Phenylpropanoid Biosynthesis Gene Expression Precedes Lignin Accumulation During Shoot Development in Lowland and Upland Switchgrass Genotypes

Saha, Prasenjit; Lin, Fan; Thibivilliers, Sandra; Xiong, Yi; Pan, Chongle; Bartley, Laura E.

doi:10.3389/fpls.2021.640930

Title: Phenylpropanoid Biosynthesis Gene Expression Precedes Lignin Accumulation During Shoot Development in Lowland and Upland Switchgrass Genotypes

Abstract

Efficient conversion of lignocellulosic biomass into biofuels is influenced by biomass composition and structure. Lignin and other cell wall phenylpropanoids, such as para -coumaric acid ( p CA) and ferulic acid (FA), reduce cell wall sugar accessibility and hamper biochemical fuel production. Toward identifying the timing and key parameters of cell wall recalcitrance across different switchgrass genotypes, this study measured cell wall composition and lignin biosynthesis gene expression in three switchgrass genotypes, A4 and AP13, representing the lowland ecotype, and VS16, representing the upland ecotype, at three developmental stages [Vegetative 3 (V3), Elongation 4 (E4), and Reproductive 3 (R3)] and three segments (S1–S3) of the E4 stage under greenhouse conditions. A decrease in cell wall digestibility and an increase in phenylpropanoids occur across development. Compared with AP13 and A4, VS16 has significantly less lignin and greater cell wall digestibility at the V3 and E4 stages; however, differences among genotypes diminish by the R3 stage. Gini correlation analysis across all genotypes revealed that lignin and p CA, but also pectin monosaccharide components, show the greatest negative correlations with digestibility. Lignin and p CA accumulation is delayed compared with expression of phenylpropanoid biosynthesis genes, while FA accumulation coincides with expression of thesemore »« less

Authors:: Saha, Prasenjit; Lin, Fan; Thibivilliers, Sandra; Xiong, Yi; Pan, Chongle; Bartley, Laura E.

Publication Date:: Mon Aug 09 00:00:00 EDT 2021

Research Org.:: Univ. of Wisconsin, Madison, WI (United States); Univ. of California, Oakland, CA (United States)

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

OSTI Identifier:: 1812401

Alternate Identifier(s):: OSTI ID: 1849056

Grant/Contract Number:: FC02-07ER64494; AC02-05CH11231; EPS-0814361

Resource Type:: Published Article

Journal Name:: Frontiers in Plant Science

Additional Journal Information:: Journal Name: Frontiers in Plant Science Journal Volume: 12; Journal ID: ISSN 1664-462X

Publisher:: Frontiers Media SA

Country of Publication:: Switzerland

Language:: English

Subject:: 09 BIOMASS FUELS; plant sciences; biomass; cell wall; digestibility; lignin; ferulic acid; switchgrass; vegetative development

Citation Formats


                    Saha, Prasenjit, Lin, Fan, Thibivilliers, Sandra, Xiong, Yi, Pan, Chongle, and Bartley, Laura E. Phenylpropanoid Biosynthesis Gene Expression Precedes Lignin Accumulation During Shoot Development in Lowland and Upland Switchgrass Genotypes.  Switzerland: N. p., 2021. 
Web.  doi:10.3389/fpls.2021.640930.

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                    Saha, Prasenjit, Lin, Fan, Thibivilliers, Sandra, Xiong, Yi, Pan, Chongle, & Bartley, Laura E. Phenylpropanoid Biosynthesis Gene Expression Precedes Lignin Accumulation During Shoot Development in Lowland and Upland Switchgrass Genotypes.  Switzerland.  https://doi.org/10.3389/fpls.2021.640930

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                    Saha, Prasenjit, Lin, Fan, Thibivilliers, Sandra, Xiong, Yi, Pan, Chongle, and Bartley, Laura E. Mon .  
"Phenylpropanoid Biosynthesis Gene Expression Precedes Lignin Accumulation During Shoot Development in Lowland and Upland Switchgrass Genotypes".  Switzerland.  https://doi.org/10.3389/fpls.2021.640930.

