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. 1992 Mar;56(1):12–31. doi: 10.1128/mr.56.1.12-31.1992

Two-way chemical signaling in Agrobacterium-plant interactions.

S C Winans 1
PMCID: PMC372852  PMID: 1579105

Abstract

The discovery in 1977 that Agrobacterium species can transfer a discrete segment of oncogenic DNA (T-DNA) to the genome of host plant cells has stimulated an intense interest in the molecular biology underlying these plant-microbe associations. This attention in turn has resulted in a series of insights about the biology of these organisms that continue to accumulate at an ever-increasing rate. This excitement was due in part to the notion that this unprecedented interkingdom DNA transfer could be exploited to create transgenic plants containing foreign genes of scientific or commercial importance. In the course of these discoveries, Agrobacterium became one of the best available models for studying the molecular interactions between bacteria and higher organisms. One extensively studied aspect of this association concerns the exchange of chemical signals between Agrobacterium spp. and host plants. Agrobacterium spp. can recognize no fewer than five classes of low-molecular-weight compounds released from plants, and other classes probably await discovery. The most widely studied of these are phenolic compounds, which stimulate the transcription of the genes needed for infection. Other compounds include specific monosaccharides and acidic environments which potentiate vir gene induction, acidic polysaccharides which induce one or more chromosomal genes, and a family of compounds called opines which are released from tumorous plant cells to the bacteria as nutrient sources. Agrobacterium spp. in return release a variety of chemical compounds to plants. The best understood is the transferred DNA itself, which contains genes that in various ways upset the balance of phytohormones, ultimately causing neoplastic cell proliferation. In addition to transferring DNA, some Agrobacterium strains directly secrete phytohormones. Finally, at least some strains release a pectinase, which degrades a component of plant cell walls.

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Selected References

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  1. Aiba H., Nakasai F., Mizushima S., Mizuno T. Phosphorylation of a bacterial activator protein, OmpR, by a protein kinase, EnvZ, results in stimulation of its DNA-binding ability. J Biochem. 1989 Jul;106(1):5–7. doi: 10.1093/oxfordjournals.jbchem.a122817. [DOI] [PubMed] [Google Scholar]
  2. Akiyoshi D. E., Klee H., Amasino R. M., Nester E. W., Gordon M. P. T-DNA of Agrobacterium tumefaciens encodes an enzyme of cytokinin biosynthesis. Proc Natl Acad Sci U S A. 1984 Oct;81(19):5994–5998. doi: 10.1073/pnas.81.19.5994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Albano M., Breitling R., Dubnau D. A. Nucleotide sequence and genetic organization of the Bacillus subtilis comG operon. J Bacteriol. 1989 Oct;171(10):5386–5404. doi: 10.1128/jb.171.10.5386-5404.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Albright L. M., Huala E., Ausubel F. M. Prokaryotic signal transduction mediated by sensor and regulator protein pairs. Annu Rev Genet. 1989;23:311–336. doi: 10.1146/annurev.ge.23.120189.001523. [DOI] [PubMed] [Google Scholar]
  5. Albright L. M., Yanofsky M. F., Leroux B., Ma D. Q., Nester E. W. Processing of the T-DNA of Agrobacterium tumefaciens generates border nicks and linear, single-stranded T-DNA. J Bacteriol. 1987 Mar;169(3):1046–1055. doi: 10.1128/jb.169.3.1046-1055.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Alt-Moerbe J., Rak B., Schröder J. A 3.6-kbp segment from the vir region of Ti plasmids contains genes responsible for border-sequence-directed production of T region circles in E. coli. EMBO J. 1986 Jun;5(6):1129–1135. doi: 10.1002/j.1460-2075.1986.tb04337.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ankenbauer R. G., Best E. A., Palanca C. A., Nester E. W. Mutants of the Agrobacterium tumefaciens virA gene exhibiting acetosyringone-independent expression of the vir regulon. Mol Plant Microbe Interact. 1991 Jul-Aug;4(4):400–406. doi: 10.1094/mpmi-4-400. [DOI] [PubMed] [Google Scholar]
  8. Ankenbauer R. G., Nester E. W. Sugar-mediated induction of Agrobacterium tumefaciens virulence genes: structural specificity and activities of monosaccharides. J Bacteriol. 1990 Nov;172(11):6442–6446. doi: 10.1128/jb.172.11.6442-6446.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Aoyama T., Takanami M., Oka A. Signal structure for transcriptional activation in the upstream regions of virulence genes on the hairy-root-inducing plasmid A4. Nucleic Acids Res. 1989 Nov 11;17(21):8711–8725. doi: 10.1093/nar/17.21.8711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Aricó B., Miller J. F., Roy C., Stibitz S., Monack D., Falkow S., Gross R., Rappuoli R. Sequences required for expression of Bordetella pertussis virulence factors share homology with prokaryotic signal transduction proteins. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6671–6675. doi: 10.1073/pnas.86.17.6671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ashby A. M., Watson M. D., Loake G. J., Shaw C. H. Ti plasmid-specified chemotaxis of Agrobacterium tumefaciens C58C1 toward vir-inducing phenolic compounds and soluble factors from monocotyledonous and dicotyledonous plants. J Bacteriol. 1988 Sep;170(9):4181–4187. doi: 10.1128/jb.170.9.4181-4187.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Bakkeren G., Koukolíková-Nicola Z., Grimsley N., Hohn B. Recovery of Agrobacterium tumefaciens T-DNA molecules from whole plants early after transfer. Cell. 1989 Jun 2;57(5):847–857. doi: 10.1016/0092-8674(89)90799-x. [DOI] [PubMed] [Google Scholar]
  13. Bergeron J., Macleod R. A., Dion P. Specificity of octopine uptake by Rhizobium and pseudomonas strains. Appl Environ Microbiol. 1990 May;56(5):1453–1458. doi: 10.1128/aem.56.5.1453-1458.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Bevan M., Barnes W. M., Chilton M. D. Structure and transcription of the nopaline synthase gene region of T-DNA. Nucleic Acids Res. 1983 Jan 25;11(2):369–385. doi: 10.1093/nar/11.2.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Bolton G. W., Nester E. W., Gordon M. P. Plant phenolic compounds induce expression of the Agrobacterium tumefaciens loci needed for virulence. Science. 1986 May 23;232(4753):983–985. doi: 10.1126/science.3085219. [DOI] [PubMed] [Google Scholar]
  16. Bouchez D., Camilleri C. Identification of a putative rol B gene on the TR-DNA of the Agrobacterium rhizogenes A4 Ri plasmid. Plant Mol Biol. 1990 Apr;14(4):617–619. doi: 10.1007/BF00027507. [DOI] [PubMed] [Google Scholar]
  17. Bouchez D., Tourneur J. Organization of the agropine synthesis region of the T-DNA of the Ri plasmid from Agrobacterium rhizogenes. Plasmid. 1991 Jan;25(1):27–39. doi: 10.1016/0147-619x(91)90004-g. [DOI] [PubMed] [Google Scholar]
