Phenolic cross-links: building and de-constructing the plant cell wall

Mnich, Ewelina; Bjarnholt, Nanna; Eudes, Aymerick; Harholt, Jesper; Holland, Claire; Jørgensen, Bodil; Larsen, Flemming Hofmann; Liu, Ming; Manat, Renil; Meyer, Anne S.; Mikkelsen, Jørn Dalgaard; Motawia, Mohammed Saddik; Muschiol, Jan; Møller, Birger Lindberg; Møller, Svenning Rune; Perzon, Alixander; Petersen, Bent Larsen; Ravn, Jonas Laukkonen; Ulvskov, Peter

doi:10.1039/C9NP00028C

Title: Phenolic cross-links: building and de-constructing the plant cell wall

Abstract

Phenolic cross-links and inter-unit linkages result from the oxidative coupling of hydroxycinnamates leading to lignin assembly and cross-linking with cell wall polysaccharides and extensin proteins.

Authors:

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Department of Plant and Environmental Sciences, University of Copenhagen, Denmark
Joint BioEnergy Institute, Emeryville, USA, Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory
Carlsberg Research Laboratory, Copenhagen, Denmark
Department of Food Science, University of Copenhagen, Denmark
Department of Bioengineering, Technical University of Denmark, Denmark
Department of Plant and Environmental Sciences, University of Copenhagen, Denmark, Carlsberg Research Laboratory, Copenhagen
Novozymes A/S, Bagsværd, Denmark

Publication Date:: 2020-07-22

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:: 1593477

Grant/Contract Number:: AC02-05CH11231

Resource Type:: Publisher's Accepted Manuscript

Journal Name:: Natural Product Reports

Additional Journal Information:: Journal Name: Natural Product Reports Journal Volume: 37 Journal Issue: 7; Journal ID: ISSN 0265-0568

Publisher:: Royal Society of Chemistry (RSC)

Country of Publication:: United Kingdom

Language:: English

Citation Formats


                    Mnich, Ewelina, Bjarnholt, Nanna, Eudes, Aymerick, Harholt, Jesper, Holland, Claire, Jørgensen, Bodil, Larsen, Flemming Hofmann, Liu, Ming, Manat, Renil, Meyer, Anne S., Mikkelsen, Jørn Dalgaard, Motawia, Mohammed Saddik, Muschiol, Jan, Møller, Birger Lindberg, Møller, Svenning Rune, Perzon, Alixander, Petersen, Bent Larsen, Ravn, Jonas Laukkonen, and Ulvskov, Peter. Phenolic cross-links: building and de-constructing the plant cell wall.  United Kingdom: N. p., 2020. 
Web.  doi:10.1039/C9NP00028C.

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                    Mnich, Ewelina, Bjarnholt, Nanna, Eudes, Aymerick, Harholt, Jesper, Holland, Claire, Jørgensen, Bodil, Larsen, Flemming Hofmann, Liu, Ming, Manat, Renil, Meyer, Anne S., Mikkelsen, Jørn Dalgaard, Motawia, Mohammed Saddik, Muschiol, Jan, Møller, Birger Lindberg, Møller, Svenning Rune, Perzon, Alixander, Petersen, Bent Larsen, Ravn, Jonas Laukkonen, & Ulvskov, Peter. Phenolic cross-links: building and de-constructing the plant cell wall.  United Kingdom.  https://doi.org/10.1039/C9NP00028C

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                    Mnich, Ewelina, Bjarnholt, Nanna, Eudes, Aymerick, Harholt, Jesper, Holland, Claire, Jørgensen, Bodil, Larsen, Flemming Hofmann, Liu, Ming, Manat, Renil, Meyer, Anne S., Mikkelsen, Jørn Dalgaard, Motawia, Mohammed Saddik, Muschiol, Jan, Møller, Birger Lindberg, Møller, Svenning Rune, Perzon, Alixander, Petersen, Bent Larsen, Ravn, Jonas Laukkonen, and Ulvskov, Peter. Wed .  
"Phenolic cross-links: building and de-constructing the plant cell wall".  United Kingdom.  https://doi.org/10.1039/C9NP00028C.

