Transport of ricin and 2S albumin precursors to the storage vacuoles of Ricinus communis endosperm involves the Golgi and VSR-like receptors

Plant Journal

Volumn 39, Issue 6, 2004, Pages 821-833

  Jolliffe, Nicholas A ^a   Brown, Joanna C ^a   Neumann, Ulla ^b   Vicré, Maïte ^b   Bachi, Angela ^c   Hawes, Chris ^b   Ceriotti, Aldo ^d   Roberts, Lynne M ^a   Frigerio, Lorenzo ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b OXFORD BROOKES UNIVERSITY   (United Kingdom)

^c Mass Spectrometry Laboratory   (Italy)

^d CNR Consiglio Nazionale delle Ricerche   (Italy)

Author keywords

Albumin; Ricin; Sorting receptor; Storage proteins; Vacuole

Indexed keywords

CELLS; ELECTRON MICROSCOPY; PROTEINS;

CELL FRACTIONATION; IMMUNOELECTRON MICROSCOPY; RICIN;

PLANTS (BOTANY);

CELLS; ELECTRON MICROSCOPY; PLANTS; PROTEINS;

CASTOR; PHASEOLUS (ANGIOSPERM); RICINUS COMMUNIS;

EID: 4944242360     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02167.x     Document Type: Article

References (42)

