Abstract
Transgenic tobacco (Nicotiana tabacum L. cv. Xanthi) plants expressing wild-type or mutant forms of the 30-kDa movement protein of tobacco mosaic virus (TMV-MP) were employed to study the effects of the TMV-MP on carbon metabolism in source leaves. Fully expanded source leaves of transgenic plants expressing the TMV-MP were found to retain more newly fixed 14C compared with control plants. Analysis of 14C-export from young leaves of TMV-MP plants, where the MP is yet to influence plasmodesmal size exclusion limit, indicated a similar pattern, in that daytime 14C export was slower in TMV-MP plants as compared to equivalent-aged leaves on control plants. Pulse-chase experiments were used to monitor radioactivity present in the different carbohydrate fractions, at specified intervals following 14CO2 labeling. These studies established that the-TMV-MP can cause a significant adjustment in short-term 14-C-photosynthate storage and export. That these effects of the TMV-MP on carbon metabolism and phloem function were not attributable to the effect of this protein on plasmodesmal size exclusion limits, per se, was established using transgenic tobacco plants expressing temperature-sensitive and C-terminal deletion mutant forms of the TMV-MP. Collectively, these studies establish the pleiotropic nature of the TMV-MP in transgenic tobacco, and the results are discussed in terms of potential sites of interaction between the TMV-MP and endogenous processes involved in regulating carbon metabolism and export.
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Abbreviations
- MP:
-
movement protein
- SEL:
-
size exclusion limit
- TMV:
-
tobacco mosaic virus
- ts:
-
temperature sensitive
References
Atkins, D., Hull, R., Wells, B., Roberts, K., Moore, P., Beachy, R.N. (1991) The tobacco mosaic virus 30K movement protein in transgenic tobacco plants is localized to plasmodesmata. J. Gen. Virol. 72, 209–211
Balachandran S., Hull, R.J., Vaadia, Y., Wolf, S., Lucas, W.J. (1995) Tobacco mosaic virus movement protein-induced change in carbon partitioning originates from the mesophyll and is independent of change in plasmodesmal size exclusion limit. Plant Cell & Environ., in press
Berna, A., Gafny, R., Wolf, S., Lucas, W.J., Holt, C.A., Beachy, R.N. (1991) The TMV movement protein: role of the C-terminal 73 amino acids in subcellular localization and function. Virology 182, 682–689
Deom, C.M., Oliver, M.J., Beachy, R.N. (1987) The 30-kilodalton gene product of tobacco mosaic virus potentiates virus movement. Science 237, 389–394
Deom, C.M., Schubert, K.R., Wolf, S., Holt, C.A., Lucas, W.J., Beachy, R.N. (1990) Molecular characterization and biological function of the movement protein of tobacco mosaic virus in transgenic plants. Proc. Natl. Acad. USA 87, 3284–3288
Deom, C.M., Wolf, S., Holt, C.A., Lucas, W.J., Beachy, R.N. (1991) Altered function of the tobacco mosaic virus movement protein in a hypersensitive host. Virology 180, 251–256
Ding, B., Haudenshild, J.S., Hull, R.J., Wolf, S., Beachy, R.N., Lucas, W.J. (1992) Secondary plasmodesmata are specific sites of localization of the tobacco mosaic movement protein in transgenic tobacco plants. Plant Cell 4, 915–928
Gafny, R., Lapidot, M., Berna, A., Holt, A., Deom, C.M., Beachy, R.N. (1992) Effects of terminal deletion mutations on function of the movement protein of tobacco mosaic virus. Virology 187, 499–507
Giaquinta, R.T. (1983) Phloem loading of sucrose. Annu. Rev. Plant Physiol. 34, 347–387
