Structural features of alternative lignin monomers associated with improved digestibility of artificially lignified maize cell walls

Grabber, John H.; Davidson, Christy; Tobimatsu, Yuki; Kim, Hoon; Lu, Fachuang; Zhu, Yimin; Opietnik, Martina; Santoro, Nicholas; Foster, Cliff E.; Yue, Fengxia; Ress, Dino; Pan, Xuejun; Ralph, John

doi:10.1016/j.plantsci.2019.02.004

Title: Structural features of alternative lignin monomers associated with improved digestibility of artificially lignified maize cell walls

Full Record
Other Related Research

Abstract

Plant biologists are seeking new approaches for modifying lignin to improve the digestion and utilization of structural polysaccharides in crop cultivars for the production of biofuels, biochemicals, and livestock. To identify promising targets for lignin bioengineering, we artificially lignified maize (Zea mays L.) cell walls with normal monolignols plus 21 structurally diverse alternative monomers to assess their suitability for lignification and for improving fiber digestibility. Lignin formation and structure were assessed by mass balance, Klason lignin, acetyl bromide lignin, gel-state 2D-NMR and thioacidolysis procedures, and digestibility was evaluated with rumen microflora and from glucose production by fungal enzymes following mild acid or base pretreatments. Highly acidic or hydrophilic monomers proved unsuitable for lignin modification because they severely depressed cell wall lignification. By contrast, monomers designed to moderately alter hydrophobicity or introduce cleavable acetal, amide, or ester functionalities into the polymer often readily formed lignin, but most failed to improve digestibility, even after chemical pretreatment. Fortunately, several types of phenylpropanoid derivatives containing multiple ester-linked catechol or pyrogallol units were identified as desirable genetic engineering targets because they readily formed wall-bound polymers and improved digestibility, presumably by blocking cross-linking of lignin to structural polysaccharides and promoting lignin fragmentation during mild acidic andmore » especially alkaline pretreatment.« less

Authors:

^[1];

^[2];

^[2]; Kim, Hoon ^[2]; Lu, Fachuang ^[2]; Zhu, Yimin ^[2]; Opietnik, Martina ^[2]; Santoro, Nicholas ^[3];

^[3]; Yue, Fengxia ^[2]; Ress, Dino ^[4];

^[5];

^[4]

US Dept. of Agriculture (USDA), Madison, WI (United States). Agricultural Research Service (ARS)
Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry, and D.O.E. Great Lakes Bioenergy Research Center, Wisconsin Energy Inst.
Michigan State Univ., East Lansing, MI (United States). D.O.E. Great Lakes Bioenergy Research Center
Department of Biochemistry, and D.O.E. Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin, Madison, WI, USA
Department of Biological Systems Engineering, University of Wisconsin, Madison, WI, USA

Publication Date:: 2019-03-13

Research Org.:: Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center

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

OSTI Identifier:: 1546966

Grant/Contract Number:: SC0018409

Resource Type:: Accepted Manuscript

Journal Name:: Plant Science

Additional Journal Information:: Journal Volume: 287; Journal ID: ISSN 0168-9452

Publisher:: Elsevier

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Lignocellulosic biomass; Forage; Plant biotechnology; Ruminal fermentation; Enzymatic saccharification

Citation Formats


                    Grabber, John H., Davidson, Christy, Tobimatsu, Yuki, Kim, Hoon, Lu, Fachuang, Zhu, Yimin, Opietnik, Martina, Santoro, Nicholas, Foster, Cliff E., Yue, Fengxia, Ress, Dino, Pan, Xuejun, and Ralph, John. Structural features of alternative lignin monomers associated with improved digestibility of artificially lignified maize cell walls.  United States: N. p., 2019. 
Web.  doi:10.1016/j.plantsci.2019.02.004.

