Involvement of bacterial TonB-dependent signaling in the generation of an oligogalacturonide damage-associated molecular pattern from plant cell walls exposed to Xanthomonas campestris pv. campestris pectate lyases
Vorhölter F-J, Wiggerich H-G, Scheidle H, Sidhu VK, Mrozek K, Küster H, Pühler A, Niehaus K (2012)
BMC Microbiology 12(1): 239.
Zeitschriftenaufsatz
| Veröffentlicht | Englisch
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Autor*in
Vorhölter, Frank-JörgUniBi;
Wiggerich, Heinrich-Günter;
Scheidle, Heiko;
Sidhu, Vishaldeep Kaur;
Mrozek, KalinaUniBi;
Küster, Helge;
Pühler, AlfredUniBi
;
Niehaus, KarstenUniBi
![](https://pub.uni-bielefeld.de/images/icon_orcid.png)
Abstract / Bemerkung
Background
Efficient perception of attacking pathogens is essential for plants. Plant defense is evoked by molecules termed elicitors. Endogenous elicitors or damage-associated molecular patterns (DAMPs) originate from plant materials upon injury or pathogen activity. While there are comparably well-characterized examples for DAMPs, often oligogalacturonides (OGAs), generated by the activity of fungal pathogens, endogenous elicitors evoked by bacterial pathogens have been rarely described. In particular, the signal perception and transduction processes involved in DAMP generation are poorly characterized.
Results
A mutant strain of the phytopathogenic bacterium Xanthomonas campestris pv. campestris deficient in exbD2, which encodes a component of its unusual elaborate TonB system, had impaired pectate lyase activity and caused no visible symptoms for defense on the non-host plant pepper (Capsicum annuum). A co-incubation of X. campestris pv. campestris with isolated cell wall material from C. annuum led to the release of compounds which induced an oxidative burst in cell suspension cultures of the non-host plant. Lipopolysaccharides and proteins were ruled out as elicitors by polymyxin B and heat treatment, respectively. After hydrolysis with trifluoroacetic acid and subsequent HPAE chromatography, the elicitor preparation contained galacturonic acid, the monosaccharide constituent of pectate. OGAs were isolated from this crude elicitor preparation by HPAEC and tested for their biological activity. While small OGAs were unable to induce an oxidative burst, the elicitor activity in cell suspension cultures of the non-host plants tobacco and pepper increased with the degree of polymerization (DP). Maximal elicitor activity was observed for DPs exceeding 8. In contrast to the X. campestris pv. campestris wild type B100, the exbD2 mutant was unable to generate elicitor activity from plant cell wall material or from pectin.
Conclusions
To our knowledge, this is the second report on a DAMP generated by bacterial features. The generation of the OGA elicitor is embedded in a complex exchange of signals within the framework of the plant-microbe interaction of C. annuum and X. campestris pv. campestris. The bacterial TonB-system is essential for the substrate-induced generation of extracellular pectate lyase activity. This is the first demonstration that a TonB-system is involved in bacterial trans-envelope signaling in the context of a pathogenic interaction with a plant.
Erscheinungsjahr
2012
Zeitschriftentitel
BMC Microbiology
Band
12
Ausgabe
1
Art.-Nr.
239
ISSN
1471-2180
Page URI
https://pub.uni-bielefeld.de/record/2537690
Zitieren
Vorhölter F-J, Wiggerich H-G, Scheidle H, et al. Involvement of bacterial TonB-dependent signaling in the generation of an oligogalacturonide damage-associated molecular pattern from plant cell walls exposed to Xanthomonas campestris pv. campestris pectate lyases. BMC Microbiology. 2012;12(1): 239.
Vorhölter, F. - J., Wiggerich, H. - G., Scheidle, H., Sidhu, V. K., Mrozek, K., Küster, H., Pühler, A., et al. (2012). Involvement of bacterial TonB-dependent signaling in the generation of an oligogalacturonide damage-associated molecular pattern from plant cell walls exposed to Xanthomonas campestris pv. campestris pectate lyases. BMC Microbiology, 12(1), 239. doi:10.1186/1471-2180-12-239
Vorhölter, Frank-Jörg, Wiggerich, Heinrich-Günter, Scheidle, Heiko, Sidhu, Vishaldeep Kaur, Mrozek, Kalina, Küster, Helge, Pühler, Alfred, and Niehaus, Karsten. 2012. “Involvement of bacterial TonB-dependent signaling in the generation of an oligogalacturonide damage-associated molecular pattern from plant cell walls exposed to Xanthomonas campestris pv. campestris pectate lyases”. BMC Microbiology 12 (1): 239.
Vorhölter, F. - J., Wiggerich, H. - G., Scheidle, H., Sidhu, V. K., Mrozek, K., Küster, H., Pühler, A., and Niehaus, K. (2012). Involvement of bacterial TonB-dependent signaling in the generation of an oligogalacturonide damage-associated molecular pattern from plant cell walls exposed to Xanthomonas campestris pv. campestris pectate lyases. BMC Microbiology 12:239.
