Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor

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.

doi:10.1073/pnas.1818275116

Title: Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor

Journal Article · Thu Apr 04 00:00:00 EDT 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1818275116· OSTI ID:1505236

^[1];

^[2]; Chen, Yan ^[3]; Parys, Katarzyna ^[4];

^[1]; Pruitt, Rory ^[1]; Chan, Leanne Jade G. ^[3]; Petzold, Christopher J. ^[3]; Long, Kelsey ^[1]; Adamchak, Clifford ^[1]; Stewart, Valley ^[5]; Belkhadir, Youssef ^[4];

^[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

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1505236

Alternate ID(s):: OSTI ID: 1561911

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 116 Journal Issue: 17; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 51 works

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References (54)

Standard Flow Liquid Chromatography for Shotgun Proteomics in Bioenergy Research González Fernández-Niño, Susana M.; Smith-Moritz, A. Michelle; Chan, Leanne Jade G. Frontiers in Bioengineering and Biotechnology, Vol. 3 https://doi.org/10.3389/fbioe.2015.00044	journal	April 2015
Substrate Specificity of the Secreted Nisin Leader Peptidase NisP Lagedroste, Marcel; Smits, Sander H. J.; Schmitt, Lutz Biochemistry, Vol. 56, Issue 30 https://doi.org/10.1021/acs.biochem.7b00524	journal	July 2017
Non-arginine-aspartate (non-RD) kinases are associated with innate immune receptors that recognize conserved microbial signatures Dardick, Chris; Schwessinger, Benjamin; Ronald, Pamela Current Opinion in Plant Biology, Vol. 15, Issue 4 https://doi.org/10.1016/j.pbi.2012.05.002	journal	August 2012
The Majority of the Type III Effector Inventory of Pseudomonas syringae pv. tomato DC3000 Can Suppress Plant Immunity Guo, Ming; Tian, Fang; Wamboldt, Yashitola Molecular Plant-Microbe Interactions, Vol. 22, Issue 9 https://doi.org/10.1094/MPMI-22-9-1069	journal	September 2009
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 Dirix, G.; Monsieurs, P.; Dombrecht, B. Peptides, Vol. 25, Issue 9 https://doi.org/10.1016/j.peptides.2003.10.028	journal	September 2004
Allosteric receptor activation by the plant peptide hormone phytosulfokine Wang, Jizong; Li, Hongju; Han, Zhifu Nature, Vol. 525, Issue 7568 https://doi.org/10.1038/nature14858	journal	August 2015
Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension Horton, Robert M.; Hunt, Henry D.; Ho, Steffan N. Gene, Vol. 77, Issue 1, p. 61-68 https://doi.org/10.1016/0378-1119(89)90359-4	journal	April 1989
A microbially derived tyrosine-sulfated peptide mimics a plant peptide hormone Pruitt, Rory N.; Joe, Anna; Zhang, Weiguo New Phytologist, Vol. 215, Issue 2 https://doi.org/10.1111/nph.14609	journal	May 2017
Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis Amano, Y.; Tsubouchi, H.; Shinohara, H. Proceedings of the National Academy of Sciences, Vol. 104, Issue 46 https://doi.org/10.1073/pnas.0706403104	journal	November 2007
Identification of a novel two-peptide lantibiotic, Haloduracin, produced by the alkaliphile Bacillus halodurans C-125 Lawton, Elaine M.; Cotter, Paul D.; Hill, Colin FEMS Microbiology Letters, Vol. 267, Issue 1 https://doi.org/10.1111/j.1574-6968.2006.00539.x	journal	February 2007
Chimeric Leader Peptides for the Generation of Non-Natural Hybrid RiPP Products Burkhart, Brandon J.; Kakkar, Nidhi; Hudson, Graham A. ACS Central Science, Vol. 3, Issue 6 https://doi.org/10.1021/acscentsci.7b00141	journal	June 2017
