BMC Microbiology | |
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 | |
Karsten Niehaus1  Alfred Pühler4  Helge Küster2  Kalina Mrozek1  Vishaldeep Kaur Sidhu3  Heiko Scheidle1  Heinrich-Günter Wiggerich4  Frank-Jörg Vorhölter4  | |
[1] Department of Proteome and Metabolome Research, Faculty of Biology, Universität Bielefeld, Universitätsstr. 25, Bielefeld, 33615, Germany;Institut für Pflanzengenetik, Naturwissenschaftliche Fakultät, Leibniz Universität Hannover, Herrenhäuser Str. 2, Hannover, 30419, Germany;Laboratory of Molecular Signaling, 5625 Fishers Lane, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Rockville, MD, 20852, USA;CeBiTec, Universität Bielefeld, Universitätsstr. 27, Bielefeld, 33615, Germany | |
关键词: Xanthomonas campestris; Pathogen; Molecular plant-microbe interaction; Trans-envelope signaling; Oligogalacturonide; DAMP; Damage-associate molecular pattern; TonB system; | |
Others : 1221703 DOI : 10.1186/1471-2180-12-239 |
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received in 2012-04-10, accepted in 2012-09-25, 发布年份 2012 | |
【 摘 要 】
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.
【 授权许可】
2012 Vorhölter et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Jones JD, Dangl JL: The plant immune system. Nature 2006, 444(7117):323-329.
- [2]Boller T, Felix G: A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 2009, 60:379-406.
- [3]Bauer Z, Gomez-Gomez L, Boller T, Felix G: Sensitivity of different ecotypes and mutants of Arabidopsis thaliana toward the bacterial elicitor flagellin correlates with the presence of receptor-binding sites. J Biol Chem 2001, 276(49):45669-45676.
- [4]Lamb C, Dixon RA: The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 1997, 48:251-275.
- [5]Wei ZM, Laby RJ, Zumoff CH, Bauer DW, He SY, Collmer A, Beer SV: Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 1992, 257(5066):85-88.
- [6]Yap MN, Rojas CM, Yang CH, Charkowski AO: Harpin mediates cell aggregation in Erwinia chrysanthemi 3937. J Bacteriol 2006, 188(6):2280-2284.
- [7]Kim JG, Jeon E, Oh J, Moon JS, Hwang I: Mutational analysis of Xanthomonas harpin HpaG identifies a key functional region that elicits the hypersensitive response in nonhost plants. J Bacteriol 2004, 186(18):6239-6247.
- [8]Li P, Lu X, Shao M, Long J, Wang J: Genetic diversity of harpins from Xanthomonas oryzae and their activity to induce hypersensitive response and disease resistance in tobacco. Sci China C Life Sci 2004, 47(5):461-469.
- [9]Alfano JR, Bauer DW, Milos TM, Collmer A: Analysis of the role of the Pseudomonas syringae pv. syringae HrpZ harpin in elicitation of the hypersensitive response in tobacco using functionally non-polar hrpZ deletion mutations, truncated HrpZ fragments, and hrmA mutations. Mol Microbiol 1996, 19(4):715-728.
- [10]Midland SL, Keen NT, Sims JJ, Midland MM, Stayton MM, Burton V, Smith MJ, Mazzola EP, Graham KJ, Clardy J: The structures of syringolide-1 and syringolide-2, novel C-glycosidic elicitors from Pseudomonas syringae pv tomato. J Org Chem 1993, 58(11):2940-2945.
- [11]Silipo A, Erbs G, Shinya T, Dow JM, Parrilli M, Lanzetta R, Shibuya N, Newman MA, Molinaro A: Glyco-conjugates as elicitors or suppressors of plant innate immunity. Glycobiology 2010, 20(4):406-419.
- [12]Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA, Washburn NR, Devera ME, Liang X, Tor M, Billiar T: The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 2007, 220:60-81.
- [13]Yamaguchi Y, Huffaker A: Endogenous peptide elicitors in higher plants. Curr Opin Plant Biol 2011, 14(4):351-357.
- [14]Chai HB, Doke N: Superoxide anion generation: a response of potato leaves to infection with Phytophtera infestans. Phytopathology 1987, 77:645-649.
