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

Abstract

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.

Authors:

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)

Publication Date:: Mon Oct 24 00:00:00 EDT 2016

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

Sponsoring Org.:: USDOE

OSTI Identifier:: 1393489

Grant/Contract Number:: FC02-07ER64494

Resource Type:: Accepted Manuscript

Journal Name:: Plant Biotechnology Journal

Additional Journal Information:: Journal Volume: 15; Journal Issue: 5; Journal ID: ISSN 1467-7644

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

Country of Publication:: United States

Language:: English

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

Citation Formats


                    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, and Harholt, Jesper. Degradation of lignin β-aryl ether units in Arabidopsis thaliana expressing LigD , LigF and LigG from Sphingomonas paucimobilis SYK-6.  United States: N. p., 2016. 
Web.  doi:10.1111/pbi.12655.

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                    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. Degradation of lignin β-aryl ether units in Arabidopsis thaliana expressing LigD , LigF and LigG from Sphingomonas paucimobilis SYK-6.  United States.  https://doi.org/10.1111/pbi.12655

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                    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, and Harholt, Jesper. Mon .  
"Degradation of lignin β-aryl ether units in Arabidopsis thaliana expressing LigD , LigF and LigG from Sphingomonas paucimobilis SYK-6".  United States.  https://doi.org/10.1111/pbi.12655.  https://www.osti.gov/servlets/purl/1393489.

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@article{osti_1393489,

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

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

  abstractNote = {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.},

  doi          = {10.1111/pbi.12655},

  journal      = {Plant Biotechnology Journal},

  number       = 5,

  volume       = 15,

  place        = {United States},

  year         = {Mon Oct 24 00:00:00 EDT 2016},

  month        = {Mon Oct 24 00:00:00 EDT 2016}

}

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Chemoselective Metal-Free Aerobic Alcohol Oxidation in Lignin
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Rahimi, Alireza; Azarpira, Ali; Kim, Hoon
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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)
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Buanafina, Marcia M. de O.; Langdon, Tim; Hauck, Barbara
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Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily
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Dixon, David P.; Hawkins, Timothy; Hussey, Patrick J.
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Hause, Bettina; Meyer, Knut; Viitanen, Paul
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Wen-jun, Shen; Forde, Brian G.
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Enzymatic "Combustion": The Microbial Degradation of Lignin
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Davin, Laurence B.; Lewis, Norman G.
Current Opinion in Biotechnology, Vol. 16, Issue 4, p. 398-406
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Sphingobium sp. SYK-6 LigG involved in lignin degradation is structurally and biochemically related to the glutathione transferase omega class
journal, October 2012

Meux, Edgar; Prosper, Pascalita; Masai, Eiji
FEBS Letters, Vol. 586, Issue 22
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The Genetics of Lignin Biosynthesis: Connecting Genotype to Phenotype
journal, December 2010

Bonawitz, Nicholas D.; Chapple, Clint
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Works referencing / citing this record:

Emerging tools, enabling technologies, and future opportunities for the bioproduction of aromatic chemicals: Emerging tools, enabling technologies, and future opportunities
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Catalytic Mechanism of Aryl-Ether Bond Cleavage in Lignin by LigF and LigG

