Skip to main content

Advertisement

SpringerLink
Log in

Grass lignin acylation: p-coumaroyl transferase activity and cell wall characteristics of C3 and C4 grasses

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Grasses are a predominant source of nutritional energy for livestock systems around the world. Grasses with high lignin content have lower energy conversion efficiencies for production of bioenergy either in the form of ethanol or to milk and meat through ruminants. Grass lignins are uniquely acylated with p-coumarates (pCA), resulting from the incorporation of monolignol p-coumarate conjugates into the growing lignin polymer within the cell wall matrix. The required acyl-transferase is a soluble enzyme (p-coumaroyl transferase, pCAT) that utilizes p-coumaroyl-CoenzymeA (pCA-CoA) as the activated donor molecule and sinapyl alcohol as the preferred acceptor molecule. Grasses (C3and C4) were evaluated for cell wall characteristics; pCA, lignin, pCAT activity, and neutral sugar composition. All C3 and C4 grasses had measurable pCAT activity, however the pCAT activities did not follow the same pattern as the pCA incorporation into lignin as expected.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Scheme 1
Fig. 1
Fig. 2
Fig. 3
Scheme 2
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

CW:

Cell wall

pCA:

p-Coumarates

FA:

Ferulates

S:

Syringyl

G:

Guaiacyl

CA-pCA:

Coniferyl p-coumarate

SA-pCA:

Sinapyl p-coumarate

pCAT:

p-Coumaroyl transferase

dHSA:

Dihydrosinapyl alcohol

dHCA:

Dihydroconiferyl alcohol

EtOH:

Ethanol

MeOH:

Methanol

TFA:

Trifluoroacetic acid

Tris:

2-Amino-2-(hydroxymethyl)-1,3-propanediol

MOPS:

4-Morpholinepropanesulfonicacid

GLC–FID:

Gas liquid chromatography–flame ionization detection

Glc:

Glucose

Xyl:

Xylose

Ara:

Arabinose

GAX:

Glucuronoarabinoxylans

References

  • Blakeney AB, Harris PJ, Henry RJ, Stone BA (1983) A simple and rapid preparation of alditol acetates for monosaccharide analysis. Carbohydr Res 113:291–299

    Article  CAS  Google Scholar 

  • Bunzel M, Ralph J, Brüning P, Steinhart H (2006) Structural identification of dehydrotriferulic and dehydrotetraferulic acids isolated from insoluble maize fiber. J Agric Food Chem 54:6409–6418

    Article  PubMed  CAS  Google Scholar 

  • Buxton DR (1991) Digestibility by rumen microorganisms of neutral sugars in perennial forage stems and leaves. Anim Feed Sci Technol 32:119–122

    Article  CAS  Google Scholar 

  • Buxton DR, Russell JR, Wedin WF (1987) Structural neutral sugars in legume and grass stems in relation to digestibility. Crop Sci 27:1279–1285

    CAS  Google Scholar 

  • Crestini C, Argyropoulos DS (1997) Structural analysis of wheat straw lignin by quantitative 31P and 2D NMR spectroscopy. The occurrence of ester bonds and α-O-4 substructures. J Agric Food Chem 45:1212–1219

    Article  CAS  Google Scholar 

  • D’-Auria JC (2006) Acyltransferases in plants: a good time to be BAHD. Curr Opin Plant Biol 9:331–340

    Article  CAS  Google Scholar 

  • Dubois M, Giles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Falkner LK, Coors JG, Ostrander BM, Kaeppler SM, Hatfield RD (2000) Lax leaf maize: cell wall composition and nutritional value. J Sci Food Agric 80:255–262

    Article  CAS  Google Scholar 

  • Freudenberg K, Neish AC (1968) Constitution and biosynthesis of lignin. Springer, Berlin

    Google Scholar 

  • Fukushima RS, Hatfield RD (2001) Extraction and isolation of lignin for utilization as a standard to determine lignin concentration using the acetyl bromide spectrophotometric method. J Agric Food Chem 49:3133–3139

