Two glycosylated vacuolar GFPs are new markers for ER-to-vacuole sorting

Plant Physiology and Biochemistry

Volumn 73, Issue , 2013, Pages 337-343

  Stigliano, Egidio ^b,c   Faraco, Marianna ^a   Neuhaus, Jean Marc ^b   Montefusco, Anna ^a   Dalessandro, Giuseppe ^a   Piro, Gabriella ^a   Di Sansebastiano, Gian Pietro ^a  

^a UNIVERSITY OF SALENTO   (Italy)

^b UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^c CNR IGV   (Italy)

Author keywords

CtVSD; GFP; Glycosylation; Golgi; Protoplast; Secretion; Vacuole

Indexed keywords

HORDEUM; NICOTIANA BENTHAMIANA; NICOTIANA TABACUM;

ALEURAIN; CHITINASE; CYSTEINE PROTEINASE; GREEN FLUORESCENT PROTEIN; N ACETYL BETA GLUCOSAMINIDASE; POLYSACCHARIDE; VEGETABLE PROTEIN;

ARTICLE; CELL VACUOLE; COATED VESICLE; CTVSD; ENDOPLASMIC RETICULUM; ENZYMOLOGY; GENETICS; GFP; GLYCOSYLATION; GOLGI; GOLGI COMPLEX; HORDEUM; METABOLISM; MUTATION; PLANT LEAF; PROTEIN TRANSPORT; PROTOPLAST; SECRETION (PROCESS); TOBACCO;

CTVSD; GFP; GLYCOSYLATION; GOLGI; PROTOPLAST; SECRETION; VACUOLE;

CHITINASE; COP-COATED VESICLES; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEASES; ENDOPLASMIC RETICULUM; GLYCOSYLATION; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; HORDEUM; MANNOSYL-GLYCOPROTEIN ENDO-BETA-N-ACETYLGLUCOSAMINIDASE; MUTATION; PLANT LEAVES; PLANT PROTEINS; POLYSACCHARIDES; PROTEIN TRANSPORT; PROTOPLASTS; TOBACCO; VACUOLES;

EID: 84886868985     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2013.10.010     Document Type: Article

References (51)