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Given the abundance of lignin in nature, multiple enzyme systems have been discovered to cleave the β-O-4 bonds, the most prevalent intermonomer linkage. In particular, stereospecific cleavage of lignin oligomers by glutathione S-transferases (GSTs) has been reported in several sphingomonads. Here in this paper, we apply quantum mechanics/molecular mechanics simulations to study the mechanism of two glutathione-dependent enzymes in the β-aryl ether catabolic pathway of Sphingomonas sp. SYK-6, namely, LigF, a β-etherase, and LigG, a lyase. For LigF, the free-energy landscape supports a SN2 reaction mechanism, with the monoaromatic leaving group being promptly neutralized upon release. Specific interactions with conservedmore »« less
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There has been great progress in the development of technology for the conversion of lignocellulosic biomass to sugars and subsequent fermentation to fuels. However, plant lignin remains an untapped source of materials for production of fuels or high value chemicals. Biological cleavage of lignin has been well characterized in fungi, in which enzymes that create free radical intermediates are used to degrade this material. In contrast, a catabolic pathway for the stereospecific cleavage of β-aryl ether units that are found in lignin has been identified in Sphingobium sp. SYK-6 bacteria. β-Aryl ether units are typically abundant in lignin, corresponding tomore »« less
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Glutathione-dependent enzymes play important protective, repair, or metabolic roles in cells. In particular, enzymes in the glutathione S-transferase (GST) superfamily function in stress responses, defense systems, or xenobiotic detoxification. Here, we identify novel features of bacterial GSTs that cleave -aryl ether bonds typically found in plant lignin. Our data reveal several original features of the reaction cycle of these GSTs, including stereospecific substrate recognition and stereoselective formation of -S-thioether linkages. Products of recombinant GSTs (LigE, LigP, and LigF) are -S-glutathionyl--ketothioethers that are degraded by a -S-thioetherase (LigG). All three Lig GSTs produced the ketone product (-S-glutathionyl- -veratrylethanone) from an achiralmore »« less
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Lignin is a combinatorial polymer comprising monoaromatic units that are linked via covalent bonds. Although lignin is a potential source of valuable aromatic chemicals, its recalcitrance to chemical or biological digestion presents major obstacles to both the production of second-generation biofuels and the generation of valuable coproducts from lignin's monoaromatic units. Degradation of lignin has been relatively well characterized in fungi, but it is less well understood in bacteria. A catabolic pathway for the enzymatic breakdown of aromatic oligomers linked via β-aryl ether bonds typically found in lignin has been reported in the bacterium Sphingobium sp. SYK-6. Here, we presentmore »« less
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In vitro methods for processing lignin and other aromatic compounds

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Enzymes for depolymerizing lignin. The enzymes include dehydrogenases, β-etherases, and glutathione lyases. The dehydrogenases can comprise one or more or LigD, LigO, LigN, and LigL. The β-etherases can comprise one or more of LigE, LigF, LigP, and BaeA. The glutathione lyases can comprise any one or more of LigG and a number of non-stereospecific, optionally recombinant glutathione lyases derived from Sphingobium sp. SYK-6, Novosphingobium aromaticivorans, Escherichia coli, Streptococcus sanguinis, Phanerochaete chrysosporium, and other microorganisms. The enzymes can be combined in compositions and/or used in methods of processing lignin or other aromatic compounds in vitro.
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Title: Degradation of lignin β-aryl ether units in Arabidopsis thaliana expressing LigD , LigF and LigG from Sphingomonas paucimobilis SYK-6

Abstract

Citation Formats

Lignin Biosynthesis journal, June 2003

A DNA Transformation–Competent Arabidopsis Genomic Library in Agrobacterium 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 journal, October 2014

Non-degradative dissolution and acetylation of ball-milled plant cell walls: high-resolution solution-state NMR journal, August 2003

Towards a carbon-negative sustainable bio-based economy journal, January 2013

Plants with genetically encoded autoluminescence 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 journal, October 2002

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

Dirigent phenoxy radical coupling advances and challenges 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 journal, January 2015

Maintenance Role of a Glutathionyl-Hydroquinone Lyase (PcpF) in Pentachlorophenol Degradation by Sphingobium chlorophenolicum ATCC 39723 journal, September 2008

Structural diversity and transcription of class III peroxidases from Arabidopsis thaliana: 73 peroxidases from Arabidopsis journal, December 2002

Sequestration and Transport of Lignin Monomeric Precursors journal, January 2011

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

Vacuolar localization of the enzymatic synthesis of hydroxycinnamic acid esters of malic acid in protoplasts from Raphanus sativus leaves journal, September 1985

