The Molecular Basis of the Agrobacterium-Plant Interaction — Characteristics of Agrobacterium virulence genes and their possible occurrence in other plant-associated bacteria -

  • Paul J. J. Hooykaas
  • Rob A. Schilperoort
Part of the NATO ASI Series book series (volume 4)


Bacterial species of the genus Agrobacterium can either induce tumours or adventitious roots from infected wound sites on a wide range of dicotyledonous plant species (Fig.1). While A.tumefaciens induces tumours which are called crown galls (Smith and Townsend 1907), A.rhizogenes (Riker 1930) provokes hairy root formation on plant species such as apple, tobacco, clover, carrot or tumour formation on plants such as sunflower and pea. Most Agrobacterium strains have a wide host range, but certain strains — usually grapevine isolates — have a limited host range, which is restricted to grapevine and a number of Nicotiana species (Panagopoulos and Psallidas 1973). There is variation among plant species (De Cleene and De Ley 1976) and even between cultivars of one particular species (Owens and Cress 1985) in their susceptibility to Agrobacterium infection, while also various parts and organs of the same plant may respond differently to this bacterium.


Hairy Root Agrobacterium Tumefaciens Crown Gall Hairy Root Disease Crown Gall Tumorigenesis 
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  1. Akiyoshi DE, Klee H, Amasino RM, Nester EW, Gordon MP (1984) T-DNA of Agrobacterium tumefaciens encodes an enzyme of cytokinin biosynthesis. Proc Natl Acad Sci USA 81: 5994–5998.PubMedCrossRefGoogle Scholar
  2. Barry GF, Rogers SG, Fraley RT, Brand L (1984) Identification of a cloned cytokinin biosynthetic gene. Proc Natl Acad Sci USA 81: 4776–4780.PubMedCrossRefGoogle Scholar
  3. Bevan MW, Chilton MD (1982) T-DNA of the Agrobacterium Ti and Ri plasmids. Ann Rev Genet 16: 357–384.PubMedCrossRefGoogle Scholar
  4. Bradley DE, Douglas CJ, Peschon J (1984) Flagella-specific bacteriophages of Agrobacterium tumefaciens: demonstration of virulence of nonmotile mutants. Can J Microbiol 30: 676–681.PubMedCrossRefGoogle Scholar
  5. Braun AC (1958) A physiological basis for autonomous growth of crown gall tumor cell. Proc Natl Acad Sci USA 44: 344–349.PubMedCrossRefGoogle Scholar
  6. Costantino P, Hooykaas PJJ, Den Dulk-Ras H, Schilperoort RA (1980) Tumor formation and rhizogenicity of Agrobacterium rhizogenes carrying Ti plasmids. Gene 11: 79–87.PubMedCrossRefGoogle Scholar
  7. Dazzo FB, Truchet GL, Sherwood JE, Hrabak EM, Abe M, Pankratz SH (1984) Specific phases of root hair attachment in the Rhizobium trifolii-clover symbiosis. Appl Env Microbiol 48: 1140–1150.Google Scholar
  8. De Cleene M, DeLey J (1976) The host range of crown gall. Botan Rev 42: 389–466.CrossRefGoogle Scholar
  9. De Framond AJ, Barton KA, Chilton MD (1983) Mini-Ti: a new vector strategy for plant genetic engineering. Bio/Technology 1: 262–269.CrossRefGoogle Scholar
  10. Douglas CJ, Halperin W, Nester EW (1982) Agrobacterium tumefaciens mutants affected in attachment to plant cells. J Bacteriol 152: 1265–1275.PubMedGoogle Scholar
  11. Douglas CJ, Staneloni RJ, Rubin RA, Nester EW (1985) Identification and genetic analysis of an Agrobacterium tumefaciens chromosomal virulence region. J Bacteriol 161: 850–860.PubMedGoogle Scholar
  12. Garfinkel DJ, Nester EW (1980) Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism. J Bacteriol 144: 732–743.PubMedGoogle Scholar
