Abstract:
Xanthomonas axonopodis pv. citri (Xac) causes citrus canker, provoking defoliation and premature fruit drop with concomitant economical damage. In plant pathogenic bacteria, lipopolysaccharides are important virulence factors, and they are being increasingly recognized as major pathogen-associated molecular patterns for plants. In general, three domains are recognized in a lipopolysaccharide: the hydrophobic lipid A, the hydrophilic O-antigen polysaccharide, and the core oligosaccharide, connecting lipidA and O-antigen. In this work, we have determined the structure of purified lipopolysaccharides obtained from Xanthomonas axonopodis pv. citri wild type and a mutant of the O-antigen ABC transporter encoded by the wzt gene. High pH anion exchange chromatography and matrix-assisted laser desorption/ionization mass spectrum analysis were performed, enabling determination of the structure not only of the released oligosaccharides and lipid A moieties but also the intact lipopolysaccharides. The results demonstrate that Xac wild type and Xacwzt LPSs are composed mainly of a penta- or tetra-acylated diglucosamine backbone attached to either two pyrophosphorylethanolaminegroupsortoonepyrophosphorylethanolamine group and one phosphorylethanolamine group. The core region consists of a branched oligosaccharide formed by Kdo 2Hex 6GalA 3Fuc3NAcRha 4 and two phosphate groups. As expected, the presence of a rhamnose homo-oligosaccharide as O-antigen was determined only in the Xac wild type lipopolysaccharide. In addition, we have examined how lipopolysaccharides from Xac function in the pathogenesis process. We analyzed the response of the different lipopolysaccharides during the stomata aperture closure cycle, the callose deposition, the expression of defense-related genes, and reactive oxygen species production in citrus leaves, suggesting a functional role of the O-antigen from Xac lipopolysaccharides in the basal response. © 2011 by The American Society for Biochemistry and Molecular Biology, Inc.
Registro:
Documento: |
Artículo
|
Título: | Structural analysis and involvement in plant innate immunity of Xanthomonas axonopodis pv. citri lipopolysaccharide |
Autor: | Casabuono, A.; Petrocelli, S.; Ottado, J.; Orellano, E.G.; Couto, A.S. |
Filiación: | Centro de Investigaciones en Hidratos de Carbono, Departamento de Química Orgánica, Universidad de Buenos Aires, Buenos Aires 1428, Argentina Molecular Biology Division, Instituto de Biología Molecular y Celular de Rosario, Consejo Nacional de Investigaciones Científicas y Técnicas (IBR-CONICET-UNR), Suipacha 531 (S2002LRK), Rosario, Argentina
|
Palabras clave: | ABC transporter; Citrus canker; Citrus leaves; Core oligosaccharide; Core region; Defense related genes; Economical damage; High-ph anion-exchange chromatographies; Lipid A; Lipopolysaccharides; Mass spectrum analysis; Matrix assisted laser desorption/ionization; O-Antigen; O-antigen polysaccharides; Pathogen-associated molecular patterns; Pathogenic bacterium; Phosphate group; Phosphorylethanolamine; Plant innate immunity; Reactive oxygen species; Virulence factors; Wild types; Xanthomonas axonopodis; Antigens; Bacteria; Citrus fruits; Desorption; Gene expression; Mass spectrometry; Oligosaccharides; Plants (botany); Polysaccharides; Spectrum analysis; Structural analysis; Plant shutdowns; ABC transporter; bacterium lipopolysaccharide; lipid A; O antigen; oligosaccharide; phosphoethanolamine; reactive oxygen metabolite; rhamnose; anion exchange chromatography; article; bacterial gene; bacterial strain; bacterium culture; bacterium mutant; biosynthesis; carbohydrate analysis; controlled study; gene expression; matrix assisted laser desorption ionization time of flight mass spectrometry; nonhuman; pathogenesis; pH; plant immunity; plant leaf; priority journal; wild type; wzt gene; Xanthomonas axonopodis; ATP-Binding Cassette Transporters; Bacterial Proteins; Carbohydrate Sequence; Citrus sinensis; Gene Expression Regulation, Plant; Host-Pathogen Interactions; Immunity, Innate; Lipopolysaccharides; Molecular Sequence Data; Peroxides; Plant Leaves; Plant Stomata; Xanthomonas axonopodis; Citrus; Tetra; Xanthomonas axonopodis pv. citri |
Año: | 2011
|
Volumen: | 286
|
Número: | 29
|
Página de inicio: | 25628
|
Página de fin: | 25643
|
DOI: |
http://dx.doi.org/10.1074/jbc.M110.186049 |
Título revista: | Journal of Biological Chemistry
|
Título revista abreviado: | J. Biol. Chem.