- [15]Bergey DR, Orozco-Cardenas M, de Mouro DS, Ryan CA: A wound- and systemin-inducible polygalacturonase in tomato leaves. Proc Natl Acad Sci USA 1999, 96:1756-1760.
- [16]Sharp JK, McNeil M, Albersheim P: The primary structures of one elicitor-active and seven elicitor-inactive hexa(beta-D-glucopyranosyl)-D-glucitols isolated from the mycelial walls of Phytophthora megasperma f. sp. glycinea. J Biol Chem 1984, 259(18):11321-11336.
- [17]Hahn MG, Darvill AG, Albersheim P: Host-pathogen interactions: XIX. The endogenous elicitor, a fragment of the a plant cell wall polysaccharide that elicits phytoalexin accumulation in soybeans. Plant Physiol 1981, 68(5):1161-1169.
- [18]Monden T, Nakamura H, Murai A: The sugar composition and partial structure of the self-induced endogenous elicitor from potato. Biochem Biophys Res Commun 1995, 215(2):768-773.
- [19]Davis KR, Lyon GD, Darvill AG, Albersheim P: Host-pathogen interactions: XXV. Endopolygalacturonic acid lyase from Erwinia carotovora elicits phytoalexin accumulation by releasing plant cell wall fragments. Plant Physiol 1984, 74(1):52-60.
- [20]Nothnagel EA, McNeil M, Albersheim P, Dell A: Host-pathogen interactions: XXII. A galacturonic acid oligosaccharide from plant cell walls elicits phytoalexins. Plant Physiol 1983, 71(4):916-926.
- [21]Cabrera JC, Boland A, Messiaen J, Cambier P, Van Cutsem P: Egg box conformation of oligogalacturonides: the time-dependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 2008, 18(6):473-482.
- [22]Kohorn BD, Johansen S, Shishido A, Todorova T, Martinez R, Defeo E, Obregon P: Pectin activation of MAP kinase and gene expression is WAK2 dependent. Plant J 2009, 60(6):974-982.
- [23]Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G: A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA 2010, 107(20):9452-9457.
- [24]Xanthomonas. Chapman & Hall, London; 1993.
- [25]Ryan RP, Vorhölter FJ, Potnis N, Jones JB, Van Sluys MA, Bogdanove AJ, Dow JM: Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. Nat Rev Microbiol 2011, 9(5):344-355.
- [26]Meyer A, Pühler A, Niehaus K: The lipopolysaccharides of the phytopathogen Xanthomonas campestris pv. campestris induce an oxidative burst reaction in cell cultures of Nicotiana tabacum. Planta 2001, 213(2):214-222.
- [27]Newman MA, Daniels MJ, Dow JM: Lipopolysaccharide from Xanthomonas campestris induces defense-related gene expression in Brassica campestris. Mol Plant Microbe Interact 1995, 8(5):778-780.
- [28]Kaczynski Z, Braun S, Lindner B, Niehaus K, Holst O: Investigation of the chemical structure and biological activity of oligosaccharides isolated from rough-type Xanthomonas campestris pv. campestris B100 lipopolysaccharide. J Endotoxin Res 2007, 13(2):101-108.
- [29]Silipo A, Molinaro A, Sturiale L, Dow JM, Erbs G, Lanzetta R, Newman MA, Parrilli M: The elicitation of plant innate immunity by lipooligosaccharide of Xanthomonas campestris. J Biol Chem 2005, 280(39):33660-33668.
- [30]Erbs G, Silipo A, Aslam S, De Castro C, Liparoti V, Flagiello A, Pucci P, Lanzetta R, Parrilli M, Molinaro A, et al.: Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity. Chem Biol 2008, 15(5):438-448.
- [31]Newman MA, von Roepenack-Lahaye E, Parr A, Daniels MJ, Dow JM: Induction of hydroxycinnamoyl-tyramine conjugates in pepper by Xanthomonas campestris, a plant defense response activated by hrp gene-dependent and hrp gene-independent mechanisms. Mol Plant Microbe Interact 2001, 14(6):785-792.
- [32]Büttner D, Bonas U: Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol Rev 2010, 34(2):107-133.
- [33]Bogdanove AJ, Schornack S, Lahaye T: TAL effectors: finding plant genes for disease and defense. Curr Opin Plant Biol 2010, 13(4):394-401.
