Skip to main content
SpringerLink
Log in

Increasing Lignin Accumulation in Arabidopsis and Poplar by Overexpressing a CCoAOMT Gene from the Dove Tree (Davidia involucrata Baill.)

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Rapid lignification and high lignin accumulation occur in the endocarps of the dove tree (Davidia involucrata) during a short developmental phase. Through transcriptome analysis, we identified a gene named DiCCoAOMT1 that plays a vital role in the rapid lignification process. The expression profile of the DiCCoAOMT1 gene was endocarp-specific, and its encoding product showed strong O-methyltransferase activity in vitro. Here, we overexpressed the DiCCoAOMT1 gene in both Arabidopsis and poplar (Populus tomentosa) to verify its function of lignin biosynthesis and accumulation. Increased plant height and lengthened pods arose in transgenic Arabidopsis lines, while elongated petioles were observed in transgenic poplar lines. Moreover, the stems exhibited enlarged xylem area, reduced pith area, and more compact cell architecture in both transgenic Arabidopsis and poplar lines. The lignin content was elevated by 26% and 20% on average in the stems of transgenic Arabidopsis and poplar lines, respectively. Furthermore, the lignin composition was altered in the transgenic lines indicated by the elevated S/G ratio. Taken together, we proposed that overexpressing the DiCCoAOMT1 gene can effectively increase lignin biosynthesis and change lignin monomer composition in both herb and woody plants. The endocarp-specific expression pattern of the DiCCoAOMT1 gene is assumed to be a key point to form the highly lignified structure in a short period, thus causing the long-period dormancy of Davidia seeds.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Barney DL, Lopez OA, King E (2007) Micropropagation of cascade huckleberry, mountain huckleberry, and oval-leaf bilberry using woody plant medium and Murashige and Skoog medium formulations. HortTechnology 17:279–284

    Article  CAS  Google Scholar 

  • Chen F, Reddy MSS, Temple S, Jackson L, Dixon RA (2010) Multi-site genetic modulation of monolignol biosynthesis suggests new routes for formation of syringyl lignin and wall-bound ferulic acid in alfalfa (Medicago sativa L.). Plant J Cell Mol Biol 48:113–124

    Article  Google Scholar 

  • Chen L, Wu F, Zhang J (2021) NAC and MYB families and lignin biosynthesis-related members identification and expression analysis in Melilotus albus. Plants 10:303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Dardick C, Callahan AM (2014) Evolution of the fruit endocarp: molecular mechanisms underlying adaptations in seed protection and dispersal strategies. Front Plant Sci 5:1–10

    Article  Google Scholar 

  • Derveaux S, Vandesompele J, Hellemans J (2010) How to do successful gene expression analysis using real-time PCR. Methods 50:227–230

    Article  CAS  PubMed  Google Scholar 

  • Díaz ML, Garbus I, Echenique V (2010) Allele-specific expression of a weeping lovegrass gene from the lignin biosynthetic pathway, caffeoyl-coenzyme A 3-O-methyltransferase. Mol Breed 26:627–637

    Article  Google Scholar 

  • Eom IY, Kim KH, Lee SM, Yi YS, Choi JW (2010) Characterization of chemical composition in poplar wood (Populus deltoides) by suppression of CCoAOMT gene expression. J Korean Wood Sci Technol 38:213–222

    Article  Google Scholar 

  • Fillatti J, Sellmer J, Mccown B, Haissig B, Comai L (1987) Agrobacterium mediated transformation and regeneration of Populus. Mol Gen Genet MGG 206:192–199

    Article  CAS  Google Scholar 

  • Fukushima RS, Hatfield RD (2004) Comparison of the acetyl bromide spectrophotometric method with other analytical lignin methods for determining lignin concentration in forage samples. J Agric Food Chem 52:3713–3720

    Article  CAS  PubMed  Google Scholar 

  • Gui J, Lam PY, Tobimatsu Y, Sun J, Li L (2020) Fiber-specific regulation of lignin biosynthesis improves biomass quality in Populus. New Phytol 226:1074–1087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo D, Chen F, Inoue K, Blount JW, Dixon RA (2001) Downregulation of caffeic acid 3-O-methyltransferase and caffeoyl CoA 3-O-methyltransferase in transgenic alfalfa: impacts on lignin structure and implications for the biosynthesis of G and S lignin. Plant Cell Online 13:73–88

