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

Title: Lipopolysaccharide O-antigen delays plant innate immune recognition of Xylella fastidiosa

Journal Article · · Nature Communications
 [1];  [2]; ORCiD logo [3];  [4]; ORCiD logo [4];  [3];  [3];  [5]; ORCiD logo [4];  [5]
  1. Univ. of California, Riverside, CA (United States). Dept. of Microbiology and Plant Pathology; None
  2. Univ. of California, Davis, CA (United States). Dept. of Viticulture and Enology and Dept. of Plant Sciences
  3. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
  4. Univ. of California, Davis, CA (United States). Dept. of Viticulture and Enology
  5. Univ. of California, Riverside, CA (United States). Dept. of Microbiology and Plant Pathology

Lipopolysaccharides (LPS) are among the known pathogen-associated molecular patterns (PAMPs). LPSs are potent elicitors of PAMP-triggered immunity (PTI), and bacteria have evolved intricate mechanisms to dampen PTI. Here we demonstrate that Xylella fastidiosa (Xf), a hemibiotrophic plant pathogenic bacterium, possesses a long chain O-antigen that enables it to delay initial plant recognition, thereby allowing it to effectively skirt initial elicitation of innate immunity and establish itself in the host. Lack of the O-antigen modifies plant perception of Xf and enables elicitation of hallmarks of PTI, such as ROS production specifically in the plant xylem tissue compartment, a tissue not traditionally considered a spatial location of PTI. To explore translational applications of our findings, we demonstrate that pre-treatment of plants with Xf LPS primes grapevine defenses to confer tolerance to Xf challenge.

Research Organization:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division
Grant/Contract Number:
SC0015662
OSTI ID:
1523394
Journal Information:
Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 9; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (118)