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@article{osti_1812401,

  title        = {Phenylpropanoid Biosynthesis Gene Expression Precedes Lignin Accumulation During Shoot Development in Lowland and Upland Switchgrass Genotypes},

  author       = {Saha, Prasenjit and Lin, Fan and Thibivilliers, Sandra and Xiong, Yi and Pan, Chongle and Bartley, Laura E.},

  abstractNote = {Efficient conversion of lignocellulosic biomass into biofuels is influenced by biomass composition and structure. Lignin and other cell wall phenylpropanoids, such as para -coumaric acid ( p CA) and ferulic acid (FA), reduce cell wall sugar accessibility and hamper biochemical fuel production. Toward identifying the timing and key parameters of cell wall recalcitrance across different switchgrass genotypes, this study measured cell wall composition and lignin biosynthesis gene expression in three switchgrass genotypes, A4 and AP13, representing the lowland ecotype, and VS16, representing the upland ecotype, at three developmental stages [Vegetative 3 (V3), Elongation 4 (E4), and Reproductive 3 (R3)] and three segments (S1–S3) of the E4 stage under greenhouse conditions. A decrease in cell wall digestibility and an increase in phenylpropanoids occur across development. Compared with AP13 and A4, VS16 has significantly less lignin and greater cell wall digestibility at the V3 and E4 stages; however, differences among genotypes diminish by the R3 stage. Gini correlation analysis across all genotypes revealed that lignin and p CA, but also pectin monosaccharide components, show the greatest negative correlations with digestibility. Lignin and p CA accumulation is delayed compared with expression of phenylpropanoid biosynthesis genes, while FA accumulation coincides with expression of these genes. The different cell wall component accumulation profiles and gene expression correlations may have implications for system biology approaches to identify additional gene products with cell wall component synthesis and regulation functions.},

  doi          = {10.3389/fpls.2021.640930},

  journal      = {Frontiers in Plant Science},

  number       = ,

  volume       = 12,

  place        = {Switzerland},

  year         = {Mon Aug 09 00:00:00 EDT 2021},

  month        = {Mon Aug 09 00:00:00 EDT 2021}

}

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Title: Phenylpropanoid Biosynthesis Gene Expression Precedes Lignin Accumulation During Shoot Development in Lowland and Upland Switchgrass Genotypes

Abstract

Citation Formats

Lignin Biosynthesis journal, June 2003

Phylogenetic variation in glycosidases and glycanases acting on plant cell wall polysaccharides, and the detection of transglycosidase and trans-β-xylanase activities: Wall-remodelling hydrolases and transglycosylases journal, June 2011

Chemical profiles of switchgrass journal, May 2010

MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms journal, May 2018

Two-year field analysis of reduced recalcitrance transgenic switchgrass journal, April 2014

Molecular Cloning and Expression of a New Class of Ortho-Diphenol-O-Methyltransferases Induced in Tobacco (Nicotiana tabacum L.) Leaves by Infection or Elicitor Treatment journal, October 1993

RNAi-suppression of barley caffeic acid O -methyltransferase modifies lignin despite redundancy in the gene family journal, October 2018

A direct approach to false discovery rates journal, August 2002

Phosphorylation is an on/off switch for 5-hydroxyconiferaldehyde O -methyltransferase activity in poplar monolignol biosynthesis journal, June 2015

Deletion of a gene cluster encoding pectin degrading enzymes in Caldicellulosiruptor bescii reveals an important role for pectin in plant biomass recalcitrance journal, October 2014

CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice journal, January 1994

Determination of the Structure and Catalytic Mechanism of Sorghum bicolor Caffeic Acid O -Methyltransferase and the Structural Impact of Three brown midrib12 Mutations journal, June 2014