|
ISSN: | 00219258
|
CODEN: | JBCHA
|
CAS: | lipid A, 95991-05-2; phosphoethanolamine, 1071-23-4, 29868-05-1; rhamnose, 10485-94-6, 3615-41-6; ATP-Binding Cassette Transporters; Bacterial Proteins; Lipopolysaccharides; Peroxides; Wzt protein, bacteria
|
Registro: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00219258_v286_n29_p25628_Casabuono |
Referencias:
- Brunings, A.M., Gabriel, D.W., (2003) Mol. Plant Pathol., 4, pp. 141-157
- Graham, J.H., Gottwald, T.R., Cubero, J., Achor, D.S., (2004) Mol. Plant Pathol., 5, pp. 1-15
- Gust, A.A., Biswas, R., Lenz, H.D., Rauhut, T., Ranf, S., Kemmerling, B., Götz, F., Nürnberger, T., (2007) J. Biol. Chem., 282, pp. 32338-32348
- Holst, O., Molinaro, A., (2009) Microbial Glycobiology: Structures, Relevance, and Applications, pp. 29-56. , (Moran, A., Brennan, P., Holst, O., and von Itszstein, M., eds) Elsevier, San Diego, CA
- Knirel, Y.A., Senchenkova, S.N., Shashkov, A.S., Esteve, C., Alcaide, E., Merino, S., Tomás, J.M., (2009) Carbohydr. Res., 344, pp. 479-483
- John, C.M., Liu, M., Jarvis, G.A., (2009) J. Lipid Res., 50, pp. 424-438
- Lindner, B., (2000) Methods Mol. Biol., 145, pp. 311-325
- Therisod, H., Labas, V., Caroff, M., (2001) Anal. Chem., 73, pp. 3804-3807
- Worrall, T.A., Lin, S., Cotter, R.J., Woods, A.S., (2000) J. Mass Spectrom., 35, pp. 647-650
- Harvey, D.J., (2009) Mass Spectrom. Rev., 28, pp. 273-361
- Dow, J.M., Osbourn, A.E., Wilson, T.J., Daniels, M.J., (1995) Mol. Plant Microbe Interact., 8, pp. 768-777
- Conrath, U., Thulke, O., Katz, V., Schwindling, S., Kohler, A., (2001) Eur. J. Plant Pathol., 107, pp. 113-119
- Zeidler, D., Zähringer, U., Gerber, I., Dubery, I., Hartung, T., Bors, W., Hutzler, P., Durner, J., (2004) Proc. Natl. Acad. Sci. U.S.A., 101, pp. 15811-15816
- Braun, S.G., Meyer, A., Holst, O., Pühler, A., Niehaus, K., (2005) Mol. Plant Microbe Interact., 18, pp. 674-681
- Newman, M.A., Von Roepenack, E., Daniels, M., Dow, M., (2000) Mol. Plant Pathol., 1, pp. 25-31
- Silipo, A., Molinaro, A., Sturiale, L., Dow, J.M., Erbs, G., Lanzetta, R., Newman, M.A., Parrilli, M., (2005) J. Biol. Chem., 280, pp. 33660-33668
- Molinaro, A., Silipo, A., Lanzetta, R., Newman, M.A., Dow, J.M., Parrilli, M., (2003) Carbohydr. Res., 338, pp. 277-281
- Silipo, A., Sturiale, L., Garozzo, D., Erbs, G., Jensen, T.T., Lanzetta, R., Dow, J.M., Molinaro, A., (2008) Chembiochem, 9, pp. 896-904
- Daurelio, L.D., Tondo, M.L., Dunger, G., Gottig, N., Ottado, J., Orellano, E.G., (2009) Book on Plant Bioassays, pp. 187-206. , (Narwal, S. S., Catalán, A. N., Sampietro, D. A., Vattuone, M. A., and Polyticka, B., eds) Chapter 10, Studium Press, LLC, Houston, TX
- Sambrook, J., Fritsch, E.F., Maniatis, T., (1989) Molecular Cloning: A Laboratory Manual, , 2nd Ed., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
- Murray, M.G., Thompson, W.F., (1980) Nucleic Acids Res., 8, pp. 4321-4325
- Katzen, F., Becker, A., Ielmini, M.V., Oddo, C.G., Ielpi, L., (1999) Appl. Environ. Microbiol., 65, pp. 278-282
