The Xanthomonas Ax21 protein is processed by the general secretory system and is secreted in association with outer membrane vesicles

PeerJ

Volumn 2014, Issue 1, 2014, Pages

  Bahar, Ofir ^a   Pruitt, Rory ^a   Luu, Dee Dee ^a   Schwessinger, Benjamin ^a   Daudi, Arsalan ^a   Liu, Furong ^a   Ruan, Randy ^a   Fontaine Bodin, Lisa ^b   Koebnik, Ralf ^b   Ronald, Pamela ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Outer membrane vesicles; PAMPs; Plant immunity; Rice; Secretion; XA21; Xanthomonas

Indexed keywords

AX21 PROTEIN; OUTER MEMBRANE PROTEIN; PROTEINASE K; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL SECRETION SYSTEM; CONTROLLED STUDY; ESCHERICHIA COLI; GENE MUTATION; GROWTH CURVE; IMMUNITY; MEMBRANE VESICLE; NONHUMAN; PLASMID; PROTEIN ANALYSIS; RICE; TYPE I SECRETION SYSTEM; WESTERN BLOTTING; XANTHOMONAS;

EID: 84895759724     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.242     Document Type: Article

References (34)

1. Altschul SF, Gish W,Miller W,Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215:403-410.
2. Bagos PG, Liakopoulos TD, Spyropoulos IC, Hamodrakas SJ. 2004. PRED-TMBB: a web server for predicting the topology of beta-barrel outer membrane proteins. Nucleic Acids Research 32:W400-W404 DOI 10.1093/nar/gkh417.
3. Burdman S, Shen Y, Lee SW, Xue Q, Ronald PC. 2004. RaxH/RaxR: a two-component regulatory system in Xanthomonas oryzae pv. oryzae required for AvrXa21 activity.Molecular Plant-Microbe Interactions 17:602-612 DOI 10.1094/MPMI.2004.17.6.602.
4. Da Silva FG, Shen Y, Dardick C, Burdman S, Yadav RC, de Leon AL, Ronald PC. 2004. Bacterial genes involved in type I secretion and sulfation are required to elicit the rice Xa21-mediated innate immune response. Molecular Plant-Microbe Interactions 17:593-601 DOI 10.1094/MPMI.2004.17.6.593.
5. Dirix G,Monsieurs P, Dombrecht B, Daniels R,Marchal K, Vanderleyden J,Michiels J. 2004. 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. Peptides 25:1425-1440 DOI 10.1016/j.peptides.2003.10.028.
6. Eren E,Murphy M, Goguen J, van den Berg B. 2010. An active site water network in the plasminogen activator pla from Yersinia pestis. Structure 18:809-818 DOI 10.1016/j.str.2010.03.013.
7. Han SW, Lee SW, Bahar O, Schwessinger B, Robinson MR, Shaw JB, Brodbelt JS, Ronald PC. 2012. Tyrosine sulfation in a Gram-negative bacterium. Nature Communication 3:1153 DOI 10.1038/ncomms2157.
8. Han SW, Sriariyanun M, Lee SW, Sharma M, Bahar O, Bower Z, Roanld PC. 2011. Small protein-mediated quorum sensing in a Gram-negative bacterium. PLoS ONE 6:e29192 DOI 10.1371/journal.pone.0029192.
9. Han SW, Sriariyanun M, Lee SW, Sharma M, Bahar O, Bower Z, Roanld PC. 2013. Retraction: small protein-mediated quorum sensing in a gram-negative bacterium. PLoS ONE 8(9) DOI 10.1371/annotation/880a72e1-9cf3-45a9-bf1c-c74ccb73fd35.
10. Hayat S, Elofsson A. 2012. BOCTOPUS: improved topology prediction of transmembrane β barrel proteins. Bioinformatics 28:516-522 DOI 10.1093/bioinformatics/btr710.
11. Holland IB, Schmitt L, Young J. 2005. Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway. Molecular Membrane Biology 22:29-39 DOI 10.1080/09687860500042013.
12. Kauffman HE, Reddy APK, Hsieh SPY,Merca SD. 1973. Improved technique for evaluating resistance of rice varieties to Xanthomonas-oryzae. Plant Disease Reporter 57:537-541.
13. Koebnik R, Locher KP, Van Gelder P. 2000. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Molecular Microbiology 37:239-253 DOI 10.1046/j.1365-2958.2000.01983.x.
14. Lee SW, Han SW, Bartley LE, Ronald PC. 2006. Unique characteristics of Xanthomonas oryzae pv. oryzae AvrXa21 and implications for plant innate immunity. Proceedings of the National Academy of Sciences of the United States of America 103:18395-18400 DOI 10.1073/pnas.0605508103.
15. Lee SW, Han SW, Sririyanum M, Park CJ, Seo YS, Ronald PC. 2009. A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science 326:850-853 DOI 10.1126/science.1173438.
16. Lee SW, Han SW, Sririyanum M, Park CJ, Seo YS, Ronald PC. 2013. Retraction. Science 342:191 DOI 10.1126/science.342.6155.191-a.