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
The xylem as battleground for plant hosts and vascular wilt pathogens journal January 2013
Lipopolysaccharide Endotoxins journal June 2002
Water Deficit Modulates the Response of Vitis vinifera to the Pierce's Disease Pathogen Xylella fastidiosa journal June 2013
Mass Spectrometric Identification of Isoforms of PR Proteins in Xylem Sap of Fungus-Infected Tomato journal October 2002
Histological study of the responses of two Vitis vinifera cultivars (resistant and susceptible) to Plasmopara viticola infections journal September 2003
News from the frontline: recent insights into PAMP-triggered immunity in plants journal August 2008
Laminarin Elicits Defense Responses in Grapevine and Induces Protection Against Botrytis cinerea and Plasmopara viticola journal December 2003
Wheat TILLING Mutants Show That the Vernalization Gene VRN1 Down-Regulates the Flowering Repressor VRN2 in Leaves but Is Not Essential for Flowering journal December 2012
Structural heterogeneity in the lipopolysaccharides of Pseudomonas syringae with O-polysaccharide chains having different repeating units journal December 2001
Bacterial Lipopolysaccharides Induce Defense Responses Associated with Programmed Cell Death in Rice Cells journal November 2006
Somatic antigens of pseudomonads: Structure of the O-specific polysaccharide of the reference strain for Pseudomonas fluorescens (IMV 4125, ATCC 13525, biovar A) journal September 1996
Lipopolysaccharide Endotoxins journal June 2002
Mass Spectrometric Identification of Isoforms of PR Proteins in Xylem Sap of Fungus-Infected Tomato journal October 2002
Xylella fastidiosa : Cause of Pierce's Disease of Grapevine and Other Emergent Diseases journal October 2002
Functions of EDS1-like and PAD4 genes in grapevine defenses against powdery mildew journal August 2014
Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction journal June 1997
Genetic analysis of ABA signal transduction pathways journal June 1998
Alcian blue fixation allows silver staining of the isolated polysaccharide component of bacterial lipopolysaccharides in polyacrylamide gels journal January 1991
Vascular Defense Responses in Rice: Peroxidase Accumulation in Xylem Parenchyma Cells and Xylem Wall Thickening journal December 2001
Molecular aspects of defence priming journal October 2011
Benzothiadiazole-primed defence responses and enhanced differential expression of defence genes in Vitis vinifera infected with biotrophic pathogens Erysiphe necator and Plasmopara viticola journal May 2012
NMR and MS evidences for a random assembled O-specific chain structure in the LPS of the bacterium Xanthomonas campestris pv. Vitians: A case of unsystematic biosynthetic polymerization journal August 2002
The O-chain polysaccharide of the lipopolysaccharide of Xanthomonascampestris pv. begoniae GSPB 525 is a partially l-xylosylated l-rhamnan journal June 1999
Location of the O-methyl groups in the O polysaccharide of Pseudomonas syringae pv. phaseolicola journal February 2001
The effects of Pierce's disease on leaf and petiole hydraulic conductance in Vitis vinifera cv. Chardonnay journal August 2009
Molecular aspects of defence priming journal October 2011
The O-polysaccharide of Pseudomonas syringae pv. mori NCPPB 1656 is a β-(1→2)-linked homopolymer of l-rhamnose journal February 2004
VitisNet: “Omics” Integration through Grapevine Molecular Networks journal December 2009
The Elicitation of Plant Innate Immunity by Lipooligosaccharide of Xanthomonas campestris journal July 2005
Structural heterogeneity in the lipopolysaccharides of Pseudomonas syringae with O-polysaccharide chains having different repeating units journal December 2001
Arsenic exposure exacerbates atherosclerotic plaque formation and increases nitrotyrosine and leukotriene biosynthesis journal November 2004
Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response journal February 2006
Structure elucidation of the O-chain from the major lipopolysaccharide of the Xanthomonas campestris strain 642 journal April 2000
Bacterial rhamnolipids are novel MAMPs conferring resistance to Botrytis cinerea in grapevine journal February 2009
Grapevine Susceptibility to Pierce's Disease II: Progression of Anatomical Symptoms journal January 2004
Pseudomonas syringae lipopolysaccharides: Immunochemical characteristics and structure as a basis for strain classification journal February 2010
Impact of phyto-oxylipins in plant defense journal July 2002
Sequence/structural analysis of xylem proteome emphasizes pathogenesis-related proteins, chitinases and β -1, 3-glucanases as key players in grapevine defense against Xylella fastidiosa journal January 2016
Improved Resistance Against Botrytis cinerea by Grapevine-Associated Bacteria that Induce a Prime Oxidative Burst and Phytoalexin Production journal July 2011
Molecular modelling of bacterial deep rough mutant lipopolysaccharide of Escherichia coli journal May 1991
Location of the O-methyl groups in the O polysaccharide of Pseudomonas syringae pv. phaseolicola journal February 2001
Somatic antigens of pseudomonads: Structure of the O-specific polysaccharide of the reference strain for Pseudomonas fluorescens (IMV 4125, ATCC 13525, biovar A) journal September 1996
Structure elucidation of the O-chain from the major lipopolysaccharide of the Xanthomonas campestris strain 642 journal April 2000
Bacterial Lipopolysaccharides Induce Defense Responses Associated with Programmed Cell Death in Rice Cells journal November 2006
O-antigen structural variation: mechanisms and possible roles in animal/plant–microbe interactions journal March 2002
From The Cover: Innate immunity in Arabidopsis thaliana: Lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes journal October 2004
Transposon Mutagenesis of Xylella fastidiosa by Electroporation of Tn 5 Synaptic Complexes journal June 2001
The O-chain polysaccharide of the lipopolysaccharide of Xanthomonascampestris pv. begoniae GSPB 525 is a partially l-xylosylated l-rhamnan journal June 1999
Functions of RPM1-interacting protein 4 in plant immunity journal January 2021
Constitutive expression of abiotic stress-inducible hot pepper CaXTH3 , which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plants journal May 2006
The genome that fuelled a Mexican scientific revolution journal March 2022
Water Deficit Modulates the Response of Vitis vinifera to the Pierce's Disease Pathogen Xylella fastidiosa journal June 2013
A simple and rapid method for the permethylation of carbohydrates journal August 1984
Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture journal March 2021
Role of Cell Surface Lipopolysaccharides in Escherichia c oli K12 Adhesion and Transport journal August 2004
Electrophoretic Analysis of Lipopolysaccharides of Purple Nonsulfur Bacteria journal April 1988
Quantification of Bacterial Lipopolysaccharides by the Purpald Assay: Measuring Formaldehyde Generated from 2-keto-3-deoxyoctonate and Heptose at the Inner Core by Periodate Oxidation journal February 1999
Fastidious Xylem-Limited Bacterial Plant Pathogens journal September 1996