- Simon, R., Priefer, U., Puhler, A., (1983) Nat. Biotechnol., 1, pp. 784-791
- Dunger, G., Arabolaza, A.L., Gottig, N., Orellano, E.G., Ottado, J., (2005) Plant Pathol., 54, pp. 781-788
- Kovach, M.E., Elzer, P.H., Hill, D.S., Robertson, G.T., Farris, M.A., Roop II, R.M., Peterson, K.M., (1995) Gene, 166, pp. 175-176
- Westphal, O., Jann, K., (1965) Methods in Carbohydrate Chemistry, pp. 83-91. , (Whistler, R. L., ed) Academic Press, Inc., New York
- Marolda, C.L., Lahiry, P., Vinés, E., Saldías, S., Valvano, M.A., (2006) Methods Mol. Biol., 347, pp. 237-252
- Tsai, C.M., Frasch, C.E., (1982) Anal. Biochem., 119, pp. 115-119
- Qureshi, N., Takayama, K., Ribi, E., (1982) J. Biol. Chem., 257, pp. 11808-11815
- Rietschel, E.T., Lüderitz, O., Volk, W.A., (1975) J. Bacteriol., 122, pp. 1180-1188
- Gottig, N., Garavaglia, B.S., Daurelio, L.D., Valentine, A., Gehring, C., Orellano, E.G., Ottado, J., (2008) Proc. Natl. Acad. Sci. U.S.A., 105, pp. 18631-18636
- Melotto, M., Underwood, W., Koczan, J., Nomura, K., He, S.Y., (2006) Cell, 126, pp. 969-980
- DeLong, J.M., Prange, R.K., Hodges, D.M., Forney, C.F., Bishop, M.C., Quilliam, M., (2002) J. Agric. Food Chem., 50, pp. 248-254
- Büttner, D., Bonas, U., (2010) FEMS Microbiol. Rev., 34, pp. 107-133
- Patil, P.B., Bogdanove, A.J., Sonti, R.V., (2007) BMC Evol. Biol., 7, p. 243
- Da Silva, A.C., Ferro, J.A., Reinach, F.C., Farah, C.S., Furlan, L.R., Quaggio, R.B., Monteiro-Vitorello, C.B., Kitajima, J.P., (2002) Nature, 417, pp. 459-463
- Van Sluys, M.A., Monteiro-Vitorello, C.B., Camargo, L.E., Menck, C.F., Da Silva, A.C., Ferro, J.A., Oliveira, M.C., Simpson, A.J., (2002) Annu. Rev. Phytopathol., 40, pp. 169-189
- Vorhölter, F.J., Niehaus, K., Pühler, A., (2001) Mol. Genet. Genomics, 266, pp. 79-95
- Sidhu, V.K., Vorhölter, F.J., Niehaus, K., Watt, S.A., (2008) BMC Microbiol., 8, p. 87
- Harvey, D.J., (2003) Int. J. Mass Spectrom., 226, pp. 1-35
- Keshavarzi, M., Soylu, S., Brown, I., Bonas, U., Nicole, M., Rossiter, J., Mansfield, J., (2004) Mol. Plant Microbe Interact., 17, pp. 805-815
- Kazan, K., Schenk, P.M., Wilson, I., Manners, J.M., (2001) Mol. Plant Pathol., 2, pp. 177-185
- Daurelio, L.D., Petrocelli, S., Blanco, F., Holuigue, L., Ottado, J., Orellano, E.G., (2011) J. Plant Physiol., 168, pp. 382-391
- Dong, X., Mindrinos, M., Davis, K.R., Ausubel, F.M., (1991) Plant Cell, 3, pp. 61-72
- Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.L., Gomez-Gomez, L., Boller, T., Sheen, J., (2002) Nature, 415, pp. 977-983
- Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E.J., Jones, J.D., Felix, G., Boller, T., (2004) Nature, 428, pp. 764-767
- Green, J., Paget, M.S., (2004) Nat. Rev. Microbiol., 2, pp. 954-966
- Ingle, R.A., Carstens, M., Denby, K.J., (2006) BioEssays, 28, pp. 880-889
- Meyer, A., Pühler, A., Niehaus, K., (2001) Planta, 213, pp. 214-222
- Zähringer, U., Lindner, B., Rietschel, E.T., (1999) Endotoxin in Health and Disease, , (Morrison, D. C., Brade, H., Opal, S., and Vogel, S., eds) Marcel Dekker, Inc., New York
