PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus

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

doi:10.1186/s12870-019-2111-5

Title: PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus

Journal Article · 10 November 2019 · BMC Plant Biology

DOI: https://doi.org/10.1186/s12870-019-2111-5 · OSTI ID:1618609

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.;

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 release and biomass production.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1618609

Journal Information:: BMC Plant Biology, Journal Name: BMC Plant Biology Journal Issue: 1 Vol. 19; ISSN 1471-2229

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (56)

Elucidating Structural Characteristics of Biomass using Solution-State 2 D NMR with a Mixture of Deuterated Dimethylsulfoxide and Hexamethylphosphoramide Yoo, Chang Geun; Pu, Yunqiao; Li, Mi ChemSusChem, Vol. 9, Issue 10 https://doi.org/10.1002/cssc.201600135	journal	April 2016
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Structural and compositional modifications in lignin of transgenic alfalfa down-regulated in caffeic acid 3-O-methyltransferase and caffeoyl coenzyme A 3-O-methyltransferase Marita, Jane M.; Ralph, John; Hatfield, Ronald D. Phytochemistry, Vol. 62, Issue 1 https://doi.org/10.1016/S0031-9422(02)00434-X	journal	January 2003
MYB Transcription Factors as Regulators of Phenylpropanoid Metabolism in Plants Liu, Jingying; Osbourn, Anne; Ma, Pengda Molecular Plant, Vol. 8, Issue 5 https://doi.org/10.1016/j.molp.2015.03.012	journal	May 2015
Plant cell wall polymers as precursors for biofuels Pauly, Markus; Keegstra, Kenneth Current Opinion in Plant Biology, Vol. 13, Issue 3 https://doi.org/10.1016/j.pbi.2009.12.009	journal	June 2010
Complexity of the transcriptional network controlling secondary wall biosynthesis Zhong, Ruiqin; Ye, Zheng-Hua Plant Science, Vol. 229 https://doi.org/10.1016/j.plantsci.2014.09.009	journal	December 2014
Transcriptional networks for lignin biosynthesis: more complex than we thought? Zhao, Qiao; Dixon, Richard A. Trends in Plant Science, Vol. 16, Issue 4, p. 227-233 https://doi.org/10.1016/j.tplants.2010.12.005	journal	April 2011
Lignification: Flexibility, Biosynthesis and Regulation Zhao, Qiao Trends in Plant Science, Vol. 21, Issue 8 https://doi.org/10.1016/j.tplants.2016.04.006	journal	August 2016
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase Barros, Jaime; Escamilla-Trevino, Luis; Song, Luhua Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10082-7	journal	April 2019
Insights of biomass recalcitrance in natural Populus trichocarpa variants for biomass conversion Yoo, Chang Geun; Yang, Yongil; Pu, Yunqiao Green Chemistry, Vol. 19, Issue 22 https://doi.org/10.1039/C7GC02219K	journal	January 2017
Cinnamoyl CoA reductase, the first committed enzyme of the lignin branch biosynthetic pathway: cloning, expression and phylogenetic relationships Lacombe, Eric; Hawkins, Simon; Van Doorsselaere, Jan The Plant Journal, Vol. 11, Issue 3 https://doi.org/10.1046/j.1365-313X.1997.11030429.x	journal	March 1997
Syringyl lignin biosynthesis is directly regulated by a secondary cell wall master switch Zhao, Q.; Wang, H.; Yin, Y. Proceedings of the National Academy of Sciences, Vol. 107, Issue 32, p. 14496-14501 https://doi.org/10.1073/pnas.1009170107	journal	July 2010
Lignin content in natural Populus variants affects sugar release Studer, M. H.; DeMartini, J. D.; Davis, M. F. Proceedings of the National Academy of Sciences, Vol. 108, Issue 15, p. 6300-6305 https://doi.org/10.1073/pnas.1009252108	journal	March 2011
Syringyl lignin production in conifers: Proof of concept in a Pine tracheary element system Wagner, Armin; Tobimatsu, Yuki; Phillips, Lorelle Proceedings of the National Academy of Sciences, Vol. 112, Issue 19 https://doi.org/10.1073/pnas.1411926112	journal	April 2015
Nonlinear partial differential equations and applications: Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells Demura, T.; Tashiro, G.; Horiguchi, G. Proceedings of the National Academy of Sciences, Vol. 99, Issue 24 https://doi.org/10.1073/pnas.232590499	journal	November 2002
Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms Osakabe, K.; Tsao, C. C.; Li, L. Proceedings of the National Academy of Sciences, Vol. 96, Issue 16 https://doi.org/10.1073/pnas.96.16.8955	journal	August 1999
