1453–1459

    Article  CAS  Google Scholar 

  • Grabber JH, Ralph J, Hatfield RD (1998) Ferulate cross-links limit the enzymatic degradation of synthetically lignified primary walls of maize. J Agric Food Chem 46:2609–2614

    Article  CAS  Google Scholar 

  • Grabber JH, Ralph J, Hatfield RD (2000) Cross-linking of maize walls by ferulate dimerization and incorporation into lignin. J Agric Food Chem 48:6106–6113

    Article  PubMed  CAS  Google Scholar 

  • Grabber JH, Ralph J, Hatfield RD (2002) Model studies of ferulate-coniferyl alcohol cross-product formation in primary maize walls: implications for lignification in grasses. J Agric Food Chem 50:6008–6016

    Article  PubMed  CAS  Google Scholar 

  • Grabber JH, Ralph J, Lapierre C, Barrière Y (2004) Genetic and molecular basis of grass cell wall degradability. I. Lignin-cell wall matrix interactions C R Biologies 327:455–465

    Article  PubMed  CAS  Google Scholar 

  • Hatfield RD, Jung HG, Ralph J, Buxton DR, Weimer PJ (1994) A comparison of the insoluble residues produced by the Klason lignin and acid detergent lignin procedures. J. Sci. Food Agric. 65:51–58

    Article  CAS  Google Scholar 

  • Hatfield RD, Grabber J, Ralph J (1997) A potential role of sinapyl p-coumarate in grass lignin formation. Annual meeting of the American society of plant physiologists, Vancouver, p 86

  • Hatfield RD, Wilson JR, Mertens DR (1999) Composition of cell walls isolated from cell types of grain sorghum stems. J Sci Food Agric 79:891–899

    Article  CAS  Google Scholar 

  • Huang L, Colas C, Ortiz de Montellano PR (2004) Oxidation of carboxylic acids by horseradish peroxidase results in prosthetic heme modification and inactiviation. J Am Chem Soc 126:12865–12873

    Article  PubMed  CAS  Google Scholar 

  • Jung HJG (2003) Maize stem tissues: ferulate deposition in developing internode cell walls. Phytochemistry 63:543–549

    Article  PubMed  CAS  Google Scholar 

  • Lam TBT, Iiyama K, Stone B (1996) Lignin and hydroxycinnamic acids in walls of brown midrib mutants of sorghum, pearl millet and maize stems. J Sci Food Agric 71:174–178

    Article  CAS  Google Scholar 

  • Lu F, Ralph J (1998a) Facile synthesis of 4-hydroxycinnamyl p-coumarates. J Agric Food Chem 46:2911–2913

    Article  CAS  Google Scholar 

  • Lu F, Ralph J (1998b) Highly selective syntheses of coniferyl and sinapyl alcohols. J Agric Food Chem 46:1794–1796

    Article  CAS  Google Scholar 

  • Lu F, Ralph J (2005) Novel β–β-structures in natural lignins incorporating acylated monolignols. In: 13th international symposium on wood, fiber, and pulping chemistry. APPITA, Auckland, p 233–237

  • MacAdam JW, Grabber JH (2002) Relationship of growth cessation with the formation of diferulate cross-links and p-coumaroylated lignins in tall fescue. Planta 215:785–793

    Article  PubMed  CAS  Google Scholar 

  • Migne C, Prensier G, Utille JP, Angibeaud P, Cornu A, Grenet E (1998) Immunocytochemical localisation of para-coumaric acid and feruloyl-arabinose in the cell walls of maize stem. J Sci Food Agric 78:373–381

    Article  CAS  Google Scholar 

  • Morrison TA, Jung HG, Buxton DR, Hatfield RD (1998) Cell-wall composition of maize internodes of varying maturity. Crop Sci 38:455–460

    Article  CAS  Google Scholar 

  • Musel G, Schindler T, Bergfeld R, Ruel K, Jacquet G, Lapierre C, Speth V, Schopfer P (1997) Structure and distribution of lignin in primary and secondary cell walls of maize coleoptiles analyzed by chemical and immunological probes. Planta 201:146–159

    Article  Google Scholar 

  • Musha Y, Goring DAI (1974) Klason and acid soluble lignin content of hardwoods. Wood Sci 7:133–134

