skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Introducing curcumin biosynthesis in Arabidopsis enhances lignocellulosic biomass processing

Abstract

Lignin is the number one cause of lignocellulosic biomass recalcitrance to industrial enzymatic hydrolysis. By partially replacing the traditional lignin monomers by alternative ones, lignin extractability can be enhanced. To design a lignin that is easier to degrade under alkaline conditions, curcumin (diferuloylmethane) was produced in the model plant Arabidopsis thaliana via simultaneous expression of the turmeric (Curcuma longa) genes DIKETIDE-CoA SYNTHASE (DCS) and CURCUMIN SYNTHASE 2 (CURS2). The transgenic plants produced a plethora of curcumin- and phenylpentanoid-derived compounds with no negative impact on growth. Catalytic hydrogenolysis gave evidence that both curcumin and phenylpentanoids were incorporated into the lignifying cell wall, thereby greatly increasing saccharification efficiency after alkaline pretreatment of the transgenic lines by 14–24% as compared with the wild type. These results reflect that non-native monomers can be synthesized and incorporated into the lignin polymer in plants to enhance their biomass processing efficiency.

Authors:
 [1];  [1]; ORCiD logo [1]; ORCiD logo [1];  [2];  [1];  [2];  [3]; ORCiD logo [3]; ORCiD logo [4];  [4]; ORCiD logo [3];  [2]; ORCiD logo [2]
  1. Ghent Univ. (Belgium); VIB Center for Plant Systems Biology, Ghent (Belgium)
  2. Ghent Univ. (Belgium); VIB Center for Plant Systems Biology, Ghent (Belgium); VIB Metabolomics Core, Ghent (Belgium)
  3. Univ. of Wisconsin, Madison, WI (United States); USDOE Great Lakes Bioenergy Research Center, Madison, WI (United States)
  4. KU Leuven, Heverlee (Belgium)
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1548319
Grant/Contract Number:  
SC0018409
Resource Type:
Accepted Manuscript
Journal Name:
Nature Plants
Additional Journal Information:
Journal Volume: 5; Journal Issue: 2; Journal ID: ISSN 2055-0278
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Oyarce, Paula, De Meester, Barbara, Fonseca, Fernando, de Vries, Lisanne, Goeminne, Geert, Pallidis, Andreas, De Rycke, Riet, Tsuji, Yukiko, Li, Yanding, Van den Bosch, Sander, Sels, Bert, Ralph, John, Vanholme, Ruben, and Boerjan, Wout. Introducing curcumin biosynthesis in Arabidopsis enhances lignocellulosic biomass processing. United States: N. p., 2019. Web. doi:10.1038/s41477-018-0350-3.
Oyarce, Paula, De Meester, Barbara, Fonseca, Fernando, de Vries, Lisanne, Goeminne, Geert, Pallidis, Andreas, De Rycke, Riet, Tsuji, Yukiko, Li, Yanding, Van den Bosch, Sander, Sels, Bert, Ralph, John, Vanholme, Ruben, & Boerjan, Wout. Introducing curcumin biosynthesis in Arabidopsis enhances lignocellulosic biomass processing. United States. doi:10.1038/s41477-018-0350-3.
Oyarce, Paula, De Meester, Barbara, Fonseca, Fernando, de Vries, Lisanne, Goeminne, Geert, Pallidis, Andreas, De Rycke, Riet, Tsuji, Yukiko, Li, Yanding, Van den Bosch, Sander, Sels, Bert, Ralph, John, Vanholme, Ruben, and Boerjan, Wout. Mon . "Introducing curcumin biosynthesis in Arabidopsis enhances lignocellulosic biomass processing". United States. doi:10.1038/s41477-018-0350-3. https://www.osti.gov/servlets/purl/1548319.
@article{osti_1548319,
title = {Introducing curcumin biosynthesis in Arabidopsis enhances lignocellulosic biomass processing},
author = {Oyarce, Paula and De Meester, Barbara and Fonseca, Fernando and de Vries, Lisanne and Goeminne, Geert and Pallidis, Andreas and De Rycke, Riet and Tsuji, Yukiko and Li, Yanding and Van den Bosch, Sander and Sels, Bert and Ralph, John and Vanholme, Ruben and Boerjan, Wout},
abstractNote = {Lignin is the number one cause of lignocellulosic biomass recalcitrance to industrial enzymatic hydrolysis. By partially replacing the traditional lignin monomers by alternative ones, lignin extractability can be enhanced. To design a lignin that is easier to degrade under alkaline conditions, curcumin (diferuloylmethane) was produced in the model plant Arabidopsis thaliana via simultaneous expression of the turmeric (Curcuma longa) genes DIKETIDE-CoA SYNTHASE (DCS) and CURCUMIN SYNTHASE 2 (CURS2). The transgenic plants produced a plethora of curcumin- and phenylpentanoid-derived compounds with no negative impact on growth. Catalytic hydrogenolysis gave evidence that both curcumin and phenylpentanoids were incorporated into the lignifying cell wall, thereby greatly increasing saccharification efficiency after alkaline pretreatment of the transgenic lines by 14–24% as compared with the wild type. These results reflect that non-native monomers can be synthesized and incorporated into the lignin polymer in plants to enhance their biomass processing efficiency.},
doi = {10.1038/s41477-018-0350-3},
journal = {Nature Plants},
number = 2,
volume = 5,
place = {United States},
year = {2019},
month = {1}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 8 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Lignin Biosynthesis
journal, June 2003


