Opines and Opine-Like Molecules Involved in Plant-Rhizobiaceae Interactions

Abstract

The first reports on opines date back to the midfifties, when Morel (1956) and Lioret (1956) independently presented their results on, respectively, the metabolism of arginine and the identification of unusual amino acids in Agrobacterium-induced crown gall tumors, at a meeting of the French Society for Plant Physiology. These tumor compounds were later purified and identified (Figure 1) as lysopine (Biemann et al., 1960), octopine (Ménagé and Morel, 1964), octopinic acid (Ménagé and Morel, 1965), nopaline (Goldmann et al., 1969) and collectively termed opines (reviews: Tempé and Schell, 1977; Tempé and Goldmann, 1982). The significance of the metabolic perturbation undergone by the crown gall cells remained unclear for several years mostly because the specificity of opines as markers of these tissues was long debated (reviewed by Tempé and Goldmann, 1982). Three observations, however, were milestones in the understanding of the role of opines in the interaction: 1) Agrobacterium can degrade opines (Lejeune and Jubier, 1968); 2) the nature of opines synthesized in a tumor depends on the inciting Agrobacterium tumefaciens strains, not on the plant as it had been initially proposed (Goldmann et al., 1968; Petit et al., 1970); and 3) the correlation between opine degradation by agrobacteria and opine synthesis in plant cells is strict: that is, a given A. tumefaciens strain can only degrade the opines synthesized by the tumors it induced (Petit et al., 1970; reviewed by Tempé and Petit, 1983). Interestingly, these features were immediately interpreted as an indication of a possible gene transfer by Petit and Tourneur (1972) — a hypothesis that was first suggested by Braun (1947) and Klein (1954) (reviewed in Braun, 1982 and in Tempé and Petit, 1983) — whereas it was understood only years later that the production of opines by the crown gall cells provided the pathogen with a selective growth advantage (Schell et al., 1979; Tempé et al., 1979). This understanding resulted also from the discovery of the Ti plasmids (Zaenen et al., 1974; Van Larebeke et al., 1974; Watson et al., 1975), the elucidation of the tumorigenesis mechanism (Chilton et al., 1977; De Beuckeleer et al., 1978; Thomashow et al., 1980; Willmitzer et al., 1980, see also other chapters in this book), the localization of the genes involved in opine synthesis and degradation on the Ti plasmids (Bomhoff et al., 1976; Montoya et al., 1977) and the demonstration of the opine-induced, conjugal activity of these plasmids (Kerr et al., 1977; Petit et al., 1978a). All these data were combined and the fundamental role of opines in the Agrobacterium-plant interaction was rationalized by the originators of “the opine concept” (Tempé et al., 1979) and “the genetic colonization theory” (Schell et al., 1979) which define opines as follows. Opines are small-size molecules, the presence of which in the crown gall tumor is triggered by the pathogen to support its multiplication and to promote the dissemination of its virulence determinants (previous reviews on this topics: Dessaux et al., 1992, 1993; Gelvin, 1992).