Skip to main content
Log in

Opine biosynthesis and catabolism genes of Agrobacterium tumefaciens and Agrobacterium rhizogenes

  • Reviews and Theoretical Articles
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

Agrobacterium is a genus of soil bacteria with the ability to transform plant cells by a T-DNA-sequence located on the pTi/pRi-plasmid containing a set of genes expressed in plant cells. Expression of these genes leads to a proliferation of transformed cells, with the subsequent formation of tumors or growths of roots and the synthesis of opines—products of the condensation of amino acids with ketoacids or sugars used by agrobacteria as a source of carbon and nitrogen. In this review, we systematized the information about most common opines in plant-Agrobacterium systems and their biosynthesis and catabolism genes, as well as the role of opines in the interaction of pathogenic Agrobacterium with plants and with other Agrobacterium strains, including the genetic consequences of such interactions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Sawada, H., Ieki, H., Oyaizu, H., and Matsumoto, S., Proposal for rejection of Agrobacterium tumefaciens and revised descriptions for the genus Agrobacterium and for Agrobacterium radiobacter and Agrobacterium rhizogenes, Int. J. Syst. Bacteriol., 1993, vol. 43, no. 4, pp. 694–702.

    Article  CAS  PubMed  Google Scholar 

  2. Storozhenko, E.M., Bolezni plodovykh kul’tur i vinograda (Diseases of Fruit Crops and Grapes), Krasnodar: Krasnodarskoe Knizhnoe Izd., 1970.

    Google Scholar 

  3. Lanak, Ya., Shimko, K., and Vanek, G., Atlas boleznei i vreditelei plodovykh, yagodnykh, ovoshchnykh kul’tur i vinograda (Atlas of Diseases and Pests of Fruits, Berries, Vegetables and Grapes), Bratislava: Priroda, 1972.

    Google Scholar 

  4. Khokhryakov, M.K., Potlaichuk, V.I., and Semenov, A.Ya., Opredelitel’ boleznei sel’skokhozyaistvennykh kul’tur (The Key to Crop Diseases), Leningrad: Kolos, 1984.

    Google Scholar 

  5. Dessaux, Y., Petit, A., and Tempé, J., Chemistry and biochemistry of opines, chemical mediators of parasitism, Phytochemistry, 1993, vol. 34, no. 1, pp. 31–38.

    Article  CAS  Google Scholar 

  6. Petit, A., David, C., Dahl, G.A., et al., Further extension of the opine concept: plasmids in Agrobacterium rhizogenes cooperate for opine degradation, Mol. Gen. Genet., 1983, no. 190, pp. 204–214.

    Google Scholar 

  7. Schell, J. and Tempé, J., Is crown gall a natural instance of gene transfer?, in Translation of Natural and Synthetic Polynucleotides, Legocki, A.B., Ed., New York: Elsevier, 1978, pp. 416–420.

    Google Scholar 

  8. Schell, J., Van Montagu, M., Beuckeleer, M., et al., Interaction and DNA transfer between Agrobacterium tumefaciens, the Ti-plasmid and the plant host, Proc. R. Soc. London, Ser. B, 1979, vol. 204, no. 155, pp. 251–266.

    Article  CAS  Google Scholar 

  9. Otten, L., Ti Plasmids, Chichester: Wiley, 2001, pp. 353–361.

    Google Scholar 

  10. Guyon, P., Chilton, M.-D., Petit, A., et al., Agropine in “null-type” crown gall tumors: evidence for generality of the opine concept, Proc. Natl. Acad. Sci. U.S.A., 1980, vol. 77, no. 5, pp. 2693–2697.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Chilton, W.S., Tempé, J., Matzke, M., et al., Succinamopine: a new crown gall opine, J. Bacteriol., 1984, vol. 157, no. 2, pp. 357–362.

