Home Generation of lignin polymer models via dehydrogenative polymerization of coniferyl alcohol and syringyl alcohol via several plant peroxidases involved in lignification and analysis of the resulting DHPs by MALDI-TOF analysis
Article
Licensed
Unlicensed Requires Authentication

Generation of lignin polymer models via dehydrogenative polymerization of coniferyl alcohol and syringyl alcohol via several plant peroxidases involved in lignification and analysis of the resulting DHPs by MALDI-TOF analysis

  • Jun Shigeto , Hiroki Honjo , Koki Fujita and Yuji Tsutsumi EMAIL logo
Published/Copyright: December 2, 2017
Become an author with De Gruyter Brill

Abstract

The mechanism of lignin dehydrogenative polymerization (DHP), made by means of horseradish peroxidase (HRP), was studied in comparison with other plant peroxidases. Interestingly, HRP is efficient for guaiacyl type polymer formation (G-DHPs), but is not efficient in the case of syringyl type DHPs (S-DHPs). It was previously demonstrated that lignification-related Arabidopsisthaliana peroxidases, AtPrx2, AtPrx25 and AtPrx71, and cationic cell-wall-bound peroxidase (CWPO-C) from Populus alba are successful to oxidize syringyl- and guaiacyl-type monomers and larger lignin-like molecules. This is the reason why in the present study the DHP formation by means of these recombinant peroxidases was tested, and all these enzymes were successful for formation of both G-DHP and S-DHP in acceptable yields. CWPO-C led to S-DHP molecular size distribution similar to that of isolated lignins.

Acknowledgments

This work was supported by the Japan Society for the Promotion of Science (JSPS), Funder ID: 10.13039/501100001691. KAKENHI Scientific Research (B) Grant Number JP17H03846 (Y.T.) and JSPS KAKENHI Young Scientists (B) Grant Number JP15K18724 (J.S.) and Scientific Research (C) Grant Number JP17K07878 (J.S.). We thank Edanz Group (www.edanzediting.com/ac) for editing a draft of the manuscript.

  1. Author contributions: Conceived and designed the experiments: JS and YT. Performed the experiments: JS and HH. Analyzed the data: JS, HH, KF and YT. Contributed to the writing of the manuscript: JS and YT. All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: None declared.

  3. Employment or leadership: None declared.

  4. Honorarium: None declared.

References

Ämmälahti, E., Brunow, G. (2000) Use of β-13C labelled coniferyl alcohol to detect “end-wise” polymerization in the formation of DHPs. Holzforschung 54:604–608.10.1515/HF.2000.102Search in Google Scholar

Barceló, A.R., Ros, L.V., Carrasco, A.E. (2007) Looking for syringyl peroxidases. Trends Plant Sci. 12:486–491.10.1016/j.tplants.2007.09.002Search in Google Scholar PubMed

Björkman, A. (1956) Studies on finely divided wood. Part I. Extraction of lignin with neutral solvents. Svensk Papperstidn. 59:477–485.Search in Google Scholar

Cosio, C., Dunand, C. (2009) Specific functions of individual class III peroxidase genes. J. Exp. Bot. 60:391–408.10.1093/jxb/ern318Search in Google Scholar PubMed

Francoz, E., Ranocha, P., Nguyen-Kim, H., Jamet, E., Burlat, V., Dunand, C. (2015) Roles of cell wall peroxidases in plant development. Phytochemistry 112:15–21.10.1016/j.phytochem.2014.07.020Search in Google Scholar PubMed

Freudenberg, K. (1968) The constitution and biosynthesis of lignin. In: Constitution and Biosynthesis of Lignin. Eds. Freudenberg, K. and Neish, A.C. Springer, Berlin, pp. 47–122.10.1007/978-3-642-85981-6_2Search in Google Scholar

Gajhede, M., Schuller, D.J., Henriksen, A., Smith, A.T., Poulos, T.L. (1997) Crystal structure of horseradish peroxidase C at 2.15 A resolution. Nat. Struct. Biol. 4:1032–1038.10.1038/nsb1297-1032Search in Google Scholar PubMed

Holmgren, A., Henriksson, G., Zhang, L. (2008) Effects of a biologically relevant antioxidant on the dehydrogenative polymerization of coniferyl alcohol. Biomacromolecules 9:3378–3382.10.1021/bm800704kSearch in Google Scholar PubMed

Kärkönen, A., Koutaniemi, S., Mustonen, M., Syrjänen, K., Brunow, G., Kilpeläinen, I. (2002) Lignification related enzymes in Picea abies suspension cultures. Physiol. Plant. 114:343–353.10.1034/j.1399-3054.2002.1140303.xSearch in Google Scholar PubMed