    Article  PubMed  CAS  Google Scholar 

  • Grabber JH, Hatfield RD, Ralph J, Zon J, Amrhein N (1995) Ferulate cross-linking in cell walls isolated from maize cell suspensions. Phytochemistry 40:1077–1082

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Grabber JH, Hatfield RD, Ralph J (1998a) Diferulate cross-links impede the enzymatic degradation of nonlignified maize walls. J Sci Food Agric 77:193–200

    Article  CAS  Google Scholar 

  • Grabber JH, Ralph J, Hatfield RD (1998b) 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 (1998c) Severe inhibition of maize wall degradation by synthetic lignins formed with coniferaldehyde. J Sci Food Agric 78:81–87

    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 

  • Harris PJ, Hartley RD (1980) Phenolic constituents of the cell walls of monocotyledons. Biochem Syst Ecol 8:153–160

    Article  CAS  Google Scholar 

  • Hartley RD, Harris PJ (1981) Phenolic constituents of the cell walls of dicotyledons. Biochem Syst Ecol 9:189–203

    Article  CAS  Google Scholar 

  • Hatfield RD (1992) Carbohydrate composition of alfalfa cell walls isolated from stem sections differing maturity. J Agric Food Chem 40:424–430

    Article  CAS  Google Scholar 

  • Hatfield RD, Weimer PJ (1995) Degradation characteristics of isolated and in-situ cell-wall Lucerne pectic polysaccharides by mixed ruminal microbes. J Sci Food Agric 69:185–196

    Article  CAS  Google Scholar 

  • Hatfield RD, Grabber JH, Ralph J, Brei K (1999a) Using the acetyl bromide assay to determine lignin concentrations in herbaceous plants: some cautionary notes. J Agric Food Chem 47:628–632

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hatfield R, Ralph J, Grabber JH (2008a) A potential role for sinapyl p-coumarate as a radical transfer mechanism in grass lignin formation. Planta 228(6):919–928

    Article  PubMed  CAS  Google Scholar 

  • Hatfield RD, Marita JM, Frost K (2008b) Characterization of p-coumarate accumulation, p-coumaroyl transferase, and cell wall changes during the development of corn stems. J Sci Food Agric 88:2529–2537

    Article  CAS  Google Scholar 

  • Iiyama K, Lam TBT (1990) Lignin in wheat internodes. Part 1: the reactivities of lignin units during alkaline nitrobenzene oxidation. J Sci Food Agric 51:481–491

    Article  CAS  Google Scholar 

  • Ishii T, Hiroi T (1990a) Isolation and characterization of feruloylated arabinoxylan oligosaccharides from bamboo shoot cell walls. Carbohydr Res 196:175–183

    Article  PubMed  CAS  Google Scholar 

  • Ishii T, Hiroi T (1990b) Linkage of phenolic acids to cell-wall polysaccharides of bamboo shoot. Carbohydr Res 206:297–310

    Article  PubMed  CAS  Google Scholar 

  • Kato Y, Nevins DJ (1985) Isolation and identification of O-(5-O-feruloyl-α-l-arabinofuranosyl)-(1–3)-O-β-d-xylopyranosyl-(1–4)-d-xylose as a component of Zea mays shoot cell-walls. Carbohydr Res 137:139–150

    Article  CAS  Google Scholar 

  • Kim H, Ralph J, Akiyama T (2008) Solution-state NMR of ball-milled whole cell walls in DMSO-d6. Bioenergy Res 1:56–66

    Article  Google Scholar 

  • Kim H, Ralph J, Lu F, Ralph SA, Boudet A-M, MacKay JJ, Sederoff RR, Ito T, Kawai S, Ohashi H, Higuchi T (2003) NMR Analysis of Lignins in CAD-deficient Plants. Part 1. Incorporation of hydroxycinnamaldehydes and hydroxybenzaldehydes into lignins. Org Biomol Chem 1:268–281

