Agrobacterium—Taxonomy of Plant-Pathogenic Rhizobium Species

  • John M. Young

Traditionally, Agrobacterium spp. have been regarded as unique, predominantly soil-inhabiting, oncogenic plant pathogenic bacteria, thus justifying their inclusion in a single genus that encompassed species allocated according to the nature of symptoms produced. Tumorigenic strains have been included in A. tumefaciens and rhizogenic strains in A. rhizogenes; each species having a wide host plant range. Other species (A. larrymoorei, A. rubi and A. vitis and) have relatively restricted host ranges. Non-pathogenic, exclusively soil-inhabiting strains have been allocated to A. radiobacter. From its inception, the authenticity of Agrobacterium was questioned because of its possible synonymy with Rhizobium, a genus until recently considered to be represented only by bacteria forming nodulating, nitrogen-fixing, symbiotic relationships with legume plants. Accumulated phenotypic and molecular evidence now shows that these two genera can be circumscribed as single taxon. Furthermore, Agrobacterium pathogenicity and Rhizobium nodulation characters are plasmid-borne and interchangeable between individual species and between members of the two genera. This evidence militates against stable nomenclature based on pathogenic characters for the genus, Agrobacterium, or for its species. According to modern approaches to classification of the two genera, all Agrobacterium spp. should be allocated to the genus Rhizobium, natural species being distinguished on the basis of phenotypic and genomic data. Differences in pathogenicity can be accommodated by nomenclature referring to the presence or absence of different oncogenic plasmids. In this chapter, the classification and nomenclature of Agrobacterium is chronicled in relation to the evolution of bacterial taxonomy as a discipline intended to inform natural relationships. The ‘agrobacteria’ are considered in the context of the diversity of related soil-inhabiting ‘rhizobia’ of which they form a sub-population.


Hairy Root Crown Gall Plant Pathogenic Bacterium Rhizobium Species Agrobacterium Radiobacter 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

12 References

  1. Abe M, Kawamura R, Higashi S, Mori S, Shibata M, Uchiumi T (1998) Transfer of the symbiotic plasmid from Rhizobium leguminosarum biovar trifolii to Agrobacterium tumefaciens. J Gen Appl Microbiol 44: 65-74PubMedCrossRefGoogle Scholar
  2. Allen EK, Allen ON (1950) Biochemical and symbiotic properties of the rhizobia. Bacteriol Rev 14: 273-330PubMedGoogle Scholar
  3. Allen ON, Holding AJ (1974) Genus II. Agrobacterium Conn. 1942. 359. In RE Buchanan, NE Gibbons, eds, Bergey’s Manual of Determinative Bacteriology, 8th ed. The Williams and Wilkins Co., Baltimore, pp 264-267Google Scholar
  4. Anderson AR, Moore LW (1979) Host specificity of the genus Agrobacterium. Phytopathol 69: 320-323CrossRefGoogle Scholar
  5. Arahal DR, Macián MC, Garay E, Pujalte MJ (2005) Thalassobius mediterraneus gen. nov., sp. nov., and reclassification of Ruegeria gelatinovorans as Thalas-sobius gelatinovorus comb. nov. Int J Syst Evol Microbiol 55: 2371-2376PubMedCrossRefGoogle Scholar
  6. Beijerinck MW, van Delden A (1902) Ueber die Assimilation des freien Stickstoffs durch Bakterien. Zentralbl Bakteriol Parasitenk Infektionskr Hyg Abt II 9: 3-43Google Scholar
  7. Bergey DH, Breed RS, Hammer BW, Huntoon FM, Murray EGD, Harrison FC (1934) Bergey’s Manual of Determinative Bacteriology, 4th ed. The Williams & Wilkins Co., BaltimoreGoogle Scholar
  8. Bergey DH, Breed RS, Murray EGD, Hitchens AP (1939) Bergey’s Manual of Determinative Bacteriology, 5th ed. The Williams & Wilkins Co., BaltimoreGoogle Scholar
  9. Bonnier C (1953) Classification et spécificité de l’hôte, dans le genre Rhizobium. Atti VI Cong Int Microbiol 6: 325-327Google Scholar