Vorhölter, F.-J., et al., 2012. Involvement of bacterial TonB-dependent signaling in the generation of an oligogalacturonide damage-associated molecular pattern from plant cell walls exposed to Xanthomonas campestris pv. campestris pectate lyases. BMC Microbiology, 12(1): 239.
F.-J. Vorhölter, et al., “Involvement of bacterial TonB-dependent signaling in the generation of an oligogalacturonide damage-associated molecular pattern from plant cell walls exposed to Xanthomonas campestris pv. campestris pectate lyases”, BMC Microbiology, vol. 12, 2012, : 239.
Vorhölter, F.-J., Wiggerich, H.-G., Scheidle, H., Sidhu, V.K., Mrozek, K., Küster, H., Pühler, A., Niehaus, K.: Involvement of bacterial TonB-dependent signaling in the generation of an oligogalacturonide damage-associated molecular pattern from plant cell walls exposed to Xanthomonas campestris pv. campestris pectate lyases. BMC Microbiology. 12, : 239 (2012).
Vorhölter, Frank-Jörg, Wiggerich, Heinrich-Günter, Scheidle, Heiko, Sidhu, Vishaldeep Kaur, Mrozek, Kalina, Küster, Helge, Pühler, Alfred, and Niehaus, Karsten. “Involvement of bacterial TonB-dependent signaling in the generation of an oligogalacturonide damage-associated molecular pattern from plant cell walls exposed to Xanthomonas campestris pv. campestris pectate lyases”. BMC Microbiology 12.1 (2012): 239.
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Vorholter FJ, Schneiker S, Goesmann A, Krause L, Bekel T, Kaiser O, Linke B, Patschkowski T, Ruckert C, Schmid J, Sidhu VK, Sieber V, Tauch A, Watt SA, Weisshaar B, Becker A, Niehaus K, Puhler A., J. Biotechnol. 134(1-2), 2008
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Vorholter FJ, Thias T, Meyer F, Bekel T, Kaiser O, Puhler A, Niehaus K., J. Biotechnol. 106(2-3), 2003
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Roper MC, Greve LC, Warren JG, Labavitch JM, Kirkpatrick BC., Mol. Plant Microbe Interact. 20(4), 2007
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He YW, Ng AY, Xu M, Lin K, Wang LH, Dong YH, Zhang LH., Mol. Microbiol. 64(2), 2007
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Tao J, He C., FEMS Microbiol. Lett. 304(1), 2010
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Tao J, He C., FEMS Microbiol. Lett. 304(1), 2010
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Huang DL, Tang DJ, Liao Q, Li XQ, He YQ, Feng JX, Jiang BL, Lu GT, Tang JL., Mol. Plant Microbe Interact. 22(3), 2009
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Jittawuttipoka T, Sallabhan R, Vattanaviboon P, Fuangthong M, Mongkolsuk S., Arch. Microbiol. 192(5), 2010
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Ryan RP, Dow JM., Trends Microbiol. 19(3), 2011
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He YW, Wu J, Zhou L, Yang F, He YQ, Jiang BL, Bai L, Xu Y, Deng Z, Tang JL, Zhang LH., Mol. Plant Microbe Interact. 24(8), 2011
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Qian W, Han ZJ, He C., Mol. Plant Microbe Interact. 21(2), 2008
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Qian W, Han ZJ, Tao J, He C., Mol. Plant Microbe Interact. 21(8), 2008
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A putative colR(XC1049)-colS(XC1050) two-component signal transduction system in Xanthomonas campestris positively regulates hrpC and hrpE operons and is involved in virulence, the hypersensitive response and tolerance to various stresses.
Zhang SS, He YQ, Xu LM, Chen BW, Jiang BL, Liao J, Cao JR, Liu D, Huang YQ, Liang XX, Tang DJ, Lu GT, Tang JL., Res. Microbiol. 159(7-8), 2008
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He YW, Boon C, Zhou L, Zhang LH., Mol. Microbiol. 71(6), 2009
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Postle K., Meth. Enzymol. 422(), 2007
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Braun V, Endriss F., Biometals 20(3-4), 2007
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Hung CH, Yang CF, Yang CY, Tseng YH., Biochem. Biophys. Res. Commun. 302(4), 2003
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Wiggerich HG, Puhler A., Microbiology (Reading, Engl.) 146 ( Pt 5)(), 2000
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Alvarez B, Alvarez J, Menendez A, Guijarro JA., Microbiology (Reading, Engl.) 154(Pt 4), 2008
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Gross A, Kapp D, Nielsen T, Niehaus K., New Phytol. 165(1), 2005
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Baier R, Schiene K, Kohring B, Flaschel E, Niehaus K., Planta 210(1), 1999
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Felix G, Duran JD, Volko S, Boller T., Plant J. 18(3), 1999
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Gomez-Gomez L, Boller T., Trends Plant Sci. 7(6), 2002
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Extracellular alkalinization and oxidative burst induced by fungal lyase in tobacco cells are not due to the perception of oligogalacturonide fragments
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Hardy MR, Townsend RR., Proc. Natl. Acad. Sci. U.S.A. 85(10), 1988
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AUTHOR UNKNOWN, 1999
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Elicitation of H2O2 production in cucumber hypocotyl segments by oligo-1,4-alpha-D-galacturonides and an oligo-beta-glucan preparation from cell walls of Phythophthora megasperma F Sp glycinea
AUTHOR UNKNOWN, 1993
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Oligosaccharides as recognition signals for the expression of defensive genes in plants
AUTHOR UNKNOWN, 1988
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Norman C, Vidal S, Palva ET., Mol. Plant Microbe Interact. 12(7), 1999
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Buttner D, Bonas U., Curr. Opin. Plant Biol. 6(4), 2003
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Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G., Plant Cell 16(12), 2004
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Koebnik R., Trends Microbiol. 13(8), 2005
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Bordes P, Lavatine L, Phok K, Barriot R, Boulanger A, Castanie-Cornet MP, Dejean G, Lauber E, Becker A, Arlat M, Gutierrez C., J. Bacteriol. 193(1), 2010
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Brown IE, Mallen MH, Charnock SJ, Davies GJ, Black GW., Biochem. J. 355(Pt 1), 2001
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Guillen D, Sanchez S, Rodriguez-Sanoja R., Appl. Microbiol. Biotechnol. 85(5), 2009
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Vorholter FJ, Niehaus K, Puhler A., Mol. Genet. Genomics 266(1), 2001
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AUTHOR UNKNOWN, 1987
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New pUC-derived cloning vectors with different selectable markers and DNA replication origins.