Tricin, a Flavonoid Monomer in Monocot Lignification
journal, February 2015


Engineered Lignin in Poplar Biomass Facilitates Cu-Catalyzed Alkaline-Oxidative Pretreatment
journal, January 2018

  • Bhalla, Aditya; Bansal, Namita; Pattathil, Sivakumar
  • ACS Sustainable Chemistry & Engineering, Vol. 6, Issue 3
  • DOI: 10.1021/acssuschemeng.7b02067

Studies on curcumin and curcuminoids: V. Alkaline Degradation of Curcumin
journal, February 1985

  • T�nnesen, Hanne Hjorth; Karlsen, Jan
  • Zeitschrift f�r Lebensmittel-Untersuchung und -Forschung, Vol. 180, Issue 2
  • DOI: 10.1007/BF01042637

Different Routes for Conifer- and Sinapaldehyde and Higher Saccharification upon Deficiency in the Dehydrogenase CAD1
journal, September 2017

  • Van Acker, Rebecca; Déjardin, Annabelle; Desmet, Sandrien
  • Plant Physiology, Vol. 175, Issue 3
  • DOI: 10.1104/pp.17.00834

Studies of curcumin and curcuminoids. XXXVI. The stoichiometry and complexation constants of cyclodextrin complexes as determined by the phase-solubility method and UV–Vis titration
journal, August 2009

  • Singh, Ravinder; Tønnesen, Hanne Hjorth; Vogensen, Stine Byskov
  • Journal of Inclusion Phenomena and Macrocyclic Chemistry, Vol. 66, Issue 3-4
  • DOI: 10.1007/s10847-009-9651-5

A rapid and non-destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana
journal, February 2010


Visualization of plant cell wall lignification using fluorescence-tagged monolignols
journal, August 2013

  • Tobimatsu, Yuki; Wagner, Armin; Donaldson, Lloyd
  • The Plant Journal, Vol. 76, Issue 3
  • DOI: 10.1111/tpj.12299

Alkaline Cleavage of Unsymmetrical β-Diketones. Ring Opening of Acylcylohexanones to Form ε-Acyl Caproic Acids 1
journal, December 1948

  • Hauser, Charles R.; Swamer, Frederic W.; Ringler, Betty I.
  • Journal of the American Chemical Society, Vol. 70, Issue 12
  • DOI: 10.1021/ja01192a016

Reductive lignocellulose fractionation into soluble lignin-derived phenolic monomers and dimers and processable carbohydrate pulps
journal, January 2015

  • Van den Bosch, S.; Schutyser, W.; Vanholme, R.
  • Energy & Environmental Science, Vol. 8, Issue 6
  • DOI: 10.1039/C5EE00204D

Photochemical dimerization of methoxy substituted cinnamic acid methyl esters
journal, March 1992


Synergetic Effects of Alcohol/Water Mixing on the Catalytic Reductive Fractionation of Poplar Wood
journal, October 2016

  • Renders, Tom; Van den Bosch, Sander; Vangeel, Thijs
  • ACS Sustainable Chemistry & Engineering, Vol. 4, Issue 12
  • DOI: 10.1021/acssuschemeng.6b01844

Hydroxycinnamate Conjugates as Potential Monolignol Replacements: In vitro Lignification and Cell Wall Studies with Rosmarinic Acid
journal, February 2012

  • Tobimatsu, Yuki; Elumalai, Sasikumar; Grabber, John H.
  • ChemSusChem, Vol. 5, Issue 4
  • DOI: 10.1002/cssc.201100573

Caffeoyl Shikimate Esterase (CSE) Is an Enzyme in the Lignin Biosynthetic Pathway in Arabidopsis
journal, August 2013


Kinetics of Alkaline Degradation of the Food Pigments Curcumin and Curcuminoids
journal, March 1997