  18. Bouzar H., Moore L. W. Isolation of different agrobacterium biovars from a natural oak savanna and tallgrass prairie. Appl Environ Microbiol. 1987 Apr;53(4):717–721. doi: 10.1128/aem.53.4.717-721.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Buchmann I., Marner F. J., Schröder G., Waffenschmidt S., Schröder J. Tumour genes in plants: T-DNA encoded cytokinin biosynthesis. EMBO J. 1985 Apr;4(4):853–859. doi: 10.1002/j.1460-2075.1985.tb03710.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Caetano-Anollés G., Crist-Estes D. K., Bauer W. D. Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J Bacteriol. 1988 Jul;170(7):3164–3169. doi: 10.1128/jb.170.7.3164-3169.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Caetano-Anollés G., Wall L. G., De Micheli A. T., Macchi E. M., Bauer W. D., Favelukes G. Role of Motility and Chemotaxis in Efficiency of Nodulation by Rhizobium meliloti. Plant Physiol. 1988 Apr;86(4):1228–1235. doi: 10.1104/pp.86.4.1228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Camilleri C., Jouanin L. The TR-DNA region carrying the auxin synthesis genes of the Agrobacterium rhizogenes agropine-type plasmid pRiA4: nucleotide sequence analysis and introduction into tobacco plants. Mol Plant Microbe Interact. 1991 Mar-Apr;4(2):155–162. doi: 10.1094/mpmi-4-155. [DOI] [PubMed] [Google Scholar]
  23. Cangelosi G. A., Ankenbauer R. G., Nester E. W. Sugars induce the Agrobacterium virulence genes through a periplasmic binding protein and a transmembrane signal protein. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6708–6712. doi: 10.1073/pnas.87.17.6708. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Cangelosi G. A., Hung L., Puvanesarajah V., Stacey G., Ozga D. A., Leigh J. A., Nester E. W. Common loci for Agrobacterium tumefaciens and Rhizobium meliloti exopolysaccharide synthesis and their roles in plant interactions. J Bacteriol. 1987 May;169(5):2086–2091. doi: 10.1128/jb.169.5.2086-2091.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Cangelosi G. A., Martinetti G., Leigh J. A., Lee C. C., Thienes C., Theines C., Nester E. W. Role for [corrected] Agrobacterium tumefaciens ChvA protein in export of beta-1,2-glucan. J Bacteriol. 1989 Mar;171(3):1609–1615. doi: 10.1128/jb.171.3.1609-1615.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Cangelosi G. A., Martinetti G., Nester E. W. Osmosensitivity phenotypes of Agrobacterium tumefaciens mutants that lack periplasmic beta-1,2-glucan. J Bacteriol. 1990 Apr;172(4):2172–2174. doi: 10.1128/jb.172.4.2172-2174.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Chang C. C., Chen C. M., Adams B. R., Trost B. M. Leucinopine, a characteristic compound of some crown-gall tumors. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3573–3576. doi: 10.1073/pnas.80.12.3573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Chelsky D., Ralph R., Jonak G. Sequence requirements for synthetic peptide-mediated translocation to the nucleus. Mol Cell Biol. 1989 Jun;9(6):2487–2492. doi: 10.1128/mcb.9.6.2487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Chen C. Y., Winans S. C. Controlled expression of the transcriptional activator gene virG in Agrobacterium tumefaciens by using the Escherichia coli lac promoter. J Bacteriol. 1991 Feb;173(3):1139–1144. doi: 10.1128/jb.173.3.1139-1144.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Chilton M. D., Drummond M. H., Merio D. J., Sciaky D., Montoya A. L., Gordon M. P., Nester E. W. Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis. Cell. 1977 Jun;11(2):263–271. doi: 10.1016/0092-8674(77)90043-5. [DOI] [PubMed] [Google Scholar]
  31. Chilton M. D., Saiki R. K., Yadav N., Gordon M. P., Quetier F. T-DNA from Agrobacterium Ti plasmid is in the nuclear DNA fraction of crown gall tumor cells. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4060–4064. doi: 10.1073/pnas.77.7.4060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Chilton W. S., Tempé J., Matzke M., Chilton M. D. Succinamopine: a new crown gall opine. J Bacteriol. 1984 Feb;157(2):357–362. doi: 10.1128/jb.157.2.357-362.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Christie P. J., Ward J. E., Jr, Gordon M. P., Nester E. W. A gene required for transfer of T-DNA to plants encodes an ATPase with autophosphorylating activity. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9677–9681. doi: 10.1073/pnas.86.24.9677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Christie P. J., Ward J. E., Winans S. C., Nester E. W. The Agrobacterium tumefaciens virE2 gene product is a single-stranded-DNA-binding protein that associates with T-DNA. J Bacteriol. 1988 Jun;170(6):2659–2667. doi: 10.1128/jb.170.6.2659-2667.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Citovsky V., DE Vos G., Zambryski P. Single-Stranded DNA Binding Protein Encoded by the virE Locus of Agrobacterium tumefaciens. Science. 1988 Apr 22;240(4851):501–504. doi: 10.1126/science.240.4851.501. [DOI] [PubMed] [Google Scholar]
  36. Close T. J., Rogowsky P. M., Kado C. I., Winans S. C., Yanofsky M. F., Nester E. W. Dual control of Agrobacterium tumefaciens Ti plasmid virulence genes. J Bacteriol. 1987 Nov;169(11):5113–5118. doi: 10.1128/jb.169.11.5113-5118.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Close T. J., Tait R. C., Kado C. I. Regulation of Ti plasmid virulence genes by a chromosomal locus of Agrobacterium tumefaciens. J Bacteriol. 1985 Nov;164(2):774–781. doi: 10.1128/jb.164.2.774-781.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Close T. J., Tait R. C., Rempel H. C., Hirooka T., Kim L., Kado C. I. Molecular characterization of the virC genes of the Ti plasmid. J Bacteriol. 1987 Jun;169(6):2336–2344. doi: 10.1128/jb.169.6.2336-2344.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Cooley M. B., D'Souza M. R., Kado C. I. The virC and virD operons of the Agrobacterium Ti plasmid are regulated by the ros chromosomal gene: analysis of the cloned ros gene. J Bacteriol. 1991 Apr;173(8):2608–2616. doi: 10.1128/jb.173.8.2608-2616.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Crews J. L., Colby S., Matthysse A. G. Agrobacterium rhizogenes mutants that fail to bind to plant cells. J Bacteriol. 1990 Nov;172(11):6182–6188. doi: 10.1128/jb.172.11.6182-6188.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Das A. Agrobacterium tumefaciens virE operon encodes a single-stranded DNA-binding protein. Proc Natl Acad Sci U S A. 1988 May;85(9):2909–2913. doi: 10.1073/pnas.85.9.2909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Das A., Pazour G. J. Delineation of the regulatory region sequences of Agrobacterium tumefaciens virB operon. Nucleic Acids Res. 1989 Jun 26;17(12):4541–4550. doi: 10.1093/nar/17.12.4541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. De Greve H., Dhaese P., Seurinck J., Lemmers M., Van Montagu M., Schell J. Nucleotide sequence and transcript map of the Agrobacterium tumefaciens Ti plasmid-encoded octopine synthase gene. J Mol Appl Genet. 1982;1(6):499–511. [PubMed] [Google Scholar]
  44. De Vos G., Zambryski P. Expression of Agrobacterium nopaline-specific VirD1, VirD2, and VirC1 proteins and their requirement for T-strand production in E. coli. Mol Plant Microbe Interact. 1989 Mar-Apr;2(2):43–52. doi: 10.1094/mpmi-2-043. [DOI] [PubMed] [Google Scholar]
