DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: PMR5, an acetylation protein at the intersection of pectin biosynthesis and defense against fungal pathogens

Abstract

Powdery mildew (Golovinomyces cichoracearum), one of the most prolific obligate biotrophic fungal pathogens worldwide, infects its host by penetrating the plant cell wall without activating the plant's innate immune system. The Arabidopsis mutant powdery mildew resistant 5 (pmr5) carries a mutation in a putative pectin acetyltransferase gene that confers enhanced resistance to powdery mildew. In this work, we show that heterologously expressed PMR5 protein transfers acetyl groups from [14C]-acetyl-CoA to oligogalacturonides. Through site-directed mutagenesis, we show that three amino acids within a highly conserved esterase domain in putative PMR5 orthologs are necessary for PMR5 function. A suppressor screen of mutagenized pmr5 seed selecting for increased powdery mildew susceptibility identified two previously characterized genes affecting the acetylation of plant cell wall polysaccharides, RWA2 and TBR. The rwa2 and tbr mutants also suppress powdery mildew disease resistance in pmr6, a mutant defective in a putative pectate lyase gene. Cell wall analysis of pmr5 and pmr6, and their rwa2 and tbr suppressor mutants, demonstrates minor shifts in cellulose and pectin composition. In direct contrast to their increased powdery mildew resistance, both pmr5 and pmr6 plants are highly susceptibile to multiple strains of the generalist necrotroph Botrytis cinerea, and have decreased camalexin production upon infectionmore » with B. cinerea. These results illustrate that cell wall composition is intimately connected to fungal disease resistance and outline a potential route for engineering powdery mildew resistance into susceptible crop species.« less

Authors:
ORCiD logo [1]; ORCiD logo [1];  [2];  [1];  [1];  [1];  [3];  [3]; ORCiD logo [4];  [2]; ORCiD logo [5];  [1]
  1. Univ. of California, Berkeley, CA (United States); Energy Biosciences Inst., Berkeley, CA (United States)
  2. Univ. of California, Davis, CA (United States)
  3. Joint BioEnergy Inst., Emeryville, CA (United States)
  4. Univ. of California, Berkeley, CA (United States); ; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Univ. of California, Berkeley, CA (United States); Joint BioEnergy Inst., Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Bioenergy Research Centers (BRC) (United States). Joint BioEnergy Inst. (JBEI); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Energy Biosciences Institute; National Science Foundation (NSF)
OSTI Identifier:
1609109
Alternate Identifier(s):
OSTI ID: 1575952
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 100; Journal Issue: 5; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; host resistance; cell wall biochemistry; fungal disease; powdery mildew; pectin acetylation; cell wall fragments

