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Title: Improving wood properties for wood utilization through multi-omics integration in lignin biosynthesis

Abstract

A multi-omics quantitative integrative analysis of lignin biosynthesis can advance the strategic engineering of wood for timber, pulp, and biofuels. Lignin is polymerized from three monomers (monolignols) produced by a grid-like pathway. The pathway in wood formation of Populus trichocarpa has at least 21 genes, encoding enzymes that mediate 37 reactions on 24 metabolites, leading to lignin and affecting wood properties. We perturb these 21 pathway genes and integrate transcriptomic, proteomic, fluxomic and phenomic data from 221 lines selected from ~2000 transgenics (6-month-old). The integrative analysis estimates how changing expression of pathway gene or gene combination affects protein abundance, metabolic-flux, metabolite concentrations, and 25 wood traits, including lignin, tree-growth, density, strength, and saccharification. The analysis then predicts improvements in any of these 25 traits individually or in combinations, through engineering expression of specific monolignol genes. The analysis may lead to greater understanding of other pathways for improved growth and adaptation.

Authors:
 [1];  [2];  [2];  [3];  [3];  [3];  [3];  [4];  [3];  [5];  [6];  [7];  [8];  [9]; ORCiD logo [10];  [11];  [11];  [8]; ORCiD logo [2];  [12] more »;  [13];  [12];  [14];  [15];  [16];  [17];  [3];  [12];  [6]; ORCiD logo [10];  [12];  [8]; ORCiD logo [18];  [19];  [20];  [3];  [21] « less
  1. Northeast Forestry Univ., Harbin (China). State Key Lab. of Tree Genetics and Breeding; North Carolina State Univ., Raleigh, NC (United States). Dept. of Forestry and Environmental Resources, Forest Biotechnology Group
  2. North Carolina State Univ., Raleigh, NC (United States). Electrical and Computer Engineering
  3. North Carolina State Univ., Raleigh, NC (United States). Dept. of Forestry and Environmental Resources, Forest Biotechnology Group
  4. Chinese Academy of Forestry, Beijing (China). State Key Lab. of Tree Genetics and Breeding
  5. North Carolina State Univ., Raleigh, NC (United States). Dept. of Forestry and Environmental Resources, Forest Biotechnology Group; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Joint BioEnergy Inst.
  6. North Carolina State Univ., Raleigh, NC (United States). Civil, Construction and Environmental Engineering
  7. National Chung-Hsing Univ., Taichung (Taiwan). Dept. of Forestry
  8. North Carolina State Univ., Raleigh, NC (United States). W.M. Keck Fourier Transform Mass Spectrometry Lab., Dept. of Chemistry
  9. National Taiwan Univ., Taipei (Taiwan). School of Forestry and Resource Conservation
  10. Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center, Wisconsin Energy Inst., Dept. of Biochemistry
  11. National Renewable Energy Lab. (NREL), Golden, CO (United States). National Bioenergy Center
  12. North Carolina State Univ., Raleigh, NC (United States). Dept. of Forest Biomaterials
  13. North Carolina State Univ., Raleigh, NC (United States). Dept. of Operations Research
  14. Beihua Univ., Jilin (China). Dept. of Forestry
  15. Northeast Forestry Univ., Harbin (China). State Key Lab. of Tree Genetics and Breeding
  16. Northeast Forestry Univ., Harbin (China). State Key Lab. of Tree Genetics and Breeding; North Carolina State Univ., Raleigh, NC (United States). Dept. of Forestry and Environmental Resources, Forest Biotechnology Group; National Taiwan Univ., Taipei (Taiwan). College of Life Science, Dept. of Life Sciences
  17. Northeast Forestry Univ., Harbin (China). State Key Lab. of Tree Genetics and Breeding; North Carolina State Univ., Raleigh, NC (United States). Dept. of Forestry and Environmental Resources, Forest Biotechnology Group
  18. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Joint BioEnergy Inst.
  19. North Carolina State Univ., Raleigh, NC (United States). Bioinformatics Research Center
  20. North Carolina State Univ., Raleigh, NC (United States). Dept. of Forestry and Environmental Resources
  21. Northeast Forestry Univ., Harbin (China). State Key Lab. of Tree Genetics and Breeding; North Carolina State Univ., Raleigh, NC (United States). Dept. of Forestry and Environmental Resources, Forest Biotechnology Group; North Carolina State Univ., Raleigh, NC (United States). Dept. of Forest Biomaterials
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Office of Biological and Environmental Research; National Natural Science Foundation of China (NNSFC); USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1435499
Alternate Identifier(s):
OSTI ID: 1460355
Report Number(s):
NREL/JA-2700-71418
Journal ID: ISSN 2041-1723
Grant/Contract Number:  
AC36-08GO28308; 31430093; 31470672; 31522014; DBI-0922391; FC02-07ER64494; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; genetic engineering; molecular engineering; secondary metabolism