  45. Dessaux Y., Guyon P., Farrand S. K., Petit A., Tempé J. Agrobacterium Ti and Ri plasmids specify enzymic lactonization of mannopine to agropine. J Gen Microbiol. 1986 Sep;132(9):2549–2559. doi: 10.1099/00221287-132-9-2549. [DOI] [PubMed] [Google Scholar]
  46. Dessaux Y., Guyon P., Petit A., Tempé J., Demarez M., Legrain C., Tate M. E., Farrand S. K. Opine utilization by Agrobacterium spp.: octopine-type Ti plasmids encode two pathways for mannopinic acid degradation. J Bacteriol. 1988 Jul;170(7):2939–2946. doi: 10.1128/jb.170.7.2939-2946.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Dessaux Y., Tempé J., Farrand S. K. Genetic analysis of mannityl opine catabolism in octopine-type Agrobacterium tumefaciens strain 15955. Mol Gen Genet. 1987 Jun;208(1-2):301–308. doi: 10.1007/BF00330457. [DOI] [PubMed] [Google Scholar]
  48. Djordjevic S. P., Chen H., Batley M., Redmond J. W., Rolfe B. G. Nitrogen fixation ability of exopolysaccharide synthesis mutants of Rhizobium sp. strain NGR234 and Rhizobium trifolii is restored by the addition of homologous exopolysaccharides. J Bacteriol. 1987 Jan;169(1):53–60. doi: 10.1128/jb.169.1.53-60.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Douglas C. J., Staneloni R. J., Rubin R. A., Nester E. W. Identification and genetic analysis of an Agrobacterium tumefaciens chromosomal virulence region. J Bacteriol. 1985 Mar;161(3):850–860. doi: 10.1128/jb.161.3.850-860.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Dylan T., Ielpi L., Stanfield S., Kashyap L., Douglas C., Yanofsky M., Nester E., Helinski D. R., Ditta G. Rhizobium meliloti genes required for nodule development are related to chromosomal virulence genes in Agrobacterium tumefaciens. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4403–4407. doi: 10.1073/pnas.83.12.4403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Dylan T., Nagpal P., Helinski D. R., Ditta G. S. Symbiotic pseudorevertants of Rhizobium meliloti ndv mutants. J Bacteriol. 1990 Mar;172(3):1409–1417. doi: 10.1128/jb.172.3.1409-1417.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Dürrenberger F., Crameri A., Hohn B., Koukolíková-Nicola Z. Covalently bound VirD2 protein of Agrobacterium tumefaciens protects the T-DNA from exonucleolytic degradation. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9154–9158. doi: 10.1073/pnas.86.23.9154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Ellis J. G., Llewellyn D. J., Walker J. C., Dennis E. S., Peacock W. J. The ocs element: a 16 base pair palindrome essential for activity of the octopine synthase enhancer. EMBO J. 1987 Nov;6(11):3203–3208. doi: 10.1002/j.1460-2075.1987.tb02636.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Engström P., Zambryski P., Van Montagu M., Stachel S. Characterization of Agrobacterium tumefaciens virulence proteins induced by the plant factor acetosyringone. J Mol Biol. 1987 Oct 20;197(4):635–645. doi: 10.1016/0022-2836(87)90470-0. [DOI] [PubMed] [Google Scholar]
  55. Farrand S. K., Tempé J., Dessaux Y. Localization and characterization of the region encoding catabolism of mannopinic acid from the octopine-type Ti plasmid pTi15955. Mol Plant Microbe Interact. 1990 Jul-Aug;3(4):259–267. doi: 10.1094/mpmi-3-259. [DOI] [PubMed] [Google Scholar]
  56. Garfinkel D. J., Nester E. W. Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism. J Bacteriol. 1980 Nov;144(2):732–743. doi: 10.1128/jb.144.2.732-743.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Gelvin S. B. Crown gall disease and hairy root disease : a sledgehammer and a tackhammer. Plant Physiol. 1990 Feb;92(2):281–285. doi: 10.1104/pp.92.2.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Ghai J., Das A. The virD operon of Agrobacterium tumefaciens Ti plasmid encodes a DNA-relaxing enzyme. Proc Natl Acad Sci U S A. 1989 May;86(9):3109–3113. doi: 10.1073/pnas.86.9.3109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Gheysen G., Montagu M. V., Zambryski P. Integration of Agrobacterium tumefaciens transfer DNA (T-DNA) involves rearrangements of target plant DNA sequences. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6169–6173. doi: 10.1073/pnas.84.17.6169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Gietl C., Koukolíková-Nicola Z., Hohn B. Mobilization of T-DNA from Agrobacterium to plant cells involves a protein that binds single-stranded DNA. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9006–9010. doi: 10.1073/pnas.84.24.9006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Grimsley N., Hohn B., Ramos C., Kado C., Rogowsky P. DNA transfer from Agrobacterium to Zea mays or Brassica by agroinfection is dependent on bacterial virulence functions. Mol Gen Genet. 1989 Jun;217(2-3):309–316. doi: 10.1007/BF02464898. [DOI] [PubMed] [Google Scholar]
  62. Habeeb L. F., Wang L., Winans S. C. Transcription of the octopine catabolism operon of the Agrobacterium tumor-inducing plasmid pTiA6 is activated by a LysR-type regulatory protein. Mol Plant Microbe Interact. 1991 Jul-Aug;4(4):379–385. doi: 10.1094/mpmi-4-379. [DOI] [PubMed] [Google Scholar]
  63. Halverson L. J., Stacey G. Signal exchange in plant-microbe interactions. Microbiol Rev. 1986 Jun;50(2):193–225. doi: 10.1128/mr.50.2.193-225.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Hawes M. C., Smith L. Y. Requirement for chemotaxis in pathogenicity of Agrobacterium tumefaciens on roots of soil-grown pea plants. J Bacteriol. 1989 Oct;171(10):5668–5671. doi: 10.1128/jb.171.10.5668-5671.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Hayman G. T., Farrand S. K. Agrobacterium plasmids encode structurally and functionally different loci for catabolism of agrocinopine-type opines. Mol Gen Genet. 1990 Sep;223(3):465–473. doi: 10.1007/BF00264455. [DOI] [PubMed] [Google Scholar]
  66. Heinemann J. A., Sprague G. F., Jr Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast. Nature. 1989 Jul 20;340(6230):205–209. doi: 10.1038/340205a0. [DOI] [PubMed] [Google Scholar]
  67. Herrera-Estrella A., Chen Z. M., Van Montagu M., Wang K. VirD proteins of Agrobacterium tumefaciens are required for the formation of a covalent DNA--protein complex at the 5' terminus of T-strand molecules. EMBO J. 1988 Dec 20;7(13):4055–4062. doi: 10.1002/j.1460-2075.1988.tb03299.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Herrera-Estrella A., Van Montagu M., Wang K. A bacterial peptide acting as a plant nuclear targeting signal: the amino-terminal portion of Agrobacterium VirD2 protein directs a beta-galactosidase fusion protein into tobacco nuclei. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9534–9537. doi: 10.1073/pnas.87.24.9534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Hess K. M., Dudley M. W., Lynn D. G., Joerger R. D., Binns A. N. Mechanism of phenolic activation of Agrobacterium virulence genes: development of a specific inhibitor of bacterial sensor/response systems. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7854–7858. doi: 10.1073/pnas.88.17.7854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Hirooka T., Rogowsky P. M., Kado C. I. Characterization of the virE locus of Agrobacterium tumefaciens plasmid pTiC58. J Bacteriol. 1987 Apr;169(4):1529–1536. doi: 10.1128/jb.169.4.1529-1536.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Hodgkin J., Kaiser D. Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2938–2942. doi: 10.1073/pnas.74.7.2938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Hooykaas P. J. Transformation of plant cells via Agrobacterium. Plant Mol Biol. 1989 Sep;13(3):327–336. doi: 10.1007/BF00025321. [DOI] [PubMed] [Google Scholar]