Tyrosine sulfation: an increasingly recognised post-translational modification of secreted proteins Stone, Martin J.; Chuang, Sara; Hou, Xu New Biotechnology, Vol. 25, Issue 5 https://doi.org/10.1016/j.nbt.2009.03.011	journal	June 2009
Bioengineering of lanthipeptides in Escherichia coli: assessing the specificity of lichenicidin and haloduracin biosynthetic machinery Caetano, T.; Barbosa, J.; Möesker, E. Research in Microbiology, Vol. 165, Issue 7 https://doi.org/10.1016/j.resmic.2014.07.006	journal	September 2014
An RTX Transporter Tethers Its Unfolded Substrate during Secretion via a Unique N-Terminal Domain Lecher, Justin; Schwarz, Christian K. W.; Stoldt, Matthias Structure, Vol. 20, Issue 10 https://doi.org/10.1016/j.str.2012.08.005	journal	October 2012
The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium Pruitt, Rory N.; Schwessinger, Benjamin; Joe, Anna Science Advances, Vol. 1, Issue 6 https://doi.org/10.1126/sciadv.1500245	journal	July 2015
Heterologous expression of bacteriocins using the mesentericin Y105 dedicated transport system by Leuconostoc mesenteroides Morisset, Dany; Frère, Jacques Biochimie, Vol. 84, Issue 5-6 https://doi.org/10.1016/S0300-9084(02)01413-X	journal	May 2002
Protein-binding assays in biological liquids using microscale thermophoresis Wienken, Christoph J.; Baaske, Philipp; Rothbauer, Ulrich Nature Communications, Vol. 1, Issue 1 https://doi.org/10.1038/ncomms1093	journal	October 2010
Genetic analysis of the colicin V secretion pathway. Zhang, L. H.; Fath, M. J.; Mahanty, H. K. Genetics, Vol. 141, Issue 1 https://doi.org/10.1093/genetics/141.1.25	journal	September 1995
A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21 Song, W. -Y.; Wang, G. -L.; Chen, L. -L. Science, Vol. 270, Issue 5243 https://doi.org/10.1126/science.270.5243.1804	journal	December 1995
Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor Doblas, Verónica G.; Smakowska-Luzan, Elwira; Fujita, Satoshi Science, Vol. 355, Issue 6322 https://doi.org/10.1126/science.aaj1562	journal	January 2017
A targeted proteomics toolkit for high-throughput absolute quantification of Escherichia coli proteins Batth, Tanveer S.; Singh, Pragya; Ramakrishnan, Vikram R. Metabolic Engineering, Vol. 26 https://doi.org/10.1016/j.ymben.2014.08.004	journal	November 2014
Mutational Analysis of Cvab, an ABC Transporter Involved in the Secretion of Active Colicin V Wu, Kai-Hui; Hsieh, Ying-Hsin; Tai, Phang C. PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0035382	journal	April 2012
Substrate Recognition Mechanism of the Peptidase Domain of the Quorum-Sensing-Signal−Producing ABC Transporter ComA from Streptococcus ^† Kotake, Yatsugu; Ishii, Seiji; Yano, Takato Biochemistry, Vol. 47, Issue 8 https://doi.org/10.1021/bi702253n	journal	February 2008
On the acquisition and analysis of microscale thermophoresis data Scheuermann, Thomas H.; Padrick, Shae B.; Gardner, Kevin H. Analytical Biochemistry, Vol. 496 https://doi.org/10.1016/j.ab.2015.12.013	journal	March 2016
In Vitro Reconstitution and Substrate Specificity of a Lantibiotic Protease ^† Furgerson Ihnken, L. A.; Chatterjee, Champak; van der Donk, Wilfred A. Biochemistry, Vol. 47, Issue 28 https://doi.org/10.1021/bi800278n	journal	July 2008
Expression of Xanthomonas oryzae pv. oryzae hrp Genes in XOM2, a Novel Synthetic Medium Tsuge, Seiji; Furutani, Ayako; Fukunaka, Rie Journal of General Plant Pathology, Vol. 68, Issue 4 https://doi.org/10.1007/PL00013104	journal	December 2002
Crystal Structure of the Peptidase Domain of Streptococcus ComA, a Bifunctional ATP-binding Cassette Transporter Involved in the Quorum-sensing Pathway Ishii, Seiji; Yano, Takato; Ebihara, Akio Journal of Biological Chemistry, Vol. 285, Issue 14 https://doi.org/10.1074/jbc.M109.093781	journal	January 2010
Bacterial Genes Involved in Type I Secretion and Sulfation Are Required to Elicit the Rice Xa21 -Mediated Innate Immune Response da Silva, Francisco Goes; Shen, Yuwei; Dardick, Christopher Molecular Plant-Microbe Interactions, Vol. 17, Issue 6 https://doi.org/10.1094/MPMI.2004.17.6.593	journal	June 2004
Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Matsubayashi, Y.; Sakagami, Y. Proceedings of the National Academy of Sciences, Vol. 93, Issue 15 https://doi.org/10.1073/pnas.93.15.7623	journal	July 1996
The leader peptide of colicin V shares consensus sequences with leader peptides that are common among peptide bacteriocins produced by Gram-positive bacteria Havarstein, L. S.; Holo, H.; Nes, I. F. Microbiology, Vol. 140, Issue 9 https://doi.org/10.1099/13500872-140-9-2383	journal	September 1994
WebLogo: A Sequence Logo Generator Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc Genome Research, Vol. 14, Issue 6, p. 1188-1190 https://doi.org/10.1101/gr.849004	journal	May 2004
An Engineered Lantibiotic Synthetase That Does Not Require a Leader Peptide on Its Substrate Oman, Trent J.; Knerr, Patrick J.; Bindman, Noah A. Journal of the American Chemical Society, Vol. 134, Issue 16 https://doi.org/10.1021/ja3017297	journal	April 2012
A second-generation expression system for tyrosine-sulfated proteins and its application in crop protection Schwessinger, Benjamin; Li, Xiang; Ellinghaus, Thomas L. Integrative Biology, Vol. 8, Issue 4 https://doi.org/10.1039/C5IB00232J	journal	January 2016
A peptide hormone required for Casparian strip diffusion barrier formation in Arabidopsis roots Nakayama, Takuya; Shinohara, Hidefumi; Tanaka, Mina Science, Vol. 355, Issue 6322 https://doi.org/10.1126/science.aai9057	journal	January 2017
Influence of Amino Acid Substitutions in the Leader Peptide on Maturation and Secretion of Mesentericin Y105 by Leuconostoc mesenteroides Aucher, W.; Lacombe, C.; Hequet, A. Journal of Bacteriology, Vol. 187, Issue 6 https://doi.org/10.1128/JB.187.6.2218-2223.2005	journal	March 2005
Mutational analysis of the putative leukotoxin transport genes in Actinobacillus actinomycetemcomitans Guthmiller, Janet M.; Kolodrubetz, David; Kraig, Ellen Microbial Pathogenesis, Vol. 18, Issue 5 https://doi.org/10.1006/mpat.1995.0028	journal	May 1995
The Rhomboid-Like Superfamily: Molecular Mechanisms and Biological Roles Freeman, Matthew Annual Review of Cell and Developmental Biology, Vol. 30, Issue 1 https://doi.org/10.1146/annurev-cellbio-100913-012944	journal	October 2014
A new method to customize protein expression vectors for fast, efficient and background free parallel cloning Scholz, Judith; Besir, Hüseyin; Strasser, Claudia BMC Biotechnology, Vol. 13, Issue 1 https://doi.org/10.1186/1472-6750-13-12	journal	January 2013
Cys ³² and His ¹⁰⁵ Are the Critical Residues for the Calcium-dependent Cysteine Proteolytic Activity of CvaB, an ATP-binding Cassette Transporter Wu, Kai-Hui; Tai, Phang C. Journal of Biological Chemistry, Vol. 279, Issue 2 https://doi.org/10.1074/jbc.M308296200	journal	October 2003
