Agrobacterium-Host Attachment and Biofilm Formation

  • Clay Fuqua

Physical association with host plant tissue is a prerequisite to Agrobacterium tumefaciens infection and subsequent disease. Mechanisms of tissue adherence have been extensively studied in mammalian pathogens, but less so in plant-associated bacteria. Cells of A. tumefaciens often attach to plant tissue by a single pole. In the appropriate environment, these attached bacteria eventually develop into multicellular assemblies called biofilms, enmeshed within exopolymeric material produced by the bacteria and possibly the plant host. It remains unclear whether all modes of plant attachment can lead to interkingdom gene transfer, or whether the conformation of the infecting agrobacterial population influences this process. A two-step model was proposed in which the bacterium initially attaches reversibly by way of interactions between a bacterial adhesin structure(s) and a plant receptor( s), followed by a more tenacious attachment coincident with production of cellulose fibrils. This adherence model, while potentially still valid, remains largely untested. Possible A. tumefaciens adherence functions, including lipopolysaccharides and cyclic β-1,2-glucans have been identified, but none has been definitively shown to mediate productive attachment to plants. Similarly, despite some promising leads, no confirmed plant receptor candidates have been identified. A. tumefaciens forms biofilms on a variety of surfaces including but not restricted to plant tissues. Studies of biofilm formation by A. tumefaciens on model surfaces have revealed a degree of structural and functional overlap with plant association, including several common cell surface structures and key regulatory pathways.


Agrobacterium Tumefaciens Crown Gall Cellulose Fibril Abiotic Surface exoR Mutant 
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9 References

  1. Amikam D, Benziman M (1989) Cyclic diguanylic acid and cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 171: 6649-6655PubMedGoogle Scholar
  2. Armitage JP, Schmitt R (1997) Bacterial chemotaxis: Rhodobacter sphaeroides and Sinorhizobium meliloti ņ variations on a theme? Microbiology 143: 3671-3682PubMedCrossRefGoogle Scholar
  3. Ashby AM, Watson MD, Loake GJ, Shaw CH (1988) Ti plasmid-specified chemotaxis of Agrobacterium tumefaciens C58C1 toward vir-inducing pheno-lic compounds and soluble factors from monocotyledonous and dicotyledo-nous plants. J Bacteriol 170: 4181-4187PubMedGoogle Scholar
  4. Ausmees N, Jacobsson K, Lindberg M (2001a) A unipolarly located, cell-surface-associated agglutinin, RapA, belongs to a family of Rhizobium-adhering proteins (Rap) in Rhizobium leguminosarum bv. trifolii. Microbiology 147: 549-559PubMedGoogle Scholar
  5. Ausmees N, Mayer R, Weinhouse H, Volman G, Amikam D, Benziman M, Lindberg M (2001b) Genetic data indicate that proteins containing the GGDEF domain possess diguanylate cyclase activity. FEMS Microbiol Lett 204: 163-167PubMedCrossRefGoogle Scholar
  6. Bash R, Matthysse AG (2002) Attachment to roots and virulence of a chvB mutant of Agrobacterium tumefaciens are temperature sensitive. Mol Plant-Microbe Interact 15: 160-163PubMedCrossRefGoogle Scholar
  7. Becker A, Puhler A (1998) Production of expolysaccharides. In HP Spaink, A Kondorosi, PJJ Hooykaas, eds, The Rhizobeaceae: Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic Publishers, Boston, pp 97-118Google Scholar
  8. Blatch GL, Lassle M (1999) The tetratricopeptide repeat: a structural motif medi-ating protein-protein interactions. Bio Essays 21: 932-939Google Scholar