  13. Hille J, Klasen I, Schilperoort R (1982) Construction and application of Rprime plasmids, carrying different segments of an octopine Ti plasmid from Agrobacterium tumefaciens for complementation of vir genes. Plasmid 7: 107–118.PubMedCrossRefGoogle Scholar
  14. Hille J, Van Kan J, Schilperoort R (1984) Trans-acting virulence functions of the octopine Ti plasmid from Agrobacterium tumefaciens. J Bacteriol 158: 754–756.PubMedGoogle Scholar
  15. Hoekema A, Hirsch PR, Hooykaas PJJ, Schilperoort RA (1983) A binary plant vector strategy based on separation of vir and T-region of the Agrobacterium tumefaciens Ti plasmid. Nature 303: 179–180.CrossRefGoogle Scholar
  16. Hoekema A, Roelvink PW, Hooykaas PJJ, Schilperoort RA (1984a) Delivery of T-DNA from the Agrobacterium tumefaciens chromosome into plant cells. EMBO J 3: 2485–2490.PubMedGoogle Scholar
  17. Hoekema A, Hooykaas PJJ, Schilperoort RA (1984b) Transfer of the octopine T-DNA segment to plant cells mediated by different types of Agrobacterium tumor-or root inducing plasmids: generality of virulence systems. J Bacteriol 158: 383–385.PubMedGoogle Scholar
  18. Hooykaas PJJ (1979) The role of plasmid determined functions in the interactions of Rhizobiaceae with plant cells. A genetic approach. Thesis, Leiden, The Netherlands.Google Scholar
  19. Hooykaas PJJ, Schilperoort RA (1984) The molecular genetics of crown gall tumorigenesis. In: Scandalios JG (ed) Molecular Genetics of Plants. Advances in Genetics, vol 22. Academic Press, Orlando, USA, pp 209–283.Google Scholar
  20. Hooykaas PJJ, 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: 477–484.Google Scholar
  21. Hooykaas PJJ, Peerbolte R, Regensburg-Tuínk AJG, De Vries P, Schilperoort RA (1982) A chromosomal linkage map of Agrobacterium tumefaciens and a comparison with the maps of Rhizobium spp. Mol Gen Genet 188: 12–17.CrossRefGoogle Scholar
  22. Hooykaas PJJ, Hofker M, Den Dulk-Ras H, Schilperoort RA (1984) A comparison of virulence determinants in an octopine Ti plasmid, a nopaline Ti plasmid, and an Ri plasmid by complementation analysis of Agrobacterium tumefaciens mutants. Plasmid 11: 195–205.PubMedCrossRefGoogle Scholar
  23. Hooykaas PJJ, Den Dulk-Ras H, Regensburg-Tuïnk AJG, Van Brussel AAN, Schilperoort RA (1985) Expression of a Rhizobium phaseoli Sym plasmid in R. trifolii and Agrobacterium tumefaciens: incompatibility with a R. trifolii Sym plasmid. Plasmid 14:47–52.PubMedCrossRefGoogle Scholar
  24. Hooykaas-Van Slogteren GMS, Hooykaas PJJ, Schilperoort RA (1984) Expression of Ti plasmid genes in monocotyledonous plants infected with Agrobacterium tumefaciens. Nature 311: 763–764.CrossRefGoogle Scholar
  25. Klapwijk PM, Scheulderman T, Schilperoort RA (1978) Coordinated regulation of octopine degradation and conjugative transfer of Ti plasmid in Agrobacterium tumefaciens: evidence for a common regulatory gene and separate operons. J Bacteriol 136: 775–785.PubMedGoogle Scholar
  26. Klee HJ, White FF, Iyer VN, Gordon MP, Nester EW (1983) Mutational analysis of the virulence region of an Agrobacterium tumefaciens Ti-plasmid. J Bacteriol 153: 878–883.PubMedGoogle Scholar
  27. Leemans J, Deblaere R, Willmitzer L, De Greve H, Hernalsteens JP, Van Montagu M, Schell J (1982) Genetic identification of functions of TL-DNA transcripts in octopine crown galls. EMBO J 1: 147–152.PubMedGoogle Scholar