    PubMed Central  CAS  PubMed  Google Scholar 

  12. Spaink, H.P., Kondorosi, A., and Hooykaas, P., The Rhizobiaceae-Molecular Biology of Model Plant-Associated Bacteria, Dordrecht: Kluwer, 1998.

    Google Scholar 

  13. Palanichelvam, K., Oger, P., Clough, S.J., et al., A second T-region of the soybean-supervirulent chrysopinetype Ti plasmid pTiChry5, and construction of a fully disarmed vir helper plasmid, Mol. Plant-Microbe Interact., 2000, vol. 13, no. 10, pp. 1081–1091.

    Article  CAS  PubMed  Google Scholar 

  14. Otten, L. and Schmidt, J., A T-DNA from the Agrobacterium tumefaciens limited-host-range strain AB2/73 contains a single oncogene, Mol. Plant-Microbe Interact., 1998, vol. 11, no. 5, pp. 335–342.

    Article  CAS  PubMed  Google Scholar 

  15. Oger, P. and Farrand, S.K., Co-evolution of the agrocinopine opines and the agrocinopine-mediated control of TraR, the quorum sensing activator of the Ti plasmid conjugation system, Mol. Microbiol., 2001, vol. 41, no. 5, pp. 1173–1185.

    Article  CAS  PubMed  Google Scholar 

  16. Pimentel, D., CRC Handbook of Pest Management in Agriculture, Boca Raton, FL: CRC Press, 1991, vol. 2, 2nd ed, pp. 311–329.

    Google Scholar 

  17. Mccardell, B.A. and Pootjes, C.F., Chemical nature of agrocin 84 and its effect on a virulent strain of Agrobacterium tumefaciens, Antimicrob. Agents Chemother., 1976, vol. 10, no. 3, pp. 498–502.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Murphy, P.J. and Roberts, W.P., A basis for agrocin 84 sensitivity in Agrobacterium radiobacter, J. Gen. Microbiol., 1979, no. 114, pp. 207–213.

    Google Scholar 

  19. Aoki, S., Kawaoka, A., Sekine, M., Ichikawa, T., et al., Sequence of the cellular T-DNA in the untransformed genome of Nicotiana glauca that is homologous to ORFs 13 and 14 of the Ri plasmid and analysis of its expression in genetic tumors of N. glauca × N. langsdorffii, Mol. Gen. Genet., 1996, vol. 243, no. 6, pp. 706–710.

    Google Scholar 

  20. Suzuki, K., Yamashita, I., and Tanaka, N., Tobacco plants were transformed by Agrobacterium rhizogenes infection during their evolution, Plant J., 2002, vol. 32, no. 5, pp. 775–787.

    Article  CAS  PubMed  Google Scholar 

  21. Matveeva, T.V., Bogomaz, D.I., Pavlova, O.A., et al., Horizontal gene transfer from genus Agrobacterium to the plant Linaria in nature, Mol. Plant-Microbe Interact., 2012, vol. 25, no. 12, pp. 1542–1551.

    Article  CAS  PubMed  Google Scholar 

  22. Suzuki, K., Tanaka, N., Kamada, H., et al., Mikimopine synthase (mis) gene on pRi1724, Gene, 2001, vol. 263, no. 1, pp. 49–58.

    Article  CAS  PubMed  Google Scholar 

  23. Flores-Mireles, A.L., Eberhard, A., and Winans, S.C., Agrobacterium tumefaciens can obtain sulphur from an opine that is synthesized by octopine synthase using S-methylmethionine as a substrate, Mol. Microbiol., 2012, vol. 84, no. 5, pp. 845–856.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Bouchez, D., Tokuhisa, J.G., Liewellyn, D.J., et al., The ocs-element is a component of the promoters of several T-DNA and plant viral genes, EMBO J., 1989, vol. 8, no. 13, pp. 4197–4204.

    PubMed Central  CAS  PubMed  Google Scholar 

  25. Hooykaas, P., Dulk-Ras, H., Ooms, G., et al., Interactions between octopine and nopaline plasmids in Agrobacterium tumefaciens, J. Bacteriol., 1980, vol. 143, no. 3, pp. 1295–1306.