  10. Bouzar H (1994) Request for a judicial opinion concerning the type species of Agrobacterium. Int J Syst Bacteriol 44: 373-374CrossRefGoogle Scholar
  11. Bouzar H, Chilton WS, Nesme X, Dessaux Y, Vaudequin V, Petit A, Jones JB, Hodge NC (1995) A new Agrobacterium strain isolated from aerial tumors on Ficus benjamina L. Appl Environ Microbiol 61: 65-73PubMedGoogle Scholar
  12. Bouzar H, Jones JB (2001) Agrobacterium larrymoorei sp. nov., a pathogen iso-lated from aerial tumours of Ficus benjamina. Int J Syst Evol Microbiol 51: 1023-1026PubMedGoogle Scholar
  13. Bradbury JF (1986) Guide to Plant Pathogenic Bacteria. CAB International Myco-logical Institute, LondonGoogle Scholar
  14. Brom S, Martínez E, Palacios R (1988) Narrow- and broad-host-range symbiotic plasmids of Rhizobium spp. strains that nodulate Phaseolus vulgaris. Appl Environ Microbiol 54: 1280-1283PubMedGoogle Scholar
  15. Broughton WJ (2003) Roses by other names: taxonomy of the Rhizobiaceae. J Bacteriol 185: 2975-2979PubMedCrossRefGoogle Scholar
  16. Brenner DJ, Staley JT, Krieg NR (2005) Classification of prokaryotic organisms and the concept of bacterial speciation. In DJ Brenner, NR Krieg, JT Staley, eds, Bergey’s Manual of Systematic Bacteriology. The Proteobacteria, Vol. 2A, 2nd ed. Springer-Verlag, New York, USA, pp 27-32Google Scholar
  17. Burkholder WH, Starr MP (1948) The generic and specific characters of phytopa-thogenic species of Pseudomonas and Xanthomonas. Phytopathol 38: 494-502Google Scholar
  18. Burr TJ, Katz BH, Bishop AL (1987) Populations of Agrobacterium in vineyard and non vineyard soils and grape roots in vineyards and nurseries. Plant Disease 71: 617-620CrossRefGoogle Scholar
  19. Chen LS, Figueredo A, Pedrosa FO, Hungria M (2000) Genetic characterization of soybean rhizobia in Paraguay. Appl Environ Microbiol 66: 5099-5103PubMedCrossRefGoogle Scholar
  20. Colwell RR (1970a) Polyphasic taxonomy of bacteria. In H Iizuka, T Hasegawa, eds, Culture Collections of Microorganisms. University Park Press, Baltimore, pp 421-426Google Scholar
  21. Colwell RR (1970b) Polyphasic taxonomy of the genus vibrio: numerical taxon-omy of Vibrio cholerae, Vibrio parahaemolyticus, and related Vibrio species. J Bacteriol 104: 410-433PubMedGoogle Scholar
  22. Conn HJ (1938) Taxonomic relationships of certain non-sporeforming rods in soil. J Bacteriol 36: 320-321Google Scholar
  23. Conn HJ (1942) Validity of the genus Alcaligenes. J Bacteriol 44: 353-360PubMedGoogle Scholar
  24. De Lajudie P, Laurent-Fulele E, Willems A, Torck U, Coopman R, Collins MD, Kersters K, Dreyfus B, Gillis M (1998a) Description of Allorhizobium undi-cola gen. nov., sp. nov. for nitrogen-fixing bacteria efficiently nodulating Neptunia natans in Senegal. Int J Syst Bacteriol 48: 1277-1290PubMedCrossRefGoogle Scholar
  25. De Lajudie P, Willems A, Nick G, Moreira F, Molouba F, Hoste B, Torck U, Neyra M, Collins MD, Lindström K, Dreyfus B, Gillis M (1998b) Characteri-zation of tropical tree rhizobia and description of Mesorhizobium plurifarium sp. nov. Int J Syst Bacteriol 48 Pt 2: 369-382CrossRefGoogle Scholar
  26. De Lajudie P, Willems A, Pot B, Dewettinck D, Maestrojuan G, Neyra M, Collins MD, Dreyfus B, Kersters K, Gillis M (1994) Polyphasic taxonomy of rhizo-bia: emendation of the genus Sinorhizobium and description of Sinorhizobium meliloti comb. nov., Sinorhizobium saheli sp. nov. and Sinorhizobium teranga sp. nov. Int J Syst Bacteriol 44: 715-733CrossRefGoogle Scholar
  27. De Ley J (1968) DNA base composition and hybridization in the taxonomy of the phytopathogenic bacteria. Annu Rev Phytopathol 6: 63-90CrossRefGoogle Scholar
  28. De Ley J (1972) Agrobacterium: intrageneric relationships and evolution. In HP Maas Geesteranus, ed, Plant Pathogenic Bacteria 1971, Proc 3rd Int Conf Pl Path Bact. Centre for Agricultural Publishing and Documentation, Wagenin-gen, pp 251-259Google Scholar
