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First published online October 2, 2003; 10.1104/pp.103.028142

Plant Physiology 133:1024-1037 (2003)
© 2003 American Society of Plant Biologists

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Vascularization, High-Volume Solution Flow, and Localized Roles for Enzymes of Sucrose Metabolism during Tumorigenesis by Agrobacterium tumefaciens1

Rebecca Wächter, Markus Langhans, Roni Aloni, Simone Götz, Anke Weilmünster, Ariane Koops, Leopoldine Temguia, Igor Mistrik, Jan Pavlovkin, Uwe Rascher, Katja Schwalm, Karen E. Koch and Cornelia I. Ullrich*

Institute of Botany, Darmstadt University of Technology, Schnittspahnstrasse 3, 64287 Darmstadt, Germany (R.W., M.L., S.G., A.W., A.K., L.T., K.S., C.I.U.); Department of Plant Sciences, Tel Aviv University, Tel Aviv 69978, Israel (R.A.); Slovak Academy of Sciences, Department of Plant Physiology, Dúbravská cesta 14, 84223 Bratislava, Slovakia (I.M., J.P.); Columbia University, Biosphere 2 Center, P.O. Box 689, Oracle, Arizona 85623 (U.R.); and Department of Horticulture Sciences, University of Florida, P.O. Box 110690, Gainesville, Florida 32611 (K.E.K.)

Vascular differentiation and epidermal disruption are associated with establishment of tumors induced by Agrobacterium tumefaciens. Here, we address the relationship of these processes to the redirection of nutrient-bearing water flow and carbohydrate delivery for tumor growth within the castor bean (Ricinus communis) host. Treatment with aminoethoxyvinyl-glycine showed that vascular differentiation and epidermal disruption were central to ethylene-dependent tumor establishment. CO2 release paralleled tumor growth, but water flow increased dramatically during the first 3 weeks. However, tumor water loss contributed little to water flow to host shoots. Tumor water loss was followed by accumulation of the osmoprotectants, sucrose (Suc) and proline, in the tumor periphery, shifting hexose-to-Suc balance in favor of sugar signals for maturation and desiccation tolerance. Concurrent activities and sites of action for enzymes of Suc metabolism changed: Vacuolar invertase predominated during initial import of Suc into the symplastic continuum, corresponding to hexose concentrations in expanding tumors. Later, Suc synthase (SuSy) and cell wall invertase rose in the tumor periphery to modulate both Suc accumulation and descending turgor for import by metabolization. Sites of abscisic acid immunolocalization correlated with both central vacuolar invertase and peripheral cell wall invertase. Vascular roles were indicated by SuSy immunolocalization in xylem parenchyma for inorganic nutrient uptake and in phloem, where resolution allowed SuSy identification in sieve elements and companion cells, which has widespread implications for SuSy function in transport. Together, data indicate key roles for ethylene-dependent vascularization and cuticular disruption in the redirection of water flow and carbohydrate transport for successful tumor establishment.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.028142.

1 This work was supported by the Deutsch Forschungsgemeinschaft/Sonderforschungsbereich (grant no. 199 to C.I.U.).

* Corresponding author; e-mail uleb{at}bio.tu-darmstadt.de; fax 49–6151–164630.

Received June 5, 2003; returned for revision July 14, 2003; accepted July 27, 2003.




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