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@article{osti_1593477,

  title        = {Phenolic cross-links: building and de-constructing the plant cell wall},

  author       = {Mnich, Ewelina and Bjarnholt, Nanna and Eudes, Aymerick and Harholt, Jesper and Holland, Claire and Jørgensen, Bodil and Larsen, Flemming Hofmann and Liu, Ming and Manat, Renil and Meyer, Anne S. and Mikkelsen, Jørn Dalgaard and Motawia, Mohammed Saddik and Muschiol, Jan and Møller, Birger Lindberg and Møller, Svenning Rune and Perzon, Alixander and Petersen, Bent Larsen and Ravn, Jonas Laukkonen and Ulvskov, Peter},

  abstractNote = {Phenolic cross-links and inter-unit linkages result from the oxidative coupling of hydroxycinnamates leading to lignin assembly and cross-linking with cell wall polysaccharides and extensin proteins.},

  doi          = {10.1039/C9NP00028C},

  journal      = {Natural Product Reports},

  number       = 7,

  volume       = 37,

  place        = {United Kingdom},

  year         = {2020},

  month        = {7}

}

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Glycosylated Polyproline II Rods with Kinks as a Structural Motif in Plant Hydroxyproline-Rich Glycoproteins † journal, March 2001

Properties of fibre boards obtained by activation of the middle lamella lignin of wood fibres with peroxidase and H2O2 before conventional pressing journal, January 1998

Biomimetic engineering of cellulose-based materials journal, July 2007

Lignin as a Possible Factor in Lodging of Cereals journal, October 1930

Laccase application in medium density fibreboard to prepare a bio-composite journal, January 2014

Plant cell wall lignification and monolignol metabolism journal, January 2013

Identification and synthesis of new ferulic acid dehydrodimers present in grass cell walls journal, January 1994

Functional characterization of two acyltransferases from Populus trichocarpa capable of synthesizing benzyl benzoate and salicyl benzoate, potential intermediates in salicinoid phenolic glycoside biosynthesis journal, May 2015

NMR characterization of altered lignins extracted from tobacco plants down-regulated for lignification enzymes cinnamylalcohol dehydrogenase and cinnamoyl-CoA reductase journal, October 1998

p -Coumaroyl-CoA:monolignol transferase (PMT) acts specifically in the lignin biosynthetic pathway in Brachypodium distachyon journal, February 2014

Highly Decorated Lignins in Leaf Tissues of the Canary Island Date Palm Phoenix canariensis journal, September 2017

Constitutive expression of a fungal glucuronoyl esterase in Arabidopsis reveals altered cell wall composition and structure: Transgenic expression of PcGCE in Arabidopsis journal, August 2012

Hydroxyproline O -arabinosyltransferase mutants oppositely alter tip growth in Arabidopsis thaliana and Physcomitrella patens journal, December 2015

New and classic families of secreted fungal heme peroxidases journal, May 2010

Identification and evolution of a plant cell wall specific glycoprotein glycosyl transferase, ExAD journal, March 2017

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

DEWAX Transcription Factor Is Involved in Resistance to Botrytis cinerea in Arabidopsis thaliana and Camelina sativa journal, July 2017

Laccase GhLac1 Modulates Broad-Spectrum Biotic Stress Tolerance via Manipulating Phenylpropanoid Pathway and Jasmonic Acid Synthesis journal, December 2017

Identification of Extensin Protein Associated with Sugar Beet Pectin journal, November 2009

Genome sequence and description of the anaerobic lignin-degrading bacterium Tolumonas lignolytica sp. nov. journal, November 2015

Insights into lignin primary structure and deconstruction from Arabidopsis thaliana COMT (caffeic acid O-methyl transferase) mutant Atomt1 journal, January 2010

p-Hydroxybenzoate groups in the lignin of aspen (populus tremula) journal, January 1955

Elicitor-Induced Spruce Stress Lignin (Structural Similarity to Early Developmental Lignins) journal, July 1995

Characterization of the extracellular γ-glutamyl transpeptidases, GGT1 and GGT2, in Arabidopsis: Apoplastic glutathione degradation in Arabidopsis journal, February 2007

Feruloylation in Grasses: Current and Future Perspectives journal, September 2009

A plant mutase that interconverts UDP-arabinofuranose and UDP-arabinopyranose journal, December 2006

Simultaneously disrupting AtPrx2 , AtPrx25 and AtPrx71 alters lignin content and structure in Arabidopsis stem : Lignin alteration by simultaneous disruption of journal, March 2015

Self-assembly of the plant cell wall requires an extensin scaffold journal, February 2008

Structural and enzymatic insights into Lambda glutathione transferases from Populus trichocarpa, monomeric enzymes constituting an early divergent class specific to terrestrial plants journal, July 2014