New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cytochrome P450-dependent monooxygenase Humphreys, J. M.; Hemm, M. R.; Chapple, C. Proceedings of the National Academy of Sciences, Vol. 96, Issue 18 https://doi.org/10.1073/pnas.96.18.10045	journal	August 1999
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 Meyermans, Hugo; Morreel, Kris; Lapierre, Catherine Journal of Biological Chemistry, Vol. 275, Issue 47, p. 36899-36909 https://doi.org/10.1074/jbc.M006915200	journal	August 2000
Molecular control of wood formation in trees Ye, Zheng-Hua; Zhong, Ruiqin Journal of Experimental Botany, Vol. 66, Issue 14 https://doi.org/10.1093/jxb/erv081	journal	March 2015
Phenylpropanoid Biosynthesis Vogt, Thomas Molecular Plant, Vol. 3, Issue 1 https://doi.org/10.1093/mp/ssp106	journal	January 2010
Global Analysis of Direct Targets of Secondary Wall NAC Master Switches in Arabidopsis Zhong, Ruiqin; Lee, Chanhui; Ye, Zheng-Hua Molecular Plant, Vol. 3, Issue 6 https://doi.org/10.1093/mp/ssq062	journal	November 2010
Phytozome: a comparative platform for green plant genomics Goodstein, David M.; Shu, Shengqiang; Howson, Russell Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr944	journal	November 2011
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
Multiple Classes of Transcription Factors Regulate the Expression of VASCULAR-RELATED NAC-DOMAIN7, a Master Switch of Xylem Vessel Differentiation Endo, Hitoshi; Yamaguchi, Masatoshi; Tamura, Taizo Plant and Cell Physiology, Vol. 56, Issue 2 https://doi.org/10.1093/pcp/pcu134	journal	September 2014
Secondary Cell Walls: Biosynthesis, Patterned Deposition and Transcriptional Regulation Zhong, Ruiqin; Ye, Zheng-Hua Plant and Cell Physiology, Vol. 56, Issue 2 https://doi.org/10.1093/pcp/pcu140	journal	October 2014
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Systematic Biology, Vol. 59, Issue 3 https://doi.org/10.1093/sysbio/syq010	journal	March 2010
Transcription switches for protoxylem and metaxylem vessel formation Kubo, M. Genes & Development, Vol. 19, Issue 16 https://doi.org/10.1101/gad.1331305	journal	August 2005
The Effects on Lignin Structure of Overexpression of Ferulate 5-Hydroxylase in Hybrid Poplar ¹ Stewart, Jaclyn J.; Akiyama, Takuya; Chapple, Clint Plant Physiology, Vol. 150, Issue 2 https://doi.org/10.1104/pp.109.137059	journal	April 2009
Functional Characterization of Poplar Wood-Associated NAC Domain Transcription Factors Zhong, Ruiqin; Lee, Chanhui; Ye, Zheng-Hua Plant Physiology, Vol. 152, Issue 2 https://doi.org/10.1104/pp.109.148270	journal	December 2009
VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 Effectively Induce Transdifferentiation into Xylem Vessel Elements under Control of an Induction System Yamaguchi, Masatoshi; Goué, Nadia; Igarashi, Hisako Plant Physiology, Vol. 153, Issue 3 https://doi.org/10.1104/pp.110.154013	journal	May 2010
Dissection of the Transcriptional Program Regulating Secondary Wall Biosynthesis during Wood Formation in Poplar Zhong, Ruiqin; McCarthy, Ryan L.; Lee, Chanhui Plant Physiology, Vol. 157, Issue 3 https://doi.org/10.1104/pp.111.181354	journal	September 2011
Essential Role of Caffeoyl Coenzyme A O -Methyltransferase in Lignin Biosynthesis in Woody Poplar Plants Zhong, Ruiqin; Morrison, W. Herbert; Himmelsbach, David S. Plant Physiology, Vol. 124, Issue 2 https://doi.org/10.1104/pp.124.2.563	journal	October 2000
CINNAMYL ALCOHOL DEHYDROGENASE-C and -D Are the Primary Genes Involved in Lignin Biosynthesis in the Floral Stem of Arabidopsis Sibout, Richard; Eudes, Aymerick; Mouille, Gregory The Plant Cell, Vol. 17, Issue 7 https://doi.org/10.1105/tpc.105.030767	journal	June 2005
The NAC Transcription Factors NST1 and NST2 of Arabidopsis Regulate Secondary Wall Thickenings and Are Required for Anther Dehiscence Mitsuda, Nobutaka; Seki, Motoaki; Shinozaki, Kazuo The Plant Cell, Vol. 17, Issue 11 https://doi.org/10.1105/tpc.105.036004	journal	October 2005
NAC Transcription Factors, NST1 and NST3, Are Key Regulators of the Formation of Secondary Walls in Woody Tissues of Arabidopsis Mitsuda, N.; Iwase, A.; Yamamoto, H. The Plant Cell, Vol. 19, Issue 1, p. 270-280 https://doi.org/10.1105/tpc.106.047043	journal	January 2007
SND1, a NAC Domain Transcription Factor, Is a Key Regulator of Secondary Wall Synthesis in Fibers of Arabidopsis Zhong, Ruiqin; Demura, Taku; Ye, Zheng-Hua The Plant Cell, Vol. 18, Issue 11 https://doi.org/10.1105/tpc.106.047399	journal	November 2006
