A fluorescent reporter protein containing AtRMR1 domains is targeted to the storage and central vacuoles in Arabidopsis thaliana and tobacco leaf cells

Plant Cell Reports

Volumn 30, Issue 10, 2011, Pages 1823-1833

  Scabone, Camila María ^a   Frigerio, Lorenzo ^b   Petruccelli, Silvana ^a  

^a CENTRO DE INVESTIGACIÓN Y DESARROLLO EN CRIOTECNOLOGÍA DE ALIMENTOS CIDCA   (Argentina)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Membrane proteins; Plant expression; PSV; RMR; Seed expression; Vacuolar sorting signal

Indexed keywords

ARABIDOPSIS PROTEIN; MEMBRANE PROTEIN; RMR1 PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CELL VACUOLE; CONFOCAL MICROSCOPY; CYTOLOGY; FLUORESCENCE; GENETICS; METABOLISM; MOLECULAR GENETICS; PLANT LEAF; PROTEIN TRANSPORT; REPORTER GENE; TOBACCO; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLUORESCENCE; GENES, REPORTER; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PROTEIN TRANSPORT; TOBACCO; VACUOLES;

ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA TABACUM;

EID: 80052758370     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-011-1089-8     Document Type: Article

References (57)

1. Ahmed SU, Bar-Peled M, Raikhel NV (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. Barrieu F, Chrispeels MJ (1999) Delivery of a secreted soluble protein to the vacuole via a membrane anchor. Plant Physiol 120: 961-968.
3. Batoko H, Zheng HQ, Hawes C, Moore I (2000) A Rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell 12: 2201-2218.
4. Benchabane M, Goulet C, Rivard D, Faye L, Gomord V, Michaud D (2008) Preventing unintended proteolysis in plant protein biofactories. Plant Biotechnol J 6: 633-648.
5. Boevink P, SantaCruz S, Hawes C, Harris N, Oparka KJ (1996) Virus-mediated delivery of the green fluorescent protein to the endoplasmic reticulum of plant cells. Plant J 10(5): 935-941.
6. Brandizzi F, Snapp E, Roberts A, Lippincott-Schwartz J, Hawes C (2002) Membrane protein transport between the ER and Golgi in tobacco leaves is energy dependent but cytoskeleton independence: evidence from selective photobleaching. Plant Cell 14: 1293-1309.
7. Carrington JC, Freed DD, Leinicke AJ (1991) Bipartite signal sequence mediates nuclear translocation of the plant polyviral Nla protein. Plant Cell 3: 953-962.
8. Chiera JM, Grabau EA, Finer JJ (2004) Ectopic expression of a soybean phytase in developing seeds of Glycine max to improve phosphorus availability. Plant Mol Biol 56: 895-904.
9. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
10. Craddock C, Hunter P, Szakacs E, Hinz G, Robinson D, 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.
11. Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR (2000) Random GFP: cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc Natl Acad Sci USA 97: 3718-3723.
12. DaSilva LL, Taylor JP, Hadlington JL, Hanton SL, Snowden CJ, Fox SJ, Foresti O, Brandizzi F, Denecke J (2005) Receptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell 17: 132-148.
13. DaSilva LLP, Foresti O, Denecke J (2006) Targeting of the plant vacuolar sorting receptor BP80 is dependent on multiple sorting signals in the cytosolic tail. Plant Cell 18(6): 1477-1497.
14. Denecke J, Botterman J, Deblaere R (1990) Protein secretion in plant cells can occur via a default pathway. Plant Cell 2: 51-59.
15. Drakakaki G, Marcel S, Arcalis E, Altmann F, Gonzalez-Melendi P, Fischer R, Christou P, Stoger E (2006) The intracellular fate of a recombinant protein is tissue dependent. Plant Physiol 141: 578-586.
