Abnormal accumulation of sugars and phenolics in tobacco roots expressing the Agrobacterium T-6b oncogene and the role of these compounds in 6b-induced growth

Molecular Plant-Microbe Interactions

Volumn 20, Issue 1, 2007, Pages 53-62

  Clément, Bernadette ^a   Perot, Jonathan ^a   Geoffroy, Pierrette ^a   Legrand, Michel ^a   Zon, Jerzy ^b   Otten, Léon ^a  

^a INST DE BIOL MOLEC DES PLANTES   (France)

^b Department of Medicinal Chemistry and Microbiology   (Poland)

Author keywords

Crown gall; Plast family

Indexed keywords

FRUCTOSE; GLUCOSE; SUCROSE;

ARTICLE; BACTERIAL GENE; BIOLOGICAL MODEL; GENE EXPRESSION; GENETICS; METABOLISM; MICROBIOLOGY; ONCOGENE; PLANT LEAF; PLANT ROOT; RHIZOBIUM; TOBACCO; TRANSGENIC PLANT;

FRUCTOSE; GENE EXPRESSION; GENES, BACTERIAL; GLUCOSE; MODELS, BIOLOGICAL; ONCOGENES; PLANT LEAVES; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; RHIZOBIUM; SUCROSE; TOBACCO;

AGROBACTERIUM; NICOTIANA TABACUM; RHIZOBIUM; VALERIANA EDULIS;

EID: 33845651825     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-20-0053     Document Type: Article

References (45)