17. McBroomAJ, Kuehn MJ. 2007. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Molecular Microbiology 63:545-558 DOI 10.1111/j.1365-2958.2006.05522.x.
18. McCarthy Y, Dow JM, Ryan RP. 2011. The Ax21 protein is a cell-cell signal regulating virulence in the nosocomial pathogen Stenotrophomonas maltophilia. Journal of Bacteriology 193:6375-6378 DOI 10.1128/JB.05949-11.
19. Michiels J, Dirix G, Vanderleyden J, Xi C. 2001. Processing and export of peptide pheromones and bacteriocins in Gram-negative bacteria. Trends in Microbiology 9:164-168 DOI 10.1016/S0966-842X(01)01979-5.
20. Natale P, Brüser T, Driessen AJM. 2008. Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane-distinct translocases and mechanisms. Biochimica et Biophysica Acta 1778:1735-1756 DOI 10.1016/j.bbamem.2007.07.015.
21. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8:785-786 DOI 10.1038/nmeth.1701.
22. Prince SM, Achtman M, Derrick JP. 2002. Crystal structure of the OpcA integral membrane adhesin from Neisseria meningitidis. Proceedings of the National Academy of Sciences of the United States of America 99:3417-3421 DOI 10.1073/pnas.062630899.
23. Qian G, Zhou Y, Zhao Y, Song Z,Wang S, Fan J, Hu B, Venturi V, Liu F. 2013. Proteomic analysis reveals novel extracellular virulence-associated proteins and functions regulated by the diffusible signal factor (DSF) in Xanthomonas oryzae pv. oryzicola. Journal of Proteome Research 12:3327-3341 DOI 10.1021/pr4001543.
24. Ronald PC. 2013. Lab life: the anatomy of retraction. Scientific American. Available at http://blogs. scientificamerican.com/food-matters/2013/10/10/lab-life-the-anatomy-of-a-retraction/.
25. Salzberg SL, Sommer DD, Schatz MC, Phillippy AM, Rabinowicz PD, Tsuge S, Furutani A, Ochiai H, Delcher AL, Kelley D,Madupu R, Puiu D, Radune D, Shumway M, Trapnell C, Aparna G, Jha G, Pandey A, Patil PB, Ishihara H,Meyer DF, Szurek B, Verdier V, Koebnik R, Dow JM, Ryan RP, Hirata H, Tsuyumu S, Lee S, Seo YS, Sriariyanun M, Ronald PC, Sonti RV, Van Sluys MA, Leach JE,White FF, Bogdanove AJ. 2008. Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics 9:204 DOI 10.1186/1471-2164-9-204.
26. Sambrook Fritsch EF,Maniatis TJ. 1989. Molecular cloning: a laboratory manual. New York: Cold Spring Harbor Laboratory Press.
27. Schwessinger B, Ronald PC. 2012. Plant innate immunity: perception of conserved microbial signatures. Annual Review of Plant Biology 63:451-482 DOI 10.1146/annurev-arplant-042811- 105518.
28. Shen Y, Sharma P, Goes da Silva F, Ronald P. 2002. The Xanthomonas oryzae pv. oryzae raxP and raxQ genes encode an ATP sulfurylase and APS kinase that are required for AvrXa21 avirulence activity. Molecular Microbiology 44:37-48 DOI 10.1046/j.1365-2958.2002.02862.x.
29. Shuguo H,Wei Z, Chao Z, Daoji W. 2012. One-step expression and tyrosine O-sulfonation of Ax21 in Escherichia coli. Applied Biochemistry and Biotechnology 166:1368-1379 DOI 10.1007/s12010-011-9525-3.
30. Song WY,Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J,Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P. 1995. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804-1806 DOI 10.1126/science.270.5243.1804.
31. Sonnhammer EL, Eddy SR, Durbin R. 1997. Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 28:405-420 DOI 10.1002/(SICI)1097- 0134(199707)28:3<405::AID-PROT10>3.0.CO;2-L.
32. Vandeputte-Rutten L, Kramer RA, Kroon J, Dekker N, Egmond MR, Gros P. 2001. Crystal structure of the outer membrane protease OmpT from Escherichia coli suggests a novel catalytic site. The EMBO Journal 20:5033-5039 DOI 10.1093/emboj/20.18.5033.
33. Wang L, Jiang W, Zhang Y,Wang S,Ma R, Sun W. 2013. Ax21-triggered immunity plays a significant role in rice defense against Xanthomonas oryzae pv. oryzicola. Phytopathology Epub ahead of print. There is only an abstract available for this paper at: http://www.ncbi.nlm.nih.gov/ pubmed/23656311.
34. Wang GL, Song WY, Ruan DL, Sideris S, Ronald PC. 1996. The cloned gene, Xa21, confers resistance to multiple Xanthomonas oryzae pv. oryzae isolates in transgenic plants. Molecular Plant Microbe Interaction 9:850-855 DOI 10.1094/MPMI-9-0850.