The MYB46 Transcription Factor Is a Direct Target of SND1 and Regulates Secondary Wall Biosynthesis in Arabidopsis Zhong, R.; Richardson, E. A.; Ye, Z.-H. The Plant Cell Online, Vol. 19, Issue 9, p. 2776-2792 https://doi.org/10.1105/tpc.107.053678	journal	September 2007
MYB58 and MYB63 Are Transcriptional Activators of the Lignin Biosynthetic Pathway during Secondary Cell Wall Formation in Arabidopsis Zhou, Jianli; Lee, Chanhui; Zhong, Ruiqin The Plant Cell, Vol. 21, Issue 1 https://doi.org/10.1105/tpc.108.063321	journal	January 2009
Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 Directly Regulates the Genes That Govern Programmed Cell Death and Secondary Wall Formation during Xylem Differentiation Ohashi-Ito, Kyoko; Oda, Yoshihisa; Fukuda, Hiroo The Plant Cell, Vol. 22, Issue 10 https://doi.org/10.1105/tpc.110.075036	journal	October 2010
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 Pyo, Hyunjin; Demura, Taku; Fukuda, Hiroo The Plant Journal, Vol. 51, Issue 6 https://doi.org/10.1111/j.1365-313X.2007.03180.x	journal	August 2007
VASCULAR-RELATED NAC-DOMAIN 7 directly regulates the expression of a broad range of genes for xylem vessel formation: Direct target genes of VND7 Yamaguchi, Masatoshi; Mitsuda, Nobutaka; Ohtani, Misato The Plant Journal, Vol. 66, Issue 4 https://doi.org/10.1111/j.1365-313X.2011.04514.x	journal	March 2011
A NAC domain protein family contributing to the regulation of wood formation in poplar: NAC domain protein family regulates wood formation Ohtani, Misato; Nishikubo, Nobuyuki; Xu, Bo The Plant Journal, Vol. 67, Issue 3 https://doi.org/10.1111/j.1365-313X.2011.04614.x	journal	June 2011
Altered lignin biosynthesis using biotechnology to improve lignocellulosic biofuel feedstocks Poovaiah, Charleson R.; Nageswara-Rao, Madhugiri; Soneji, Jaya R. Plant Biotechnology Journal, Vol. 12, Issue 9 https://doi.org/10.1111/pbi.12225	journal	July 2014
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production Himmel, M. E.; Ding, S.-Y.; Johnson, D. K. Science, Vol. 315, Issue 5813, p. 804-807 https://doi.org/10.1126/science.1137016	journal	February 2007
Lignin Valorization: Improving Lignin Processing in the Biorefinery Ragauskas, A. J.; Beckham, G. T.; Biddy, M. J. Science, Vol. 344, Issue 6185, p. 1246843-1246843 https://doi.org/10.1126/science.1246843	journal	May 2014
Cellulosic Biofuels Carroll, Andrew; Somerville, Chris Annual Review of Plant Biology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.arplant.043008.092125	journal	June 2009
Lignin Biosynthesis Boerjan, Wout; Ralph, John; Baucher, Marie Annual Review of Plant Biology, Vol. 54, Issue 1, p. 519-546 https://doi.org/10.1146/annurev.arplant.54.031902.134938	journal	June 2003
Metabolic Channeling in Plants Winkel, Brenda S. J. Annual Review of Plant Biology, Vol. 55, Issue 1 https://doi.org/10.1146/annurev.arplant.55.031903.141714	journal	June 2004
Comprehensive Analysis of NAC Domain Transcription Factor Gene Family in Populus trichocarpa Hu, Ruibo; Qi, Guang; Kong, Yingzhen BMC Plant Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2229-10-145	journal	January 2010
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 Yang, Yongil; Yoo, Chang Geun; Guo, Hao-Bo Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0760-x	journal	March 2017
The Poplar MYB Master Switches Bind to the SMRE Site and Activate the Secondary Wall Biosynthetic Program during Wood Formation Zhong, Ruiqin; McCarthy, Ryan L.; Haghighat, Marziyeh PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0069219	journal	July 2013
Arabidopsis NAC Domain Proteins, VND1 to VND5, Are Transcriptional Regulators of Secondary Wall Biosynthesis in Vessels Zhou, Jianli; Zhong, Ruiqin; Ye, Zheng-Hua PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0105726	journal	August 2014
NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants Nakano, Yoshimi; Yamaguchi, Masatoshi; Endo, Hitoshi Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00288	journal	May 2015
The poplar PtrWNDs are transcriptional activators of secondary cell wall biosynthesis Zhong, Ruiqin; Ye, Zheng-Hua Plant Signaling & Behavior, Vol. 5, Issue 4 https://doi.org/10.4161/psb.5.4.11400	journal	April 2010

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59 BASIC BIOLOGICAL SCIENCES
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Poplus
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Sinapyl alcohol
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Title: PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus

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