Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter March 10, 2022

HSQC-NMR analysis of bamboo (Phyllostachys nigra)-cultured cell lignin produced under different phytohormone conditions

Chen Qu, Shinjiro Ogita, Haruo Kawamoto and Takao Kishimoto
From the journal Holzforschung

Abstract

Bamboo-cultured cells (BCCs) were produced under three phytohormone conditions. BCC lignin was then isolated and characterized by heteronuclear single-quantum coherence-nuclear magnetic resonance (HSQC-NMR) analysis. HSQC-NMR analysis revealed that all three BCC lignin samples were composed of guaiacyl (G), syringyl (S), oxidized syringyl (S′), and p-hydroxyphenyl (H) units. p-Coumaric acid (pCA) and ferulic acid (FA) were identified as well. Main lignin substructures, including β-O-4, β-5, and β-β, were also detected. However, β-O-4/α-O-4, spirodienone, dibenzodioxocin, or tricin structures were absent in the BCC lignin. The BCC lignin contained higher proportions of H, FA, and β-5 structures, but less proportions of S, S′, and β-O-4 structures than the mature bamboo lignin. The removal of auxin 2,4-dichlorophenoxyacetic acid (2,4-D) from the subculture medium promoted G unit formations. Nevertheless, it suppressed H and pCA unit formations. Cytokinin 6-benzyladenine (BA) promoted H and β-β structure formations as well but suppressed β-O-4 formations than in the mature bamboo and BCC lignin produced under phytohormone free conditions.


Corresponding authors: Chen Qu, International Advanced Energy Science Research and Education Center, Graduate School of Energy Science, Kyoto University, Yoshida-Honmachi, Kyoto 606-8501, Japan, E-mail: ; and Takao Kishimoto, Department of Biotechnology, Bioorganic Chemistry Laboratory, Faculty of Engineering, Toyama Prefectural University, Imizu 939-0398, Japan, E-mail:

Acknowledgments

The authors thank Mr. Jiaqi Wang (Kyoto University) for kindly providing NMR analysis support.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: None declared.

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Aloni, R., Tollier, M.T., and Monties, B. (1990). The role of auxin and gibberellin in controlling lignin formation in primary phloem fibers and in xylem of Coleus blumei Stems. Plant Physiol. 94: 1743–1747, https://doi.org/10.1104/pp.94.4.1743.Search in Google Scholar

Barcelo, A. R., Gomez, R.L.V., Gabald, C., Lopez-Serrano, M., Pomar, F., Carrion, J.S., and Pedreño, M.A. (2004). Basic peroxidases: the gateway for lignin evolution. Phytochemistry Rev. 3: 61–78, https://doi.org/10.1023/b:phyt.0000047803.49815.1a.10.1023/B:PHYT.0000047803.49815.1aSearch in Google Scholar

Cesarino, I. (2019). Structural features and regulation of lignin deposited upon biotic and abiotic stresses. Curr. Opin. Biotechnol. 56: 209–214, https://doi.org/10.1016/j.copbio.2018.12.012.Search in Google Scholar

Eberhardt, T.L., Bernards, M.A., He, L., Davin, L.B., Wootenll, J.B., and Lewis, N.G. (1993). Lignification in cell suspension cultures of Pinus taeda. J. Biol. Chem. 268: 21088–21096, https://doi.org/10.1016/s0021-9258(19)36897-8.Search in Google Scholar

Fujii, Y., Azuma, J., Marchessault, H.R., Morin, G.F., Aibara, S., and Okamura, K. (1993). Chemical composition change of bamboo accompanying its growth. Holzforschung 46: 109, https://doi.org/10.1515/hfsg.1993.47.2.109.Search in Google Scholar

Fukushima, K. and Terashima, N. (1991a). Heterogeneity in formation of lignin. Part XV: formation and structure of lignin in compression wood of Pinus thunbergii studied by microautoradiography. Wood Sci. Technol. 25: 371–381, https://doi.org/10.1007/bf00226177.Search in Google Scholar