  28. Lundquist RC, Close TJ, Kado CI (1984) Genetic complementation of Agrobacterium tumefaciens Ti plasmid mutants in the virulence region. Mol Gen Genet 193: 1–7.PubMedCrossRefGoogle Scholar
  29. Matthysse AG (1983) Role of bacterial cellulose fibrils in Agrobacterium tumefaciens infection. J Bacteriol 154: 906–915.PubMedGoogle Scholar
  30. Messens E, Lenaerts A, Van Montagu M, Hedges RW (1985) Genetic basis for opine secretion from crown gall tumour cells. Mol Gen Genet 199: 344–348.CrossRefGoogle Scholar
  31. Nester EW, Kosuge T (1981) Plasmids specifying plant hyperplasias. Ann Rev Microbiol 35: 531–565.CrossRefGoogle Scholar
  32. Offringa IA, Melchers LS, Regensburg-Tuink AJG, Costantino P, Schilperoort RA, Hooykaas PJJ (1986) Complementation of Agrobacterium tumefaciens Ti aux mutants by genes from the TR-region of the Ri plasmid of Agrobacterium rhizogenes. iProc Natl Acad Sci USA 83:.Google Scholar
  33. Okker RJH, Spaink H, Hille J, Van Brussel TAN, Lugtenberg B, Schilperoort RA (1984) Plant-inducible virulence promoter of the Agrobacterium tumefaciens Ti plasmid. Nature 312: 564–566.PubMedCrossRefGoogle Scholar
  34. Ooms G, Molendijk L, Schilperoort RA (1982) Double infection of tobacco plants by two complementing octopine T-region mutants of Agrobacterium tumefaciens. Plant Mol Biol 1: 217–226.CrossRefGoogle Scholar
  35. Owens LD, Cress DE (1985) Genotypic variability of soybean response to Agrobacterium strains harboring the Ti or Ri plasmid. Plant Physiol 77: 87–94.PubMedCrossRefGoogle Scholar
  36. Panagopoulos CG, Psallidas PG (1973) Characteristics of Greek isolates of Agrobacterium tumefaciens (Smith and Townsend) Conn. J Appl Bact 36: 233–240.CrossRefGoogle Scholar
  37. Peerbolte R (1986) The fate of T-DNA during vegetative and generative propagation — crown gall and hairy root tissues of Nicotiana spp — Thesis, Leiden, The Netherlands.Google Scholar
  38. Petit A, Tempe J (1978) Isolation of Agrobacterium Ti-plasmid regulatory mutants. Mol Gen Genet 167: 147–155.CrossRefGoogle Scholar
  39. Petit A, Delhaye S, Tempé J, Morel G (1970) Recherches sur les guanidines des tissues de crown-gall. Mise en évidence d’une relation biochimique spécifique entre les souches d’Agrobacterium tumefaciens et les tumeurs qu’elles induisent. Physiol Végét 8: 205–213.Google Scholar
  40. Powell GK, Morris RO (1986) Nucleotide sequence and expression of a Pseudomonas savastanoi cytokinin biosynthetic gene: homology with Agrobacterium tumefaciens tmr and tzs loci. Nucl Ac Res 14: 2555–2565.CrossRefGoogle Scholar
  41. Prakash RK, Schilperoort RA (1982) Relationship between nif plasmids of fast-growing Rhizobium species and Ti plasmids of Agrobacterium tumefaciens. J Bacteriol 149: 1129–1134.PubMedGoogle Scholar
  42. Puvanesarajah V, Schell FM, Stacey G, Douglas CJ, Nester EW (1985) Role for 2-linked-β-d-glucan in the virulence of Agrobacterium tumefaciens. J Bacteriol 164: 102–106.PubMedGoogle Scholar
  43. Riker AJ (1930) Studies on infectious hairy root of nursery apple trees. J Agr Res 41: 507–540.Google Scholar
  44. Risuleo G, Battistoni P, Costantinó P (1982) Regions of homology between tumorigenic plasmids from Agrobacterium rhizogenes and Agrobacterium tumefaciens. Plasmid 7: 45–51.PubMedCrossRefGoogle Scholar
  45. Schröder G, Waffenschmidt S, Weiler EW, Schröder J (1984) The T-region of Ti-plasmids codes for an enzyme synthesizing indole-3-acetic acid. Eur J Biochem 138: 387–391.PubMedCrossRefGoogle Scholar
