Fasciation induction by the phytopathogen Rhodococcus fascians depends upon a linear plasmid encoding a cytokinin synthase gene (original) (raw)
Abstract
Rhodococcus fascians is a nocardiform bacteria that induces leafy galls (fasciation) on dicotyledonous and several monocotyledonous plants. The wild-type strain D188 contained a conjugative, 200 kb linear extrachromosomal element, pFiD188. Linear plasmid-cured strains were avirulent and reintroduction of this linear element restored virulence. Pulsed field electrophoresis indicated that the chromosome might also be a linear molecule of 4 megabases. Three loci involved in phytopathogenicity have been identified by insertion mutagenesis of this Fi plasmid. Inactivation of the fas locus resulted in avirulent strains, whereas insertions in the two other loci affected the degree of virulence, yielding attenuated (att) and hypervirulent (hyp) bacteria. One of the genes within the fas locus encoded an isopentenyltranferase (IPT) with low homology to analogous proteins from Gram-negative phytopathogenic bacteria. IPT activity was detected after expression of this protein in Escherichia coli cells. In R.fascians, ipt expression could only be detected in bacteria induced with extracts from fasciated tissue. R.fascians strains without the linear plasmid but containing this fas locus alone could not provoke any phenotype on plants, indicating additional genes from the linear plasmid were also essential for virulence. These studies, the first genetic analysis of the interaction of a Gram-positive bacterium with plants, suggest that a novel mechanism for plant tumour induction has evolved in R.fascians independently from the other branches of the eubacteria.
Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Akiyoshi D. E., Regier D. A., Gordon M. P. Cytokinin production by Agrobacterium and Pseudomonas spp. J Bacteriol. 1987 Sep;169(9):4242–4248. doi: 10.1128/jb.169.9.4242-4248.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Akiyoshi D. E., Regier D. A., Gordon M. P. Nucleotide sequence of the tzs gene from Pseudomonas solanacearum strain K60. Nucleic Acids Res. 1989 Nov 11;17(21):8886–8886. doi: 10.1093/nar/17.21.8886. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Akiyoshi D. E., Regier D. A., Jen G., Gordon M. P. Cloning and nucleotide sequence of the tzs gene from Agrobacterium tumefaciens strain T37. Nucleic Acids Res. 1985 Apr 25;13(8):2773–2788. doi: 10.1093/nar/13.8.2773. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barbour A. G., Garon C. F. Linear plasmids of the bacterium Borrelia burgdorferi have covalently closed ends. Science. 1987 Jul 24;237(4813):409–411. doi: 10.1126/science.3603026. [DOI] [PubMed] [Google Scholar]
- Barry G. F., Rogers S. G., Fraley R. T., Brand L. Identification of a cloned cytokinin biosynthetic gene. Proc Natl Acad Sci U S A. 1984 Aug;81(15):4776–4780. doi: 10.1073/pnas.81.15.4776. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Botterman J., Zabeau M. A standardized vector system for manipulation and enhanced expression of genes in Escherichia coli. DNA. 1987 Dec;6(6):583–591. doi: 10.1089/dna.1987.6.583. [DOI] [PubMed] [Google Scholar]
- Brutlag D. L., Dautricourt J. P., Maulik S., Relph J. Improved sensitivity of biological sequence database searches. Comput Appl Biosci. 1990 Jul;6(3):237–245. doi: 10.1093/bioinformatics/6.3.237. [DOI] [PubMed] [Google Scholar]
- Casadaban M. J., Cohen S. N. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol. 1980 Apr;138(2):179–207. doi: 10.1016/0022-2836(80)90283-1. [DOI] [PubMed] [Google Scholar]
- Chu G., Vollrath D., Davis R. W. Separation of large DNA molecules by contour-clamped homogeneous electric fields. Science. 1986 Dec 19;234(4783):1582–1585. doi: 10.1126/science.3538420. [DOI] [PubMed] [Google Scholar]
- Desomer J., Crespi M., Van Montagu M. Illegitimate integration of non-replicative vectors in the genome of Rhodococcus fascians upon electrotransformation as an insertional mutagenesis system. Mol Microbiol. 1991 Sep;5(9):2115–2124. doi: 10.1111/j.1365-2958.1991.tb02141.x. [DOI] [PubMed] [Google Scholar]
- Desomer J., Dhaese P., Montagu M. V. Transformation of Rhodococcus fascians by High-Voltage Electroporation and Development of R. fascians Cloning Vectors. Appl Environ Microbiol. 1990 Sep;56(9):2818–2825. doi: 10.1128/aem.56.9.2818-2825.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Desomer J., Dhaese P., Van Montagu M. Conjugative transfer of cadmium resistance plasmids in Rhodococcus fascians strains. J Bacteriol. 1988 May;170(5):2401–2405. doi: 10.1128/jb.170.5.2401-2405.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ferdows M. S., Barbour A. G. Megabase-sized linear DNA in the bacterium Borrelia burgdorferi, the Lyme disease agent. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5969–5973. doi: 10.1073/pnas.86.15.5969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldberg S. B., Flick J. S., Rogers S. G. Nucleotide sequence of the tmr locus of Agrobacterium tumefaciens pTi T37 T-DNA. Nucleic Acids Res. 1984 Jun 11;12(11):4665–4677. doi: 10.1093/nar/12.11.4665. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983 Jun 5;166(4):557–580. doi: 10.1016/s0022-2836(83)80284-8. [DOI] [PubMed] [Google Scholar]