Identification and suppression of the p‐ coumaroyl CoA:hydroxycinnamyl alcohol transferase in Zea mays L. journal, May 2014

Decreased Polysaccharide Feruloylation Compromises Plant Cell Wall Integrity and Increases Susceptibility to Necrotrophic Fungal Pathogens journal, May 2016

Biochemical and phenotypical characterization of transgenic tomato plants overexpressing a basic peroxidase journal, August 1999

Structural Identification of Dehydrotriferulic and Dehydrotetraferulic Acids Isolated from Insoluble Maize Bran Fiber journal, August 2006

Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis journal, June 2006

An Arabidopsis Cell Wall Proteoglycan Consists of Pectin and Arabinoxylan Covalently Linked to an Arabinogalactan Protein journal, January 2013

Arabidopsis leucine-rich repeat extensin (LRX) proteins modify cell wall composition and influence plant growth journal, June 2015

Kinetics of Enzyme-Catalyzed Cross-Linking of Feruloylated Arabinan from Sugar Beet journal, November 2011

The Peroxidase Gene Family in Plants: A Phylogenetic Overview journal, October 2003

Investigation of the wetting behaviour of natural lignin - a contribution to the cohesion theory of water transport in plants journal, September 1989

Bacterial catabolism of lignin-derived aromatics: New findings in a recent decade: Update on bacterial lignin catabolism: Bacterial catabolism of lignin-derived aromatics journal, November 2017

Lignin and lignans in plant defence: Insight from expression profiling of cinnamyl alcohol dehydrogenase genes during development and following fungal infection in Populus journal, December 2014

Paving the Way for Lignin Valorisation: Recent Advances in Bioengineering, Biorefining and Catalysis journal, June 2016

Xylan and xylan derivatives - biopolymers with valuable properties, 1. Naturally occurring xylans structures, isolation procedures and properties journal, June 2000

Development and Application of a Methodology to Determine Free Ferulic Acid and Ferulic Acid Ester-Linked to Different Types of Carbohydrates in Cereal Products journal, September 2012

Cytochrome P450 93G1 Is a Flavone Synthase II That Channels Flavanones to the Biosynthesis of Tricin O -Linked Conjugates in Rice journal, May 2014

Glucuronoarabinoxylans from maize kernel cell walls are more complex than those from sorghum kernel cell walls journal, November 2000

Action of diverse peroxidases and laccases on six cell wall-related phenolic compounds journal, November 1999

Pilot-scale production of fiberboards made by laccase oxidized wood fibers: board properties and evidence for cross-linking of lignin journal, November 2002

Hydroxycinnamates in lignification journal, August 2009

Complex Regulation of Prolyl-4-Hydroxylases Impacts Root Hair Expansion journal, May 2015

Di-isodityrosine, a novel tetrametric derivative of tyrosine in plant cell wall proteins: a new potential cross-link journal, April 1996

Diferulic acids in the cell wall may contribute to the suppression of shoot growth in the first phase of salt stress in maize journal, June 2014

A feruloyl transferase involved in the biosynthesis of suberin and suberin-associated wax is required for maturation and sealing properties of potato periderm: FHT function in potato periderm
journal, January 2010

The Structure of Plant Cell Walls: I. The Macromolecular Components of the Walls of Suspension-cultured Sycamore Cells with a Detailed Analysis of the Pectic Polysaccharides
journal, January 1973

Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls
journal, September 2015

Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees
journal, August 1999

Dehydrodimers of Ferulic Acid in Maize Grain Pericarp and Aleurone: Resistance Factors to Fusarium graminearum
journal, June 2003

Bright Side of Lignin Depolymerization: Toward New Platform Chemicals
journal, January 2018

Lignin modification improves fermentable sugar yields for biofuel production
journal, June 2007

Enzyme resistant feruloylated xylooligomer analogues from thermochemically treated corn fiber contain large side chains, ethyl glycosides and novel sites of acetylation
journal, November 2013

Feruloylated Arabinoxylans Are Oxidatively Cross-Linked by Extracellular Maize Peroxidase but Not by Horseradish Peroxidase
journal, September 2009

The Intracellular Localization of the Vanillin Biosynthetic Machinery in Pods of Vanilla planifolia
journal, November 2017

Isolation and structural identification of complex feruloylated heteroxylan side-chains from maize bran
journal, June 2006

