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Title: A 5-Enolpyruvylshikimate 3-Phosphate Synthase Functions as a Transcriptional Repressor in Populus

Abstract

Long-lived perennial plants, with distinctive habits of inter-annual growth, defense, and physiology, are of great economic and ecological importance. However, some biological mechanisms resulting from genome duplication and functional divergence of genes in these systems remain poorly studied. Here, we discovered an association between a poplar (Populus trichocarpa) 5-enolpyruvylshikimate 3-phosphate synthase gene (PtrEPSP) and lignin biosynthesis. Functional characterization of PtrEPSP revealed that this isoform possesses a helix-turn-helix motif in the N terminus and can function as a transcriptional repressor that regulates expression of genes in the phenylpropanoid pathway in addition to performing its canonical biosynthesis function in the shikimate pathway. We demonstrated that this isoform can localize in the nucleus and specifically binds to the promoter and represses the expression of a SLEEPER-like transcriptional regulator, which itself specifically binds to the promoter and represses the expression of PtrMYB021 (known as MYB46 in Arabidopsis thaliana), a master regulator of the phenylpropanoid pathway and lignin biosynthesis. Analyses of overexpression and RNAi lines targeting PtrEPSP confirmed the predicted changes in PtrMYB021 expression patterns. These results demonstrate that PtrEPSP in its regulatory form and PtrhAT form a transcriptional hierarchy regulating phenylpropanoid pathway and lignin biosynthesis in Populus.

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [3]; ORCiD logo [3]; ORCiD logo [1]; ORCiD logo [4]; ORCiD logo [4]; ORCiD logo [1]; ORCiD logo [5]; ORCiD logo [5]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [6]; ORCiD logo [6] more »; ORCiD logo [7]; ORCiD logo [7]; ORCiD logo [8]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [9] « less
  1. BioEnergy Science Center and Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831
  2. Department of Biochemistry and Cellular and Molecular Biology, University of Tennessee, Knoxville, Tennessee 37996
  3. U.S. Department of Energy Joint Genome Institute, Walnut Creek, California 94598
  4. BioDiscovery Institute and Department of Biological Sciences, University of North Texas, Denton, Texas 76203
  5. Bioscience Center, National Renewable Energy Laboratory, Golden, Colorado 80401
  6. Department of Biology, West Virginia University, Morgantown, West Virginia 26506
  7. ArborGen, Ridgeville, South Carolina 29472
  8. U.S. Department of Energy Joint Genome Institute, Walnut Creek, California 94598, HudsonAlpha Institute for Biotechnology, Huntsville, Alabama 35806
  9. BioEnergy Science Center and Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, U.S. Department of Energy Joint Genome Institute, Walnut Creek, California 94598
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1441118
Alternate Identifier(s):
OSTI ID: 1457659; OSTI ID: 1474739; OSTI ID: 1616062
Report Number(s):
NREL/JA-2700-71648
Journal ID: ISSN 1040-4651; /plantcell/30/7/1645.atom
Grant/Contract Number:  
AC05-00OR22725; AC36-08GO28308
Resource Type:
Published Article
Journal Name:
Plant Cell
Additional Journal Information:
Journal Name: Plant Cell Journal Volume: 30 Journal Issue: 7; Journal ID: ISSN 1040-4651
Publisher:
American Society of Plant Biologists
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; poplar; lignin biosynthesis; transcriptional repressors; populus

