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Title: The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium

Journal Article · · Science Advances
 [1];  [2];  [1];  [3];  [3];  [4];  [5];  [6];  [3];  [3];  [3];  [3];  [3];  [3];  [3];  [3];  [7];  [6];  [8];  [3] more »;  [1];  [4];  [9];  [9];  [10];  [6];  [7];  [5];  [4];  [1] « less
  1. Univ. of California, Davis, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of California, Davis, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Australian National Univ., Canberra, ACT (Australia)
  3. Univ. of California, Davis, CA (United States)
  4. Univ. of Tubingen (Germany)
  5. Univ. of Texas, Austin, TX (United States)
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  7. Univ. of California, Irvine, CA (United States)
  8. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Davis, CA (United States)
  9. Council of Scientific & Industrial Research (CSIR)–Inst. of Microbial Technology, Chandigarh (India)
  10. CSIR–Centre for Cellular and Molecular Biology, Hyderabad (India)

Surveillance of the extracellular environment by immune receptors is of central importance to eukaryotic survival. The rice receptor kinase XA21, which confers robust resistance to most strains of the Gram-negative bacterium Xanthomonas oryzae pv. oryzae (Xoo), is representative of a large class of cell surface immune receptors in plants and animals. We report the identification of a previously undescribed Xoo protein, called RaxX, which is required for activation of XA21-mediated immunity. Xoo strains that lack RaxX, or carry mutations in the single RaxX tyrosine residue (Y41), are able to evade XA21-mediated immunity. Y41 of RaxX is sulfated by the prokaryotic tyrosine sulfotransferase RaxST. Sulfated, but not nonsulfated, RaxX triggers hallmarks of the plant immune response in an XA21-dependent manner. A sulfated, 21-amino acid synthetic RaxX peptide (RaxX21-sY) is sufficient for this activity. Xoo field isolates that overcome XA21-mediated immunity encode an alternate raxX allele, suggesting that coevolutionary interactions between host and pathogen contribute to RaxX diversification. RaxX is highly conserved in many plant pathogenic Xanthomonas species. The new insights gained from the discovery and characterization of the sulfated protein, RaxX, can be applied to the development of resistant crop varieties and therapeutic reagents that have the potential to block microbial infection of both plants and animals.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); US Israel Binational Science Foundation; European Molecular Biology Organization; Human Frontiers Science Program; Council of Scientific and Industrial Research; Monsanto’s Beachell-Borlaug International Scholars Program
Grant/Contract Number:
AC02-05CH11231; GM59962; 2 2011062; ALTF 1290-2011; LT000674/2012; BSC0117; R21 GM099028; F1155
OSTI ID:
1625946
Alternate ID(s):
OSTI ID: 1836253
Journal Information:
Science Advances, Vol. 1, Issue 6; ISSN 2375-2548
Publisher:
AAASCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 161 works
Citation information provided by
Web of Science

References (67)

