PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus
Abstract
Background: Plant secondary cell wall is a renewable feedstock for biofuels and biomaterials production. Arabidopsis VASCULAR-RELATED NAC DOMAIN (VND) has been demonstrated to be a key transcription factor regulating secondary cell wall biosynthesis. However, less is known about its role in the woody species.Results: Here we report the functional characterization of Populus deltoides WOOD-ASSOCIATED NAC DOMAIN protein 3 (PdWND3A), a sequence homolog of Arabidopsis VND4 and VND5 that are members of transcription factor networks regulating secondary cell wall biosynthesis. PdWND3A was expressed at higher level in the xylem than in other tissues. The stem tissues of transgenic P. deltoides overexpressing PdWND3A (OXPdWND3A) contained more vessel cells than that of wild-type plants. Furthermore, lignin content and lignin monomer syringyl and guaiacyl (S/G) ratio were higher in OXPdWND3A transgenic plants than in wild-type plants. Consistent with these observations, the expression of FERULATE 5-HYDROXYLASE1 (F5H1), encoding an enzyme involved in the biosynthesis of sinapyl alcohol (S unit monolignol), was elevated in OXPdWND3A transgenic plants. Saccharification analysis indicated that the rate of sugar release was reduced in the transgenic plants. In addition, OXPdWND3A transgenic plants produced lower amounts of biomass than wild-type plants.Conclusions: PdWND3A affects lignin biosynthesis and composition and negatively impacts sugar releasemore »
- Authors:
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1618609
- Alternate Identifier(s):
- OSTI ID: 1626852; OSTI ID: 1761683
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Published Article
- Journal Name:
- BMC Plant Biology
- Additional Journal Information:
- Journal Name: BMC Plant Biology Journal Volume: 19 Journal Issue: 1; Journal ID: ISSN 1471-2229
- Publisher:
- Springer Science + Business Media
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Plant Sciences; F5H; Lignin; Poplus; Saccharification; Sinapyl alcohol; S/G ratio; VND
Citation Formats
Yang, Yongil, Yoo, Chang Geun, Rottmann, William, Winkeler, Kimberly A., Collins, Cassandra M., Gunter, Lee E., Jawdy, Sara S., Yang, Xiaohan, Pu, Yunqiao, Ragauskas, Arthur J., Tuskan, Gerald A., and Chen, Jin-Gui. PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus. United Kingdom: N. p., 2019.
Web. doi:10.1186/s12870-019-2111-5.
Yang, Yongil, Yoo, Chang Geun, Rottmann, William, Winkeler, Kimberly A., Collins, Cassandra M., Gunter, Lee E., Jawdy, Sara S., Yang, Xiaohan, Pu, Yunqiao, Ragauskas, Arthur J., Tuskan, Gerald A., & Chen, Jin-Gui. PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus. United Kingdom. https://doi.org/10.1186/s12870-019-2111-5
Yang, Yongil, Yoo, Chang Geun, Rottmann, William, Winkeler, Kimberly A., Collins, Cassandra M., Gunter, Lee E., Jawdy, Sara S., Yang, Xiaohan, Pu, Yunqiao, Ragauskas, Arthur J., Tuskan, Gerald A., and Chen, Jin-Gui. Mon .
"PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus". United Kingdom. https://doi.org/10.1186/s12870-019-2111-5.