Copy to clipboard


                    Grabber, John H., Davidson, Christy, Tobimatsu, Yuki, Kim, Hoon, Lu, Fachuang, Zhu, Yimin, Opietnik, Martina, Santoro, Nicholas, Foster, Cliff E., Yue, Fengxia, Ress, Dino, Pan, Xuejun, & Ralph, John. Structural features of alternative lignin monomers associated with improved digestibility of artificially lignified maize cell walls.  United States.  https://doi.org/10.1016/j.plantsci.2019.02.004

Copy to clipboard


                    Grabber, John H., Davidson, Christy, Tobimatsu, Yuki, Kim, Hoon, Lu, Fachuang, Zhu, Yimin, Opietnik, Martina, Santoro, Nicholas, Foster, Cliff E., Yue, Fengxia, Ress, Dino, Pan, Xuejun, and Ralph, John. Wed .  
"Structural features of alternative lignin monomers associated with improved digestibility of artificially lignified maize cell walls".  United States.  https://doi.org/10.1016/j.plantsci.2019.02.004.  https://www.osti.gov/servlets/purl/1546966.

Copy to clipboard


                    
@article{osti_1546966,

  title        = {Structural features of alternative lignin monomers associated with improved digestibility of artificially lignified maize cell walls},

  author       = {Grabber, John H. and Davidson, Christy and Tobimatsu, Yuki and Kim, Hoon and Lu, Fachuang and Zhu, Yimin and Opietnik, Martina and Santoro, Nicholas and Foster, Cliff E. and Yue, Fengxia and Ress, Dino and Pan, Xuejun and Ralph, John},

  abstractNote = {Plant biologists are seeking new approaches for modifying lignin to improve the digestion and utilization of structural polysaccharides in crop cultivars for the production of biofuels, biochemicals, and livestock. To identify promising targets for lignin bioengineering, we artificially lignified maize (Zea mays L.) cell walls with normal monolignols plus 21 structurally diverse alternative monomers to assess their suitability for lignification and for improving fiber digestibility. Lignin formation and structure were assessed by mass balance, Klason lignin, acetyl bromide lignin, gel-state 2D-NMR and thioacidolysis procedures, and digestibility was evaluated with rumen microflora and from glucose production by fungal enzymes following mild acid or base pretreatments. Highly acidic or hydrophilic monomers proved unsuitable for lignin modification because they severely depressed cell wall lignification. By contrast, monomers designed to moderately alter hydrophobicity or introduce cleavable acetal, amide, or ester functionalities into the polymer often readily formed lignin, but most failed to improve digestibility, even after chemical pretreatment. Fortunately, several types of phenylpropanoid derivatives containing multiple ester-linked catechol or pyrogallol units were identified as desirable genetic engineering targets because they readily formed wall-bound polymers and improved digestibility, presumably by blocking cross-linking of lignin to structural polysaccharides and promoting lignin fragmentation during mild acidic and especially alkaline pretreatment.},

  doi          = {10.1016/j.plantsci.2019.02.004},

  journal      = {Plant Science},

  number       = ,

  volume       = 287,

  place        = {United States},

  year         = {2019},

  month        = {3}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Accepted Manuscript (DOE)

Publisher's Version of Record

https://doi.org/10.1016/j.plantsci.2019.02.004

Other availability

Search WorldCat to find libraries that may hold this journal

Citation Metrics:

Cited by: 11 works

Citation information provided by
Web of Science

Save / Share:

Export Metadata

Save to My Library

Similar Records in DOE PAGES and OSTI.GOV collections:

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

Journal Article Yuki, Tobimatsu ; Sasikumar, Elumalai ; Grabber, John H. ; ... - ChemSusChem

The plasticity of lignin biosynthesis should permit the inclusion of new compatible phenolic monomers, such as rosmarinic acid (RA) and analogous catechol derivatives, into cell-wall lignins that are consequently less recalcitrant to biomass processing. In vitro lignin polymerization experiments revealed that RA readily underwent peroxidase-catalyzed copolymerization with monolignols and lignin oligomers to form polymers with new benzodioxane inter-unit linkages. Incorporation of RA permitted extensive depolymerization of synthetic lignins by mild alkaline hydrolysis, presumably by cleavage of ester intra-unit linkages within RA. Copolymerization of RA with monolignols into maize cell walls by in situ peroxidases significantly enhanced alkaline lignin extractability andmore »« less
https://doi.org/10.1002/cssc.201100573
Impact of lignin polymer backbone esters on ionic liquid pretreatment of poplar