Vieira J, Messing J., Gene 100(), 1991
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Becker A, Schmidt M, Jager W, Puhler A., Gene 162(1), 1995
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Hagerman AE, Blau DM, McClure AL., Anal. Biochem. 151(2), 1985
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Hsiao YM, Fang MC, Sun PF, Tseng YH., J. Agric. Food Chem. 57(14), 2009
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Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, Kalinowski J, Linke B, Rupp O, Giegerich R, Puhler A., Nucleic Acids Res. 31(8), 2003
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Blom J, Albaum SP, Doppmeier D, Puhler A, Vorholter FJ, Zakrzewski M, Goesmann A., BMC Bioinformatics 10(), 2009
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The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae.
Pieretti I, Royer M, Barbe V, Carrere S, Koebnik R, Cociancich S, Couloux A, Darrasse A, Gouzy J, Jacques MA, Lauber E, Manceau C, Mangenot S, Poussier S, Segurens B, Szurek B, Verdier V, Arlat M, Rott P., BMC Genomics 10(), 2009
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Insights into genome plasticity and pathogenicity of the plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria revealed by the complete genome sequence.
Thieme F, Koebnik R, Bekel T, Berger C, Boch J, Buttner D, Caldana C, Gaigalat L, Goesmann A, Kay S, Kirchner O, Lanz C, Linke B, McHardy AC, Meyer F, Mittenhuber G, Nies DH, Niesbach-Klosgen U, Patschkowski T, Ruckert C, Rupp O, Schneiker S, Schuster SC, Vorholter FJ, Weber E, Puhler A, Bonas U, Bartels D, Kaiser O., J. Bacteriol. 187(21), 2005
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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, Won Lee S, Seo YS, Sriariyanum M, Ronald PC, Sonti RV, Van Sluys MA, Leach JE, White FF, Bogdanove AJ., BMC Genomics 9(), 2008
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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, Won Lee S, Seo YS, Sriariyanum M, Ronald PC, Sonti RV, Van Sluys MA, Leach JE, White FF, Bogdanove AJ., BMC Genomics 9(), 2008
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Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity
AUTHOR UNKNOWN, 2005
AUTHOR UNKNOWN, 2005
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics.
Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B., Nucleic Acids Res. 37(Database issue), 2008
PMID: 18838391
Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B., Nucleic Acids Res. 37(Database issue), 2008
PMID: 18838391
AUTHOR UNKNOWN, 1989
The influence of lipopolysaccharide content on the apparent B cell stimulating activity of anti-mu preparations.
Wilder JA, Cowdery JS, Ashman RF., J. Immunol. Methods 110(1), 1988
PMID: 3259611
Wilder JA, Cowdery JS, Ashman RF., J. Immunol. Methods 110(1), 1988
PMID: 3259611
Human resistin stimulates the pro-inflammatory cytokines TNF-alpha and IL-12 in macrophages by NF-kappaB-dependent pathway.
Silswal N, Singh AK, Aruna B, Mukhopadhyay S, Ghosh S, Ehtesham NZ., Biochem. Biophys. Res. Commun. 334(4), 2005
PMID: 16039994
Silswal N, Singh AK, Aruna B, Mukhopadhyay S, Ghosh S, Ehtesham NZ., Biochem. Biophys. Res. Commun. 334(4), 2005
PMID: 16039994
Quantification of hydrogen peroxide in plant extracts by the chemoluminescence reaction with luminol
AUTHOR UNKNOWN, 1982
AUTHOR UNKNOWN, 1982
A revised medium for rapid growth and bioassays with tobacco tissue culture
AUTHOR UNKNOWN, 1962
AUTHOR UNKNOWN, 1962
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