    Article  PubMed  CAS  Google Scholar 

  • Kutsuki H, Shimada M, Higuchi T (1982) Distribution and roles of p-hydroxycinnamate:CoA ligase in lignin biosynthesis. Phytochemistry 21:267–271

    Article  CAS  Google Scholar 

  • Lam TBT, Iiyama K, Stone BA (1992a) Changes in phenolic acids from internode walls of wheat and Phalaris during maturation. Phytochemistry 31:2655–2658

    Article  CAS  Google Scholar 

  • Lam TBT, Iiyama K, Stone BA (1992b) Cinnamic acid bridges between cell wall polymers in wheat and phalaris internodes. Phytochemistry 31:1179–1183

    Article  Google Scholar 

  • Lindl T, Dreuzaler F, Hahlbrock K (1973) Synthesis of p-coumaroyl coenzyme A with a partially purified p-coumarate: CoA ligase from cell suspension cultures of soybean (Glycine max). Biochim Biophys Acta 302:457–464

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lu F, Ralph J (1999) Detection and determination of p-coumaroylated units in lignins. J Agric Food Chem 47:1988–1992

    Article  PubMed  CAS  Google Scholar 

  • Lu F, Ralph J (2002) Preliminary evidence for sinapyl acetate as a lignin monomer in kenaf. Chem Commun 90–91

  • Luderitz T, Schatz G, Grisebach H (1982) Enzymic syntesis of lignin precursors—purification and properties of 4-coumarate: CoA ligase from cambial sap of spruce (Picea abies L.). Eur J Biochem 123:583–586

    PubMed  CAS  Google Scholar 

  • MacAdam JW, Grabber JH (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

    Article  PubMed  CAS  Google Scholar 

  • Meyermans H, Morreel K, Lapierre C, Pollet B, De Bruyn A, Busson R, Herdewijn P, Devreese B, Van Beeumen J, Marita JM, Ralph J, Chen C, Burggraeve B, Van Montagu M, Messens E, Boerjan W (2000) Modifications in lignin and accumulation of phenolic glucosides in poplar xylem upon down-regulation of caffeoyl-coenzyme A O-methyltransferase, an enzyme involved in lignin biosynthesis. J Biol Chem 275:36899–36909

    Article  PubMed  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 

  • Pollock CJ, Cairns AJ (1991) Fructan metabolism in grasses and cereals. Annu Rev Plant Physiol 42:77–101

    Article  CAS  Google Scholar 

  • Ralph J, Helm RF (1993) Lignin/hydroxycinnamic acid/polysaccharide complexes: synthetic models for regiochemical characterization. In: Jung HG, Buxton DR, Hatfield RD, Ralph J (eds) Forage cell wall structure and digestibility. ASA-CSSA-SSSA, Madison, pp 201–246

    Google Scholar 

  • Ralph J, Hatfield RD, Quideau S, Helm RF, Grabber JH, Jung H-JG (1994a) 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, Quideau S, Grabber JH, Hatfield RD (1994b) Identification and synthesis of new ferulic acid dehydrodimers present in grass cell walls. J Chem Soc Perkin Trans 1:3485–3498

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ralph J, Marita JM, Ralph SA, Hatfield RD, Lu F, Ede RM, Peng J, Quideau S, Helm RF, Grabber JH, Kim H, Jimenez-Monteon G, Zhang Y, Jung H-JG, Landucci LL, MacKay JJ, Sederoff RR, Chapple C, Boudet AM (1999) Solution-state NMR of lignins. In: Argyropoulos DS, Rials T (eds) Advances in lignocellulosics characterization. TAPPI Press, Atlanta, pp 55–108

    Google Scholar 

  • Ralph J, Bunzel M, Marita JM, Hatfield RD, Lu F, Kim H, Grabber JH, Ralph SA, Jimenez-Monteon G, Steinhart H (2000) Diferulates analysis: new diferulates and disinapates in insoluble cereal fibre. Polyphénol Actual 19:13–17