On the formation of lignin polysaccharide networks in Norway spruce
journal, March 2015

Maize stem tissues: ferulate deposition in developing internode cell walls
journal, July 2003

The suppression of AtPrx52 affects fibers but not xylem lignification in Arabidopsis by altering the proportion of syringyl units
journal, December 2014

Expression analysis of the Arabidopsis peroxidase multigenic family
journal, May 2004

Reactive oxygen species in cell wall metabolism and development in plants
journal, April 2015

Down-regulation of four putative arabinoxylan feruloyl transferase genes from family PF02458 reduces ester-linked ferulate content in rice cell walls
journal, December 2009

Molecular characterization of two Arabidopsis thaliana glycosyltransferase mutants, rra1 and rra2, which have a reduced residual arabinose content in a polymer tightly associated with the cellulosic wall residue
journal, March 2007

Identification of the pI 4.6 extensin peroxidase from Lycopersicon esculentum using proteomics and reverse-genomics
journal, April 2015

Extensin network formation in Vitis vinifera callus cells is an essential and causal event in rapid and H2O2-induced reduction in primary cell wall hydration
journal, January 2011

Quantification of lignin–carbohydrate linkages with high-resolution NMR spectroscopy
journal, February 2011

Ferulate Cross-Links Limit the Enzymatic Degradation of Synthetically Lignified Primary Walls of Maize
journal, July 1998

Structure of β-D-(1→4′)Xylan Hydrate
journal, July 1971

Active and total microbial communities in forest soil are largely different and highly stratified during decomposition
journal, July 2011

Characterization of a Second Arabidopsis thaliana Prolyl 4-Hydroxylase with Distinct Substrate Specificity
journal, November 2004

Glycosylated Polyproline II Rods with Kinks as a Structural Motif in Plant Hydroxyproline-Rich Glycoproteins ^†
journal, March 2001

Properties of fibre boards obtained by activation of the middle lamella lignin of wood fibres with peroxidase and H2O2 before conventional pressing
journal, January 1998

Biomimetic engineering of cellulose-based materials
journal, July 2007

Lignin as a Possible Factor in Lodging of Cereals
journal, October 1930

Laccase application in medium density fibreboard to prepare a bio-composite
journal, January 2014

Plant cell wall lignification and monolignol metabolism
journal, January 2013

Identification and synthesis of new ferulic acid dehydrodimers present in grass cell walls
journal, January 1994

Functional characterization of two acyltransferases from Populus trichocarpa capable of synthesizing benzyl benzoate and salicyl benzoate, potential intermediates in salicinoid phenolic glycoside biosynthesis
journal, May 2015

NMR characterization of altered lignins extracted from tobacco plants down-regulated for lignification enzymes cinnamylalcohol dehydrogenase and cinnamoyl-CoA reductase
journal, October 1998

p -Coumaroyl-CoA:monolignol transferase (PMT) acts specifically in the lignin biosynthetic pathway in Brachypodium distachyon
journal, February 2014

Highly Decorated Lignins in Leaf Tissues of the Canary Island Date Palm Phoenix canariensis
journal, September 2017

Constitutive expression of a fungal glucuronoyl esterase in Arabidopsis reveals altered cell wall composition and structure: Transgenic expression of PcGCE in Arabidopsis
journal, August 2012

Hydroxyproline O -arabinosyltransferase mutants oppositely alter tip growth in Arabidopsis thaliana and Physcomitrella patens
journal, December 2015

New and classic families of secreted fungal heme peroxidases
journal, May 2010

Identification and evolution of a plant cell wall specific glycoprotein glycosyl transferase, ExAD
journal, March 2017

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

DEWAX Transcription Factor Is Involved in Resistance to Botrytis cinerea in Arabidopsis thaliana and Camelina sativa
journal, July 2017

Laccase GhLac1 Modulates Broad-Spectrum Biotic Stress Tolerance via Manipulating Phenylpropanoid Pathway and Jasmonic Acid Synthesis
journal, December 2017

Identification of Extensin Protein Associated with Sugar Beet Pectin
journal, November 2009

Genome sequence and description of the anaerobic lignin-degrading bacterium Tolumonas lignolytica sp. nov.
journal, November 2015

Insights into lignin primary structure and deconstruction from Arabidopsis thaliana COMT (caffeic acid O-methyl transferase) mutant Atomt1
journal, January 2010

p-Hydroxybenzoate groups in the lignin of aspen (populus tremula)
journal, January 1955

