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Title: Acetylation of cell wall is required for structural integrity of the leaf surface and exerts a global impact on plant stress responses

Abstract

The epidermis on leaves protects plants from pathogen invasion and provides a waterproof barrier. It consists of a layer of cells that is surrounded by thick cell walls, which are partially impregnated by highly hydrophobic cuticular components. We show that the Arabidopsis T-DNA insertion mutants of REDUCED WALL ACETYLATION 2 (rwa2), previously identified as having reduced O-acetylation of both pectins and hemicelluloses, exhibit pleiotrophic phenotype on the leaf surface. The cuticle layer appeared diffused and was significantly thicker and underneath cell wall layer was interspersed with electron-dense deposits. A large number of trichomes were collapsed and surface permeability of the leaves was enhanced in rwa2 as compared to the wild type. A massive reprogramming of the transcriptome was observed in rwa2 as compared to the wild type, including a coordinated up-regulation of genes involved in responses to abiotic stress, particularly detoxification of reactive oxygen species and defense against microbial pathogens (e.g., lipid transfer proteins, peroxidases). In accordance, peroxidase activities were found to be elevated in rwa2 as compared to the wild type. In conclusion, these results indicate that cell wall acetylation is essential for maintaining the structural integrity of leaf epidermis, and that reduction of cell wall acetylation leads tomore » global stress responses in Arabidopsis.« less

Authors:
 [1];  [1];  [1];  [2];  [3];  [3];  [1];  [4];  [5];  [6];  [1]
  1. Copenhagen Plant Science Center, Frederiksberg (Denmark); Univ. of Copenhagen (Denmark)
  2. Univ. of California, Davis, CA (United States)
  3. Univ. of Copenhagen (Denmark)
  4. Univ. of Lausanne, Lausanne (Switzerland)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
  6. Univ. of California, Davis, CA (United States); Danish National Research Foundation Center DynaMO, Frederiksberg (Denmark)
Publication Date:
Research Org.:
University of California, Berkeley, CA (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:
1254007
Alternate Identifier(s):
OSTI ID: 1257260
Grant/Contract Number:  
AC02-05CH11231; 1339125; 1021861; 001-2011-4; 12-131834; AC02–05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; cellwallacetylation; trichomes; cuticles; epidermis; Botrytiscinerea; peroxidase; mRNAsequencing; cell wall acetylation; Botrytis cinerea; mRNA sequencing

Citation Formats

Nafisi, Majse, Stranne, Maria, Fimognari, Lorenzo, Atwell, Susanna, Martens, Helle J., Pedas, Pai R., Hansen, Sara F., Nawrath, Christiane, Scheller, Henrik V., Kliebenstein, Daniel J., and Sakuragi, Yumiko. Acetylation of cell wall is required for structural integrity of the leaf surface and exerts a global impact on plant stress responses. United States: N. p., 2015. Web. doi:10.3389/fpls.2015.00550.
Nafisi, Majse, Stranne, Maria, Fimognari, Lorenzo, Atwell, Susanna, Martens, Helle J., Pedas, Pai R., Hansen, Sara F., Nawrath, Christiane, Scheller, Henrik V., Kliebenstein, Daniel J., & Sakuragi, Yumiko. Acetylation of cell wall is required for structural integrity of the leaf surface and exerts a global impact on plant stress responses. United States. https://doi.org/10.3389/fpls.2015.00550
Nafisi, Majse, Stranne, Maria, Fimognari, Lorenzo, Atwell, Susanna, Martens, Helle J., Pedas, Pai R., Hansen, Sara F., Nawrath, Christiane, Scheller, Henrik V., Kliebenstein, Daniel J., and Sakuragi, Yumiko. Wed . "Acetylation of cell wall is required for structural integrity of the leaf surface and exerts a global impact on plant stress responses". United States. https://doi.org/10.3389/fpls.2015.00550. https://www.osti.gov/servlets/purl/1254007.
@article{osti_1254007,
title = {Acetylation of cell wall is required for structural integrity of the leaf surface and exerts a global impact on plant stress responses},
author = {Nafisi, Majse and Stranne, Maria and Fimognari, Lorenzo and Atwell, Susanna and Martens, Helle J. and Pedas, Pai R. and Hansen, Sara F. and Nawrath, Christiane and Scheller, Henrik V. and Kliebenstein, Daniel J. and Sakuragi, Yumiko},
abstractNote = {The epidermis on leaves protects plants from pathogen invasion and provides a waterproof barrier. It consists of a layer of cells that is surrounded by thick cell walls, which are partially impregnated by highly hydrophobic cuticular components. We show that the Arabidopsis T-DNA insertion mutants of REDUCED WALL ACETYLATION 2 (rwa2), previously identified as having reduced O-acetylation of both pectins and hemicelluloses, exhibit pleiotrophic phenotype on the leaf surface. The cuticle layer appeared diffused and was significantly thicker and underneath cell wall layer was interspersed with electron-dense deposits. A large number of trichomes were collapsed and surface permeability of the leaves was enhanced in rwa2 as compared to the wild type. A massive reprogramming of the transcriptome was observed in rwa2 as compared to the wild type, including a coordinated up-regulation of genes involved in responses to abiotic stress, particularly detoxification of reactive oxygen species and defense against microbial pathogens (e.g., lipid transfer proteins, peroxidases). In accordance, peroxidase activities were found to be elevated in rwa2 as compared to the wild type. In conclusion, these results indicate that cell wall acetylation is essential for maintaining the structural integrity of leaf epidermis, and that reduction of cell wall acetylation leads to global stress responses in Arabidopsis.},
doi = {10.3389/fpls.2015.00550},
journal = {Frontiers in Plant Science},
number = ,
volume = 6,
place = {United States},
year = {Wed Jul 22 00:00:00 EDT 2015},
month = {Wed Jul 22 00:00:00 EDT 2015}
}