  9. Bouzar H, Moore LW (1987) Isolation of different Agrobacterium biovars from a natural oak savanna and tallgrass prairie. Appl Environm Microbiol 53: 717-721Google Scholar
  10. Boyle EC, Finlay BB (2003) Bacterial pathogenesis: exploiting cellular adherence. Curr Opin Cell Biol 15: 633-639PubMedCrossRefGoogle Scholar
  11. Breedveld MW, Miller KJ (1994) Cyclic beta-glucans of members of the family Rhizobiaceae. Microbiol Rev 58: 145-161PubMedGoogle Scholar
  12. Breedveld MW, Miller KJ (1998) Cell-surface beta-glucans. In HP Spaink, A Kondorosi, PJJ Hooykaas, eds, The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic Publishers, Boston, pp 81-96Google Scholar
  13. Brencic A, Angert ER, Winans SC (2005) Unwounded plants elicit Agrobacterium vir gene induction and T-DNA transfer: transformed plant cells produce opines yet are tumor free. Mol Microbiol 57: 1522-1531PubMedCrossRefGoogle Scholar
  14. Burdman S, Okon Y, Jurkevitch E (2000) Surface characteristics of Azospirillum brasilense in relation to cell aggregation and attachment to plant roots. Crit Rev Microbiol 26: 91-110PubMedCrossRefGoogle Scholar
  15. Burr TJ, Katz BH, Bishop AL (1987) Populations of Agrobacterium in vineyard and nonvineyard soils and grape roots in vineyards and nurseries. Plant Dis 71: 617-620CrossRefGoogle Scholar
  16. Cangelosi GA, Hung L, Puvanesarajah V, Stacey G, Ozga DA, Leigh JA, Nester EW (1987) Common loci for Agrobacterium tumefaciens and Rhizobium meliloti exopolysaccharide synthesis and their roles in plant interactions. J Bacteriol 169: 2086-2091PubMedGoogle Scholar
  17. Cangelosi GA, Martinetti G, Leigh JA, Lee CC, Theines C, Nester EW (1989) Role for Agrobacterium tumefaciens ChvA protein in export of beta-1,2-glucan. J Bacteriol 171: 1609-1615PubMedGoogle Scholar
  18. Chesnokova O, Coutinho JB, Khan IH, Mikhail MS, Kado CI (1997) Characteri-zation of flagella genes of Agrobacterium tumefaciens, and the effect of a bald strain on virulence. Mol Microbiol 23: 579-590PubMedCrossRefGoogle Scholar
  19. Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E (2005) Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol 59: 451-485PubMedCrossRefGoogle Scholar
  20. Cortez N, Carrillo N, Pasternak C, Balzer A, Klug G (1998) Molecular cloning and expression analysis of the Rhodobacter capsulatus sodB gene, encoding an iron superoxide dismutase. J Bacteriol 180: 5413-5420.PubMedGoogle Scholar
  21. Danhorn T, Hentzer M, Givskov M, Parsek MR, Fuqua C (2004) Phosphorus limi-tation enhances biofilm formation of the plant pathogen Agrobacterium tume-faciens through the PhoR-PhoB regulatory system. J Bacteriol 186: 4492-4501PubMedCrossRefGoogle Scholar
  22. Dardanelli M, Angelini J, Fabra A (2003) A calcium-dependent bacterial surface protein is involved in the attachment of rhizobia to peanut roots. Can J Micro-biol 49: 399-405CrossRefGoogle Scholar
  23. D’Argenio DA, Miller SI (2004) Cyclic di-GMP as a bacterial second messenger. Microbiology 150: 2497-2502PubMedCrossRefGoogle Scholar
  24. De Cleene M, De Ley J (1976) The host range of crown gall. Bot Rev 42: 389-466CrossRefGoogle Scholar
  25. Deakin WJ, Parker VE, Wright EL, Ashcroft KJ, Loake GJ, Shaw CH (1999) Agrobacterium tumefaciens possesses a fourth flagelin gene located in a large gene cluster concerned with flagellar structure, assembly and motility. Micro-biology 145: 1397-1407Google Scholar
  26. Douglas CJ, Halperin W, Nester EW (1982) Agrobacterium tumefaciens mutants affected in attachment to plant cells. J Bacteriol 152: 1265-1275PubMedGoogle Scholar