Citation Formats

Chiniquy, Dawn, Underwood, William, Corwin, Jason, Ryan, Andrew, Szemenyei, Heidi, Lim, Candice C., Stonebloom, Solomon H., Birdseye, Devon S., Vogel, John, Kliebenstein, Daniel, Scheller, Henrik V., and Somerville, Shauna. PMR5, an acetylation protein at the intersection of pectin biosynthesis and defense against fungal pathogens. United States: N. p., 2019. Web. doi:10.1111/tpj.14497.
Chiniquy, Dawn, Underwood, William, Corwin, Jason, Ryan, Andrew, Szemenyei, Heidi, Lim, Candice C., Stonebloom, Solomon H., Birdseye, Devon S., Vogel, John, Kliebenstein, Daniel, Scheller, Henrik V., & Somerville, Shauna. PMR5, an acetylation protein at the intersection of pectin biosynthesis and defense against fungal pathogens. United States. https://doi.org/10.1111/tpj.14497
Chiniquy, Dawn, Underwood, William, Corwin, Jason, Ryan, Andrew, Szemenyei, Heidi, Lim, Candice C., Stonebloom, Solomon H., Birdseye, Devon S., Vogel, John, Kliebenstein, Daniel, Scheller, Henrik V., and Somerville, Shauna. Wed . "PMR5, an acetylation protein at the intersection of pectin biosynthesis and defense against fungal pathogens". United States. https://doi.org/10.1111/tpj.14497. https://www.osti.gov/servlets/purl/1609109.
@article{osti_1609109,
title = {PMR5, an acetylation protein at the intersection of pectin biosynthesis and defense against fungal pathogens},
author = {Chiniquy, Dawn and Underwood, William and Corwin, Jason and Ryan, Andrew and Szemenyei, Heidi and Lim, Candice C. and Stonebloom, Solomon H. and Birdseye, Devon S. and Vogel, John and Kliebenstein, Daniel and Scheller, Henrik V. and Somerville, Shauna},
abstractNote = {Powdery mildew (Golovinomyces cichoracearum), one of the most prolific obligate biotrophic fungal pathogens worldwide, infects its host by penetrating the plant cell wall without activating the plant's innate immune system. The Arabidopsis mutant powdery mildew resistant 5 (pmr5) carries a mutation in a putative pectin acetyltransferase gene that confers enhanced resistance to powdery mildew. In this work, we show that heterologously expressed PMR5 protein transfers acetyl groups from [14C]-acetyl-CoA to oligogalacturonides. Through site-directed mutagenesis, we show that three amino acids within a highly conserved esterase domain in putative PMR5 orthologs are necessary for PMR5 function. A suppressor screen of mutagenized pmr5 seed selecting for increased powdery mildew susceptibility identified two previously characterized genes affecting the acetylation of plant cell wall polysaccharides, RWA2 and TBR. The rwa2 and tbr mutants also suppress powdery mildew disease resistance in pmr6, a mutant defective in a putative pectate lyase gene. Cell wall analysis of pmr5 and pmr6, and their rwa2 and tbr suppressor mutants, demonstrates minor shifts in cellulose and pectin composition. In direct contrast to their increased powdery mildew resistance, both pmr5 and pmr6 plants are highly susceptibile to multiple strains of the generalist necrotroph Botrytis cinerea, and have decreased camalexin production upon infection with B. cinerea. These results illustrate that cell wall composition is intimately connected to fungal disease resistance and outline a potential route for engineering powdery mildew resistance into susceptible crop species.},
doi = {10.1111/tpj.14497},
journal = {The Plant Journal},
number = 5,
volume = 100,
place = {United States},
year = {Wed Aug 14 00:00:00 EDT 2019},
month = {Wed Aug 14 00:00:00 EDT 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 28 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

The Cooperative Activities of CSLD2, CSLD3, and CSLD5 Are Required for Normal Arabidopsis Development
journal, November 2011

  • Yin, Lan; Verhertbruggen, Yves; Oikawa, Ai
  • Molecular Plant, Vol. 4, Issue 6
  • DOI: 10.1093/mp/ssr026

Novel eukaryotic enzymes modifying cell-surface biopolymers
journal, January 2010


The Powdery Mildews: A Review of the World's Most Familiar (Yet Poorly Known) Plant Pathogens
journal, September 2008


The cell wall-associated kinases, WAKs, as pectin receptors
journal, January 2012


Optimization of pathogenicity assays to study the Arabidopsis thaliana - Xanthomonas campestris pv. campestris pathosystem
journal, May 2005


Isolation and characterization of powdery mildew-resistant Arabidopsis mutants
journal, February 2000

  • Vogel, J.; Somerville, S.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 4
  • DOI: 10.1073/pnas.030531997

Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition: PMR5 is required for powdery mildew susceptibility
journal, December 2004


The human Cas1 protein: A sialic acid-specific O-acetyltransferase?
journal, October 2010


Quantification of disease progression of several microbial pathogens on Arabidopsis thaliana using real-time fluorescence PCR
journal, November 2003


Extracellular H 2 O 2 Induced by Oligogalacturonides Is Not Involved in the Inhibition of the Auxin-Regulated rolB Gene Expression in Tobacco Leaf Explants
journal, April 2000

  • Bellincampi, Daniela; Dipierro, Nunzio; Salvi, Giovanni
  • Plant Physiology, Vol. 122, Issue 4
  • DOI: 10.1104/pp.122.4.1379

The Effect of Lignin Removal by Alkaline Peroxide Pretreatment on the Susceptibility of Corn Stover to Purified Cellulolytic and Xylanolytic Enzymes
journal, February 2009

  • Selig, Michael J.; Vinzant, Todd B.; Himmel, Michael E.
  • Applied Biochemistry and Biotechnology, Vol. 155, Issue 1-3
  • DOI: 10.1007/s12010-008-8511-x

Contrasting Mechanisms of Defense Against Biotrophic and Necrotrophic Pathogens
journal, September 2005


Growth of the plant cell wall
journal, November 2005

  • Cosgrove, Daniel J.
  • Nature Reviews Molecular Cell Biology, Vol. 6, Issue 11, p. 850-861
  • DOI: 10.1038/nrm1746