Processing and export of peptide pheromones and bacteriocins in Gram-negative bacteria journal April 2001
Plant and Animal Sensors of Conserved Microbial Signatures journal November 2010
Efficient expression of tyrosine-sulfated proteins in E. coli using an expanded genetic code journal November 2009
The Xanthomonas oryzae pv.◊oryzae raxP and raxQ genes encode an ATP sulphurylase and adenosine-5′-phosphosulphate kinase that are required for AvrXa21 avirulence activity: Bacterial avirulence determinants journal April 2002
Breeding the Thai jasmine rice variety KDML105 for non-age-related broad-spectrum resistance to bacterial blight disease based on combined marker-assisted and phenotypic selection journal October 2012
AAV-expressed eCD4-Ig provides durable protection from multiple SHIV challenges journal February 2015
Xa26 , a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein journal December 2003
Improvement of Bacterial Blight Resistance of ‘Minghui 63’, an Elite Restorer Line of Hybrid Rice, by Molecular Marker-Assisted Selection journal January 2000
A Renaissance of Elicitors: Perception of Microbe-Associated Molecular Patterns and Danger Signals by Pattern-Recognition Receptors journal June 2009
The Cloned Gene, Xa21, Confers Resistance to Multiple Xanthomonas oryzae pv. oryzae Isolates in Transgenic Plants journal January 1996
Fine-scale population structure and evidence for local adaptation in Australian giant black tiger shrimp (Penaeus monodon) using SNP analysis journal September 2020
Marker assisted introgression of bacterial blight resistance in Samba Mahsuri, an elite indica rice variety journal September 2007
Identification of a Biosynthetic Gene Cluster in Rice for Momilactones journal October 2007
The plant immune system journal November 2006
PSKR1 and PSY1R-mediated regulation of plant defense responses journal May 2013
An improved suicide vector for construction of chromosomal insertion mutations in bacteria journal September 1992
Integrating marker assisted background analysis with foreground selection for identification of superior bacterial blight resistant recombinants in Basmati rice journal April 2008
Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A journal January 2008
A Biological Sensor for Iron Available to Bacteria in Their Habitats on Plant Surfaces journal January 1994
Defective LPS Signaling in C3H/HeJ and C57BL/10ScCr Mice: Mutations in Tlr4 Gene journal December 1998
Plant PRRs and the Activation of Innate Immune Signaling journal April 2014
Characterization of a PR-10 Pathogenesis-Related Gene Family Induced in Rice During Infection with Magnaporthe grisea journal July 2001
Retraction journal October 2013
Advances in plant biotechnology and its adoption in developing countries journal April 2003
Plant and Animal Pathogen Recognition Receptors Signal through Non-RD Kinases journal January 2006
The broad bacterial blight resistance of rice line CBB23 is triggered by a novel transcription activator-like (TAL) effector of Xanthomonas oryzae pv. oryzae: AvrXa23 triggers broad disease resistance in rice journal December 2013
Identification of a Family of Avirulence Genes from Xanthomonas oryzae pv. oryzae journal January 1992
Tyrosine sulfation in a Gram-negative bacterium journal January 2012
A nonRD receptor-like kinase prevents nodule early senescence and defense-like reactions during symbiosis journal June 2014
A Versatile Platform for Single- and Multiple-Unnatural Amino Acid Mutagenesis in Escherichia coli journal February 2013
Non-arginine-aspartate (non-RD) kinases are associated with innate immune receptors that recognize conserved microbial signatures journal August 2012
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data journal April 2012
Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis journal November 2007
Plant Innate Immunity: Perception of Conserved Microbial Signatures journal June 2012
mProphet: automated data processing and statistical validation for large-scale SRM experiments journal March 2011
Pathotype and Genetic Diversity amongst Indian Isolates of Xanthomonas oryzae pv. oryzae journal November 2013
Skyline: an open source document editor for creating and analyzing targeted proteomics experiments journal February 2010
A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21 journal December 1995
Ectopic expression of rice Xa21 overcomes developmentally controlled resistance to Xanthomonas oryzae pv. oryzae journal November 2010
Posttranslationally Modified Small-Peptide Signals in Plants journal April 2014
An XA21-Associated Kinase (OsSERK2) Regulates Immunity Mediated by the XA21 and XA3 Immune Receptors journal May 2014
The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5 journal April 2001
Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A journal January 2008
Bacterial Genes Involved in Type I Secretion and Sulfation Are Required to Elicit the Rice Xa21 -Mediated Innate Immune Response journal June 2004
Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization journal January 2014
Recombinant expression of selectively sulfated proteins in Escherichia coli journal October 2006
Fls2 journal June 2000
Plants have a sensitive perception system for the most conserved domain of bacterial flagellin: Plants perceive a conserved domain of bacterial flagellin journal May 1999
Biosynthesis of Rice Phytoalexin: Enzymatic Conversion of 3β-Hydroxy-9β-pimara-7,15-dien-19,6β-olide to Momilactone A journal January 2002
Perception of the Bacterial PAMP EF-Tu by the Receptor EFR Restricts Agrobacterium-Mediated Transformation journal May 2006
A Novel Rice PR10 Protein, RSOsPR10, Specifically Induced in Roots by Biotic and Abiotic Stresses, Possibly via the Jasmonic Acid Signaling Pathway journal May 2004
The Xanthomonas Ax21 protein is processed by the general secretory system and is secreted in association with outer membrane vesicles journal January 2014
Introgression of bacterial blight resistance genes Xa7, Xa21, Xa22 and Xa23 into hybrid rice restorer lines by molecular marker-assisted selection journal July 2012
The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors journal April 2010
mProphet: automated data processing and statistical validation for large-scale SRM experiments text January 2011
The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner journal November 2012
An XA21-Associated Kinase (OsSERK2) regulates immunity mediated by the XA21 and XA3 immune receptors journal December 2013
The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1 journal October 2014
Direct Identification of Tyrosine Sulfation by using Ultraviolet Photodissociation Mass Spectrometry journal May 2014
Crystal structure of human tyrosylprotein sulfotransferase-2 reveals the mechanism of protein tyrosine sulfation reaction journal March 2013
Genomically Recoded Organisms Expand Biological Functions journal October 2013
A Rice Semi-Dwarf Gene, Tan-Ginbozu (D35), Encodes the Gibberellin Biosynthesis Enzyme, ent-Kaurene Oxidase journal March 2004
Transgenic Expression of the Dicotyledonous Pattern Recognition Receptor EFR in Rice Leads to Ligand-Dependent Activation of Defense Responses journal March 2015
Tyrosine Sulfation of the Amino Terminus of CCR5 Facilitates HIV-1 Entry journal March 1999
High-throughput Database Search and Large-scale Negative Polarity Liquid Chromatography–Tandem Mass Spectrometry with Ultraviolet Photodissociation for Complex Proteomic Samples journal May 2013
Mutagenesis of all Eight avr Genes in Xanthomonas campestris pv. campestris Had No Detected Effect on Pathogenicity, But One avr Gene Affected Race Specificity journal December 2005
A B-lectin receptor kinase gene conferring rice blast resistance journal June 2006