  29. De Ley J (1974) Phylogeny of the prokaryotes. Taxon 23: 291-300CrossRefGoogle Scholar
  30. De Ley J, Tijtgat R, De Smedt J, Michiels M (1973) Thermal stability of DNA: DNA hybrids within the genus Agrobacterium. J Gen Microbiol 78: 241-252Google Scholar
  31. Duggar BM (1909) Fungous diseases of plants. Ginn & Co., BostonGoogle Scholar
  32. Dye DW, Bradbury JF, Goto M, Hayward AC, Lelliott RA, Schroth MN (1980) International standards for naming pathovars of phytopathogenic bacteria and list of pathovar names and pathotype strains. Rev Pl Pathol 59: 153-168Google Scholar
  33. Eardly BD, Nour SM, van Berkum P, Selander RK (2005) Rhizobial 16S rRNA and dnaK genes: mosaicism and the uncertain phylogenetic placement of Rhizobium galegae. Appl Environ Microbiol 71: 1328-1335PubMedCrossRefGoogle Scholar
  34. Euzéby JP (1997-2006) List of bacterial names with standing in nomenclature: a folder available on the internet (updated: March, 2006; revised URL: Int J Syst Evol Microbiol 47: 590-592
  35. Farrand SK, Van Berkum PB, Oger P (2003) Agrobacterium is a definable genus of the family Rhizobiaceae. Int J Syst Evol Microbiol 53: 1681-1687PubMedCrossRefGoogle Scholar
  36. Gao J, Terefework Z, Chen W-X, Lindstrom K (2001) Genetic diversity of rhizo-bia isolated from Astragalus adsurgens growing in different geographical regions of China. J Biotechnol 91: 155-168PubMedCrossRefGoogle Scholar
  37. Gaunt MW, Turner SL, Rigottier-Gois L, Lloyd-Macgilp SA, Young JPW (2001) Phylogenies of atpD and recA support the small subunit rRNA-based classifi-cation of rhizobia. Int J Syst Evol Microbiol 51: 2037-2048PubMedGoogle Scholar
  38. Genetello C, Van Larebeke N, Holsters M, De Picker A, Van Montagu M, Schell J (1977) Ti plasmids of Agrobacterium as conjugative plasmids. Nature 265: 561-563PubMedCrossRefGoogle Scholar
  39. George ML, Young JPW, Borthakur D (1994) Genetic characterization of Rhizo-bium sp. strain TAL1145 that nodulates tree legumes. FEMS Microbiol Lett 40: 208-215Google Scholar
  40. Ghosh W, Roy P (2006) Mesorhizobium thiogangeticum sp. nov., a novel sulfur-oxidizing chemolithoautotroph from rhizosphere soil of an Indian tropical leguminous plant. Int J Syst Evol Microbiol 56: 91-97PubMedCrossRefGoogle Scholar
  41. Gillis M, Vandamme P, De Vos P, Swings J, Kersters K (2005) Polyphasic taxon-omy. In DJ Brenner, NR Krieg, JT Staley, eds, Bergey’s Manual of System-atic Bacteriology. The Proteobacteria, Vol. 2A, 2nd ed. Springer-Verlag, New York, USA, pp 43-48Google Scholar
  42. Goodfellow M, O’Donnell AG (1993) Roots of bacterial systematics. In M Goodfellow, AG O’Donnell, eds, Handbook of New Bacterial Systematics. Academic Press, London, San Diego, pp 3-54Google Scholar
  43. Graham PH (1964) The application of computer techniques to the taxonomy of the root nodule bacteria of legumes. J Gen Microbiol 35: 511-517Google Scholar
  44. Graham PH (1976) Identification and classification of root nodule bacteria. In Symbiotic Nitrogen Fixation in Plants. International Biological Programme 7. University Press, Cambridge, pp 99-112Google Scholar
  45. Han S-Z, Wang E-T, Chen W-X (2005) Diverse bacteria isolated from root nod-ules of Phaseolus vulgaris and species within the genera Campylotropis and Cassia grown in China. Syst Appl Microbiol 28: 265-276PubMedCrossRefGoogle Scholar
  46. Heberlein GT, De Ley J, Tijtgat R (1967) Deoxyribonucleic acid homology and taxonomy of Agrobacterium, Rhizobium, and Chromobacterium. J Bacteriol 94: 116-124PubMedGoogle Scholar
  47. Hildebrand EM (1940) Cane gall of brambles caused by Phytomonas rubi n. sp. J Agr Res 61: 685-696Google Scholar
  48. Holmes B (1988) The taxonomy of Agrobacterium, Acta Hort 225: 47-52Google Scholar
  49. Holmes B, Roberts P (1981) The classification, identification and nomenclature of agrobacteria. J Appl Bacteriol 50: 443-467Google Scholar