  46. Smidt M, Kosuge T (1978) The role of indole-3-acetic acid accumulation by alpha-methyl tryptophan-resistant mutants of Pseudomonas savastanoi in gall formation on oleanders. Physiol Plant Pathol 13: 203–214.CrossRefGoogle Scholar
  47. Smith EF, Townsend CO (1907) A plant tumor of bacterial origin. Science 25: 671–673.PubMedCrossRefGoogle Scholar
  48. Stachel SE, Messens E, Van Montagu M, Zambryski P (1985) Identification of the signal molecules produced by wounded plant cells that activate T-DNA transfer in Agrobacterium tumefaciens. Nature 318: 624–629.CrossRefGoogle Scholar
  49. Stachel SE, Nester EW, Zambryski PC (1986) A plant cell factor induces Agrobacterium tumefaciensvir gene expression. Proc Natl Acad Sci USA 83: 379–383.PubMedCrossRefGoogle Scholar
  50. Tempé J, Goldmann A (1982) Occurence and biosynthesis of opines. In: Kahl G, Schell J (eds) Molecular Biology of Plant Tumors, Acad Press New York, pp 427–449.Google Scholar
  51. Thomashow LS, Reeves S, Thomashow MF (1984) Crown gall oncogenesis: evidence that a T-DNA gene from the Agrobacterium Ti plasmid pTiA6 encodes an enzyme that catalyzes synthesis of indoleacetic acid. Proc Natl Acad Sci USA 81: 5071–5075.PubMedCrossRefGoogle Scholar
  52. Thomashow MF, Hugly S, Buchholz WG, Thomashow LS (1986) Molecular basis for the auxin-independent phenotype of crown gall tumor tissues. Science 231: 616–618.PubMedCrossRefGoogle Scholar
  53. Vanderleyden JP, Verdickt KM, Waelkens FM, Van Gool AP, Mergeay M (1985) Construction and characterization of R-prime plasmid carrying a chromosomal virulence region of Agrobacterium tumefaciens. Abstract First Intern Congress on Plant Mol Biol p 161.Google Scholar
  54. Van Montagu M, Schell J (1982) The Ti plasmids of Agrobacterium. Curr Topics 96: 237–254.Google Scholar
  55. Van Onckelen H, Prinsen E, Inzé D, Rüdeisheim P, Van Lijsebettens M, Follin A, Schell J, Van Montagu M, De Greef J (1986) Agrobacterium T-DNA gene 1 codes for tryptophan 2-monooxygenase activity in tobacco crown gall cells. FEBS Lett 198: 357–360.CrossRefGoogle Scholar
  56. Van Veen RJM, Den Dulk-Ras H, Hooykaas PJJ, Schilperoort RA (1986) Chromosomal nodulation genes: Sym-plasmid containing Agrobacterium strains need chromosomal virulence genes (chvA and chvB) for nodulation. J Bacteriol.Google Scholar
  57. White FF, Nester EW (1980) Relationship of plasmids responsible for hairy root and crown gall tumorigenicity. J Bacteriol 144: 710–720.PubMedGoogle Scholar
  58. Willmitzer L, Simons G, Schell J (1982) The TL-DNA in octopine crown-gall tumours codes for seven well-defined polyadenylated transcripts. EMBO J 1: 139–146.PubMedGoogle Scholar
  59. Wilson EE (1935) The olive knot disease: its inception, development, and control. Hilgardia 9: 231–264.Google Scholar
  60. Yadav NS, Vanderleyden J, Bennett DR, Barnes WM, Chilton MD (1982) Short direct repeats flank the T-DNA on a nopaline Ti plasmid. Proc Natl Acad Sci USA 79: 6322–6326.PubMedCrossRefGoogle Scholar
  61. Yamada T, Palm CJ, Brooks B, Kosuge T (1985) Nucleotide sequences of the Pseudomonas savastanoi indoleacetic acid genes show homology with Agrobacterium tumefaciens T-DNA. Proc Natl Acad Sci USA 82: 6522–6526.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1986

Authors and Affiliations

  • Paul J. J. Hooykaas
    • 1
  • Rob A. Schilperoort
    • 1
  1. 1.Dept. Plant Molecular Biology, Biochemistry LabLeiden UniversityLeidenThe Netherlands

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