@article{osti_1618609,
title = {PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus},
author = {Yang, Yongil and Yoo, Chang Geun and Rottmann, William and Winkeler, Kimberly A. and Collins, Cassandra M. and Gunter, Lee E. and Jawdy, Sara S. and Yang, Xiaohan and Pu, Yunqiao and Ragauskas, Arthur J. and Tuskan, Gerald A. and Chen, Jin-Gui},
abstractNote = {Background: Plant secondary cell wall is a renewable feedstock for biofuels and biomaterials production. Arabidopsis VASCULAR-RELATED NAC DOMAIN (VND) has been demonstrated to be a key transcription factor regulating secondary cell wall biosynthesis. However, less is known about its role in the woody species.Results: Here we report the functional characterization of Populus deltoides WOOD-ASSOCIATED NAC DOMAIN protein 3 (PdWND3A), a sequence homolog of Arabidopsis VND4 and VND5 that are members of transcription factor networks regulating secondary cell wall biosynthesis. PdWND3A was expressed at higher level in the xylem than in other tissues. The stem tissues of transgenic P. deltoides overexpressing PdWND3A (OXPdWND3A) contained more vessel cells than that of wild-type plants. Furthermore, lignin content and lignin monomer syringyl and guaiacyl (S/G) ratio were higher in OXPdWND3A transgenic plants than in wild-type plants. Consistent with these observations, the expression of FERULATE 5-HYDROXYLASE1 (F5H1), encoding an enzyme involved in the biosynthesis of sinapyl alcohol (S unit monolignol), was elevated in OXPdWND3A transgenic plants. Saccharification analysis indicated that the rate of sugar release was reduced in the transgenic plants. In addition, OXPdWND3A transgenic plants produced lower amounts of biomass than wild-type plants.Conclusions: PdWND3A affects lignin biosynthesis and composition and negatively impacts sugar release and biomass production.},
doi = {10.1186/s12870-019-2111-5},
journal = {BMC Plant Biology},
number = 1,
volume = 19,
place = {United Kingdom},
year = {2019},
month = {11}
}
https://doi.org/10.1186/s12870-019-2111-5
Web of Science
Works referenced in this record:
Lignin Biosynthesis
journal, June 2003
- Boerjan, Wout; Ralph, John; Baucher, Marie
- Annual Review of Plant Biology, Vol. 54, Issue 1, p. 519-546
Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 Directly Regulates the Genes That Govern Programmed Cell Death and Secondary Wall Formation during Xylem Differentiation
journal, October 2010
- Ohashi-Ito, Kyoko; Oda, Yoshihisa; Fukuda, Hiroo
- The Plant Cell, Vol. 22, Issue 10
Insights of biomass recalcitrance in natural Populus trichocarpa variants for biomass conversion
journal, January 2017
- Yoo, Chang Geun; Yang, Yongil; Pu, Yunqiao
- Green Chemistry, Vol. 19, Issue 22
Structural and compositional modifications in lignin of transgenic alfalfa down-regulated in caffeic acid 3-O-methyltransferase and caffeoyl coenzyme A 3-O-methyltransferase
journal, January 2003
- Marita, Jane M.; Ralph, John; Hatfield, Ronald D.
- Phytochemistry, Vol. 62, Issue 1
Syringyl lignin production in conifers: Proof of concept in a Pine tracheary element system
journal, April 2015
- Wagner, Armin; Tobimatsu, Yuki; Phillips, Lorelle
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 19
Essential Role of Caffeoyl Coenzyme A O -Methyltransferase in Lignin Biosynthesis in Woody Poplar Plants
journal, October 2000
- Zhong, Ruiqin; Morrison, W. Herbert; Himmelsbach, David S.
- Plant Physiology, Vol. 124, Issue 2
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010
- Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
- Systematic Biology, Vol. 59, Issue 3
Metabolic Channeling in Plants
journal, June 2004
- Winkel, Brenda S. J.
- Annual Review of Plant Biology, Vol. 55, Issue 1
The poplar PtrWNDs are transcriptional activators of secondary cell wall biosynthesis
journal, April 2010
- Zhong, Ruiqin; Ye, Zheng-Hua
- Plant Signaling & Behavior, Vol. 5, Issue 4
The MYB46 Transcription Factor Is a Direct Target of SND1 and Regulates Secondary Wall Biosynthesis in Arabidopsis
journal, September 2007
- Zhong, R.; Richardson, E. A.; Ye, Z.-H.
- The Plant Cell Online, Vol. 19, Issue 9, p. 2776-2792
Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms
journal, August 1999
- Osakabe, K.; Tsao, C. C.; Li, L.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 16
Arabidopsis NAC Domain Proteins, VND1 to VND5, Are Transcriptional Regulators of Secondary Wall Biosynthesis in Vessels
journal, August 2014
- Zhou, Jianli; Zhong, Ruiqin; Ye, Zheng-Hua
- PLoS ONE, Vol. 9, Issue 8
VASCULAR-RELATED NAC-DOMAIN 7 directly regulates the expression of a broad range of genes for xylem vessel formation: Direct target genes of VND7
journal, March 2011
- Yamaguchi, Masatoshi; Mitsuda, Nobutaka; Ohtani, Misato
- The Plant Journal, Vol. 66, Issue 4
NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants
journal, May 2015
- Nakano, Yoshimi; Yamaguchi, Masatoshi; Endo, Hitoshi
- Frontiers in Plant Science, Vol. 6
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
journal, February 2007
- Himmel, M. E.; Ding, S.-Y.; Johnson, D. K.