1. Appert, C., Zon, J., and Amrhein, N. 2003. Kinetic analysis of the inhibition of phenylalanine ammonia-lyase by 2-aminoindan-2-phosphonic acid and other phenylalanine analogues. Phytochemistry 62:415-422.
2. Bagyan, I. L., Revenkova, E. V., Pozmogova, G. E., Kraev, A. S., and Skryabin, K. G. 1995. 5′-regulatory region of Agrobacterium tumefaciens T-DNA gene 6b directs organ-specific, wound-inducible and auxin-inducible expression in transgenic tobacco. Plant Mol. Biol. 29:1299-1304.
3. Baskin, T. I., Remillong, E. L., and Wilson, J. E. 2001. The impact of mannose and other carbon sources on the elongation and diameter of the primary root of Arabidopsis thaliana. Aust. J. Plant Physiol. 28:481-488.
4. Bonnard, G., Tinland, B., Paulus, F., Szegedi, E., and Otten, L. 1989. Nucleotide sequence, evolutionary origin and biological role of a rearranged cytokinin gene isolated from a wide host range biotype III Agrobacterium strain. Mol. Gen. Genet. 216:428-438.
5. Buer, C. S., Wasteneys, G. O., and Masle, J. 2003. Ethylene modulates root-wave responses in Arabidopsis. Plant Physiol. 132:1085-1096.
6. Chandran, D., Reinders, A., and Ward, J. 2003. Substrate specificity of the Arabidopsis thaliana sucrose transporter AtSUC2. J. Biol. Chem. 278:44320-44325.
7. Clément, B., Pollmann, S., Weiler, E., Urbanczyk-Wochniak, E., and Otten, L. 2006. The Agrobacterium vitis T-6b oncoprotein induces auxin-independent cell expansion in tobacco. Plant J. 45:1017-1027.
8. Eksittikul, T., Chulavatnatol, M., and Limpaseni, T. 2001. Characterization of sucrose uptake system in cassava (Manihot esculenta Crantz). Plant Sci. 160:733-737.
9. Freixes, S., Thibaud, M.-C., Tardieu, F., and Muller, B. 2002. Root elongation and branching is related to local hexose concentration in Arabidopsis thaliana seedlings. Plant Cell Environ. 25:1357-1366.
10. Gális, I. I., Simek, P., Macas, J., Zahradnickova, H., Vlasak, J., Wabiko, H., Van Dongen, W., Van Onckelen, H. A., and Ondrej, M. 1999. The Agrobacterium tumefaciens C58-6b gene confers resistance to N(6)-benzyladenine without modifying cytokinin metabolism in tobacco seedlings. Planta 209:453-461.
11. Gális, I., Simek, P., van Onckelen, H., Kakiuchi, Y., and Wabiko, H. 2002. Resistance of transgenic tobacco seedlings expressing the Agrobacterium tumefaciens C58-6b gene, to growth-inhibitory levels of cytokinin is associated with elevated IAA levels and activation of phenylpropanoid metabolism. Plant Cell Physiol. 43:939-950.
12. Gális, I., Kakiuchi, Y., Simek, P., and Wabiko, H. 2004. Agrobacterium tumefaciens AK-6e gene modulates phenolic compound metabolism in tobacco. Phytochemistry 65:169-179.
13. Grémillon, L., Helfer, A., Clément, B., and Otten, L. 2004. New plant growth-modifying properties of the Agrobacterium T-6b oncogene revealed by the use of a dexamethasone-inducible promoter. Plant J. 37:218-228.
14. Helfer, A., Pien, S., and Otten, L. 2002. Functional diversity and mutational analysis of Agrobacterium 6B oncoproteins. Mol. Genet. Genomics 267:577-586.
15. Helfer, A., Clément, B., Michler, P., and Otten, L. 2003. The Agrobacterium oncogene AB-6b causes a graft-transmissible enation syndrome in tobacco. Plant Mol. Biol. 52:483-493.
16. Hoffmann, L., Besseau, S., Geoffroy, P., Ritzenthaler, C., Meyer, D., Lapierre, C., Pollet, B., and Legrand, M. 2004. Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell 16:1446-1465.
17. Hooykaas, P. J. J., den Dulk-Ras, H., and Schilperoort, R. A. 1988. The Agrobacterium tumefaciens T-DNA gene 6b is an one gene. Plant Mol. Biol. 11:791-794.
18. Huss, B., Tinland, B., Paulus, F., Walter, B., and Otten, L. 1990. Functional analysis of a complex oncogene arrangement in biotype III Agrobacterium tumefaciens strains. Plant Mol. Biol. 14:173-186.
19. Jacobs, M., and Rubery, P. 1988. Naturally occurring auxin transport regulators. Science 241:346-349.
20. Kakiuchi, Y., Galis, I., Tamogami, S., and Wabiko, H. 2006. Reduction of polar auxin transport in tobacco by the tumorigenic Agrobacterium tumefaciens AK-6b gene. Planta 223:237-247.
21. Kitakura, S., Fujita, T., Ueno, Y., Terakura, S., Wabiko, H., and Machida, Y. 2002. The protein encoded by the oncogene 6b from Agrobacterium tumefaciens interacts with a nuclear protein of tobacco. Plant Cell 14:451-463.
22. La Camera, S., Gouzerh, G., Dhondt, S., Hoffmann, L., Fritig, B., Legrand, M., and Heitz, T. 2004. Metabolic reprogramming in plant innate immunity: The contributions of phenylpropanoid and oxylipin pathways. Immunol. Rev. 198:267-284.