A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export Havarstein, Leiv Sigve; Diep, Dzung Bao; Nes, Ingolf F. Molecular Microbiology, Vol. 16, Issue 2 https://doi.org/10.1111/j.1365-2958.1995.tb02295.x	journal	April 1995
Insights into AMS/PCAT transporters from biochemical and structural characterization of a double Glycine motif protease Bobeica, Silvia C.; Dong, Shi-Hui; Huo, Liujie eLife, Vol. 8 https://doi.org/10.7554/eLife.42305	journal	January 2019
The Xanthomonas Ax21 protein is processed by the general secretory system and is secreted in association with outer membrane vesicles Bahar, Ofir; Pruitt, Rory; Luu, Dee Dee PeerJ, Vol. 2 https://doi.org/10.7717/peerj.242	journal	January 2014
Mutagenesis of all Eight avr Genes in Xanthomonas campestris pv. campestris Had No Detected Effect on Pathogenicity, But One avr Gene Affected Race Specificity Castañeda, Adriana; Reddy, Joseph D.; El-Yacoubi, Basma Molecular Plant-Microbe Interactions, Vol. 18, Issue 12 https://doi.org/10.1094/MPMI-18-1306	journal	December 2005
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
Expression and Characterization of the Peptidase Domain of Streptococcus pneumoniae ComA, a Bifunctional ATP-binding Cassette Transporter Involved in Quorum Sensing Pathway Ishii, Seiji; Yano, Takato; Hayashi, Hideyuki Journal of Biological Chemistry, Vol. 281, Issue 8 https://doi.org/10.1074/jbc.M512516200	journal	December 2005
ATP-dependent leader peptide cleavage by NukT, a bifunctional ABC transporter, during lantibiotic biosynthesis Nishie, Mami; Shioya, Kouki; Nagao, Jun-ichi Journal of Bioscience and Bioengineering, Vol. 108, Issue 6 https://doi.org/10.1016/j.jbiosc.2009.06.002	journal	December 2009
Identification of a Family of Avirulence Genes from Xanthomonas oryzae pv. oryzae Hopkins, C. M. Molecular Plant-Microbe Interactions, Vol. 5, Issue 6 https://doi.org/10.1094/MPMI-5-451	journal	January 1992
Contribution of the glutamine 19 side chain to transition-state stabilization in the oxyanion hole of papain Menard, Robert; Carriere, Julie; Laflamme, Pierre Biochemistry, Vol. 30, Issue 37 https://doi.org/10.1021/bi00101a002	journal	September 1991
Tyrosine sulfation in a Gram-negative bacterium Han, Sang-Wook; Lee, Sang-Won; Bahar, Ofir Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms2157	journal	January 2012
Secreted Peptide Signals Required for Maintenance of Root Stem Cell Niche in Arabidopsis Matsuzaki, Y.; Ogawa-Ohnishi, M.; Mori, A. Science, Vol. 329, Issue 5995 https://doi.org/10.1126/science.1191132	journal	August 2010
Tyrosine Sulfation of the Amino Terminus of CCR5 Facilitates HIV-1 Entry Farzan, Michael; Mirzabekov, Tajib; Kolchinsky, Peter Cell, Vol. 96, Issue 5 https://doi.org/10.1016/S0092-8674(00)80577-2	journal	March 1999
Suppression of bacterial infection in rice by treatment with a sulfated peptide: Suppression of bacterial infection in rice Wei, Tong; Chern, Mawsheng; Liu, Furong Molecular Plant Pathology, Vol. 17, Issue 9 https://doi.org/10.1111/mpp.12368	journal	April 2016
Follow the leader: the use of leader peptides to guide natural product biosynthesis Oman, Trent J.; van der Donk, Wilfred A. Nature Chemical Biology, Vol. 6, Issue 1 https://doi.org/10.1038/nchembio.286	journal	December 2009
Type I secretion systems – a story of appendices Kanonenberg, Kerstin; Schwarz, Christian K. W.; Schmitt, Lutz Research in Microbiology, Vol. 164, Issue 6 https://doi.org/10.1016/j.resmic.2013.03.011	journal	July 2013

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