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

Mnich, Ewelina; Vanholme, Ruben; Oyarce, Paula; Liu, Sarah; Lu, Fachuang; Goeminne, Geert; Jorgensen, Bodil; Motawie, Mohammed S.; Boerjan, Wout; Ralph, John; Ulvskov, Peter; Moller, Birger L.; Bjarnholt, Nanna; Harholt, Jesper

doi:10.1111/pbi.12655

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

Journal Article · Mon Oct 24 00:00:00 EDT 2016 · Plant Biotechnology Journal

DOI:https://doi.org/10.1111/pbi.12655· OSTI ID:1393489

Mnich, Ewelina ^[1]; Vanholme, Ruben ^[2]; Oyarce, Paula ^[2]; Liu, Sarah ^[3]; Lu, Fachuang ^[3]; Goeminne, Geert ^[4]; Jorgensen, Bodil ^[1]; Motawie, Mohammed S. ^[1]; Boerjan, Wout ^[2]; Ralph, John ^[3]; Ulvskov, Peter ^[1]; Moller, Birger L. ^[5]; Bjarnholt, Nanna ^[1]; Harholt, Jesper ^[5]

Univ. of Copenhagen, Frederiksberg C (Denmark)
Ghent Univ., Ghent (Belgium); VIB, Ghent (Belgium)
Wisconsin Energy Institute, Madison, WI (United States)
VIB, Ghent (Belgium)
Univ. of Copenhagen, Frederiksberg C (Denmark); Carlsberg Research Lab., Copenhagen (Denmark)

Here, lignin is a major polymer in the secondary plant cell wall and composed of hydrophobic interlinked hydroxyphenylpropanoid units. The presence of lignin hampers conversion of plant biomass into biofuels; plants with modified lignin are therefore being investigated for increased digestibility. The bacterium Sphingomonas paucimobilis produces lignin-degrading enzymes including LigD, LigF and LigG involved in cleaving the most abundant lignin interunit linkage, the β-aryl ether bond. In this study, we expressed the LigD, LigF and LigG (LigDFG) genes in Arabidopsis thaliana to introduce postlignification modifications into the lignin structure. The three enzymes were targeted to the secretory pathway. Phenolic metabolite profiling and 2D HSQC NMR of the transgenic lines showed an increase in oxidized guaiacyl and syringyl units without concomitant increase in oxidized β-aryl ether units, showing lignin bond cleavage. Saccharification yield increased significantly in transgenic lines expressing LigDFG, showing the applicability of our approach. Additional new information on substrate specificity of the LigDFG enzymes is also provided.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Wisconsin Energy Institute, Madison, WI (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: FC02-07ER64494

OSTI ID:: 1393489

Journal Information:: Plant Biotechnology Journal, Vol. 15, Issue 5; ISSN 1467-7644

Publisher:: Society for Experimental Biology; Association of Applied BiologyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 24 works

Citation information provided by
Web of Science

References (61)