Solution-State NMR of Lignocellulosic Biomass journal, June 2011

Chemoselective Metal-Free Aerobic Alcohol Oxidation in Lignin journal, April 2013

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

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

Immunolocalization of 1- O -sinapoylglucose:malate sinapoyltransferase in Arabidopsis thaliana 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 journal, January 1995

Coordinate Expression and Independent Subcellular Targeting of Multiple Proteins from a Single Transgene journal, May 2004

Genetic and Biochemical Investigations on Bacterial Catabolic Pathways for Lignin-Derived Aromatic Compounds journal, January 2007

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

Plant cell wall polymers as precursors for biofuels journal, June 2010

Simultaneous in vivo truncation of pectic side chains journal, June 2009

Polycistronic Viral Vectors journal, September 2002

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

Rhamnogalacturonan I in Solanum tuberosum tubers contains complex arabinogalactan structures journal, May 2004

S-(4-Nitrophenacyl)glutathione is a specific substrate for glutathione transferase omega 1-1 journal, March 2008

USER fusion: a rapid and efficient method for simultaneous fusion and cloning of multiple PCR products journal, March 2007

Whole plant cell wall characterization using solution-state 2D NMR journal, August 2012

Efficient transformation of Agrobacterium spp. by high voltage electroporation 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) journal, April 2010

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

Genetic and Biochemical Investigations on Bacterial Catabolic Pathways for Lignin-Derived Aromatic Compounds journal, January 2007

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 journal, August 2002

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

Improvement of biomass through lignin modification journal, May 2008

Simultaneous in vivo truncation of pectic side chains journal, June 2009

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

Towards engineering glucosinolates into non-cruciferous plants journal, October 2008

Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily journal, January 2009

Small Glycosylated Lignin Oligomers Are Stored in Arabidopsis Leaf Vacuoles journal, February 2015

Roles of the Enantioselective Glutathione S-Transferases in Cleavage of -Aryl Ether journal, March 2003

Phenylcoumaran Benzylic Ether Reductase Prevents Accumulation of Compounds Formed under Oxidative Conditions in Poplar Xylem journal, September 2014

Lignin engineering journal, June 2008

Ratiometric Fluorescence-Imaging Assays of Plant Membrane Traffic Using Polyproteins journal, November 2006

Unique aspects of the grass cell wall journal, June 2008

Lignin Biosynthesis journal, June 2003

A DNA Transformation–Competent Arabidopsis Genomic Library in Agrobacterium journal, October 1991

Sphingobium sp. SYK-6 LigG involved in lignin degradation is structurally and biochemically related to the glutathione transferase omega class journal, October 2012

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

Roles for Stress-inducible Lambda Glutathione Transferases in Flavonoid Metabolism in Plants as Identified by Ligand Fishing journal, September 2010

Phenylcoumaran Benzylic Ether Reductase Prevents Accumulation of Compounds Formed under Oxidative Conditions in Poplar Xylem journal, September 2014

A Group of Sequence-Related Sphingomonad Enzymes Catalyzes Cleavage of β-Aryl Ether Linkages in Lignin β-Guaiacyl and β-Syringyl Ether Dimers journal, October 2014

The origin and evolution of lignin biosynthesis: Tansley review journal, June 2010

Unexpected variation in lignin journal, April 1999

Towards a carbon-negative sustainable bio-based economy journal, January 2013

Signal Peptide of Potato PinII Enhances the Expression of Cry1Ac in Transgenic Tobacco journal, August 2004

Enzymatic "Combustion": The Microbial Degradation of Lignin journal, October 1987

The functions of inter- and intracellular glutathione transport systems in plants journal, October 2001

Sequestration and Transport of Lignin Monomeric Precursors journal, January 2011

Identification of Three Alcohol Dehydrogenase Genes Involved in the Stereospecific Catabolism of Arylglycerol- -Aryl Ether by Sphingobium sp. Strain SYK-6 journal, June 2009