  50. Hooykaas PJ, Klapwijk PM, Nuti MP, Schilperoort RA, Rörsch A (1977) Transfer of the Agrobacterium tumefaciens Ti plasmid to avirulent agrobacteria and to Rhizobium ex planta. J Gen Microbiol 98: 477-484Google Scholar
  51. Hungria M, Campio RJ, Chueire LMO, Grange L, Megias M (2001) Symbiotic ef-fectiveness of fast-growing rhizobial strains isolated from soybean nodules in Brazil. Biol Fert Soils 33: 387-394CrossRefGoogle Scholar
  52. Jarvis BDW, Sivakumaran SW, Tighe SW, Gillis M (1966) Identification of Agrobacterium and Rhizobium species based on cellular fatty acid composi-tion. Pl Soil 184: 143-158CrossRefGoogle Scholar
  53. Jordan DC (1984) Genus1. Rhizobium Frank 1889, 339AL. In NR Krieg, JG Holt, eds, Bergey’s Manual of Systematic Bacteriology, 7th ed. The Williams & Wilkins Co., Baltimore, pp 235-242Google Scholar
  54. Jordan DC, Allen ON (1974) Family III. Rhizobiaceae Conn 1938, 321, In RE Buchanan, NE Gibbons, eds, Bergey’s Manual of Determinative Bacteriology, 8th ed. The Williams & Wilkins Co., Baltimore, pp 261-262Google Scholar
  55. Jumas-Bilak E, Michaux-Charachon S, Bourg G, Ramuz M, Allardet-Servent A (1998) Unconventional genomic organization in the alpha subgroup of the Proteobacteria. J Bacteriol 180: 2749-2755PubMedGoogle Scholar
  56. Keane PJ, Kerr A, New PB (1970) Crown gall of stone fruit. II. Identification and nomenclature of Agrobacterium isolates. Aus J Biol Sci 23: 585-595Google Scholar
  57. Kerr A (1969a) Crown gall of stonefruit. I. Isolation of Agrobacterium tumefa-ciens and related fruits. Aus J Biol Sci 22: 111-116Google Scholar
  58. Kerr A (1969b) Transfer of virulence between isolates of Agrobacterium. Nature 223: 1175-1176CrossRefGoogle Scholar
  59. Kerr A (1992) The genus Agrobacterium. In A Balows, HG Trüper, M Dworkin, W Harder, K-H Schleifer, eds, The Prokaryotes - a Handbook on the Biology of Bacteria, Vol. 3, 2ed ed. Springer-Verlag, Heidelberg, pp 2214-2235Google Scholar
  60. Kerr A, Panagopoulos CG (1977) Biotypes of Agrobacterium radiobacter var. tu-mefaciens and their biological control. Phytopath Z 90: 172-179CrossRefGoogle Scholar
  61. Kerr A, Young JM, Panagopoulos CG (1978) Genus II. Agrobacterium Conn 1942. In Young JM, Dye DW, Bradbury JF, Panagopoulos CG, Robbs CF, eds, A proposed nomenclature and classification for plant pathogenic bacteria. NZ J Agric Res 21: 153-177Google Scholar
  62. Kersters K, De Ley J (1975) Identification and grouping of bacteria by numerical analysis of their electrophoretic protein patterns. J Gen Microbiol 87: 333-342PubMedGoogle Scholar
  63. Kersters K, De Ley J (1984) Genus III. Agrobacterium Conn. In NR Krieg, JG Holt, eds, Bergey’s Manual of Systematic Bacteriology, Vol. 1, 8th ed. The Williams and Wilkins Co., Baltimore-London, pp 244-254Google Scholar
  64. Kersters K, De Ley J, Sneath PHA, Sackin M (1973) Numerical taxonomic analy-sis of Agrobacterium. J Gen Microbiol 78: 227-239Google Scholar
  65. Kersters K, Ludwig W, Vancanneyt M, De Vos P, Gillis P, Schleifer K-H (1996) Recent changes in the classification of pseudomonads. Syst App Microbiol 19: 465-477Google Scholar
  66. Kuykendall LD (2005) Family Rhizobiaceae Conn 1938, 321AL. In DJ Brenner, NR Krieg, JT Staley, GM Garrity, eds, Bergey’s Manual of Systematic Bacte-riology. The Proteobacteria, Vol. 2C, 2ed ed. Springer-Verlag, New York, pp 324-325Google Scholar
  67. Kuykendall LD, Young JM, Martínez-Romero E, Kerr A, Sawada H (2005) Genus Rhizobium Frank 1889, 338AL emend. In DJ Brenner, NR Krieg, JT Staley, GM Garrity, eds, Bergey’s Manual of Systematic Bacteriology. The Proteo-bacteria, Vol. 2C, 2ed ed. Springer-Verlag, New York, pp 325-340Google Scholar
  68. Kwon SW, Park JY, Kim JS, Kang JW, Cho YH, Lim CK, Parker MA, Lee GB (2005) Phylogenetic analysis of the genera Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium on the basis of 16S rRNA gene and internally transcribed spacer region sequences. Int J Syst Evol Microbiol 55: 263-270Google Scholar