- Heidekamp F., Dirkse W. G., Hille J., van Ormondt H. Nucleotide sequence of the Agrobacterium tumefaciens octopine Ti plasmid-encoded tmr gene. Nucleic Acids Res. 1983 Sep 24;11(18):6211–6223. doi: 10.1093/nar/11.18.6211. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kalkus J., Reh M., Schlegel H. G. Hydrogen autotrophy of Nocardia opaca strains is encoded by linear megaplasmids. J Gen Microbiol. 1990 Jun;136(6):1145–1151. doi: 10.1099/00221287-136-6-1145. [DOI] [PubMed] [Google Scholar]
- Kinashi H., Shimaji M., Sakai A. Giant linear plasmids in Streptomyces which code for antibiotic biosynthesis genes. 1987 Jul 30-Aug 5Nature. 328(6129):454–456. doi: 10.1038/328454a0. [DOI] [PubMed] [Google Scholar]
- Klämbt D., Thies G., Skoog F. Isolation of cytokinins from Corynebacterium fascians. Proc Natl Acad Sci U S A. 1966 Jul;56(1):52–59. doi: 10.1073/pnas.56.1.52. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Lerouge P., Roche P., Faucher C., Maillet F., Truchet G., Promé J. C., Dénarié J. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature. 1990 Apr 19;344(6268):781–784. doi: 10.1038/344781a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Macdonald E. M., Powell G. K., Regier D. A., Glass N. L., Roberto F., Kosuge T., Morris R. O. Secretion of Zeatin, Ribosylzeatin, and Ribosyl-1'' -Methylzeatin by Pseudomonas savastanoi: Plasmid-Coded Cytokinin Biosynthesis. Plant Physiol. 1986 Nov;82(3):742–747. doi: 10.1104/pp.82.3.742. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meinhardt F., Kempken F., Kämper J., Esser K. Linear plasmids among eukaryotes: fundamentals and application. Curr Genet. 1990 Feb;17(2):89–95. doi: 10.1007/BF00312851. [DOI] [PubMed] [Google Scholar]
- Murai N., Skoog F., Doyle M. E., Hanson R. S. Relationships between cytokinin production, presence of plasmids, and fasciation caused by strains of Corynebacterium fascians. Proc Natl Acad Sci U S A. 1980 Jan;77(1):619–623. doi: 10.1073/pnas.77.1.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
- O'Donnell M. J., Rowe B. R., Lawson N., Horton A., Gyde O. H., Barnett A. H. Placebo-controlled trial of lisinopril in normotensive diabetic patients with incipient nephropathy. J Hum Hypertens. 1993 Aug;7(4):327–332. [PubMed] [Google Scholar]
- Powell G. K., Hommes N. G., Kuo J., Castle L. A., Morris R. O. Inducible expression of cytokinin biosynthesis in Agrobacterium tumefaciens by plant phenolics. Mol Plant Microbe Interact. 1988 Jul-Aug;1(6):235–242. doi: 10.1094/mpmi-1-235. [DOI] [PubMed] [Google Scholar]
- Powell G. K., Morris R. O. Nucleotide sequence and expression of a Pseudomonas savastanoi cytokinin biosynthetic gene: homology with Agrobacterium tumefaciens tmr and tzs loci. Nucleic Acids Res. 1986 Mar 25;14(6):2555–2565. doi: 10.1093/nar/14.6.2555. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Romano C. P., Hein M. B., Klee H. J. Inactivation of auxin in tobacco transformed with the indoleacetic acid-lysine synthetase gene of Pseudomonas savastanoi. Genes Dev. 1991 Mar;5(3):438–446. doi: 10.1101/gad.5.3.438. [DOI] [PubMed] [Google Scholar]
- Sakaguchi K. Invertrons, a class of structurally and functionally related genetic elements that includes linear DNA plasmids, transposable elements, and genomes of adeno-type viruses. Microbiol Rev. 1990 Mar;54(1):66–74. doi: 10.1128/mr.54.1.66-74.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scarbrough E., Armstrong D. J., Skoog F., Frihart C. R., Leonard N. J. Isolation of cis-Zeatin from Corynebacterium fascians Cultures. Proc Natl Acad Sci U S A. 1973 Dec;70(12 Pt 1-2):3825–3829. doi: 10.1073/pnas.70.12.3825. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Van Kaer L., Van Montagu M., Dhaese P. Transcriptional control in the EcoRI-F immunity region of Bacillus subtilis phage phi 105. Identification and unusual structure of the operator. J Mol Biol. 1987 Sep 5;197(1):55–67. doi: 10.1016/0022-2836(87)90609-7. [DOI] [PubMed] [Google Scholar]
- Van Larebeke N., Genetello C., Schell J., Schilperoort R. A., Hermans A. K., Van Montagu M., Hernalsteens J. P. Acquisition of tumour-inducing ability by non-oncogenic agrobacteria as a result of plasmid transfer. Nature. 1975 Jun 26;255(5511):742–743. doi: 10.1038/255742a0. [DOI] [PubMed] [Google Scholar]
- Vervliet G., Holsters M., Teuchy H., Van Montagu M., Schell J. Characterization of different plaque-forming and defective temperate phages in Agrobacterium. J Gen Virol. 1975 Jan;26(1):33–48. doi: 10.1099/0022-1317-26-1-33. [DOI] [PubMed] [Google Scholar]
- White F. F., Taylor B. H., Huffman G. A., Gordon M. P., Nester E. W. Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes. J Bacteriol. 1985 Oct;164(1):33–44. doi: 10.1128/jb.164.1.33-44.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
- 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]