Heineke, D., Wildenberger, K., Sonnewald, U., Willmitzer, L., Heldt, H.W. (1994) Accumulation of hexoses in leaf vacuoles: Studies with transgenic tobacco plants expressing yeast-derived invertase in the cytosol, vacuole or apoplasm. Planta 194, 29–41
Huber, S.C., Huber, J.A.L., McMichael, Jr., R.W. (1992) The regulation of sucrose synthesis in leaves. In: Carbon partitioning within and between organisms, pp. 1–26, Pollock, C.J., Farrar, J.F., Gordon, A.J., eds. BIOS Scientific Publishers, Oxford
Leonard, D.A., Zaitlin,M. (1982) A temperature-sensitive strain of tobacco mosaic virus defective in cell-to-cell movement generates an altered viral-coded protein. Virology 117, 416–424
Lucas, W.J., Gilbertson, R.L. (1994) Plasmodesmata in relation to viral movement within leaf tissues. Annu. Rev. Phytopathol. 32, 387–411
Lucas, W.J., Olesinski, A.A., Hull, R.J., Haudenshield, J., Deom, C.M., Beachy, R.N., Wolf, S. (1993) Influence of the tobacco mosaic virus 30-kDa movement protein on carbon metabolism and photosynthate partitioning in transgenic tobacco plants. Planta 190, 88–96
Meshi, T., Watanabe, Y., Saito, T., Sugimoto, A., Maeda, T., Okada, Y. (1987) Function of the 30 kD protein of tobacco mosaic virus: Involvement in cell-to-cell movement and dispensability for replication. EMBO J. 6, 2557–2563
Moore, P.J., Fenczik, C.A., Deom, C.M., Beachy, R.N. (1992) Developmental changes in plasmodesmata in transgenic tobacco expressing the movement protein of tobacco mosaic virus. Protoplasma 170, 115–127
Ohno, T., Takamatsu, N., Meshi, T., Okada, Y., Nishiguchi, M., Kiko, Y. (1983) Single amino acid substitution in 30K protein of TMV defective in virus transport function. Virology 131, 255–258
Robards, A.W., Lucas, W.J. (1990) Plasmodesmata. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 369–419
Stitt, M., Quick, W.P. (1989) Photosynthetic carbon partitioning: its regulation and possibilities for manipulation. Physiol. Plant. 77, 633–641.
Tucker, J.E., Mauzerall, D., Tucker, E.B. (1989) Symplastic transport of carboxyfluorescein in staminal hairs of Setcreasea purpurea is diffusive and includes loss to the vacuole. Plant Physiol. 90, 1143–1147
van Bel, A.J.E. (1992) Pathway and mechanisms of phloem loading. In: Carbon partitioning within and between organisms, pp. 53–70, Pollock, C.J., Farrar, J.F., Gordon, A.J., eds. BIOS Scientific Publishers, Oxford
Waigmann, E., Lucas, W.J., Citovsky, V., Zambryski, P. (1994) Direct functional assay for tobacco mosaic virus cell-to-cell movement protein and identification of a domain involved in increasing plasmodesmal permeability. Proc. Natl. Acad. Sci. USA 91, 1433–1437
Wolf, S., Deom, C.M., Beachy, R.N., Lucas, W.J. (1989) Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246, 377–379
Wolf, S., Deom, C.M., Beachy, R.N., Lucas, W.J. (1991) Plasmodesmata function is probed using transgenic tobacco plants that express a virus movement protein. Plant Cell 3, 593–604
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This work was supported by United State-Israel Binational Agricultural Research Development Fund grant No. 90-00070 (S.W. and W.J.L). We thank Roger N. Beachy for generously providing some of the transgenic plant lines employed in this study. This paper is a contribution from the Uri Kinamon Laboratory. A.A.O. was supported by a scholarship from the Kinamon Foundation.
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Olesinski, A.A., Lucas, W.J., Galun, E. et al. Pleiotropic effects of tobacco-mosaic-virus movement protein on carbon metabolism in transgenic tobacco plants. Planta 197, 118–126 (1995). https://doi.org/10.1007/BF00239947
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DOI: https://doi.org/10.1007/BF00239947