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Title: A Transcriptomic Analysis of Xylan Mutants Does Not Support the Existence of a Secondary Cell Wall Integrity System in Arabidopsis

Abstract

Yeast have long been known to possess a cell wall integrity (CWI) system, and recently an analogous systemhas been described for the primary walls of plants (PCWI) that leads to changes in plant growth and cell wall composition. A similar system has been proposed to exist for secondary cell walls (SCWI). However, there is little data to support this. Here, we analyzed the stem transcriptome of a set of cell wall biosynthetic mutants in order to investigate whether cell wall damage, in this case caused by aberrant xylan synthesis, activates a signaling cascade or changes in cell wall synthesis gene expression. Our data revealed remarkably few changes to the transcriptome. We hypothesize that this is because cells undergoing secondary cell wall thickening have entered a committed programme leading to cell death, and therefore a SCWI system would have limited impact. The absence of transcriptomic responses to secondary cell wall alterations may facilitate engineering of the secondary cell wall of plants.

Authors:
 [1];  [2];  [1]
  1. Univ. of Cambridge (United Kingdom). Dept. of Biohemistry
  2. Univ. of Cambridge (United Kingdom). Dept. of Biohemistry; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1465453
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 9; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Faria-Blanc, Nuno, Mortimer, Jenny C., and Dupree, Paul. A Transcriptomic Analysis of Xylan Mutants Does Not Support the Existence of a Secondary Cell Wall Integrity System in Arabidopsis. United States: N. p., 2018. Web. doi:10.3389/fpls.2018.00384.
Faria-Blanc, Nuno, Mortimer, Jenny C., & Dupree, Paul. A Transcriptomic Analysis of Xylan Mutants Does Not Support the Existence of a Secondary Cell Wall Integrity System in Arabidopsis. United States. doi:10.3389/fpls.2018.00384.
Faria-Blanc, Nuno, Mortimer, Jenny C., and Dupree, Paul. Tue . "A Transcriptomic Analysis of Xylan Mutants Does Not Support the Existence of a Secondary Cell Wall Integrity System in Arabidopsis". United States. doi:10.3389/fpls.2018.00384. https://www.osti.gov/servlets/purl/1465453.
@article{osti_1465453,
title = {A Transcriptomic Analysis of Xylan Mutants Does Not Support the Existence of a Secondary Cell Wall Integrity System in Arabidopsis},
author = {Faria-Blanc, Nuno and Mortimer, Jenny C. and Dupree, Paul},
abstractNote = {Yeast have long been known to possess a cell wall integrity (CWI) system, and recently an analogous systemhas been described for the primary walls of plants (PCWI) that leads to changes in plant growth and cell wall composition. A similar system has been proposed to exist for secondary cell walls (SCWI). However, there is little data to support this. Here, we analyzed the stem transcriptome of a set of cell wall biosynthetic mutants in order to investigate whether cell wall damage, in this case caused by aberrant xylan synthesis, activates a signaling cascade or changes in cell wall synthesis gene expression. Our data revealed remarkably few changes to the transcriptome. We hypothesize that this is because cells undergoing secondary cell wall thickening have entered a committed programme leading to cell death, and therefore a SCWI system would have limited impact. The absence of transcriptomic responses to secondary cell wall alterations may facilitate engineering of the secondary cell wall of plants.},
doi = {10.3389/fpls.2018.00384},
journal = {Frontiers in Plant Science},
number = ,
volume = 9,
place = {United States},
year = {2018},
month = {3}
}

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Cited by: 7 works
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Works referenced in this record:

Expression of a bacterial 3-dehydroshikimate dehydratase reduces lignin content and improves biomass saccharification efficiency
journal, January 2015

  • Eudes, Aymerick; Sathitsuksanoh, Noppadon; Baidoo, Edward E. K.
  • Plant Biotechnology Journal, Vol. 13, Issue 9
  • DOI: 10.1111/pbi.12310

Expansion of the Receptor-Like Kinase/Pelle Gene Family and Receptor-Like Proteins in Arabidopsis
journal, June 2003