Structure of bacterial lipopolysaccharides journal November 2003
Prior exposure to lipopolysaccharide potentiates expression of plant defenses in response to bacteria journal February 2002
Structure of bacterial lipopolysaccharides journal November 2003
Structural Determination of theO-Specific Polysaccharide from theXanthomonas fragariaeLipopolysaccharide Fraction journal March 2001
Histological study of the responses of two Vitis vinifera cultivars (resistant and susceptible) to Plasmopara viticola infections journal September 2003
Expression of α-Expansin and Xyloglucan Endotransglucosylase/Hydrolase Genes Associated with Shoot Elongation Enhanced by Anoxia, Ethylene and Carbon Dioxide in Arrowhead (Sagittaria pygmaea Miq.) Tubers journal July 2005
Xylella fastidiosa Infection and Ethylene Exposure Result in Xylem and Water Movement Disruption in Grapevine Shoots journal December 2006
Early molecular events in PAMP-triggered immunity journal August 2009
The Structures of Lipopolysaccharides from Plant-Associated Gram-Negative Bacteria journal December 2009
Transposon Mutagenesis of Xylella fastidiosa by Electroporation of Tn 5 Synaptic Complexes journal June 2001
Functions of EDS1-like and PAD4 genes in grapevine defenses against powdery mildew journal August 2014
Structure of the O-specific polysaccharides of the lipopolysaccharides of Xanthomonas campestris pv. vignicola GSPB 2795 and GSPB 2796 journal December 2000
The plant immune system journal November 2006
Living in two Worlds: The Plant and Insect Lifestyles of Xylella fastidiosa journal September 2008
Vascular coating: a barrier to colonization by the pathogen in Verticillium wilt of tomato journal February 1989
Building lipid barriers: biosynthesis of cutin and suberin journal May 2008
Quantification of Bacterial Lipopolysaccharides by the Purpald Assay: Measuring Formaldehyde Generated from 2-keto-3-deoxyoctonate and Heptose at the Inner Core by Periodate Oxidation journal February 1999
Benzothiadiazole-primed defence responses and enhanced differential expression of defence genes in Vitis vinifera infected with biotrophic pathogens Erysiphe necator and Plasmopara viticola journal May 2012
A simple and rapid method for the permethylation of carbohydrates journal August 1984
News from the frontline: recent insights into PAMP-triggered immunity in plants journal August 2008
The role of lipopolysaccharides in induction of plant defence responses journal September 2003
Fastidious Xylem-Limited Bacterial Plant Pathogens journal September 1996
From The Cover: Innate immunity in Arabidopsis thaliana: Lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes journal October 2004
Identification of Xylella fastidiosa Antivirulence Genes: Hemagglutinin Adhesins Contribute to X. fastidiosa Biofilm Maturation and Colonization and Attenuate Virulence journal August 2005
Arsenic exposure exacerbates atherosclerotic plaque formation and increases nitrotyrosine and leukotriene biosynthesis journal November 2004
Building lipid barriers: biosynthesis of cutin and suberin journal May 2008
Bacterial elicitation and evasion of plant innate immunity journal August 2006
Vascular Occlusions in Grapevines with Pierce’s Disease Make Disease Symptom Development Worse journal January 2013
Genetic analysis of ABA signal transduction pathways journal June 1998
Impact of phyto-oxylipins in plant defense journal July 2002
Dynamics of the Lipopolysaccharide Assembly on the Surface of Escherichia c oli journal September 1999
Molecular and chemical characterization of the lipopolysaccharide O‐antigen and its role in the virulence of Yersinia enterocolitica serotype O:8 journal January 1997
Molecular modelling of bacterial deep rough mutant lipopolysaccharide of Escherichia coli journal May 1991
Role of Cell Surface Lipopolysaccharides in Escherichia c oli K12 Adhesion and Transport journal August 2004
The O-polysaccharide of Pseudomonas syringae pv. mori NCPPB 1656 is a β-(1→2)-linked homopolymer of l-rhamnose journal February 2004
Electrophoretic Analysis of Lipopolysaccharides of Purple Nonsulfur Bacteria journal April 1988
Wheat TILLING Mutants Show That the Vernalization Gene VRN1 Down-Regulates the Flowering Repressor VRN2 in Leaves but Is Not Essential for Flowering journal December 2012
The effects of Pierce's disease on leaf and petiole hydraulic conductance in Vitis vinifera cv. Chardonnay journal August 2009
Prior exposure to lipopolysaccharide potentiates expression of plant defenses in response to bacteria journal February 2002
The Elicitation of Plant Innate Immunity by Lipooligosaccharide of Xanthomonas campestris journal July 2005
Vascular Occlusions in Grapevines with Pierce’s Disease Make Disease Symptom Development Worse journal January 2013
Laminarin Elicits Defense Responses in Grapevine and Induces Protection Against Botrytis cinerea and Plasmopara viticola journal December 2003
A Large Family of Class III Plant Peroxidases journal May 2001
Vascular Defense Responses in Rice: Peroxidase Accumulation in Xylem Parenchyma Cells and Xylem Wall Thickening journal December 2001
Structure of the O-specific polysaccharides of the lipopolysaccharides of Xanthomonas campestris pv. vignicola GSPB 2795 and GSPB 2796 journal December 2000
Lipopolysaccharide and Its Interactions with Plants book January 2011
Constitutive expression of abiotic stress-inducible hot pepper CaXTH3 , which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plants journal May 2006
A simple, rapid, and reliable protocol to localize hydrogen peroxide in large plant organs by DAB-mediated tissue printing journal December 2014
Bacterial elicitation and evasion of plant innate immunity journal August 2006
O-antigen structural variation: mechanisms and possible roles in animal/plant–microbe interactions journal March 2002
VitisNet: “Omics” Integration through Grapevine Molecular Networks journal December 2009
Improved Resistance Against Botrytis cinerea by Grapevine-Associated Bacteria that Induce a Prime Oxidative Burst and Phytoalexin Production journal July 2011
Expression of α-Expansin and Xyloglucan Endotransglucosylase/Hydrolase Genes Associated with Shoot Elongation Enhanced by Anoxia, Ethylene and Carbon Dioxide in Arrowhead (Sagittaria pygmaea Miq.) Tubers journal July 2005
Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture journal November 2022
Sequence/structural analysis of xylem proteome emphasizes pathogenesis-related proteins, chitinases and β -1, 3-glucanases as key players in grapevine defense against Xylella fastidiosa journal January 2016
Pseudomonas spp.-induced systemic resistance to Botrytis cinerea is associated with induction and priming of defence responses in grapevine journal October 2009
The genome sequence of the plant pathogen Xylella fastidiosa journal July 2000
Pseudomonas syringae lipopolysaccharides: Immunochemical characteristics and structure as a basis for strain classification journal February 2010
A Rhamnose-Rich O-Antigen Mediates Adhesion, Virulence, and Host Colonization for the Xylem-Limited Phytopathogen Xylella fastidiosa journal June 2013

