Abstract
Using noninvasive imaging techniques, we compared phloem unloading of the membrane-impermeant, fluorescent solute carboxyfluorescein (CF) with that of potato virus X expressing the gene for the green fluorescent protein. Although systemic virus transport took considerably longer to occur than did CF transport, unloading of both solute and virus occurred predominantly from the class III vein network, a highly branched veinal system found between class II veins. The minor veins (classes IV and V) played no role in solute or virus import but were shown to be functional in xylem transport at the time of import by labeling with Texas Red dextran. After virus exit from the class III phloem, the minor veins eventually became infected by cell-to-cell virus movement from the mesophyll. During the sink/source transition, phloem unloading of CF was inhibited from class III veins before the cessation of phloem import through them, suggesting a symplastic isolation of the phloem in class III veins before its involvement in export. The progression of the sink/source transition for carbon was unaffected by the presence of the virus in the sink leaf. However, the virus was unable to cross the sink/source boundary for carbon that was present at the time of viral entry, suggesting a limited capacity for cell-to-cell virus movement into the apical (source) region of the leaf. A functional model of the sink/source transition in Nicotiana benthamiana is presented. This model provides a framework for the analysis of solute and virus movement in leaves.
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Selected References
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- Angell S. M., Davies C., Baulcombe D. C. Cell-to-cell movement of potato virus X is associated with a change in the size-exclusion limit of plasmodesmata in trichome cells of Nicotiana clevelandii. Virology. 1996 Feb 1;216(1):197–201. doi: 10.1006/viro.1996.0046. [DOI] [PubMed] [Google Scholar]
- Baulcombe D. C., Chapman S., Santa Cruz S. Jellyfish green fluorescent protein as a reporter for virus infections. Plant J. 1995 Jun;7(6):1045–1053. doi: 10.1046/j.1365-313x.1995.07061045.x. [DOI] [PubMed] [Google Scholar]
- Biddulph O., Cory R. Translocation of C Metabolites in the Phloem of the Bean Plant. Plant Physiol. 1965 Jan;40(1):119–129. doi: 10.1104/pp.40.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carrington J. C., Kasschau K. D., Mahajan S. K., Schaad M. C. Cell-to-Cell and Long-Distance Transport of Viruses in Plants. Plant Cell. 1996 Oct;8(10):1669–1681. doi: 10.1105/tpc.8.10.1669. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chapman S., Kavanagh T., Baulcombe D. Potato virus X as a vector for gene expression in plants. Plant J. 1992 Jul;2(4):549–557. doi: 10.1046/j.1365-313x.1992.t01-24-00999.x. [DOI] [PubMed] [Google Scholar]
- Cruz S. S., Chapman S., Roberts A. G., Roberts I. M., Prior D. A., Oparka K. J. Assembly and movement of a plant virus carrying a green fluorescent protein overcoat. Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6286–6290. doi: 10.1073/pnas.93.13.6286. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ding X., Shintaku M. H., Carter S. A., Nelson R. S. Invasion of minor veins of tobacco leaves inoculated with tobacco mosaic virus mutants defective in phloem-dependent movement. Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):11155–11160. doi: 10.1073/pnas.93.20.11155. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fellows R. J., Geiger D. R. Structural and Physiological Changes in Sugar Beet Leaves during Sink to Source Conversion. Plant Physiol. 1974 Dec;54(6):877–885. doi: 10.1104/pp.54.6.877. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heinlein M., Epel B. L., Padgett H. S., Beachy R. N. Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science. 1995 Dec 22;270(5244):1983–1985. doi: 10.1126/science.270.5244.1983. [DOI] [PubMed] [Google Scholar]
- Leisner S. M., Turgeon R., Howell S. H. Effects of host plant development and genetic determinants on the long-distance movement of cauliflower mosaic virus in Arabidopsis. Plant Cell. 1993 Feb;5(2):191–202. doi: 10.1105/tpc.5.2.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riesmeier J. W., Hirner B., Frommer W. B. Potato sucrose transporter expression in minor veins indicates a role in phloem loading. Plant Cell. 1993 Nov;5(11):1591–1598. doi: 10.1105/tpc.5.11.1591. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schmalstig J. G., Geiger D. R. Phloem Unloading in Developing Leaves of Sugar Beet : I. Evidence for Pathway through the Symplast. Plant Physiol. 1985 Sep;79(1):237–241. doi: 10.1104/pp.79.1.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schmalstig J. G., Geiger D. R. Phloem Unloading in Developing Leaves of Sugar Beet : II. Termination of Phloem Unloading. Plant Physiol. 1987 Jan;83(1):49–52. doi: 10.1104/pp.83.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stadler R., Brandner J., Schulz A., Gahrtz M., Sauer N. Phloem Loading by the PmSUC2 Sucrose Carrier from Plantago major Occurs into Companion Cells. Plant Cell. 1995 Oct;7(10):1545–1554. doi: 10.1105/tpc.7.10.1545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Truernit E., Sauer N. The promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene directs expression of beta-glucuronidase to the phloem: evidence for phloem loading and unloading by SUC2. Planta. 1995;196(3):564–570. doi: 10.1007/BF00203657. [DOI] [PubMed] [Google Scholar]
- Turgeon R. Termination of nutrient import and development of vein loading capacity in albino tobacco leaves. Plant Physiol. 1984 Sep;76(1):45–48. doi: 10.1104/pp.76.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang N., Fisher D. B. The Use of Fluorescent Tracers to Characterize the Post-Phloem Transport Pathway in Maternal Tissues of Developing Wheat Grains. Plant Physiol. 1994 Jan;104(1):17–27. doi: 10.1104/pp.104.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