Development of feedstocks for cellulosic biofuels journal, May 2012

Latitudinal Adaptation of Switchgrass Populations journal, January 2004

Switchgrass Genomic Diversity, Ploidy, and Evolution: Novel Insights from a Network-Based SNP Discovery Protocol journal, January 2013

Downregulation of p‐ COUMAROYL ESTER 3‐ HYDROXYLASE in rice leads to altered cell wall structures and improves biomass saccharification journal, July 2018

Maize feedstocks with improved digestibility reduce the costs and environmental impacts of biomass pretreatment and saccharification journal, March 2016

Hierarchical classification of switchgrass genotypes using SSR and chloroplast sequences: ecotypes, ploidies, gene pools, and cultivars journal, November 2010

The Switchgrass Genome: Tools and Strategies journal, January 2011

QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient journal, June 2019

Switchgrass (Panicum virgatum) possesses a divergent family of cinnamoyl CoA reductases with distinct biochemical properties journal, September 2009

GenBank journal, December 2011

HMMER web server: 2018 update journal, June 2018

Rapid Assessment of Lignin Content and Structure in Switchgrass (Panicum virgatum L.) Grown Under Different Environmental Conditions journal, October 2009

Net energy of cellulosic ethanol from switchgrass journal, January 2008

A High-Throughput Platform for Screening Milligram Quantities of Plant Biomass for Lignocellulose Digestibility journal, January 2010

A Genomics Approach to Deciphering Lignin Biosynthesis in Switchgrass journal, November 2013

Cell Wall Composition and Candidate Biosynthesis Gene Expression During Rice Development journal, August 2016

Characterization of 5-Hydroxyconiferaldehyde O-Methyltransferase in Oryza sativa journal, January 2013

A Spatial Accommodation by Neighboring Cells Is Required for Organ Initiation in Arabidopsis journal, January 2014

Spatial gradients in cell wall composition and transcriptional profiles along elongating maize internodes journal, January 2014

Switchgrass Growth and Effects on Biomass Accumulation, Moisture Content, and Nutrient Removal journal, January 2017

Simultaneous regulation of F5H in COMT ‐ RNA i transgenic switchgrass alters effects of COMT suppression on syringyl lignin biosynthesis journal, October 2018

Adaptations between Ecotypes and along Environmental Gradients in Panicum virgatum journal, May 2014

Genome-Wide Characterization of the Lignification Toolbox in Arabidopsis journal, November 2003

Functional characterization of the switchgrass (Panicum virgatum) R2R3-MYB transcription factor PvMYB4 for improvement of lignocellulosic feedstocks journal, October 2011

Genetic Diversity of Twelve Switchgrass Populations Using Molecular and Morphological Markers journal, January 2010

Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass journal, February 2011

Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data journal, March 2003

Developmental Control of Lignification in Stems of Lowland Switchgrass Variety Alamo and the Effects on Saccharification Efficiency journal, October 2009

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

Designing the deconstruction of plant cell walls journal, June 2008

Modifying lignin to improve bioenergy feedstocks: strengthening the barrier against pathogens?† journal, January 2013

Chemical composition and response to dilute-acid pretreatment and enzymatic saccharification of alfalfa, reed canarygrass, and switchgrass journal, October 2006

Describing and Quantifying Growth Stages of Perennial Forage Grasses journal, January 1991

Molecular breeding of switchgrass for use as a biofuel crop journal, December 2007

Biomass yield and quality of 20 switchgrass populations in southern Iowa, USA journal, December 2002

Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks journal, November 2003

Overexpression of a BAHD Acyltransferase, OsAt10 , Alters Rice Cell Wall Hydroxycinnamic Acid Content and Saccharification journal, February 2013

Standardization of Switchgrass Sample Collection for Cell Wall and Biomass Trait Analysis journal, January 2013