Lignin Biosynthesis Boerjan, Wout; Ralph, John; Baucher, Marie Annual Review of Plant Biology, Vol. 54, Issue 1, p. 519-546 https://doi.org/10.1146/annurev.arplant.54.031902.134938	journal	June 2003
A DNA Transformation–Competent Arabidopsis Genomic Library in Agrobacterium Lazo, Gerard R.; Stein, Pascal A.; Ludwig, Robert A. Bio/Technology, Vol. 9, Issue 10 https://doi.org/10.1038/nbt1091-963	journal	October 1991
A Group of Sequence-Related Sphingomonad Enzymes Catalyzes Cleavage of β-Aryl Ether Linkages in Lignin β-Guaiacyl and β-Syringyl Ether Dimers Gall, Daniel L.; Ralph, John; Donohue, Timothy J. Environmental Science & Technology, Vol. 48, Issue 20 https://doi.org/10.1021/es503886d	journal	October 2014
Non-degradative dissolution and acetylation of ball-milled plant cell walls: high-resolution solution-state NMR Lu, Fachuang; Ralph, John The Plant Journal, Vol. 35, Issue 4 https://doi.org/10.1046/j.1365-313X.2003.01817.x	journal	August 2003
Towards a carbon-negative sustainable bio-based economy Vanholme, Bartel; Desmet, Tom; Ronsse, Frederik Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00174	journal	January 2013
Plants with genetically encoded autoluminescence Mitiouchkina, Tatiana; Mishin, Alexander S.; Somermeyer, Louisa Gonzalez Nature Biotechnology, Vol. 38, Issue 8 https://doi.org/10.1038/s41587-020-0500-9	journal	April 2020
Specific degradation ofβ-aryl ether linkage in synthetic lignin (dehydrogenative polymerizate) by bacterial enzymes ofSphingomonas paucimobilis SYK-6 produced in recombinantEscherichia coli Sonoki, Tomonori; Iimura, Yosuke; Masai, Eiji Journal of Wood Science, Vol. 48, Issue 5 https://doi.org/10.1007/BF00770705	journal	October 2002
Caffeoyl Shikimate Esterase (CSE) Is an Enzyme in the Lignin Biosynthetic Pathway in Arabidopsis Vanholme, R.; Cesarino, I.; Rataj, K. Science, Vol. 341, Issue 6150 https://doi.org/10.1126/science.1241602	journal	August 2013
Dirigent phenoxy radical coupling advances and challenges Davin, Laurence B.; Lewis, Norman G. Current Opinion in Biotechnology, Vol. 16, Issue 4, p. 398-406 https://doi.org/10.1016/j.copbio.2005.06.010	journal	August 2005
Introduction of chemically labile substructures into Arabidopsis lignin through the use of LigD, the Cα-dehydrogenase from Sphingobium sp. strain SYK-6 Tsuji, Yukiko; Vanholme, Ruben; Tobimatsu, Yuki Plant Biotechnology Journal, Vol. 13, Issue 6 https://doi.org/10.1111/pbi.12316	journal	January 2015
Maintenance Role of a Glutathionyl-Hydroquinone Lyase (PcpF) in Pentachlorophenol Degradation by Sphingobium chlorophenolicum ATCC 39723 Huang, Yan; Xun, Randy; Chen, Guanjun Journal of Bacteriology, Vol. 190, Issue 23 https://doi.org/10.1128/jb.00489-08	journal	September 2008
Structural diversity and transcription of class III peroxidases from Arabidopsis thaliana: 73 peroxidases from Arabidopsis Welinder, Karen G.; Justesen, Annemarie F.; Kjaersgård, Inger V. H. European Journal of Biochemistry, Vol. 269, Issue 24 https://doi.org/10.1046/j.1432-1033.2002.03311.x	journal	December 2002
Sequestration and Transport of Lignin Monomeric Precursors Liu, Chang-Jun; Miao, Yu-Chen; Zhang, Ke-Wei Molecules, Vol. 16, Issue 1 https://doi.org/10.3390/molecules16010710	journal	January 2011
Systematic Structural Characterization of Metabolites in Arabidopsis via Candidate Substrate-Product Pair Networks Morreel, Kris; Saeys, Yvan; Dima, Oana The Plant Cell, Vol. 26, Issue 3 https://doi.org/10.1105/tpc.113.122242	journal	March 2014
Vacuolar localization of the enzymatic synthesis of hydroxycinnamic acid esters of malic acid in protoplasts from Raphanus sativus leaves Strack, Dieter; Sharma, Vinay Physiologia Plantarum, Vol. 65, Issue 1 https://doi.org/10.1111/j.1399-3054.1985.tb02357.x	journal	September 1985
Solution-State NMR of Lignocellulosic Biomass Lu, Fachuang; Ralph, John Journal of Biobased Materials and Bioenergy, Vol. 5, Issue 2 https://doi.org/10.1166/jbmb.2011.1131	journal	June 2011
Chemoselective Metal-Free Aerobic Alcohol Oxidation in Lignin Rahimi, Alireza; Azarpira, Ali; Kim, Hoon Journal of the American Chemical Society, Vol. 135, Issue 17, p. 6415-6418 https://doi.org/10.1021/ja401793n	journal	April 2013
Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant Bonawitz, Nicholas D.; Kim, Jeong Im; Tobimatsu, Yuki Nature, Vol. 509, Issue 7500, p. 376-380 https://doi.org/10.1038/nature13084	journal	March 2014
Lignin biosynthesis perturbations affect secondary cell wall composition and saccharification yield in Arabidopsis thaliana Van Acker, Rebecca; Vanholme, Ruben; Storme, Véronique Biotechnology for Biofuels, Vol. 6, Article No. 46 https://doi.org/10.1186/1754-6834-6-46	journal	January 2013
Immunolocalization of 1- O -sinapoylglucose:malate sinapoyltransferase in Arabidopsis thaliana Hause, Bettina; Meyer, Knut; Viitanen, Paul Planta, Vol. 215, Issue 1 https://doi.org/10.1007/s00425-001-0716-y	journal	May 2002