Introduction of chemically labile substructures into Arabidopsis lignin through the use of LigD, the Cα-dehydrogenase from Sphingobium sp. strain SYK-6
journal, January 2015

  • Tsuji, Yukiko; Vanholme, Ruben; Tobimatsu, Yuki
  • Plant Biotechnology Journal, Vol. 13, Issue 6
  • DOI: 10.1111/pbi.12316

Saccharification Protocol for Small-scale Lignocellulosic Biomass Samples to Test Processing of Cellulose into Glucose
journal, January 2016


Systematic Structural Characterization of Metabolites in Arabidopsis via Candidate Substrate-Product Pair Networks
journal, March 2014


Inhibition of the c-Jun N-terminal kinase (JNK) signaling pathway by curcumin
journal, July 1998


Studies on curcumin and curcuminoids
journal, June 2007


Metabolic engineering of novel lignin in biomass crops
journal, October 2012


Mass Spectrometry-Based Fragmentation as an Identification Tool in Lignomics
journal, October 2010

  • Morreel, Kris; Kim, Hoon; Lu, Fachuang
  • Analytical Chemistry, Vol. 82, Issue 19
  • DOI: 10.1021/ac100968g

Self-processing 2A-polyproteins - a system for co-ordinate expression of multiple proteins in transgenic plants
journal, February 1999


Mass Spectrometry-Based Sequencing of Lignin Oligomers
journal, June 2010


AtMetExpress Development: A Phytochemical Atlas of Arabidopsis Development
journal, December 2009

  • Matsuda, Fumio; Hirai, Masami Y.; Sasaki, Eriko
  • Plant Physiology, Vol. 152, Issue 2
  • DOI: 10.1104/pp.109.148031

Lignins: Natural polymers from oxidative coupling of 4-hydroxyphenyl- propanoids
journal, January 2004


Lignin Valorization through Catalytic Lignocellulose Fractionation: A Fundamental Platform for the Future Biorefinery
journal, June 2016


Lignin Valorization: Improving Lignin Processing in the Biorefinery
journal, May 2014

  • Ragauskas, A. J.; Beckham, G. T.; Biddy, M. J.
  • Science, Vol. 344, Issue 6185, p. 1246843-1246843
  • DOI: 10.1126/science.1246843

Chemical Pulping Advantages of Zip-lignin Hybrid Poplar
journal, August 2017


Formic-acid-induced depolymerization of oxidized lignin to aromatics
journal, November 2014

  • Rahimi, Alireza; Ulbrich, Arne; Coon, Joshua J.
  • Nature, Vol. 515, Issue 7526, p. 249-252
  • DOI: 10.1038/nature13867

Vessel-Specific Reintroduction of CINNAMOYL-COA REDUCTASE1 (CCR1) in Dwarfed ccr1 Mutants Restores Vessel and Xylary Fiber Integrity and Increases Biomass
journal, November 2017

  • De Meester, Barbara; de Vries, Lisanne; Özparpucu, Merve
  • Plant Physiology, Vol. 176, Issue 1
  • DOI: 10.1104/pp.17.01462

Synthesis of substituted truxillic acids from p-coumaric and ferulic acid: simulation of photodimerization in plant cell walls
journal, May 1992

  • Morrison, W. Herbert.; Hartley, Roy D.; Himmelsbach, David S.
  • Journal of Agricultural and Food Chemistry, Vol. 40, Issue 5
  • DOI: 10.1021/jf00017a012

Monolignol ferulate conjugates are naturally incorporated into plant lignins
journal, October 2016

  • Karlen, Steven D.; Zhang, Chengcheng; Peck, Matthew L.
  • Science Advances, Vol. 2, Issue 10
  • DOI: 10.1126/sciadv.1600393

Downregulation of Cinnamoyl-Coenzyme A Reductase in Poplar: Multiple-Level Phenotyping Reveals Effects on Cell Wall Polymer Metabolism and Structure
journal, November 2007

  • Leplé, Jean-Charles; Dauwe, Rebecca; Morreel, Kris
  • The Plant Cell, Vol. 19, Issue 11
  • DOI: 10.1105/tpc.107.054148

Identification and characterization of multiple curcumin synthases from the herb Curcuma longa
journal, July 2009


Mutation of the Inducible ARABIDOPSIS THALIANA CYTOCHROME P450 REDUCTASE2 Alters Lignin Composition and Improves Saccharification
journal, October 2014

  • Sundin, Lisa; Vanholme, Ruben; Geerinck, Jan
  • Plant Physiology, Vol. 166, Issue 4
  • DOI: 10.1104/pp.114.245548

A click chemistry strategy for visualization of plant cell wall lignification
journal, January 2014

