Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 Sep;177(17):4963–4968. doi: 10.1128/jb.177.17.4963-4968.1995

Intragenic recombination of a single plant pathogen gene provides a mechanism for the evolution of new host specificities.

Y Yang 1, D W Gabriel 1
PMCID: PMC177271  PMID: 7665472

Abstract

Gene pthA is required for virulence of Xanthomonas citri on citrus plants and has pleiotropic pathogenicity and avirulence functions when transferred to many different xanthomonads. DNA sequencing revealed that pthA belongs to a family of Xanthomonas avirulence/pathogenicity genes characterized by nearly identical 102-bp tandem repeats in the central region. By inserting an nptI-sac cartridge into the tandemly repeated region of pthA as a selective marker, intragenic recombination among homologous repeats was observed in both Xanthomonas spp. and Escherichia coli. Intragenic recombination within pthA created new genes with novel host specificities and altered pathogenicity and/or avirulence phenotypes. Many pthA recombinants gained or lost avirulence function in pathogenicity assays on bean, citrus, and cotton cultivars. Although the ability to induce cell division (hyperplastic cankers) on citrus could be lost, this ability was not acquired on cotton or bean plants. Intragenic recombination therefore provides a genetic mechanism for the generation of multiple, different, and gratuitous avirulence genes from a single, required, host-specific pathogenicity gene.

