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Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor
Abstract
The rice immune receptor XA21 is activated by the sulfated microbial peptide required for activation of XA21-mediated immunity X (RaxX) produced by Xanthomonas oryzae pv. oryzae(Xoo). Mutational studies and targeted proteomics revealed that the RaxX precursor peptide (proRaxX) is processed and secreted by the protease/transporter RaxB, the function of which can be partially fulfilled by a noncognate peptidase-containing transporter component B (PctB). proRaxX is cleaved at a Gly–Gly motif, yielding a mature peptide that retains the necessary elements for RaxX function as an immunogen and host peptide hormone mimic. These results indicate that RaxX is a prokaryotic member of a previously unclassified and understudied group of eukaryotic tyrosine sulfated ribosomally synthesized, posttranslationally modified peptides (RiPPs). We further demonstrate that sulfated RaxX directly binds XA21 with high affinity. This work reveals a complete, previously uncharacterized biological process: bacterial RiPP biosynthesis, secretion, binding to a eukaryotic receptor, and triggering of a robust host immune response.
- Authors:
-
[1];
[2];
[1];
[2]
- Department of Plant Pathology, University of California, Davis, CA 95616,, The Genome Center, University of California, Davis, CA 95616,
- Department of Plant Pathology, University of California, Davis, CA 95616,, The Genome Center, University of California, Davis, CA 95616,, Feedstocks Division, Joint Bioenergy Institute, Emeryville, CA 94608,
- Technology Division, Joint Bioenergy Institute, Emeryville, CA 94608,
- Gregor Mendel Institute, Austrian Academy of Sciences, 1030 Vienna, Austria,
- Department of Microbiology &, Molecular Genetics, University of California, Davis, CA 95616
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1505236
- Alternate Identifier(s):
- OSTI ID: 1561911
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Journal Article: Published Article
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 17; Journal ID: ISSN 0027-8424
- Publisher:
- Proceedings of the National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Luu, Dee Dee, Joe, Anna, Chen, Yan, Parys, Katarzyna, Bahar, Ofir, Pruitt, Rory, Chan, Leanne Jade G., Petzold, Christopher J., Long, Kelsey, Adamchak, Clifford, Stewart, Valley, Belkhadir, Youssef, and Ronald, Pamela C. Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor. United States: N. p., 2019.
Web. doi:10.1073/pnas.1818275116.
Luu, Dee Dee, Joe, Anna, Chen, Yan, Parys, Katarzyna, Bahar, Ofir, Pruitt, Rory, Chan, Leanne Jade G., Petzold, Christopher J., Long, Kelsey, Adamchak, Clifford, Stewart, Valley, Belkhadir, Youssef, & Ronald, Pamela C. Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor. United States. https://doi.org/10.1073/pnas.1818275116
Luu, Dee Dee, Joe, Anna, Chen, Yan, Parys, Katarzyna, Bahar, Ofir, Pruitt, Rory, Chan, Leanne Jade G., Petzold, Christopher J., Long, Kelsey, Adamchak, Clifford, Stewart, Valley, Belkhadir, Youssef, and Ronald, Pamela C. 2019.
"Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor". United States. https://doi.org/10.1073/pnas.1818275116.
@article{osti_1505236,
title = {Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor},
author = {Luu, Dee Dee and Joe, Anna and Chen, Yan and Parys, Katarzyna and Bahar, Ofir and Pruitt, Rory and Chan, Leanne Jade G. and Petzold, Christopher J. and Long, Kelsey and Adamchak, Clifford and Stewart, Valley and Belkhadir, Youssef and Ronald, Pamela C.},
abstractNote = {The rice immune receptor XA21 is activated by the sulfated microbial peptide required for activation of XA21-mediated immunity X (RaxX) produced by Xanthomonas oryzae pv. oryzae(Xoo). Mutational studies and targeted proteomics revealed that the RaxX precursor peptide (proRaxX) is processed and secreted by the protease/transporter RaxB, the function of which can be partially fulfilled by a noncognate peptidase-containing transporter component B (PctB). proRaxX is cleaved at a Gly–Gly motif, yielding a mature peptide that retains the necessary elements for RaxX function as an immunogen and host peptide hormone mimic. These results indicate that RaxX is a prokaryotic member of a previously unclassified and understudied group of eukaryotic tyrosine sulfated ribosomally synthesized, posttranslationally modified peptides (RiPPs). We further demonstrate that sulfated RaxX directly binds XA21 with high affinity. This work reveals a complete, previously uncharacterized biological process: bacterial RiPP biosynthesis, secretion, binding to a eukaryotic receptor, and triggering of a robust host immune response.},
doi = {10.1073/pnas.1818275116},
url = {https://www.osti.gov/biblio/1505236},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
issn = {0027-8424},
number = 17,
volume = 116,
place = {United States},
year = {Thu Apr 04 00:00:00 EDT 2019},
month = {Thu Apr 04 00:00:00 EDT 2019}
}
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Works referenced in this record:
Standard Flow Liquid Chromatography for Shotgun Proteomics in Bioenergy Research
journal, April 2015
- González Fernández-Niño, Susana M.; Smith-Moritz, A. Michelle; Chan, Leanne Jade G.