A Thermostable Xylanase from Clostridium thermocellum Expressed at High Levels in the Apoplast of Transgenic Tobacco Has No Detrimental Effects and Is Easily Purified Herbers, K.; Wilke, I.; Sonnewald, U. Nature Biotechnology, Vol. 13, Issue 1 https://doi.org/10.1038/nbt0195-63	journal	January 1995
Coordinate Expression and Independent Subcellular Targeting of Multiple Proteins from a Single Transgene El Amrani, Abdelhak; Barakate, Abdellah; Askari, Barak M. Plant Physiology, Vol. 135, Issue 1 https://doi.org/10.1104/pp.103.032649	journal	May 2004
Genetic and Biochemical Investigations on Bacterial Catabolic Pathways for Lignin-Derived Aromatic Compounds Masai, Eiji; Katayama, Yoshihiro; Fukuda, Masao Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 1 https://doi.org/10.1271/bbb.60437	journal	January 2007
Mass Spectrometry-Based Sequencing of Lignin Oligomers Morreel, Kris; Dima, Oana; Kim, Hoon Plant Physiology, Vol. 153, Issue 4 https://doi.org/10.1104/pp.110.156489	journal	June 2010
Plant cell wall polymers as precursors for biofuels Pauly, Markus; Keegstra, Kenneth Current Opinion in Plant Biology, Vol. 13, Issue 3 https://doi.org/10.1016/j.pbi.2009.12.009	journal	June 2010
Simultaneous in vivo truncation of pectic side chains Øbro, Jens; Borkhardt, Bernhard; Harholt, Jesper Transgenic Research, Vol. 18, Issue 6 https://doi.org/10.1007/s11248-009-9285-9	journal	June 2009
Polycistronic Viral Vectors de Felipe, P. Current Gene Therapy, Vol. 2, Issue 3 https://doi.org/10.2174/1566523023347742	journal	September 2002
Lignins: Natural polymers from oxidative coupling of 4-hydroxyphenyl- propanoids Ralph, John; Lundquist, Knut; Brunow, Gösta Phytochemistry Reviews, Vol. 3, Issue 1-2, p. 29-60 https://doi.org/10.1023/B:PHYT.0000047809.65444.a4	journal	January 2004
Rhamnogalacturonan I in Solanum tuberosum tubers contains complex arabinogalactan structures Øbro, Jens; Harholt, Jesper; Scheller, Henrik Vibe Phytochemistry, Vol. 65, Issue 10 https://doi.org/10.1016/j.phytochem.2004.05.002	journal	May 2004
S-(4-Nitrophenacyl)glutathione is a specific substrate for glutathione transferase omega 1-1 Board, Philip G.; Coggan, Marjorie; Cappello, Jean Analytical Biochemistry, Vol. 374, Issue 1 https://doi.org/10.1016/j.ab.2007.09.029	journal	March 2008
USER fusion: a rapid and efficient method for simultaneous fusion and cloning of multiple PCR products Geu-Flores, F.; Nour-Eldin, H. H.; Nielsen, M. T. Nucleic Acids Research, Vol. 35, Issue 7 https://doi.org/10.1093/nar/gkm106	journal	March 2007
Whole plant cell wall characterization using solution-state 2D NMR Mansfield, Shawn D.; Kim, Hoon; Lu, Fachuang Nature Protocols, Vol. 7, Issue 9 https://doi.org/10.1038/nprot.2012.064	journal	August 2012
Efficient transformation of Agrobacterium spp. by high voltage electroporation Wen-jun, Shen; Forde, Brian G. Nucleic Acids Research, Vol. 17, Issue 20 https://doi.org/10.1093/nar/17.20.8385	journal	January 1989
Targeting expression of a fungal ferulic acid esterase to the apoplast, endoplasmic reticulum or golgi can disrupt feruloylation of the growing cell wall and increase the biodegradability of tall fescue (Festuca arundinacea) Buanafina, Marcia M. de O.; Langdon, Tim; Hauck, Barbara Plant Biotechnology Journal, Vol. 8, Issue 3 https://doi.org/10.1111/j.1467-7652.2009.00485.x	journal	April 2010
AtMetExpress Development: A Phytochemical Atlas of Arabidopsis Development Matsuda, Fumio; Hirai, Masami Y.; Sasaki, Eriko Plant Physiology, Vol. 152, Issue 2 https://doi.org/10.1104/pp.109.148031	journal	December 2009
pGD vectors: versatile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves: DsRed and GFP vectors for co-expression in plants Goodin, Michael M.; Dietzgen, Ralf G.; Schichnes, Denise The Plant Journal, Vol. 31, Issue 3 https://doi.org/10.1046/j.1365-313X.2002.01360.x	journal	August 2002
Improvement of biomass through lignin modification Li, Xu; Weng, Jing-Ke; Chapple, Clint The Plant Journal, Vol. 54, Issue 4 https://doi.org/10.1111/j.1365-313X.2008.03457.x	journal	May 2008
Towards engineering glucosinolates into non-cruciferous plants Geu-Flores, Fernando; Olsen, Carl Erik; Halkier, Barbara Ann Planta, Vol. 229, Issue 2 https://doi.org/10.1007/s00425-008-0825-y	journal	October 2008
Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily Dixon, David P.; Hawkins, Timothy; Hussey, Patrick J. Journal of Experimental Botany, Vol. 60, Issue 4 https://doi.org/10.1093/jxb/ern365	journal	January 2009
Small Glycosylated Lignin Oligomers Are Stored in Arabidopsis Leaf Vacuoles Dima, Oana; Morreel, Kris; Vanholme, Bartel The Plant Cell, Vol. 27, Issue 3 https://doi.org/10.1105/tpc.114.134643	journal	February 2015
Roles of the Enantioselective Glutathione S-Transferases in Cleavage of -Aryl Ether Masai, E.; Ichimura, A.; Sato, Y. Journal of Bacteriology, Vol. 185, Issue 6 https://doi.org/10.1128/JB.185.6.1768-1775.2003	journal	March 2003
