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Title: Finding New Cell Wall Regulatory Genes in Populus trichocarpa Using Multiple Lines of Evidence

Abstract

Understanding the regulatory network controlling cell wall biosynthesis is of great interest in Populus trichocarpa, both because of its status as a model woody perennial and its importance for lignocellulosic products. We searched for genes with putatively unknown roles in regulating cell wall biosynthesis using an extended network-based Lines of Evidence (LOE) pipeline to combine multiple omics data sets in P. trichocarpa, including gene coexpression, gene comethylation, population level pairwise SNP correlations, and two distinct SNP-metabolite Genome Wide Association Study (GWAS) layers. By incorporating validation, ranking, and filtering approaches we produced a list of nine high priority gene candidates for involvement in the regulation of cell wall biosynthesis. We subsequently performed a detailed investigation of candidate gene GROWTH-REGULATING FACTOR 9 (PtGRF9). To investigate the role of PtGRF9 in regulating cell wall biosynthesis, we assessed the genome-wide connections of PtGRF9 and a paralog across data layers with functional enrichment analyses, predictive transcription factor binding site analysis, and an independent comparison to eQTN data. Our findings indicate that PtGRF9 likely affects the cell wall by directly repressing genes involved in cell wall biosynthesis, such as PtCCoAOMT and PtMYB.41, and indirectly by regulating homeobox genes. Furthermore, evidence suggests that PtGRF9 paralogs may actmore » as transcriptional co-regulators that direct the global energy usage of the plant. Using our extended pipeline, we show multiple lines of evidence implicating the involvement of these genes in cell wall regulatory functions and demonstrate the value of this method for prioritizing candidate genes for experimental validation.« less

Authors:
 [1];  [2];  [1];  [3];  [1]; ORCiD logo [4];  [1]; ORCiD logo [2]; ORCiD logo [5];  [2];  [2];  [6];  [7];  [8];  [9];  [10];  [2];  [11];  [11];  [9] more »; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [1] « less
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Oak Ridge Associated Univ. (ORAU), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Oak Ridge Associated Univ. (ORAU), Oak Ridge, TN (United States); Johns Hopkins Univ., Baltimore, MD (United States)
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF)
  6. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States). Univ. of Tennessee Inst. of Agriculture
  7. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
  8. HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
  9. West Virginia Univ., Morgantown, WV (United States)
  10. Univ. of Tennessee, Knoxville, TN (United States). Univ. of Tennessee Inst. of Agriculture
  11. Univ. of North Texas, Denton, TX (United States). BioDiscovery Inst.
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1633173
Alternate Identifier(s):
OSTI ID: 1616073
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 10; Journal Issue: n/a; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; lines of evidence; cell wall; regulation; Genome Wide Association Study; candidate gene identification; network analysis; multi-omic; Populus trichocarpa

