Connections between virus movement, macromolecular signaling and assimilate allocation

Current Opinion in Plant Biology

Volumn 2, Issue 3, 1999, Pages 192-197

  Lucas, William J ^a   Wolf, Shmuel ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0033151543     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5266(99)80035-1     Document Type: Article

References (51)

1. Lucas WJ, Gilbertson RL: Plasmodesmata in relation to viral movement within leaf tissues. Annu Rev Phytopath 1994, 32:387-411.
2. Carrington JC, Kasschau KD, Mahajan SK, Schaad MC: Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 1996, 8:1669-1681.
3. Itaya A, Hickman H, Bao YM, Nelson R, Ding B: Cell-to-cell trafficking of cucumber mosaic virus movement protein green fluorescent protein fusion produced by biolistic gene bombardment in tobacco. Plant J 1997, 2:1223-1230.
4. Itaya A, Woo YM, Masuta C, Bao Y, Nelson RS, Ding B: Developmental regulation of intercellular protein trafficking through plasmodesmata in tobacco leaf epidermis. Plant Physiol 1998, 118:373-385.
5. Oparka KJ, Prior DA, Santa Cruz S, Padgett HS, Beachy RN: Gating of epidermal plasmodesmata is restricted to the leading edge of expanding infection sites of tobacco mosaic virus (TMV). Plant J 1997, 12:781-789.
6. Canto T, Prior DA, Hellwald KH, Oparka KJ, Palukaitis P: Characterization of cucumber mosaic virus. IV. Movement protein and coat protein are both essential for cell-to-cell movement of cucumber mosaic virus. Virology 1997, 237:237-248.
7. Blackman LM, Boevink P, Cruz SS, Palukaitis P, Oparka KJ: The movement protein of cucumber mosaic virus traffics into sieve elements in minor veins of Nicotiana clevelandii. Plant Cell 1998, 10:525-538. This work reports on the transport of a viral movement protein through the plasmodesmata connecting the companion cells to their neighboring functional (enucleate) sieve elements.
8. Reichel C, Beachy RN: Tobacco mosaic virus infection induces severe morphological changes of the endoplasmic reticulum. Proc Natl Acad Sci USA 1998, 95:11169-11174.
9. Lucas WJ, Wolf S: Plasmodesmata: The intercellular organelle of green plants. Trends Cell Biol 1993, 3:308-315.
10. Lucas WJ, Bouché-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S: Selective trafficking of KNOTTED1 and its mRNA through plant plasmodesmata. Science 1995, 270:1980-1983.
11. Mezitt LM, Lucas WJ: Plasmodesmal cell-to-cell transport of proteins and nucleic acids. Plant Mol Biol 1996, 32:251-273.
12. Balachandran S, Xiang Y, Schobert C, Thompson GA, Lucas WJ: Phloem sap proteins of Cucurbita maxima and Ricinus communis have the capacity to traffic cell to cell through plasmodesmata. Proc Natl Acad Sci USA 1997, 94:14150-14155. This paper describes microinjection experiments in which proteins present in the phloem translocation stream were shown to have the capacity to interact with plasmodesmata to mediate their own cell-to-cell transport. This work identified the phloem sap as an important source of proteins for the study of supracellular control over plant processes.
13. Ishiwatari Y, Fujiwara T, McFarland KC, Nemoto K, Hayashi H, Chino M, Lucas WJ: Rice phloem thioredoxin h has the capacity to mediate its own cell-to-cell transport through plasmodesmata. Planta 1998, 205:12-22.
14. Perbal MC, Haughn G, Saedler H, Schwarz-Sommer Z: Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 1996, 122:3433-3441.
15. Kragler F, Monzer J, Shash K, Xoconostle-Cázares B, Lucas WJ: Cell to-cell transport of proteins: Requirement for unfolding and characterization of binding to a putative plasmodesmal receptor. Plant J 1998, 15:367-381. A range of techniques were employed to probe the events associated with the transport of proteins through plasmodesmal micro-channels. These experiments established that viral MP and endogenous proteins interact with a common plasmodesmal receptor. Additionally, these authors were successful in developing a method that permitted the isolation and direct analysis of endogenous proteins involved in macromolecular transport through plasmodesmata.
16. Xoconostle-Cázares B, Xiang Y, Ruiz-Medrano R, Wang H-L, Monzer J, Yoo B-C, McFarland KC, Franceschi VR, Lucas WJ: Plant paralog to viral movement protein potentiates transport of mRNA into the phloem. Science 1999, 283:94-98. This study reports on the application of an antibody directed against a viral movement protein to identify a protein in the phloem sap of pumpkin that has properties equivalent to its viral paralog. A combination of microinjection and grafting experiments provided evidence that this protein mediates the entry of RNA into the phloem long-distance translocation stream.