  73. Howard E. A., Winsor B. A., De Vos G., Zambryski P. Activation of the T-DNA transfer process in Agrobacterium results in the generation of a T-strand-protein complex: Tight association of VirD2 with the 5' ends of T-strands. Proc Natl Acad Sci U S A. 1989 Jun;86(11):4017–4021. doi: 10.1073/pnas.86.11.4017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Huang M. L., Cangelosi G. A., Halperin W., Nester E. W. A chromosomal Agrobacterium tumefaciens gene required for effective plant signal transduction. J Bacteriol. 1990 Apr;172(4):1814–1822. doi: 10.1128/jb.172.4.1814-1822.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Huang Y., Morel P., Powell B., Kado C. I. VirA, a coregulator of Ti-specified virulence genes, is phosphorylated in vitro. J Bacteriol. 1990 Feb;172(2):1142–1144. doi: 10.1128/jb.172.2.1142-1144.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Ishino Y., Shinagawa H., Makino K., Tsunasawa S., Sakiyama F., Nakata A. Nucleotide sequence of the lig gene and primary structure of DNA ligase of Escherichia coli. Mol Gen Genet. 1986 Jul;204(1):1–7. doi: 10.1007/BF00330179. [DOI] [PubMed] [Google Scholar]
  77. Iuchi S., Matsuda Z., Fujiwara T., Lin E. C. The arcB gene of Escherichia coli encodes a sensor-regulator protein for anaerobic repression of the arc modulon. Mol Microbiol. 1990 May;4(5):715–727. doi: 10.1111/j.1365-2958.1990.tb00642.x. [DOI] [PubMed] [Google Scholar]
  78. Jayaswal R. K., Veluthambi K., Gelvin S. B., Slightom J. L. Double-stranded cleavage of T-DNA and generation of single-stranded T-DNA molecules in Escherichia coli by a virD-encoded border-specific endonuclease from Agrobacterium tumefaciens. J Bacteriol. 1987 Nov;169(11):5035–5045. doi: 10.1128/jb.169.11.5035-5045.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Jin S. G., Prusti R. K., Roitsch T., Ankenbauer R. G., Nester E. W. Phosphorylation of the VirG protein of Agrobacterium tumefaciens by the autophosphorylated VirA protein: essential role in biological activity of VirG. J Bacteriol. 1990 Sep;172(9):4945–4950. doi: 10.1128/jb.172.9.4945-4950.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Jin S. G., Roitsch T., Christie P. J., Nester E. W. The regulatory VirG protein specifically binds to a cis-acting regulatory sequence involved in transcriptional activation of Agrobacterium tumefaciens virulence genes. J Bacteriol. 1990 Feb;172(2):531–537. doi: 10.1128/jb.172.2.531-537.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Jin S., Roitsch T., Ankenbauer R. G., Gordon M. P., Nester E. W. The VirA protein of Agrobacterium tumefaciens is autophosphorylated and is essential for vir gene regulation. J Bacteriol. 1990 Feb;172(2):525–530. doi: 10.1128/jb.172.2.525-530.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. John M. C., Amasino R. M. Expression of an Agrobacterium Ti plasmid gene involved in cytokinin biosynthesis is regulated by virulence loci and induced by plant phenolic compounds. J Bacteriol. 1988 Feb;170(2):790–795. doi: 10.1128/jb.170.2.790-795.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Joos H., Inzé D., Caplan A., Sormann M., Van Montagu M., Schell J. Genetic analysis of T-DNA transcripts in nopaline crown galls. Cell. 1983 Apr;32(4):1057–1067. doi: 10.1016/0092-8674(83)90290-8. [DOI] [PubMed] [Google Scholar]
  84. Kamoun S., Cooley M. B., Rogowsky P. M., Kado C. I. Two chromosomal loci involved in production of exopolysaccharide in Agrobacterium tumefaciens. J Bacteriol. 1989 Mar;171(3):1755–1759. doi: 10.1128/jb.171.3.1755-1759.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Kanemoto R. H., Powell A. T., Akiyoshi D. E., Regier D. A., Kerstetter R. A., Nester E. W., Hawes M. C., Gordon M. P. Nucleotide sequence and analysis of the plant-inducible locus pinF from Agrobacterium tumefaciens. J Bacteriol. 1989 May;171(5):2506–2512. doi: 10.1128/jb.171.5.2506-2512.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Kennedy M. J. Role of motility, chemotaxis, and adhesion in microbial ecology. Ann N Y Acad Sci. 1987;506:260–273. doi: 10.1111/j.1749-6632.1987.tb23825.x. [DOI] [PubMed] [Google Scholar]
  87. Kingsman A., Willetts N. The requirements for conjugal DNA synthesis in the donor strain during flac transfer. J Mol Biol. 1978 Jul 5;122(3):287–300. doi: 10.1016/0022-2836(78)90191-2. [DOI] [PubMed] [Google Scholar]
  88. Klapwijk P. M., Schilperoort R. A. Negative control of octopine degradation and transfer genes of octopine Ti plasmids in Agrobacterium tumefaciens. J Bacteriol. 1979 Aug;139(2):424–431. doi: 10.1128/jb.139.2.424-431.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Kuhn A., Wickner W., Kreil G. The cytoplasmic carboxy terminus of M13 procoat is required for the membrane insertion of its central domain. Nature. 1986 Jul 24;322(6077):335–339. doi: 10.1038/322335a0. [DOI] [PubMed] [Google Scholar]
  90. Kuldau G. A., De Vos G., Owen J., McCaffrey G., Zambryski P. The virB operon of Agrobacterium tumefaciens pTiC58 encodes 11 open reading frames. Mol Gen Genet. 1990 Apr;221(2):256–266. doi: 10.1007/BF00261729. [DOI] [PubMed] [Google Scholar]
  91. Leake R., Kerr D., Rinaldi F. Steroid hormones and growth factors in breast cancer. Ann N Y Acad Sci. 1990;595:236–241. doi: 10.1111/j.1749-6632.1990.tb34297.x. [DOI] [PubMed] [Google Scholar]
  92. Leemans J., Deblaere R., Willmitzer L., De Greve H., Hernalsteens J. P., Van Montagu M., Schell J. Genetic Identification of functions of TL-DNA transcripts in octopine crown galls. EMBO J. 1982;1(1):147–152. doi: 10.1002/j.1460-2075.1982.tb01138.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Leroux B., Yanofsky M. F., Winans S. C., Ward J. E., Ziegler S. F., Nester E. W. Characterization of the virA locus of Agrobacterium tumefaciens: a transcriptional regulator and host range determinant. EMBO J. 1987 Apr;6(4):849–856. doi: 10.1002/j.1460-2075.1987.tb04830.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Lippincott B. B., Lippincott J. A. Bacterial attachment to a specific wound site as an essential stage in tumor initiation by Agrobacterium tumefaciens. J Bacteriol. 1969 Feb;97(2):620–628. doi: 10.1128/jb.97.2.620-628.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Long S. R. Rhizobium-legume nodulation: life together in the underground. Cell. 1989 Jan 27;56(2):203–214. doi: 10.1016/0092-8674(89)90893-3. [DOI] [PubMed] [Google Scholar]
  96. Machida Y., Sakurai M., Kiyokawa S., Ubasawa A., Suzuki Y., Ikeda J. E. Nucleotide sequence of the insertion sequence found in the T-DNA region of mutant Ti plasmid pTiA66 and distribution of its homologues in octopine Ti plasmid. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7495–7499. doi: 10.1073/pnas.81.23.7495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Manoil C., Beckwith J. A genetic approach to analyzing membrane protein topology. Science. 1986 Sep 26;233(4771):1403–1408. doi: 10.1126/science.3529391. [DOI] [PubMed] [Google Scholar]
