skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Arabidopsis Dehiscence Zone Polygalacturonase 1 (ADPG1) releases latent defense signals in stems with reduced lignin content

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [1]; ORCiD logo [2]; ORCiD logo [3];  [4];  [5];  [6]; ORCiD logo [4];  [7]; ORCiD logo [2]; ORCiD logo [8]; ORCiD logo [8]; ORCiD logo [9]
  1. Univ. of North Texas, Denton, TX (United States). BioDiscovery Inst. and Dept. of Biological Sciences
  2. Univ. of Leeds, Leeds (United Kingdom). Faculty of Biological Sciences
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center; Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center; Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center and Dept. of Plant Biology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation
  5. Univ. of Georgia, Athens, GA (United States). Dept. of Genetics
  6. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation; Univ. of Georgia, Athens, GA (United States). Dept. of Genetics
  7. Univ. of North Texas, Denton, TX (United States). BioDiscovery Inst. and Dept. of Biological Sciences; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center
  8. Ghent Univ. (Belguim). Dept. of Plant Biotechnology and Bioinformatics; Vlaams Inst. voor Biotechnologie, Ghent (Belguim). Center for Plant Systems Biology
  9. Univ. of North Texas, Denton, TX (United States). BioDiscovery Inst. and Dept. of Biological Sciences; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center and Center for Bioenergy Innovation

There is considerable interest in engineering plant cell wall components, particularly lignin, to improve forage quality and biomass properties for processing to fuels and bioproducts. However, modifying lignin content and/or composition in transgenic plants through down-regulation of lignin biosynthetic enzymes can induce expression of defense response genes in the absence of biotic or abiotic stress. Arabidopsis thaliana lines with altered lignin through down-regulation of hydroxycinnamoyl CoA:shikimate/quinate hydroxycinnamoyl transferase (HCT) or loss of function of cinnamoyl CoA reductase 1 (CCR1) express a suite of pathogenesis-related (PR) protein genes. The plants also exhibit extensive cell wall remodeling associated with induction of multiple cell wall-degrading enzymes, a process which renders the corresponding biomass a substrate for growth of the cellulolytic thermophile Caldicellulosiruptor bescii lacking a functional pectinase gene cluster. The cell wall remodeling also results in the release of size- and charge-heterogeneous pectic oligosaccharide elicitors of PR gene expression. Genetic analysis shows that both in planta PR gene expression and release of elicitors are the result of ectopic expression in xylem of the gene Arabidopsis Dehiscence Zone Polygalacturonase 1 (ADPG1), which is normally expressed during anther and silique dehiscence. These data highlight the importance of pectin in cell wall integrity and the value of lignin modification as a tool to interrogate the informational content of plant cell walls.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); USDOE Bioenergy Research Centers (BRC) (United States). Center for Bioenergy Innovation (CBI)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)' National Science Foundation (NSF)
Grant/Contract Number:
AC05-00OR22725; PIEF-GA-2013-625270; DBI-0421683; IOS-0923992
OSTI ID:
1625055
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 117, Issue 6; ISSN 0027-8424
Publisher:
National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 39 works
Citation information provided by
Web of Science

References (77)