    PubMed Central  CAS  PubMed  Google Scholar 

  26. Moriguchi, K., Maeda, Y., Satou, M., et al., The complete nucleotide sequence of a plant root-inducing (Ri) plasmid indicates its chimeric structure and evolutionary relationship between tumor-inducing (Ti) and symbiotic (Sym) plasmids in Rhizobiaceae, Mol. Biol., 2001, vol. 307, pp. 771–784.

    Article  CAS  Google Scholar 

  27. Otten, L., Canaday, J., Gerard, J.-C., et al., Evolution of agrobacteria and their Ti plasmids—a review, Mol. Plant-Microbe Interact., 1992, vol. 5, no. 4, pp. 279–287.

    Article  CAS  PubMed  Google Scholar 

  28. Weller, S.A., Stead, E., and Young, J.P.W., Acquisition of an Agrobacterium Ri plasmid and pathogenicity by other α-proteobacteria in cucumber and tomato crops affected by root mat, Appl. Environ. Microbiol., 2004, vol. 70, no. 5, pp. 2779–2785.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Kim, H.S., Yi, H., Myung, J., et al., Opine-based Agrobacterium competitiveness: dual expression control of the agrocinopine catabolism (acc) operon by agrocinopines and phosphate levels, J. Bacteriol., 2008, vol. 190, no. 10, pp. 3700–3711.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Zanker, H., Lintig, J., and Schröber, J., Opine transport genes in the octopine (occ) and nopaline (noc) catabolic regions in Ti plasmids of Agrobacterium tumefaciens, J. Bacteriol., 1992, vol. 174, no. 3, pp. 841–849.

    PubMed Central  CAS  PubMed  Google Scholar 

  31. Kreusch, D., Lintig, J., and Schröber, J., Ti plasmid encoded octopine and nopaline catabolism in Agrobacterium: specificities of the LysR-type regulators OccR and NocR, and protein-induced DNA bending, Mol. Gen. Genet., 1995, vol. 249, no. 1, pp. 102–110.

    Article  CAS  PubMed  Google Scholar 

  32. Lintig, J., Kreusch, D., and Schröber, J., Opine-regulated promoters and LysR-type regulators in the nopaline (noc) and octopine (occ) regions of Ti plasmids of Agrobacterium tumefaciens, J. Bacteriol., 1994, vol. 176, no. 2, pp. 495–503.

    Google Scholar 

  33. Pappas, M., Cell-cell signaling and the Agrobacterium tumefaciens Ti plasmid copy number fluctuations, Plasmid, 2008, vol. 60, no. 2, pp. 89–107.

    Article  CAS  PubMed  Google Scholar 

  34. Hong, S.B., Hwang, I., Dessaux, Y., et al., A T-DNA gene required for agropine biosynthesis by transformed plants is functionally and evolutionarily related to a Ti plasmid gene required for catabolism of agropine by Agrobacterium strains, J. Bacteriol., 1997, vol. 179, no. 15, pp. 4831–4840.

    PubMed Central  CAS  PubMed  Google Scholar 

  35. Canfield, M.L. and Moore, L.W., Isolation and characterization of opine utilizing strains of Agrobacterium tumefaciens and fluorescent strains of Pseudomonas spp. from rootstocks of Malus, Phytopathology, 1991, vol. 1, no. 4, pp. 440–443.

    Article  Google Scholar 

  36. Nautiyal, C.S. and Dion, P., Characterization of the opine-utilizing microflora associated with samples of soil and plants, Appl. Environ. Microbiol., 1990, vol. 56, no. 8, pp. 2576–2579.

    PubMed Central  PubMed  Google Scholar 

  37. Moore, L.W., Chilton, W.S., and Canfield, M.L., Diversity of opines and opine-catabolizing bacteria isolated from naturally occurring crown gall tumors, Appl. Environ. Microbiol., 1997, vol. 63, no. 1, pp. 201–207.

