Abstract
Most of the known 4-coumarate:coenzyme A ligase (4CL) isoforms lack CoA-ligation activity for sinapic acid. Therefore, there is some doubt as to whether sinapic acid contributes to sinapyl alcohol biosynthesis. In this study, we characterized the enzyme activity of a protein mixture extracted from the developing xylem of Robinia pseudoacacia. The crude protein mixture contained at least two 4CLs with sinapic acid 4-CoA ligation activity. The crude enzyme preparation displayed negligible sinapaldehyde dehydrogenase activity, but showed ferulic acid 5-hydroxylation activity and 5-hydroxyferulic acid O-methyltransferase activity; these activities were retained in the presence of competitive substrates (coniferaldehyde and 5-hydroxyconiferaldehyde, respectively). 5-Hydroxyferulic acid and sinapic acid accumulated in the developing xylem of R. pseudoacacia, suggesting, in part at least, sinapic acid is a sinapyl alcohol precursor in this species.
Similar content being viewed by others
References
Allina SM, Pri-Hadash A, Theilmann DA, Ellis BE, Douglas CJ (1998) 4-Coumarate:coenzyme A ligase in hybrid poplar. Properties of native enzymes, cDNA cloning, and analysis of recombinant enzymes. Plant Physiol 116:743–754
Barros J, Serk H, Granlund I, Pesquet E (2015) The cell biology of lignification in higher plants. Ann Bot 115:1053–1074
Chapple CC, Vogt T, Ellis BE, Somerville CR (1992) An Arabidopsis mutant defective in the general phenylpropanoid pathway. Plant Cell 4:1413–1424
Chen HC et al (2013) Monolignol pathway 4-coumaric acid:coenzyme A ligases in Populus trichocarpa: novel specificity, metabolic regulation, and simulation of coenzyme A ligation fluxes. Plant Physiol 161:1501–1516
Costa MA et al (2005) Characterization in vitro and in vivo of the putative multigene 4-coumarate:CoA ligase network in Arabidopsis: syringyl lignin and sinapate/sinapyl alcohol derivative formation. Phytochemistry 66:2072–2091
Cukovic D, Ehlting J, VanZiffle JA, Douglas CJ (2001) Structure and evolution of 4-coumarate:coenzyme A ligase (4CL) gene families. Biol Chem 382:645–654
Ehlting J, Buttner D, Wang Q, Douglas CJ, Somssich IE, Kombrink E (1999) Three 4-coumarate:coenzyme A ligases in Arabidopsis thaliana represent two evolutionarily divergent classes in angiosperms. Plant J 19:9–20
Gross GG, Zenk MH (1966) Darstellung und Eigenschaften von Coenzym A-Thioestern substituierter Zimtsäuren. Z Naturforsch B 21:683–690
Gui J, Shen J, Li L (2011) Functional characterization of evolutionarily divergent 4-coumarate:coenzyme a ligases in rice. Plant Physiol 157:574–586
Hamada K, Tsutsumi Y, Nishida T (2003) Treatment of poplar callus with ferulic and sinapic acids II: effects on related monolignol biosynthetic enzyme activities. J Wood Sci 49:366–370
Hamada K, Nishida T, Yamauchi K, Fukushima K, Kondo R, Tsutsumi Y (2004) 4-Coumarate:coenzyme A ligase in black locust (Robinia pseudoacacia) catalyses the conversion of sinapate to sinapoyl-CoA. J Plant Res 117:303–310
Hamberger B, Hahlbrock K (2004) The 4-coumarate:CoA ligase gene family in Arabidopsis thaliana comprises one rare, sinapate-activating and three commonly occurring isoenzymes. Proc Natl Acad Sci 101:2209–2214
Higuchi T (2003) Pathways for monolignol biosynthesis via metabolic grids: coniferyl aldehyde 5-hydroxylase, a possible key enzyme in angiosperm syringyl lignin biosynthesis. Proc Jpn Acad B Phys 79:227–236
Hu WJ et al (1998) Compartmentalized expression of two structurally and functionally distinct 4-coumarate:CoA ligase genes in aspen (Populus tremuloides). Proc Natl Acad Sci 95:5407–5412
Humphreys JM, Hemm MR, Chapple C (1999) New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cytochrome P450-dependent monooxygenase. Proc Natl Acad Sci 96:10045–10050