Citation Formats

Xie, Meng, Muchero, Wellington, Bryan, Anthony C., Yee, Kelsey, Guo, Hao-Bo, Zhang, Jin, Tschaplinski, Timothy J., Singan, Vasanth R., Lindquist, Erika, Payyavula, Raja S., Barros-Rios, Jaime, Dixon, Richard, Engle, Nancy, Sykes, Robert W., Davis, Mark, Jawdy, Sara S., Gunter, Lee E., Thompson, Olivia, DiFazio, Stephen P., Evans, Luke M., Winkeler, Kim, Collins, Cassandra, Schmutz, Jeremy, Guo, Hong, Kalluri, Udaya, Rodriguez, Miguel, Feng, Kai, Chen, Jin-Gui, and Tuskan, Gerald A. A 5-Enolpyruvylshikimate 3-Phosphate Synthase Functions as a Transcriptional Repressor in Populus. United States: N. p., 2018. Web. https://doi.org/10.1105/tpc.18.00168.
Xie, Meng, Muchero, Wellington, Bryan, Anthony C., Yee, Kelsey, Guo, Hao-Bo, Zhang, Jin, Tschaplinski, Timothy J., Singan, Vasanth R., Lindquist, Erika, Payyavula, Raja S., Barros-Rios, Jaime, Dixon, Richard, Engle, Nancy, Sykes, Robert W., Davis, Mark, Jawdy, Sara S., Gunter, Lee E., Thompson, Olivia, DiFazio, Stephen P., Evans, Luke M., Winkeler, Kim, Collins, Cassandra, Schmutz, Jeremy, Guo, Hong, Kalluri, Udaya, Rodriguez, Miguel, Feng, Kai, Chen, Jin-Gui, & Tuskan, Gerald A. A 5-Enolpyruvylshikimate 3-Phosphate Synthase Functions as a Transcriptional Repressor in Populus. United States. https://doi.org/10.1105/tpc.18.00168
Xie, Meng, Muchero, Wellington, Bryan, Anthony C., Yee, Kelsey, Guo, Hao-Bo, Zhang, Jin, Tschaplinski, Timothy J., Singan, Vasanth R., Lindquist, Erika, Payyavula, Raja S., Barros-Rios, Jaime, Dixon, Richard, Engle, Nancy, Sykes, Robert W., Davis, Mark, Jawdy, Sara S., Gunter, Lee E., Thompson, Olivia, DiFazio, Stephen P., Evans, Luke M., Winkeler, Kim, Collins, Cassandra, Schmutz, Jeremy, Guo, Hong, Kalluri, Udaya, Rodriguez, Miguel, Feng, Kai, Chen, Jin-Gui, and Tuskan, Gerald A. Mon . "A 5-Enolpyruvylshikimate 3-Phosphate Synthase Functions as a Transcriptional Repressor in Populus". United States. https://doi.org/10.1105/tpc.18.00168.
@article{osti_1441118,
title = {A 5-Enolpyruvylshikimate 3-Phosphate Synthase Functions as a Transcriptional Repressor in Populus},
author = {Xie, Meng and Muchero, Wellington and Bryan, Anthony C. and Yee, Kelsey and Guo, Hao-Bo and Zhang, Jin and Tschaplinski, Timothy J. and Singan, Vasanth R. and Lindquist, Erika and Payyavula, Raja S. and Barros-Rios, Jaime and Dixon, Richard and Engle, Nancy and Sykes, Robert W. and Davis, Mark and Jawdy, Sara S. and Gunter, Lee E. and Thompson, Olivia and DiFazio, Stephen P. and Evans, Luke M. and Winkeler, Kim and Collins, Cassandra and Schmutz, Jeremy and Guo, Hong and Kalluri, Udaya and Rodriguez, Miguel and Feng, Kai and Chen, Jin-Gui and Tuskan, Gerald A.},
abstractNote = {Long-lived perennial plants, with distinctive habits of inter-annual growth, defense, and physiology, are of great economic and ecological importance. However, some biological mechanisms resulting from genome duplication and functional divergence of genes in these systems remain poorly studied. Here, we discovered an association between a poplar (Populus trichocarpa) 5-enolpyruvylshikimate 3-phosphate synthase gene (PtrEPSP) and lignin biosynthesis. Functional characterization of PtrEPSP revealed that this isoform possesses a helix-turn-helix motif in the N terminus and can function as a transcriptional repressor that regulates expression of genes in the phenylpropanoid pathway in addition to performing its canonical biosynthesis function in the shikimate pathway. We demonstrated that this isoform can localize in the nucleus and specifically binds to the promoter and represses the expression of a SLEEPER-like transcriptional regulator, which itself specifically binds to the promoter and represses the expression of PtrMYB021 (known as MYB46 in Arabidopsis thaliana), a master regulator of the phenylpropanoid pathway and lignin biosynthesis. Analyses of overexpression and RNAi lines targeting PtrEPSP confirmed the predicted changes in PtrMYB021 expression patterns. These results demonstrate that PtrEPSP in its regulatory form and PtrhAT form a transcriptional hierarchy regulating phenylpropanoid pathway and lignin biosynthesis in Populus.},
doi = {10.1105/tpc.18.00168},
journal = {Plant Cell},
number = 7,
volume = 30,
place = {United States},
year = {2018},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1105/tpc.18.00168

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