Biomass formation and sugar release efficiency of Populus modified by altered expression of a NAC transcription factor

Raja S. Payyavula; Raghuram Badmi; Sara S. Jawdy; Miguel Rodriguez; Lee Gunter; Robert W. Sykes; Kimberly A. Winkeler; Cassandra M. Collins; William H. Rottmann; Jin Gui Chen; Xiaohan Yang; Gerald A. Tuskan; Udaya C. Kalluri

doi:10.1002/pld3.419

Biomass formation and sugar release efficiency of Populus modified by altered expression of a NAC transcription factor

Raja S. Payyavula, Raghuram Badmi, Sara S. Jawdy, Miguel Rodriguez, Lee Gunter, Robert W. Sykes, Kimberly A. Winkeler, Cassandra M. Collins, William H. Rottmann, Jin Gui Chen, Xiaohan Yang, Gerald A. Tuskan, Udaya C. Kalluri

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

Abstract

Woody biomass is an important feedstock for biofuel production. Manipulation of wood properties that enable efficient conversion of biomass to biofuel reduces cost of biofuel production. Wood cell wall composition is regulated at several levels that involve expression of transcription factors such as wood-/secondary cell wall-associated NAC domains (WND or SND). In Arabidopsis thaliana, SND1 regulates cell wall composition through activation of its down-stream targets such as MYBs. The functional aspects of SND1 homologs in the woody Populus have been studied through transgenic manipulation. In this study, we investigated the role of PdWND1B, Populus SND1 sequence ortholog, in wood formation using transgenic manipulation through over-expression or silencing under the control of a vascular-specific 4-coumarate-CoA ligase (4CL) promoter. As compared with control plants, PdWND1B-RNAi plants were shorter in height, with significantly reduced stem diameter and dry biomass, whereas there were no significant differences in growth and productivity of PdWND1B over-expression plants. Conversely, PdWND1B over-expression lines showed a significant reduction in cellulose and increase in lignin content, whereas there was no significant impact on lignin content of downregulated lines. Stem carbohydrate composition analysis revealed a decrease in glucose, mannose, arabinose, and galactose, but an increase in xylose in the over-expression lines. Transcriptome analysis revealed upregulation of several downstream transcription factors and secondary cell wall related structural genes in the PdWND1B over-expression lines, partly explaining the observed phenotypic changes in cell wall chemistry. Relative to the control, glucose release efficiency and ethanol production from stem biomass was significantly reduced in over-expression lines. Our results show that PdWND1B is an important factor determining biomass productivity, cell wall chemistry and its conversion to biofuels in Populus.

Original language	English
Article number	e419
Journal	Plant Direct
Volume	6
Issue number	8
DOIs	https://doi.org/10.1002/pld3.419
State	Published - Aug 2022

Funding

We thank Brock Carter and Zackary Moore for inventory, propagation, and maintenance of plants in ORNL greenhouses. This manuscript has been authored by UT-Battelle, LLC under Contract No. DE-AC05-00OR22725 with the U.S. Department of Energy. The U.S. Government retains, and the publisher, by accepting the article for publication, acknowledges that the U.S. Government retains a non-exclusive, paid-up, irrevocable, world-wide license to publish or reproduce the published form of this manuscript, or allow others to do so, for U.S. Government purposes. The Department of Energy will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan (http://energy.gov/downloads/doe-public-access-plan). This work was supported by the U.S. Department of Energy (DOE) BioEnergy Science Center and Center for Bioenergy Innovation projects. The BioEnergy Science Center and Center for Bioenergy Innovation are a Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. This manuscript has been authored by UT‐Battelle, LLC under Contract No. DE‐AC05‐00OR22725 with the U.S. Department of Energy. Funding information 4CL 4‐ ‐CoA CCR CesA COMT O GT43 KOR PAL SUSY

Funders	Funder number
BioEnergy Science Center and Center for Bioenergy Innovation
BioEnergy Science Center and Center for Bioenergy Innovation are a Bioenergy Research Center
DOE Public Access Plan
U.S. Government
U.S. Department of Energy
Office of Science
Biological and Environmental Research
Oak Ridge National Laboratory	DE-AC05-00OR22725

Keywords

MYB
NAC transcription factor
SND
WND1B
biomass
cell wall
cellulose
lignin
sugar release

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1002/pld3.419

Cite this

Payyavula, R. S., Badmi, R., Jawdy, S. S., Rodriguez, M., Gunter, L., Sykes, R. W., Winkeler, K. A., Collins, C. M., Rottmann, W. H., Chen, J. G., Yang, X., Tuskan, G. A., & Kalluri, U. C. (2022). Biomass formation and sugar release efficiency of Populus modified by altered expression of a NAC transcription factor. Plant Direct, 6(8), Article e419. https://doi.org/10.1002/pld3.419

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abstract = "Woody biomass is an important feedstock for biofuel production. Manipulation of wood properties that enable efficient conversion of biomass to biofuel reduces cost of biofuel production. Wood cell wall composition is regulated at several levels that involve expression of transcription factors such as wood-/secondary cell wall-associated NAC domains (WND or SND). In Arabidopsis thaliana, SND1 regulates cell wall composition through activation of its down-stream targets such as MYBs. The functional aspects of SND1 homologs in the woody Populus have been studied through transgenic manipulation. In this study, we investigated the role of PdWND1B, Populus SND1 sequence ortholog, in wood formation using transgenic manipulation through over-expression or silencing under the control of a vascular-specific 4-coumarate-CoA ligase (4CL) promoter. As compared with control plants, PdWND1B-RNAi plants were shorter in height, with significantly reduced stem diameter and dry biomass, whereas there were no significant differences in growth and productivity of PdWND1B over-expression plants. Conversely, PdWND1B over-expression lines showed a significant reduction in cellulose and increase in lignin content, whereas there was no significant impact on lignin content of downregulated lines. Stem carbohydrate composition analysis revealed a decrease in glucose, mannose, arabinose, and galactose, but an increase in xylose in the over-expression lines. Transcriptome analysis revealed upregulation of several downstream transcription factors and secondary cell wall related structural genes in the PdWND1B over-expression lines, partly explaining the observed phenotypic changes in cell wall chemistry. Relative to the control, glucose release efficiency and ethanol production from stem biomass was significantly reduced in over-expression lines. Our results show that PdWND1B is an important factor determining biomass productivity, cell wall chemistry and its conversion to biofuels in Populus.",

