Bacterial Flagella: Twist and Stick, or Dodge across the Kingdoms

PLoS Pathogens

Volumn 11, Issue 1, 2015, Pages 1-15

  Rossez, Yannick ^a   Wolfson, Eliza B ^b   Holmes, Ashleigh ^a   Gally, David L ^b   Holden, Nicola J ^a  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; TOLL LIKE RECEPTOR 5;

ADHESION; ANTIGEN RECOGNITION; BACTERIAL FLAGELLUM; BIOPHYSICS; ENTEROPATHOGENIC ESCHERICHIA COLI; HOST PARASITE INTERACTION; IMMUNE EVASION; INNATE IMMUNITY; LISTERIA MONOCYTOGENES; MICROBIAL COLONIZATION; MUCUS; NONHUMAN; PLANT TISSUE; PSEUDOMONAS AERUGINOSA; REVIEW; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SIGNAL TRANSDUCTION; STENOTROPHOMONAS MALTOPHILIA; ANIMAL; BACTERIUM; BACTERIUM ADHERENCE; CHEMISTRY; CHEMOTAXIS; EVOLUTION; FLAGELLUM; HOST PATHOGEN INTERACTION; HUMAN; MAMMAL; MICROBIOLOGY; MOVEMENT (PHYSIOLOGY); PHYSIOLOGY; PLANT; ULTRASTRUCTURE;

ANIMALIA; BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA; SALMONELLA ENTERICA;

ANIMALS; BACTERIA; BACTERIAL ADHESION; BIOLOGICAL EVOLUTION; CHEMOTAXIS; FLAGELLA; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; MAMMALS; MOVEMENT; PLANTS;

EID: 84923844712     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004483     Document Type: Review

References (113)

1. Sourjik V, Wingreen NS, (2012) Responding to chemical gradients: bacterial chemotaxis. Curr Opin Cell Biol 24: 262–268. doi: 10.1016/j.ceb.2011.11.008 22169400
2. Egelman EH, (2010) Reducing irreducible complexity: divergence of quaternary structure and function in macromolecular assemblies. Curr Opin Cell Biol 22: 68–74. doi: 10.1016/j.ceb.2009.11.007 20006482
3. Evans LD, Poulter S, Terentjev EM, Hughes C, Fraser GM, (2013) A chain mechanism for flagellum growth. Nature 504: 287–290. doi: 10.1038/nature12682 24213633
4. Rossez Y, Holmes A, Wolfson EB, Gally DL, Mahajan A, et al. (2014) Flagella interact with ionic plant lipids to mediate adherence of pathogenic Escherichia coli to fresh produce plants. Environ Microbiol 16: 2181–2195. doi: 10.1111/1462-2920.12315 24148193
5. Haiko J, Westerlund-Wikström B, (2013) The role of the bacterial flagellum in adhesion and virulence. Biology 2: 1242–1267. doi: 10.3390/biology2041242 24833223
6. Pratt LA, Kolter R, (1998) Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30: 285–293. 9791174
7. Friedlander RS, Vlamakis H, Kim P, Khan M, Kolter R, et al. (2013) Bacterial flagella explore microscale hummocks and hollows to increase adhesion. Proc Natl Acad Sci USA 110: 5624–5629. doi: 10.1073/pnas.1219662110 23509269
8. Magariyama Y, Sugiyama S, Muramoto K, Maekawa Y, Kawagishi I, et al. (1994) Very fast flagellar rotation. Nature 371: 752. 7935835
9. Haefele DM, Lindow SE, (1987) Flagellar motility confers epiphytic fitness advantages upon Pseudomonas syringae. Appl Environ Microbiol 53: 2528–2533. 16347469
10. Michiels KW, Croes CL, Vanderleyden J, (1991) Two different modes of attachment of Azospirillum brasilense Sp7 to wheat roots. J Gen Microbiol 137: 2241–2246.