Application of the Gini Correlation Coefficient to Infer Regulatory Relationships in Transcriptome Analysis journal, July 2012

Comparison of the Acetyl Bromide Spectrophotometric Method with Other Analytical Lignin Methods for Determining Lignin Concentration in Forage Samples journal, June 2004

Sustainable bioenergy production from marginal lands in the US Midwest journal, January 2013

Downregulation of pectin biosynthesis gene GAUT4 leads to reduced ferulate and lignin-carbohydrate cross-linking in switchgrass journal, January 2019

Structural Basis for the Modulation of Lignin Monomer Methylation by Caffeic Acid/5-Hydroxyferulic Acid 3/5- O -Methyltransferase journal, June 2002

Investigating plant cell wall components that affect biomass recalcitrance in poplar and switchgrass journal, January 2013

Phylogenetic, Molecular, and Biochemical Characterization of Caffeic Acid o -Methyltransferase Gene Family in Brachypodium distachyon journal, January 2013

Statistical significance for genomewide studies journal, July 2003

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

Comparison of growth and performance in upland and lowland switchgrass types to water and nitrogen stress journal, January 2003

Comparative transcriptome profiling of upland (VS16) and lowland (AP13) ecotypes of switchgrass journal, November 2016

Lignin Biosynthesis
journal, June 2003

Phylogenetic variation in glycosidases and glycanases acting on plant cell wall polysaccharides, and the detection of transglycosidase and trans-β-xylanase activities: Wall-remodelling hydrolases and transglycosylases
journal, June 2011

Chemical profiles of switchgrass
journal, May 2010

MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms
journal, May 2018

Two-year field analysis of reduced recalcitrance transgenic switchgrass
journal, April 2014

Molecular Cloning and Expression of a New Class of Ortho-Diphenol-O-Methyltransferases Induced in Tobacco (Nicotiana tabacum L.) Leaves by Infection or Elicitor Treatment
journal, October 1993

RNAi-suppression of barley caffeic acid O -methyltransferase modifies lignin despite redundancy in the gene family
journal, October 2018

A direct approach to false discovery rates
journal, August 2002

Phosphorylation is an on/off switch for 5-hydroxyconiferaldehyde O -methyltransferase activity in poplar monolignol biosynthesis
journal, June 2015

Deletion of a gene cluster encoding pectin degrading enzymes in Caldicellulosiruptor bescii reveals an important role for pectin in plant biomass recalcitrance
journal, October 2014

CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice
journal, January 1994

Determination of the Structure and Catalytic Mechanism of Sorghum bicolor Caffeic Acid O -Methyltransferase and the Structural Impact of Three brown midrib12 Mutations
journal, June 2014

Development of feedstocks for cellulosic biofuels
journal, May 2012

Latitudinal Adaptation of Switchgrass Populations
journal, January 2004

Switchgrass Genomic Diversity, Ploidy, and Evolution: Novel Insights from a Network-Based SNP Discovery Protocol
journal, January 2013

Downregulation of p‐ COUMAROYL ESTER 3‐ HYDROXYLASE in rice leads to altered cell wall structures and improves biomass saccharification
journal, July 2018

Maize feedstocks with improved digestibility reduce the costs and environmental impacts of biomass pretreatment and saccharification
journal, March 2016

Hierarchical classification of switchgrass genotypes using SSR and chloroplast sequences: ecotypes, ploidies, gene pools, and cultivars
journal, November 2010

The Switchgrass Genome: Tools and Strategies
journal, January 2011

QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient
journal, June 2019

Switchgrass (Panicum virgatum) possesses a divergent family of cinnamoyl CoA reductases with distinct biochemical properties
journal, September 2009

GenBank
journal, December 2011

HMMER web server: 2018 update
journal, June 2018

Rapid Assessment of Lignin Content and Structure in Switchgrass (Panicum virgatum L.) Grown Under Different Environmental Conditions
journal, October 2009

