Opines and Agrobacterium: Molecular Mechanisms that Drive a Successful Microbe-Host Interaction.


We are interested in the problem of how the Ti plasmid insures that it carries the genes for the catabolism of precisely those opines that are produced by the crown gall tumors that it induces. Corollaries to this question include those concerning the origins of these genes, and how they, and the activities of their products have been altered to provide the functions required for opine synthesis by the plant and catabolism by the bacterium. To this end, we have been studying the genes involved in the synthesis by the tumor, and the catabolism by the bacterium of a family of four mannose-containing metabolites called the mannityl opines. We have discovered that the three key genes responsible for catabolism of these four opines are duplicates of the three genes, located in the T-region of the Ti plasmid, responsible for the production of the opines by the crown gall tumors. These genes are homologous at the DNA and protein sequence levels, and among two of the pairs, the two proteins of each exhibit similar enzymatic activities. From an analysis of this system, and also of a progenitor opine system, we have proposed a step-wise course of evolution of the mannityl opine system. The evolution of this opine system, we suggest, has occurred as a response by Agrobacterium to the emergence of other soil microflora that can utilize the predecessors of the mannityl opines. Thus, in addition to providing us with information on the current status of a microbe-host relationship, our studies give us clues as to how this system evolved, as well as hints at the selection pressures in nature that led to this genetic adaptation.

Recent publications relevant to this theme:

Hong, S.-B., Dessaux, Y., Chilton, W.S., and Farrand, S.K. Organization and regulation of the mannopine cyclase-associated opine catabolism genes in Agrobacterium tumefaciens strain 15955. J. Bacteriol. 175:401-410, 1993

Hong, S.-B., and Farrand, S.K. Functional role of the Ti plasmid-encoded catabolic mannopine cyclase in mannityl opine catabolism by Agrobacterium. J. Bacteriol. 176:3576-3583, 1994

Hong, S.-B. and Farrand, S.K. Purification and characterization of catabolic mannopine cyclase encoded by the Agrobacterium tumefaciens Ti plasmid pTi15955. J.Bacteriol. 178:2427-2430, 1996

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. 178:3275-3284, 1996

Kim, K.-S., Chilton, W.S., and Farrand, S.K. A Ti plasmid-encoded enzyme required for degradation of mannopine is functionally homologous to the T-region-encoded enzyme required for synthesis of this opine in crown gall tumors. J. Bacteriol. 178:3285-3292, 1996

Hong, S.-B., Hwang, I., Dessaux, Y., Guyon, P., Kim, K.-S., and Farrand, S. K. 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. J. Bacteriol. 179:4831-4840, 1997.

Kim,H., and Farrand, S. K. Characterization of the acc operon from the nopaline-type Ti plasmid pTiC58 of Agrobacterium tumefaciens strain C58 which encodes utilization of agrocinopines A+B and susceptibility to agrocin 84. J. Bacteriol. 179:7559-7572, 1997

Kim, H., and Farrand, S. K. Opine catabolic loci from Agrobacterium plasmids confer chemotaxis to their cognate substrates. Mol. Plant-Microbe Interact. 11:131-143, 1998.

Dessaux, Y., Petit, A., Farrand, S. K., and Murphy, P. J. Opines and Opine-Like Molecules Involved in Plant-Rhizobiaceae Interactions. In: H. P. Spank, A. Kondorosi, and P. J. J. Hooykaas, (Eds). The Rhizobiaceae. Kluwer Academic Publishing Co., Dorrecht, The Neterlands, In press, 1998.