Oligosaccharins—oligosaccharides that regulate growth, development and defence responses in plants journal January 1992
A Novel Approach to Dissect the Abscission Process in Arabidopsis journal September 2012
Plant defensins: Defense, development and application journal November 2009
Host-Pathogen Interactions: VI. A Single Plant Protein Efficiently Inhibits Endopolygalacturonases Secreted by Colletotrichum Lindemuthianum and Aspergillus Niger journal March 1973
Lignin modification improves fermentable sugar yields for biofuel production journal June 2007
Host-Pathogen Interactions: XI. Composition and Structure of Wall-released Elicitor Fractions journal May 1976
The AtrbohD-Mediated Oxidative Burst Elicited by Oligogalacturonides in Arabidopsis Is Dispensable for the Activation of Defense Responses Effective against Botrytis cinerea journal September 2008
Deletion of a gene cluster encoding pectin degrading enzymes in Caldicellulosiruptor bescii reveals an important role for pectin in plant biomass recalcitrance journal October 2014
The primary structures of one elicitor-active and seven elicitor-inactive hexa(beta-D-glucopyranosyl)-D-glucitols isolated from the mycelial walls of Phytophthora megasperma f. sp. glycinea. journal September 1984
Association of hemicellulose- and pectin-modifying gene expression with Eucalyptus globulus secondary growth journal August 2011
A Comprehensive Toolkit of Plant Cell Wall Glycan-Directed Monoclonal Antibodies journal April 2010
Host-Pathogen Interactions: X. Fractionation and Biological Activity of an Elicitor Isolated from the Mycelial Walls of Phytophthora megasperma var. sojae journal May 1976
Convergent Evolution of Syringyl Lignin Biosynthesis via Distinct Pathways in the Lycophyte Selaginella and Flowering Plants journal April 2010
The role of the secondary cell wall in plant resistance to pathogens journal August 2014
Loss of Arabidopsis GAUT12/IRX8 causes anther indehiscence and leads to reduced G lignin associated with altered matrix polysaccharide deposition journal July 2014
Down-regulation of hydroxycinnamoyl CoA: Shikimate hydroxycinnamoyl transferase in transgenic alfalfa affects lignification, development and forage quality journal June 2007
Pectic Cell Wall Fragments Regulate Tobacco Thin-Cell-Layer Explant Morphogenesis. journal August 1989
Salicylic acid mediates the reduced growth of lignin down-regulated plants journal November 2011
Host-Pathogen Interactions: XXII. A Galacturonic Acid Oligosaccharide from Plant Cell Walls Elicits Phytoalexins journal April 1983
Host-Pathogen Interactions: XXIV. Fragments Isolated from Suspension-Cultured Sycamore Cell Walls Inhibit the Ability of the Cells to Incorporate [ 14 C]Leucine into Proteins journal July 1983
Cell wall integrity signaling in plants: “To grow or not to grow that's the question” journal March 2016
Activation of Plant Innate Immunity by Extracellular High Mobility Group Box 3 and Its Inhibition by Salicylic Acid journal March 2016
Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.) journal January 2011
The NAC Transcription Factors NST1 and NST2 of Arabidopsis Regulate Secondary Wall Thickenings and Are Required for Anther Dehiscence journal October 2005
Elicitors and defense gene induction in plants with altered lignin compositions journal June 2018
The Simultaneous Repression of CCR and CAD, Two Enzymes of the Lignin Biosynthetic Pathway, Results in Sterility and Dwarfism in Arabidopsis thaliana journal January 2011
Manipulation of the morphogenetic pathways of tobacco explants by oligosaccharins journal April 1985
Silencing of Hydroxycinnamoyl-Coenzyme A Shikimate/Quinate Hydroxycinnamoyltransferase Affects Phenylpropanoid Biosynthesis journal May 2004
Plant defensins journal December 2002
The Pattern of Distribution of Pectin, Peroxidase and Lignin in the Middle Lamella of Secondary Xylem Fibres in Alfalfa (Medicago sativa) journal February 2005
Ectopic Defense Gene Expression Is Associated with Growth Defects in Medicago truncatula Lignin Pathway Mutants journal July 2019
Redirection of the phenylpropanoid pathway to feruloyl malate in Arabidopsis mutants deficient for cinnamoyl-CoA reductase 1 journal November 2007
Carbohydrate-Active Enzymes Involved in the Secondary Cell Wall Biogenesis in Hybrid Aspen journal February 2005
Expression of polygalacturonases and evidence to support their role during cell separation processes in Arabidopsis thaliana journal October 2007
Host-Pathogen Interactions: XIX. THE ENDOGENOUS ELICITOR, A FRAGMENT OF A PLANT CELL WALL POLYSACCHARIDE THAT ELICITS PHYTOALEXIN ACCUMULATION IN SOYBEANS journal November 1981
Nonlinear partial differential equations and applications: Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells journal November 2002