11. Holden N, Pritchard L, Toth I, (2009) Colonization outwith the colon: plants as an alternative environmental reservoir for human pathogenic enterobacteria. FEMS Microbiol Rev 33: 689–703. doi: 10.1111/j.1574-6976.2008.00153.x 19076238
12. Grad YH, Lipsitch M, Feldgarden M, Arachchi HM, Cerqueira GC, et al. (2012) Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011. Proc Natl Acad Sci USA 109: 3065–3070. doi: 10.1073/pnas.1121491109 22315421
13. Berger CN, Shaw RK, Ruiz-Perez F, Nataro JP, Henderson IR, et al. (2009) Interaction of enteroaggregative Escherichia coli with salad leaves. Environ Microbiol Rep 1: 234–239. doi: 10.1111/j.1758-2229.2009.00037.x 23765852
14. Gorski L, Duhé JM, Flaherty D, (2009) The use of flagella and motility for plant colonization and fitness by different strains of the foodborne pathogen Listeria monocytogenes. PLoS ONE 4: e5142. doi: 10.1371/journal.pone.0005142 19357783
15. Kroupitski Y, Golberg D, Belausov E, Pinto R, Swartzberg D, et al. (2009) Internalization of Salmonella enterica in leaves is induced by light and involves chemotaxis and penetration through open stomata. Appl Environ Microbiol 75: 6076–6086. doi: 10.1128/AEM.01084-09 19648358
16. Saldana Z, Sanchez E, Xicohtencatl-Cortes J, Puente JL, Giron JA, (2011) Surface structures involved in plant stomata and leaf colonization by Shiga-toxigenic Escherichia coli O157:H7. Front Microbiol 2: 119. doi: 10.3389/fmicb.2011.00119 21887151
17. Shaw RK, Berger CN, Pallen MJ, Sjoeling A, Frankel G, (2011) Flagella mediate attachment of enterotoxigenic Escherichia coli to fresh salad leaves. Environ Microbiol Rep 3: 112–117. doi: 10.1111/j.1758-2229.2010.00195.x 23761239
18. Cooley MB, Miller WG, Mandrell RE, (2003) Colonization of Arabidopsis thaliana with Salmonella enterica and enterohemorrhagic Escherichia coli O157:H7 and competition by Enterobacter asburiae. Appl Environ Microbiol 69: 4915–4926. 12902287
19. Mahenthiralingam E, Speert DP, (1995) Nonopsonic phagocytosis of Pseudomonas aeruginosa by macrophages and polymorphonuclear leukocytes requires the presence of the bacterial flagellum. Infect Immun 63: 4519–4523. 7591095
20. Dons L, Eriksson E, Jin Y, Rottenberg ME, Kristensson K, et al. (2004) Role of flagellin and the two-component CheA/CheY system of Listeria monocytogenes in host cell invasion and virulence. Infect Immun 72: 3237–3244. 15155625
21. Erdem AL, Avelino F, Xicohtencatl-Cortes J, Giron JA, (2007) Host protein binding and adhesive properties of H6 and H7 flagella of attaching and effacing Escherichia coli. J Bacteriol 189: 7426–7435. 17693516
22. Mahajan A, Currie CG, Mackie S, Tree J, McAteer S, et al. (2009) An investigation of the expression and adhesin function of H7 flagella in the interaction of Escherichia coli O157: H7 with bovine intestinal epithelium. Cell Microbiol 11: 121–137. doi: 10.1111/j.1462-5822.2008.01244.x 19016776
23. Giron JA, Torres AG, Freer E, Kaper JB, (2002) The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 44: 361–379. 11972776
24. Song YC, Jin S, Louie H, Ng D, Lau R, et al. (2004) FlaC, a protein of Campylobacter jejuni TGH9011 (ATCC43431) secreted through the flagellar apparatus, binds epithelial cells and influences cell invasion. Mol Microbiol 53: 541–553. 15228533
25. McGuckin MA, Linden SK, Sutton P, Florin TH, (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9: 265–278. doi: 10.1038/nrmicro2538 21407243
26. Schreiber S, Konradt M, Groll C, Scheid P, Hanauer G, et al. (2004) The spatial orientation of Helicobacter pylori in the gastric mucus. Proc Natl Acad Sci USA 101: 5024–5029. 15044704