- [34]Cunnac S, Wilson A, Nuwer J, Kirik A, Baranage G, Mudgett MB: A conserved carboxylesterase is a suppressor of AvrBst-elicited resistence in Arabidopsis. Plant Cell 2007, 19(2):688-705.
- [35]Canonne J, Marino D, Jauneau A, Pouzet C, Briere C, Roby D, Rivas S: The Xanthomonas type III effector XopD targets the Arabidopsis transcription factor MYB30 to suppress plant defense. Plant Cell 2011, 23(9):3498-3511.
- [36]Szczesny R, Jordan M, Schramm C, Schulz S, Cogez V, Bonas U, Büttner D: Functional characterization of the Xcs and Xps type II secretion systems from the plant pathogenic bacterium Xanthomonas campestris pv vesicatoria. New Phytol 2010, 187(4):983-1002.
- [37]Nasuno S, Starr MP: Polygalacturonic acid trans-eliminase of Xanthomonas campestris. Biochem J 1967, 104(1):178-185.
- [38]Dow JM, Scofield G, Trafford K, Turner PC, Daniels MJ: A gene cluster in Xanthomonas campestris pv. campestris required for pathogenicity controls the excretion of polygalacturonate lyase and other enzymes. Physiol Mol Plant Pathol 1987, 31:261-271.
- [39]Dow JM, Milligan DE, Jamieson L, Barber CE, Daniels MJ: Molecular cloning of a polygalacturonate lyase gene from Xanthomonas campestris pv. campestris and role of the gene product in pathogenicity. Physiol Mol Plant P 1989, 35:113-120.
- [40]Xiao Z, Boyd J, Grosse S, Beauchemin M, Coupe E, Lau PC: Mining Xanthomonas and Streptomyces genomes for new pectinase-encoding sequences and their heterologous expression in Escherichia coli. Appl Microbiol Biotechnol 2008, 78(6):973-981.
- [41]Hsiao YM, Zheng MH, Hu RM, Yang TC, Tseng YH: Regulation of the pehA gene encoding the major polygalacturonase of Xanthomonas campestris by Clp and RpfF. Microbiology 2008, 154(Pt 3):705-713.
- [42]Bogdanove AJ, Koebnik R, Lu H, Furutani A, Angiuoli SV, Patil PB, Van Sluys MA, Ryan RP, Meyer DF, Han SW, et al.: Two new complete genome sequences offer insight into host and tissue specificity of plant pathogenic Xanthomonas spp. J Bacteriol 2011, 193(19):5450-5464.
- [43]da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR, Quaggio RB, Monteiro-Vitorello CB, Van Sluys MA, Almeida NF, Alves LM, et al.: Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 2002, 417(6887):459-463.
- [44]He YQ, Zhang L, Jiang BL, Zhang ZC, Xu RQ, Tang DJ, Qin J, Jiang W, Zhang X, Liao J, et al.: Comparative and functional genomics reveals genetic diversity and determinants of host specificity among reference strains and a large collection of Chinese isolates of the phytopathogen Xanthomonas campestris pv. campestris. Genome Biol 2007, 8(10):R218. BioMed Central Full Text
- [45]Qian W, Jia Y, Ren SX, He YQ, Feng JX, Lu LF, Sun Q, Ying G, Tang DJ, Tang H, et al.: Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris. Genome Res 2005, 15(6):757-767.
- [46]Vorhölter FJ, Schneiker S, Goesmann A, Krause L, Bekel T, Kaiser O, Linke B, Patschkowski T, Rückert C, Schmid J, et al.: The genome of Xanthomonas campestris pv. campestris B100 and its use for the reconstruction of metabolic pathways involved in xanthan biosynthesis. J Biotechnol 2008, 134(1–2):33-45.
- [47]Vorhölter FJ, Thias T, Meyer F, Bekel T, Kaiser O, Pühler A, Niehaus K: Comparison of two Xanthomonas campestris pathovar campestris genomes revealed differences in their gene composition. J Biotechnol 2003, 106(2–3):193-202.
- [48]Roper MC, Greve LC, Warren JG, Labavitch JM, Kirkpatrick BC: Xylella fastidiosa requires polygalacturonase for colonization and pathogenicity in Vitis vinifera grapevines. Mol Plant Microbe Interact 2007, 20(4):411-419.