Net energy of cellulosic ethanol from switchgrass
journal, January 2008

A High-Throughput Platform for Screening Milligram Quantities of Plant Biomass for Lignocellulose Digestibility
journal, January 2010

A Genomics Approach to Deciphering Lignin Biosynthesis in Switchgrass
journal, November 2013

Cell Wall Composition and Candidate Biosynthesis Gene Expression During Rice Development
journal, August 2016

Characterization of 5-Hydroxyconiferaldehyde O-Methyltransferase in Oryza sativa
journal, January 2013

A Spatial Accommodation by Neighboring Cells Is Required for Organ Initiation in Arabidopsis
journal, January 2014

Spatial gradients in cell wall composition and transcriptional profiles along elongating maize internodes
journal, January 2014

Switchgrass Growth and Effects on Biomass Accumulation, Moisture Content, and Nutrient Removal
journal, January 2017

Simultaneous regulation of F5H in COMT ‐ RNA i transgenic switchgrass alters effects of COMT suppression on syringyl lignin biosynthesis
journal, October 2018

Adaptations between Ecotypes and along Environmental Gradients in Panicum virgatum
journal, May 2014

Genome-Wide Characterization of the Lignification Toolbox in Arabidopsis
journal, November 2003

Functional characterization of the switchgrass (Panicum virgatum) R2R3-MYB transcription factor PvMYB4 for improvement of lignocellulosic feedstocks
journal, October 2011

Genetic Diversity of Twelve Switchgrass Populations Using Molecular and Morphological Markers
journal, January 2010

Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass
journal, February 2011

Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data
journal, March 2003

Developmental Control of Lignification in Stems of Lowland Switchgrass Variety Alamo and the Effects on Saccharification Efficiency
journal, October 2009

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

Designing the deconstruction of plant cell walls
journal, June 2008

Modifying lignin to improve bioenergy feedstocks: strengthening the barrier against pathogens?†
journal, January 2013

Chemical composition and response to dilute-acid pretreatment and enzymatic saccharification of alfalfa, reed canarygrass, and switchgrass
journal, October 2006

Describing and Quantifying Growth Stages of Perennial Forage Grasses
journal, January 1991

Molecular breeding of switchgrass for use as a biofuel crop
journal, December 2007

Biomass yield and quality of 20 switchgrass populations in southern Iowa, USA
journal, December 2002

Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003

Overexpression of a BAHD Acyltransferase, OsAt10 , Alters Rice Cell Wall Hydroxycinnamic Acid Content and Saccharification
journal, February 2013

Standardization of Switchgrass Sample Collection for Cell Wall and Biomass Trait Analysis
journal, January 2013

Application of the Gini Correlation Coefficient to Infer Regulatory Relationships in Transcriptome Analysis
journal, July 2012

Comparison of the Acetyl Bromide Spectrophotometric Method with Other Analytical Lignin Methods for Determining Lignin Concentration in Forage Samples
journal, June 2004

Sustainable bioenergy production from marginal lands in the US Midwest
journal, January 2013

Downregulation of pectin biosynthesis gene GAUT4 leads to reduced ferulate and lignin-carbohydrate cross-linking in switchgrass
journal, January 2019

Structural Basis for the Modulation of Lignin Monomer Methylation by Caffeic Acid/5-Hydroxyferulic Acid 3/5- O -Methyltransferase
journal, June 2002

Investigating plant cell wall components that affect biomass recalcitrance in poplar and switchgrass
journal, January 2013

Phylogenetic, Molecular, and Biochemical Characterization of Caffeic Acid o -Methyltransferase Gene Family in Brachypodium distachyon
journal, January 2013

Statistical significance for genomewide studies
journal, July 2003

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

Comparison of growth and performance in upland and lowland switchgrass types to water and nitrogen stress
journal, January 2003

Comparative transcriptome profiling of upland (VS16) and lowland (AP13) ecotypes of switchgrass
journal, November 2016