Citation Formats

Wang, Jack P., Matthews, Megan L., Williams, Cranos M., Shi, Rui, Yang, Chenmin, Tunlaya-Anukit, Sermsawat, Chen, Hsi-Chuan, Li, Quanzi, Liu, Jie, Lin, Chien-Yuan, Naik, Punith, Sun, Ying-Hsuan, Loziuk, Philip L., Yeh, Ting-Feng, Kim, Hoon, Gjersing, Erica, Shollenberger, Todd, Shuford, Christopher M., Song, Jina, Miller, Zachary, Huang, Yung-Yun, Edmunds, Charles W., Liu, Baoguang, Sun, Yi, Lin, Ying-Chung Jimmy, Li, Wei, Chen, Hao, Peszlen, Ilona, Ducoste, Joel J., Ralph, John, Chang, Hou-Min, Muddiman, David C., Davis, Mark F., Smith, Chris, Isik, Fikret, Sederoff, Ronald, and Chiang, Vincent L. Improving wood properties for wood utilization through multi-omics integration in lignin biosynthesis. United States: N. p., 2018. Web. https://doi.org/10.1038/s41467-018-03863-z.
Wang, Jack P., Matthews, Megan L., Williams, Cranos M., Shi, Rui, Yang, Chenmin, Tunlaya-Anukit, Sermsawat, Chen, Hsi-Chuan, Li, Quanzi, Liu, Jie, Lin, Chien-Yuan, Naik, Punith, Sun, Ying-Hsuan, Loziuk, Philip L., Yeh, Ting-Feng, Kim, Hoon, Gjersing, Erica, Shollenberger, Todd, Shuford, Christopher M., Song, Jina, Miller, Zachary, Huang, Yung-Yun, Edmunds, Charles W., Liu, Baoguang, Sun, Yi, Lin, Ying-Chung Jimmy, Li, Wei, Chen, Hao, Peszlen, Ilona, Ducoste, Joel J., Ralph, John, Chang, Hou-Min, Muddiman, David C., Davis, Mark F., Smith, Chris, Isik, Fikret, Sederoff, Ronald, & Chiang, Vincent L. Improving wood properties for wood utilization through multi-omics integration in lignin biosynthesis. United States. https://doi.org/10.1038/s41467-018-03863-z
Wang, Jack P., Matthews, Megan L., Williams, Cranos M., Shi, Rui, Yang, Chenmin, Tunlaya-Anukit, Sermsawat, Chen, Hsi-Chuan, Li, Quanzi, Liu, Jie, Lin, Chien-Yuan, Naik, Punith, Sun, Ying-Hsuan, Loziuk, Philip L., Yeh, Ting-Feng, Kim, Hoon, Gjersing, Erica, Shollenberger, Todd, Shuford, Christopher M., Song, Jina, Miller, Zachary, Huang, Yung-Yun, Edmunds, Charles W., Liu, Baoguang, Sun, Yi, Lin, Ying-Chung Jimmy, Li, Wei, Chen, Hao, Peszlen, Ilona, Ducoste, Joel J., Ralph, John, Chang, Hou-Min, Muddiman, David C., Davis, Mark F., Smith, Chris, Isik, Fikret, Sederoff, Ronald, and Chiang, Vincent L. Fri . "Improving wood properties for wood utilization through multi-omics integration in lignin biosynthesis". United States. https://doi.org/10.1038/s41467-018-03863-z. https://www.osti.gov/servlets/purl/1435499.
@article{osti_1435499,
title = {Improving wood properties for wood utilization through multi-omics integration in lignin biosynthesis},
author = {Wang, Jack P. and Matthews, Megan L. and Williams, Cranos M. and Shi, Rui and Yang, Chenmin and Tunlaya-Anukit, Sermsawat and Chen, Hsi-Chuan and Li, Quanzi and Liu, Jie and Lin, Chien-Yuan and Naik, Punith and Sun, Ying-Hsuan and Loziuk, Philip L. and Yeh, Ting-Feng and Kim, Hoon and Gjersing, Erica and Shollenberger, Todd and Shuford, Christopher M. and Song, Jina and Miller, Zachary and Huang, Yung-Yun and Edmunds, Charles W. and Liu, Baoguang and Sun, Yi and Lin, Ying-Chung Jimmy and Li, Wei and Chen, Hao and Peszlen, Ilona and Ducoste, Joel J. and Ralph, John and Chang, Hou-Min and Muddiman, David C. and Davis, Mark F. and Smith, Chris and Isik, Fikret and Sederoff, Ronald and Chiang, Vincent L.},
abstractNote = {A multi-omics quantitative integrative analysis of lignin biosynthesis can advance the strategic engineering of wood for timber, pulp, and biofuels. Lignin is polymerized from three monomers (monolignols) produced by a grid-like pathway. The pathway in wood formation of Populus trichocarpa has at least 21 genes, encoding enzymes that mediate 37 reactions on 24 metabolites, leading to lignin and affecting wood properties. We perturb these 21 pathway genes and integrate transcriptomic, proteomic, fluxomic and phenomic data from 221 lines selected from ~2000 transgenics (6-month-old). The integrative analysis estimates how changing expression of pathway gene or gene combination affects protein abundance, metabolic-flux, metabolite concentrations, and 25 wood traits, including lignin, tree-growth, density, strength, and saccharification. The analysis then predicts improvements in any of these 25 traits individually or in combinations, through engineering expression of specific monolignol genes. The analysis may lead to greater understanding of other pathways for improved growth and adaptation.},
doi = {10.1038/s41467-018-03863-z},
journal = {Nature Communications},
number = 1,
volume = 9,
place = {United States},
year = {2018},
month = {4}
}