The Genetics of Lignin Biosynthesis: Connecting Genotype to Phenotype journal, December 2010

Small Glycosylated Lignin Oligomers Are Stored in Arabidopsis Leaf Vacuoles journal, February 2015

Lignin engineering journal, June 2008

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

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

Stereochemical Features of Glutathione-dependent Enzymes in the Sphingobium sp. Strain SYK-6 β-Aryl Etherase Pathway journal, February 2014

Rhamnogalacturonan I in Solanum tuberosum tubers contains complex arabinogalactan structures journal, May 2004

Autohydrolysis of plant xylans by apoplastic expression of thermophilic bacterial endo-xylanases journal, April 2010

Ratiometric Fluorescence-Imaging Assays of Plant Membrane Traffic Using Polyproteins journal, November 2006

Autohydrolysis of plant xylans by apoplastic expression of thermophilic bacterial endo-xylanases journal, April 2010

Whole plant cell wall characterization using solution-state 2D NMR journal, August 2012

S-(4-Nitrophenacyl)glutathione is a specific substrate for glutathione transferase omega 1-1 journal, March 2008

Unique aspects of the grass cell wall journal, June 2008

Lignin Biosynthesis
journal, June 2003

A DNA Transformation–Competent Arabidopsis Genomic Library in Agrobacterium
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
journal, October 2014

Non-degradative dissolution and acetylation of ball-milled plant cell walls: high-resolution solution-state NMR
journal, August 2003

Towards a carbon-negative sustainable bio-based economy
journal, January 2013

Plants with genetically encoded autoluminescence
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
journal, October 2002

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

Dirigent phenoxy radical coupling advances and challenges
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
journal, January 2015

Maintenance Role of a Glutathionyl-Hydroquinone Lyase (PcpF) in Pentachlorophenol Degradation by Sphingobium chlorophenolicum ATCC 39723
journal, September 2008

Structural diversity and transcription of class III peroxidases from Arabidopsis thaliana: 73 peroxidases from Arabidopsis
journal, December 2002

Sequestration and Transport of Lignin Monomeric Precursors
journal, January 2011

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

Vacuolar localization of the enzymatic synthesis of hydroxycinnamic acid esters of malic acid in protoplasts from Raphanus sativus leaves
journal, September 1985

Solution-State NMR of Lignocellulosic Biomass
journal, June 2011

Chemoselective Metal-Free Aerobic Alcohol Oxidation in Lignin
journal, April 2013

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

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

Immunolocalization of 1- O -sinapoylglucose:malate sinapoyltransferase in Arabidopsis thaliana
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
journal, January 1995

Coordinate Expression and Independent Subcellular Targeting of Multiple Proteins from a Single Transgene
journal, May 2004

Genetic and Biochemical Investigations on Bacterial Catabolic Pathways for Lignin-Derived Aromatic Compounds
journal, January 2007

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

Plant cell wall polymers as precursors for biofuels
journal, June 2010

Simultaneous in vivo truncation of pectic side chains
journal, June 2009

Polycistronic Viral Vectors
journal, September 2002

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

Rhamnogalacturonan I in Solanum tuberosum tubers contains complex arabinogalactan structures
journal, May 2004

S-(4-Nitrophenacyl)glutathione is a specific substrate for glutathione transferase omega 1-1
journal, March 2008

USER fusion: a rapid and efficient method for simultaneous fusion and cloning of multiple PCR products
journal, March 2007

Whole plant cell wall characterization using solution-state 2D NMR
journal, August 2012

Efficient transformation of Agrobacterium spp. by high voltage electroporation
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)
journal, April 2010

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

Genetic and Biochemical Investigations on Bacterial Catabolic Pathways for Lignin-Derived Aromatic Compounds
journal, January 2007