    Article  CAS  Google Scholar 

  • He B, Li Z, Hao X, He Y (2014) A new technique of fast paraffin sectioning in plant tissues. Chin Bull Bot 49:203–208

    Article  CAS  Google Scholar 

  • Jiang XH, She CW, Zhu YH, Liu XM (2014) Cloning and expression analysis of the Lonicera japonica Thunb. chlorogenic acid synthetase gene (LjCCoAOMT1) in rice. Genet Mol Res 13:2166–2176

    Article  CAS  PubMed  Google Scholar 

  • Lapierre C, Pollet B, Rolando C (1995) New insights into the molecular architecture of hardwood lignins by chemical degradative methods. Res Chem Intermed 21:397–412

    Article  CAS  Google Scholar 

  • Li X, Chen W, Zhao Y, Xiang Y, Jiang H, Zhu S, Cheng B (2013) Downregulation of caffeoyl-CoA O-methyltransferase (CCoAOMT) by RNA interference leads to reduced lignin production in maize straw. Genet Mol Biol 36:540–546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li M, Dong X, Peng J, Xu W, Ren R, Liu J, Cao F, Liu Z (2016) De novo transcriptome sequencing and gene expression analysis reveal potential mechanisms of seed abortion in dove tree (Davidia involucrata Baill.). BMC Plant Biol 16:1–21

    Article  Google Scholar 

  • Liu Q, Luo L, Zheng L (2018) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19:335–351

    Article  PubMed  PubMed Central  Google Scholar 

  • Murashige T, Skoog F (2006) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  Google Scholar 

  • Ns A, Fei LA, Ax A, Hz A, Yz A, Ying WA, Xd D, Cw C, Xx A, Zha C (2020) Lignin synthesis mediated by CCoAOMT enzymes is required for the tolerance against excess Cu in Oryza sativa. Environ Exp Bot 175:104059

    Article  Google Scholar 

  • Pang S, Ong SS, Lee HH, Zamri Z, Kandasamy KI, Choong CY, Wickneswari R (2014) Isolation and characterization of CCoAOMT in interspecific hybrid of Acacia auriculiformis x Acacia mangium—a key gene in lignin biosynthesis. Genet Mol Res Gmr 13:7217–7238

    Article  CAS  PubMed  Google Scholar 

  • Qiao Z (2016) Lignification: flexibility, biosynthesis and regulation. Trends Plant Sci 21:713–721

    Article  Google Scholar 

  • Raes J, Rohde A, Christensen JH, Boerjan PW (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Río J, Rencoret J, Gutiérrez A, Kim AH, Ralphbc J (2017) Hydroxystilbenes are monomers in palm fruit endocarp Lignins1[OPEN]. Plant Physiol 174:2072–2082

    Article  Google Scholar 

  • Sakamoto S, Kamimura N, Tokue Y, Nakata MT, Yamamoto M, Hu S, Masai E, Mitsuda N, Kajita S (2020) Identification of enzymatic genes with the potential to reduce biomass recalcitrance through lignin manipulation in Arabidopsis. Biotechnol Biofuels 13:97–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigeto J, Ueda Y, Sasaki S, Fujita K, Tsutsumi Y (2016) Enzymatic activities for lignin monomer intermediates highlight the biosynthetic pathway of syringyl monomers in Robinia pseudoacacia. J Plant Res 130:203–210

    Article  PubMed  Google Scholar 

  • Simon C, Lion C, Huss B, Blervacq AS, Spriet C, Guérardel Y, Biot C, Hawkins S (2017) BLISS: shining a light on lignification in plants. Plant Signal Behav 12:e1359366

    Article  PubMed  PubMed Central  Google Scholar 

  • Song G, Chen Q, Callow P, Mandujano M, Han X, Cuenca B, Bonito G, Medina-Mora C, Fulbright D, Guyer D (2021) Efficient micropropagation of chestnut hybrids (Castanea spp.) using modified woody plant medium and zeatin riboside. Hortic Plant J 7:174–180

    Article  CAS  Google Scholar 

  • Stewart CNJ, Via LE (1993) A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. Biotechniques 14:748–750