Kishimoto, T., Chiba, W., Saito, K., Fukushima, K., Uraki, Y., Ubukata, M. (2010) Influence of syringyl to guaiacyl ratio on the structure of natural and synthetic lignins. J. Agric. Food Chem. 58:895–901.10.1021/jf9035172Search in Google Scholar PubMed

Koutaniemi, S., Malmberg, H.A., Simola, L.K., Teeri, T.H., Kärkönen, A. (2015) Norway spruce (Picea abies) laccases: characterization of a laccase in a lignin-forming tissue culture. J. Integr. Plant Biol. 57:341–348.10.1111/jipb.12333Search in Google Scholar PubMed

Landucci, L.L., Ralph, S.A., Hammel, K.E. (1998) 13C-NMR characterisation of guaiacyl, guaiacyl/syringyl, and syringyl dehydrogenation polymers. Holzforschung 52:160–170.10.1515/hfsg.1998.52.2.160Search in Google Scholar

Li, Q., Koda, K., Yoshinaga, A., Takabe, K., Shimomura, M., Hirai, Y., Tamai, Y., Uraki, Y. (2015) Dehydrogenative polymerization of coniferyl alcohol in artificial polysaccharides matrices: effects of xylan on the polymerization. J. Agric. Food Chem. 63:4613–4620.10.1021/acs.jafc.5b01070Search in Google Scholar

Marjamaa, K., Kukkola, E.M., Fagerstedt, K.V. (2009) The role of xylem class III peroxidases in lignification. J. Exp. Bot. 60:367–376.10.1093/jxb/ern278Search in Google Scholar

Minibayeva, F., Beckett, R.P., Kranner, I. (2015) Roles of apoplastic peroxidases in plant response to wounding. Phytochemistry 112:122–129.10.1016/j.phytochem.2014.06.008Search in Google Scholar

Moon, S.J., Kwon, M., Choi, D., Won, K., Kim, Y.H., Choi, I.G., Choi, J.W. (2012) In vitro analysis of the monolignol coupling mechanism using dehydrogenative polymerization in the presence of peroxidases and controlled feeding ratios of coniferyl and sinapyl alcohol. Phytochemistry 82:15–21.10.1016/j.phytochem.2012.07.006Search in Google Scholar

Øsstergaard, L., Teilum, K., Mirza, O., Mattsson, O., Petersen, M., Welinder, K.G., Mundy, J., Gajhede, M., Henriksen, A. (2000) Arabidopsis ATP A2 peroxidase. Expression and high-resolution structure of a plant peroxidase with implications for lignification. Plant Mol. Biol. 44:231–243.Search in Google Scholar

Ralph, J., Lundquis, K., Brunow, G., Lu, F., Kim, H., Schatz1, P.F., Marita1, J.M., Hatfield1, R.D., Ralph, S.A., Christensen, J.H., Boerjan, W. (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenyl-propanoids. Phytochem. Rev. 3:29–60.10.1023/B:PHYT.0000047809.65444.a4Search in Google Scholar

Ren, L.L., Liu, Y.J., Liu, H.J., Qian, T.T., Qi, L.W., Wang, X.R., Zeng, Q.Y. (2014) Subcellular relocalization and positive selection play key roles in the retention of duplicate genes of Populus class III peroxidase family. Plant Cell 26:2404–2419.10.1105/tpc.114.124750Search in Google Scholar

Sarkanen, K.V. (1971) Precursors and their polymerisation. Chapter 4, 95–163. In: Lignins – Occurence, Formation, Structure and Reactions. Eds. Sarkanen, K.V. and Ludwig, C.H. Wiley-Interscience, New-York, p. 916.Search in Google Scholar

Sarkanen, K.V. and Ludwig, C.H. (Eds). Lignins – Occurence, Formation, Structure and Reactions. Wiley-Interscience, New-York, 1971, p. 916.Search in Google Scholar

Sasaki, S., Nishida, T., Tsutsumi, Y., Kondo, R. (2004) Lignin dehydrogenative polymerization mechanism: a poplar cell wall peroxidase directly oxidizes polymer lignin and produces in vitro dehydrogenative polymer rich in beta-O-4 linkage. FEBS Lett. 562:197–201.10.1016/S0014-5793(04)00224-8Search in Google Scholar