23. Lalonde, S., Boles, E., Hellmann, H., Barker, L., Patrick, J. W., Frommer, W. B., and Ward, J. M. 1999. The dual function of sugar carriers: Transport and sugar sensing. Plant Cell 11:707-726.
24. Levesque, H., Delepelaire, P., Rouzé, P., Slightom, J., and Tepfer, D. 1988. Common evolutionary origin of the central portion of the Ri TL-DNA of Agrobacterium rhizogenes and the Ti T-DNAs of Agrobacterium tumefaciens. Plant Mol. Biol. 11:731-744.
25. Lin, W., Schmitt, M. R., Hitz, W. D., and Giaquinta, R. T. 1984. Sugar transport in isolated corn root protoplasts. Plant Physiol. 76:894-897.
26. Muller, B., Stosser, M., and Tardieu, F. 1998. Spatial distributions of tissue expansion and cell division rates are related to irradiance and to sugar content in the growing zone of maize roots. Plant Cell Environ. 21:149-158.
27. Murashige, T., and Skoog, F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15:473-497.
28. Niggeweg, R., Michael, A., and Martin, C. 2004. Engineering plants with increased levels of the antioxidant chlorogenic acid. Nat. Biotechnol. 22:746-753.
29. Nilsson, O., and Olsson, O. 1997. Getting to the root: The role of the Agrobacterium rhizogenes rol genes in the formation of hairy roots. Physiol. Plant. 100:463-473.
30. Otten, L., and Heifer, A. 2001. Biological activity of the rolB-like 5′ end of the A4-orf8 gene from the Agrobacterium rhizogenes TL-DNA. Mol. Plant-Microbe Interact. 14:405-411.
31. Paulus, F., Huss, B., Tinland, B., Herrmann, A., Canaday, J., and Otten, L. 1991. Role of T-region borders in Agrobacterium host range. Mol. Plant-Microbe Interact. 4:163-172.
32. Peiter, E., and Schubert, S. 2003. Sugar uptake and proton release by protoplasts from the infected zone of Vicia faba L. nodules: Evidence against apoplastic sugar supply of infected cells. J. Exp. Bot. 54:1691-1700.
33. Scharte, J., Schön, H., and Weiss, E. 2005. Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae. Plant Cell Environ. 28:1421-1435.
34. Spanier, K., Schell, J., and Schreier, P. H. 1989. A functional analysis of T-DNA gene 6b: The fine tuning of cytokinins effects on shoot development. Mol. Gen. Genet. 219:209-216.
35. Swiech, R., Browning, S., Molsen, D., Stenger, D. C., and Holbrook, G. P. 2001. Photosynthetic responses of sugar beet and Nicotiana benthamiana Domin. infected with beet curly top virus. Physiol. Mol. Plant Pathol. 58:43-52.
36. Terakura, S., Kitakura, S., Ishikawa, M., Ueno, Y., Fujita, T., Machida, C., Wabiko, H., and Machida, Y. 2006. Oncogene 6b from Agrobacterium tumefaciens induces abaxial cell division at late stage of development and modifies vascular development in petioles. Plant Cell Physiol. 47:664-672.
37. Tinland, B., Huss, B., Paulus, F., Bonnard, G., and Otten, L. 1989. Agrobacterium tumefaciens 6b genes are strain-specific and affect the activity of auxin as well as cytokinin genes. Mol. Gen. Genet. 219:217-224.
38. Tinland, B., Rohfritsch, O., Michler, P., and Otten, L. 1990. Agrobacterium tumefaciens T-DNA gene 6b stimulates rol-induced root formation, permits growth at high auxin concentrations and increases root size. Mol. Gen. Genet. 223:1-10.
39. Tinland, B., Fournier, P., Heckel, T., and Otten, L. 1992. Expression of a chimeric heat-shock inducible Agrobacterium 6b oncogene in Nicotiana rustica. Plant Mol. Biol. 18:921-930.
40. Toko, K., Iiyama, S., Tanaka, C., Hayashi, K., Yamafuji, K., and Yamafuji, K. 1987. Relation of growth process to spatial patterns of electric potential and enzyme activity in bean roots. Biophys. Chem. 27:39-58.
41. Umber, M., Voll, L., Weber, A., Michler, P., and Otten, L. 2002. The rolB-like part of the Agrobacterium rhizogenes orf8 gene inhibits sucrose export in tobacco. Mol. Plant-Microbe Interact. 15:956-962.
42. Umber, M., Clément, B., and Otten, L. 2005. The T-DNA oncogene A4-orf8 from Agrobacterium rhizogenes strain A4 induces abnormal growth in tobacco. Mol. Plant-Microbe Interact. 18:205-211.
43. Wabiko, H., and Minemura, M. 1996. Exogenous phytohormone-independent growth and regeneration of tobacco plants transgenic for the 6b gene of Agrobacterium tumefaciens AKE10. Plant Physiol. 112:939-951.
44. Walter, A., Feil, R., and Schurr, U. 2003. Expansion dynamics, metabolite composition and substance transfer of the primary root growth zone of Zea mays L. grown in different external nutrient availabilities. Plant Cell Environ. 26:1451-1466.
45. Zon, J., and Amrhein, N. 1992. Inhibitors of phenylalanine ammonia-lyase: 2-aminoindan-2-phosphonic acid and related compounds. Liebigs Ann. Chem. 1992:625-628.