1. Ahmed, S.U., Bar-Peled, M. and Raikhel, N.V. (1997) Cloning and subcellular location of an Arabidopsis receptor-like protein that shares common features with protein-sorting receptors of eukaryotic cells. Plant Physiol. 114, 325-336.
2. Anelli, T., Alessio, M., Mezghrani, A., Simmen, T., Talamo, F., Bachi, A. and Sitia, R. (2002) ERp44, a novel endoplasmic reticulum folding assistant of the thioredoxin family. EMBO J. 21, 835-844.
3. Bassham, D. C. and Raikhel, N. V. (2000) Unique features of the plant vacuolar sorting machinery. Curr. Opin. Cell Biol. 12, 491-495.
4. Bollini, R. and Chrispeels, M.J. (1979) The rough endoplasmic reticulum is the site of reserve-protein synthesis in developing Phaseolus vulgaris cotyledons. Planta, 146, 487-501.
5. Brown, J.C., Jolliffe, N.A., Frigerio, L. and Roberts, L.M. (2003) Sequence-specific, Golgi-dependent targeting of the castor bean 2S albumin to the vacuole in tobacco protoplasts. Plant J. 36, 711-719.
6. Cao, X., Rogers, S.W., Butler, J., Beevers, L. and Rogers, J.C. (2000) Structural requirements for ligand binding by a probable plant vacuolar sorting receptor. Plant Cell, 12, 493-506.
7. Frigerio, L., Vitale, A., Lord, J.M., Ceriotti, A. and Roberts, L.M. (1998) Free ricin A chain, proricin and native toxin have different cellular fates when expressed in tobacco protoplasts. J. Biol. Chem. 273, 14194-14199.
8. Frigerio, L., Jolliffe, N.A., Di Cola, A., Hernández Felipe, D., Paris, N., Neuhaus, J.-M., Lord, J.M., Ceriotti, A. and Roberts, L.M. (2001) The internal propeptide of the ricin precursor carries a sequence-specific determinant for vacuolar sorting. Plant Physiol. 126, 167-175.
9. Fukusawa, T., Hara-Nishimura, I. and Nishimura, M. (1988) Biosynthesis, intracellular transport and in vivo processing of 11S globulin precursor proteins of developing castor bean endosperm. Plant Cell Physiol. 29, 339-345.
10. Fulton, R.J., Blakey, D.C., Knowles, P.P., Uhr, J.W., Thorpe, P.E. and Vitetta, E.S. (1986) Purification of ricin A1, A2, and B chains and characterization of their toxicity. J. Biol. Chem. 261, 5314-5319.
11. Gietl, C. and Schmid, M. (2001) Ricinosomes: an organelle for developmentally regulated programmed cell death in senescing plant tissues. Naturwissenschaften, 88, 49-58.
12. Gifford, D., Greenwood, J. and Bewley, J. (1982) Deposition of matrix and crystalloid storage proteins during protein body development in the endosperm of Ricinus communis L. - cv Hale seeds. Plant Physiol. 69, 1471-1478.
13. Hara-Nishimura, I., Shimada, T., Hatano, K., Takeuchi, Y. and Nishimura, M. (1998) Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles. Plant Cell, 10, 825-836.
14. Hillmer, S., Movafeghi, A., Robinson, D.G. and Hinz, G. (2001) Vacuolar storage proteins are sorted in the cis-cisternae of the pea cotyledon Golgi apparatus. J. Cell Biol. 152, 41-50.
15. Irwin, S.D., Keen, J.N., Findlay, J.B.C. and Lord, J.M. (1990) The Ricinus communis 2S albumin precursor: a single preproprotein may be processed into two different heterodimeric storage proteins. Mol. Gen. Genet. 222, 400-408.
16. Jauh, G.-Y., Phillips, T.E. and Rogers, J.C. (1999) Tonoplast intrinsic protein isoforms as markers for vacuolar functions. Plant Cell, 11, 1867-1882.
17. Johnson, K.D., Höfte, H. and Chrispeels, M.J. (1990) An intrinsic tonoplast protein of protein storage vacuoles in seeds is structurally related to a bacterial solute transporter (GlpF). Plant Cell, 2, 525-532.
18. Jolliffe, N.A., Ceriotti, A., Frigerio, L. and Roberts, L.M. (2003) The position of the proricin vacuolar targeting signal is functionally important. Plant Mol. Biol. 51, 631-641.
19. Kirsch, T., Paris, N., Butler, J.M., Beevers, L. and Rogers, J.C. (1994) Purification and initial characterization of a potential plant vacuolar targeting receptor. Proc. Natl Acad. Sci. USA, 91, 3403-3407.
20. Kirsch, T., Saalbach, G., Raikhel, N. V. and Beevers, L. (1996) Interaction of a potential vacuolar targeting receptor with amino- and carboxyl-terminal targeting determinants. Plant Physiol. 111, 469-474.
21. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
22. Lainé, A.-C., Gomord, V. and Faye, L. (1991) Xylose-specific antibodies as markers of subcompartmentation of terminal glycosylation in the Golgi apparatus of sycamore cells. FEBS Lett. 295, 179-184.
23. Lord, J.M. (1985a) Precursors of ricin and Ricinus communis agglutinin. Glycosylation and processing during synthesis and intracellular transport. Eur. J. Biochem. 146, 411-416.
24. Lord, J.M. (1985b) Synthesis and intracellular transport of lectin and storage protein precursors in endosperm from castor bean. Eur. J. Biochem. 146, 403-409.
25. Lord, J. and Harley, S. (1985) Ricinus communis agglutinin B-chain contains a fucosylated oligosaccharide side-chain not present on ricin B-chain. FEBS Lett. 189, 72-76.
26. Matsuoka, K. and Neuhaus, J.-M. (1999) Cis-elements of protein transport to the plant vacuoles. J. Exp. Bot. 50, 165-174.
27. Pantoja-Uceda, D., Bruix, M., Gimenez-Gallego, G., Rico, M. and Santoro, J. (2003) Solution structure of RicC3, a 2S albumin storage protein from Ricinus communis. Biochemistry, 42, 13839-13847.
28. Paris, N. and Neuhaus, J.M. (2002) BP-80 as a vacuolar sorting receptor. Plant Mol. Biol. 50, 903-914.
29. Pedrazzini, E., Giovinazzo, G., Bielli, A., de Virgilio, M., Frigerio, L., Pesca, M., Faoro, F., Bollini, R., Ceriotti, A. and Vitale, A. (1997) Protein quality control along the route to the plant vacuole. Plant Cell 9, 1869-1880.
30. Sanderfoot, A.A., Ahmed, S.U., Marty-Mazars, D., Rapoport, I., Kirchhausen, T., Marty, F. and Raikhel, N.V. (1998) A putative vacuolar cargo receptor partially colocalizes with AtPEP12p on a prevacuolar compartment in Arabidopsis roots. Proc. Natl Acad. Sci. USA, 95, 9920-9925.
31. Schmid, M., Simpson, D.J., Sarioglu, H., Lottspeich, F. and Gietl, C. (2001) The ricinosomes of senescing plant tissue bud from the endoplasmic reticulum. Proc. Natl Acad. Sci. USA, 98, 5353-5358.
32. Shimada, T., Kuroyanagi, M., Nishimura, M. and Hara-Nishimura, I. (1997) A pumpkin 72-kDa membrane protein of precursor accumulating vesicles has characteristics of a vacuolar sorting receptor. Plant Cell Physiol. 38, 1414-1420.
33. Shimada, T., Watanabe, E., Tamura, K., Hayashi, Y., Nishimura, M. and Hara-Nishimura, I. (2002) A vacuolar sorting receptor PV72 on the membrane of vesicles that accumulate precursors of seed storage proteins (PAC vesicles). Plant Cell Physiol 43, 1086-1095.
34. Shimada, T., Fuji, K., Tamura, K., Kondo, M., Nishimura, M. and Hara-Nishimura, I. (2003) Vacuolar sorting receptor for seed storage proteins in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 100, 16095-16100.
35. Shy, G., Ehler, L., Herman, E. and Galili, G. (2001) Expression patterns of genes encoding endomembrane proteins support a reduced function of the Golgi in wheat endosperm during the onset of storage protein deposition. J Exp Bot 52, 2387-2388.
36. Spurr, A.R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31-43.
37. Steinbrecht, R. and Müller, M. (1987) Freeze-substitution and freeze-drying, in: Freeze-substitution and freeze-drying, Springer Verlag, Berlin, 149-172.
38. Studer, D., Graber, W., Al-Amoudi, A. and Eggli, P. (2001) A new approach for cryofixation by high-pressure freezing. J. Microsc. 203, 285-294.
39. Tully, R.E. and Beevers, H. (1976) Protein bodies of castor bean endosperms. Isolation, fractionation and characterisation of protein components. Plant Physiol. 58, 710-716.
40. Vitale, A. and Raikhel, N. V. (1999) What do proteins need to reach different vacuoles? Trends Plant Sci. 4, 149-155.
41. Watanabe, E., Shimada, T., Kuroyanagi, M., Nishimura, M. and Hara-Nishimura, I. (2002) Calcium-mediated association of a putative vacuolar sorting receptor PV72 with a propeptide of 2S albumin. J Biol Chem 277, 8708-8715.
42. Youle, R.J. and Huang, A.H.C. (1976) Protein bodies from the endosperm of castor bean. Subfractionation, protein components, lectins and changes during germination. Plant Physiol. 58, 703-709.