    PubMed Central  CAS  PubMed  Google Scholar 

  38. Tremblay, G., Gagliardo, R., Chilton, W.S., et al., Diversity among opine-utilizing bacteria: identification of coryneform isolates, Appl. Environ. Microbiol., 1987, vol. 53, no. 7, pp. 1519–1524.

    PubMed Central  CAS  PubMed  Google Scholar 

  39. Zanker, H., Lurz, G., Langridge, U., et al., Octopine and nopaline oxidases from Ti plasmids of Agrobacterium tumefaciens: molecular analysis, relationship, and functional characterization, J. Bacteriol., 1994, vol. 176, no. 15, pp. 4511–4517.

    PubMed Central  CAS  PubMed  Google Scholar 

  40. Kim, K.S. and Farrand, S.K., Ti plasmid-encoded genes responsible for catabolism of the crown gall opine mannopine by Agrobacterium tumefaciens are homologs of the T-region genes responsible for synthesis of this opine by the plant tumor, J. Bacteriol., 1996, vol. 178, no. 11, pp. 3275–3284.

    PubMed Central  CAS  PubMed  Google Scholar 

  41. Os, N., Smits, S., Schmitt, L., et al., Control of D-octopine formation in scallop adductor muscle as revealed through thermodynamic studies of octopine dehydrogenase, J. Exp. Biol., 2012, vol. 215, no. 9, pp. 1515–1522.

    Article  PubMed  Google Scholar 

  42. Dion, P., Utilization of octopine by marine bacteria isolated from mollusks, Can. J. Microbiol., 1986, vol. 32, no. 12, pp. 959–963.

    Article  CAS  Google Scholar 

  43. Asano, Y., Yamaguchi, K., and Kondo, K., A new NAD+-dependent opine dehydrogenase from Arthrobacter sp. strain 1C, J. Bacteriol., 1989, vol. 171, no. 8, pp. 4466–4471.

    PubMed Central  CAS  PubMed  Google Scholar 

  44. Beauchamp, C.J., Chilton, W.S., Dion, P., et al., Fungal catabolism of crown gall opines, Appl. Environ. Microbiol., 1990, vol. 56, no. 1, pp. 150–155.

    PubMed Central  CAS  PubMed  Google Scholar 

  45. Bouzar, H. and Moore, L.W., Isolation of different Agrobacterium biovars from a natural oak savanna and tallgrass prairie, Appl. Environ. Microbiol., 1987, vol. 53, no. 4, pp. 717–721.

    PubMed Central  CAS  PubMed  Google Scholar 

  46. Dandurishvili, N., Toklikishvili, N., Ovadis, M., et al., Broad-range antagonistic rhizobacteria Pseudomonas fluorescens and Serratia plymuthica suppress Agrobacterium crown gall tumors on tomato plants, J. Appl. Microbiol., 2011, vol. 110, no. 1, pp. 341–352.

    Article  CAS  PubMed  Google Scholar 

  47. Graves, A.C. and Goldman, S.L., Agrobacterium tumefaciens-mediated transformation of the monocot genus Gladiolus: detection of expression of T-DNA-encoded genes, J. Bacteriol., 1987, vol. 169, no. 4, pp. 1745–1746.

    PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to I. A. Vladimirov.

Additional information

Original Russian Text © I.A. Vladimirov, T.V. Matveeva, L.A. Lutova, 2015, published in Genetika, 2015, Vol. 51, No. 2, pp. 137–146.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vladimirov, I.A., Matveeva, T.V. & Lutova, L.A. Opine biosynthesis and catabolism genes of Agrobacterium tumefaciens and Agrobacterium rhizogenes . Russ J Genet 51, 121–129 (2015). https://doi.org/10.1134/S1022795415020167

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795415020167

Keywords

Navigation