Sasaki, S., Nonaka, D., Wariishi, H., Tsutsumi, Y., Kondo, R. (2008) Role of Tyr residues on the protein surface of cationic cell-wall-peroxidase (CWPO-C) from poplar: potential oxidation sites for oxidative polymerization of lignin. Phytochemistry 69:348–355.10.1016/j.phytochem.2007.08.020Search in Google Scholar PubMed

Schweers, W., Faix, O. (1973) Comparative investigation on lignin polymer models (DHPs) with various composition. Part 1. Preparation of DHPs by means of the monolignols p-coumar alcohol, coniferyl alcohol, and sinapin alcohol (in German). Holzforschung 27:208–213.10.1515/hfsg.1973.27.6.208Search in Google Scholar

Shigeto, J., Tsutsumi, Y. (2016) Divers functions and reactions of class III peroxidases. New Phytol. 209:1395–1402.10.1111/nph.13738Search in Google Scholar

Shigeto, J., Itoh, Y., Tsutsumi, Y., Kondo, R. (2012) Identification of Tyr74 and Tyr177 as substrate oxidation sites in cationic cell wall-bound peroxidase from Populus alba L. FEBS J. 279:348–357.10.1111/j.1742-4658.2011.08429.xSearch in Google Scholar

Shigeto, J., Kiyonaga, Y., Fujita, K., Kondo, R., Tsutsumi, Y. (2013) Putative cationic cell-wall-bound peroxidase homologues in Arabidopsis, AtPrx2, AtPrx25, and AtPrx71, are involved in lignification. J. Agric. Food Chem. 61:3781–3788.10.1021/jf400426gSearch in Google Scholar

Shigeto, J., Nagano, M., Fujita, K., Tsutsumi, Y. (2014) Catalytic profile of Arabidopsis peroxidases, AtPrx-2, 25 and 71, contributing to stem lignification. PLoS One 9:e105332.10.1371/journal.pone.0105332Search in Google Scholar

Shigeto, J., Itoh, Y., Hirao, S., Ohira, K., Fujita, K., Tsutsumi, Y. (2015) Simultaneously disrupting AtPrx2, AtPrx25 and AtPrx71 alters lignin content and structure in Arabidopsis stem. J. Integr. Plant Biol. 57:349–356.10.1111/jipb.12334Search in Google Scholar

Tobimatsu, Y., Takano, T., Kamitakahara, H., Nakatsubo, F. (2010) Reactivity of syringyl quinone methide intermediates in dehydrogenative polymerization. Part 2: pH effect in horseradish peroxidase-catalyzed polymerization of sinapyl alcohol. Holzforschung 64:183–192.10.1515/hf.2010.027Search in Google Scholar

Tognolli, M., Penel, C., Greppin, H., Simon, P. (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288:129–138.10.1016/S0378-1119(02)00465-1Search in Google Scholar

Wariishi, H., Sheng, D.W., Gold, M.H. (1994) Oxidation of ferrocytochrome-C by lignin peroxidase. Biochemistry 33:5545–5552.10.1021/bi00184a025Search in Google Scholar PubMed

Warinowski, T., Koutaniemi, S., Kärkönen, A., Sundberg, I., Toikka, M., Simola, L.K., Kilpeläinen, I., Teeri, T.H. (2016) Peroxidases bound to the growing lignin polymer produce natural like extracellular lignin in a cell culture of Norway spruce. Front. Plant Sci. 7:1523–1533.10.3389/fpls.2016.01523Search in Google Scholar PubMed PubMed Central

Welinder, K.G. (1985) Plant peroxidases. Their primary, secondary and tertiary structures, and relation to cytochrome c peroxidase. Eur. J. Biochem. 151:497–504.Search in Google Scholar

Yoshioka, K., Ando, D., Watanabe, T. (2012) A comparative study of matrix- and nano-assisted laser desorption/ionisation time-of-flight mass spectrometry of isolated and synthetic lignin. Phytochem. Anal. 23:248–253.10.1002/pca.1350Search in Google Scholar PubMed

Zhao, Q., Nakashima, J., Chen, F., Yin, Y., Fu, C., Yun, J., Shao, H., Wang, X., Wang, Z.Y., Dixon, R.A. (2013) Laccase is necessary and non-redundant with peroxidase for lignin polymerization during vascular development in Arabidopsis. Plant Cell 25:3976–3987.10.1105/tpc.113.117770Search in Google Scholar PubMed PubMed Central

Received: 2017-8-3
Accepted: 2017-11-4
Published Online: 2017-12-2
Published in Print: 2018-3-28

©2018 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 27.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/hf-2017-0125/html
Scroll to top button