The constitutive expression of Arabidopsis plasmodesmal-associated class 1 reversibly glycosylated polypeptide impairs plant development and virus spread

Journal of Experimental Botany

Volumn 61, Issue 1, 2010, Pages 131-142

  Zavaliev, Raul ^a   Sagi, Guy ^a   Gera, Abed ^b   Epel, Bernard L ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b VOLCANI CENTER   (Israel)

Author keywords

Callose; Plasmodesmata; Reversibly glycosylated polypeptide; Starch accumulation; Stunting; Tobacco mosaic virus; Virus spread

Indexed keywords

ARABIDOPSIS PROTEIN; CALLOSE; CARBON; CHLOROPHYLL; GLUCAN; GLYCOPROTEIN; GREEN FLUORESCENT PROTEIN; RGP1 PROTEIN, ARABIDOPSIS; STARCH;

ARABIDOPSIS; ARTICLE; CYTOLOGY; FLOWER; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYDROPONICS; METABOLISM; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLASMODESMA; TOBACCO; TOBACCO MOSAIC VIRUS; TRANSGENIC PLANT; VIROLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARBON RADIOISOTOPES; CHLOROPHYLL; FLOWERS; GLUCANS; GLYCOPROTEINS; GREEN FLUORESCENT PROTEINS; HYDROPONICS; PLANT DISEASES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PLASMODESMATA; STARCH; TOBACCO; TOBACCO MOSAIC VIRUS;

ARABIDOPSIS; NICOTIANA TABACUM; TOBACCO MOSAIC VIRUS;

EID: 72049124851     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erp301     Document Type: Article

References (40)