- [49]He YW, Ng AY, Xu M, Lin K, Wang LH, Dong YH, Zhang LH: Xanthomonas campestris cell-cell communication involves a putative nucleotide receptor protein Clp and a hierarchical signalling network. Mol Microbiol 2007, 64(2):281-292.
- [50]Tao J, He C: Response regulator, VemR, positively regulates the virulence and adaptation of Xanthomonas campestris pv. campestris. FEMS Microbiol Lett 2010, 304(1):20-28.
- [51]Huang DL, Tang DJ, Liao Q, Li XQ, He YQ, Feng JX, Jiang BL, Lu GT, Tang JL: The Zur of Xanthomonas campestris is involved in hypersensitive response and positively regulates the expression of the hrp cluster via hrpX but not hrpG. Mol Plant Microbe Interact 2009, 22(3):321-329.
- [52]Jittawuttipoka T, Sallabhan R, Vattanaviboon P, Fuangthong M, Mongkolsuk S: Mutations of ferric uptake regulator (fur) impair iron homeostasis, growth, oxidative stress survival, and virulence of Xanthomonas campestris pv. campestris. Arch Microbiol 2010, 192(5):331-339.
- [53]Ryan RP, Dow JM: Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria. Trends Microbiol 2011, 19(3):145-152.
- [54]He YW, Wu J, Zhou L, Yang F, He YQ, Jiang BL, Bai L, Xu Y, Deng Z, Tang JL, et al.: Xanthomonas campestris diffusible factor is 3-hydroxybenzoic acid and is associated with xanthomonadin biosynthesis, cell viability, antioxidant activity, and systemic invasion. Mol Plant Microbe Interact 2011, 24(8):948-957.
- [55]Qian W, Han ZJ, He C: Two-component signal transduction systems of Xanthomonas spp.: a lesson from genomics. Mol Plant Microbe Interact 2008, 21(2):151-161.
- [56]Qian W, Han ZJ, Tao J, He C: Genome-scale mutagenesis and phenotypic characterization of two-component signal transduction systems in Xanthomonas campestris pv. campestris ATCC 33913. Mol Plant Microbe Interact 2008, 21(8):1128-1138.
- [57]Zhang SS, He YQ, Xu LM, Chen BW, Jiang BL, Liao J, Cao JR, Liu D, Huang YQ, Liang XX, et al.: A putative colRXC1049-colSXC1050 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. Res Microbiol 2008, 159(7–8):569-578.
- [58]He YW, Boon C, Zhou L, Zhang LH: Co-regulation of Xanthomonas campestris virulence by quorum sensing and a novel two-component regulatory system RavS/RavR. Mol Microbiol 2009, 71(6):1464-1476.
- [59]Postle K: TonB system, in vivo assays and characterization. Methods Enzymol 2007, 422:245-269.
- [60]Noinaj N, Guillier M, Barnard TJ, Buchanan SK: TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 2010, 64:43-60.
- [61]Braun V, Endriss F: Energy-coupled outer membrane transport proteins and regulatory proteins. Biometals 2007, 20(3–4):219-231.
- [62]Blanvillain S, Meyer D, Boulanger A, Lautier M, Guynet C, Denance N, Vasse J, Lauber E, Arlat M: Plant carbohydrate scavenging through TonB-dependent receptors: a feature shared by phytopathogenic and aquatic bacteria. PLoS One 2007, 2(2):e224.
- [63]Boulanger A, Dejean G, Lautier M, Glories M, Zischek C, Arlat M, Lauber E: Identification and regulation of the N-acetylglucosamine utilization pathway of the plant pathogenic bacterium Xanthomonas campestris pv. campestris. J Bacteriol 2010, 192(6):1487-1497.
- [64]Wiggerich HG, Klauke B, Köplin R, Priefer UB, Puhler A: Unusual structure of the tonB-exb DNA region of Xanthomonas campestris pv. campestris: tonB, exbB, and exbD1 are essential for ferric iron uptake, but exbD2 is not. J Bacteriol 1997, 179(22):7103-7110.
- [65]Hung CH, Yang CF, Yang CY, Tseng YH: Involvement of tonB-exbBD1D2 operon in infection of Xanthomonas campestris phage phi L7. Biochem Biophys Res Commun 2003, 302(4):878-884.