  27. Douglas CJ, Staneloni RJ, Rubin RA, Nester EW (1985) Identification and genetic analysis of an Agrobacterium tumefaciens chromsomal virulence region. J Bacteriol 161: 850-860PubMedGoogle Scholar
  28. Escudero J, Hohn B (1997) Transfer and integration of T-DNA without cell injury in the host plant. Plant Cell 9: 2135-2142PubMedCrossRefGoogle Scholar
  29. Fletcher M (1996) Bacterial attachment in aquatic environments: a diversity of surfaces and adhesion strategies. In M Fletcher, ed, Bacterial Adhesion: Mo-lecular and Ecological Diversity. Wiley-Liss, New York, pp 1-24Google Scholar
  30. Fullner KJ, Lara JC, Nester EW (1996) Pilus assembly by Agrobacterium T-DNA transfer genes. Science 273: 1107-1109PubMedCrossRefGoogle Scholar
  31. Garfinkel DJ, Nester EW (1980) Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism. J Bacteriol 144: 732-743PubMedGoogle Scholar
  32. Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, Qurollo B, Goldman BS, Cao Y, Askenazi M, Halling H, Mullin L, Houmiel K, Gordon J, Vaudin M, Iartchouk O, Epp A, Liu F, Wollam C, Allinger M, Doughty D, Scott C, Lappas C, Markelz B, Flanagan C, Crowell C, Gurson J, Lomo C, Sear C, Strub G, Cielo C, Slater S (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294: 2323-2328PubMedCrossRefGoogle Scholar
  33. Guilhabert MR, Kirkpatrick BC (2005) Identification of Xylella fastidiosa anti-virulence genes: hemagglutinin adhesins contribute a biofilm maturation to X. fastidios and colonization and attenuate virulence. Mol Plant Microbe Interact 18: 856-868PubMedCrossRefGoogle Scholar
  34. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2: 95-108PubMedCrossRefGoogle Scholar
  35. Hinsa SM, Espinosa-Urgel M, Ramos JL, O’Toole GA (2003) Transition from re-versible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted pro-tein. Mol Microbiol 49: 905-918PubMedCrossRefGoogle Scholar
  36. Hirsch AM, Lum MR, Downie JA (2001) What makes the rhizobia-legume sym-biosis so special? Plant Physiol 127: 1484-1492PubMedCrossRefGoogle Scholar
  37. Holford ICR (1997) Soil phosphorous: its measurement and its uptake by plants. Aus J Biol Res 35: 227-239Google Scholar
  38. Hooykaas PJ, Klapwijk PM, Nuti MP, Schilperoort RA, Rorsch A (1977) Transfer of the Agrobacterium tumefaciens Ti plasmid to avirulent agrobacteria and to Rhizobium ex planta. J Gen Microbiol 98: 477-484Google Scholar
  39. Hwang HH, Gelvin SB (2004) Plant proteins that interact with VirB2, the Agro-bacterium tumefaciens pilin protein, mediate plant transformation. Plant Cell 16: 3148-3167PubMedCrossRefGoogle Scholar
  40. Hynes MF, Simon R, Puhler A (1985) The development of plasmid-free strains of Agrobacterium tumefaciens by using incompatibility with a Rhizobium meliloti plasmid to eliminate pAtC58. Plasmid 13: 99-105PubMedCrossRefGoogle Scholar
  41. Jenal U (2004) Cyclic di-guanosine-monophosphate comes of age: a novel secon-dary messenger involved in modulating cell surface structures in bacteria? Curr Opin Microbiol 7: 185-191PubMedCrossRefGoogle Scholar
  42. Judd PK, Kumar RB, Das A (2005) Spatial location and requirements for the as-sembly of the Agrobacterium tumefaciens type IV secretion apparatus. Proc Natal Acad Sci USA 102: 11498-11503CrossRefGoogle Scholar
  43. Justice SS, Hung C, Theriot JA, Fletcher DA, Anderson GG, Footer MJ, Hultgren SJ (2004) Differentiation and developmental pathways of uropathogenic Es-cherichia coli in urinary tract pathogenesis. Proc Natl Acad Sci USA 101: 1333-1338PubMedCrossRefGoogle Scholar