17. Jorgensen RA, Atkinson RG, Forster RLS, Lucas WJ: An RNA-based information superhighway in plants. Science 1998, 279:1486-1487. A plasmodesmal-based model is developed to explain results from plant and viral studies indicating the operation of post-transcriptional gene silencing and systemic acquired silencing in plants.
18. Kühn C, Franceschi VR, Schulz A, Lemoine R, Frommer WB: Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 1997, 275:1298-1300. This study provides the first direct evidence of RNA trafficking from the companion cells, via plasmodesmata, into the enucleate sieve elements.
19. Golecki B, Schulz A, Thompson GA: Translocation of structural P proteins in the phloem. Plant Cell 1999, 11:127-140.
20. Imlau A, Truernit E, Sauer N: Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 1999, 11:309-322.
21. Sasaki T, Chino M, Hayashi H, Fujiwara T: Detection of several mRNA species in rice phloem sap. Plant Cell Physiol 1998, 39:895-897.
22. Palauqui JC, Elmayan T, Pollien JM, Vaucheret H: Systemic acquired silencing: Transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 1997, 16:4738-4745. In this study, the authors used heterografts between various transgenic tobacco lines to prove that cosuppression of the nitrate reductase gene, in developing leaves, involves the transmission of a sequence-specific signal via the phloem. An RNA molecule is the most likely candidate for this signal [17•].
23. Palauqui JC, Vaucheret H: Transgenes are dispensable for the RNA degradation step of cosuppression. Proc Natl Acad Sci USA 1998, 95:9675-9680.
24. Lindbo JA, Silva-Rosales L, Proebsting WM, Dougherty WG: Induction of a highly specific antiviral state in transgenic plants: Implications for regulation of gene expression and virus resistance. Plant Cell 1993, 5:1749-1759.
25. Tanzer MM, Thompson WF, Law MD, Wernsman EA, Uknes S: Characterization of post-transcriptionally suppressed transgene expression that confers resistance to tobacco etch virus infection in tobacco. Plant Cell 1997, 9:1411-1423.
26. Ratcliff F, Harrison BD, Baulcombe DC: A similarity between viral defense and gene silencing in plants. Science 1997, 276:1558-1560.
27. Ruiz MT, Voinnet O, Baulcombe DC: Initiation and maintenance of virus-induced gene silencing. Plant Cell 1998, 10:937-946. This study demonstrated that an endogenous gene, the phytoene desaturase (PDS) of Nicotiana benthamiana, could be silenced by infecting plants with a virus vector carrying inserts of the PDS gene. Comparative experiments performed using PDS and GFP provided important insights into initiation of post-transcriptional gene silencing, its tissue specificity and the maintenance of the systemic acquired silencing condition.
28. Al-Kaff NS, Covey SN, Kreike MM, Page AM, Pinder R, Dale PJ: Transcriptional and post-transcriptional plant gene silencing in response to a pathogen. Science 1998, 279:2113-2115.
29. Brigneti G, Voinnet O, Li WX, Ji LH, Ding SW, Baulcombe DC: Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 1998, 17:6739-6746. In this elegant study, the HC-Pro of potato virus Y and the 2b gene of cucumber mosaic virus are shown to act as suppressors of systemic acquired silencing. Interestingly, HC-Pro appears to block the maintenance of post-transcriptional gene silencing in tissues where silencing has already been activated, whereas the 2b gene seems to interfere, in some way, with the initiation of post-transcriptional gene silencing in developing sink organs.
30. Kasschau KD, Carrington JC: A counterdefensive strategy of plant viruses: Suppression of posttranscriptional gene silencing. Cell 1998, 95:461-470. Plants expressing β-glucuronidase (GUS) as a transgene were used as a tool to identify the potyviral component involved in interdiction of the host antiviral surveillance system. Genetic crosses and segregation analysis revealed that the P1/HC-Pro transgene suppressed post-transcriptional gene silencing of the GUS transcript. Nuclear run-on assays confirmed that P1/HC-Pro acts at the post-transcriptional level.
31. Anandalakshmi R, Pruss GJ, Ge X, Marathe R, Mallory AC, Smith TH, Vance VB: A viral suppressor of gene silencing in plants. Proc Natl Acad Sci USA 1998, 95:13079-13084.
32. Beclin C, Berthome R, Palauqui JC, Tepfer M, Vaucheret H: Infection of tobacco or Arabidopsis plants by CMV counteracts systemic post-transcriptional silencing of nonviral (trans)genes. Virology 1998, 252:313-317.