Full Text

The Full Text of this article is available as a PDF (372.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albertini A. M., Hofer M., Calos M. P., Miller J. H. On the formation of spontaneous deletions: the importance of short sequence homologies in the generation of large deletions. Cell. 1982 Jun;29(2):319–328. doi: 10.1016/0092-8674(82)90148-9. [DOI] [PubMed] [Google Scholar]
  2. Bonas U., Conrads-Strauch J., Balbo I. Resistance in tomato to Xanthomonas campestris pv vesicatoria is determined by alleles of the pepper-specific avirulence gene avrBs3. Mol Gen Genet. 1993 Apr;238(1-2):261–269. doi: 10.1007/BF00279555. [DOI] [PubMed] [Google Scholar]
  3. Bonas U., Stall R. E., Staskawicz B. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol Gen Genet. 1989 Jul;218(1):127–136. doi: 10.1007/BF00330575. [DOI] [PubMed] [Google Scholar]
  4. Dangl J. L. Pièce de Résistance: novel classes of plant disease resistance genes. Cell. 1995 Feb 10;80(3):363–366. doi: 10.1016/0092-8674(95)90485-9. [DOI] [PubMed] [Google Scholar]
  5. De Feyter R., Gabriel D. W. Use of cloned DNA methylase genes to increase the frequency of transfer of foreign genes into Xanthomonas campestris pv. malvacearum. J Bacteriol. 1991 Oct;173(20):6421–6427. doi: 10.1128/jb.173.20.6421-6427.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. De Feyter R., Yang Y., Gabriel D. W. Gene-for-genes interactions between cotton R genes and Xanthomonas campestris pv. malvacearum avr genes. Mol Plant Microbe Interact. 1993 Mar-Apr;6(2):225–237. doi: 10.1094/mpmi-6-225. [DOI] [PubMed] [Google Scholar]
  7. DeFeyter R., Kado C. I., Gabriel D. W. Small, stable shuttle vectors for use in Xanthomonas. Gene. 1990 Mar 30;88(1):65–72. doi: 10.1016/0378-1119(90)90060-5. [DOI] [PubMed] [Google Scholar]
  8. Dickinson M. J., Jones D. A., Jones J. D. Close linkage between the Cf-2/Cf-5 and Mi resistance loci in tomato. Mol Plant Microbe Interact. 1993 May-Jun;6(3):341–347. doi: 10.1094/mpmi-6-341. [DOI] [PubMed] [Google Scholar]
  9. Goebl M., Yanagida M. The TPR snap helix: a novel protein repeat motif from mitosis to transcription. Trends Biochem Sci. 1991 May;16(5):173–177. doi: 10.1016/0968-0004(91)90070-c. [DOI] [PubMed] [Google Scholar]
  10. Hopkins C. M., White F. F., Choi S. H., Guo A., Leach J. E. Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact. 1992 Nov-Dec;5(6):451–459. doi: 10.1094/mpmi-5-451. [DOI] [PubMed] [Google Scholar]
  11. Joosten M. H., Cozijnsen T. J., De Wit P. J. Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature. 1994 Jan 27;367(6461):384–386. doi: 10.1038/367384a0. [DOI] [PubMed] [Google Scholar]
  12. Keen N. T. Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet. 1990;24:447–463. doi: 10.1146/annurev.ge.24.120190.002311. [DOI] [PubMed] [Google Scholar]
  13. Knoop V., Staskawicz B., Bonas U. Expression of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria is not under the control of hrp genes and is independent of plant factors. J Bacteriol. 1991 Nov;173(22):7142–7150. doi: 10.1128/jb.173.22.7142-7150.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kobayashi D. Y., Tamaki S. J., Trollinger D. J., Gold S., Keen N. T. A gene from Pseudomonas syringae pv. glycinea with homology to avirulence gene D from P. s. pv. tomato but devoid of the avirulence phenotype. Mol Plant Microbe Interact. 1990 Mar-Apr;3(2):103–111. doi: 10.1094/mpmi-3-103. [DOI] [PubMed] [Google Scholar]
  15. Martin G. B., Brommonschenkel S. H., Chunwongse J., Frary A., Ganal M. W., Spivey R., Wu T., Earle E. D., Tanksley S. D. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science. 1993 Nov 26;262(5138):1432–1436. doi: 10.1126/science.7902614. [DOI] [PubMed] [Google Scholar]
  16. Petes T. D., Hill C. W. Recombination between repeated genes in microorganisms. Annu Rev Genet. 1988;22:147–168. doi: 10.1146/annurev.ge.22.120188.001051. [DOI] [PubMed] [Google Scholar]
  17. Ried J. L., Collmer A. An nptI-sacB-sacR cartridge for constructing directed, unmarked mutations in gram-negative bacteria by marker exchange-eviction mutagenesis. Gene. 1987;57(2-3):239–246. doi: 10.1016/0378-1119(87)90127-2. [DOI] [PubMed] [Google Scholar]
  18. Sikorski R. S., Boguski M. S., Goebl M., Hieter P. A repeating amino acid motif in CDC23 defines a family of proteins and a new relationship among genes required for mitosis and RNA synthesis. Cell. 1990 Jan 26;60(2):307–317. doi: 10.1016/0092-8674(90)90745-z. [DOI] [PubMed] [Google Scholar]
  19. Staskawicz B. J., Ausubel F. M., Baker B. J., Ellis J. G., Jones J. D. Molecular genetics of plant disease resistance. Science. 1995 May 5;268(5211):661–667. doi: 10.1126/science.7732374. [DOI] [PubMed] [Google Scholar]
  20. Swarup S., Yang Y., Kingsley M. T., Gabriel D. W. An Xanthomonas citri pathogenicity gene, pthA, pleiotropically encodes gratuitous avirulence on nonhosts. Mol Plant Microbe Interact. 1992 May-Jun;5(3):204–213. doi: 10.1094/mpmi-5-204. [DOI] [PubMed] [Google Scholar]
  21. Wren B. W. A family of clostridial and streptococcal ligand-binding proteins with conserved C-terminal repeat sequences. Mol Microbiol. 1991 Apr;5(4):797–803. doi: 10.1111/j.1365-2958.1991.tb00752.x. [DOI] [PubMed] [Google Scholar]
  22. Xu B. W., Paszty C., Lurquin P. F. A plasmid-based method to quantitate homologous recombination frequencies in gram-negative bacteria. Biotechniques. 1988 Sep;6(8):752–760. [PubMed] [Google Scholar]
  23. 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]
  24. van der Voorn L., Ploegh H. L. The WD-40 repeat. FEBS Lett. 1992 Jul 28;307(2):131–134. doi: 10.1016/0014-5793(92)80751-2. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES