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Title: An Arabidopsis gene regulatory network for secondary cell wall synthesis

Abstract

The plant cell wall is an important factor for determining cell shape, function and response to the environment. Secondary cell walls, such as those found in xylem, are composed of cellulose, hemicelluloses and lignin and account for the bulk of plant biomass. The coordination between transcriptional regulation of synthesis for each polymer is complex and vital to cell function. A regulatory hierarchy of developmental switches has been proposed, although the full complement of regulators remains unknown. In this paper, we present a protein–DNA network between Arabidopsis thaliana transcription factors and secondary cell wall metabolic genes with gene expression regulated by a series of feed-forward loops. This model allowed us to develop and validate new hypotheses about secondary wall gene regulation under abiotic stress. Distinct stresses are able to perturb targeted genes to potentially promote functional adaptation. Finally, these interactions will serve as a foundation for understanding the regulation of a complex, integral plant component.

Authors:
 [1];  [2];  [1];  [1];  [1];  [1];  [2];  [2];  [2];  [2];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [3];  [5];  [4] more »;  [6];  [9];  [9];  [10];  [9];  [2];  [1] « less
  1. Univ. of California, Davis, CA (United States). Dept. of Plant Biology and Genome Center
  2. Univ. of Massachusetts, Amherst, MA (United States). Biology Dept.
  3. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  4. Univ. of California, Davis, CA (United States). Dept. of Plant Biology
  5. Univ. of California, Davis, CA (United States). Dept. of Plant Sciences
  6. Univ. of California, Davis, CA (United States). Genome Center and Dept. of Computer Science
  7. Cold Spring Harbor Lab., NY (United States)
  8. Cold Spring Harbor Lab., NY (United States); US Dept. of Agriculture (USDA)., Ithaca, NY (United States)
  9. Univ. of California, San Diego, CA (United States). Section of Cell and Developmental Biology
  10. Univ. of Cambridge (United Kingdom). Theory of Condensed Matter Group
Publication Date:
Research Org.:
Univ. of Massachusetts, Amherst, MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1347111
Grant/Contract Number:  
FG02-08ER64700
Resource Type:
Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 517; Journal Issue: 7536; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; regulatory networks; plant development