  98. Matsumoto S., Ito Y., Hosoi T., Takahashi Y., Machida Y. Integration of Agrobacterium T-DNA into a tobacco chromosome: possible involvement of DNA homology between T-DNA and plant DNA. Mol Gen Genet. 1990 Dec;224(3):309–316. doi: 10.1007/BF00262423. [DOI] [PubMed] [Google Scholar]
  99. Matthysse A. G. Characterization of nonattaching mutants of Agrobacterium tumefaciens. J Bacteriol. 1987 Jan;169(1):313–323. doi: 10.1128/jb.169.1.313-323.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Matthysse A. G. Role of bacterial cellulose fibrils in Agrobacterium tumefaciens infection. J Bacteriol. 1983 May;154(2):906–915. doi: 10.1128/jb.154.2.906-915.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Maurel C., Brevet J., Barbier-Brygoo H., Guern J., Tempé J. Auxin regulates the promoter of the root-inducing rolB gene of Agrobacterium rhizogenes in transgenic tobacco. Mol Gen Genet. 1990 Aug;223(1):58–64. doi: 10.1007/BF00315797. [DOI] [PubMed] [Google Scholar]
  102. Mayerhofer R., Koncz-Kalman Z., Nawrath C., Bakkeren G., Crameri A., Angelis K., Redei G. P., Schell J., Hohn B., Koncz C. T-DNA integration: a mode of illegitimate recombination in plants. EMBO J. 1991 Mar;10(3):697–704. doi: 10.1002/j.1460-2075.1991.tb07999.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. McBride K. E., Knauf V. C. Genetic analysis of the virE operon of the Agrobacterium Ti plasmid pTiA6. J Bacteriol. 1988 Apr;170(4):1430–1437. doi: 10.1128/jb.170.4.1430-1437.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Melchers L. S., Maroney M. J., den Dulk-Ras A., Thompson D. V., van Vuuren H. A., Schilperoort R. A., Hooykaas P. J. Octopine and nopaline strains of Agrobacterium tumefaciens differ in virulence; molecular characterization of the virF locus. Plant Mol Biol. 1990 Feb;14(2):249–259. doi: 10.1007/BF00018565. [DOI] [PubMed] [Google Scholar]
  105. Melchers L. S., Regensburg-Tuïnk A. J., Schilperoort R. A., Hooykaas P. J. Specificity of signal molecules in the activation of Agrobacterium virulence gene expression. Mol Microbiol. 1989 Jul;3(7):969–977. doi: 10.1111/j.1365-2958.1989.tb00246.x. [DOI] [PubMed] [Google Scholar]
  106. Melchers L. S., Regensburg-Tuïnk T. J., Bourret R. B., Sedee N. J., Schilperoort R. A., Hooykaas P. J. Membrane topology and functional analysis of the sensory protein VirA of Agrobacterium tumefaciens. EMBO J. 1989 Jul;8(7):1919–1925. doi: 10.1002/j.1460-2075.1989.tb03595.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Melchers L. S., Thompson D. V., Idler K. B., Schilperoort R. A., Hooykaas P. J. Nucleotide sequence of the virulence gene virG of the Agrobacterium tumefaciens octopine Ti plasmid: significant homology between virG and the regulatory genes ompR, phoB and dye of E. coli. Nucleic Acids Res. 1986 Dec 22;14(24):9933–9942. doi: 10.1093/nar/14.24.9933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Messens E., Dekeyser R., Stachel S. E. A nontransformable Triticum monococcum monocotyledonous culture produces the potent Agrobacterium vir-inducing compound ethyl ferulate. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4368–4372. doi: 10.1073/pnas.87.11.4368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. Miller J. F., Mekalanos J. J., Falkow S. Coordinate regulation and sensory transduction in the control of bacterial virulence. Science. 1989 Feb 17;243(4893):916–922. doi: 10.1126/science.2537530. [DOI] [PubMed] [Google Scholar]
  110. Miller K. J., Kennedy E. P., Reinhold V. N. Osmotic adaptation by gram-negative bacteria: possible role for periplasmic oligosaccharides. Science. 1986 Jan 3;231(4733):48–51. doi: 10.1126/science.3941890. [DOI] [PubMed] [Google Scholar]
  111. Morel P., Powell B. S., Kado C. I. Mise en évidence de trois domaines fonctionnels responsables d'une activité kinase chez VirA, une protéine sensorielle transmembranaire codée par le plasmide Ti d'Agrobacterium tumefaciens. C R Acad Sci III. 1990;310(2):21–26. [PubMed] [Google Scholar]
  112. Morel P., Powell B. S., Rogowsky P. M., Kado C. I. Characterization of the virA virulence gene of the nopaline plasmid, pTiC58, of Agrobacterium tumefaciens. Mol Microbiol. 1989 Sep;3(9):1237–1246. doi: 10.1111/j.1365-2958.1989.tb00274.x. [DOI] [PubMed] [Google Scholar]
  113. Morris J. W., Morris R. O. Identification of an Agrobacterium tumefaciens virulence gene inducer from the pinaceous gymnosperm Pseudotsuga menziesii. Proc Natl Acad Sci U S A. 1990 May;87(9):3614–3618. doi: 10.1073/pnas.87.9.3614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Murphy P. J., Heycke N., Banfalvi Z., Tate M. E., de Bruijn F., Kondorosi A., Tempé J., Schell J. Genes for the catabolism and synthesis of an opine-like compound in Rhizobium meliloti are closely linked and on the Sym plasmid. Proc Natl Acad Sci U S A. 1987 Jan;84(2):493–497. doi: 10.1073/pnas.84.2.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  115. Murphy P. J., Heycke N., Trenz S. P., Ratet P., de Bruijn F. J., Schell J. Synthesis of an opine-like compound, a rhizopine, in alfalfa nodules is symbiotically regulated. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9133–9137. doi: 10.1073/pnas.85.23.9133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Owens L. D., Smigocki A. C. Transformation of Soybean Cells Using Mixed Strains of Agrobacterium tumefaciens and Phenolic Compounds. Plant Physiol. 1988 Nov;88(3):570–573. doi: 10.1104/pp.88.3.570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  117. Parke D., Ornston L. N., Nester E. W. Chemotaxis to plant phenolic inducers of virulence genes is constitutively expressed in the absence of the Ti plasmid in Agrobacterium tumefaciens. J Bacteriol. 1987 Nov;169(11):5336–5338. doi: 10.1128/jb.169.11.5336-5338.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Pazour G. J., Das A. Characterization of the VirG binding site of Agrobacterium tumefaciens. Nucleic Acids Res. 1990 Dec 11;18(23):6909–6913. doi: 10.1093/nar/18.23.6909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. Pazour G. J., Das A. virG, an Agrobacterium tumefaciens transcriptional activator, initiates translation at a UUG codon and is a sequence-specific DNA-binding protein. J Bacteriol. 1990 Mar;172(3):1241–1249. doi: 10.1128/jb.172.3.1241-1249.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Pazour G. J., Ta C. N., Das A. Mutants of Agrobacterium tumefaciens with elevated vir gene expression. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6941–6945. doi: 10.1073/pnas.88.16.6941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Peralta E. G., Hellmiss R., Ream W. Overdrive, a T-DNA transmission enhancer on the A. tumefaciens tumour-inducing plasmid. EMBO J. 1986 Jun;5(6):1137–1142. doi: 10.1002/j.1460-2075.1986.tb04338.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Peralta E. G., Ream L. W. T-DNA border sequences required for crown gall tumorigenesis. Proc Natl Acad Sci U S A. 1985 Aug;82(15):5112–5116. doi: 10.1073/pnas.82.15.5112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  123. Peters N. K., Frost J. W., Long S. R. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science. 1986 Aug 29;233(4767):977–980. doi: 10.1126/science.3738520. [DOI] [PubMed] [Google Scholar]
