Functional specialization within the vacuolar sorting receptor family: VSR1, VSR3 and VSR4 sort vacuolar storage cargo in seeds and vegetative tissues

Plant Journal

Volumn 64, Issue 4, 2010, Pages 577-588

  Zouhar, Jan ^a   Muñoz, Alfonso ^a   Rojo, Enrique ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

gene family; germination; seed; sorting receptor; storage proteins; vacuole

Indexed keywords

EXPRESSION PATTERNS; FUNCTIONAL DATAS; GENE FAMILIES; GENETIC SCREENS; GERMINATION; MAP-BASED CLONING; RING-H2; SHOOT APEX; STORAGE PROTEINS; TRANSMEMBRANES; VACUOLE; VEGETATIVE TISSUE;

CLONING; GENES; HISTOLOGY; PROTEINS; SEED;

SORTING;

ARABIDOPSIS PROTEIN; CELL RECEPTOR; CLV3 PROTEIN, ARABIDOPSIS; DIAGNOSTIC AGENT; ELP PROTEIN, ARABIDOPSIS; HYBRID PROTEIN; MEMBRANE PROTEIN; RMR1 PROTEIN, ARABIDOPSIS; SEED STORAGE PROTEIN; VSR3 PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CELL VACUOLE; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PLANT; PLANT LEAF; PLANT SEED;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; GERMINATION; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PLANT LEAVES; PLANT SHOOTS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT FUSION PROTEINS; SEED STORAGE PROTEINS; SEEDS; VACUOLES;

EID: 78449233232     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04349.x     Document Type: Article

References (42)