Citation Formats

Taylor-Teeples, M., Lin, L., de Lucas, M., Turco, G., Toal, T. W., Gaudinier, A., Young, N. F., Trabucco, G. M., Veling, M. T., Lamothe, R., Handakumbura, P. P., Xiong, G., Wang, C., Corwin, J., Tsoukalas, A., Zhang, L., Ware, D., Pauly, M., Kliebenstein, D. J., Dehesh, K., Tagkopoulos, I., Breton, G., Pruneda-Paz, J. L., Ahnert, S. E., Kay, S. A., Hazen, S. P., and Brady, S. M. An Arabidopsis gene regulatory network for secondary cell wall synthesis. United States: N. p., 2014. Web. doi:10.1038/nature14099.
Taylor-Teeples, M., Lin, L., de Lucas, M., Turco, G., Toal, T. W., Gaudinier, A., Young, N. F., Trabucco, G. M., Veling, M. T., Lamothe, R., Handakumbura, P. P., Xiong, G., Wang, C., Corwin, J., Tsoukalas, A., Zhang, L., Ware, D., Pauly, M., Kliebenstein, D. J., Dehesh, K., Tagkopoulos, I., Breton, G., Pruneda-Paz, J. L., Ahnert, S. E., Kay, S. A., Hazen, S. P., & Brady, S. M. An Arabidopsis gene regulatory network for secondary cell wall synthesis. United States. https://doi.org/10.1038/nature14099
Taylor-Teeples, M., Lin, L., de Lucas, M., Turco, G., Toal, T. W., Gaudinier, A., Young, N. F., Trabucco, G. M., Veling, M. T., Lamothe, R., Handakumbura, P. P., Xiong, G., Wang, C., Corwin, J., Tsoukalas, A., Zhang, L., Ware, D., Pauly, M., Kliebenstein, D. J., Dehesh, K., Tagkopoulos, I., Breton, G., Pruneda-Paz, J. L., Ahnert, S. E., Kay, S. A., Hazen, S. P., and Brady, S. M. Wed . "An Arabidopsis gene regulatory network for secondary cell wall synthesis". United States. https://doi.org/10.1038/nature14099. https://www.osti.gov/servlets/purl/1347111.
@article{osti_1347111,
title = {An Arabidopsis gene regulatory network for secondary cell wall synthesis},
author = {Taylor-Teeples, M. and Lin, L. and de Lucas, M. and Turco, G. and Toal, T. W. and Gaudinier, A. and Young, N. F. and Trabucco, G. M. and Veling, M. T. and Lamothe, R. and Handakumbura, P. P. and Xiong, G. and Wang, C. and Corwin, J. and Tsoukalas, A. and Zhang, L. and Ware, D. and Pauly, M. and Kliebenstein, D. J. and Dehesh, K. and Tagkopoulos, I. and Breton, G. and Pruneda-Paz, J. L. and Ahnert, S. E. and Kay, S. A. and Hazen, S. P. and Brady, S. M.},
abstractNote = {The plant cell wall is an important factor for determining cell shape, function and response to the environment. Secondary cell walls, such as those found in xylem, are composed of cellulose, hemicelluloses and lignin and account for the bulk of plant biomass. The coordination between transcriptional regulation of synthesis for each polymer is complex and vital to cell function. A regulatory hierarchy of developmental switches has been proposed, although the full complement of regulators remains unknown. In this paper, we present a protein–DNA network between Arabidopsis thaliana transcription factors and secondary cell wall metabolic genes with gene expression regulated by a series of feed-forward loops. This model allowed us to develop and validate new hypotheses about secondary wall gene regulation under abiotic stress. Distinct stresses are able to perturb targeted genes to potentially promote functional adaptation. Finally, these interactions will serve as a foundation for understanding the regulation of a complex, integral plant component.},
doi = {10.1038/nature14099},
journal = {Nature (London)},
number = 7536,
volume = 517,
place = {United States},
year = {Wed Dec 24 00:00:00 EST 2014},
month = {Wed Dec 24 00:00:00 EST 2014}
}

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Arabidopsis mRNA decay landscape arises from specialized RNA decay substrates, decapping-mediated feedback, and redundancy
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  • Sorenson, Reed S.; Deshotel, Malia J.; Johnson, Katrina
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 7
  • DOI: 10.1073/pnas.1712312115

Molecular mechanisms governing differential robustness of development and environmental responses in plants
journal, October 2015

  • Lachowiec, Jennifer; Queitsch, Christine; Kliebenstein, Daniel J.
  • Annals of Botany, Vol. 117, Issue 5
  • DOI: 10.1093/aob/mcv151

PlanExp: intuitive integration of complex RNA-seq datasets with planarian omics resources
journal, October 2019


Novel cell surface luciferase reporter for high-throughput yeast one-hybrid screens
journal, July 2017

  • Bonaldi, Katia; Li, Zheng; Kang, S. Earl
  • Nucleic Acids Research, Vol. 45, Issue 18
  • DOI: 10.1093/nar/gkx682

TF2Network: predicting transcription factor regulators and gene regulatory networks in Arabidopsis using publicly available binding site information
posted_content, November 2017

  • Kulkarni, Shubhada R.; Vaneechoutte, Dries; Van de Velde, Jan
  • Nucleic Acids Research
  • DOI: 10.1101/173559

The Flowering Hormone Florigen Accelerates Secondary Cell Wall Biogenesis to Harmonize Vascular Maturation with Reproductive Development
posted_content, November 2018

  • Shalit-Kaneh, Akiva; Eviatar-Ribak, Tamar; Horev, Guy
  • Proceedings of the National Academy of Sciences
  • DOI: 10.1101/476028