  124. Powell B. S., Kado C. I. Specific binding of VirG to the vir box requires a C-terminal domain and exhibits a minimum concentration threshold. Mol Microbiol. 1990 Dec;4(12):2159–2166. doi: 10.1111/j.1365-2958.1990.tb00577.x. [DOI] [PubMed] [Google Scholar]
  125. Powell B. S., Powell G. K., Morris R. O., Rogowsky P. M., Kado C. I. Nucleotide sequence of the virG locus of the Agrobacterium tumefaciens plasmid pTiC58. Mol Microbiol. 1987 Nov;1(3):309–316. doi: 10.1111/j.1365-2958.1987.tb01937.x. [DOI] [PubMed] [Google Scholar]
  126. Powell B. S., Rogowsky P. M., Kado C. I. virG of Agrobacterium tumefaciens plasmid pTiC58 encodes a DNA-binding protein. Mol Microbiol. 1989 Mar;3(3):411–419. doi: 10.1111/j.1365-2958.1989.tb00186.x. [DOI] [PubMed] [Google Scholar]
  127. Rathjen F. G., Schachner M. Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J. 1984 Jan;3(1):1–10. doi: 10.1002/j.1460-2075.1984.tb01753.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Regier D. A., Akiyoshi D. E., Gordon M. P. Nucleotide sequence of the tzs gene from Agrobacterium rhizogenes strain A4. Nucleic Acids Res. 1989 Nov 11;17(21):8885–8885. doi: 10.1093/nar/17.21.8885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. Reverchon S., Huang Y., Bourson C., Robert-Baudouy J. Nucleotide sequences of the Erwinia chrysanthemi ogl and pelE genes negatively regulated by the kdgR gene product. Gene. 1989 Dec 21;85(1):125–134. doi: 10.1016/0378-1119(89)90472-1. [DOI] [PubMed] [Google Scholar]
  130. Robinette D., Matthysse A. G. Inhibition by Agrobacterium tumefaciens and Pseudomonas savastanoi of development of the hypersensitive response elicited by Pseudomonas syringae pv. phaseolicola. J Bacteriol. 1990 Oct;172(10):5742–5749. doi: 10.1128/jb.172.10.5742-5749.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. Rodriguez-Palenzuela P., Burr T. J., Collmer A. Polygalacturonase is a virulence factor in Agrobacterium tumefaciens biovar 3. J Bacteriol. 1991 Oct;173(20):6547–6552. doi: 10.1128/jb.173.20.6547-6552.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  132. Rogowsky P. M., Close T. J., Chimera J. A., Shaw J. J., Kado C. I. Regulation of the vir genes of Agrobacterium tumefaciens plasmid pTiC58. J Bacteriol. 1987 Nov;169(11):5101–5112. doi: 10.1128/jb.169.11.5101-5112.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  133. Roitsch T., Wang H., Jin S. G., Nester E. W. Mutational analysis of the VirG protein, a transcriptional activator of Agrobacterium tumefaciens virulence genes. J Bacteriol. 1990 Oct;172(10):6054–6060. doi: 10.1128/jb.172.10.6054-6060.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  134. Rong L., Karcher S. J., O'Neal K., Hawes M. C., Yerkes C. D., Jayaswal R. K., Hallberg C. A., Gelvin S. B. picA, a novel plant-inducible locus on the Agrobacterium tumefaciens chromosome. J Bacteriol. 1990 Oct;172(10):5828–5836. doi: 10.1128/jb.172.10.5828-5836.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  135. Ryder M. H., Tate M. E., Jones G. P. Agrocinopine A, a tumor-inducing plasmid-coded enzyme product, is a phosphodiester of sucrose and L-arabinose. J Biol Chem. 1984 Aug 10;259(15):9704–9710. [PubMed] [Google Scholar]
  136. Sahi S. V., Chilton M. D., Chilton W. S. Corn metabolites affect growth and virulence of Agrobacterium tumefaciens. Proc Natl Acad Sci U S A. 1990 May;87(10):3879–3883. doi: 10.1073/pnas.87.10.3879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Schmülling T., Schell J., Spena A. Single genes from Agrobacterium rhizogenes influence plant development. EMBO J. 1988 Sep;7(9):2621–2629. doi: 10.1002/j.1460-2075.1988.tb03114.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  138. Schröder G., Waffenschmidt S., Weiler E. W., Schröder J. The T-region of Ti plasmids codes for an enzyme synthesizing indole-3-acetic acid. Eur J Biochem. 1984 Jan 16;138(2):387–391. doi: 10.1111/j.1432-1033.1984.tb07927.x. [DOI] [PubMed] [Google Scholar]
  139. Sen P., Pazour G. J., Anderson D., Das A. Cooperative binding of Agrobacterium tumefaciens VirE2 protein to single-stranded DNA. J Bacteriol. 1989 May;171(5):2573–2580. doi: 10.1128/jb.171.5.2573-2580.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  140. Shaw C. H., Ashby A. M., Brown A., Royal C., Loake G. J., Shaw C. H. virA and virG are the Ti-plasmid functions required for chemotaxis of Agrobacterium tumefaciens towards acetosyringone. Mol Microbiol. 1988 May;2(3):413–417. doi: 10.1111/j.1365-2958.1988.tb00046.x. [DOI] [PubMed] [Google Scholar]
  141. Shaw C. H., Watson M. D., Carter G. H., Shaw C. H. The right hand copy of the nopaline Ti-plasmid 25 bp repeat is required for tumour formation. Nucleic Acids Res. 1984 Aug 10;12(15):6031–6041. doi: 10.1093/nar/12.15.6031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  142. Shen W. H., Petit A., Guern J., Tempé J. Hairy roots are more sensitive to auxin than normal roots. Proc Natl Acad Sci U S A. 1988 May;85(10):3417–3421. doi: 10.1073/pnas.85.10.3417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  143. Shimoda N., Toyoda-Yamamoto A., Nagamine J., Usami S., Katayama M., Sakagami Y., Machida Y. Control of expression of Agrobacterium vir genes by synergistic actions of phenolic signal molecules and monosaccharides. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6684–6688. doi: 10.1073/pnas.87.17.6684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  144. Shirasu K., Morel P., Kado C. I. Characterization of the virB operon of an Agrobacterium tumefaciens Ti plasmid: nucleotide sequence and protein analysis. Mol Microbiol. 1990 Jul;4(7):1153–1163. doi: 10.1111/j.1365-2958.1990.tb00690.x. [DOI] [PubMed] [Google Scholar]
  145. Simpson R. B., O'Hara P. J., Kwok W., Montoya A. L., Lichtenstein C., Gordon M. P., Nester E. W. DNA from the A6S/2 crown gall tumor contains scrambled Ti-plasmid sequences near its junctions with plant DNA. Cell. 1982 Jul;29(3):1005–1014. doi: 10.1016/0092-8674(82)90464-0. [DOI] [PubMed] [Google Scholar]
  146. Singh K., Tokuhisa J. G., Dennis E. S., Peacock W. J. Saturation mutagenesis of the octopine synthase enhancer: correlation of mutant phenotypes with binding of a nuclear protein factor. Proc Natl Acad Sci U S A. 1989 May;86(10):3733–3737. doi: 10.1073/pnas.86.10.3733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  147. Sinkar V. P., Pythoud F., White F. F., Nester E. W., Gordon M. P. rolA locus of the Ri plasmid directs developmental abnormalities in transgenic tobacco plants. Genes Dev. 1988 Jun;2(6):688–697. doi: 10.1101/gad.2.6.688. [DOI] [PubMed] [Google Scholar]
  148. Smith E. F., Townsend C. O. A PLANT-TUMOR OF BACTERIAL ORIGIN. Science. 1907 Apr 26;25(643):671–673. doi: 10.1126/science.25.643.671. [DOI] [PubMed] [Google Scholar]
  149. Spanier K., Schell J., Schreier P. H. A functional analysis of T-DNA gene 6b: the fine tuning of cytokinin effects on shoot development. Mol Gen Genet. 1989 Oct;219(1-2):209–216. doi: 10.1007/BF00261179. [DOI] [PubMed] [Google Scholar]