- Frontiers in Bioengineering and Biotechnology, Vol. 3
Substrate Specificity of the Secreted Nisin Leader Peptidase NisP
journal, July 2017
- Lagedroste, Marcel; Smits, Sander H. J.; Schmitt, Lutz
- Biochemistry, Vol. 56, Issue 30
Non-arginine-aspartate (non-RD) kinases are associated with innate immune receptors that recognize conserved microbial signatures
journal, August 2012
- Dardick, Chris; Schwessinger, Benjamin; Ronald, Pamela
- Current Opinion in Plant Biology, Vol. 15, Issue 4
The Majority of the Type III Effector Inventory of Pseudomonas syringae pv. tomato DC3000 Can Suppress Plant Immunity
journal, September 2009
- Guo, Ming; Tian, Fang; Wamboldt, Yashitola
- Molecular Plant-Microbe Interactions, Vol. 22, Issue 9
Peptide signal molecules and bacteriocins in Gram-negative bacteria: a genome-wide in silico screening for peptides containing a double-glycine leader sequence and their cognate transporters
journal, September 2004
- Dirix, G.; Monsieurs, P.; Dombrecht, B.
- Peptides, Vol. 25, Issue 9
Allosteric receptor activation by the plant peptide hormone phytosulfokine
journal, August 2015
- Wang, Jizong; Li, Hongju; Han, Zhifu
- Nature, Vol. 525, Issue 7568
Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension
journal, April 1989
- Horton, Robert M.; Hunt, Henry D.; Ho, Steffan N.
- Gene, Vol. 77, Issue 1, p. 61-68
A microbially derived tyrosine-sulfated peptide mimics a plant peptide hormone
journal, May 2017
- Pruitt, Rory N.; Joe, Anna; Zhang, Weiguo
- New Phytologist, Vol. 215, Issue 2
Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis
journal, November 2007
- Amano, Y.; Tsubouchi, H.; Shinohara, H.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 46
Identification of a novel two-peptide lantibiotic, Haloduracin, produced by the alkaliphile Bacillus halodurans C-125
journal, February 2007
- Lawton, Elaine M.; Cotter, Paul D.; Hill, Colin
- FEMS Microbiology Letters, Vol. 267, Issue 1
Chimeric Leader Peptides for the Generation of Non-Natural Hybrid RiPP Products
journal, June 2017
- Burkhart, Brandon J.; Kakkar, Nidhi; Hudson, Graham A.
- ACS Central Science, Vol. 3, Issue 6
Tyrosine sulfation: an increasingly recognised post-translational modification of secreted proteins
journal, June 2009
- Stone, Martin J.; Chuang, Sara; Hou, Xu
- New Biotechnology, Vol. 25, Issue 5
Bioengineering of lanthipeptides in Escherichia coli: assessing the specificity of lichenicidin and haloduracin biosynthetic machinery
journal, September 2014
- Caetano, T.; Barbosa, J.; Möesker, E.
- Research in Microbiology, Vol. 165, Issue 7
An RTX Transporter Tethers Its Unfolded Substrate during Secretion via a Unique N-Terminal Domain
journal, October 2012
- Lecher, Justin; Schwarz, Christian K. W.; Stoldt, Matthias
- Structure, Vol. 20, Issue 10
The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium
journal, July 2015
- Pruitt, Rory N.; Schwessinger, Benjamin; Joe, Anna
- Science Advances, Vol. 1, Issue 6
Heterologous expression of bacteriocins using the mesentericin Y105 dedicated transport system by Leuconostoc mesenteroides
journal, May 2002
- Morisset, Dany; Frère, Jacques
- Biochimie, Vol. 84, Issue 5-6
Protein-binding assays in biological liquids using microscale thermophoresis
journal, October 2010
- Wienken, Christoph J.; Baaske, Philipp; Rothbauer, Ulrich
- Nature Communications, Vol. 1, Issue 1
Genetic analysis of the colicin V secretion pathway.
journal, September 1995
- Zhang, L. H.; Fath, M. J.; Mahanty, H. K.
