Convergent Evolution of Amadori Opine Catabolic Systems in Plasmids ofAgrobacterium tumefaciens

Abstract

Deoxyfructosyl glutamine (DFG, referred to elsewhere as dfg) is a naturally occurring Amadori compound found in rotting fruits and vegetables. DFG also is an opine and is found in tumors induced by chrysopine-type strains of Agrobacterium tumefaciens. Such strains catabolize this opine via a pathway coded for by their plasmids. NT1, a derivative of the nopaline-type A. tumefaciens strain C58 lacking pTiC58, can utilize DFG as the sole carbon source. Genes for utilization of DFG were mapped to the 543-kb accessory plasmid pAtC58. Two cosmid clones of pAtC58 allowed UIA5, a plasmid-free derivative of C58, harboring pSa-C that expresses MocC (mannopine [MOP] oxidoreductase that oxidizes MOP to DFG), to grow by using MOP as the sole carbon source. Genetic analysis of subclones indicated that the genes for utilization of DFG are located in a 6.2-kb BglII Opines are produced by crown gall tumor cells, which are induced by pathogenic Agrobacterium spp. (8,56). Genes for the biosynthesis of these compounds are encoded by the T region of Ti (tumor-inducing) or Ri (root-inducing) plasmids, which are present in the plant pathogens. During infection, the T region is transferred to plant cells and stably integrated into the nuclear genome. The genes for production of opines and plant hormones encoded in the integrated DNA are expressed, and opines are released from the transformed plant cells into soil, where they can be utilized by the pathogenic bacterium as carbon and energy sources (8,42,51). The genes for the utilization of the opines by the bacterium also are located on the virulence plasmids, but in segments outside of the T-DNA region. Opines play key roles in the interkingdom interactions between Agrobacterium spp. and infected plants, promoting selective growth of the pathogenic bacterium (15,39,45,54), inducing Ti plasmid conjugal transfer (11, 42), acting as attractants for agrobacterial strains (27), and inhibiting growth of certain agrobacterial strains (16,29).Among the more than 20 known opines, the chrysopine family (5, 7) is produced by tumors induced by A. tumefaciens Chry strains, Ficus strains, and IIBV7 (5, 52). This family of Amadori-type compounds includes N-1-deoxy-D-fructosyl-Lglutamine (DFG, referred to elsewhere as dfg), commonly called santhopine; N-1-deoxy-D-fructosyl-L-glutamate (DFGA, referred to elsewhere as dfga); N-1-deoxy-D-fructosyl-5-oxo-Lproline (DFOP, referred to elsewhere as dfop); and chrysopine, the spiropyranosyl lactone of DFG (5). Chemically, these compounds are closely related to the mannityl opines (Fig. 1). DFG and DFGA are the deoxyfructosyl analogs of mannopine (MOP) and mannopinic acid (MOA), respectively, and chrysopine and DFOP are deoxyfructosyl analogs of agropine (AGR) and agropinic acid, respectively. These similarities suggest a close relatedness in catabolic pathways and also in the genes coding for the enzymes for their catabolism between the two families of opines. In this regard, DFG is an intermediate in the pathway for the catabolism of AGR and MOP coded for b...

Genes for utilization of deoxyfructosyl glutamine (DFG), an amadori compound, are widely dispersed in the family Rhizobiaceae

“…These enzymes, which can form and disrupt imine linkages, are not classical Amadoriases. The second pathway, coded for by pAtC58, another, very large plasmid present in strain C58, involves an oxidase, SocD that is phylogenetically related to several Amadoriases of bacterial and fungal origins [2]. In the absence of the Ti plasmid‐coded MOP catabolism system, this enzyme is essential for the ability of the bacteria to utilize DFG.…”

Structural Basis for High Specificity of Amadori Compound and Mannopine Opine Binding in Bacterial Pathogens

“…Conversely, Baek et al (25) observed that the genomic region of the At plasmid of strain C58 coding for the PBP SocA and its membrane transporter mediates mannopine import, suggesting that SocA may bind mannopine. However, the strain C58 lacks the gene encoding the enzyme MocC that degrades mannopine into DFG.…”

“…Therefore, MotA and the mannopine-degrading enzyme MocC are not present in this strain, which cannot grow when mannopine is the sole source of carbon and nitrogen. In contrast, A. tumefaciens strain C58 can grow when DFG is the sole resource (25). Remarkably, the constitutive expression of the mannopine-degrading enzyme MocC in A. tumefaciens C58 conferred upon this strain the capability to grow on mannopine.…”

“…Structural data on mannityl-opine-PBP complexes is currently lacking. In this study we investigated and compared the structural and biochemical properties of two PBPs sharing 5% sequence identity, MotA and SocA, that have been associated with the assimilation of mannopine using genetic approaches (mapping of gene regions and defective mutants) and opine uptake/transport experiments (22)(23)(24)(25). MotA belongs to the mannopine transport system encoded by the Ti plasmid of the A. tumefaciens strain B6 ( Fig.…”

Buffet hypothesis for microbial nutrition at the rhizosphere

“…In the rhizosphere different Amadori compounds ( N -glycosylamines) may be found that form spontaneously from decomposing plant material or by Agrobacterium spp. (Baek et al, 2003). …”