Fukushima, K. and Terashima, N. (1991b). Heterogeneity in formation of lignin. XIV. Formation and structure of lignin in differentiating xylem of Ginkgo bilobu. Holzforschung 45: 87–94, https://doi.org/10.1515/hfsg.1991.45.2.87.Search in Google Scholar

Khadr, A., Wang, Y.-H., Zhang, R.-R., Wang, X.-R., Xu, Z.-S., and Xiong, A.-S. (2020). Cytokinin (6-benzylaminopurine) elevates lignification and the expression of genes involved in lignin biosynthesis of carrot. Protoplasma 257: 1507–1517, https://doi.org/10.1007/s00709-020-01527-8.Search in Google Scholar PubMed

Kim, H. and Ralph, J. (2010). Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6/pyridine-d5. Org. Biomol. Chem. 8: 576–591, https://doi.org/10.1039/b916070a.Search in Google Scholar PubMed PubMed Central

Kim, H., Padmakshan, D., Li, Y., Jorge, R., Roald, H.D., and Ralph, J. (2017). Characterization and elimination of the undesirable protein residues in plant cell wall materials for enhancing lignin analysis by solution-state nuclear magnetic resonance spectroscopy. Biomacromolecules 18: 4184–4195, https://doi.org/10.1021/acs.biomac.7b01223.Search in Google Scholar PubMed

Lan, W., Lu, F., Regner, M., Zhu, Y., Rencoret, J., Ralph, A.S., Zakai, I.U., Morreel, K., Boerjan, W., and Ralph, J. (2015). Tricin, a flavonoid monomer in monocot lignification. Plant Physiol. 127: 1284–1295, https://doi.org/10.1104/pp.114.253757.Search in Google Scholar PubMed PubMed Central

Lange, M.B., Lapierre, C., and Sandermann, H.J. (1995). Elicitor-induced spruce stress lignin (structural similarity to early developmental lignins). Plant Physiol. 108: 1277–1287, https://doi.org/10.1104/pp.108.3.1277.Search in Google Scholar PubMed PubMed Central

Lapierre, C. (2010). Lignin and lignans: advances in chemistry: determining lignin structure by chemical degradations. CRC Press, Boca Raton, FL.Search in Google Scholar

Lundquist, K. (1992). Methods in lignin chemistry: isolation and purification. Springer-Verlag, London.Search in Google Scholar

Ogita, S. (2005). Callus and cell suspension culture of bamboo plant, Phyllostachys nigra. Plant Biotechnol. 22: 119–125, https://doi.org/10.5511/plantbiotechnology.22.119.Search in Google Scholar

Ogita, S., Nomura, T., Kishimoto, T., and Kato, Y. (2012). A novel xylogenic suspension culture model for exploring lignification in phyllostachys bamboo. Plant Methods 8: 40, https://doi.org/10.1186/1746-4811-8-40.Search in Google Scholar PubMed PubMed Central

Ogita, S., Noura, T., Kato, Y., Uehara-Yamaguchi, Y., Inoue, K., Yoshida, T., Sakurai, T., Shinozaki, K., and Mochida, K. (2018). Tanscriptional alterations during proliferation and lignification in Phyllostachys nigra cells. Sci. Rep. 8: 11347, https://doi.org/10.1038/s41598-018-29645-7.Search in Google Scholar PubMed PubMed Central

Pesquet, E., Wagner, A., Grabber, J.H., and Pesquet, E. (2019). Cell culture systems: invaluable tools to investigate lignin formation and cell wall properties. Curr. Opin. Plant Biol. 56: 215–222, https://doi.org/10.1016/j.copbio.2019.02.001.Search in Google Scholar PubMed

Qu, C., Kishimoto, T., Kishino, M., Hamada, M., and Nakajima, N. (2011). Heteronuclear single-quantum coherence nuclear magnetic resonance (HSQC-NMR) characterization of acetylated fir (Abies sachallnensis MAST) wood regenerated from ionic liquid. J. Agric. Food Chem. 59: 5382–5389, https://doi.org/10.1021/jf200498n.Search in Google Scholar PubMed