Initiation and regulation of vascular tissue identity in the Arabidopsis embryo
preprint, November 2019

  • Smit, Margot E.; Llavata-Peris, Cristina I.; Roosjen, Mark
  • DOI: 10.1101/832501

Genes and networks regulating root anatomy and architecture
journal, May 2015

  • Wachsman, Guy; Sparks, Erin E.; Benfey, Philip N.
  • New Phytologist, Vol. 208, Issue 1
  • DOI: 10.1111/nph.13469

NorWood: a gene expression resource for evo-devo studies of conifer wood development
journal, February 2017

  • Jokipii-Lukkari, Soile; Sundell, David; Nilsson, Ove
  • New Phytologist, Vol. 216, Issue 2
  • DOI: 10.1111/nph.14458

Genetic engineering of grass cell wall polysaccharides for biorefining
journal, June 2017

  • Bhatia, Rakesh; Gallagher, Joe A.; Gomez, Leonardo D.
  • Plant Biotechnology Journal, Vol. 15, Issue 9
  • DOI: 10.1111/pbi.12764

Gene regulatory networks for lignin biosynthesis in switchgrass (Panicum virgatum )
journal, September 2018

  • Rao, Xiaolan; Chen, Xin; Shen, Hui
  • Plant Biotechnology Journal, Vol. 17, Issue 3
  • DOI: 10.1111/pbi.13000

The Class II KNOX genes KNAT3 and KNAT7 work cooperatively to influence deposition of secondary cell walls that provide mechanical support to Arabidopsis stems
journal, November 2019

  • Wang, Shumin; Yamaguchi, Masatoshi; Grienenberger, Etienne
  • The Plant Journal, Vol. 101, Issue 2
  • DOI: 10.1111/tpj.14541

Improving total saccharification yield of Arabidopsis plants by vessel-specific complementation of caffeoyl shikimate esterase (cse) mutants
journal, July 2016


Dynamics of gene expression during development and expansion of vegetative stem internodes of bioenergy sorghum
journal, June 2017

  • Kebrom, Tesfamichael H.; McKinley, Brian; Mullet, John E.
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0848-3

An essential role for Abscisic acid in the regulation of xylem fibre differentiation
journal, January 2018


Genome-wide association mapping in winter barley for grain yield and culm cell wall polymer content using the high-throughput CoMPP technique
journal, March 2017


Cell wall heterogeneity in root development of arabidopsis
text, January 2021


Regulation of Lignin Biosynthesis and Its Role in Growth-Defense Tradeoffs
journal, September 2018


Plant vascular development: from early specification to differentiation
journal, November 2015

  • De Rybel, Bert; Mähönen, Ari Pekka; Helariutta, Yrjö
  • Nature Reviews Molecular Cell Biology, Vol. 17, Issue 1
  • DOI: 10.1038/nrm.2015.6

Transcriptome analysis reveals the role of the root hairs as environmental sensors to maintain plant functions under water-deficiency conditions
journal, November 2015

  • Kwasniewski, Miroslaw; Daszkowska-Golec, Agata; Janiak, Agnieszka
  • Journal of Experimental Botany, Vol. 67, Issue 4
  • DOI: 10.1093/jxb/erv498

SECONDARY WALL ASSOCIATED MYB1 is a positive regulator of secondary cell wall thickening in Brachypodium distachyon and is not found in the Brassicaceae
journal, September 2018

  • Handakumbura, Pubudu P.; Brow, Kathryn; Whitney, Ian P.
  • The Plant Journal, Vol. 96, Issue 3
  • DOI: 10.1111/tpj.14047

A Gene Regulatory Network for Cellular Reprogramming in Plant Regeneration.
text, January 2018

  • Ikeuchi, Momoko; Shibata, Michitaro; Rymen, Bart
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.23703

The Plant Cell Wall: A Complex and Dynamic Structure As Revealed by the Responses of Genes under Stress Conditions
journal, August 2016

  • Houston, Kelly; Tucker, Matthew R.; Chowdhury, Jamil
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.00984