  69. Lapage SP, Sneath PHA, Lessel EF, Skerman VBD, Seeliger HPR, Clark WA, (1975) International Code of Nomenclature of Bacteria - Bacteriological Code, 1996 Revision. American Society of Microbiology, Washington: 1-180Google Scholar
  70. Lapage SP, Sneath PHA, Lessel EF, Skerman VBD, Seeliger HPR, Clark WA (1992) International Code of Nomenclature of Bacteria - Bacteriological Code, 1990 Revision. American Society of Microbiology, Washington: 1-189Google Scholar
  71. Lelliott RA (1972) The genus Xanthomonas. In HP Maas Geesteranus, ed, Plant Pathogenic Bacteria 1971, Proc 3rd Int Conf Pl Path Bact. Centre for Agricul-tural Publishing and Documentation, Wageningen, pp 269-271Google Scholar
  72. Lindström K, Laguerre G, Normand P, Rassmussen U, Heulin T, De Lajudie P, Martínez-Romero E, Chen W-X (1998) Taxonomy and phylogeny of diazotrophs. In C Elmerich, A Kondorosi, WE William, eds, Biological Nitrogen Fixation for the 21st Century: Proceedings of the 11th International Congress on Nitrogen Fixation Institut Pasteur, Paris, France, 1997, July 20-25. Kluwer Academic, Dordrecht, pp 559-570.Google Scholar
  73. Lindström K, Martínez-Romero ME (2005), International Committee on Systemat-ics of Prokaryotes; Subcommittee on the taxonomy of Agrobacterium and Rhizobium. Minutes of the meeting, 26 July 2004, Toulouse, France. Int J Syst Evol Microbiol 55: 1383CrossRefGoogle Scholar
  74. Liu J, Wang ET, Chen WX (2005) Diverse rhizobia associated with woody leg-umes Wisteria sinensis, Cercis racemosa and Amorpha fruticosa grown in the temperate zone of China. Syst Appl Microbiol 28: 465-477PubMedCrossRefGoogle Scholar
  75. Ludwig W, Schleifer K-H (1999) Phylogeny of bacteria beyond the 16S rDNA standard. ASM News 65: 752-757Google Scholar
  76. Martínez-Romero E, Palacios R, Sánchez F (1987) Nitrogen-fixing nodules in-duced by Agrobacterium tumefaciens harboring Rhizobium phaseoli plasmids. J Bacteriol 169: 2828-2833Google Scholar
  77. Meyer OO (2005) Genus IV. CarbophilusGoogle Scholar
  78. Meyer, Stackebrandt and Auling, G, 1994, 182VP. In DJ Brenner, NR Krieg, JT Staley, GM Garrity, eds, Bergey’s Manual of Systematic Bacteriology. The Proteobacteria, Vol. 2C, 2nd ed. Springer-Verlag, New York, pp 346-347Google Scholar
  79. Moffett ML, Colwell RR (1968) Adansonian analysis of the Rhizobiaceae. J Gen Microbiol 51: 245-266PubMedGoogle Scholar
  80. Moore LW, Bouzar H, Burr TJ (2001) Agrobacterium. In NW Schaad, JB Jones, W Chun, eds, Laboratory Guide for Identification of Plant Pathogenic Bacte-ria. American Phytopathological Society Press, St. Paul, Minnesota, pp 17-33Google Scholar
  81. Mougel C, Thioulouse J, Perrière G, Nesme X (2002) A mathematical method for determining genome divergence and species delineation using AFLP. Int J Syst Evol Microbiol 52: 573-586PubMedGoogle Scholar
  82. Nour SM, Cleyet-Marel JC, Normand P, Fernandez MP (1995) Genomic hetero-geneity of strains nodulating chickpeas (Cicer arietinum L.) and description of Rhizobium mediterraneum sp. nov. Int J Syst Bacteriol 45: 640-648PubMedCrossRefGoogle Scholar
  83. Ophel K, Kerr A (1990) Agrobacterium vitis sp. nov. for strains of Agrobacterium biovar 3 from grapevines. Int J Syst Bacteriol 40: 236-241CrossRefGoogle Scholar
  84. Østerås M, Stanley J, Finan TM (1995) Identification of Rhizobium-specific inter-genic mosaic elements within an essential two-component regulatory system of Rhizobium species. J Bacteriol 177: 5485-5494PubMedGoogle Scholar
  85. Panagopoulos CG, Psallidas PG (1973) Characteristics of Greek Isolates of Agro-bacterium tumefaciens (E. F. Smith & Townsend) Conn. J Appl Bacteriol 36: 233-240Google Scholar
  86. Panagopoulos CG, Psallidas PG, Alivizatos AS (1978) Studies on biotype 3 of Agrobacterium radiobacter var. tumefaciens. In Station de Pathologie Végétale et Phytobactériologie, ed., Plant Pathogenic Bacteria Proc 4th Inter-nat Conf Plant Path Bact, Angers, France, pp 221-228Google Scholar