Phenylcoumaran Benzylic Ether Reductase Prevents Accumulation of Compounds Formed under Oxidative Conditions in Poplar Xylem Niculaes, C.; Morreel, K.; Kim, H. The Plant Cell, Vol. 26, Issue 9 https://doi.org/10.1105/tpc.114.125260	journal	September 2014
Lignin engineering Vanholme, R.; Morreel, K.; Ralph, J. Current Opinion in Plant Biology, Vol. 11, Issue 3, p. 278-285 https://doi.org/10.1016/j.pbi.2008.03.005	journal	June 2008
Ratiometric Fluorescence-Imaging Assays of Plant Membrane Traffic Using Polyproteins Samalova, Marketa; Fricker, Mark; Moore, Ian Traffic, Vol. 7, Issue 12 https://doi.org/10.1111/j.1600-0854.2006.00502.x	journal	November 2006
Unique aspects of the grass cell wall Vogel, J. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.03.002	journal	June 2008
Sphingobium sp. SYK-6 LigG involved in lignin degradation is structurally and biochemically related to the glutathione transferase omega class Meux, Edgar; Prosper, Pascalita; Masai, Eiji FEBS Letters, Vol. 586, Issue 22 https://doi.org/10.1016/j.febslet.2012.09.036	journal	October 2012
Roles for Stress-inducible Lambda Glutathione Transferases in Flavonoid Metabolism in Plants as Identified by Ligand Fishing Dixon, David P.; Edwards, Robert Journal of Biological Chemistry, Vol. 285, Issue 47 https://doi.org/10.1074/jbc.m110.164806	journal	September 2010
The origin and evolution of lignin biosynthesis: Tansley review Weng, Jing-Ke; Chapple, Clint New Phytologist, Vol. 187, Issue 2 https://doi.org/10.1111/j.1469-8137.2010.03327.x	journal	June 2010
Unexpected variation in lignin Sederoff, Ronald R.; MacKay, John J.; Ralph, John Current Opinion in Plant Biology, Vol. 2, Issue 2 https://doi.org/10.1016/s1369-5266(99)80029-6	journal	April 1999
Signal Peptide of Potato PinII Enhances the Expression of Cry1Ac in Transgenic Tobacco Liu, Yun-Jun; Yuan, Yuan; Zheng, Jun Acta Biochimica et Biophysica Sinica, Vol. 36, Issue 8 https://doi.org/10.1093/abbs/36.8.553	journal	August 2004
Enzymatic "Combustion": The Microbial Degradation of Lignin Kirk, T. K.; Farrell, R. L. Annual Review of Microbiology, Vol. 41, Issue 1, p. 465-501 https://doi.org/10.1146/annurev.mi.41.100187.002341	journal	October 1987
The functions of inter- and intracellular glutathione transport systems in plants Foyer, Christine H.; Theodoulou, Frederica L.; Delrot, Serge Trends in Plant Science, Vol. 6, Issue 10 https://doi.org/10.1016/s1360-1385(01)02086-6	journal	October 2001
Identification of Three Alcohol Dehydrogenase Genes Involved in the Stereospecific Catabolism of Arylglycerol- -Aryl Ether by Sphingobium sp. Strain SYK-6 Sato, Y.; Moriuchi, H.; Hishiyama, S. Applied and Environmental Microbiology, Vol. 75, Issue 16 https://doi.org/10.1128/AEM.00880-09	journal	June 2009
The Genetics of Lignin Biosynthesis: Connecting Genotype to Phenotype Bonawitz, Nicholas D.; Chapple, Clint Annual Review of Genetics, Vol. 44, Issue 1, p. 337-363 https://doi.org/10.1146/annurev-genet-102209-163508	journal	December 2010
Metabolic engineering of novel lignin in biomass crops Vanholme, Ruben; Morreel, Kris; Darrah, Chiarina New Phytologist, Vol. 196, Issue 4 https://doi.org/10.1111/j.1469-8137.2012.04337.x	journal	October 2012
Stereochemical Features of Glutathione-dependent Enzymes in the Sphingobium sp. Strain SYK-6 β-Aryl Etherase Pathway Gall, Daniel L.; Kim, Hoon; Lu, Fachuang Journal of Biological Chemistry, Vol. 289, Issue 12 https://doi.org/10.1074/jbc.M113.536250	journal	February 2014
Autohydrolysis of plant xylans by apoplastic expression of thermophilic bacterial endo-xylanases Borkhardt, Bernhard; Harholt, Jesper; Ulvskov, Peter Plant Biotechnology Journal, Vol. 8, Issue 3 https://doi.org/10.1111/j.1467-7652.2010.00506.x	journal	April 2010
The still mysterious roles of cysteine-containing glutathione transferases in plants Lallement, Pierre-Alexandre; Brouwer, Bastiaan; Keech, Olivier Frontiers in Pharmacology, Vol. 5 https://doi.org/10.3389/fphar.2014.00192	journal	August 2014
Structural and enzymatic insights into Lambda glutathione transferases from Populus trichocarpa, monomeric enzymes constituting an early divergent class specific to terrestrial plants Lallement, Pierre-Alexandre; Meux, Edgar; Gualberto, José M. Biochemical Journal, Vol. 462, Issue 1 https://doi.org/10.1042/bj20140390	journal	July 2014
Characterisation of Acidic and Basic Apoplastic Peroxidases from Needles of Norway Spruce (Picea abies, L., Karsten) with Respect to Lignifying Substrates Otter, T.; Polle, A. Plant and Cell Physiology, Vol. 38, Issue 5 https://doi.org/10.1093/oxfordjournals.pcp.a029209	journal	January 1997
Two barley alpha-amylase gene families are regulated differently in aleurone cells. Rogers, J. C. Journal of Biological Chemistry, Vol. 260, Issue 6 https://doi.org/10.1016/S0021-9258(19)83685-2	journal	March 1985

Cited By (5)

Emerging tools, enabling technologies, and future opportunities for the bioproduction of aromatic chemicals: Emerging tools, enabling technologies, and future opportunities Machas, Michael; Kurgan, Gavin; Jha, Amit K. Journal of Chemical Technology & Biotechnology, Vol. 94, Issue 1 https://doi.org/10.1002/jctb.5762	journal	August 2018
Introducing curcumin biosynthesis in Arabidopsis enhances lignocellulosic biomass processing Oyarce, Paula; De Meester, Barbara; Fonseca, Fernando Nature Plants, Vol. 5, Issue 2 https://doi.org/10.1038/s41477-018-0350-3	journal	January 2019
Phenolic cross-links: building and de-constructing the plant cell wall Mnich, Ewelina; Bjarnholt, Nanna; Eudes, Aymerick Natural Product Reports https://doi.org/10.1039/c9np00028c	journal	January 2020
RNAi-suppression of barley caffeic acid O -methyltransferase modifies lignin despite redundancy in the gene family Daly, Paul; McClellan, Christopher; Maluk, Marta Plant Biotechnology Journal, Vol. 17, Issue 3 https://doi.org/10.1111/pbi.13001	journal	October 2018
Biodegradation of lignin by Pseudomonas sp. Q18 and the characterization of a novel bacterial DyP-type peroxidase Yang, Chenxian; Yue, Fangfang; Cui, Yanlong Journal of Industrial Microbiology & Biotechnology, Vol. 45, Issue 10 https://doi.org/10.1007/s10295-018-2064-y	journal	July 2018