Genome-Wide Association Studies for Five Forage Quality-Related Traits in Sorghum (Sorghum bicolor L.)
journal, August 2018


Wood and water: How trees modify wood development to cope with drought
journal, March 2019

  • Rodriguez‐Zaccaro, F. Daniela; Groover, Andrew
  • PLANTS, PEOPLE, PLANET, Vol. 1, Issue 4
  • DOI: 10.1002/ppp3.29

Downregulating aspen xylan biosynthetic GT43 genes in developing wood stimulates growth via reprograming of the transcriptome
journal, April 2018

  • Ratke, Christine; Terebieniec, Barbara K.; Winestrand, Sandra
  • New Phytologist, Vol. 219, Issue 1
  • DOI: 10.1111/nph.15160

Comparative transcriptome profiling and morphology provide insights into endocarp cleaving of apricot cultivar (Prunus armeniaca L.)
journal, April 2017


Over-expression of poplar NAC15 gene enhances wood formation in transgenic tobacco
preprint, January 2020


Cell Wall Heterogeneity in Root Development of Arabidopsis
journal, August 2016

  • Somssich, Marc; Khan, Ghazanfar Abbas; Persson, Staffan
  • Frontiers in Plant Science, Vol. 07
  • DOI: 10.3389/fpls.2016.01242

Secondary Wall Regulating NACs Differentially Bind at the Promoter at a CELLULOSE SYNTHASE A4 Cis-eQTL
journal, December 2018


Over-expression of poplar NAC15 gene enhances wood formation in transgenic tobacco
preprint, January 2020


Hierarchical and Dynamic Regulation of Defense-Responsive Specialized Metabolism by WRKY and MYB Transcription Factors
journal, January 2020


Modified expression of ZmMYB167 in Brachypodium distachyon and Zea mays leads to increased cell wall lignin and phenolic content
journal, June 2019


A sorghum NAC gene is associated with variation in biomass properties and yield potential
journal, July 2018

  • Xia, Jingnu; Zhao, Yunjun; Burks, Payne
  • Plant Direct, Vol. 2, Issue 7
  • DOI: 10.1002/pld3.70

Systems Identification and Characterization of Cell Wall Reassembly and Degradation Related Genes in Glycine max (L.) Merill, a Bioenergy Legume
journal, September 2017

  • Nawaz, Muhammad Amjad; Rehman, Hafiz Mamoon; Imtiaz, Muhammad
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/s41598-017-11495-4

Transcriptional alterations during proliferation and lignification in Phyllostachys nigra cells
journal, July 2018


Co-expression network analyses identify functional modules associated with development and stress response in Gossypium arboreum
journal, December 2016

  • You, Qi; Zhang, Liwei; Yi, Xin
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep38436

Novel tool to quantify cell wall porosity relates wall structure to cell growth and drug uptake
journal, February 2019

  • Liu, Xiaohui; Li, Jiazhou; Zhao, Heyu
  • Journal of Cell Biology, Vol. 218, Issue 4
  • DOI: 10.1083/jcb.201810121

A genetic framework for H2O2 induced cell death in Arabidopsis thaliana
journal, October 2015


An efficient transient expression system for gene function analysis in rose
journal, December 2017


Improving total saccharification yield of Arabidopsis plants by vessel-specific complementation of caffeoyl shikimate esterase (cse) mutants
journal, July 2016


Dynamics of gene expression during development and expansion of vegetative stem internodes of bioenergy sorghum
journal, June 2017

  • Kebrom, Tesfamichael H.; McKinley, Brian; Mullet, John E.
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0848-3

The Arabidopsis RCC1 Family Protein TCF1 Regulates Freezing Tolerance and Cold Acclimation through Modulating Lignin Biosynthesis
journal, September 2015


SUMO modification of LBD30 by SIZ1 regulates secondary cell wall formation in Arabidopsis thaliana
journal, January 2019


Genome Regions Associated with Functional Performance of Soybean Stem Fibers in Polypropylene Thermoplastic Composites
journal, July 2015