  87. Peix A, Rivas R, Trujillo ME, Vancanneyt M, Velázquez E, Willems A (2005) Reclassification of Agrobacterium ferrugineum LMG 128 as Hoeflea marina gen. nov., sp. nov. Int J Syst Evol Microbiol 55: 1163-1166PubMedCrossRefGoogle Scholar
  88. Popoff MY, Kersters K, Kiredjian M, Miras I, Coynault C (1984) Position tax-onomique de souches de Agrobacterium d’origine hospitalière. Ann Microbiol 135A: 427-442Google Scholar
  89. Pribram E (1933) Klassification der Shizomyceten, F. Deuticke, LeipzigGoogle Scholar
  90. Riker AJ, Banfield WM, Wright WH, Keitt GW, Sagen HE (1930) Studies on in-fectious hairy root of nursery trees of apples. J Agr Res 41: 507-540Google Scholar
  91. Rome S, Fernandez MP, Brunel B, Normand P, Cleyet-Marel JC (1996) Si-norhizobium medicae sp. nov., isolated from annual Medicago spp. Int J Syst Bacteriol 46: 972-980PubMedCrossRefGoogle Scholar
  92. Rüger HJ, Höfle MG (1992) Marine star-shaped-aggregate-forming bacteria: Agrobacterium atlanticum sp. nov.; Agrobacterium meteori sp. nov.; Agro-bacterium ferrugineum sp. nov., nom. rev.; Agrobacterium gelatinovorum sp. nov., nom. rev.; and Agrobacterium stellulatum sp. nov., nom. rev. Int J Syst Bacteriol 42: 133-143PubMedCrossRefGoogle Scholar
  93. Sadowsky MJ, Graham PH (1998) Soil biology of the Rhizobiaceae. In HP Spaink, A Kondorosi, PJJ Hooykaas, eds, The Rhizobiaceae: Molecular Biol-ogy of Model Plant-Associated Bacteria. Kluwer Academic Publications, Dordrecht, pp 155-172Google Scholar
  94. Salmassi TM, Venkateswaren K, Satomi M, Newman DK, Nealson KH, Hering JG (2001) Isolation and characterization of Agrobacterium albertimagni, strain AOL15, sp. nov., a new arsenite oxidizing bacterium isolated from Hot Creek. Cited in EMBL Nucleotide Sequence Database: Accession AF316615Google Scholar
  95. Sawada H, Ieki H (1992a) Crown gall of kiwifruit caused by Agrobacterium tume-faciens in Japan. Plant Dis 76: 212Google Scholar
  96. Sawada H, Ieki H (1992b) Phenotypic characteristics of the genus Agrobacterium. Ann Phytopathol Soc Jpn 58: 37-45Google Scholar
  97. Sawada H, Ieki H, Oyaizu H, Matsumoto S (1993) Proposal for rejection of Agro-bacterium tumefaciens and revised descriptions for the genus Agrobacterium and for Agrobacterium radiobacter and Agrobacterium rhizogenes. Int J Syst Bacteriol 43: 694-702PubMedCrossRefGoogle Scholar
  98. Sawada H, Kuykendall LD, Young JM (2003) Changing concepts in the systemat-ics of bacterial nitrogen-fixing legume symbionts. J Gen Appl Microbiol 49: 155-179PubMedCrossRefGoogle Scholar
  99. Segovia L, Piñero D, Palacios R, Martinez-Romero E (1991) Genetic structure of a soil population of nonsymbiotic Rhizobium leguminosarum. Appl Environ Microbiol 57: 426-433PubMedGoogle Scholar
  100. Skerman VBD, McGowan V, Sneath PHA (1980) Approved lists of bacterial names. Int J Syst Bacteriol 30: 225-420CrossRefGoogle Scholar
  101. Smith EF, Townsend CO (1907) A plant tumor of bacterial origin. Science 25: 671-673PubMedCrossRefGoogle Scholar
  102. Sneath PHA (1984) Bacterial nomenclature. In NR Krieg, JG Holt, eds, Bergey’s Manual of Systematic Bacteriology. The Williams & Wilkins, Baltimore, pp 19-23Google Scholar
  103. Sneath PHA (1988) The phenetic and cladistic approaches. In DL Hawksworth, ed, Prospects in Systematics. Clarendon Press, Oxford, pp 252-273Google Scholar
  104. Sneath PHA (2005) Bacterial nomenclature. In DJ Brenner, NR Krieg, JT Staley, eds, Bergey’s Manual of Systematic Bacteriology. The Proteobacteria, Vol. 2A, 2nd. Springer-Verlag, New York, USA, pp 83-88Google Scholar
  105. Sokal RR, Sneath PHA (1963) Principles of Numerical Taxonomy. W.H. Free-man, San FranciscoGoogle Scholar
  106. Stackebrandt E, Woese CR (1984) The phylogeny of prokaryotes. Microbiol Sci 1: 117-122PubMedGoogle Scholar