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Works referenced in this record:

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Roles of cell wall peroxidases in plant development
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Arabidopsis GLASSY HAIR genes promote trichome papillae development
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Kunitz Trypsin Inhibitor: An Antagonist of Cell Death Triggered by Phytopathogens and Fumonisin B1 in Arabidopsis
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Xylan O-Acetylation Impacts Xylem Development and Enzymatic Recalcitrance as Indicated by the Arabidopsis Mutant tbl29
journal, July 2013

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  • Molecular Plant, Vol. 6, Issue 4
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The Arabidopsis DUF231 Domain-Containing Protein ESK1 Mediates 2-O- and 3-O-Acetylation of Xylosyl Residues in Xylan
journal, May 2013

  • Yuan, Youxi; Teng, Quincy; Zhong, Ruiqin
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  • DOI: 10.1093/pcp/pct070

Buckling as an origin of ordered cuticular patterns in flower petals
journal, March 2013

  • Antoniou Kourounioti, Rea L.; Band, Leah R.; Fozard, John A.
  • Journal of The Royal Society Interface, Vol. 10, Issue 80
  • DOI: 10.1098/rsif.2012.0847

Analysis of Xyloglucan Fucosylation in Arabidopsis
journal, April 2003

  • Perrin, Robyn M.; Jia, Zhonghua; Wagner, Tanya A.
  • Plant Physiology, Vol. 132, Issue 2
  • DOI: 10.1104/pp.102.016642

Spatial Imaging, Speciation, and Quantification of Selenium in the Hyperaccumulator Plants Astragalus bisulcatus and Stanleya pinnata
journal, August 2006

  • Freeman, John L.; Zhang, Li Hong; Marcus, Matthew A.
  • Plant Physiology, Vol. 142, Issue 1
  • DOI: 10.1104/pp.106.081158

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

Reduced Wall Acetylation Proteins Play Vital and Distinct Roles in Cell Wall O -Acetylation in Arabidopsis
journal, September 2013

  • Manabe, Yuzuki; Verhertbruggen, Yves; Gille, Sascha
  • Plant Physiology, Vol. 163, Issue 3
  • DOI: 10.1104/pp.113.225193

O-Acetylated Oligosaccharides from Pectins of Potato Tuber Cell Walls
journal, April 1997


The Isolation of Plant Cuticle with Pectic Enzymes.
journal, January 1955


Secretome Analysis Reveals an Arabidopsis Lipase Involved in Defense against Alternaria brassicicola
journal, August 2005


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

O -Acetylation of Arabidopsis Hemicellulose Xyloglucan Requires AXY4 or AXY4L, Proteins with a TBL and DUF231 Domain
journal, November 2011

  • Gille, Sascha; de Souza, Amancio; Xiong, Guangyan
  • The Plant Cell, Vol. 23, Issue 11
  • DOI: 10.1105/tpc.111.091728

Glycolate Oxidase Modulates Reactive Oxygen Species–Mediated Signal Transduction during Nonhost Resistance in Nicotiana benthamiana and Arabidopsis
journal, January 2012

  • Rojas, Clemencia M.; Senthil-Kumar, Muthappa; Wang, Keri
  • The Plant Cell, Vol. 24, Issue 1
  • DOI: 10.1105/tpc.111.093245

Identification of Botrytis cinerea susceptibility loci in Arabidopsis thaliana
journal, May 2004


Zinc distribution and speciation in Arabidopsis halleri  ×  Arabidopsis lyrata progenies presenting various zinc accumulation capacities
journal, November 2009


Arabidopsis thaliana plant defensin AtPDF1.1 is involved in the plant response to biotic stress
journal, June 2010


ATP citrate lyase activity is post-translationally regulated by sink strength and impacts the wax, cutin and rubber biosynthetic pathways
journal, June 2014

  • Xing, Shufan; van Deenen, Nicole; Magliano, Pasqualina
  • The Plant Journal, Vol. 79, Issue 2
  • DOI: 10.1111/tpj.12559

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

Lipid Trafficking in Plant Cells
journal, July 2014

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TBL10 is required for O -acetylation of pectic rhamnogalacturonan-I in Arabidopsis thaliana
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PMR 5, an acetylation protein at the intersection of pectin biosynthesis and defense against fungal pathogens
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A Biostimulant Obtained from the Seaweed Ascophyllum nodosum Protects Arabidopsis thaliana from Severe Oxidative Stress
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Report on the Current Inventory of the Toolbox for Plant Cell Wall Analysis: Proteinaceous and Small Molecular Probes
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Genome-Wide Analysis of Gene Expression Provides New Insights into Waterlogging Responses in Barley (Hordeum vulgare L.)
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