1. 2-terminal propeptide-containing vacuolar proteins in Arabidopsis thaliana. J. Cell Biol. 149, 1335-1344.
2. Andreasson, E., Bolt Jorgensen, L., Hoglund, A.S., Rask, L., and, Meijer, J., (2001) Different myrosinase and idioblast distribution in Arabidopsis and Brassica napus. Plant Physiol. 127, 1750-1763.
3. Avila, E.L., Brown, M., Pan, S., Desikan, R., Neill, S.J., Girke, T., Surpin, M., and, Raikhel, N.V., (2008) Expression analysis of Arabidopsis vacuolar sorting receptor 3 reveals a putative function in guard cells. J. Exp. Bot. 59, 1149-1161.
4. 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.
5. Castelli, S., and, Vitale, A., (2005) The phaseolin vacuolar sorting signal promotes transient, strong membrane association and aggregation of the bean storage protein in transgenic tobacco. J. Exp. Bot. 56, 1379-1387.
6. Craddock, C.P., Hunter, P.R., Szakacs, E., Hinz, G., Robinson, D.G., and, Frigerio, L., (2008) Lack of a vacuolar sorting receptor leads to non-specific missorting of soluble vacuolar proteins in Arabidopsis seeds. Traffic, 9, 408-416.
7. Crofts, A.J., Leborgne-Castel, N., Hillmer, S., Robinson, D.G., Phillipson, B., Carlsson, L.E., Ashford, D.A., and, Denecke, J., (1999) Saturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow. Plant Cell, 11, 2233-2248.
8. Denecke, J., Botterman, J., and, Deblaere, R., (1990) Protein secretion in plant cells can occur via a default pathway. Plant Cell, 2, 51-59.
9. Ebine, K., Okatani, Y., Uemura, T., etal. (2008) A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. Plant Cell, 20, 3006-3021.
10. Fuji, K., Shimada, T., Takahashi, H., Tamura, K., Koumoto, Y., Utsumi, S., Nishizawa, K., Maruyama, N., and, Hara-Nishimura, I., (2007) Arabidopsis vacuolar sorting mutants (green fluorescent seed) can be identified efficiently by secretion of vacuole-targeted green fluorescent protein in their seeds. Plant Cell, 19, 597-609.
11. Ghosh, P., Dahms, N.M., and, Kornfeld, S., (2003) Mannose 6-phosphate receptors: new twists in the tale. Nat. Rev. Mol. Cell Biol. 4, 202-212. (Pubitemid 36288042)
12. Hinz, G., Colanesi, S., Hillmer, S., Rogers, J.C., and, Robinson, D.G., (2007) Localization of vacuolar transport receptors and cargo proteins in the Golgi apparatus of developing Arabidopsis embryos. Traffic, 8, 1452-1464.
13. Jolliffe, N.A., Brown, J.C., Neumann, U., Vicre, M., Bachi, A., Hawes, C., Ceriotti, A., Roberts, L.M., and, Frigerio, L., (2004) Transport of ricin and 2S albumin precursors to the storage vacuoles of Ricinus communis endosperm involves the Golgi and VSR-like receptors. Plant J. 39, 821-833.
14. 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.
15. Laval, V., Masclaux, F., Serin, A., Carriere, M., Roldan, C., Devic, M., Pont-Lezica, R.F., and, Galaud, J.P., (2003) Seed germination is blocked in Arabidopsis putative vacuolar sorting receptor (atbp80) antisense transformants. J. Exp. Bot. 54, 213-221.
16. Li, L., Shimada, T., Takahashi, H., Ueda, H., Fukao, Y., Kondo, M., Nishimura, M., and, Hara-Nishimura, I., (2006) MAIGO2 is involved in exit of seed storage proteins from the endoplasmic reticulum in Arabidopsis thaliana. Plant Cell, 18, 3535-3547.
17. Von Lupke, A., Schauermann, G., Feussner, I., and, Hinz, G., (2008) Peripheral membrane proteins mediate binding of vacuolar storage proteins to membranes of the secretory pathway of developing pea cotyledons. J. Exp. Bot. 59, 1327-1340.
18. Manfield, I.W., Jen, C.H., Pinney, J.W., Michalopoulos, I., Bradford, J.R., Gilmartin, P.M., and, Westhead, D.R., (2006) Arabidopsis co-expression tool (ACT): web server tools for microarray-based gene expression analysis. Nucleic Acids Res. 34, W504-W509.
19. Marcusson, E.G., Horazdovsky, B.F., Cereghino, J.L., Gharakhanian, E., and, Emr, S.D., (1994) The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell, 77, 579-586.
20. Miao, Y., Yan, P.K., Kim, H., Hwang, I., and, Jiang, L., (2006) Localization of green fluorescent protein fusions with the seven Arabidopsis vacuolar sorting receptors to prevacuolar compartments in tobacco BY-2 cells. Plant Physiol. 142, 945-962.
21. Niemes, S., Langhans, M., Viotti, C., Scheuring, D., San Wan Yan, M., Jiang, L., Hillmer, S., Robinson, D.G., and, Pimpl, P., (2010) Retromer recycles vacuolar sorting receptors from the trans-Golgi network. Plant J. 61, 107-121.
22. Oliviusson, P., Heinzerling, O., Hillmer, S., Hinz, G., Tse, Y.C., Jiang, L., and, Robinson, D.G., (2006) Plant retromer, localized to the prevacuolar compartment and microvesicles in Arabidopsis, may interact with vacuolar sorting receptors. Plant Cell, 18, 1239-1252.
23. Otegui, M.S., Herder, R., Schulze, J., Jung, R., and, Staehelin, L.A., (2006) The proteolytic processing of seed storage proteins in Arabidopsis embryo cells starts in the multivesicular bodies. Plant Cell, 18, 2567-2581.
24. Park, M., Lee, D., Lee, G.J., and, Hwang, I., (2005) AtRMR1 functions as a cargo receptor for protein trafficking to the protein storage vacuole. J. Cell Biol. 170, 757-767.
25. Park, J.H., Oufattole, M., and, Rogers, J.C., (2007) Golgi-mediated vacuolar sorting in plant cells: RMR proteins are sorting receptors for the protein aggregation/membrane internalization pathway. Plant Sci. 172, 728.
26. Petersen, C.M., Nielsen, M.S., Nykjaer, A., Jacobsen, L., Tommerup, N., Rasmussen, H.H., Roigaard, H., Gliemann, J., Madsen, P., and, Moestrup, S.K., (1997) Molecular identification of a novel candidate sorting receptor purified from human brain by receptor-associated protein affinity chromatography. J. Biol. Chem. 272, 3599-3605.
27. Phillipson, B.A., Pimpl, P., DaSilva, L.L., Crofts, A.J., Taylor, J.P., Movafeghi, A., Robinson, D.G., and, Denecke, J., (2001) Secretory bulk flow of soluble proteins is efficient and COPII dependent. Plant Cell, 13, 2005-2020.
28. Pompa, A., De Marchis, F., Vitale, A., Arcioni, S., and, Bellucci, M., (2010) An engineered C-terminal disulfide bond can partially replace the phaseolin vacuolar sorting signal. Plant J. 61, 782-791.
29. Rojo, E., Sharma, V.K., Kovaleva, V., Raikhel, N.V., and, Fletcher, J.C., (2002) CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell, 14, 969-977.
30. Rojo, E., Zouhar, J., Carter, C., Kovaleva, V., and, Raikhel, N.V., (2003) A unique mechanism for protein processing and degradation in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 100, 7389-7394.
31. 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.
32. Sanmartin, M., Ordonez, A., Sohn, E.J., Robert, S., Sanchez-Serrano, J.J., Surpin, M.A., Raikhel, N.V., and, Rojo, E., (2007) Divergent functions of VTI12 and VTI11 in trafficking to storage and lytic vacuoles in Arabidopsis. Proc. Natl Acad. Sci. USA, 104, 3645-3650.
33. Santos-Mendoza, M., Dubreucq, B., Baud, S., Parcy, F., Caboche, M., and, Lepiniec, L., (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J. 54, 608-620.
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. DaSilva, L.L., Taylor, J.P., Hadlington, J.L., Hanton, S.L., Snowden, C.J., Fox, S.J., Foresti, O., Brandizzi, F., and, Denecke, J., (2005) Receptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell, 17, 132-148.
36. Sohn, E.J., Rojas-Pierce, M., Pan, S., Carter, C., Serrano-Mislata, A., Madueno, F., Rojo, E., Surpin, M., and, Raikhel, N.V., (2007) The shoot meristem identity gene TFL1 is involved in flower development and trafficking to the protein storage vacuole. Proc. Natl Acad. Sci. USA, 104, 18801-18806.
37. Tucker, M.R., and, Laux, T., (2007) Connecting the paths in plant stem cell regulation. Trends Cell Biol. 17, 403-410.
38. Wang, D., Weaver, N.D., Kesarwani, M., and, Dong, X., (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science, 308, 1036-1040.
39. 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.
40. Watanabe, E., Shimada, T., Tamura, K., Matsushima, R., Koumoto, Y., Nishimura, M., and, Hara-Nishimura, I., (2004) An ER-localized form of PV72, a seed-specific vacuolar sorting receptor, interferes the transport of an NPIR-containing proteinase in Arabidopsis leaves. Plant Cell Physiol. 45, 9-17.
41. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and, Gruissem, W., (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.
42. Zouhar, J., Rojo, E., and, Bassham, D.C., (2009) AtVPS45 is a positive regulator of the SYP41/SYP61/VTI12 SNARE complex involved in trafficking of vacuolar cargo. Plant Physiol. 149, 1668-1678.