- [66]Wiggerich HG, Pühler A: The exbD2 gene as well as the iron-uptake genes tonB, exbB and exbD1 of Xanthomonas campestris pv. campestris are essential for the induction of a hypersensitive response on pepper (Capsicum annuum). Microbiology 2000, 146(Pt 5):1053-1060.
- [67]Alvarez B, Alvarez J, Menendez A, Guijarro JA: A mutant in one of two exbD loci of a TonB system in Flavobacterium psychrophilum shows attenuated virulence and confers protection against cold water disease. Microbiology 2008, 154(Pt 4):1144-1151.
- [68]Shirley M, Lamont IL: Role of TonB1 in pyoverdine-mediated signaling in Pseudomonas aeruginosa. J Bacteriol 2009, 191(18):5634-5640.
- [69]Gross A, Kapp D, Nielsen T, Niehaus K: Endocytosis of Xanthomonas campestris pathovar campestris lipopolysaccharides in non-host plant cells of Nicotiana tabacum. New Phytol 2005, 165(1):215-226.
- [70]Baier R, Schiene K, Kohring B, Flaschel E, Niehaus K: Alfalfa and tobacco cells react differently to chitin oligosaccharides and Sinorhizobium meliloti nodulation factors. Planta 1999, 210(1):157-164.
- [71]Felix G, Duran JD, Volko S, Boller T: Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 1999, 18(3):265-276.
- [72]Gomez-Gomez L, Boller T: Flagellin perception: a paradigm for innate immunity. Trends Plant Sci 2002, 7(6):251-256.
- [73]Nürnberger T, Wirtz W, Nennstiel D, Hahlbrock K, Jabs T, Zimmermann S, Scheel D: Signal perception and intracellular signal transduction in plant pathogen defense. J Recept Signal Transduct Res 1997, 17(1–3):127-136.
- [74]Rouet-Mayer M-A, Mathieu Y, Cazale A-C, Guern J, Lauriere C: Extracellular alkalinization and oxidative burst induced by fungal lyase in tobacco cells are not due to the perception of oligogalacturonide fragments. Plant Physiol Biochem 1997, 35(4):321-330.
- [75]Hardy MR, Townsend RR: Separation of positional isomers of oligosaccharides and glycopeptides by high-performance anion-exchange chromatography with pulsed amperometric detection. Proc Natl Acad Sci USA 1988, 85(10):3289-3293.
- [76]Moerschbacher BM, Mierau M, Graessner B, Noll U, Mort AJ: Small oligomers of galacturonic acid are endogenous suppressors of disease resistance reactions in wheat leaves. J Exp Bot 1999, 50(334):605-612.
- [77]Svalheim O, Robertsen B: 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. Physiol Plantarum 1993, 88(4):675-681.
- [78]Ryan CA: Oligosaccharides as recognition signals for the expression of defensive genes in plants. Biochemistry 1988, 27(25):8879-8883.
- [79]Norman C, Vidal S, Palva ET: Oligogalacturonide-mediated induction of a gene involved in jasmonic acid synthesis in response to the cell-wall-degrading enzymes of the plant pathogen Erwinia carotovora. Mol Plant Microbe Interact 1999, 12(7):640-644.
- [80]Stamp N: Out of the quagmire of plant defense hypotheses. Q Rev Biol 2003, 78(1):23-55.
- [81]Büttner D, Bonas U: Common infection strategies of plant and animal pathogenic bacteria. Curr Opin Plant Biol 2003, 6(4):312-319.
- [82]Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G: The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 2004, 16(12):3496-3507.
- [83]Aslam SN, Erbs G, Morrissey KL, Newman MA, Chinchilla D, Boller T, Molinaro A, Jackson RW, Cooper RM: Microbe-associated molecular pattern (MAMP) signatures, synergy, size and charge: influences on perception or mobility and host defence responses. Mol Plant Pathol 2009, 10(3):375-387.
- [84]Koebnik R: TonB-dependent trans-envelope signalling: the exception or the rule? Trends Microbiol 2005, 13(8):343-347.
- [85]Bordes P, Lavatine L, Phok K, Barriot R, Boulanger A, Castanie-Cornet MP, Dejean G, Lauber E, Becker A, Arlat M, et al.: Insights into the extracytoplasmic stress response of Xanthomonas campestris pv. campestris: role and regulation of σE-dependent activity. J Bacteriol 2011, 193(1):246-264.