Citation Formats

Furches, Anna K., Kainer, David, Weighill, Deborah, Large, Annabel L., Jones, Piet C., Walker, Angelica M., Romero, Jonathon C., Gazolla, Joao Gabriel Felipe Machado, Joubert, Wayne, Shah, Manesh, Streich, Jared C., Ranjan, Priya, Schmutz, Jeremy, Sreedasyam, Avinash, Macaya-Sanz, David, Zhao, Nan, Martin, Madhavi Z., Rao, Xiaolan, Dixon, Richard A., DiFazio, Stephen, Tschaplinski, Timothy J., Chen, Jin-Gui, Tuskan, Gerald A., and Jacobson, Daniel A. Finding New Cell Wall Regulatory Genes in Populus trichocarpa Using Multiple Lines of Evidence. United States: N. p., 2019. Web. doi:10.3389/fpls.2019.01249.
Furches, Anna K., Kainer, David, Weighill, Deborah, Large, Annabel L., Jones, Piet C., Walker, Angelica M., Romero, Jonathon C., Gazolla, Joao Gabriel Felipe Machado, Joubert, Wayne, Shah, Manesh, Streich, Jared C., Ranjan, Priya, Schmutz, Jeremy, Sreedasyam, Avinash, Macaya-Sanz, David, Zhao, Nan, Martin, Madhavi Z., Rao, Xiaolan, Dixon, Richard A., DiFazio, Stephen, Tschaplinski, Timothy J., Chen, Jin-Gui, Tuskan, Gerald A., & Jacobson, Daniel A. Finding New Cell Wall Regulatory Genes in Populus trichocarpa Using Multiple Lines of Evidence. United States. https://doi.org/10.3389/fpls.2019.01249
Furches, Anna K., Kainer, David, Weighill, Deborah, Large, Annabel L., Jones, Piet C., Walker, Angelica M., Romero, Jonathon C., Gazolla, Joao Gabriel Felipe Machado, Joubert, Wayne, Shah, Manesh, Streich, Jared C., Ranjan, Priya, Schmutz, Jeremy, Sreedasyam, Avinash, Macaya-Sanz, David, Zhao, Nan, Martin, Madhavi Z., Rao, Xiaolan, Dixon, Richard A., DiFazio, Stephen, Tschaplinski, Timothy J., Chen, Jin-Gui, Tuskan, Gerald A., and Jacobson, Daniel A. Tue . "Finding New Cell Wall Regulatory Genes in Populus trichocarpa Using Multiple Lines of Evidence". United States. https://doi.org/10.3389/fpls.2019.01249. https://www.osti.gov/servlets/purl/1633173.
@article{osti_1633173,
title = {Finding New Cell Wall Regulatory Genes in Populus trichocarpa Using Multiple Lines of Evidence},
author = {Furches, Anna K. and Kainer, David and Weighill, Deborah and Large, Annabel L. and Jones, Piet C. and Walker, Angelica M. and Romero, Jonathon C. and Gazolla, Joao Gabriel Felipe Machado and Joubert, Wayne and Shah, Manesh and Streich, Jared C. and Ranjan, Priya and Schmutz, Jeremy and Sreedasyam, Avinash and Macaya-Sanz, David and Zhao, Nan and Martin, Madhavi Z. and Rao, Xiaolan and Dixon, Richard A. and DiFazio, Stephen and Tschaplinski, Timothy J. and Chen, Jin-Gui and Tuskan, Gerald A. and Jacobson, Daniel A.},
abstractNote = {Understanding the regulatory network controlling cell wall biosynthesis is of great interest in Populus trichocarpa, both because of its status as a model woody perennial and its importance for lignocellulosic products. We searched for genes with putatively unknown roles in regulating cell wall biosynthesis using an extended network-based Lines of Evidence (LOE) pipeline to combine multiple omics data sets in P. trichocarpa, including gene coexpression, gene comethylation, population level pairwise SNP correlations, and two distinct SNP-metabolite Genome Wide Association Study (GWAS) layers. By incorporating validation, ranking, and filtering approaches we produced a list of nine high priority gene candidates for involvement in the regulation of cell wall biosynthesis. We subsequently performed a detailed investigation of candidate gene GROWTH-REGULATING FACTOR 9 (PtGRF9). To investigate the role of PtGRF9 in regulating cell wall biosynthesis, we assessed the genome-wide connections of PtGRF9 and a paralog across data layers with functional enrichment analyses, predictive transcription factor binding site analysis, and an independent comparison to eQTN data. Our findings indicate that PtGRF9 likely affects the cell wall by directly repressing genes involved in cell wall biosynthesis, such as PtCCoAOMT and PtMYB.41, and indirectly by regulating homeobox genes. Furthermore, evidence suggests that PtGRF9 paralogs may act as transcriptional co-regulators that direct the global energy usage of the plant. Using our extended pipeline, we show multiple lines of evidence implicating the involvement of these genes in cell wall regulatory functions and demonstrate the value of this method for prioritizing candidate genes for experimental validation.},
doi = {10.3389/fpls.2019.01249},
journal = {Frontiers in Plant Science},
number = n/a,
volume = 10,
place = {United States},
year = {Tue Oct 08 00:00:00 EDT 2019},
month = {Tue Oct 08 00:00:00 EDT 2019}
}

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Cited by: 7 works
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Figures / Tables:

FIGURE 1 FIGURE 1: Overview of the method for identifying new candidate genes involved in cell wall regulation through data layering and calculation of LOE scores.

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Works referencing / citing this record:

A High-Performance Computing Implementation of Iterative Random Forest for the Creation of Predictive Expression Networks
journal, December 2019


A High-Performance Computing Implementation of Iterative Random Forest for the Creation of Predictive Expression Networks
journal, December 2019


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.