    CAS  Google Scholar 

  • Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz PF, Marita JM, Hatfield RD, Ralph SA, Christensen JH, Boerjan W (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenylpropanoids. Phytochem Rev 3:29–60

    Article  CAS  Google Scholar 

  • Saeman JF, Moore WE, Millett MA (1963) Sugar units present. Hydrolysis and quantitative paper chromatography. In: Whistler RL (ed) Cellulose. Academic, New York, pp 54–69

    Google Scholar 

  • Sanchez J, Mancha M (1981) Synthesis of acyl-CoAs by isolated spinach chloroplasts in relation to added CoA and ATP. Planta 153:519–523

    Article  CAS  Google Scholar 

  • Scalbert A, Monties B, Rolando C, Sierra-Escudero A (1986) Formation of ether linkage between phenolic acids and Gramineae lignin: a possible mechanism involving quinone methides. Holzforschung 40:191–195

    Article  CAS  Google Scholar 

  • Scobbie L, Russell W, Provan GJ, Chesson A (1993) The newly extended maize internode: a model for the study of secondary cell wall formation and consequences for digestibility. J Sci Food Agric 61:217–225

    Article  CAS  Google Scholar 

  • Shea EM, Hatfield RD (1993) Characterization of a pectic fraction from smooth bromegrass cell walls using an endopolygalacturonase. J Agric Food Chem 41:380–387

    Article  CAS  Google Scholar 

  • Smith DCC (1955) Ester groups in lignin. Nature 176:267–268

    Article  CAS  Google Scholar 

  • Stockigt J, Zenk MH (1975) Chemical synthesis and properties of hydroxycinnamoyl-coenzyme A derivatives. Z Naturforsch C Biosci 30C:352–358

    Google Scholar 

  • Yelle DJ, Ralph J, Frihart CR (2007) Using high-resolution solution-state NMR spectroscopy to investigate pMDI reactions with wood. Wood-base Composites Center Spring 2007 Industry Advisory Board Meeting and Technical Forum, University of British Columbia, British Columbia

  • Yelle DJ, Ralph J, Frihart CR (2008) Characterization of nonderivatized plant cell walls using high-resolution solution-state NMR spectroscopy. Magn Reson Chem 46:508–517

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported with funding from NRI-CGP (Plant Biochemistry Section—Grant No. 2004-03034) and was partially funded by Monsanto Company (CRADA No. 58-3K95-2-938) and ArborGen, LLC (CRADA No. 58-3K95-8-598). Mention of a trademark or proprietary product does not constitute a guarantee or warranty of product by the USDA and does not imply its approval to the exclusion of other products that may also be suitable. A special thanks to Lindsay Stafslien for her dedication and help in processing the samples.

Author information

Authors and Affiliations

  1. U.S. Dairy Forage Research Center, USDA-Agricultural Research Service, 1925 Linden Drive, Madison, WI, 53706, USA

    Ronald D. Hatfield, Jane M. Marita, Kenneth Frost, John Grabber & John Ralph

  2. Department of Agronomy, University of Wisconsin, Madison, WI, 53706, USA

    John Grabber

  3. Department of Biochemistry, University of Wisconsin, Madison, WI, 53706, USA

    John Ralph, Fachuang Lu & Hoon Kim

Authors
  1. Ronald D. Hatfield
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jane M. Marita
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kenneth Frost
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. John Grabber
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John Ralph
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fachuang Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hoon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ronald D. Hatfield.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hatfield, R.D., Marita, J.M., Frost, K. et al. Grass lignin acylation: p-coumaroyl transferase activity and cell wall characteristics of C3 and C4 grasses. Planta 229, 1253–1267 (2009). https://doi.org/10.1007/s00425-009-0900-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-009-0900-z

Keywords

Search

Navigation