  44. Kado CI (1992) Plant pathogenic bacteria. In A. I. Balows, H. G. Truper, M. Dworkin, W. Harder, K-H Schleifer, eds, The Prokaryotes, 2 ed, vol 1. Springer-Verlag, New YorkGoogle Scholar
  45. Kawagishi I, Muller V, Williams AW, Irikura VM, Macnab RM (1992) Subdivi-sion of flagellar region III of the Escherichia coli and Salmonella typhi-murium chromosomes and identification of two additional flagellar genes. J Gen Microbiol 138: 1051-1065PubMedGoogle Scholar
  46. Kelly BA, Kado CI (2002) Agrobacterium-mediated T-DNA transfer and integra-tion into the chromosome of Streptomyces lividans. Mol Plant Pathol 3: 125-134CrossRefGoogle Scholar
  47. Kim H, Farrand SK (1998) Opine catabolic loci from Agrobacterium plasmids confer chemotaxis to their cognate substrates. Mol Plant Microbe Interact 11: 131-143PubMedCrossRefGoogle Scholar
  48. Knutton S, Rosenshine I, Pallen MJ, Nisan I, Neves BC, Bain C, Wolff C, Dougan G, Frankel G (1998) A novel EspA-associated surface organelle of enteropa-thogenic Escherichia coli involved in protein translocation into epithelial cells. Embo J 17: 2166-2176PubMedCrossRefGoogle Scholar
  49. Korner H, Sofia HJ, Zumft WG (2003) Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by con-trolling alternative gene programs. FEMS Microbiol Rev 27: 559-592PubMedCrossRefGoogle Scholar
  50. Kunik T, Tzfira T, Kapulnik Y, Gafni Y, Dingwall C, Citovsky V (2001) Genetic transformation of HeLa cells by Agrobacterium. Proc Natl Acad Sci USA 98: 1871-1876PubMedCrossRefGoogle Scholar
  51. Lacroix B, Tzfira T, Vainstein A, Citovsky V (2006) A case of promiscuity: Agrobacterium’s endless hunt for new partners. Trends Genet 22: 29-37PubMedCrossRefGoogle Scholar
  52. Lai EM, Chesnokova O, Banta LM, Kado CI (2000) Genetic and environmental factors affecting T-pilin export and T-pilus biogenesis in relation to flagella-tion of Agrobacterium tumefaciens. J Bacteriol 182: 3705-3716PubMedCrossRefGoogle Scholar
  53. Lai EM, Eisenbrandt R, Kalkum M, Lanka E, Kado CI (2002) Biogenesis of T pili in Agrobacterium tumefaciens requires precise VirB2 propilin cleavage and cyclization. J Bacteriol 184: 327-330PubMedCrossRefGoogle Scholar
  54. Langaee TY, Gagnon L, Huletsky A (2000) Inactivation of the ampD gene in Pseudomonas aeruginosa leads to moderate-basal-level and hyperinducible AmpC beta-lactamase expression. Antimicrob Agents Chemother 44: 583-589PubMedCrossRefGoogle Scholar
  55. Laus MC, Logman TJ, Lamers GE, Van Brussel AA, Carlson RW, Kijne JW (2006) A novel polar surface polysaccharide from Rhizobium leguminosarum binds host plant lectin. Mol Microbiol 59: 1704-1713PubMedCrossRefGoogle Scholar
  56. Lazazzera BA, Beinert H, Khoroshilova N, Kennedy MC, Kiley PJ (1996) DNA binding and dimerization of the Fe-S-containing FNR protein from Es-cherichia coli are regulated by oxygen. J Biol Chem 271: 2762-2768PubMedCrossRefGoogle Scholar
  57. Lippincott BB, Lippincott JA (1969) Bacterial attachment to a specific wound site as an essential stage in tumor initiation by Agrobacterium tumefaciens. J Bac-teriol 97: 620-628Google Scholar
  58. Lugtenberg BJJ, Chin-A-Woeng TF, Bloemberg GV (2002) Microbe-plant inter-actions: principles and mechanisms. Antonie Van Leeuwenhoek 81: 373-383PubMedCrossRefGoogle Scholar
  59. Marshall KC, Stout R, Mitchell R (1971) Mechanisms of the initial events in the sorption of marine bacteria to surfaces. J Gen Microbiol 68: 337-348Google Scholar
  60. Matthysse AG (1983) Role of bacterial cellulose fibrils in Agrobacterium tumefa-ciens infection. J Bacteriol 154: 906-915PubMedGoogle Scholar