Cited By (39)

Molecular genetics and evolution of disease resistance in cereals journal July 2016
The pattern-recognition receptor CORE of Solanaceae detects bacterial cold-shock protein journal November 2016
PAMPs, PRRs, effectors and R-genes associated with citrus–pathogen interactions journal January 2017
Expression of the Arabidopsis thaliana immune receptor EFR in Medicago truncatula reduces infection by a root pathogenic bacterium, but not nitrogen-fixing rhizobial symbiosis journal September 2018
MAMP-triggered plant immunity mediated by the LysM-receptor kinase CERK1 journal November 2018
Contribution of recent technological advances to future resistance breeding text January 2019
Regulation of pattern recognition receptor signalling in plants journal August 2016
Expression of the Arabidopsis thaliana immune receptor EFR in Medicago truncatula reduces infection by a root pathogenic bacterium, but not nitrogen‐fixing rhizobial symbiosis text January 2019
Rice Routes of Countering Xanthomonas oryzae journal October 2018
Expression Profile of Defense Genes in Rice Lines Pyramided with Resistance Genes Against Bacterial Blight, Fungal Blast and Insect Gall Midge journal July 2018
Genomic screens identify a new phytobacterial microbe-associated molecular pattern and the cognate Arabidopsis receptor-like kinase that mediates its immune elicitation journal May 2016
Exploring the mechanism and efficient use of a durable gene-mediated resistance to bacterial blight disease in rice journal January 2018
Four tyrosine residues of the rice immune receptor XA21 are not required for interaction with the co-receptor OsSERK2 or resistance to Xanthomonas oryzae pv. oryzae journal January 2018
Silencing of the Rice Gene LRR1 Compromises Rice Xa21 Transcript Accumulation and XA21-Mediated Immunity journal May 2017
Overexpression of Rice Auxilin-Like Protein, XB21, Induces Necrotic Lesions, up-Regulates Endocytosis-Related Genes, and Confers Enhanced Resistance to Xanthomonas oryzae pv. oryzae journal June 2017
Lsp family proteins regulate antibiotic biosynthesis in Lysobacter enzymogenes OH11 journal June 2017
OsLRR-RLK1, an early responsive leucine-rich repeat receptor-like kinase, initiates rice defense responses against a chewing herbivore journal June 2018
Identification of a locus in maize controlling response to a host-selective toxin derived from Cochliobolus heterostrophus, causal agent of southern leaf blight journal September 2018
Population genomic insights into variation and evolution of Xanthomonas oryzae pv. oryzae journal January 2017
The rice XA21 ectodomain fused to the Arabidopsis EFR cytoplasmic domain confers resistance to Xanthomonas oryzae pv. oryzae journal January 2018
SlBIR3 Negatively Regulates PAMP Responses and Cell Death in Tomato journal September 2017
PAMPs, PRRs, effectors and R-genes associated with citrus–pathogen interactions journal June 2017
Variation and inheritance of the Xanthomonas raxX‐raxSTAB gene cluster required for activation of XA21‐mediated immunity journal February 2019
OsLRR-RLK1, an early responsive leucine-rich repeat receptor-like kinase, initiates rice defense responses against a chewing herbivore text January 2018
Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor journal April 2019
An update on molecular mechanism of disease resistance genes and their application for genetic improvement of rice journal November 2019
Pattern recognition receptors and signaling in plant-microbe interactions journal February 2018
Resistance Genes and their Interactions with Bacterial Blight/Leaf Streak Pathogens (Xanthomonas oryzae) in Rice (Oryza sativa L.)—an Updated Review journal January 2020
Fusarium oxysporum colonizes the stem of resistant tomato plants, the extent varying with the R-gene present journal September 2018
LRR-RLK family from two Citrus species: genome-wide identification and evolutionary aspects journal August 2016
Apoplastic invasion patterns triggering plant immunity: plasma membrane sensing at the frontline journal July 2019
Contribution of recent technological advances to future resistance breeding journal February 2019
PRRs and NB-LRRs: From Signal Perception to Activation of Plant Innate Immunity journal April 2019
Genetic modification to improve disease resistance in crops journal July 2019
Marker assisted introgression of genes governing resistance to bacterial blight and blast diseases into an elite Basmati rice variety, ‘Pusa Basmati 1509’ journal January 2020
Transcriptional insights into the pyramided resistance to rice bacterial blight journal August 2018
The Rice Xa3 Gene Confers Resistance to Xanthomonas oryzae pv. oryzae in the Model Rice Kitaake Genetic Background journal February 2020
Expression of the Arabidopsis thaliana immune receptor EFR in Medicago truncatula reduces infection by a root pathogenic bacterium, but not nitrogen‐fixing rhizobial symbiosis text January 2019
Mutation of the rice XA21 predicted nuclear localization sequence does not affect resistance to Xanthomonas oryzae pv. oryzae journal January 2016

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