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 · 11 November 2019 · BMC Plant Biology

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

Yang, Yongil ^[1]; Yoo, Chang Geun ^[2]; Rottmann, William ^[3]; Winkeler, Kimberly A. ^[3]; Collins, Cassandra M. ^[3]; Gunter, Lee E. ^[4]; Jawdy, Sara S. ^[4]; Yang, Xiaohan ^[4]; Pu, Yunqiao ^[2]; Ragauskas, Arthur J. ^[5]; Tuskan, Gerald A. ^[4];

^[4]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). UT-Oak Ridge Institute for Biological Science
ArborGen, Inc., Ridgeville, SC (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). UT-Oak Ridge Institute for Biological Science; Univ. of Tennessee, Knoxville, TN (United States). Department of Chemical and Biomolecular Engineering & Department of Forestry, Wildlife, and Fisheries

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. 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 Office of Science (SC), Biological and Environmental Research (BER); USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1618609

Alternate ID(s):: OSTI ID: 1626852; OSTI ID: 1761683

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

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 44 works

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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
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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
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
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
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
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
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
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
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
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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
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
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 [Supplemental Data] Yang, Yongil; Yoo, Chang; Guo, Hao-Bo figshare-Supplementary information for journal article at DOI: 10.1186/s13068-017-0760-x, 8 files https://doi.org/10.6084/m9.figshare.c.3725197	collection	March 2017

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59 BASIC BIOLOGICAL SCIENCES
Plant Sciences
F5H
Lignin
Poplus
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VND

MOESM5 of PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus Yang, Yongil; Yoo, Chang; Rottmann, William https://doi.org/10.6084/m9.figshare.10287958.v1 The current record is supplemented by this text	text	January 2019
PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus Yang, Yongil; Yoo, Chang; Rottmann, William https://doi.org/10.6084/m9.figshare.c.4734306 The current record is supplemented by this collection	collection	January 2019
MOESM1 of PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus Yang, Yongil; Yoo, Chang; Rottmann, William https://doi.org/10.6084/m9.figshare.10287934 The current record is supplemented by this dataset	dataset	January 2019
MOESM3 of PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus Yang, Yongil; Yoo, Chang; Rottmann, William https://doi.org/10.6084/m9.figshare.10287946.v1 The current record is supplemented by this audiovisual	audiovisual	January 2019
MOESM3 of PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus Yang, Yongil; Yoo, Chang; Rottmann, William https://doi.org/10.6084/m9.figshare.10287946 The current record is supplemented by this audiovisual	audiovisual	January 2019
MOESM4 of PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus Yang, Yongil; Yoo, Chang; Rottmann, William https://doi.org/10.6084/m9.figshare.10287952 The current record is supplemented by this text	text	January 2019
PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus Yang, Yongil; Yoo, Chang; Rottmann, William https://doi.org/10.6084/m9.figshare.c.4734306.v1 The current record is supplemented by this collection	collection	January 2019
MOESM1 of PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus Yang, Yongil; Yoo, Chang; Rottmann, William https://doi.org/10.6084/m9.figshare.10287934.v1 The current record is supplemented by this dataset	dataset	January 2019
MOESM2 of PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus Yang, Yongil; Yoo, Chang; Rottmann, William https://doi.org/10.6084/m9.figshare.10287940.v1 The current record is supplemented by this text	text	January 2019
MOESM2 of PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus Yang, Yongil; Yoo, Chang; Rottmann, William https://doi.org/10.6084/m9.figshare.10287940 The current record is supplemented by this text	text	January 2019
MOESM4 of PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus Yang, Yongil; Yoo, Chang; Rottmann, William https://doi.org/10.6084/m9.figshare.10287952.v1 The current record is supplemented by this text	text	January 2019
MOESM5 of PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus Yang, Yongil; Yoo, Chang; Rottmann, William https://doi.org/10.6084/m9.figshare.10287958 The current record is supplemented by this text	text	January 2019

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

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