Elicitor-Induced Spruce Stress Lignin (Structural Similarity to Early Developmental Lignins)
journal, July 1995

Characterization of the extracellular γ-glutamyl transpeptidases, GGT1 and GGT2, in Arabidopsis: Apoplastic glutathione degradation in Arabidopsis
journal, February 2007

Feruloylation in Grasses: Current and Future Perspectives
journal, September 2009

A plant mutase that interconverts UDP-arabinofuranose and UDP-arabinopyranose
journal, December 2006

Simultaneously disrupting AtPrx2 , AtPrx25 and AtPrx71 alters lignin content and structure in Arabidopsis stem : Lignin alteration by simultaneous disruption of
journal, March 2015

Self-assembly of the plant cell wall requires an extensin scaffold
journal, February 2008

Structural and enzymatic insights into Lambda glutathione transferases from Populus trichocarpa, monomeric enzymes constituting an early divergent class specific to terrestrial plants
journal, July 2014

Identification and suppression of the p‐ coumaroyl CoA:hydroxycinnamyl alcohol transferase in Zea mays L.
journal, May 2014

Decreased Polysaccharide Feruloylation Compromises Plant Cell Wall Integrity and Increases Susceptibility to Necrotrophic Fungal Pathogens
journal, May 2016

Biochemical and phenotypical characterization of transgenic tomato plants overexpressing a basic peroxidase
journal, August 1999

Structural Identification of Dehydrotriferulic and Dehydrotetraferulic Acids Isolated from Insoluble Maize Bran Fiber
journal, August 2006

Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis
journal, June 2006

An Arabidopsis Cell Wall Proteoglycan Consists of Pectin and Arabinoxylan Covalently Linked to an Arabinogalactan Protein
journal, January 2013

Arabidopsis leucine-rich repeat extensin (LRX) proteins modify cell wall composition and influence plant growth
journal, June 2015

Kinetics of Enzyme-Catalyzed Cross-Linking of Feruloylated Arabinan from Sugar Beet
journal, November 2011

The Peroxidase Gene Family in Plants: A Phylogenetic Overview
journal, October 2003

Investigation of the wetting behaviour of natural lignin - a contribution to the cohesion theory of water transport in plants
journal, September 1989

Bacterial catabolism of lignin-derived aromatics: New findings in a recent decade: Update on bacterial lignin catabolism: Bacterial catabolism of lignin-derived aromatics
journal, November 2017

Lignin and lignans in plant defence: Insight from expression profiling of cinnamyl alcohol dehydrogenase genes during development and following fungal infection in Populus
journal, December 2014

Paving the Way for Lignin Valorisation: Recent Advances in Bioengineering, Biorefining and Catalysis
journal, June 2016

Xylan and xylan derivatives - biopolymers with valuable properties, 1. Naturally occurring xylans structures, isolation procedures and properties
journal, June 2000

Development and Application of a Methodology to Determine Free Ferulic Acid and Ferulic Acid Ester-Linked to Different Types of Carbohydrates in Cereal Products
journal, September 2012

Cytochrome P450 93G1 Is a Flavone Synthase II That Channels Flavanones to the Biosynthesis of Tricin O -Linked Conjugates in Rice
journal, May 2014

Glucuronoarabinoxylans from maize kernel cell walls are more complex than those from sorghum kernel cell walls
journal, November 2000

Action of diverse peroxidases and laccases on six cell wall-related phenolic compounds
journal, November 1999

Pilot-scale production of fiberboards made by laccase oxidized wood fibers: board properties and evidence for cross-linking of lignin
journal, November 2002

Hydroxycinnamates in lignification
journal, August 2009

Complex Regulation of Prolyl-4-Hydroxylases Impacts Root Hair Expansion
journal, May 2015

Di-isodityrosine, a novel tetrametric derivative of tyrosine in plant cell wall proteins: a new potential cross-link
journal, April 1996

Diferulic acids in the cell wall may contribute to the suppression of shoot growth in the first phase of salt stress in maize
journal, June 2014

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

Overexpression of a rice BAHD acyltransferase gene in switchgrass (Panicum virgatum L.) enhances saccharification
journal, September 2018

Precursor-Directed Combinatorial Biosynthesis of Cinnamoyl, Dihydrocinnamoyl, and Benzoyl Anthranilates in Saccharomyces cerevisiae
journal, October 2015