The Growth Reduction Associated with Repressed Lignin Biosynthesis in Arabidopsis thaliana Is Independent of Flavonoids journal May 2010
Oligosaccharides as Signals and Substrates in the Plant Cell Wall journal September 1993
Pectins: structure, biosynthesis, and oligogalacturonide-related signaling journal July 2001
Vessel-Specific Reintroduction of CINNAMOYL-COA REDUCTASE1 (CCR1) in Dwarfed ccr1 Mutants Restores Vessel and Xylary Fiber Integrity and Increases Biomass journal November 2017
Plant cell surface receptor-mediated signaling – a common theme amid diversity journal January 2018
Chemically Induced Conditional Rescue of the Reduced Epidermal Fluorescence8 Mutant of Arabidopsis Reveals Rapid Restoration of Growth and Selective Turnover of Secondary Metabolite Pools journal December 2013
Lignin deficiency in transgenic flax resulted in plants with improved mechanical properties journal March 2007
Oligogalacturonide production upon Arabidopsis thalianaBotrytis cinerea interaction journal September 2019
Host–pathogen interactions journal August 2008
Oligosaccharins journal September 1985
Poplar Carbohydrate-Active Enzymes. Gene Identification and Expression Analyses journal January 2006
Aggregation during Coniferyl Alcohol Polymerization in Pectin Solution:  A Biomimetic Approach of the First Steps of Lignification journal March 2005
A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides journal May 2010
Linear β-1,3 Glucans Are Elicitors of Defense Responses in Tobacco journal November 2000
Two phenylalanine ammonia lyase isoforms are involved in the elicitor-induced response of rice to the fungal pathogen Magnaporthe oryzae journal February 2012
Signaling role of oligogalacturonides derived during cell wall degradation journal November 2012
Relation between Chemical Structure and Supramolecular Organization of Synthetic Lignin−Pectin Particles journal November 2009
Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development journal January 2013
Downregulation of pectin biosynthesis gene GAUT4 leads to reduced ferulate and lignin-carbohydrate cross-linking in switchgrass journal January 2019
Structure-activity relationships of biologically active oligosaccharides journal September 1991
The role of plant cell wall polysaccharide composition in disease resistance journal April 2004
ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 Are Polygalacturonases Required for Cell Separation during Reproductive Development in Arabidopsis journal January 2009
Plant immunity triggered by engineered in vivo release of oligogalacturonides, damage-associated molecular patterns journal April 2015
Transcriptional Regulation of Abscission Zones journal June 2019
Ethylene production in B otrytis cinerea‐ and oligogalacturonide‐induced immunity requires calcium‐dependent protein kinases journal November 2015
Activation tagging of Arabidopsis POLYGALACTURONASE INVOLVED IN EXPANSION2 promotes hypocotyl elongation, leaf expansion, stem lignification, mechanical stiffening, and lodging journal February 2017
Altering the Cell Wall and Its Impact on Plant Disease: From Forage to Bioenergy journal August 2014
Inhibition of 2,4-Dichlorophenoxyacetic Acid-Stimulated Elongation of Pea Stem Segments by a Xyloglucan Oligosaccharide journal June 1984
Proteinase inhibitor-inducing factor activity in tomato leaves resides in oligosaccharides enzymically released from cell walls journal June 1981
Cell Wall Ultrastructure of Stem Wood, Roots, and Needles of a Conifer Varies in Response to Moisture Availability journal June 2016
Examination of the Abscission-Associated Transcriptomes for Soybean, Tomato, and Arabidopsis Highlights the Conserved Biosynthesis of an Extensible Extracellular Matrix and Boundary Layer journal December 2015
Pectic Cell Wall Fragments Regulate Tobacco Thin-Cell-Layer Explant Morphogenesis journal August 1989
Cloning and characterization of irregular xylem4 (irx4):a severely lignin-deficient mutant of Arabidopsis journal April 2001
The Plant Cell Wall Integrity Maintenance Mechanism—Concepts for Organization and Mode of Action journal November 2014
Phytoalexins and Their Elicitors--A Defense Against Microbial Infection in Plants journal January 1984
Phytoalexins and their Elicitors-A Defense Against Microbial Infection in Plants journal June 1984
Oligosaccharins: structures and signal transduction journal December 1994
Molecular basis of symbiotic host specificity in rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals journal December 1991
Antimicrobial intermediates of the general phenylpropanoid and lignin specific pathways journal May 2000
Loosening lignin's grip on biofuel production journal July 2007
Dna journal October 1985

Cited By (1)

Pectin-derived immune elicitors in response to lignin modification in plants journal February 2020