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author = "Payyavula, {Raja S.} and Raghuram Badmi and Jawdy, {Sara S.} and Miguel Rodriguez and Lee Gunter and Sykes, {Robert W.} and Winkeler, {Kimberly A.} and Collins, {Cassandra M.} and Rottmann, {William H.} and Chen, {Jin Gui} and Xiaohan Yang and Tuskan, {Gerald A.} and Kalluri, {Udaya C.}",

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AU - Payyavula, Raja S.

AU - Badmi, Raghuram

AU - Jawdy, Sara S.

AU - Rodriguez, Miguel

AU - Gunter, Lee

AU - Sykes, Robert W.

AU - Winkeler, Kimberly A.

AU - Collins, Cassandra M.

AU - Rottmann, William H.

AU - Chen, Jin Gui

AU - Yang, Xiaohan

AU - Tuskan, Gerald A.

AU - Kalluri, Udaya C.

N1 - Publisher Copyright: © 2022 Oak Ridge National Laboratory, managed by UT- Battelle, LLC and The Authors. Plant Direct published by American Society of Plant Biologists and the Society for Experimental Biology and John Wiley & Sons Ltd.

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Y1 - 2022/8

N2 - Woody biomass is an important feedstock for biofuel production. Manipulation of wood properties that enable efficient conversion of biomass to biofuel reduces cost of biofuel production. Wood cell wall composition is regulated at several levels that involve expression of transcription factors such as wood-/secondary cell wall-associated NAC domains (WND or SND). In Arabidopsis thaliana, SND1 regulates cell wall composition through activation of its down-stream targets such as MYBs. The functional aspects of SND1 homologs in the woody Populus have been studied through transgenic manipulation. In this study, we investigated the role of PdWND1B, Populus SND1 sequence ortholog, in wood formation using transgenic manipulation through over-expression or silencing under the control of a vascular-specific 4-coumarate-CoA ligase (4CL) promoter. As compared with control plants, PdWND1B-RNAi plants were shorter in height, with significantly reduced stem diameter and dry biomass, whereas there were no significant differences in growth and productivity of PdWND1B over-expression plants. Conversely, PdWND1B over-expression lines showed a significant reduction in cellulose and increase in lignin content, whereas there was no significant impact on lignin content of downregulated lines. Stem carbohydrate composition analysis revealed a decrease in glucose, mannose, arabinose, and galactose, but an increase in xylose in the over-expression lines. Transcriptome analysis revealed upregulation of several downstream transcription factors and secondary cell wall related structural genes in the PdWND1B over-expression lines, partly explaining the observed phenotypic changes in cell wall chemistry. Relative to the control, glucose release efficiency and ethanol production from stem biomass was significantly reduced in over-expression lines. Our results show that PdWND1B is an important factor determining biomass productivity, cell wall chemistry and its conversion to biofuels in Populus.

AB - Woody biomass is an important feedstock for biofuel production. Manipulation of wood properties that enable efficient conversion of biomass to biofuel reduces cost of biofuel production. Wood cell wall composition is regulated at several levels that involve expression of transcription factors such as wood-/secondary cell wall-associated NAC domains (WND or SND). In Arabidopsis thaliana, SND1 regulates cell wall composition through activation of its down-stream targets such as MYBs. The functional aspects of SND1 homologs in the woody Populus have been studied through transgenic manipulation. In this study, we investigated the role of PdWND1B, Populus SND1 sequence ortholog, in wood formation using transgenic manipulation through over-expression or silencing under the control of a vascular-specific 4-coumarate-CoA ligase (4CL) promoter. As compared with control plants, PdWND1B-RNAi plants were shorter in height, with significantly reduced stem diameter and dry biomass, whereas there were no significant differences in growth and productivity of PdWND1B over-expression plants. Conversely, PdWND1B over-expression lines showed a significant reduction in cellulose and increase in lignin content, whereas there was no significant impact on lignin content of downregulated lines. Stem carbohydrate composition analysis revealed a decrease in glucose, mannose, arabinose, and galactose, but an increase in xylose in the over-expression lines. Transcriptome analysis revealed upregulation of several downstream transcription factors and secondary cell wall related structural genes in the PdWND1B over-expression lines, partly explaining the observed phenotypic changes in cell wall chemistry. Relative to the control, glucose release efficiency and ethanol production from stem biomass was significantly reduced in over-expression lines. Our results show that PdWND1B is an important factor determining biomass productivity, cell wall chemistry and its conversion to biofuels in Populus.

KW - MYB

KW - NAC transcription factor

KW - SND

KW - WND1B

KW - biomass

KW - cell wall

KW - cellulose

KW - lignin

KW - sugar release

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Biomass formation and sugar release efficiency of Populus modified by altered expression of a NAC transcription factor

Abstract

Funding

Keywords

UN SDGs

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