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Works referenced in this record:

Specific down-regulation of PAL genes by artificial microRNAs in Populus trichocarpa
journal, August 2010


Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation
journal, December 2006

  • Lu, Peng; Vogel, Christine; Wang, Rong
  • Nature Biotechnology, Vol. 25, Issue 1
  • DOI: 10.1038/nbt1270

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

  • Hu, Wen-Jing; Harding, Scott A.; Lung, Jrhau
  • Nature Biotechnology, Vol. 17, Issue 8, p. 808-812
  • DOI: 10.1038/11758

Tissue and cell-type co-expression networks of transcription factors and wood component genes in Populus trichocarpa
journal, January 2017


Natural genetic variability reduces recalcitrance in poplar
journal, May 2016

  • Bhagia, Samarthya; Muchero, Wellington; Kumar, Rajeev
  • Biotechnology for Biofuels, Vol. 9, Issue 1
  • DOI: 10.1186/s13068-016-0521-2

Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6/pyridine-d5
journal, January 2010

  • Kim, Hoon; Ralph, John
  • Org. Biomol. Chem., Vol. 8, Issue 3
  • DOI: 10.1039/b916070a

Genetic Transformation of Populus trichocarpa Genotype Nisqually-1: A Functional Genomic Tool for Woody Plants
journal, November 2006

  • Song, Jingyuan; Lu, Shanfa; Chen, Zenn-Zong
  • Plant and Cell Physiology, Vol. 47, Issue 11, p. 1582-1589
  • DOI: 10.1093/pcp/pcl018

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

  • Wang, Jack P.; Chuang, Ling; Loziuk, Philip L.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 27
  • DOI: 10.1073/pnas.1510473112

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

  • Chen, Fang; Dixon, Richard A.
  • Nature Biotechnology, Vol. 25, Issue 7, p. 759-761
  • DOI: 10.1038/nbt1316

Membrane protein complexes catalyze both 4- and 3-hydroxylation of cinnamic acid derivatives in monolignol biosynthesis
journal, December 2011

