Biology of Crown Gall Tumors

Specific adaptive mechanisms for water and nutrient acquisition and the suppression of shoot and root differentiation characterize crown gall tumor development. Strong vascularization like in animal and human tumors is the most prominent and important feature of tumor proliferation. Vascular bundles consisting of phloem and xylem are from the onset of tumor initiation functionally connected to the host bundle. At the host/tumor interface the vessel number is considerably increased and interrupted by multiseriate rays. These altered structures enhance water flow into the tumor parenchyma and, together with the disruption of epidermis and cuticle, substantially support tumor transpiration. Expression of the T-DNA-encoded genes for abundant auxin and cytokinin biosynthesis trigger a cascade of further phytohormones, which are essential for tumor development as well. Auxin accumulation is particularly enhanced by the expression of the T-DNA-located gene 6b for phenylpropanoids, hence for flavonoid biosynthesis. Spatio-temporal distribution patterns of the bioactive free and conjugated auxin and cytokinins, ethylene and abscisic acid match well the sites of highest chalcone synthase (CHS) expression and hence flavonoid concentration. Flavonoids accumulate at the sites of strongest free auxin accumulation and prevent basipetal auxin efflux, thus maintaining high auxin and cytokinin concentrations for induction and development of the vascular system. The considerable auxin- and cytokininenhanced ethylene emission is causally related with the development of the enlarged xylem in the tumor/host interface and the aerenchyma, which is important for aerobic energy metabolism; ethylene finally induces the accumulation of abscisic acid (ABA) in the tumor and host leaves. ABA in turn leads to diminished shoot water loss by enhancing closure of host leaf stomata, so that a stronger water supply to the tumor is guaranteed. In addition, ABA accumulation in the tumor periphery enhances accumulation of osmoprotectants such as sucrose and proline, to prevent tumor desiccation. Tumors accumulate high solute concentrations. The expression of root-specific K+-influx channels (AKT1 and AtKC1) is upregulated while genes of anion transporters at the plasma membrane are down-regulated; therefore, an important role is attributed to phloem transport for xylem-derived nutrient import into the tumor parenchyma. The phloem sieve element/companion cell complex is well coupled to the tumor parenchyma by numerous plasmodesmata. Spatio-temporal analysis of the activity of sucrose degrading enzymes and of sugar accumulation confirm symplastic metabolite phloem unloading. In conclusion, predominantly auxin and cytokinin-induced ethylene have a key role for successful tumor establishment by tumor vascularization and, together with cuticular disruption, by redirecting of water flow and symplastic phloem unloading of carbohydrate, amino acid and anion import.