  61. Matthysse AG (1987) Characterization of nonattaching mutants of Agrobacterium tumefaciens. J Bacteriol 169: 313-323PubMedGoogle Scholar
  62. Matthysse AG (1994) Conditioned medium promotes the attachment of Agrobac-terium tumefaciens strain NT1 to carrot cells. Protoplasma 183: 131-136CrossRefGoogle Scholar
  63. Matthysse AG, Holmes KV, Gurlitz RHG (1981) Elaboration of cellulose fibrils by Agrobacterium tumefaciens during attachment to carrot cells. J Bacteriol 145: 583-595PubMedGoogle Scholar
  64. Matthysse AG, Kijne JW (1998) Attachment of Rhizobiaceae to plant cells. In HP Spaink, A Kondorosi, PJJ Hooykaas, eds, The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic Publishers, Dordrecht/Boston/London, pp 235-249Google Scholar
  65. Matthysse AG, Marry M, Krall L, Kaye M, Ramey BE, Fuqua C, White AR (2005) The effect of cellulose overproduction on binding and biofilm forma-tion on roots by Agrobacterium tumefaciens. Mol Plant Microbe Interact 18: 1002-1010PubMedCrossRefGoogle Scholar
  66. Matthysse AG, McMahan S (1998) Root colonization by Agrobacterium tumefa-ciens is reduced in cel, attB, attD, and attR mutants. Appl Environ Microbiol 64: 2341-2345PubMedGoogle Scholar
  67. Matthysse AG, McMahan S (2001) The effect of the Agrobacterium tumefaciens attR mutation on attachment and root colonization differs between legumes and other dicots. Appl Environ Microbiol 67: 1070-1075PubMedCrossRefGoogle Scholar
  68. Matthysse AG, Thomas DL, White AR (1995a) Mechanism of cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 177: 1076-1081PubMedGoogle Scholar
  69. Matthysse AG, White S, Lightfoot R (1995b) Genes required for cellulose synthe-sis in Agrobacterium tumefaciens. J Bacteriol 177: 1069-1075PubMedGoogle Scholar
  70. Matthysse AG, Yarnall H, Boles SB, McMahan S (2000) A region of the Agro-bacterium tumefaciens chromosome containing genes required for virulence and attachment to host cells. Biochim Biophys Acta 1490: 208-212PubMedGoogle Scholar
  71. Matthysse AG, Yarnall HA, Young N (1996) Requirement for genes with homol-ogy to ABC transport systems for attachment and virulence of Agrobacterium tumefaciens. J Bacteriol 178: 5302-5308PubMedGoogle Scholar
  72. Mills AL, Powelson DK (1996) Bacterial interactions with surfaces in soils. In M Fletcher, ed, Bacterial Adhesion: Molecular and Ecological Diversity. Wiley-Liss, New York, pp 25-57Google Scholar
  73. Minnemeyer SL, Lightfoot R, Matthysse AG (1991) A semiquantitative bioassay for relative virulence of Agrobacterium tumefaciens strains on Bryophyllum daigremontiana. J Bacteriol 173: 7723-7724PubMedGoogle Scholar
  74. Monds RD, Silby MW, Mahanty HK (2001) Expression of the Pho regulon nega-tively regulates biofilm formation by Pseudomonas aureofaciens PA147-2. Mol Microbiol 42: 415-426PubMedCrossRefGoogle Scholar
  75. Morris CE, Monier JM (2003) The ecological significance of biofilm formation by plant-associated bacteria. Annu Rev Phytopathol 41: 429-453PubMedCrossRefGoogle Scholar
  76. Nair GR, Liu Z, Binns AN (2003) Re-examining the role of the accessory plasmid pAtC58 in the virulence of Agrobacterium tumefaciens strain C58. Plant Physiol 133: 989-999PubMedCrossRefGoogle Scholar
  77. Noel KD, Duelli DM (2000) Rhizobium lipopolysacchride and its role in symbio-sis. In EW Triplett, ed, Prokaryotic Nitrogen Fixation: A Model System for the Analysis of a Biological Process. Horizon Scientific Press,, Norfolk, UK, pp 415-431Google Scholar
  78. Nougayrede JP, Fernandes PJ, Donnenberg MS (2003) Adhesion of enteropatho-genic Escherichia coli to host cells. Cell Microbiol 5: 359-372PubMedCrossRefGoogle Scholar
