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

Journal Article · · The Plant Journal
DOI:https://doi.org/10.1111/tpj.14497· OSTI ID:1609109
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)

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.

Research Organization:
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 Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Energy Biosciences Institute; National Science Foundation (NSF)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1609109
Alternate ID(s):
OSTI ID: 1575952
Journal Information:
The Plant Journal, Vol. 100, Issue 5; ISSN 0960-7412
Publisher:
Society for Experimental BiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 28 works
Citation information provided by
Web of Science

References (72)

The Cooperative Activities of CSLD2, CSLD3, and CSLD5 Are Required for Normal Arabidopsis Development journal November 2011
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
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
Analysis of oligogalacturonic acids with 50 or fewer residues by high-performance anion-exchange chromatography and pulsed amperometric detection journal February 1990
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
The Effect of Lignin Removal by Alkaline Peroxide Pretreatment on the Susceptibility of Corn Stover to Purified Cellulolytic and Xylanolytic Enzymes journal February 2009
Contrasting Mechanisms of Defense Against Biotrophic and Necrotrophic Pathogens journal September 2005
Growth of the plant cell wall journal November 2005
Plant Cell Walls: Figure 1. journal October 2010
Resistance to Botrytis cinerea Induced in Arabidopsis by Elicitors Is Independent of Salicylic Acid, Ethylene, or Jasmonate Signaling But Requires PHYTOALEXIN DEFICIENT3 journal March 2007
The Plant Cell Wall: A Dynamic Barrier Against Pathogen Invasion journal January 2012
Cell wall disassembly in ripening fruit journal January 2006
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
Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity: Secondary metabolites influence Arabidopsis/Botrytis interactions journal September 2005
Methyl esterification of pectin plays a role during plant–pathogen interactions and affects plant resistance to diseases journal November 2012
ARABINAN DEFICIENT 1 Is a Putative Arabinosyltransferase Involved in Biosynthesis of Pectic Arabinan in Arabidopsis journal December 2005
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
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
Three Pectin Methylesterase Inhibitors Protect Cell Wall Integrity for Arabidopsis Immunity to Botrytis journal January 2017
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
Demethylation of oligogalacturonides by FaPE1 in the fruits of the wild strawberry Fragaria vesca triggers metabolic and transcriptional changes associated with defence and development of the fruit journal January 2011
Influence of the Degree of Polymerization of Oligogalacturonates and of Esterification Pattern of Pectin on Their Recognition by Monoclonal Antibodies journal July 1992
Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses journal August 2012
TRICHOME BIREFRINGENCE and Its Homolog AT5G01360 Encode Plant-Specific DUF231 Proteins Required for Cellulose Biosynthesis in Arabidopsis journal April 2010
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
Deep sequencing of voodoo lily (Amorphophallus konjac): an approach to identify relevant genes involved in the synthesis of the hemicellulose glucomannan journal May 2011
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
TRICHOME BIREFRINGENCE-LIKE27 Affects Aluminum Sensitivity by Modulating the O -Acetylation of Xyloglucan and Aluminum-Binding Capacity in Arabidopsis journal July 2014
The Ectopic Expression of a Pectin Methyl Esterase Inhibitor Increases Pectin Methyl Esterification and Limits Fungal Diseases in Wheat journal September 2011
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets journal March 2016
A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides journal May 2010
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
Distinct Defenses Induced in Wheat Against Powdery Mildew by Acetylated and Nonacetylated Oligogalacturonides journal December 2010
Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development journal January 2013
Transgenic expression of pectin methylesterase inhibitors limits tobamovirus spread in tobacco and Arabidopsis: PMEIs limit tobamovirus infection journal December 2013
Transgenic Expression of a Fungal endo -Polygalacturonase Increases Plant Resistance to Pathogens and Reduces Auxin Sensitivity journal December 2007
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
The Role of the Plant-Specific ALTERED XYLOGLUCAN9 Protein in Arabidopsis Cell Wall Polysaccharide O- Acetylation journal February 2015
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
Two-way mixed-effects methods for joint association analysis using both host and pathogen genomes journal May 2018
O -Acetylation of Arabidopsis Hemicellulose Xyloglucan Requires AXY4 or AXY4L, Proteins with a TBL and DUF231 Domain journal November 2011
The Arabidopsis DUF231 Domain-Containing Protein ESK1 Mediates 2-O- and 3-O-Acetylation of Xylosyl Residues in Xylan journal May 2013
PMR6 , a Pectate Lyase–Like Gene Required for Powdery Mildew Susceptibility in Arabidopsis journal September 2002
TBL3 and TBL31, Two Arabidopsis DUF231 Domain Proteins, are Required for 3- O -Monoacetylation of Xylan journal November 2015
Two Arabidopsis proteins synthesize acetylated xylan in vitro journal September 2014
Biosynthesis of Pectin journal April 2010
TBL10 is required for O -acetylation of pectic rhamnogalacturonan-I in Arabidopsis thaliana journal September 2018
Pectin structure and biosynthesis journal June 2008
Three Members of the Arabidopsis Glycosyltransferase Family 8 Are Xylan Glucuronosyltransferases journal June 2012
Plant cell wall dynamics and wall-related susceptibility in plant–pathogen interactions journal May 2014
Cytokinesis in the Arabidopsis Embryo Involves the Syntaxin-Related KNOLLE Gene Product journal January 1996
CsWAKL08, a pathogen-induced wall-associated receptor-like kinase in sweet orange, confers resistance to citrus bacterial canker via ROS control and JA signaling journal April 2020
An SHR–SCR module specifies legume cortical cell fate to enable nodulation journal December 2020
Integrated analyses of the transcriptome and small RNA of the hemiparasitic plant Monochasma savatieri before and after establishment of parasite-host association journal February 2021
Rapid quantification of plant-powdery mildew interactions by qPCR and conidiospore counts text January 2012

Cited By (1)