27. Eaton K, Morgan D, Krakowka S, (1992) Motility as a factor in the colonisation of gnotobiotic piglets by Helicobacter pylori. J Med Microbiol 37: 123–127. 1629897
28. Ottemann KM, Lowenthal AC, (2002) Helicobacter pylori uses motility for initial colonization and to attain robust infection. Infect Immun 70: 1984–1990. 11895962
29. Clyne M, Ocroinin T, Suerbaum S, Josenhans C, Drumm B, (2000) Adherence of isogenic flagellum-negative mutants of Helicobacter pylori and Helicobacter mustelae to human and ferret gastric epithelial cells. Infect Immun 68: 4335–4339. 10858255
30. Kim JC, Yoon JW, Kim C-H, Park M-S, Cho S-H, (2012) Repression of flagella motility in enterohemorrhagic Escherichia coli O157: H7 by mucin components. Biochem Biophys Res Comm 423: 789–792. doi: 10.1016/j.bbrc.2012.06.041 22713459
31. McCormick B, Stocker B, Laux D, Cohen P, (1988) Roles of motility, chemotaxis, and penetration through and growth in intestinal mucus in the ability of an avirulent strain of Salmonella typhimurium to colonize the large intestine of streptomycin-treated mice. Infect Immun 56: 2209–2217. 3044995
32. McCormick BA, Laux DC, Cohen PS, (1990) Neither motility nor chemotaxis plays a role in the ability of Escherichia coli F-18 to colonize the streptomycin-treated mouse large intestine. Infect Immun 58: 2957–2961. 2201640
33. Liu Z, Miyashiro T, Tsou A, Hsiao A, Goulian M, et al. (2008) Mucosal penetration primes Vibrio cholerae for host colonization by repressing quorum sensing. Proc Natl Acad Sci USA 105: 9769–9774. doi: 10.1073/pnas.0802241105 18606988
34. Zgair AK, Chhibber S, (2011) Adhesion of Stenotrophomonas maltophilia to mouse tracheal mucus is mediated through flagella. J Med Microbiol 60: 1032–1037. doi: 10.1099/jmm.0.026377-0 21415208
35. Erdem AL, Avelino F, Xicohtencatl-Cortes J, Girón JA, (2007) Host protein binding and adhesive properties of H6 and H7 flagella of attaching and effacing Escherichia coli. J Bacteriol 189: 7426–7435. 17693516
36. Scharfman A, Arora SK, Delmotte P, Van Brussel E, Mazurier J, et al. (2001) Recognition of Lewis x derivatives present on mucins by flagellar components of Pseudomonas aeruginosa. Infect Immun 69: 5243–5248. 11500392
37. Arora SK, Ritchings BW, Almira EC, Lory S, Ramphal R, (1998) The Pseudomonas aeruginosa flagellar cap protein, FliD, is responsible for mucin adhesion. Infect Immun 66: 1000–1007. 9488388
38. Troge A, Scheppach W, Schroeder BO, Rund SA, Heuner K, et al. (2012) More than a marine propeller – the flagellum of the probiotic Escherichia coli strain Nissle 1917 is the major adhesin mediating binding to human mucus. Int J Med Microbiol 302: 304–314. doi: 10.1016/j.ijmm.2012.09.004 23131416
39. Rossez Y, Maes E, Darroman TL, Gosset P, Ecobichon C, et al. (2012) Almost all human gastric mucin O-glycans harbor blood group A, B or H antigens and are potential binding sites for Helicobacter pylori. Glycobiol 22: 1193–1206. doi: 10.1093/glycob/cws072 22522599
40. Robbe C, Capon C, Coddeville B, Michalski J, (2004) Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract. Biochem J 384: 307–316. 15361072
41. Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP, et al. (2005) Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307: 1955–1959. 15790854
42. Peekhaus N, Conway T, (1998) What’s for dinner?: Entner-Doudoroff metabolism in Escherichia coli. J Bacteriol 180: 3495–3502. 9657988
43. RdO Pinheiro, Boddey LH, James EK, Sprent JI, Boddey RM, (2002) Adsorption and anchoring of Azospirillum strains to roots of wheat seedlings. Plant Soil 246: 151–166.