16. Faye L, Gomord V (2010) Success stories in molecular farming: a brief overview. Plant Biotechnol J 8: 525-528.
17. Fischer R, Stoger E, Schillberg S, Christou P, Twyman R (2004) Plant-based production of biopharmaceuticals. Curr Opin Plant Biol 7: 152-158.
18. Frigerio L, Virgilio MD, Prada A, Faoro F, Vitale A (1998) Sorting of phaseolin to the vacuole is saturable and requires a short C-terminal peptide. Plant Cell 10: 1031-1042.
19. Frigerio L, Vine ND, Pedrazzini E, Hein MB, Wang F, Ma JKC, Vitale A (2000) Assembly, secretion and vacuolar delivery of a hybrid immunoglobulin in plants. Plant Physiol 123: 1483-1493.
20. Fujiki Y, Hubbard AL, Fowler S, Lazarow PB (1982) Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J Cell Biol 93: 97-102.
21. Gillespie JE, Rogers SW, Deery M, Dupree P, Rogers JC (2005) A unique family of proteins associated with internalized membranes in protein storage vacuoles of the Brassicaceae. Plant J 41: 429-441.
22. Herman EM, Larkins BA (1999) Protein storage bodies and vacuoles. Plant Cell 11: 601-614.
23. Hinz G, Colanesi S, Hillmer S, Rogers JC, Robinson DG (2007) Localization of vacuolar transport receptors and cargo proteins in the Golgi apparatus of developing Arabidopsis embryos. Traffic 8: 1452-1464.
24. Holkeri H, Vitale A (2001) Vacuolar sorting determinants within a plant storage protein trimer act cumulatively. Traffic 2: 737-741.
25. Hunter PR, Craddock CP, Di Benedetto S, Roberts LM, Frigerio L (2007) Fluorescent reporter proteins for the tonoplast and the vacuolar lumen identify a single vacuolar compartment in Arabidopsis cells. Plant Physiol 145: 1371-1382.
26. Jiang L, Phillips TE, Rogers SW, Rogers JC (2000) Biogenesis of the protein storage vacuole crystalloid. J Cell Biol 150: 755-769.
27. Jolliffe NA, Craddock CP, Frigerio L (2005) Pathways for protein transport to seed storage vacuoles. Biochem Soc Trans 33(5): 1016-1018.
28. Kirsch T, Paris N, Butler JM, Beevers L, Rogers JC (1994) Purification and initial characterization of a potential plant vacuolar targeting receptor. Proc Natl Acad Sci USA 91: 3403-3407.
29. Ma JKC, Barros E, Bock R, Christou P, Dale PJ, Dix PJ, Fischer R, Irwin J, Mahoney R, Pezzotti M, Schillberg S, Sparrow P, Stoger E, Twyman RM (2005) Molecular farming for new drugs and vaccines: current perspectives on the production of pharmaceuticals in transgenic plants. EMBO Rep 6: 593-599.
30. Maruyama N, Mun LC, Tatsuhara M, Sawada M, Ishimoto M, Utsumi S (2006) Multiple vacuolar sorting determinants exist in soybean 11S globulin. Plant Cell 18: 1253-1273.
31. Matsuoka K, Nakamura K (1999) Large alkyl side-chains of isoleucine and leucine in the NPIRL region constitute the core of the vacuolar sorting determinant of sporamin precursor. Plant Mol Biol 41: 825-835.
32. Matsuoka K, Neuhaus J (1999) Cis-elements of protein transport to the plant vacuoles. J Exp Bot 50: 165-174.
33. Miao Y, Yan PK, Kim H, Hwang I, 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.
34. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104(1): 34-41.
35. Neuhaus J, Rogers J (1998) Sorting of proteins to vacuoles in plant cells. Plant Mol Biol 38: 127-144.
36. Neuhaus J-M, Sticher L, Meins F Jr, Boller T (1991) A short C-terminal sequence is necessary and sufficient for the targeting of chitinases to the plant vacuole. Proc Natl Acad Sci USA 88: 10362-10366.
37. Paris N, Neuhaus JM (2002) BP-80 as a vacuolar sorting receptor. Plant Mol Biol 50: 903-914.
38. Paris N, Rogers SW, Jiang L, Kirsch T, Beevers L, Phillips TE, Rogers JC (1997) Molecular cloning and further characterization of a probable plant vacuolar sorting receptor. Plant Physiol 115: 29-39.