  107. Stanier RY, Palleroni NJ, Doudoroff M (1966) The aerobic pseudomonads: a taxonomic study. J Gen Microbiol 43: 159-271PubMedGoogle Scholar
  108. Starr MP, Weiss JE (1943) Growth of phytopathogenic bacteria in a synthetic as-paragine medium. Phytopathol 33: 313-318Google Scholar
  109. Süle S (1978) Biotypes of Agrobacterium tumefaciens in Hungary. J Appl Bacte-riol 44: 207-213Google Scholar
  110. Tan ZY, Xu XD, Wang ET, Gao JL, Martinez-Romero E, Chen WX (1997) Phylogenetic and genetic relationships of Mesorhizobium tianshanense and related rhizobia. Int J Syst Bacteriol 47: 874-879PubMedCrossRefGoogle Scholar
  111. Tepfer D (1984) Transformation of several species of higher plants by Agrobacte-rium rhizogenes: sexual transmission of the transformed genotype and pheno-type. Cell 37: 959-967PubMedCrossRefGoogle Scholar
  112. Tighe SW, de Lajudie P, Dipietro K, Lindström K, Nick G, Jarvis BDW (2000) Analysis of cellular fatty acids and phenotypic relationships of Agrobacte-rium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium species using the Sherlock Microbial Identification System. Int J Syst Evol Microbiol 50: 787-801PubMedGoogle Scholar
  113. Uchino Y, Hamada T, Yokota A (2002) Proposal of Pseudorhodobacter ferrugi-neus gen. nov., comb. nov., for a non-photosynthetic marine bacterium, Agro-bacterium ferrugineum, related to the genus Rhodobacter. J Gen Appl Microbiol 48: 309-319PubMedCrossRefGoogle Scholar
  114. Uchino Y, Hirata A, Yokota A, Sugiyama J (1998) Reclassification of marine Agrobacterium species: proposals of Stappia stellulata gen. nov., comb. nov., Stappia aggregata sp. nov., nom. rev., Ruegeria atlantica gen. nov., comb. nov., Ruegeria gelatinovora comb. nov., Ruegeria algicola comb. nov., and Ahrensia kieliense gen. nov., sp. nov., nom. rev. J Gen Appl Microbiol 44: 201-210PubMedCrossRefGoogle Scholar
  115. Ueda K, Seki T, Kudo T, Yoshida T, Kataoka M (1999) Two distinct mechanisms cause heterogeneity of 16S rRNA. J Bacteriol 181: 78-82PubMedGoogle Scholar
  116. Van Larebeke N, Genetello C, Schell J, Schilperoort RA, Hermans AK, Van Montagu M, Hernalsteens JP (1975) Acquisition of tumour-inducing ability by non-oncogenic agrobacteria as a result of plasmid transfer. Nature 255: 742-743PubMedCrossRefGoogle Scholar
  117. Vandamme P, Pot B, Gillis M, de Vos P, Kersters K, Swings J (1996) Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 60: 407-438PubMedGoogle Scholar
  118. Velázquez E, Peix A, Zurdo-Piñeiro JL, Palomo JL, Mateos PF, Rivas R, Muñoz-Adelantado E, Toro N, García-Benavides P, Martínez-Molina E (2005) The coexistence of symbiosis and pathogenicity-determining genes in Rhizobium rhizogenes strains enable them to induce nodules and tumors or hairy roots in plants. Mol Plant Microbe Interact 18: 1325-1332PubMedCrossRefGoogle Scholar
  119. Watson B, Currier TC, Gordon MP, Chilton M-D, Nester EW (1975) Plasmid re-quired for virulence of Agrobacterium tumefaciens. J Bacteriol 123: 255-264PubMedGoogle Scholar
  120. Weibgen U, Russa R, Yokota A, Mayer H (1993) Taxonomic significance of the lipopolysaccharide composition of the three biovars of Agrobacterium tumefaciens. Syst Appl Microbiol 16: 177-182Google Scholar
  121. Weller SA, Stead DE, Young JPW (2004) Acquisition of an Agrobacterium Ri plasmid and pathogenicity by other Į-proteobacteria in cucumber and tomato crops affected by root mat. Appl Environ Microbiol 70: 2778-2785CrossRefGoogle Scholar
  122. White LO (1972) The taxonomy of the crown-gall organism Agrobacterium tume-faciens and its relationship to rhizobia and other agrobacteria. J Gen Micro-biol 72: 565-574Google Scholar
  123. Willems A, Collins MD (1993) Phylogenetic analysis of rhizobia and agrobacteria based on 16S rRNA gene sequences. Int J Syst Bacteriol 43: 305-313PubMedCrossRefGoogle Scholar