44. Watt M, Hugenholtz P, White R, Vinall K, (2006) Numbers and locations of native bacteria on field-grown wheat roots quantified by fluorescence in situ hybridization (FISH). Environ Microbiol 8: 871–884. 16623744
45. Driouich A, Follet-Gueye M-L, Vicré-Gibouin M, Hawes M, (2013) Root border cells and secretions as critical elements in plant host defense. Curr Opin Plant Biol 16: 489–495. doi: 10.1016/j.pbi.2013.06.010 23856080
46. Bucior I, Pielage JF, Engel JN, (2012) Pseudomonas aeruginosa pili and flagella mediate distinct binding and signaling events at the apical and basolateral surface of airway epithelium. PLoS Path 8: e1002616. doi: 10.1371/journal.ppat.1002616 22496644
47. Ketko AK, Lin C, Moore BB, LeVine AM, (2013) Surfactant protein A binds flagellin enhancing phagocytosis and IL-1β production. PLoS ONE 8: e82680. doi: 10.1371/journal.pone.0082680 24312669
48. Feldman M, Bryan R, Rajan S, Scheffler L, Brunnert S, et al. (1998) Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 66: 43–51. 9423837
49. Rogers TJ, Thorpe CM, Paton AW, Paton JC, (2012) Role of lipid rafts and flagellin in invasion of colonic epithelial cells by Shiga-toxigenic Escherichia coli O113: H21. Infect Immun 80: 2858–2867. doi: 10.1128/IAI.00336-12 22689816
50. Roy K, Hilliard GM, Hamilton DJ, Luo J, Ostmann MM, et al. (2008) Enterotoxigenic Escherichia coli EtpA mediates adhesion between flagella and host cells. Nature 457: 594–598. doi: 10.1038/nature07568 19060885
51. Rossez Y, Holmes A, Wolfson EB, Gally DL, Mahajan A, et al. (2013) Flagella interact with ionic plant lipids to mediate adherence of pathogenic Escherichia coli to fresh produce plants. Environ Microbiol 16: 2181–2195. doi: 10.1111/1462-2920.12315 24148193
52. Misselwitz B, Barrett N, Kreibich S, Vonaesch P, Andritschke D, et al. (2012) Near surface swimming of Salmonella Typhimurium explains target-site selection and cooperative invasion. PLoS Pathog 8: e1002810. doi: 10.1371/journal.ppat.1002810 22911370
53. Lai MA, Quarles EK, López-Yglesias AH, Zhao X, Hajjar AM, et al. (2013) Innate immune detection of flagellin positively and negatively regulates Salmonella infection. PLoS ONE 8: e72047. doi: 10.1371/journal.pone.0072047 23977202
54. Lockman HA, Curtiss R, (1990) Salmonella typhimurium mutants lacking flagella or motility remain virulent in BALB/c mice. Infect Immun 58: 137–143. 2152887
55. Olsen JE, Hoegh-Andersen KH, Casadesús J, Rosenkranzt J, Chadfield MS, et al. (2013) The role of flagella and chemotaxis genes in host pathogen interaction of the host adapted Salmonella enterica serovar Dublin compared to the broad host range serovar S. Typhimurium. BMC Microbiol 13: 67. doi: 10.1186/1471-2180-13-67 23530934
56. Cullender TC, Chassaing B, Janzon A, Kumar K, Muller CE, et al. (2013) Innate and adaptive immunity interact to quench microbiome flagellar motility in the gut. Cell Host Microbe 14: 571–581. doi: 10.1016/j.chom.2013.10.009 24237702
57. Yonekura K, Maki-Yonekura S, Namba K, (2003) Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424: 643–650. 12904785
58. Reid SD, Selander RK, Whittam TS, (1999) Sequence diversity of flagellin (fliC) alleles in pathogenic Escherichia coli. J Bacteriol 181: 153–160. 9864325
59. Brenner F, Villar R, Angulo F, Tauxe R, Swaminathan B, (2000) Salmonella nomenclature. J Clin Microbiol 38: 2465–2467. 10878026