  • Chen, H. -C.; Li, Q.; Shuford, C. M.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 52
  • DOI: 10.1073/pnas.1116416109

Ultrafast and memory-efficient alignment of short DNA sequences to the human genome
journal, January 2009


Effect of Lignin Genetic Modification on Wood Anatomy of Aspen Trees
journal, January 2010


TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
journal, January 2013


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


Skyline: an open source document editor for creating and analyzing targeted proteomics experiments
journal, February 2010


The Cellulase-Mediated Saccharification on Wood Derived from Transgenic Low-Lignin Lines of Black Cottonwood (Populus trichocarpa)
journal, August 2012

  • Min, Douyong; Li, Quanzi; Jameel, Hasan
  • Applied Biochemistry and Biotechnology, Vol. 168, Issue 4
  • DOI: 10.1007/s12010-012-9833-2

Salicylic acid mediates the reduced growth of lignin down-regulated plants
journal, November 2011

  • Gallego-Giraldo, L.; Escamilla-Trevino, L.; Jackson, L. A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 51
  • DOI: 10.1073/pnas.1117873108

BioNumbers—the database of key numbers in molecular and cell biology
journal, October 2009

  • Milo, Ron; Jorgensen, Paul; Moran, Uri
  • Nucleic Acids Research, Vol. 38, Issue suppl_1
  • DOI: 10.1093/nar/gkp889

Improving total saccharification yield of Arabidopsis plants by vessel-specific complementation of caffeoyl shikimate esterase (cse) mutants
journal, July 2016


Highly Specific Gene Silencing by Artificial MicroRNAs in Arabidopsis
journal, March 2006

  • Schwab, Rebecca; Ossowski, Stephan; Riester, Markus
  • The Plant Cell, Vol. 18, Issue 5
  • DOI: 10.1105/tpc.105.039834

A scaling normalization method for differential expression analysis of RNA-seq data
journal, March 2010


Towards a Systems Approach for Lignin Biosynthesis in Populus trichocarpa: Transcript Abundance and Specificity of the Monolignol Biosynthetic Genes
journal, December 2009

  • Shi, Rui; Sun, Ying-Hsuan; Li, Quanzi
  • Plant and Cell Physiology, Vol. 51, Issue 1
  • DOI: 10.1093/pcp/pcp175

High-Throughput Screening Techniques for Biomass Conversion
journal, October 2009


The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


Regulation of phenylalanine ammonia-lyase (PAL) gene family in wood forming tissue of Populus trichocarpa
journal, June 2013


Reciprocal cross-regulation of VND and SND multigene TF families for wood formation in Populus trichocarpa
journal, October 2017

  • Lin, Ying-Chung Jimmy; Chen, Hao; Li, Quanzi
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 45
  • DOI: 10.1073/pnas.1714422114

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


Populus trichocarpa cell wall chemistry and ultrastructure trait variation, genetic control and genetic correlations
journal, December 2012

  • Porth, Ilga; Klápště, Jaroslav; Skyba, Oleksandr
  • New Phytologist, Vol. 197, Issue 3, p. 777-790
  • DOI: 10.1111/nph.12014

Comprehensive Quantification of Monolignol-Pathway Enzymes in Populus trichocarpa by Protein Cleavage Isotope Dilution Mass Spectrometry
journal, May 2012

  • Shuford, Christopher M.; Li, Quanzi; Sun, Ying-Hsuan
  • Journal of Proteome Research, Vol. 11, Issue 6
  • DOI: 10.1021/pr300205a

BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010


Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa
journal, June 2013

  • Lu, S.; Li, Q.; Wei, H.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 26
  • DOI: 10.1073/pnas.1308936110

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

  • Van Acker, Rebecca; Vanholme, Ruben; Storme, Véronique
  • Biotechnology for Biofuels, Vol. 6, Article No. 46
  • DOI: 10.1186/1754-6834-6-46

Transgenic poplars with reduced lignin show impaired xylem conductivity, growth efficiency and survival: Transgenic poplars with reduced lignin
journal, February 2011


Splice variant of the SND1 transcription factor is a dominant negative of SND1 members and their regulation in Populus trichocarpa
journal, August 2012