- [86]Brown IE, Mallen MH, Charnock SJ, Davies GJ, Black GW: Pectate lyase 10A from Pseudomonas cellulosa is a modular enzyme containing a family 2a carbohydrate-binding module. Biochem J 2001, 355(Pt 1):155-165.
- [87]Guillén D, Sánchez S, Rodríguez-Sanoja R: Carbohydrate-binding domains: multiplicity of biological roles. Appl Microbiol Biotechnol 2010, 85(5):1241-1249.
- [88]Vorhölter FJ, Niehaus K, Pühler A: Lipopolysaccharide biosynthesis in Xanthomonas campestris pv. campestris: a cluster of 15 genes is involved in the biosynthesis of the LPS O-antigen and the LPS core. Mol Genet Genomics 2001, 266(1):79-95.
- [89]Bullock WO, Fernandez JM, Short JM: XL1-Blue: a high efficiency plasmid transforming recA Escherichia coli strain with beta-galactosidase selection. Biotechniques 1987, 5(4):376-379.
- [90]Vieira J, Messing J: New pUC-derived cloning vectors with different selectable markers and DNA replication origins. Gene 1991, 100:189-194.
- [91]Becker A, Schmidt M, Jäger W, Pühler A: New gentamicin-resistance and lacZ promoter-probe cassettes suitable for insertion mutagenesis and generation of transcriptional fusions. Gene 1995, 162(1):37-39.
- [92]Hagerman AE, Blau DM, McClure AL: Plate assay for determining the time of production of protease, cellulase, and pectinases by germinating fungal spores. Anal Biochem 1985, 151(2):334-342.
- [93]Hsiao YM, Fang MC, Sun PF, Tseng YH: Clp and RpfF up-regulate transcription of pelA1 gene encoding the major pectate lyase in Xanthomonas campestris pv. campestris. J Agric Food Chem 2009, 57(14):6207-6215.
- [94]Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, Kalinowski J, Linke B, Rupp O, Giegerich R, et al.: GenDB - an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 2003, 31(8):2187-2195.
- [95]Blom J, Albaum SP, Doppmeier D, Puhler A, Vorhölter FJ, Zakrzewski M, Goesmann A: EDGAR: A software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 2009, 10(1):154. BioMed Central Full Text
- [96]Pieretti I, Royer M, Barbe V, Carrere S, Koebnik R, Cociancich S, Couloux A, Darrasse A, Gouzy J, Jacques MA, et al.: The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics 2009, 10:616. BioMed Central Full Text
- [97]Thieme F, Koebnik R, Bekel T, Berger C, Boch J, Büttner D, Caldana C, Gaigalat L, Goesmann A, Kay S, et al.: Insights into genome plasticity and pathogenicity of the plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria revealed by the complete genome sequence. J Bacteriol 2005, 187(21):7254-7266.
- [98]Salzberg SL, Sommer DD, Schatz MC, Phillippy AM, Rabinowicz PD, Tsuge S, Furutani A, Ochiai H, Delcher AL, Kelley D, et al.: Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics 2008, 9:204. BioMed Central Full Text
- [99]Ochiai H, Inoue V, Takeya M, Sasaki A, Kaku H: Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity. Jarq-Jpn Agr Res Q 2005, 39(4):275-287.
- [100]Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B: The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 2009, 37(Database issue):D233-D238.
- [101]Sambrook H, Fritsch EF, Maniatis T: Molecular cloning: a laboraratory manual. 2nd edition. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY; 1989.
- [102]Wilder JA, Cowdery JS, Ashman RF: The influence of lipopolysaccharide content on the apparent B cell stimulating activity of anti-μ preparations. J Immunol Methods 1988, 110(1):63-68.
- [103]Silswal N, Singh AK, Aruna B, Mukhopadhyay S, Ghosh S, Ehtesham NZ: Human resistin stimulates the pro-inflammatory cytokines TNF-alpha and IL-12 in macrophages by NF-kappaB-dependent pathway. Biochem Biophys Res Commun 2005, 334(4):1092-1101.
- [104]Warm E, Laties GG: Quantification of hydrogen peroxide in plant extracts by the chemoluminescence reaction with luminol. Phytochem 1982, 21:827-831.
- [105]Murashige T, Skoog F: A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 1962, 15:473-497.