- Science, Vol. 315, Issue 5813, p. 804-807
A NAC domain protein family contributing to the regulation of wood formation in poplar: NAC domain protein family regulates wood formation
journal, June 2011
- Ohtani, Misato; Nishikubo, Nobuyuki; Xu, Bo
- The Plant Journal, Vol. 67, Issue 3
Functional Characterization of Poplar Wood-Associated NAC Domain Transcription Factors
journal, December 2009
- Zhong, Ruiqin; Lee, Chanhui; Ye, Zheng-Hua
- Plant Physiology, Vol. 152, Issue 2
Phytozome: a comparative platform for green plant genomics
journal, November 2011
- Goodstein, David M.; Shu, Shengqiang; Howson, Russell
- Nucleic Acids Research, Vol. 40, Issue D1
The NAC Transcription Factors NST1 and NST2 of Arabidopsis Regulate Secondary Wall Thickenings and Are Required for Anther Dehiscence
journal, October 2005
- Mitsuda, Nobutaka; Seki, Motoaki; Shinozaki, Kazuo
- The Plant Cell, Vol. 17, Issue 11
Secondary Cell Walls: Biosynthesis, Patterned Deposition and Transcriptional Regulation
journal, October 2014
- Zhong, Ruiqin; Ye, Zheng-Hua
- Plant and Cell Physiology, Vol. 56, Issue 2
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001
- Livak, Kenneth J.; Schmittgen, Thomas D.
- Methods, Vol. 25, Issue 4
NIH Image to ImageJ: 25 years of image analysis
journal, June 2012
- Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
- Nature Methods, Vol. 9, Issue 7
SND1, a NAC Domain Transcription Factor, Is a Key Regulator of Secondary Wall Synthesis in Fibers of Arabidopsis
journal, November 2006
- Zhong, Ruiqin; Demura, Taku; Ye, Zheng-Hua
- The Plant Cell, Vol. 18, Issue 11
Cellulosic Biofuels
journal, June 2009
- Carroll, Andrew; Somerville, Chris
- Annual Review of Plant Biology, Vol. 60, Issue 1
Transcription switches for protoxylem and metaxylem vessel formation
journal, August 2005
- Kubo, M.
- Genes & Development, Vol. 19, Issue 16
The Poplar MYB Master Switches Bind to the SMRE Site and Activate the Secondary Wall Biosynthetic Program during Wood Formation
journal, July 2013
- Zhong, Ruiqin; McCarthy, Ryan L.; Haghighat, Marziyeh
- PLoS ONE, Vol. 8, Issue 7
Lignin Valorization: Improving Lignin Processing in the Biorefinery
journal, May 2014
- Ragauskas, A. J.; Beckham, G. T.; Biddy, M. J.
- Science, Vol. 344, Issue 6185, p. 1246843-1246843
MYB Transcription Factors as Regulators of Phenylpropanoid Metabolism in Plants
journal, May 2015
- Liu, Jingying; Osbourn, Anne; Ma, Pengda
- Molecular Plant, Vol. 8, Issue 5
Nonlinear partial differential equations and applications: Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells
journal, November 2002
- Demura, T.; Tashiro, G.; Horiguchi, G.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 24
Complexity of the transcriptional network controlling secondary wall biosynthesis
journal, December 2014
- Zhong, Ruiqin; Ye, Zheng-Hua
- Plant Science, Vol. 229
Lignin content in natural Populus variants affects sugar release
journal, March 2011
- Studer, M. H.; DeMartini, J. D.; Davis, M. F.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 15, p. 6300-6305
The Pfam protein families database: towards a more sustainable future
journal, December 2015
- Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y.
- Nucleic Acids Research, Vol. 44, Issue D1
Lignification: Flexibility, Biosynthesis and Regulation
journal, August 2016
- Zhao, Qiao
- Trends in Plant Science, Vol. 21, Issue 8
Dissection of the Transcriptional Program Regulating Secondary Wall Biosynthesis during Wood Formation in Poplar
journal, September 2011
- Zhong, Ruiqin; McCarthy, Ryan L.; Lee, Chanhui
- Plant Physiology, Vol. 157, Issue 3
Molecular control of wood formation in trees
journal, March 2015
- Ye, Zheng-Hua; Zhong, Ruiqin
- Journal of Experimental Botany, Vol. 66, Issue 14
VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 Effectively Induce Transdifferentiation into Xylem Vessel Elements under Control of an Induction System
journal, May 2010
- Yamaguchi, Masatoshi; Goué, Nadia; Igarashi, Hisako
- Plant Physiology, Vol. 153, Issue 3
Multiple Classes of Transcription Factors Regulate the Expression of VASCULAR-RELATED NAC-DOMAIN7, a Master Switch of Xylem Vessel Differentiation
journal, September 2014
- Endo, Hitoshi; Yamaguchi, Masatoshi; Tamura, Taizo
- Plant and Cell Physiology, Vol. 56, Issue 2
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
NAC Transcription Factors, NST1 and NST3, Are Key Regulators of the Formation of Secondary Walls in Woody Tissues of Arabidopsis
journal, January 2007
- Mitsuda, N.; Iwase, A.; Yamamoto, H.