60. Popoff MY, Bockemühl J, Gheesling LL, (2003) Supplement 2001 (no. 45) to the Kauffmann–White scheme. Res Microbiol 154: 173–174. 12706505
61. Beatson SA, Minamino T, Pallen MJ, (2006) Variation in bacterial flagellins: from sequence to structure. Trend Microbiol 14: 151–155. 16540320
62. Yonekura K, Maki-Yonekura S, Namba K, (2003) Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424: 643–650. 12904785
63. Felix G, Duran JD, Volko S, Boller T, (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18: 265–276. 10377992
64. Lemaitre B, Reichhart JM, Hoffmann JA, (1997) Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci USA 94: 14614–14619. 9405661
65. McDermott PF, Ciacci-Woolwine F, Snipes JA, Mizel SB, (2000) High-affinity interaction between gram-negative flagellin and a cell surface polypeptide results in human monocyte activation. Infect Immun 68: 5525–5529. 10992449
66. Eaves-Pyles TD, Wong HR, Odoms K, Pyles RB, (2001) Salmonella flagellin-dependent proinflammatory responses are localized to the conserved amino and carboxyl regions of the protein. J Immunol 167: 7009–7016. 11739521
67. Smith KD, Andersen-Nissen E, Hayashi F, Strobe K, Bergman MA, et al. (2003) Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nature Immunol 4: 1247–1253. 14625549
68. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099–1103. 11323673
69. Zhao Y, Yang J, Shi J, Gong Y-N, Lu Q, et al. (2011) The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477: 596–600. doi: 10.1038/nature10510 21918512
70. Gomez-Gomez L, Boller T, (2000) FLS2: an LRR receptor–like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003–1011. 10911994
71. Ausubel FM, (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6: 973–979. 16177805
72. Jacchieri SG, Torquato R, Brentani RR, (2003) Structural study of binding of flagellin by Toll-like receptor 5. J Bacteriol 185: 4243–4247. 12837800
73. S-i Yoon, Kurnasov O, Natarajan V, Hong M, Gudkov AV, et al. (2012) Structural basis of TLR5-flagellin recognition and signaling. Science 335: 859–864. doi: 10.1126/science.1215584 22344444
74. Gómez-Gómez L, Boller T, (2000) FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003–1011. 10911994
75. Felix G, Duran JD, Volko S, Boller T, (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18: 265–276. 10377992
76. Cai R, Lewis J, Yan S, Liu H, Clarke CR, et al. (2011) The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Path 7: e1002130. doi: 10.1371/journal.ppat.1002130 21901088
77. Clarke CR, Chinchilla D, Hind SR, Taguchi F, Miki R, et al. (2013) Allelic variation in two distinct Pseudomonas syringae flagellin epitopes modulates the strength of plant immune responses but not bacterial motility. New Phytol 200: 847–860. doi: 10.1111/nph.12408 23865782
78. Halff EF, Diebolder CA, Versteeg M, Schouten A, Brondijk TH, et al. (2012) Formation and structure of a NAIP5-NLRC4 inflammasome induced by direct interactions with conserved N- and C-terminal regions of flagellin. J Biol Chem 287: 38460–38472. doi: 10.1074/jbc.M112.393512 23012363
79. Lightfield KL, Persson J, Brubaker SW, Witte CE, von Moltke J, et al. (2008) Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat Immunol 9: 1171–1178. doi: 10.1038/ni.1646 18724372
80. Wei HL, Chakravarthy S, Worley JN, Collmer A, (2013) Consequences of flagellin export through the type III secretion system of Pseudomonas syringae reveal a major difference in the innate immune systems of mammals and the model plant Nicotiana benthamiana. Cell Microbiol 15: 601–618. doi: 10.1111/cmi.12059 23107228
