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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:
 [1];  [1];  [1];  [1];  [2];  [1];  [1];  [3];  [3];  [1];  [4];  [4];  [1];  [5];  [5];  [1];  [1];  [1];  [6];  [6] more »;  [7];  [7];  [8];  [2];  [1];  [1];  [1];  [1];  [1] « less
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Univ. of Tennessee, Knoxville, TN (United States)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Univ. of North Texas, Denton, TX (United States)
  5. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  6. West Virginia Univ., Morgantown, WV (United States)
  7. ArborGen Inc., Ridgeville, SC (United States)
  8. HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1457659
Alternate Identifier(s):
OSTI ID: 1441118
Report Number(s):
NREL/JA-2700-71648
Journal ID: ISSN 1040-4651
Grant/Contract Number:
AC36-08GO28308
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Plant Cell
Additional Journal Information:
Journal Name: Plant Cell; 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 L., Guo, Hao-bo, Zhang, Jin, Tschaplinski, Timothy, Singan, Vasanth R., Lindquist, Erika, Payyavula, Raja S., Barros-Rios, Jaime, Dixon, Richard A., Engle, Nancy, Sykes, Robert W., Davis, Mark, Jawdy, Sara, Gunter, Lee E., Thompson, Olivia, DiFazio, Stephen P., Evans, Luke M., Winkler, 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. doi:10.1105/tpc.18.00168.
Xie, Meng, Muchero, Wellington, Bryan, Anthony C., Yee, Kelsey L., Guo, Hao-bo, Zhang, Jin, Tschaplinski, Timothy, Singan, Vasanth R., Lindquist, Erika, Payyavula, Raja S., Barros-Rios, Jaime, Dixon, Richard A., Engle, Nancy, Sykes, Robert W., Davis, Mark, Jawdy, Sara, Gunter, Lee E., Thompson, Olivia, DiFazio, Stephen P., Evans, Luke M., Winkler, 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. doi:10.1105/tpc.18.00168.
Xie, Meng, Muchero, Wellington, Bryan, Anthony C., Yee, Kelsey L., Guo, Hao-bo, Zhang, Jin, Tschaplinski, Timothy, Singan, Vasanth R., Lindquist, Erika, Payyavula, Raja S., Barros-Rios, Jaime, Dixon, Richard A., Engle, Nancy, Sykes, Robert W., Davis, Mark, Jawdy, Sara, Gunter, Lee E., Thompson, Olivia, DiFazio, Stephen P., Evans, Luke M., Winkler, 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. doi:10.1105/tpc.18.00168. https://www.osti.gov/servlets/purl/1457659.
@article{osti_1457659,
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 L. and Guo, Hao-bo and Zhang, Jin and Tschaplinski, Timothy and Singan, Vasanth R. and Lindquist, Erika and Payyavula, Raja S. and Barros-Rios, Jaime and Dixon, Richard A. and Engle, Nancy and Sykes, Robert W. and Davis, Mark and Jawdy, Sara and Gunter, Lee E. and Thompson, Olivia and DiFazio, Stephen P. and Evans, Luke M. and Winkler, 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 = ,
volume = ,
place = {United States},
year = {Mon Jun 11 00:00:00 EDT 2018},
month = {Mon Jun 11 00:00:00 EDT 2018}
}

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