  124. Willems A, Fernandez-Lopez M, Munoz-Adelantado E, Goris J, De Vos P, Martinez-Romero E, Toro N, Gillis M (2003) Description of new Ensifer strains from nodules and proposal to transfer Ensifer adhaerens Casida 1982 to Sinorhizobium as Sinorhizobium adhaerens comb. nov. Request for an opinion. Int J Syst Evol Microbiol 53: 1207-1217PubMedCrossRefGoogle Scholar
  125. Willmitzer L, De Beuckeleer M, Lemmers M, van Montagu M, Schell J (1980) DNA from Ti plasmid present in nucleus and absent from plastids of crown gall plants. Nature 287: 359-361CrossRefGoogle Scholar
  126. Woese CR (1987) Bacterial evolution. Microbiol Rev 51: 221-271PubMedGoogle Scholar
  127. Wolde-Meskel E, Terefework Z, Frostegård A, Lindström K (2005) Genetic di-versity and phylogeny of rhizobia isolated from agroforestry legume species in southern Ethiopia. Int J Syst Evol Microbiol 55: 1439-1452PubMedCrossRefGoogle Scholar
  128. Young JM (2000a) Recent systematics developments and implications for plant pathogenic bacteria. In FG Priest, M Goodfellow, eds, Applied Microbial Sys-tematics. Kluwer, Dordrecht, pp 133-160Google Scholar
  129. Young JM (2000b) Suggestions for avoiding on-going confusion from the Bacte-riological Code. Int J Syst Evol Microbiol 50: 1687-1698PubMedGoogle Scholar
  130. Young JM (2001) Implications of alternative classifications and horizontal gene transfer for bacterial taxonomy. Int J Syst Evol Microbiol 51: 945-953PubMedGoogle Scholar
  131. Young JM, Dye DW, Bradbury JF, Panagopoulos CG, Robbs CF (1978) A pro-posed nomenclature and classification for plant pathogenic bacteria. NZ J Agric Res 21: 153-177Google Scholar
  132. Young JM, Kerr A, Sawada H (2005) Genus Agrobacterium Conn 1942, 359AL. In DJ Brenner, NR Krieg, JT Staley, GM Garrity, eds, Bergey’s Manual of Sys-tematic Bacteriology. The Proteobacteria, Vol. 2C, 2ed ed. Springer-Verlag, New York, pp 340-345Google Scholar
  133. Young JM, Kuykendall LD, Martinez-Romero E, Kerr A, Sawada H (2001) A re-vision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizo-bium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radio-bacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int J Syst Evol Microbiol 51: 89-103PubMedGoogle Scholar
  134. Young JM, Kuykendall LD, Martinez-Romero E, Kerr A, Sawada H (2003) Clas-sification and nomenclature of Agrobacterium and Rhizobium - a reply to Farrand, van Berkum and Oger. Int J Syst Evol Microbiol 53: 1689-1695PubMedCrossRefGoogle Scholar
  135. Young JM, Park DC, Weir BS (2004) Diversity of 16S rDNA sequences of Rhizo-bium spp. implications for species determinations. FEMS Microbiol Lett 238: 125-131PubMedGoogle Scholar
  136. Young JM, Pennycook SR, Watson DRW (2006a) Proposal that Agrobacterium radiobacter has priority over Agrobacterium tumefaciens. Request for an opinion. Int J Syst Evol Microbiol 56: 491-493PubMedCrossRefGoogle Scholar
  137. Young JM, Takikawa Y, Gardan L, Stead DE (1992) Changing concepts in the taxonomy of plant pathogenic bacteria. Annu Rev Phytopathol 30: 67-105CrossRefGoogle Scholar
  138. Young JPW, Huakka KE (1996) Diversity and phylogeny of rhizobia. New Phy-tolol 133: 87-94CrossRefGoogle Scholar
  139. Young JPW, Crossman LC, Johnston AWB, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson ARJ, Todd JD, Poole PS, Mauchline TH, East AK, Quail MA, Churcher C, Arrowsmith C, Cherevach I, Chillingworth T, Clarke K, Cronin A, Davis P, Fraser A, Hance Z, Hauser H, Jagels K, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Sanders M, Simmonds M, Whitehead S, Parkhill J (2006b) The genome of Rhizobium leguminosarum has recogniz-able core and accessory components. Genome Biology 7: R34, pp 1-26 []
  140. Zeigler DR (2003) Gene sequences useful for predicting relatedness of whole ge-nomes in bacteria. Int J Syst Evol Microbiol 53: 1893-1900PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • John M. Young
    • 1
  1. 1.Landcare ResearchAucklandNew Zealand

Personalised recommendations