  • Li, Q.; Lin, Y. -C.; Sun, Y. -H.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 36
  • DOI: 10.1073/pnas.1212977109

A simple improved-throughput xylem protoplast system for studying wood formation
journal, August 2014


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

  • Bonawitz, Nicholas D.; Kim, Jeong Im; Tobimatsu, Yuki
  • Nature, Vol. 509, Issue 7500, p. 376-380
  • DOI: 10.1038/nature13084

An essential role of caffeoyl shikimate esterase in monolignol biosynthesis in Medicago truncatula
journal, June 2016

  • Ha, Chan Man; Escamilla-Trevino, Luis; Yarce, Juan Carlos Serrani
  • The Plant Journal, Vol. 86, Issue 5
  • DOI: 10.1111/tpj.13177

Pretreatment: the key to unlocking low-cost cellulosic ethanol
journal, January 2008

  • Yang, Bin; Wyman, Charles E.
  • Biofuels, Bioproducts and Biorefining, Vol. 2, Issue 1
  • DOI: 10.1002/bbb.49

Wood specific gravity-mechanical property relationship at species level
journal, June 1997


Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6/pyridine-d5
journal, January 2010

  • Kim, Hoon; Ralph, John
  • Org. Biomol. Chem., Vol. 8, Issue 3
  • DOI: 10.1039/B916070A

    Works referencing / citing this record:

    Quantitative fermentation of unpretreated transgenic poplar by Caldicellulosiruptor bescii
    journal, August 2019

    • Straub, Christopher T.; Khatibi, Piyum A.; Wang, Jack P.
    • Nature Communications, Vol. 10, Issue 1
    • DOI: 10.1038/s41467-019-11376-6

    Secondary cell wall biosynthesis
    journal, November 2018

    • Zhong, Ruiqin; Cui, Dongtao; Ye, Zheng‐Hua
    • New Phytologist, Vol. 221, Issue 4
    • DOI: 10.1111/nph.15537

    Synergistic effects of tung oil and heat treatment on physicochemical properties of bamboo materials
    journal, September 2019


    Research on the Physico-Mechanical Properties of Moso Bamboo with Thermal Treatment in Tung Oil and Its Influencing Factors
    journal, February 2019

    • Tang, Tong; Chen, Xiufang; Zhang, Bo
    • Materials, Vol. 12, Issue 4
    • DOI: 10.3390/ma12040599

    Rhamnogalacturonan‐I is a determinant of cell–cell adhesion in poplar wood
    journal, October 2019

    • Yang, Haibing; Benatti, Matheus R.; Karve, Rucha A.
    • Plant Biotechnology Journal, Vol. 18, Issue 4
    • DOI: 10.1111/pbi.13271

    Use of the lignocellulose-degrading bacterium Caldicellulosiruptor bescii to assess recalcitrance and conversion of wild-type and transgenic poplar
    journal, March 2020

    • Straub, Christopher T.; Bing, Ryan G.; Wang, Jack P.
    • Biotechnology for Biofuels, Vol. 13, Issue 1
    • DOI: 10.1186/s13068-020-01675-2

    Fibre‐specific regulation of lignin biosynthesis improves biomass quality in Populus
    journal, January 2020

    • Gui, Jinshan; Lam, Pui Ying; Tobimatsu, Yuki
    • New Phytologist, Vol. 226, Issue 4
    • DOI: 10.1111/nph.16411

    Enzyme-Enzyme Interactions in Monolignol Biosynthesis
    journal, January 2019


    Regulation of Lignin Biosynthesis and Its Role in Growth-Defense Tradeoffs
    journal, September 2018


    Systems and Synthetic Biology of Forest Trees: A Bioengineering Paradigm for Woody Biomass Feedstocks
    journal, June 2019

    • Myburg, Alexander A.; Hussey, Steven G.; Wang, Jack P.
    • Frontiers in Plant Science, Vol. 10
    • DOI: 10.3389/fpls.2019.00775

    A systems biology view of wood formation in Eucalyptus grandis trees submitted to different potassium and water regimes
    journal, April 2019

    • Ployet, Raphael; Veneziano Labate, Mônica T.; Regiani Cataldi, Thais
    • New Phytologist, Vol. 223, Issue 2
    • DOI: 10.1111/nph.15802