Cited By (21)

Tyrosine phosphorylation of the lectin receptor‐like kinase LORE regulates plant immunity journal January 2020
Pseudomonas can survive bacteriocin-mediated killing via a persistence-like mechanism posted_content March 2020
Molecular Effects of Xylella fastidiosa and Drought Combined Stress in Olive Trees journal October 2019
Lessons from One Fastidious Bacterium to Another: What Can We Learn about Liberibacter Species from Xylella fastidiosa journal September 2019
Loss of wbpL disrupts O ‐polysaccharide synthesis and impairs virulence of plant‐associated Pseudomonas strains journal August 2019
Genome-wide identification of Pseudomonas syringae genes required for fitness during colonization of the leaf surface and apoplast journal September 2019
The Role of Pseudomonas aeruginosa Lipopolysaccharide in Bacterial Pathogenesis and Physiology journal December 2019
The genetic basis of sex determination in grapevines (Vitis spp.) posted_content December 2019
Infections of the Xylella fastidiosa subsp. pauca Strain "De Donno" in Alfalfa (Medicago sativa) Elicits an Overactive Immune Response text January 2019
The genetic basis of sex determination in grapevines (Vitis spp.) posted_content December 2019
Bacterial and plant produced lipids can exacerbate the Olive Quick Decline Syndrome caused by Xylella posted_content December 2019
Molecular Profiling of Pierce’s Disease Outlines the Response Circuitry of Vitis vinifera to Xylella fastidiosa Infection journal June 2018
Infections of the Xylella fastidiosa subsp. pauca Strain “De Donno” in Alfalfa (Medicago sativa) Elicits an Overactive Immune Response journal September 2019
Trans-Graft Protection Against Pierce’s Disease Mediated by Transgenic Grapevine Rootstocks journal February 2019
Trans-Graft Protection Against Pierce’s Disease Mediated by Transgenic Grapevine Rootstocks journal February 2019
Ionomic Differences between Susceptible and Resistant Olive Cultivars Infected by Xylella fastidiosa in the Outbreak Area of Salento, Italy journal November 2019
Infections of the Xylella fastidiosa subsp. pauca Strain “De Donno” in Alfalfa (Medicago sativa) Elicits an Overactive Immune Response journal September 2019
Molecular Effects of Xylella fastidiosa and Drought Combined Stress in Olive Trees journal October 2019
Patterns of inter- and intrasubspecific homologous recombination inform eco-evolutionary dynamics of Xylella fastidiosa journal May 2019
Ionomic Differences between Susceptible and Resistant Olive Cultivars Infected by Xylella fastidiosa in the Outbreak Area of Salento, Italy journal November 2019
Recognition of Elicitors in Grapevine: From MAMP and DAMP Perception to Induced Resistance journal September 2019