1. Almon E, Horowitz M, Wang HL, Lucas WJ, Zamski E, Wolf S. 1997. Phloem-specific expression of the Tobacco mosaic virus movement protein alters carbon metabolism and partitioning in transgenic potato plants. Plant Physiology 115, 1599-1607.
2. Arsenault JL, Pouleur S, Messier C, Guay R. 1995. WinRHIZO(TM), a root-measuring system with a unique overlap correction method. HortScience 30, 906.
3. Balachandran S, Hull RJ, Vaadia Y, Wolf S, Lucas WJ. 1995. Alteration in carbon partitioning induced by the movement protein of Tobacco mosaic virus originates in the mesophyll and is independent of change in the plasmodesmal size exclusion limit. Plant, Cell and Environment 18, 1301-1310.
4. Baluska F, Samaj J, Napier R, Volkmann D. 1999. Maize calreticulin localizes preferentially to plasmodesmata in root apex. The Plant Journal 19, 481-488.
5. Bayer E, Thomas CL, Maule AJ. 2004. Plasmodesmata in Arabidopsis thaliana suspension cells. Protoplasma 223, 93-102.
6. Biemelt S, Sonnewald U. 2006. Plant-microbe interactions to probe regulation of plant carbon metabolism. Journal of Plant Physiology 163, 307-318.
7. Crawford KM, Zambryski PC. 2001. Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. Plant Physiology 125, 1802-1812.
8. De Pino V, Boran M, Norambuena L, Gonzalez M, Reyes F, Orellana A, Moreno S. 2007. Complex formation regulates the glycosylation of the reversibly glycosylated polypeptide. Planta 226, 335-345.
9. Delgado IJ, Wang ZH, de Rocher A, Keegstra K, Raikhel NV. 1998. Cloning and characterization of AtRGP1: a reversibly autoglycosylated Arabidopsis protein implicated in cell wall biosynthesis. Plant Physiology 116, 1339-1349.
10. Dhugga KS. 2006. Golgi glucan synthases. In: Hayashi T, ed. The science and lore of the plant cell wall: biosynthesis, structure and function. Boca Raton: BrownWalker Press, 114-122.
11. Dhugga KS, Tiwari SC, Ray PM. 1997. A reversibly glycosylated polypeptide (RGP1) possibly involved in plant cell wall synthesis: purification, gene cloning, and trans-Golgi localization. Proceedings of the National Academy of Sciences, USA 94, 7679-7684.
12. Dhugga KS, Ulvskov P, Gallagher SR, Ray PM. 1991. Plant polypeptides reversibly glycosylated by UDP-glucose. Possible components of Golgi beta-glucan synthase in pea cells. Journal of Biological Chemistry 266, 21977-21984.
13. Drakakaki G, Zabotina O, Delgado I, Robert S, Keegstra K, Raikhel N. 2006. Arabidopsis reversibly glycosylated polypeptides 1 and 2 are essential for pollen development. Plant Physiology 142, 1480-1492.
14. Epel BL, Kuchuck B, Kotlizky G, Shurtz S, Erlanger M, Yahalom A. 1995. Isolation and characterization of plasmodesmata. Methods in Cell Biology 50, 237-253.
15. Epel BL, van Lent JWM, Cohen L, Kotlizky G, Katz A, Yahalom A. 1996. A 41 kDa protein isolated from maize mesocotyl cell walls immunolocalizes to plasmodesmata. Protoplasma 191, 70-78.
16. Faulkner CR, Blackman LM, Cordwell SJ, Overall RL. 2005. Proteomic identification of putative plasmodesmatal proteins from Chara corallina. Proteomics 5, 2866-2875.
17. Guenoune-Gelbart D, Elbaum M, Sagi G, Levy A, Epel BL. 2008. Tobacco mosaic virus (TMV) replicase and movement protein function synergistically in facilitating TMV spread by lateral diffusion in the plasmodesmal desmotubule of Nicotiana benthamiana. Molecular Plant-Microbe Interactions 21, 335-345.
18. Heinlein M, Epel BL. 2004. Macromolecular transport and signalling through plasmodesmata. International Review of Cytology 235, 93-164.
19. Herbers K, Tacke E, Hazirezaei M, Krause KP, Melzer M, Rohde W, Sonnewald U. 1997. Expression of a luteoviral movement protein in transgenic plants leads to carbohydrate accumulation and reduced photosynthetic capacity in source leaves. The Plant Journal 12, 1045-1056.
20. Herbers K, Takahata Y, Melzer M, Mock HP, Hajirezaei M, Sonnewald H. 2000. Regulation of carbohydrate partitioning during the interaction of Potato virus Y with tobacco. Molecular Plant Pathology 1, 51-59.
21. Hoagland DR, Arnon DI. 1950. The water-culture method of growing plants without soil. California Agricultural Experiment Station Circular 347.
22. Hofius D, Herbers K, Melzer M, Omid A, Tacke E, Wolf S, Sonnewald U. 2001. Evidence for expression level-dependent modulation of carbohydrate status and viral resistance by the Potato leaf roll virus movement protein in transgenic tobacco plants. The Plant Journal 28, 529-543.
23. Hull R. 2002. Matthews' plant virology: Academic Press.
24. Jones H, Martin RV, Porter HK. 1959. Translocation of 14carbon in tobacco following assimilation of 14carbon dioxide by a single leaf. Annals of Botany 23, 493-508.
25. Kobayashi K, Kim I, Cho E, Zambryski P. 2005. Plasmodesmata and plant morphogenesis. In: Oparka KJ, ed. Plasmodesmata. Annual Plant Reviews, Vol.18. Oxford: Blackwell Publishing, 90-112.
26. Kronberg K, Vogel F, Rutten T, Hajirezaei MR, Sonnewald U, Hofius D. 2007. The silver lining of a viral agent: increasing seed yield and harvest index in Arabidopsis by ectopic expression of the Potato leaf roll virus movement protein. Plant Physiology 145, 905-918.
27. Lalonde S, Wipf D, Frommer WB. 2004. Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annual Review of Plant Biology 55, 341-372.
28. Langeveld SM, Vennik M, Kottenhagen M, Van Wijk R, Buijk A, Kijne JW, de Pater S. 2002. Glucosylation activity and complex formation of two classes of reversibly glycosylated polypeptides. Plant Physiology 129, 278-289.
29. Lee JY, Taoka K, Yoo BC, Ben-Nissan G, Kim DJ, Lucas WJ. 2005. Plasmodesmal-associated protein kinase in tobacco and Arabidopsis recognizes a subset of non-cell-autonomous proteins. The Plant Cell 17, 2817-2831.
30. Levy A, Erlanger M, Rosenthal M, Epel BL. 2007. A plasmodesmata- associated beta-1,3-glucanase in Arabidopsis. The Plant Journal 49, 669-682.
31. Liarzi O, Epel BL. 2005. Development of a quantitative tool for measuring changes in the coefficient of conductivity of plasmodesmata induced by developmental, biotic, and abiotic signals. Protoplasma 225, 67-76.
32. McDaniel CN. 1996. Developmental physiology of floral initiation in Nicotiana tabacum L. Journal of Experimental Botany 47, 465-475.
33. Moran R. 1982. Formulae for determination of chlorophyllous pigments extracted with N,N-dimethylformamide. Plant Physiology 69, 1376-1381.
34. Olesinski AA, Almon E, Navot N, Perl A, Galun E, Lucas WJ, Wolf S. 1996. Tissue specific expression of the Tobacco mosaic virus movement protein in transgenic potato plants alters plasmodesmal function and carbohydrate partitioning. Plant Physiology 111, 541-550.
35. Rinne PL, van den Boogaard R, Mensink MG, Kopperud C, Kormelink R, Goldbach R, van der Schoot C. 2005. Tobacco plants respond to the constitutive expression of the tospovirus movement protein NS(M) with a heat-reversible sealing of plasmodesmata that impairs development. The Plant Journal 43, 688-707.
36. Sagi G, Katz A, Guenoune-Gelbart D, Epel BL. 2005. Class 1 reversibly glycosylated polypeptides are plasmodesmal-associated proteins delivered to plasmodesmata via the Golgi apparatus. The Plant Cell 17, 1788-1800.
37. Selth LA, Dogra SC, Rasheed MS, Randles JW, Rezaian MA. 2006. Identification and characterization of a host reversibly glycosylated peptide that interacts with the Tomato leaf curl virus V1 protein. Plant Molecular Biology 61, 297-310.
38. Testasecca P, Wald FA, Cozzarin ME, Moreno S. 2004. Regulation of self-glycosylation of reversibly glycosylated polypeptides from Solanum tuberosum. Physiologia Plantarum 121, 27-34.
39. Thomas CL, Bayer EM, Ritzenthaler C, Fernandez-Calvino L, Maule AJ. 2008. Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biology 6, e7.
40. Turgeon R, Webb JA. 1973. Leaf development and phloem transport in Cucurbita pepo: maturation of the minor veins. Planta 113, 179-191.