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
journal, August 2002

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

Improvement of biomass through lignin modification
journal, May 2008

Simultaneous in vivo truncation of pectic side chains
journal, June 2009

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

Towards engineering glucosinolates into non-cruciferous plants
journal, October 2008

Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily
journal, January 2009

Small Glycosylated Lignin Oligomers Are Stored in Arabidopsis Leaf Vacuoles
journal, February 2015

Roles of the Enantioselective Glutathione S-Transferases in Cleavage of -Aryl Ether
journal, March 2003

Phenylcoumaran Benzylic Ether Reductase Prevents Accumulation of Compounds Formed under Oxidative Conditions in Poplar Xylem
journal, September 2014

Lignin engineering
journal, June 2008

Ratiometric Fluorescence-Imaging Assays of Plant Membrane Traffic Using Polyproteins
journal, November 2006

Unique aspects of the grass cell wall
journal, June 2008

Lignin Biosynthesis
journal, June 2003

A DNA Transformation–Competent Arabidopsis Genomic Library in Agrobacterium
journal, October 1991

Sphingobium sp. SYK-6 LigG involved in lignin degradation is structurally and biochemically related to the glutathione transferase omega class
journal, October 2012

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

Roles for Stress-inducible Lambda Glutathione Transferases in Flavonoid Metabolism in Plants as Identified by Ligand Fishing
journal, September 2010

Phenylcoumaran Benzylic Ether Reductase Prevents Accumulation of Compounds Formed under Oxidative Conditions in Poplar Xylem
journal, September 2014

A Group of Sequence-Related Sphingomonad Enzymes Catalyzes Cleavage of β-Aryl Ether Linkages in Lignin β-Guaiacyl and β-Syringyl Ether Dimers
journal, October 2014

The origin and evolution of lignin biosynthesis: Tansley review
journal, June 2010

Unexpected variation in lignin
journal, April 1999

Towards a carbon-negative sustainable bio-based economy
journal, January 2013

Signal Peptide of Potato PinII Enhances the Expression of Cry1Ac in Transgenic Tobacco
journal, August 2004

Enzymatic "Combustion": The Microbial Degradation of Lignin
journal, October 1987

The functions of inter- and intracellular glutathione transport systems in plants
journal, October 2001

Sequestration and Transport of Lignin Monomeric Precursors
journal, January 2011

Identification of Three Alcohol Dehydrogenase Genes Involved in the Stereospecific Catabolism of Arylglycerol- -Aryl Ether by Sphingobium sp. Strain SYK-6
journal, June 2009

The Genetics of Lignin Biosynthesis: Connecting Genotype to Phenotype
journal, December 2010

Small Glycosylated Lignin Oligomers Are Stored in Arabidopsis Leaf Vacuoles
journal, February 2015

Lignin engineering
journal, June 2008

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

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

Stereochemical Features of Glutathione-dependent Enzymes in the Sphingobium sp. Strain SYK-6 β-Aryl Etherase Pathway
journal, February 2014

Rhamnogalacturonan I in Solanum tuberosum tubers contains complex arabinogalactan structures
journal, May 2004

Autohydrolysis of plant xylans by apoplastic expression of thermophilic bacterial endo-xylanases
journal, April 2010

Ratiometric Fluorescence-Imaging Assays of Plant Membrane Traffic Using Polyproteins
journal, November 2006

Autohydrolysis of plant xylans by apoplastic expression of thermophilic bacterial endo-xylanases
journal, April 2010

Whole plant cell wall characterization using solution-state 2D NMR
journal, August 2012

S-(4-Nitrophenacyl)glutathione is a specific substrate for glutathione transferase omega 1-1
journal, March 2008

Unique aspects of the grass cell wall
journal, June 2008

Chemoselective Metal-Free Aerobic Alcohol Oxidation in Lignin
journal, April 2013

The still mysterious roles of cysteine-containing glutathione transferases in plants
journal, August 2014

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)
journal, April 2010