    CAS  Google Scholar 

  • Myton KE, Fry SC (1994) Intraprotoplasmic feruloylation of arabinoxylans in Festuca arundinacea cell cultures. Planta 193:326–330

    Article  CAS  Google Scholar 

  • Ralph J, Hatfield RD, Quideau S, Helm RF, Grabber JH, Jung H-JG (1994) Pathway of p-coumaric acid incorporation into maize lignin as revealed by NMR. J Am Chem Soc 116:9448–9456

    Article  CAS  Google Scholar 

  • Ralph J, Grabber JH, Hatfield RD (1995) Lignin-ferulate cross-links in grasses: active incorporation of ferulate polysaccharide esters into ryegrass lignins. Carbohydr Res 275:167–178

    Article  CAS  Google Scholar 

  • Santiago R, Malvar RA, Baamonde MD, Revilla P, Souto XC (2005) Free phenols in maize pith and their relationship with resistence to Sesamia nonagrioides (Lepidoptera: Noctuidae) attack. J Econ Entomol 98:1349–1356

    Article  PubMed  CAS  Google Scholar 

  • Santiago R, Butron A, Arnason JT, Reid LM, Souto XC, Malvar RA (2006) Putative role of pith cell wall phenylpropanoids in Sesamia nonagrioides (Lepidoptera: Noctuidae) resistance. J Ag Food Chem 54:2274–2279

    Article  CAS  Google Scholar 

  • Saulnier L, Crepeau MJ, Lahaye M, Thibault JF, Garcia-Conesa MT, Kroon PA, Williamson G (1999) Isolation and structural determination of two 5,5′-diferuloyl oligosaccharides indicate that maize heteroxylans are covalently cross-linked by oxidatively coupled ferulates. Carbohydr Res 320:82–92

    Article  CAS  Google Scholar 

  • Schooneveld-Bergmans MEF, Dignum MJW, Grabber JH, Beldman G, Voragen AGJ (1999) Studies on the oxidative cross-linking of feruloylated arabinoxylans from wheat flour and wheat bran. Carbohydr Polymers 38:309–317

    Article  CAS  Google Scholar 

  • Schopfer P (1996) Hydrogen peroxide-mediated cell-wall stiffening in vitro in maize coleoptiles. Planta 199:43–49

    Article  CAS  Google Scholar 

  • Steel RGD, Torrie JH (1980) Principles and procedures of statistics. McGraw-Hill Publishing Co., New York, pp 633

    Google Scholar 

  • Sukalovic VHT, Vuletic M, Vucinic Z (2005) The role of p-coumaric acid in oxidative and peroxidative cycle of the ionically bound peroxidase of the maize root cell wall. Plant Sci 168:931–938

    Article  CAS  Google Scholar 

  • Takahama U, Oniki T, Shimokawa H (1996) A possible mechanism for the oxidation of sinapyl alcohol by peroxidase-dependent reactions in the apoplast: enhancement of the oxidation by hydroxycinnamic acids and components of the apoplast. Plant Cell Physiol 37:499–504

    CAS  Google Scholar 

  • Terashima N, Fukushima K, He L-F, Takabe K (1993) Comprehensive model of the lignified plant cell wall. In: Jung HG, Buxton DR, Hatfield RD, Ralph J (eds) Forage cell wall structure and digestibility. ASA-CSSA-SSSA, Madison, pp 247–270

    Google Scholar 

Download references

Acknowledgments

The authors thank Hoon Kim for providing some of the coniferyl and sinapyl alcohols used in our experiments. Christy Davidson is gratefully acknowledged for assisting with the preparation and analysis of cell walls. Ronald Hatfield and Jane Marita are recognized for helping with p-hydroxycinnamate analyses by GLC-FID and GLC-MS. The authors also thank John Ralph for his insightful comments, which enhanced the manuscript. This work was supported in part by USDA-NRI (1994-37500-0580, 1996-35304-3864, and 2003-35103-13834). Mention of a trademark or proprietary product does not constitute a guarantee or warranty of the product by the USDA and does not imply its approval to the exclusion of other products that may also be suitable.

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Correspondence to John H. Grabber.

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Grabber, J.H., Lu, F. Formation of syringyl-rich lignins in maize as influenced by feruloylated xylans and p-coumaroylated monolignols. Planta 226, 741–751 (2007). https://doi.org/10.1007/s00425-007-0521-3

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  • DOI: https://doi.org/10.1007/s00425-007-0521-3

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