  79. Ohnishi K, Ohto Y, Aizawa S-I, Macnab RM, Iino T (1994) FlgD is a scaffolding protein needed for flagellar hook assembly in Salmonella typhimurium. J Bac-teriol 176: 2272-2281Google Scholar
  80. O’Toole GA, Pratt LA, Watnick PI, Newman DK, Weaver VB, Kolter R (1999) Genetic approaches to study of biofilms. Methods Enzymol 310: 91-109PubMedCrossRefGoogle Scholar
  81. Parsek MR, Fuqua C (2004) Biofilms 2003: emerging themes and challenges in studies of surface-associated microbial life. J Bacteriol 186: 4427-4440PubMedCrossRefGoogle Scholar
  82. Parsek MR, Singh PK (2003) Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 57: 677-701PubMedCrossRefGoogle Scholar
  83. Paul R, Weiser S, Amiot NC, Chan C, Schirmer T, Giese B, Jenal U (2004) Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 18: 715-727PubMedCrossRefGoogle Scholar
  84. Pizarro-Cerda J, Cossart P (2006) Bacterial adhesion and entry into host cells. Cell 124: 715-727PubMedCrossRefGoogle Scholar
  85. Pueppke SG, Hawes MC (1985) Understanding the binding of bacteria to plant surfaces. Trends Biotechnol 3: 310-313CrossRefGoogle Scholar
  86. Puvanesarajah V, Schell FM, Stacey G, Douglas CJ, Nester EW (1985) Role for 2-linked-beta-D-glucan in the virulence of Agrobacterium tumefaciens. J Bac-teriol 164: 102-106Google Scholar
  87. Ramey BE (2004) Biofilm formation by Agrobacterium tumefaciens and its role in plant interactions. Doctoral dissertation, Indiana University, BloomingtonGoogle Scholar
  88. Ramey BE, Koutsoudis M, von Bodman SB, Fuqua C (2004a) Biofilm formation in plant-microbe associations. Curr Opin Microbiol 7: 602-609PubMedCrossRefGoogle Scholar
  89. Ramey BE, Matthysse AG, Fuqua C (2004b) The FNR-type transcriptional regula-tor SinR controls maturation of Agrobacterium tumefaciens biofilms. Mol Microbiol 52: 1495-1511PubMedCrossRefGoogle Scholar
  90. Reed JW, Glazebrook J, Walker GC (1991) The exoR gene of Rhizobium meliloti affects RNA levels of other exo genes but lacks homology to known transcrip-tional regulators. J Bacteriol 173: 3789-3794PubMedGoogle Scholar
  91. Reuhs BL, Kim JS, Matthysse AG (1997) Attachment of Agrobacterium tumefa-ciens to carrot cells and Arabidopsis wound sites is correlated with the pres-ence of a cell-associated, acidic polysaccharide. J Bacteriol 179: 5372-5379PubMedGoogle Scholar
  92. Rojas CM, Ham JH, Deng WL, Doyle JJ, Collmer A (2002) HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC16 on Nicotiana clevelandii seedlings. Proc Natl Acad Sci USA 99: 13142-13147PubMedCrossRefGoogle Scholar
  93. Romling U (2002) Molecular biology of cellulose production in bacteria. Res Mi-crobiol 153: 205-212Google Scholar
  94. Rosenberg C, Huguet T (1984) The pAtC58 plasmid of Agrobacterium tumefa-ciens is not essential for tumour induction. Mol Gen Genet 196: 533-536CrossRefGoogle Scholar
  95. Russo DM, Williams A, Edwards A, Posadas DM, Finnie C, Dankert M, Downie JA, Zorreguieta A (2006) Proteins exported via the PrsD-PrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum. J Bacteriol 188: 4474-4486PubMedCrossRefGoogle Scholar
  96. Shaw CH, Loake GJ, Brown AP, Garrett CS, Deakin W, Alton G, Hall M, Jones SA, Oleary M, Primavesi L (1991) Isolation and characterization of behav-ioral mutants and genes of Agrobacterium tumefaciens. J Gen Microbiol 137: 1939-1953Google Scholar
  97. Smit G, Logman TJJ, Boerrigter METI, Kijne JW, Lugtenberg BJJ (1989) Purifi-cation and partial characterization of the Rhizobium leguminosarum biovar viciae Ca2+-dependent adhesin, which mediates the first step in attachment of cells of the family Rhizobiaceae to plant root hair tips. J Bacteriol 171: 4054-4062PubMedGoogle Scholar