Qu, C., Kishimoto, T., Ogita, S., Hamada, M., and Nakajima, N. (2012). Dissolution and acetylation of ball-milled birch (Betula platyphylla) and bamboo (Phyllostachys nigra) in the ionic liquid [Bmim]Cl for HSQC-NMR analysis. Holzforschung 66: 607–614, https://doi.org/10.1515/hf.2011.186.Search in Google Scholar

Qu, C., Kishimoto, T., Hamada, M., and Nakajima, N. (2013). Dissolution of ball-milled plant cell walls in ionic liquid systems at room temperature: application to NMR analysis. Holzforschung 67: 25–32, https://doi.org/10.1515/hf-2012-0037.Search in Google Scholar

Qu, C., Ogita, S., and Kishimoto, T. (2020). Characterization of immature bamboo (phyllostachys nigra) component changes with its growth via heteronuclear single-quantum coherence nuclear magnetic resonance spectroscopy. J. Agric. Food Chem. 68: 9896–9905, https://doi.org/10.1021/acs.jafc.0c02258.Search in Google Scholar PubMed

Ralph, J. and Landucci, L.L. (2010). Lignin and lignans: advances in chemistry: NMR of lignins. CRC Press, Boca Raton, FL.Search in Google Scholar

Rencoret, J., Gutierrez, A., Nieto, L., Jimenez-Barbero, J., Faulds, C.B., Kim, H., Ralph, J., Martinez, A.T., and Rio, J.C. (2011). Lignin composition and structure in young versus adult Eucalyptus globules plants. Plant Physiol. 155: 667–628, https://doi.org/10.1104/pp.110.167254.Search in Google Scholar PubMed PubMed Central

Schaller, G.E., Bishopp, A., and Kieber, J.J. (2015). The yin-yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell 27: 44–63, https://doi.org/10.1105/tpc.114.133595.Search in Google Scholar PubMed PubMed Central

Terashima, N., Nakashima, J., and Takabe, K. (1998). Lignin and lignan biosynthesis: proposed structure for protolignin plant cell wall. American Chemical Society, Washington, DC, USA.Search in Google Scholar

Tokunaga, N., Sakakibara, N., Umezawa, T., Ito, Y., Fukuda, H., and Sato, Y. (2005). Involvement of extracellular dilignols in lignification during tracheary element differentiation of isolated zinnia mesophyll cells. Plant Cell Physiol. 46: 224–232, https://doi.org/10.1093/pcp/pci017.Search in Google Scholar PubMed

Vanholme, R., Demedts, B., Morreel, K., Ralph, J., and Boerjan, W. (2010). Lignin biosynthesis and structure. Plant Physiol. 153: 895–905, https://doi.org/10.1104/pp.110.155119.Search in Google Scholar PubMed PubMed Central

Xu, J., Ge, X., and Dolan, M.C. (2011). Towards high-yield production of pharmaceutical proteins with plant cell suspension cultures. Biotechnol. Adv. 21: 278–299, https://doi.org/10.1016/j.biotechadv.2011.01.002.Search in Google Scholar PubMed

Yamamura, M., Wada, S., Sakakibara, N., Nakatsubo, T., Suzuki, S., Hattori, T., Takeda, M., Sakurai, N., Suzuki, H., Shibata, D., et al.. (2011). Occurrence of guaiacyl/p-hydroxyphenyl lignin in Arabidopsis thaliana T87 cells. Plant Biotechnol. 28: 1–8, https://doi.org/10.5511/plantbiotechnology.10.0823c.Search in Google Scholar


Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/hf-2021-0229).


Received: 2021-11-19
Accepted: 2022-02-11
Published Online: 2022-03-10
Published in Print: 2022-06-27

© 2022 Walter de Gruyter GmbH, Berlin/Boston

Scroll Up Arrow