Knobloch KH, Hahlbrock K (1975) Isoenzymes of p-coumarate: CoA ligase from cell suspension cultures of Glycine max. Eur J Biochem 52:311–320
Kumar M, Campbell L, Turner S (2016) Secondary cell walls: biosynthesis and manipulation. J Exp Bot 67:515–531
Landry LG, Chapple CC, Last RL (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiol 109:1159–1166
Li L, Popko JL, Umezawa T, Chiang VL (2000) 5-Hydroxyconiferyl aldehyde modulates enzymatic methylation for syringyl monolignol formation, a new view of monolignol biosynthesis in angiosperms. J Biol Chem 275:6537–6545
Li Y, Kim JI, Pysh L, Chapple C (2015) Four isoforms of Arabidopsis 4-Coumarate:CoA ligase have overlapping yet distinct roles in phenylpropanoid metabolism. Plant Physiol 169:2409–2421
Lindermayr C et al (2002) Divergent members of a soybean (Glycine max L.) 4-coumarate:coenzyme A ligase gene family. Eur J Biochem 269:1304–1315
Lozoya E, Hoffmann H, Douglas C, Schulz W, Scheel D, Hahlbrock K (1988) Primary structures and catalytic properties of isoenzymes encoded by the two 4-coumarate: CoA ligase genes in parsley. Eur J Biochem 176:661–667
Lüderitz T, Schatz G, Grisebach H (1982) Enzymic synthesis 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
Nair RB, Bastress KL, Ruegger MO, Denault JW, 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
Osakabe K et al (1999) Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms. Proc Natl Acad Sci 96:8955–8960
Shi R, Sun YH, Li Q, Heber S, Sederoff R, Chiang VL (2010) Towards a systems approach for lignin biosynthesis in Populus trichocarpa: transcript abundance and specificity of the monolignol biosynthetic genes. Plant Cell Physiol 51:144–163
Souza Cde A, Barbazuk B, Ralph SG, Bohlmann J, Hamberger B, Douglas CJ (2008) Genome-wide analysis of a land plant-specific acyl:coenzyme A synthetase (ACS) gene family in Arabidopsis, poplar, rice and Physcomitrella. New Phytol 179:987–1003
Stöckigt J, Zenk MH (1975) Chemical syntheses and properties of hydroxycinnamoyl-coenzyme A derivatives. Z Naturforsch C 30:352–358
Sun H, Li Y, Feng S, Zou W, Guo K, Fan C, Si S, Peng L (2013) Analysis of five rice 4-coumarate:coenzyme A ligase enzyme activity and stress response for potential roles in lignin and flavonoid biosynthesis in rice. Biochem Biophys Res Commun 430:1151–1156
Vanholme R et al (2013) Caffeoyl shikimate esterase (CSE) is an enzyme in the lignin biosynthetic pathway in Arabidopsis. Science 341:1103–1106
Yamauchi K, Yasuda S, Fukushima K (2002) Evidence for the biosynthetic pathway from sinapic acid to syringyl lignin using labeled sinapic acid with stable isotope at both methoxy groups in Robinia pseudoacacia and Nerium indicum. J Agric Food Chem 50:3222–3227
Yamauchi K, Yasuda S, Hamada K, Tsutsumi Y, Fukushima K (2003) Multiform biosynthetic pathway of syringyl lignin in angiosperms. Planta 216:496–501
Acknowledgements
We thank Prof. Umezawa T. and Dr. Nakatsubo T. (Research Institute for Sustainable Humanosphere, Kyoto Uniyersity) for providing the substrates (5-hydroxyfelulic acid, 5-hydoroxyconiferyl aldehyde and 5-hydroxyconiferyl alcohol). This work was supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI Scientific Research (B) Grant Number 26292097 (Y.T.), JSPS KAKENHI Exploratory Research Grant Number 15K14774 (Y.T.) and JSPS KAKENHI Young Scientists (B) Grant Number 15K18724 (J.S.).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Shigeto, J., Ueda, Y., Sasaki, S. et al. Enzymatic activities for lignin monomer intermediates highlight the biosynthetic pathway of syringyl monomers in Robinia pseudoacacia . J Plant Res 130, 203–210 (2017). https://doi.org/10.1007/s10265-016-0882-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-016-0882-4