Journal Article Kim, Kwang Ho ; Dutta, Tanmoy ; Ralph, John ; ... - Biotechnology for Biofuels

Biomass pretreatment remains an essential step in lignocellulosic biofuel production, largely to facilitate the efficient removal of lignin and increase enzyme accessibility to the polysaccharides. In recent years, there have been significant efforts in planta to reduce lignin content or modify its composition to overcome the inherent recalcitrance that it imposes on lignocellulosic biomass during processing. Here, transgenic poplar lines in which monolignol ferulate conjugates were synthesized during cell wall development to introduce, during lignification, readily cleavable ester linkages into the lignin polymer backbone (i.e., "zip lignin"), along with wild-type (WT) controls, were pretreated with different ionic liquids (ILs). Themore »« less
Cited by 39
https://doi.org/10.1186/s13068-017-0784-2
Suppression of CINNAMOYL-CoA REDUCTASE increases the level of monolignol ferulates incorporated into maize lignins

Journal Article Smith, Rebecca A. ; Cass, Cynthia L. ; Mazaheri, Mona ; ... - Biotechnology for Biofuels

Background.The cell wall polymer lignin provides structural support and rigidity to plant cell walls, and therefore to the plant body. However, the recalcitrance associated with lignin impedes the extraction of polysaccharides from the cell wall to make plant-based biofuels and biomaterials. The cell wall digestibility can be improved by introducing labile ester bonds into the lignin backbone that can be easily broken under mild base treatment at room temperature. The FERULOYL-CoA MONOLIGNOL TRANSFERASE (FMT) enzyme, which may be naturally found in many plants, uses feruloyl-CoA and monolignols to synthesize the ester-linked monolignol ferulate conjugates. A mutation in the first lignin-specificmore »« less
Cited by 28
https://doi.org/10.1186/s13068-017-0793-1
Maize Tricin-Oligolignol Metabolites and their Implications for Monocot Lignification

Journal Article Lan, Wu ; Morreel, Kris ; Lu, Fachuang ; ... - Plant Physiology (Bethesda)

Lignin is an abundant aromatic plant cell wall polymer consisting of phenylpropanoid units in which the aromatic rings display various degrees of methoxylation. Tricin [5,7-dihydroxy-2-(4-hydroxy-3,5-dimethoxyphenyl)-4H-chromen-4-one], a flavone, was recently established as a true monomer in grass lignins. To elucidate the incorporation pathways of tricin into grass lignin, the metabolites of maize (Zea mays) were extracted from lignifying tissues and profiled using the recently developed ‘candidate substrate product pair’ algorithm applied to ultra-high-performance liquid chromatography and Fourier transform-ion cyclotron resonance-mass spectrometry. Twelve tricin-containing products (each with up to eight isomers), including those derived from the various monolignol acetate and p-coumarate conjugates,more »« less
Cited by 58
https://doi.org/10.1104/pp.16.02012

Full Text Available
Overexpression of the rice BAHD acyltransferase AT10 increases xylan-bound p-coumarate and reduces lignin in Sorghum bicolor

Journal Article Tian, Yang ; Lin, Chien-Yuan ; Park, Joon-Hyun ; ... - Biotechnology for Biofuels

Abstract Background The development of bioenergy crops with reduced recalcitrance to enzymatic degradation represents an important challenge to enable the sustainable production of advanced biofuels and bioproducts. Biomass recalcitrance is partly attributed to the complex structure of plant cell walls inside which cellulose microfibrils are protected by a network of hemicellulosic xylan chains that crosslink with each other or with lignin via ferulate (FA) bridges. Overexpression of the rice acyltransferase OsAT10 is an effective bioengineering strategy to lower the amount of FA involved in the formation of cell wall crosslinks and thereby reduce cell wall recalcitrance. The annual crop sorghummore »« less
https://doi.org/10.1186/s13068-021-02068-9

Similar Records