Modeling hormonal control of cambium proliferation
journal, February 2017


Genome-wide association mapping in winter barley for grain yield and culm cell wall polymer content using the high-throughput CoMPP technique
journal, March 2017


SeqEnrich: A tool to predict transcription factor networks from co-expressed Arabidopsis and Brassica napus gene sets
journal, June 2017


A Transcriptomic Analysis of Xylan Mutants Does Not Support the Existence of a Secondary Cell Wall Integrity System in Arabidopsis.
journalarticle, January 2018

  • Faria-Blanc, Nuno; Mortimer, Jenny C.; Dupree, Paul
  • Frontiers Media SA
  • DOI: 10.17863/cam.22010

Over-expression of poplar NAC15 gene enhances wood formation in transgenic tobacco
preprint, January 2020


NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants
journal, May 2015

  • Nakano, Yoshimi; Yamaguchi, Masatoshi; Endo, Hitoshi
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00288

Molecular Mechanisms for Vascular Development and Secondary Cell Wall Formation
journal, March 2016


Drought Stress Predominantly Endures Arabidopsis thaliana to Pseudomonas syringae Infection
journal, June 2016

  • Gupta, Aarti; Dixit, Sandeep K.; Senthil-Kumar, Muthappa
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.00808

The Plant Cell Wall: A Complex and Dynamic Structure As Revealed by the Responses of Genes under Stress Conditions
journal, August 2016

  • Houston, Kelly; Tucker, Matthew R.; Chowdhury, Jamil
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.00984

Cell Wall Heterogeneity in Root Development of Arabidopsis
journal, August 2016

  • Somssich, Marc; Khan, Ghazanfar Abbas; Persson, Staffan
  • Frontiers in Plant Science, Vol. 07
  • DOI: 10.3389/fpls.2016.01242

Studying Secondary Growth and Bast Fiber Development: The Hemp Hypocotyl Peeks behind the Wall
journal, November 2016


4-Coumarate-CoA Ligase-Like Gene OsAAE3 Negatively Mediates the Rice Blast Resistance, Floret Development and Lignin Biosynthesis
journal, January 2017


Concurrent Drought Stress and Vascular Pathogen Infection Induce Common and Distinct Transcriptomic Responses in Chickpea
journal, March 2017

  • Sinha, Ranjita; Gupta, Aarti; Senthil-Kumar, Muthappa
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.00333

Regulation of Plant Growth and Development: A Review From a Chromatin Remodeling Perspective
journal, August 2018

  • Ojolo, Simon P.; Cao, Shijiang; Priyadarshani, S. V. G. N.
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.01232

Regulation of Lignin Biosynthesis and Its Role in Growth-Defense Tradeoffs
journal, September 2018


Recent Advances in the Transcriptional Regulation of Secondary Cell Wall Biosynthesis in the Woody Plants
journal, October 2018


Xylan in the Middle: Understanding Xylan Biosynthesis and Its Metabolic Dependencies Toward Improving Wood Fiber for Industrial Processing
journal, February 2019

  • Wierzbicki, Martin P.; Maloney, Victoria; Mizrachi, Eshchar
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.00176

Finding New Cell Wall Regulatory Genes in Populus trichocarpa Using Multiple Lines of Evidence
journal, October 2019


Rice Genome-Scale Network Integration Reveals Transcriptional Regulators of Grass Cell Wall Synthesis
journal, October 2019

  • Zhao, Kangmei; Lin, Fan; Romero-Gamboa, Sandra P.
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.01275

Xylem Cell Wall Formation in Pioneer Roots and Stems of Populus trichocarpa (Torr. & Gray)
journal, November 2019

  • Marzec-Schmidt, Katarzyna; Ludwików, Agnieszka; Wojciechowska, Natalia
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.01419

Hierarchical and Dynamic Regulation of Defense-Responsive Specialized Metabolism by WRKY and MYB Transcription Factors
journal, January 2020