- Genetics, Vol. 141, Issue 1
A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21
journal, December 1995
- Song, W. -Y.; Wang, G. -L.; Chen, L. -L.
- Science, Vol. 270, Issue 5243
Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor
journal, January 2017
- Doblas, Verónica G.; Smakowska-Luzan, Elwira; Fujita, Satoshi
- Science, Vol. 355, Issue 6322
A targeted proteomics toolkit for high-throughput absolute quantification of Escherichia coli proteins
journal, November 2014
- Batth, Tanveer S.; Singh, Pragya; Ramakrishnan, Vikram R.
- Metabolic Engineering, Vol. 26
Mutational Analysis of Cvab, an ABC Transporter Involved in the Secretion of Active Colicin V
journal, April 2012
- Wu, Kai-Hui; Hsieh, Ying-Hsin; Tai, Phang C.
- PLoS ONE, Vol. 7, Issue 4
Substrate Recognition Mechanism of the Peptidase Domain of the Quorum-Sensing-Signal−Producing ABC Transporter ComA from Streptococcus †
journal, February 2008
- Kotake, Yatsugu; Ishii, Seiji; Yano, Takato
- Biochemistry, Vol. 47, Issue 8
On the acquisition and analysis of microscale thermophoresis data
journal, March 2016
- Scheuermann, Thomas H.; Padrick, Shae B.; Gardner, Kevin H.
- Analytical Biochemistry, Vol. 496
In Vitro Reconstitution and Substrate Specificity of a Lantibiotic Protease †
journal, July 2008
- Furgerson Ihnken, L. A.; Chatterjee, Champak; van der Donk, Wilfred A.
- Biochemistry, Vol. 47, Issue 28
Expression of Xanthomonas oryzae pv. oryzae hrp Genes in XOM2, a Novel Synthetic Medium
journal, December 2002
- Tsuge, Seiji; Furutani, Ayako; Fukunaka, Rie
- Journal of General Plant Pathology, Vol. 68, Issue 4
Crystal Structure of the Peptidase Domain of Streptococcus ComA, a Bifunctional ATP-binding Cassette Transporter Involved in the Quorum-sensing Pathway
journal, January 2010
- Ishii, Seiji; Yano, Takato; Ebihara, Akio
- Journal of Biological Chemistry, Vol. 285, Issue 14
Bacterial Genes Involved in Type I Secretion and Sulfation Are Required to Elicit the Rice Xa21 -Mediated Innate Immune Response
journal, June 2004
- da Silva, Francisco Goes; Shen, Yuwei; Dardick, Christopher
- Molecular Plant-Microbe Interactions, Vol. 17, Issue 6
Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L.
journal, July 1996
- Matsubayashi, Y.; Sakagami, Y.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 15
The leader peptide of colicin V shares consensus sequences with leader peptides that are common among peptide bacteriocins produced by Gram-positive bacteria
journal, September 1994
- Havarstein, L. S.; Holo, H.; Nes, I. F.
- Microbiology, Vol. 140, Issue 9
WebLogo: A Sequence Logo Generator
journal, May 2004
- Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc
- Genome Research, Vol. 14, Issue 6, p. 1188-1190
An Engineered Lantibiotic Synthetase That Does Not Require a Leader Peptide on Its Substrate
journal, April 2012
- Oman, Trent J.; Knerr, Patrick J.; Bindman, Noah A.
- Journal of the American Chemical Society, Vol. 134, Issue 16
A second-generation expression system for tyrosine-sulfated proteins and its application in crop protection
journal, January 2016
- Schwessinger, Benjamin; Li, Xiang; Ellinghaus, Thomas L.
- Integrative Biology, Vol. 8, Issue 4
A peptide hormone required for Casparian strip diffusion barrier formation in Arabidopsis roots
journal, January 2017
- Nakayama, Takuya; Shinohara, Hidefumi; Tanaka, Mina
- Science, Vol. 355, Issue 6322
Influence of Amino Acid Substitutions in the Leader Peptide on Maturation and Secretion of Mesentericin Y105 by Leuconostoc mesenteroides
journal, March 2005
- Aucher, W.; Lacombe, C.; Hequet, A.