    CAS  PubMed  Google Scholar 

  • Teng RM, Wang YX, Li H, Lin SJ, Zhuang J (2021) Effects of shading on lignin biosynthesis in the leaf of tea plant (Camellia sinensis (L.) O. Kuntze). Mol Genet Genomics 296:1–13

    Article  Google Scholar 

  • Walker AM, Sattler SA, Regner M, Jones JP, Ralph J (2016) The structure and catalytic mechanism of sorghum bicolor caffeoyl-CoA O-methyltransferase1. Plant Physiol 172:78–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weng JK, Chapple C (2010) The origin and evolution of lignin biosynthesis. New Phytol 187:273–285

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Yan Z, Dong X, Cao F, Li M (2019) Cloning and characterization of a CCoAOMT gene involved in rapid lignification of endocarp in dove tree (Davidia involucrata Baill.). Biotechnol Biotechnol Equip 32:1398–1406

    Article  Google Scholar 

  • Ye ZH, Zhong R, Morrison WH, Himmelsbach DS (2001) Caffeoyl coenzyme A O-methyltransferase and lignin biosynthesis. Phytochemistry 57:1177–1185

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Hu R, Wang H, Cao Y, He G, Fu C, Zhou G (2013) MlWRKY12, a novel miscanthus transcription factor, participates in pith secondary cell wall formation and promotes flowering. Plant Sci 212:1–9

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Henriques R, Lin S, Niu Q, Chua N (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1:641–646

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Zhang Y, Xu J, Niu X, Qi J, Tao A, Zhang L, Fang P, Lin LH, Su J (2014) The CCoAOMT1 gene from jute (Corchorus capsularis L.) is involved in lignin biosynthesis in Arabidopsis thaliana. Gene 546:398–402

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Ni R, Wang PY, Zhu TT, Sun CJ, Lou HX, Cheng AX (2019) Isolation and functional characterization of two caffeoyl coenzyme A 3- O -methyltransferases from the fern species Polypodiodes amoena. Plant Physiol Biochem 136:169–177

    Article  CAS  PubMed  Google Scholar 

  • Zhao S, Wen J, Wang H, Zhang Z, Li X (2016) Changes in lignin content and activity of related enzymes in the endocarp during the walnut shell development period. Hortic Plant J 2:141–147

    Article  Google Scholar 

  • Zhao D, Luan Y, Shi W, Zhang X, Meng J, Tao J (2021) A Paeonia ostii caffeoyl-CoA O-methyltransferase confers drought stress tolerance by promoting lignin synthesis and ROS scavenging. Plant Sci 303:110765A

    Article  Google Scholar 

  • Zhong R (2000) Essential role of caffeoyl coenzyme A O-methyltransferase in lignin biosynthesis in woody poplar plants. Plant Physiol 124:563–569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by Grants from the Key Research Projects of Hunan Provincial Department of Education (20A521), the Natural Science Foundation of Hunan Province (2021JJ31144), and the Innovation Project of Forestry Science and Technology in Hunan Province (XLK201984).

Author information

Author notes

  1. Jian Li and Xiaomin Ji have contributed equally to this work.

Authors and Affiliations

  1. College of Life Science and Technology, Central South University of Forestry and Technology, Changsha, 410004, China

    Jian Li, Xiaomin Ji, Rongjie Mao & Meng Li

  2. College of Horticulture and Landscape, Hunan Agricultural University, Changsha, 410004, China

    Fuxiang Cao

Authors
  1. Jian Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaomin Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rongjie Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fuxiang Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Meng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ML and FC designed the experimental scheme; RM provided the endocarp materials and transcriptome data of Davidia; JL and XJ performed experiments and data analysis; ML and JL wrote the manuscript. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Meng Li.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest in submitting this manuscript.

Additional information

Handling Editor: Abdul Latif Khan.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 756 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, J., Ji, X., Mao, R. et al. Increasing Lignin Accumulation in Arabidopsis and Poplar by Overexpressing a CCoAOMT Gene from the Dove Tree (Davidia involucrata Baill.). J Plant Growth Regul 42, 4095–4105 (2023). https://doi.org/10.1007/s00344-022-10872-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-022-10872-2

Keywords

Search

Navigation