Structure of cellulose-deficient secondary cell walls from the irx3 mutant of Arabidopsis thaliana
journal, September 2002


Are designer plant cell walls a realistic aspiration or will the plasticity of the plant's metabolism win out?
journal, April 2014


Powerful regulatory systems and post-transcriptional gene silencing resist increases in cellulose content in cell walls of barley
journal, January 2015


Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure
journal, July 2009

  • Coleman, H. D.; Yan, J.; Mansfield, S. D.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 31
  • DOI: 10.1073/pnas.0900188106

Downregulation of caffeoyl-CoA O-methyltransferase (CCoAOMT) by RNA interference leads to reduced lignin production in maize straw
journal, January 2013


Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana
journal, May 2003


Caffeoyl Shikimate Esterase (CSE) Is an Enzyme in the Lignin Biosynthetic Pathway in Arabidopsis
journal, August 2013


The role of the secondary cell wall in plant resistance to pathogens
journal, August 2014


Arabidopsis irregular xylem8 and irregular xylem9 : Implications for the Complexity of Glucuronoxylan Biosynthesis
journal, February 2007


Engineering of plants with improved properties as biofuels feedstocks by vessel-specific complementation of xylan biosynthesis mutants
journal, January 2012

  • Petersen, Pia Damm; Lau, Jane; Ebert, Berit
  • Biotechnology for Biofuels, Vol. 5, Issue 1, Article No. 84
  • DOI: 10.1186/1754-6834-5-84

Preprocessing of oligonucleotide array data
journal, June 2004


A Receptor-like Kinase Mediates the Response of Arabidopsis Cells to the Inhibition of Cellulose Synthesis
journal, June 2007


Plant cell wall integrity maintenance as an essential component of biotic stress response mechanisms
journal, January 2012


Cell wall integrity signaling in plants: “To grow or not to grow that's the question”
journal, March 2016


A Battery of Transcription Factors Involved in the Regulation of Secondary Cell Wall Biosynthesis in Arabidopsis
journal, October 2008


Neighboring Parenchyma Cells Contribute to Arabidopsis Xylem Lignification, while Lignification of Interfascicular Fibers Is Cell Autonomous
journal, October 2013

  • Smith, Rebecca A.; Schuetz, Mathias; Roach, Melissa
  • The Plant Cell, Vol. 25, Issue 10
  • DOI: 10.1105/tpc.113.117176

Controlled silencing of 4-coumarate:CoA ligase alters lignocellulose composition without affecting stem growth
journal, January 2011


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


From hybridization theory to microarray data analysis: performance evaluation
journal, December 2011


Non-Cell-Autonomous Postmortem Lignification of Tracheary Elements in Zinnia elegans
journal, April 2013


A comparison of normalization methods for high density oligonucleotide array data based on variance and bias
journal, January 2003


Wall-associated Kinase WAK1 Interacts with Cell Wall Pectins in a Calcium-induced Conformation
journal, February 2005

  • Decreux, Annabelle; Messiaen, Johan
  • Plant and Cell Physiology, Vol. 46, Issue 2
  • DOI: 10.1093/pcp/pci026

Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis
journal, December 2007


Genes involved in the biosynthesis of lignin precursors in Arabidopsis thaliana
journal, August 2003


Transcription switches for protoxylem and metaxylem vessel formation
journal, August 2005


Resistance against Herbicide Isoxaben and Cellulose Deficiency Caused by Distinct Mutations in Same Cellulose Synthase Isoform CESA6
journal, February 2002

  • Desprez, Thierry; Vernhettes, Samantha; Fagard, Mathilde
  • Plant Physiology, Vol. 128, Issue 2
  • DOI: 10.1104/pp.010822

eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant
journal, June 1998

  • Xin, Z.; Browse, J.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 13
  • DOI: 10.1073/pnas.95.13.7799

Virus-Induced Silencing of a Plant Cellulose Synthase Gene
journal, May 2000

  • Burton, Rachel A.; Gibeaut, David M.; Bacic, Antony
  • The Plant Cell, Vol. 12, Issue 5
  • DOI: 10.1105/tpc.12.5.691

Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) heynh.
journal, November 1980