  150. Spena A., Schmülling T., Koncz C., Schell J. S. Independent and synergistic activity of rol A, B and C loci in stimulating abnormal growth in plants. EMBO J. 1987 Dec 20;6(13):3891–3899. doi: 10.1002/j.1460-2075.1987.tb02729.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  151. Stachel S. E., Nester E. W. The genetic and transcriptional organization of the vir region of the A6 Ti plasmid of Agrobacterium tumefaciens. EMBO J. 1986 Jul;5(7):1445–1454. doi: 10.1002/j.1460-2075.1986.tb04381.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  152. Stachel S. E., Nester E. W., Zambryski P. C. A plant cell factor induces Agrobacterium tumefaciens vir gene expression. Proc Natl Acad Sci U S A. 1986 Jan;83(2):379–383. doi: 10.1073/pnas.83.2.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  153. Stachel S. E., Timmerman B., Zambryski P. Activation of Agrobacterium tumefaciens vir gene expression generates multiple single-stranded T-strand molecules from the pTiA6 T-region: requirement for 5' virD gene products. EMBO J. 1987 Apr;6(4):857–863. doi: 10.1002/j.1460-2075.1987.tb04831.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  154. Stachel S. E., Zambryski P. C. Agrobacterium tumefaciens and the susceptible plant cell: a novel adaptation of extracellular recognition and DNA conjugation. Cell. 1986 Oct 24;47(2):155–157. doi: 10.1016/0092-8674(86)90437-x. [DOI] [PubMed] [Google Scholar]
  155. Stachel S. E., Zambryski P. C. Bacteria-yeast conjugation. Generic trans-kingdom sex? Nature. 1989 Jul 20;340(6230):190–191. doi: 10.1038/340190a0. [DOI] [PubMed] [Google Scholar]
  156. Stachel S. E., Zambryski P. C. virA and virG control the plant-induced activation of the T-DNA transfer process of A. tumefaciens. Cell. 1986 Aug 1;46(3):325–333. doi: 10.1016/0092-8674(86)90653-7. [DOI] [PubMed] [Google Scholar]
  157. Steck T. R., Close T. J., Kado C. I. High levels of double-stranded transferred DNA (T-DNA) processing from an intact nopaline Ti plasmid. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2133–2137. doi: 10.1073/pnas.86.7.2133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  158. Steck T. R., Lin T. S., Kado C. I. VirD2 gene product from the nopaline plasmid pTiC58 has at least two activities required for virulence. Nucleic Acids Res. 1990 Dec 11;18(23):6953–6958. doi: 10.1093/nar/18.23.6953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  159. Steck T. R., Morel P., Kado C. I. Vir box sequences in Agrobacterium tumefaciens pTiC58 and A6. Nucleic Acids Res. 1988 Sep 12;16(17):8736–8736. doi: 10.1093/nar/16.17.8736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  160. Stock J. B., Ninfa A. J., Stock A. M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev. 1989 Dec;53(4):450–490. doi: 10.1128/mr.53.4.450-490.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  161. Stout V., Gottesman S. RcsB and RcsC: a two-component regulator of capsule synthesis in Escherichia coli. J Bacteriol. 1990 Feb;172(2):659–669. doi: 10.1128/jb.172.2.659-669.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  162. Tabata S., Hooykaas P. J., Oka A. Sequence determination and characterization of the replicator region in the tumor-inducing plasmid pTiB6S3. J Bacteriol. 1989 Mar;171(3):1665–1672. doi: 10.1128/jb.171.3.1665-1672.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  163. Tamamoto S., Aoyama T., Takanami M., Oka A. Binding of the regulatory protein VirG to the phased signal sequences upstream from virulence genes on the hairy-root-inducing plasmid. J Mol Biol. 1990 Oct 20;215(4):537–547. doi: 10.1016/S0022-2836(05)80166-4. [DOI] [PubMed] [Google Scholar]
  164. Thomashow L. S., Reeves S., Thomashow M. F. 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 U S A. 1984 Aug;81(16):5071–5075. doi: 10.1073/pnas.81.16.5071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  165. Thomashow M. F., Nutter R., Montoya A. L., Gordon M. P., Nester E. W. Integration and organization of Ti plasmid sequences in crown gall tumors. Cell. 1980 Mar;19(3):729–739. doi: 10.1016/s0092-8674(80)80049-3. [DOI] [PubMed] [Google Scholar]
  166. Thompson D. V., Melchers L. S., Idler K. B., Schilperoort R. A., Hooykaas P. J. Analysis of the complete nucleotide sequence of the Agrobacterium tumefaciens virB operon. Nucleic Acids Res. 1988 May 25;16(10):4621–4636. doi: 10.1093/nar/16.10.4621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  167. Timmerman B., Van Montagu M., Zambryski P. vir-induced recombination in Agrobacterium. Physical characterization of precise and imprecise T-circle formation. J Mol Biol. 1988 Sep 20;203(2):373–384. doi: 10.1016/0022-2836(88)90005-8. [DOI] [PubMed] [Google Scholar]
  168. Tomkinson A. E., Totty N. F., Ginsburg M., Lindahl T. Location of the active site for enzyme-adenylate formation in DNA ligases. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):400–404. doi: 10.1073/pnas.88.2.400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  169. Toro N., Datta A., Carmi O. A., Young C., Prusti R. K., Nester E. W. The Agrobacterium tumefaciens virC1 gene product binds to overdrive, a T-DNA transfer enhancer. J Bacteriol. 1989 Dec;171(12):6845–6849. doi: 10.1128/jb.171.12.6845-6849.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  170. Toro N., Datta A., Yanofsky M., Nester E. Role of the overdrive sequence in T-DNA border cleavage in Agrobacterium. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8558–8562. doi: 10.1073/pnas.85.22.8558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  171. Usami S., Okamoto S., Takebe I., Machida Y. Factor inducing Agrobacterium tumefaciens vir gene expression is present in monocotyledonous plants. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3748–3752. doi: 10.1073/pnas.85.11.3748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  172. Usami S, Morikawa S, Takebe I, Machida Y. Absence in monocotyledonous plants of the diffusible plant factors inducing T-DNA circularization and vir gene expression in Agrobacterium. Mol Gen Genet. 1987 Sep;209(2):221–226. doi: 10.1007/BF00329646. [DOI] [PubMed] [Google Scholar]
  173. Valdivia R. H., Wang L., Winans S. C. Characterization of a putative periplasmic transport system for octopine accumulation encoded by Agrobacterium tumefaciens Ti plasmid pTiA6. J Bacteriol. 1991 Oct;173(20):6398–6405. doi: 10.1128/jb.173.20.6398-6405.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  174. Veluthambi K., Jayaswal R. K., Gelvin S. B. Virulence genes A, G, and D mediate the double-stranded border cleavage of T-DNA from the Agrobacterium Ti plasmid. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1881–1885. doi: 10.1073/pnas.84.7.1881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  175. Veluthambi K., Krishnan M., Gould J. H., Smith R. H., Gelvin S. B. Opines stimulate induction of the vir genes of the Agrobacterium tumefaciens Ti plasmid. J Bacteriol. 1989 Jul;171(7):3696–3703. doi: 10.1128/jb.171.7.3696-3703.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  176. Vernade D., Herrera-Estrella A., Wang K., Van Montagu M. Glycine betaine allows enhanced induction of the Agrobacterium tumefaciens vir genes by acetosyringone at low pH. J Bacteriol. 1988 Dec;170(12):5822–5829. doi: 10.1128/jb.170.12.5822-5829.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  177. Virts E. L., Gelvin S. B. Analysis of transfer of tumor-inducing plasmids from Agrobacterium tumefaciens to Petunia protoplasts. J Bacteriol. 1985 Jun;162(3):1030–1038. doi: 10.1128/jb.162.3.1030-1038.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  178. Wang K., Herrera-Estrella A., Van Montagu M. Overexpression of virD1 and virD2 genes in Agrobacterium tumefaciens enhances T-complex formation and plant transformation. J Bacteriol. 1990 Aug;172(8):4432–4440. doi: 10.1128/jb.172.8.4432-4440.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  179. Wang K., Stachel S. E., Timmerman B., VAN Montagu M., Zambryski P. C. Site-Specific Nick in the T-DNA Border Sequence as a Result of Agrobacterium vir Gene Expression. Science. 1987 Jan 30;235(4788):587–591. doi: 10.1126/science.235.4788.587. [DOI] [PubMed] [Google Scholar]