- Silipo, A., Molinaro, A., Lanzetta, R., Parrilli, M., Lindner, B., Holst, O., (2004) Eur. J. Org. Chem., 2004, pp. 1336-1343
- Kulshin, V.A., Zähringer, U., Lindner, B., Frasch, C.E., Tsai, C.M., Dmitriev, B.A., Rietschel, E.T., (1992) J. Bacteriol., 174, pp. 1793-1800
- Dow, M., Newman, M.A., Von Roepenack, E., (2000) Annu. Rev. Phytopathol., 38, pp. 241-261
- Raetz, C.R., Whitfield, C., (2002) Annu. Rev. Biochem., 71, pp. 635-700
- Molinaro, A., Lanzetta, R., Evidente, A., Parrilli, M., Holst, O., (1999) FEMS Microbiol. Lett., 181, pp. 49-53
- Shashkov, A.S., Senchenkova, S.N., Laux, P., Ahohuendo, B.C., Kecskés, M.L., Rudolph, K., Knirel, Y.A., (2000) Carbohydr. Res., 323, pp. 235-239
- Molinaro, A., De Castro, C., Lanzetta, R., Parrilli, M., Petersen, B.O., Broberg, A., Duus, J.Ø., (2002) Eur. J Biochem., 269, pp. 4185-4193
- Bedini, E., De Castro, C., Erbs, G., Mangoni, L., Dow, J.M., Newman, M.A., Parrilli, M., Unverzagt, C., (2005) J. Am. Chem. Soc., 127, pp. 2414-2416
- Brown, I., Trethowan, J., Kerry, M., Mansfield, J., Bolwell, G.P., (1998) Plant J., 15, pp. 333-343
- Zeng, W., Melotto, M., He, S.Y., (2010) Curr. Opin. Biotechnol., 21, pp. 599-603
- Gómez-Gómez, L., (2004) Mol. Immunol., 41, pp. 1055-1062
- Felix, G., Duran, J.D., Volko, S., Boller, T., (1999) Plant J., 18, pp. 265-276
- Newman, M.A., Daniels, M.J., Dow, J.M., (1995) Mol. Plant Microbe Interact., 8, pp. 778-780
- Fujikawa, T., Ishihara, H., Leach, J.E., Tsuyumu, S., (2006) Mol. Plant Microbe Interact., 19, pp. 342-349
- Edreva, A., (2005) Gen. Appl. Plant Physiol., 31, pp. 105-124
- Mishina, T.E., Zeier, J., (2007) Plant J., 50, pp. 500-513
Citas:
---------- APA ----------
Casabuono, A., Petrocelli, S., Ottado, J., Orellano, E.G. & Couto, A.S.
(2011)
. Structural analysis and involvement in plant innate immunity of Xanthomonas axonopodis pv. citri lipopolysaccharide. Journal of Biological Chemistry, 286(29), 25628-25643.
http://dx.doi.org/10.1074/jbc.M110.186049---------- CHICAGO ----------
Casabuono, A., Petrocelli, S., Ottado, J., Orellano, E.G., Couto, A.S.
"Structural analysis and involvement in plant innate immunity of Xanthomonas axonopodis pv. citri lipopolysaccharide"
. Journal of Biological Chemistry 286, no. 29
(2011) : 25628-25643.
http://dx.doi.org/10.1074/jbc.M110.186049---------- MLA ----------
Casabuono, A., Petrocelli, S., Ottado, J., Orellano, E.G., Couto, A.S.
"Structural analysis and involvement in plant innate immunity of Xanthomonas axonopodis pv. citri lipopolysaccharide"
. Journal of Biological Chemistry, vol. 286, no. 29, 2011, pp. 25628-25643.
http://dx.doi.org/10.1074/jbc.M110.186049---------- VANCOUVER ----------
Casabuono, A., Petrocelli, S., Ottado, J., Orellano, E.G., Couto, A.S. Structural analysis and involvement in plant innate immunity of Xanthomonas axonopodis pv. citri lipopolysaccharide. J. Biol. Chem. 2011;286(29):25628-25643.
http://dx.doi.org/10.1074/jbc.M110.186049