33. Voinnet O, Vain P, Angell S, Baulcombe DC: Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 1998, 95:177-187. Experiments presented in this paper demonstrate that sequence-specific post-transcriptional gene silencing can be initiated within a small group of cells in a mature source leaf. Although the spread of the post-transcriptional gene silencing condition was slow, it was able to move, via the phloem, to initiate systemic acquired silencing in developing sink leaves.
34. Thorpe MR, Minchin PEH: Mechanisms of long-and short-distance transport from sources to sinks. In Photoassimilate Distribution in Plants and Crops: Source-Sink Relationships. Edited by Zamski E, Schaffer AA. New York: Dekker, 1996:261-282.
35. Pollock CJ: Resource use efficiency and crop performance: What is the link? In A Molecular Approach to Primary Metabolism in Plants. Edited by Foyer CH, Quick P. London: Taylor and Francis; 1997:327-336.
36. Patrick JW: Phloem unloading: Sieve element unloading and post sieve element transport. Annu Rev Plant Physiol Plant Mol Biol 1997, 48:191-222.
37. Stitt M: Plasmodesmata play an essential role in sucrose export from leaves: A step toward an integration of metabolic biochemistry and cell biology. Plant Cell 1996, 8:565-571.
38. Lucas WJ, Olesinski A, Hull RJ, Haudenshield J, Deom CM, Beachy RN, Wolf S: Influence of the tobacco mosaic virus 30-kDa movement protein on carbon metabolism and photosynthate partitioning in transgenic tobacco plants. Planta 1993, 190:88-96.
39. Olesinski AA, Lucas WJ, Galun E, Wolf S: Pleiotropic effect of tobacco mosaic virus movement protein on carbon metabolism in transgenic tobacco plants. Planta 1995, 197:118-126.
40. Herbers K, Tacke E, Hazirezaei M, Krause K-P, Melzer M, Rohde W, Sonnewald U: Expression of a luteoviral movement protein in transgenic plants leads to carbohydrate accumulation and reduced photosynthetic capacity in source leaves. Plant J 1997, 12:1045-1056.
41. Tecsi LI, Smith AM, Maule AJ, Leegood RC: Relationships between viral infection and carbohydrate accumulation and metabolism. In Carbon Partitioning and Source-Sink Interactions in Plants. Edited by Madore MA, Lucas WJ. Rockville, Maryland: American Society of Plant Physiologists; 1995:130-140.
42. Tecsi LI, Maule AJ, Smith AM, Leegood RC: A spatial analysis of physiological changes associated with infection of cotyledons of marrow plants with cucumber mosaic virus. Plant Physiol 1996, 111:975-985.
43. 2 assimilation and starch content associated with the susceptible interaction between cucumber mosaic virus and a cucurbit host. Plant J 1994, 5:837-847.
44. Wolf S, Lucas WJ: Plasmodesmatal-mediated plant communication network: Implications for controlling carbon metabolism and resource allocation. In A Molecular Approach to Primary Metabolism in Plants. Edited by Foyer CH, Quick P. London: Taylor and Francis; 1997:219-236.
45. Balachandran S, Hull R, Vaadia Y, Wolf S, Lucas WJ: Alteration in carbon partitioning induced by the movement protein of tobacco mosaic virus originates in the mesophyll and is independent of change in plasmodesmal size exclusion limit. Plant Cell Environ 1995, 18:1301-1310.
46. Balachandran S, Hull R, Martins RJ, Vaadia Y, Lucas WJ: Influence of environmental stress on biomass partitioning in transgenic tobacco plants expressing the movement protein of tobacco mosaic virus. Plant Physiol 1997, 114:475-481.
47. Almon E, Horowitz M, Wang H-L, Lucas WJ, Zamski E, Wolf S: Phloem-specific expression of TMV-MP alters carbon metabolism and partitioning in transgenic potato plants. Plant Physiol 1997, 115:1599-1607. Physiological studies conducted on transgenic potato plants expressing the TMV-MP under different promoters provided further evidence that the TMV-MP can interfere with a putative endogenous communication network that controls resource allocation within the plant.
48. Olesinski AA, Almon E, Navot N, Perl A, Galun E, Lucas WJ, Wolf S: Tissue-specific expression of the tobacco mosaic virus movement protein in transgenic potato plants alters plasmodesmal function and carbohydrate partitioning. Plant Physiol 1996, 111:541-550.
49. Lucas WJ, Balachandran S, Park J, Wolf S: Plasmodesmal companion cell-mesophyll communication in the control over carbon metabolism and phloem transport: Insight gained from viral movement proteins. J Exp Bot 1996, 47:1119-1128.
50. 2 environment surrounding the whole plant. These experiments provide strong support for the hypothesis that plants integrate photosynthetic capacity on a whole-plant basis.
51. Scheible W-R, Lauerer M, Schulze E-D, Caboche M, Stitt M: Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco. Plant J 1997, 11:671-691.