39. Park M, Lee D, Lee G-J, Hwang I (2005) AtRMR1 functions as a cargo receptor for protein trafficking to the protein storage vacuole. J Cell Biol 170(5): 757-767.
40. Park JH, Oufattole M, Rogers JC (2007) Golgi-mediated vacuolar sorting in plant cells: RMR proteins are sorting receptors for the protein aggregation/membrane internalization pathway. Plant Sci 172: 728-745.
41. Petruccelli S, Otegui MS, Lareu F, Tran Dinh O, Fitchette AC, Circosta A, Rumbo M, Bardor M, Carcamo R, Gomord V, Beachy RN (2006) A KDEL-tagged monoclonal antibody is efficiently retained in the endoplasmic reticulum in leaves, but is both partially secreted and sorted to protein storage vacuoles in seeds. Plant Biotechnol J 4: 511-527.
42. Petruccelli S, Molina MI, Lareu FJ, Circosta A (2007) Two short sequences from amaranth 11S globulin are sufficient to target green fluorescent protein and beta-glucuronidase to vacuoles in Arabidopsis cells. Plant Physiol Biochem 45: 400-409.
43. Robert S, Zouhar J, Carter C, Raikhel N (2007) Isolation of intact vacuoles from Arabidopsis rosette leaf-derived protoplasts. Nat Protoc 2: 259-262.
44. Saint-Jean B, Seveno-Carpentier E, Alcon C, Neuhaus JM, Paris N (2010) The cytosolic tail dipeptide Ile-Met of the pea receptor BP80 is required for recycling from the prevacuole and for endocytosis. Plant Cell 22(8): 2825-2837.
45. Samalova M, Fricker M, Moore I (2006) Ratiometric fluorescence-imaging assays of plant membrane traffic using polyproteins. Traffic 1701-1723.
46. Shaner NC, Steinbach PA, Tsien RY (2005) A guide to choosing fluorescent proteins. Nat Methods 2: 905-909.
47. Shimada T, Fuji K, Tamura K, Kondo M, Nishimura M, Hara-Nishimura I et al (2003) Vacuolar sorting receptor for seed storage proteins in Arabidopsis thaliana. Proc Natl Acad Sci USA 100(26): 16095-16100.
48. Snapp EL, Sharma A, Lippincott-schwartz J, Hegde RS (2006) Monitoring chaperone engagement of substrates in the endoplasmic reticulum of live cells. Proc Natl Acad Sci USA 103(17): 6536-6541.
49. Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1(4): 2019-2025.
50. Stoger E, Ma JK-C, Fischer R, Christou P (2005) Sowing the seeds of success: pharmaceutical proteins from plants. Curr Opin Biotechnol 16: 167-173.
51. van Droogenbroeck B, Cao J, Stadlmann J, Altmann F, Colanesi S, Hillmer S, Robinson DG, van Lerberge E, Terryn N, van Montagu M, Liang M, Depicker A, De Jaeger G (2007) Aberrant localization and underglycosylation of highly accumulating single-chain Fv-Fc antibodies in transgenic Arabidopsis seeds. Proc Natl Acad Sci USA 104: 1430-1435.
52. Vitale A, Hinz G (2005) Sorting of proteins to storage vacuoles: how many mechanisms? Trends Plant Sci 10: 316-323.
53. Vitale A, Raikhel NV (1999) What do proteins need to reach different vacuoles? Trends Plant Sci 4: 149-155.
54. Wang H, Rogers JC, Jiang L (2011) Plant RMR proteins: unique vacuolar sorting receptors that couple ligand sorting with membrane internalization. FEBS J 278: 59-68.
55. Wu FH, Shen SC, Lee LY, Lee SH, Chan MT, Lin CS (2009) Tape-Arabidopsis Sandwich-a simpler Arabidopsis protoplast isolation method. Plant Methods 5: 16.
56. Zouhar J, Rojo E (2009) Plant vacuoles: where did they come from and where are they heading? Curr Opin Plant Biol 12: 677-684.
57. Zouhar J, Muñoz A, Rojo E (2010) Functional specialization within the vacuolar sorting receptor family: VSR1, VSR3 and VSR4 sort vacuolar storage cargo in seeds and vegetative tissues. Plant J. doi: 10. 1111/j. 1365-313X. 2010. 04349. x.