81. McQuiston JR, Fields PI, Tauxe RV, Logsdon JM, Jr. (2008) Do Salmonella carry spare tyres? Trends Microbiol 16: 142–148. doi: 10.1016/j.tim.2008.01.009 18375124
82. Alm R, Guerry P, Trust T, (1993) The Campylobacter sigma 54 flaB flagellin promoter is subject to environmental regulation. J Bacteriol 175: 4448–4455. 8331072
83. Silverman M, Zieg J, Hilmen M, Simon M, (1979) Phase variation in Salmonella: genetic analysis of a recombinational switch. Proc Natl Acad Sci USA 76: 391–395. 370828
84. Smith NH, Selander RK, (1991) Molecular genetic basis for complex flagellar antigen expression in a triphasic serovar of Salmonella. Proc Natl Acad Sci USA 88: 956–960. 1992487
85. Dobbin HS, Hovde CJ, Williams CJ, Minnich SA, (2006) The Escherichia coli O157 flagellar regulatory gene flhC and not the flagellin gene fliC impacts colonization of cattle. Infect Immun 74: 2894–2905. 16622228
86. Darrasse A, Carrere S, Barbe V, Boureau T, Arrieta-Ortiz ML, et al. (2013) Genome sequence of Xanthomonas fuscans subsp. fuscans strain 4834-R reveals that flagellar motility is not a general feature of xanthomonads. BMC Genomics 14: 761. doi: 10.1186/1471-2164-14-761 24195767
87. Ikeda JS, Schmitt CK, Darnell SC, Watson PR, Bispham J, et al. (2001) Flagellar phase variation of Salmonella enterica serovar Typhimurium contributes to virulence in the murine typhoid infection model but does not influence Salmonella-induced enteropathogenesis. Infect Immun 69: 3021–3030. 11292720
88. Andersen-Nissen E, Smith KD, Strobe KL, Barrett SL, Cookson BT, et al. (2005) Evasion of Toll-like receptor 5 by flagellated bacteria. Proc Natl Acad Sci USA 102: 9247–9252. 15956202
89. Yang J, Zhang E, Liu F, Zhang Y, Zhong M, et al. (2014) Flagellins of Salmonella Typhi and nonpathogenic Escherichia coli are differentially recognized through the NLRC4 pathway in macrophages. J Innate Immun 6: 47–57. doi: 10.1159/000351476 23816851
90. Galkin VE, Yu X, Bielnicki J, Heuser J, Ewing CP, et al. (2008) Divergence of quaternary structures among bacterial flagellar filaments. Science 320: 382–385. doi: 10.1126/science.1155307 18420936
91. Sun W, Dunning FM, Pfund C, Weingarten R, Bent AF, (2006) Within-species flagellin polymorphism in Xanthomonas campestris pv campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2-dependent defenses. Plant Cell 18: 764–779. 16461584
92. Garcia AV, Charrier A, Schikora A, Bigeard J, Pateyron S, et al. (2014) Salmonella enterica flagellin is recognized via FLS2 and activates PAMP-triggered immunity in Arabidopsis thaliana. Mol Plant 7: 657–674. doi: 10.1093/mp/sst145 24198231
93. Trdá L, Fernandez O, Boutrot F, Héloir M-C, Kelloniemi J, et al. (2014) The grapevine flagellin receptor VvFLS2 differentially recognizes flagellin-derived epitopes from the endophytic growth-promoting bacterium Burkholderia phytofirmans and plant pathogenic bacteria. New Phytol 201: 1371–1384. doi: 10.1111/nph.12592 24491115
94. Shan L, He P, Li J, Heese A, Peck SC, et al. (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microb 4: 17–27. doi: 10.1016/j.chom.2008.05.017 18621007
95. Xiang T, Zong N, Zou Y, Wu Y, Zhang J, et al. (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18: 74–80. 18158241