  • Tobimatsu, Yuki; Wouwer, Dorien Van de; Allen, Eric
  • Chem. Commun., Vol. 50, Issue 82
  • DOI: 10.1039/C4CC04692G

Degradation of lignin β-aryl ether units in Arabidopsis thaliana expressing LigD , LigF and LigG from Sphingomonas paucimobilis SYK-6
journal, November 2016

  • Mnich, Ewelina; Vanholme, Ruben; Oyarce, Paula
  • Plant Biotechnology Journal, Vol. 15, Issue 5
  • DOI: 10.1111/pbi.12655

Plant Cell Biology: The ABC of Monolignol Transport
journal, July 2012


Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998


Lignin biosynthesis perturbations affect secondary cell wall composition and saccharification yield in Arabidopsis thaliana
journal, January 2013

  • Van Acker, Rebecca; Vanholme, Ruben; Storme, Véronique
  • Biotechnology for Biofuels, Vol. 6, Article No. 46
  • DOI: 10.1186/1754-6834-6-46

Improved saccharification and ethanol yield from field-grown transgenic poplar deficient in cinnamoyl-CoA reductase
journal, December 2013

  • Van Acker, R.; Leple, J. -C.; Aerts, D.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 2
  • DOI: 10.1073/pnas.1321673111

Impact of lignin polymer backbone esters on ionic liquid pretreatment of poplar
journal, April 2017


Genetic engineering of Arabidopsis to overproduce disinapoyl esters, potential lignin modification molecules
journal, February 2017


Profiling of Oligolignols Reveals Monolignol Coupling Conditions in Lignifying Poplar Xylem
journal, October 2004


Monolignol Ferulate Transferase Introduces Chemically Labile Linkages into the Lignin Backbone
journal, April 2014


Curcuminoid Biosynthesis by Two Type III Polyketide Synthases in the Herb Curcuma longa
journal, March 2009

  • Katsuyama, Yohei; Kita, Tomoko; Funa, Nobutaka
  • Journal of Biological Chemistry, Vol. 284, Issue 17
  • DOI: 10.1074/jbc.M900070200

Significant Lability of Guaiacylglycerol β-Phenacyl Ether under Alkaline Conditions
journal, October 2007

  • Imai, Aiko; Yokoyama, Tomoya; Matsumoto, Yuji
  • Journal of Agricultural and Food Chemistry, Vol. 55, Issue 22
  • DOI: 10.1021/jf071147d

Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant
journal, March 2014

  • Bonawitz, Nicholas D.; Kim, Jeong Im; Tobimatsu, Yuki
  • Nature, Vol. 509, Issue 7500, p. 376-380
  • DOI: 10.1038/nature13084

Stability of curcumin in buffer solutions and characterization of its degradation products
journal, August 1997

  • Wang, Ying-Jan; Pan, Min-Hsiung; Cheng, Ann-Lii
  • Journal of Pharmaceutical and Biomedical Analysis, Vol. 15, Issue 12
  • DOI: 10.1016/S0731-7085(96)02024-9

Designer lignins: harnessing the plasticity of lignification
journal, February 2016


Formation of substituted truxillic and truxinic acids in plant cell walls—a rationale
journal, July 1993


A rapid and simple method to isolate pure alpha-cellulose
journal, January 2000


Mechanism of the Hydrolytic Cleavage of Carbon—Carbon Bonds. I. Alkaline Hydrolysis of β-Diketones 1
journal, March 1951

  • Pearson, Ralph G.; Mayerle, Evan A.
  • Journal of the American Chemical Society, Vol. 73, Issue 3
  • DOI: 10.1021/ja01147a012

A Systems Biology View of Responses to Lignin Biosynthesis Perturbations in Arabidopsis
journal, September 2012

  • Vanholme, Ruben; Storme, Véronique; Vanholme, Bartel
  • The Plant Cell, Vol. 24, Issue 9
  • DOI: 10.1105/tpc.112.102574

Structural Redesigning Arabidopsis Lignins into Alkali-Soluble Lignins through the Expression of p- Coumaroyl-CoA:Monolignol Transferase PMT
journal, January 2016

  • Sibout, Richard; Le Bris, Philippe; Legée, Frédéric
  • Plant Physiology, Vol. 170, Issue 3
  • DOI: 10.1104/pp.15.01877

    Works referencing / citing this record:

    Pretreatment of sweet sorghum straw and its enzymatic digestion: insight into the structural changes and visualization of hydrolysis process
    journal, November 2019


    Pretreatment of sweet sorghum straw and its enzymatic digestion: insight into the structural changes and visualization of hydrolysis process
    journal, November 2019