  • Koornneef, M.; van der Veen, J. H.
  • Theoretical and Applied Genetics, Vol. 58, Issue 6
  • DOI: 10.1007/BF00265176

O-Acetylation of glucuronoxylan in Arabidopsis thaliana wild type and its change in xylan biosynthesis mutants
journal, March 2014

  • Chong, Sun-Li; Virkki, Liisa; Maaheimo, Hannu
  • Glycobiology, Vol. 24, Issue 6
  • DOI: 10.1093/glycob/cwu017

Arabidopsis Heterotrimeric G-protein Regulates Cell Wall Defense and Resistance to Necrotrophic Fungi
journal, January 2012

  • Delgado-Cerezo, Magdalena; Sánchez-Rodríguez, Clara; Escudero, Viviana
  • Molecular Plant, Vol. 5, Issue 1
  • DOI: 10.1093/mp/ssr082

Loss-of-Function Mutation of REDUCED WALL ACETYLATION2 in Arabidopsis Leads to Reduced Cell Wall Acetylation and Increased Resistance to Botrytis cinerea
journal, January 2011

  • Manabe, Yuzuki; Nafisi, Majse; Verhertbruggen, Yves
  • Plant Physiology, Vol. 155, Issue 3
  • DOI: 10.1104/pp.110.168989

4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein
journal, August 2012

  • Urbanowicz, B. R.; Pena, M. J.; Ratnaparkhe, S.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 35
  • DOI: 10.1073/pnas.1208097109

Glucuronic Acid Moieties on Xylan Are Functionally Equivalent to O -Acetyl-Substituents
journal, July 2015


Identification of Novel Genes in Arabidopsis Involved in Secondary Cell Wall Formation Using Expression Profiling and Reverse Genetics
journal, June 2005

  • Brown, David M.; Zeef, Leo A. H.; Ellis, Joanne
  • The Plant Cell, Vol. 17, Issue 8
  • DOI: 10.1105/tpc.105.031542

Significance analysis of microarrays applied to the ionizing radiation response
journal, April 2001

  • Tusher, V. G.; Tibshirani, R.; Chu, G.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 9, p. 5116-5121
  • DOI: 10.1073/pnas.091062498

Impairment of Cellulose Synthases Required for Arabidopsis Secondary Cell Wall Formation Enhances Disease Resistance
journal, March 2007

  • Hernández-Blanco, Camilo; Feng, Dong Xin; Hu, Jian
  • The Plant Cell, Vol. 19, Issue 3
  • DOI: 10.1105/tpc.106.048058

A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides
journal, May 2010

  • Brutus, A.; Sicilia, F.; Macone, A.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 20
  • DOI: 10.1073/pnas.1000675107

Lignification: different mechanisms for a versatile polymer
journal, February 2015


Lignin biosynthesis perturbations affect secondary cell wall composition and saccharification yield in Arabidopsis thaliana
journal, January 2013

  • Van Acker, Rebecca; Vanholme, Ruben; Storme, Véronique
  • Biotechnology for Biofuels, Vol. 6, Article No. 46
  • DOI: 10.1186/1754-6834-6-46

Characterization of IRX10 and IRX10-like reveals an essential role in glucuronoxylan biosynthesis in Arabidopsis
journal, February 2009


An extracellular network of Arabidopsis leucine-rich repeat receptor kinases
journal, January 2018

  • Smakowska-Luzan, Elwira; Mott, G. Adam; Parys, Katarzyna
  • Nature, Vol. 553, Issue 7688
  • DOI: 10.1038/nature25184

The Role of the Plant-Specific ALTERED XYLOGLUCAN9 Protein in Arabidopsis Cell Wall Polysaccharide O- Acetylation
journal, February 2015

  • Schultink, Alex; Naylor, Dan; Dama, Murali
  • Plant Physiology, Vol. 167, Issue 4
  • DOI: 10.1104/pp.114.256479

Enhancing cellulose utilization for fuels and chemicals by genetic modification of plant cell wall architecture
journal, April 2015