- Journal of Bacteriology, Vol. 187, Issue 6
Mutational analysis of the putative leukotoxin transport genes in Actinobacillus actinomycetemcomitans
journal, May 1995
- Guthmiller, Janet M.; Kolodrubetz, David; Kraig, Ellen
- Microbial Pathogenesis, Vol. 18, Issue 5
The Rhomboid-Like Superfamily: Molecular Mechanisms and Biological Roles
journal, October 2014
- Freeman, Matthew
- Annual Review of Cell and Developmental Biology, Vol. 30, Issue 1
A new method to customize protein expression vectors for fast, efficient and background free parallel cloning
journal, January 2013
- Scholz, Judith; Besir, Hüseyin; Strasser, Claudia
- BMC Biotechnology, Vol. 13, Issue 1
Cys 32 and His 105 Are the Critical Residues for the Calcium-dependent Cysteine Proteolytic Activity of CvaB, an ATP-binding Cassette Transporter
journal, October 2003
- Wu, Kai-Hui; Tai, Phang C.
- Journal of Biological Chemistry, Vol. 279, Issue 2
A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export
journal, April 1995
- Havarstein, Leiv Sigve; Diep, Dzung Bao; Nes, Ingolf F.
- Molecular Microbiology, Vol. 16, Issue 2
Insights into AMS/PCAT transporters from biochemical and structural characterization of a double Glycine motif protease
journal, January 2019
- Bobeica, Silvia C.; Dong, Shi-Hui; Huo, Liujie
- eLife, Vol. 8
The Xanthomonas Ax21 protein is processed by the general secretory system and is secreted in association with outer membrane vesicles
journal, January 2014
- Bahar, Ofir; Pruitt, Rory; Luu, Dee Dee
- PeerJ, Vol. 2
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
- Castañeda, Adriana; Reddy, Joseph D.; El-Yacoubi, Basma
- Molecular Plant-Microbe Interactions, Vol. 18, Issue 12
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011
- Sievers, Fabian; Wilm, Andreas; Dineen, David
- Molecular Systems Biology, Vol. 7, Issue 1
Expression and Characterization of the Peptidase Domain of Streptococcus pneumoniae ComA, a Bifunctional ATP-binding Cassette Transporter Involved in Quorum Sensing Pathway
journal, December 2005
- Ishii, Seiji; Yano, Takato; Hayashi, Hideyuki
- Journal of Biological Chemistry, Vol. 281, Issue 8
ATP-dependent leader peptide cleavage by NukT, a bifunctional ABC transporter, during lantibiotic biosynthesis
journal, December 2009
- Nishie, Mami; Shioya, Kouki; Nagao, Jun-ichi
- Journal of Bioscience and Bioengineering, Vol. 108, Issue 6
Identification of a Family of Avirulence Genes from Xanthomonas oryzae pv. oryzae
journal, January 1992
- Hopkins, C. M.
- Molecular Plant-Microbe Interactions, Vol. 5, Issue 6
Contribution of the glutamine 19 side chain to transition-state stabilization in the oxyanion hole of papain
journal, September 1991
- Menard, Robert; Carriere, Julie; Laflamme, Pierre
- Biochemistry, Vol. 30, Issue 37
Tyrosine sulfation in a Gram-negative bacterium
journal, January 2012
- Han, Sang-Wook; Lee, Sang-Won; Bahar, Ofir
- Nature Communications, Vol. 3, Issue 1
Secreted Peptide Signals Required for Maintenance of Root Stem Cell Niche in Arabidopsis
journal, August 2010
- Matsuzaki, Y.; Ogawa-Ohnishi, M.; Mori, A.
- Science, Vol. 329, Issue 5995
Tyrosine Sulfation of the Amino Terminus of CCR5 Facilitates HIV-1 Entry
journal, March 1999
- Farzan, Michael; Mirzabekov, Tajib; Kolchinsky, Peter
- Cell, Vol. 96, Issue 5
Suppression of bacterial infection in rice by treatment with a sulfated peptide: Suppression of bacterial infection in rice
journal, April 2016
- Wei, Tong; Chern, Mawsheng; Liu, Furong
- Molecular Plant Pathology, Vol. 17, Issue 9
Follow the leader: the use of leader peptides to guide natural product biosynthesis
journal, December 2009
- Oman, Trent J.; van der Donk, Wilfred A.
- Nature Chemical Biology, Vol. 6, Issue 1
Type I secretion systems – a story of appendices
journal, July 2013
- Kanonenberg, Kerstin; Schwarz, Christian K. W.; Schmitt, Lutz
- Research in Microbiology, Vol. 164, Issue 6