- The Plant Cell, Vol. 19, Issue 1, p. 270-280
TERE; a novel cis-element responsible for a coordinated expression of genes related to programmed cell death and secondary wall formation during differentiation of tracheary elements: Tracheary-element-regulating cis-element
journal, August 2007
- Pyo, Hyunjin; Demura, Taku; Fukuda, Hiroo
- The Plant Journal, Vol. 51, Issue 6
Transcriptional networks for lignin biosynthesis: more complex than we thought?
journal, April 2011
- Zhao, Qiao; Dixon, Richard A.
- Trends in Plant Science, Vol. 16, Issue 4, p. 227-233
New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cytochrome P450-dependent monooxygenase
journal, August 1999
- Humphreys, J. M.; Hemm, M. R.; Chapple, C.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 18
The Effects on Lignin Structure of Overexpression of Ferulate 5-Hydroxylase in Hybrid Poplar 1
journal, April 2009
- Stewart, Jaclyn J.; Akiyama, Takuya; Chapple, Clint
- Plant Physiology, Vol. 150, Issue 2
Global Analysis of Direct Targets of Secondary Wall NAC Master Switches in Arabidopsis
journal, November 2010
- Zhong, Ruiqin; Lee, Chanhui; Ye, Zheng-Hua
- Molecular Plant, Vol. 3, Issue 6
4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase
journal, April 2019
- Barros, Jaime; Escamilla-Trevino, Luis; Song, Luhua
- Nature Communications, Vol. 10, Issue 1
Overexpression of a Domain of Unknown Function 266-containing protein results in high cellulose content, reduced recalcitrance, and enhanced plant growth in the bioenergy crop Populus
journal, March 2017
- Yang, Yongil; Yoo, Chang Geun; Guo, Hao-Bo
- Biotechnology for Biofuels, Vol. 10, Issue 1
Comprehensive Analysis of NAC Domain Transcription Factor Gene Family in Populus trichocarpa
journal, January 2010
- Hu, Ruibo; Qi, Guang; Kong, Yingzhen
- BMC Plant Biology, Vol. 10, Issue 1
Plant cell wall polymers as precursors for biofuels
journal, June 2010
- Pauly, Markus; Keegstra, Kenneth
- Current Opinion in Plant Biology, Vol. 13, Issue 3
Cinnamoyl CoA reductase, the first committed enzyme of the lignin branch biosynthetic pathway: cloning, expression and phylogenetic relationships
journal, March 1997
- Lacombe, Eric; Hawkins, Simon; Van Doorsselaere, Jan
- The Plant Journal, Vol. 11, Issue 3
CINNAMYL ALCOHOL DEHYDROGENASE-C and -D Are the Primary Genes Involved in Lignin Biosynthesis in the Floral Stem of Arabidopsis
journal, June 2005
- Sibout, Richard; Eudes, Aymerick; Mouille, Gregory
- The Plant Cell, Vol. 17, Issue 7
Syringyl lignin biosynthesis is directly regulated by a secondary cell wall master switch
journal, July 2010
- Zhao, Q.; Wang, H.; Yin, Y.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 32, p. 14496-14501
Modifications in Lignin and Accumulation of Phenolic Glucosides in Poplar Xylem upon Down-regulation of Caffeoyl-Coenzyme A O-Methyltransferase, an Enzyme Involved in Lignin Biosynthesis
journal, August 2000
- Meyermans, Hugo; Morreel, Kris; Lapierre, Catherine
- Journal of Biological Chemistry, Vol. 275, Issue 47, p. 36899-36909
Altered lignin biosynthesis using biotechnology to improve lignocellulosic biofuel feedstocks
journal, July 2014
- Poovaiah, Charleson R.; Nageswara-Rao, Madhugiri; Soneji, Jaya R.
- Plant Biotechnology Journal, Vol. 12, Issue 9
Elucidating Structural Characteristics of Biomass using Solution-State 2 D NMR with a Mixture of Deuterated Dimethylsulfoxide and Hexamethylphosphoramide
journal, April 2016
- Yoo, Chang Geun; Pu, Yunqiao; Li, Mi
- ChemSusChem, Vol. 9, Issue 10
MYB58 and MYB63 Are Transcriptional Activators of the Lignin Biosynthetic Pathway during Secondary Cell Wall Formation in Arabidopsis
journal, January 2009
- Zhou, Jianli; Lee, Chanhui; Zhong, Ruiqin
- The Plant Cell, Vol. 21, Issue 1