Similar Records

Catalytic Mechanism of Aryl-Ether Bond Cleavage in Lignin by LigF and LigG

Journal Article · Tue Nov 05 00:00:00 EST 2019 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1393489

Prates, Erica Teixeira; Crowley, Michael F.; Skaf, Munir S.; +1 more

Structural and Biochemical Characterization of the Early and Late Enzymes in the Lignin β-Aryl Ether Cleavage Pathway from Sphingobium sp. SYK-6

Journal Article · Thu Mar 03 00:00:00 EST 2016 · Journal of Biological Chemistry · OSTI ID:1393489

Pereira, Jose Henrique; Heins, Richard A.; Gall, Daniel L.; +9 more

Stereochemical Features of Glutathione-dependent Enzymes in the Sphingobium sp. Strain SYK-6 β-Aryl Etherase Pathway

Journal Article · Fri Feb 07 00:00:00 EST 2014 · Journal of Biological Chemistry · OSTI ID:1393489

Gall, Daniel L.; Kim, Hoon; Lu, Fachuang; +3 more

Related Subjects

60 APPLIED LIFE SCIENCES
59 BASIC BIOLOGICAL SCIENCES
biofuel
lignin modification
bacteria
Sphingomonas paucimobilis
Ligβ-aryl ether
saccharification yield

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

Citation Formats

References (61)

Cited By (5)

Similar Records

Related Subjects