Plant Cell Walls: Figure 1.
journal, October 2010


The Plant Cell Wall: A Dynamic Barrier Against Pathogen Invasion
journal, January 2012


Cell wall disassembly in ripening fruit
journal, January 2006

  • Brummell, David A.
  • Functional Plant Biology, Vol. 33, Issue 2
  • DOI: 10.1071/FP05234

The structure, function, and biosynthesis of plant cell wall pectic polysaccharides
journal, September 2009


The Quantitative Basis of the Arabidopsis Innate Immune System to Endemic Pathogens Depends on Pathogen Genetics
journal, February 2016


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


The irregular xylem9 Mutant is Deficient in Xylan Xylosyltransferase Activity
journal, September 2007

  • Lee, C.; O'Neill, M. A.; Tsumuraya, Y.
  • Plant and Cell Physiology, Vol. 48, Issue 11
  • DOI: 10.1093/pcp/pcm135

Methyl esterification of pectin plays a role during plant–pathogen interactions and affects plant resistance to diseases
journal, November 2012

  • Lionetti, Vincenzo; Cervone, Felice; Bellincampi, Daniela
  • Journal of Plant Physiology, Vol. 169, Issue 16
  • DOI: 10.1016/j.jplph.2012.05.006

ARABINAN DEFICIENT 1 Is a Putative Arabinosyltransferase Involved in Biosynthesis of Pectic Arabinan in Arabidopsis
journal, December 2005

  • Harholt, Jesper; Jensen, Jacob Krüger; Sørensen, Susanne Oxenbøll
  • Plant Physiology, Vol. 140, Issue 1
  • DOI: 10.1104/pp.105.072744

Toward a Systems Approach to Understanding Plant Cell Walls
journal, December 2004


A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta
journal, September 2003

  • Curtis, Mark D.; Grossniklaus, Ueli
  • Plant Physiology, Vol. 133, Issue 2, p. 462-469
  • DOI: 10.1104/pp.103.027979

A new mathematical model for relative quantification in real-time RT-PCR
journal, May 2001


Closing the ranks to attack by powdery mildew
journal, August 2000


Acetylation of cell wall is required for structural integrity of the leaf surface and exerts a global impact on plant stress responses
journal, July 2015

  • Nafisi, Majse; Stranne, Maria; Fimognari, Lorenzo
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00550

Three Pectin Methylesterase Inhibitors Protect Cell Wall Integrity for Arabidopsis Immunity to Botrytis
journal, January 2017

  • Lionetti, Vincenzo; Fabri, Eleonora; De Caroli, Monica
  • Plant Physiology, Vol. 173, Issue 3
  • DOI: 10.1104/pp.16.01185

Cas1p is a membrane protein necessary for the O-acetylation of the Cryptococcus neoformans capsular polysaccharide
journal, October 2001


Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis
journal, November 2006

  • Kämper, Jörg; Kahmann, Regine; Bölker, Michael
  • Nature, Vol. 444, Issue 7115
  • DOI: 10.1038/nature05248

Influence of the Degree of Polymerization of Oligogalacturonates and of Esterification Pattern of Pectin on Their Recognition by Monoclonal Antibodies
journal, July 1992

  • Liners, Françoise; Thibault, Jean-François; Van Cutsem, Pierre
  • Plant Physiology, Vol. 99, Issue 3
  • DOI: 10.1104/pp.99.3.1099

Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses
journal, August 2012

  • O'Connell, Richard J.; Thon, Michael R.; Hacquard, Stéphane
  • Nature Genetics, Vol. 44, Issue 9
  • DOI: 10.1038/ng.2372

TRICHOME BIREFRINGENCE and Its Homolog AT5G01360 Encode Plant-Specific DUF231 Proteins Required for Cellulose Biosynthesis in Arabidopsis
journal, April 2010

  • Bischoff, Volker; Nita, Silvia; Neumetzler, Lutz
  • Plant Physiology, Vol. 153, Issue 2
  • DOI: 10.1104/pp.110.153320

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

Arabidopsis ESK1 encodes a novel regulator of freezing tolerance: ESK1 encodes a novel protein
journal, February 2007


Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana
journal, March 1996


The Ectopic Expression of a Pectin Methyl Esterase Inhibitor Increases Pectin Methyl Esterification and Limits Fungal Diseases in Wheat
journal, September 2011

  • Volpi, Chiara; Janni, Michela; Lionetti, Vincenzo
  • Molecular Plant-Microbe Interactions, Vol. 24, Issue 9
  • DOI: 10.1094/MPMI-01-11-0021

MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

  • Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
  • Molecular Biology and Evolution, Vol. 33, Issue 7
  • DOI: 10.1093/molbev/msw054

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

Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998


Expansive Phenotypic Landscape of Botrytis cinerea Shows Differential Contribution of Genetic Diversity and Plasticity
journal, April 2016

  • Corwin, Jason A.; Subedy, Anushriya; Eshbaugh, Robert
  • Molecular Plant-Microbe Interactions, Vol. 29, Issue 4
  • DOI: 10.1094/MPMI-09-15-0196-R

Distinct Defenses Induced in Wheat Against Powdery Mildew by Acetylated and Nonacetylated Oligogalacturonides
journal, December 2010

  • Randoux, Béatrice; Renard-Merlier, Delphine; Mulard, Ghislain
  • Phytopathology, Vol. 100, Issue 12
  • DOI: 10.1094/PHYTO-03-10-0086

Transgenic expression of pectin methylesterase inhibitors limits tobamovirus spread in tobacco and Arabidopsis: PMEIs limit tobamovirus infection
journal, December 2013

  • Lionetti, Vincenzo; Raiola, Alessandro; Cervone, Felice
  • Molecular Plant Pathology, Vol. 15, Issue 3
  • DOI: 10.1111/mpp.12090

Transgenic Expression of a Fungal endo -Polygalacturonase Increases Plant Resistance to Pathogens and Reduces Auxin Sensitivity
journal, December 2007

  • Ferrari, Simone; Galletti, Roberta; Pontiggia, Daniela
  • Plant Physiology, Vol. 146, Issue 2
  • DOI: 10.1104/pp.107.109686

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


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

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

Rapid quantification of plant-powdery mildew interactions by qPCR and conidiospore counts
journal, January 2012


The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector
journal, September 1986

  • Koncz, Csaba; Schell, Jeff
  • MGG Molecular & General Genetics, Vol. 204, Issue 3
  • DOI: 10.1007/BF00331014

Two-way mixed-effects methods for joint association analysis using both host and pathogen genomes
journal, May 2018

  • Wang, Miaoyan; Roux, Fabrice; Bartoli, Claudia
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 24
  • DOI: 10.1073/pnas.1710980115

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

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
  • Plant and Cell Physiology, Vol. 54, Issue 7
  • DOI: 10.1093/pcp/pct070

PMR6 , a Pectate Lyase–Like Gene Required for Powdery Mildew Susceptibility in Arabidopsis
journal, September 2002

  • Vogel, John P.; Raab, Theodore K.; Schiff, Celine
  • The Plant Cell, Vol. 14, Issue 9
  • DOI: 10.1105/tpc.003509

TBL3 and TBL31, Two Arabidopsis DUF231 Domain Proteins, are Required for 3- O -Monoacetylation of Xylan
journal, November 2015

  • Yuan, Youxi; Teng, Quincy; Zhong, Ruiqin
  • Plant and Cell Physiology, Vol. 57, Issue 1
  • DOI: 10.1093/pcp/pcv172

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

Biosynthesis of Pectin
journal, April 2010

  • Harholt, J.; Suttangkakul, A.; Vibe Scheller, H.
  • Plant Physiology, Vol. 153, Issue 2, p. 384-395
  • DOI: 10.1104/pp.110.156588

TBL10 is required for O -acetylation of pectic rhamnogalacturonan-I in Arabidopsis thaliana
journal, September 2018

  • Stranne, Maria; Ren, Yanfang; Fimognari, Lorenzo
  • The Plant Journal, Vol. 96, Issue 4
  • DOI: 10.1111/tpj.14067

Pectin structure and biosynthesis
journal, June 2008


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

Plant cell wall dynamics and wall-related susceptibility in plant–pathogen interactions
journal, May 2014

  • Bellincampi, Daniela; Cervone, Felice; Lionetti, Vincenzo
  • Frontiers in Plant Science, Vol. 5
  • DOI: 10.3389/fpls.2014.00228

Cytokinesis in the Arabidopsis Embryo Involves the Syntaxin-Related KNOLLE Gene Product
journal, January 1996


An SHR–SCR module specifies legume cortical cell fate to enable nodulation
journal, December 2020


Rapid quantification of plant-powdery mildew interactions by qPCR and conidiospore counts
text, January 2012


Works referencing / citing this record:

Engineering of Bioenergy Crops: Dominant Genetic Approaches to Improve Polysaccharide Properties and Composition in Biomass
journal, March 2020