96. Hann DR, Domínguez – Ferreras A, Motyka V, Dobrev PI, Schornack S, et al. (2014) The Pseudomonas type III effector HopQ1 activates cytokinin signaling and interferes with plant innate immunity. New Phytol 201: 585–598. doi: 10.1111/nph.12544 24124900
97. Melotto M, Underwood W, Koczan J, Nomura K, He SY, (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969–980. 16959575
98. Montillet JL, Leonhardt N, Mondy S, Tranchimand S, Rumeau D, et al. (2013) An abscisic acid-independent oxylipin pathway controls stomatal closure and immune defense in Arabidopsis. PLoS Biol 11: e1001513 doi: 10.1371/journal.pbio.1001513 23526882
99. Underwood W, Melotto M, He SY, (2007) Role of plant stomata in bacterial invasion. Cell Microbiol 9: 1621–1629. 17419713
100. Roy D, Panchal S, Rosa BA, Melotto M, (2013) Escherichia coli O157:H7 induces stronger plant immunity than Salmonella enterica Typhimurium SL1344. Phytopathol 103: 326–332. doi: 10.1094/PHYTO-09-12-0230-FI 23301812
101. Bardoel BW, van der Ent S, Pel MJ, Tommassen J, Pieterse CM, et al. (2011) Pseudomonas evades immune recognition of flagellin in both mammals and plants. PLoS Path 7: e1002206. doi: 10.1371/journal.ppat.1002206 21901099
102. Ichinose Y, Taguchi F, Yamamoto M, Ohnishi-Kameyama M, Atsumi T, et al. (2013) Flagellin glycosylation is ubiquitous in a broad range of phytopathogenic bacteria. J Gen Plant Pathol 79: 359–365.
103. Ewing CP, Andreishcheva E, Guerry P, (2009) Functional characterization of flagellin glycosylation in Campylobacter jejuni 81–176. J Bacteriol 191: 7086–7093. doi: 10.1128/JB.00378-09 19749047
104. Hirai H, Takai R, Iwano M, Nakai M, Kondo M, et al. (2011) Glycosylation regulates specific induction of rice immune responses by Acidovorax avenae flagellin. J Biol Chem 286: 25519–25530. doi: 10.1074/jbc.M111.254029 21628471
105. Logan SM, Trust TJ, Guerry P, (1989) Evidence for posttranslational modification and gene duplication of Campylobacter flagellin. J Bacteriol 171: 3031–3038. 2722741
106. Brimer CD, Montie T, (1998) Cloning and comparison of fliC genes and identification of glycosylation in the flagellin of Pseudomonas aeruginosa a-type strains. J Bacteriol 180: 3209–3217. 9620973
107. Sun L, Jin M, Ding W, Yuan J, Kelly J, et al. (2013) Post-translational modification of flagellin FlaB in Shewanella oneidensis. J Bacteriol 195: 2550–2561. doi: 10.1128/JB.00015-13 23543712
108. de Zoete MR, Keestra AM, Wagenaar JA, van Putten JP, (2010) Reconstitution of a functional Toll-like receptor 5 binding site in Campylobacter jejuni flagellin. J Biol Chem 285: 12149–12158. doi: 10.1074/jbc.M109.070227 20164175
109. Arora SK, Neely AN, Blair B, Lory S, Ramphal R, (2005) Role of motility and flagellin glycosylation in the pathogenesis of Pseudomonas aeruginosa burn wound infections. Infect Immun 73: 4395–4398. 15972536
110. Szymanski CM, Burr DH, Guerry P, (2002) Campylobacter protein glycosylation affects host cell interactions. Infect Immun 70: 2242. 11895996
111. Taguchi F, Suzuki T, Takeuchi K, Inagaki Y, Toyoda K, et al. (2009) Glycosylation of flagellin from Pseudomonas syringae pv. tabaci 6605 contributes to evasion of host tobacco plant surveillance system. Physiol Mol Plant Pathol 74: 11–17.
112. Tronick SR, Martinez RJ, (1971) Methylation of the flagellin of Salmonella typhimurium. J Bacteriol 105: 211–219. 5541007
113. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera—A visualization system for exploratory research and analysis. J Comput Chem 25: 1605–1612. 15264254