IRX14 and IRX14-LIKE, Two Glycosyl Transferases Involved in Glucuronoxylan Biosynthesis and Drought Tolerance in Arabidopsis
journal, September 2010

  • Keppler, Brian D.; Showalter, Allan M.
  • Molecular Plant, Vol. 3, Issue 5
  • DOI: 10.1093/mp/ssq028

Xylan O-Acetylation Impacts Xylem Development and Enzymatic Recalcitrance as Indicated by the Arabidopsis Mutant tbl29
journal, July 2013

  • Xiong, Guangyan; Cheng, Kun; Pauly, Markus
  • Molecular Plant, Vol. 6, Issue 4
  • DOI: 10.1093/mp/sst014

Progress of Lignification Mediated by Intercellular Transportation of Monolignols During Tracheary Element Differentiation of Isolated Zinnia Mesophyll Cells
journal, September 2001

  • Hosokawa, Mami; Suzuki, Shiro; Umezawa, Toshiaki
  • Plant and Cell Physiology, Vol. 42, Issue 9
  • DOI: 10.1093/pcp/pce124

Up against the Wall: Is Yeast Cell Wall Integrity Ensured by Mechanosensing in Plasma Membrane Microdomains?
journal, November 2014

  • Kock, Christian; Dufrêne, Yves F.; Heinisch, Jürgen J.
  • Applied and Environmental Microbiology, Vol. 81, Issue 3
  • DOI: 10.1128/AEM.03273-14

Monolignol Ferulate Transferase Introduces Chemically Labile Linkages into the Lignin Backbone
journal, April 2014


An Arabidopsis gene regulatory network for secondary cell wall synthesis
journal, December 2014

  • Taylor-Teeples, M.; Lin, L.; de Lucas, M.
  • Nature, Vol. 517, Issue 7536
  • DOI: 10.1038/nature14099

Two Arabidopsis proteins synthesize acetylated xylan in vitro
journal, September 2014

  • Urbanowicz, Breeanna R.; Peña, Maria J.; Moniz, Heather A.
  • The Plant Journal, Vol. 80, Issue 2
  • DOI: 10.1111/tpj.12643

Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant
journal, March 2014

  • Bonawitz, Nicholas D.; Kim, Jeong Im; Tobimatsu, Yuki
  • Nature, Vol. 509, Issue 7500, p. 376-380
  • DOI: 10.1038/nature13084

Molecular aspects of methionine biosynthesis
journal, June 2003


Absence of branches from xylan in Arabidopsis gux mutants reveals potential for simplification of lignocellulosic biomass
journal, September 2010

  • Mortimer, J. C.; Miles, G. P.; Brown, D. M.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 40
  • DOI: 10.1073/pnas.1005456107

Three Members of the Arabidopsis Glycosyltransferase Family 8 Are Xylan Glucuronosyltransferases
journal, June 2012

  • Rennie, Emilie A.; Hansen, Sara Fasmer; Baidoo, Edward E. K.
  • Plant Physiology, Vol. 159, Issue 4
  • DOI: 10.1104/pp.112.200964

A gene stacking approach leads to engineered plants with highly increased galactan levels in Arabidopsis
journal, December 2014


A Systems Biology View of Responses to Lignin Biosynthesis Perturbations in Arabidopsis
journal, September 2012

  • Vanholme, Ruben; Storme, Véronique; Vanholme, Bartel
  • The Plant Cell, Vol. 24, Issue 9
  • DOI: 10.1105/tpc.112.102574

    Works referencing / citing this record:

    Poplar carbohydrate‐active enzymes: whole‐genome annotation and functional analyses based on RNA expression data
    journal, July 2019

    • Kumar, Vikash; Hainaut, Matthieu; Delhomme, Nicolas
    • The Plant Journal, Vol. 99, Issue 4
    • DOI: 10.1111/tpj.14417

    Poplar carbohydrate‐active enzymes: whole‐genome annotation and functional analyses based on RNA expression data
    journal, July 2019

    • Kumar, Vikash; Hainaut, Matthieu; Delhomme, Nicolas
    • The Plant Journal, Vol. 99, Issue 4
    • DOI: 10.1111/tpj.14417