  180. Ward J. E., Akiyoshi D. E., Regier D., Datta A., Gordon M. P., Nester E. W. Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid. J Biol Chem. 1988 Apr 25;263(12):5804–5814. [PubMed] [Google Scholar]
  181. Ward J. E., Akiyoshi D. E., Regier D., Datta A., Gordon M. P., Nester E. W. Correction: characterization of the virB operon from Agrobacterium tumefaciens Ti plasmid. J Biol Chem. 1990 Mar 15;265(8):4768–4768. [PubMed] [Google Scholar]
  182. Ward J. E., Jr, Dale E. M., Christie P. J., Nester E. W., Binns A. N. Complementation analysis of Agrobacterium tumefaciens Ti plasmid virB genes by use of a vir promoter expression vector: virB9, virB10, and virB11 are essential virulence genes. J Bacteriol. 1990 Sep;172(9):5187–5199. doi: 10.1128/jb.172.9.5187-5199.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  183. Waters V. L., Hirata K. H., Pansegrau W., Lanka E., Guiney D. G. Sequence identity in the nick regions of IncP plasmid transfer origins and T-DNA borders of Agrobacterium Ti plasmids. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1456–1460. doi: 10.1073/pnas.88.4.1456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  184. Weising K., Schell J., Kahl G. Foreign genes in plants: transfer, structure, expression, and applications. Annu Rev Genet. 1988;22:421–477. doi: 10.1146/annurev.ge.22.120188.002225. [DOI] [PubMed] [Google Scholar]
  185. White F. F., Nester E. W. Hairy root: plasmid encodes virulence traits in Agrobacterium rhizogenes. J Bacteriol. 1980 Mar;141(3):1134–1141. doi: 10.1128/jb.141.3.1134-1141.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  186. Willmitzer L., Schmalenbach W., Schell J. Transcription of T-DNA in octopine and nopaline crown gall tumours is inhibited by low concentrations of alpha-amanitin. Nucleic Acids Res. 1981 Oct 10;9(19):4801–4812. doi: 10.1093/nar/9.19.4801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  187. Winans S. C., Allenza P., Stachel S. E., McBride K. E., Nester E. W. Characterization of the virE operon of the Agrobacterium Ti plasmid pTiA6. Nucleic Acids Res. 1987 Jan 26;15(2):825–837. doi: 10.1093/nar/15.2.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  188. Winans S. C. An Agrobacterium two-component regulatory system for the detection of chemicals released from plant wounds. Mol Microbiol. 1991 Oct;5(10):2345–2350. doi: 10.1111/j.1365-2958.1991.tb02080.x. [DOI] [PubMed] [Google Scholar]
  189. Winans S. C., Ebert P. R., Stachel S. E., Gordon M. P., Nester E. W. A gene essential for Agrobacterium virulence is homologous to a family of positive regulatory loci. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8278–8282. doi: 10.1073/pnas.83.21.8278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  190. Winans S. C., Kerstetter R. A., Nester E. W. Transcriptional regulation of the virA and virG genes of Agrobacterium tumefaciens. J Bacteriol. 1988 Sep;170(9):4047–4054. doi: 10.1128/jb.170.9.4047-4054.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  191. Winans S. C., Kerstetter R. A., Ward J. E., Nester E. W. A protein required for transcriptional regulation of Agrobacterium virulence genes spans the cytoplasmic membrane. J Bacteriol. 1989 Mar;171(3):1616–1622. doi: 10.1128/jb.171.3.1616-1622.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  192. Winans S. C. Transcriptional induction of an Agrobacterium regulatory gene at tandem promoters by plant-released phenolic compounds, phosphate starvation, and acidic growth media. J Bacteriol. 1990 May;172(5):2433–2438. doi: 10.1128/jb.172.5.2433-2438.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  193. Winans S. C., Walker G. C. Conjugal transfer system of the IncN plasmid pKM101. J Bacteriol. 1985 Jan;161(1):402–410. doi: 10.1128/jb.161.1.402-410.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  194. Yadav N. S., Vanderleyden J., Bennett D. R., Barnes W. M., Chilton M. D. Short direct repeats flank the T-DNA on a nopaline Ti plasmid. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6322–6326. doi: 10.1073/pnas.79.20.6322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  195. Yanofsky M. F., Nester E. W. Molecular characterization of a host-range-determining locus from Agrobacterium tumefaciens. J Bacteriol. 1986 Oct;168(1):244–250. doi: 10.1128/jb.168.1.244-250.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  196. Yanofsky M. F., Porter S. G., Young C., Albright L. M., Gordon M. P., Nester E. W. The virD operon of Agrobacterium tumefaciens encodes a site-specific endonuclease. Cell. 1986 Nov 7;47(3):471–477. doi: 10.1016/0092-8674(86)90604-5. [DOI] [PubMed] [Google Scholar]
  197. Young C., Nester E. W. Association of the virD2 protein with the 5' end of T strands in Agrobacterium tumefaciens. J Bacteriol. 1988 Aug;170(8):3367–3374. doi: 10.1128/jb.170.8.3367-3374.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  198. Zambryski P. Basic processes underlying Agrobacterium-mediated DNA transfer to plant cells. Annu Rev Genet. 1988;22:1–30. doi: 10.1146/annurev.ge.22.120188.000245. [DOI] [PubMed] [Google Scholar]
  199. Zambryski P., Depicker A., Kruger K., Goodman H. M. Tumor induction by Agrobacterium tumefaciens: analysis of the boundaries of T-DNA. J Mol Appl Genet. 1982;1(4):361–370. [PubMed] [Google Scholar]
  200. Zambryski P., Tempe J., Schell J. Transfer and function of T-DNA genes from agrobacterium Ti and Ri plasmids in plants. Cell. 1989 Jan 27;56(2):193–201. doi: 10.1016/0092-8674(89)90892-1. [DOI] [PubMed] [Google Scholar]
  201. Zorreguieta A., Ugalde R. A. Formation in Rhizobium and Agrobacterium spp. of a 235-kilodalton protein intermediate in beta-D(1-2) glucan synthesis. J Bacteriol. 1986 Sep;167(3):947–951. doi: 10.1128/jb.167.3.947-951.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  202. de Iannino N. I., Ugalde R. A. Biochemical characterization of avirulent Agrobacterium tumefaciens chvA mutants: synthesis and excretion of beta-(1-2)glucan. J Bacteriol. 1989 May;171(5):2842–2849. doi: 10.1128/jb.171.5.2842-2849.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  203. von Lintig J., Zanker H., Schröder J. Positive regulators of opine-inducible promoters in the nopaline and octopine catabolism regions of Ti plasmids. Mol Plant Microbe Interact. 1991 Jul-Aug;4(4):370–378. doi: 10.1094/mpmi-4-370. [DOI] [PubMed] [Google Scholar]

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