  98. Swart S, Smit G, Lugtenberg BJJ, Kijne JW (1993) Restoration of attachment, virulence and nodulation of Agrobacterium tumefaciens chvB mutants by rhi-cadhesin. Mol Microbiol 10: 597-605PubMedCrossRefGoogle Scholar
  99. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132: 44-51PubMedCrossRefGoogle Scholar
  100. Wanner BL (1995) Signal transduction and cross regulation in the Escherichia coli phosphate regulaon by PhoR, CreC, and acetyl phosphate. In JA Hoch, TJ Silhavy, eds, Two-Component Signal Transduction. ASM Press, Washington D.C., pp 203-221Google Scholar
  101. Whatley MH, Bodwin JS, Lippincott BB, Lippincott JA (1976) Role of Agrobac-terium cell envelope lipopolysaccharide in infection site attachment. Infect Immun 13: 1080-1083PubMedGoogle Scholar
  102. Winans SC (1990) Transcriptional induction of an Agrobacterium regulatory gene at tandem promoters by plant-released phenolic compounds, phosphate starva-tion, and acidic growth media. J Bacteriol 172: 2433-2438PubMedGoogle Scholar
  103. Winans SC (1992) Two-way chemical signalling in Agrobacterium-plant interac-tions. Microbiol Rev 56: 12-31PubMedGoogle Scholar
  104. Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, Okura VK, Zhou Y, Chen L, Wood GE, Almeida Jr. NF, Woo L, Chen Y, Paulsen IT, Eisen JA, Karp PD, Bovee Sr. D, Chapman P, Clendenning J, Deatherage G, Gillet W, Grant C, Kutyavin T, Levy R, Li MJ, McClelland E, Palmieri P, Raymond C, Rouse R, Saenphimmachak C, Wu Z, Romero P, Gordon D, Zhang S, Yoo H, Tao Y, Biddle P, Jung M, Krespan W, Perry M, Gordon-Kamm B, Liao L, Kim S, Hendrick C, Zhao ZY, Dolan M, Chumley F, Tingey SV, Tomb JF, Gordon MP, Olson MV, Nester EW (2001) The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294: 2317-2323PubMedCrossRefGoogle Scholar
  105. Yao SY, Luo L, Har KJ, Becker A, Ruberg S, Yu GQ, Zhu JB, Cheng HP (2004) Sinorhizobium meliloti ExoR and ExoS proteins regulate both succinoglycan and flagellum production. J Bacteriol 186: 6042-6049PubMedCrossRefGoogle Scholar
  106. Yuan ZC, Zaheer R, Finan TM (2006) Regulation and properties of PstSCAB, a high-affinity, high-velocity phosphate transport system of Sinorhizobium meliloti. J Bacteriol 188: 1089-1102PubMedCrossRefGoogle Scholar
  107. Zhang HB, Wang LH, Zhang LH (2002) Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 99: 4638-4643PubMedCrossRefGoogle Scholar
  108. Zhu Y, Nam J, Humara JM, Mysore KS, Lee LY, Cao H, Valentine L, Li J, Kaiser AD, Kopecky AL, Hwang HH, Bhattacharjee S, Rao PK, Tzfira T, Rajagopal J, Yi H, Veena, Yadav BS, Crane YM, Lin K, Larcher Y, Gelvin MJ, Knue M, Ramos C, Zhao X, Davis SJ, Kim SI, Ranjith-Kumar CT, Choi YJ, Hallan VK, Chattopadhyay S, Sui X, Ziemienowicz A, Matthysse AG, Citovsky V, Hohn B, Gelvin SB (2003) Identification of Arabidopsis rat mutants. Plant Physiol 132: 494-505PubMedCrossRefGoogle Scholar
  109. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agro-bacterium-mediated transformation. Cell 125: 749-760PubMedCrossRefGoogle Scholar
  110. Zorreguieta A, Geremia RA, Cavaignac S, Cangelosi GA, Nester EW, Ugalde RA (1988) Identification of the product of an Agrobacterium tumefaciens chro-mosomal virulence gene. Mol Plant Microbe Interact 1: 121-127PubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Clay Fuqua
    • 1
  1. 1.Department of BiologyIndiana UniversityBloomingtonUSA

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