1. Vitale A., Hinz G. Sorting of proteins to storage vacuoles: how many mechanisms?. Trends Plant Sci. 2005, 10(7):316-323.
2. van Droogenbroeck B., Cao J., Stadlmann J., Altmann F., Colanesi S., Hillmer S., Robinson D.G., van Lerberge E., Terryn N., van Montagu M., Liang M., Depicker A., De Jaeger G. Aberrant localization and underglycosylation of highly accumulating single-chain Fv-Fc antibodies in transgenic Arabidopsis seeds. Proc. Natl. Acad. Sci. 2007, 104(4):1430-1435.
3. Arcalis E., Stadlmann J., Marcel S., Drakakaki G., Winter V., Rodriguez J., Fischer R., Altmann F., Stöger E. The changing fate of a secretory glycoprotein in developing maize endosperm. Plant Physiol. 2010, 153(2):693-702.
4. Boothe J., Nykiforuk C., Shen Y., Zaplachinski S., Szarka S., Kuhlman P., Murray E., Morck D., Moloney M.M. Seed-based expression systems for plant molecular farming. Plant Biotechnol. J. 2010, 8(5):588-606.
5. Di Sansebastiano G.P., Paris N., Marc-Martin S., Neuhaus J.-M. Regeneration of a lytic central vacuole and of neutral peripheral vacuoles can be visualized by green fluorescent proteins targeted to either type of vacuoles. Plant Physiol. 2001, 126(1):78-86.
6. Sanmartín M., Ordóñez A., Sohn E., Robert S., Sánchez-Serrano J.J., Surpin M.A., Raikhel N.V., Rojo E. Divergent functions of VTI12 and VTI11 in trafficking to storage and lytic vacuoles in Arabidopsis. Proc. Natl. Acad. Sci. 2007, 104(9):3645-3650.
7. Flückiger R., De Caroli M., Piro G., Dalessandro G., Neuhaus J.-M., Di Sansebastiano G.P. Vacuolar system distribution in Arabidopsis tissues, visualized using GFP fusion proteins. J.Exp. Bot. 2003, 54(387):1577-1584.
8. Ahmed S.U., Rojo E., Kovaleva V., Venkataraman S., Dombrowski J.E., Matsuoka K., Raikhel N.V. The plant vacuolar sorting receptor AtELP is involved in transport of NH(2)-terminal propeptide-containing vacuolar proteins in Arabidopsis thaliana. J.Cell Biol. 2000, 149(7):1335-1344.
9. Park J.H., Oufattole M., Rogers J.C. Golgi-mediated vacuolar sorting in plant cells: RMR proteins are sorting receptors for the protein aggregation/membrane internalization pathway. Plant Sci. 2007, 172:728-745.
10. Zouhar J., Muñoz A., Rojo E. Functional specialization within the vacuolar sorting receptor family: VSR1, VSR3 and VSR4 sort vacuolar storage cargo in seeds and vegetative tissues. Plant J. 2010, 64(4):577-588.
11. Zouhar J., Rojo E., Bassham D.C. AtVPS45 is a positive regulator of the SYP41/SYP61/VTI12 SNARE complex involved in trafficking of vacuolar cargo. Plant Physiol. 2009, 149(4):1668-1678.
12. Poustka F., Irani N.G., Feller A., Lu Y., Pourcel L., Frame K., Grotewold E. Atrafficking pathway for anthocyanins overlaps with the endoplasmic reticulum-to-vacuole protein-sorting route in Arabidopsis and contributes to the formation of vacuolar inclusions. Plant Physiol. 2007, 145(4):1323-1335.
13. Hara-Nishimura I., Shimada T., Hatano K., Takeuchi Y., Nishimura M. Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles. Plant Cell 1998, 10(5):825-836.
14. Park M., Kim S.J., Vitale A., Hwang I. Identification of the protein storage vacuole and protein targeting to the vacuole in leaf cells of three plant species. Plant Physiol. 2004, 134(2):625-639.
15. De Marchis F., Bellucci M., Pompa A. Traffic of human alfa-mannosidase in plant cells suggests the presence of a new endoplasmic reticulum-to-vacuole pathway without involving the Golgi complex. Plant Physiol. 2013, 161(4):1769-1782.
16. Helenius A., Aebi M. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 2004, 73:1019-1049.
17. Pattison R.J., Amtmann A. N-glycan production in the endoplasmic reticulum of plants. Trends Plant Sci. 2009, 14(2):92-99.
18. Strasser R., Steinkellner H., Borén M., Altmann F., Mach L., Glössl J., Mucha J. Molecular cloning of cDNA encoding N-acetylglucosaminyltransferase II from Arabidopsis thaliana. Glycoconj. J. 1999, 16(12):787-791.
19. Liebminger E., Hüttner S., Vavra U., Fischl R., Schoberer J., Grass J., Blaukopf C., Seifert G.J., Altmann F., Mach L., Strasser R. Class I alpha-mannosidases are required for N-glycan processing and root development in Arabidopsis thaliana. Plant Cell 2009, 21(12):3850-3867.
20. Strasser R., Bondili J.S., Vavra U., Schoberer J., Svoboda B., Glössl J., Léonard R., Stadlmann J., Altmann F., Steinkellner H., Mach L. Aunique β1,3-galactosyltransferase is indispensable for the biosynthesis of N-glycans containing Lewis a structures in Arabidopsis thaliana. Plant Cell 2007, 19(7):2278-2292.
21. Lerouge P., Cabanes-Macheteau M., Rayon C., Fischette-Laine A.C., Gomord V., Faye L. N-glycoprotein biosynthesis in plants: recent developments and future trends. Plant Mol. Biol. 1998, 38(1-2):31-48.
22. Paris N., Saint-Jean B., Faraco M., Krzeszowiec W., Dalessandro G., Neuhaus J.-M., Di Sansebastiano G.P. Expression of a glycosylated GFP as a bivalent reporter in exocytosis. Plant Cell Rep. 2009, 29(1):79-86.
23. Di Sansebastiano G.P., Renna L., Gigante M., De Caroli M., Piro G., Dalessandro G. Green fluorescent protein reveals variability in vacuoles of three plant species. Biol. Plant. 2007, 51(1):49-55.
24. Verweij W., Spelt C., Di Sansebastiano G.P., Vermeer J., Reale L., Ferranti F., Koes R., Quattrocchio F. An H+ P-ATPase on the tonoplast determines vacuolar pH and flower colour. Nat. Cell Biol. 2008, 10(12):1456-1462.
25. De Benedictis M., Bleve G., Faraco M., Stigliano E., Grieco F., Piro G., Dalessandro G., Di Sansebastiano G.P. AtSYP51/52 functions diverge in the post-Golgi traffic and differently affect vacuolar sorting. Mol. Plant 2013, 6(3):916-930.
26. Di Sansebastiano G.P., Paris N., Marc-Martin S., Neuhaus J.-M. Specific accumulation of GFP in a non-acidic vacuolar compartment via a C-terminal propeptide-mediated sorting pathway. Plant J. 1998, 15(4):449-457.
27. De Caroli M., Lenucci M.S., Di Sansebastiano G.P., Dalessandro G., De Lorenzo G., Piro G. Protein trafficking to the cell wall occurs through mechanisms distinguishable from default sorting in tobacco. Plant J. 2011, 65(2):295-308.
28. Crofts A.J., Leborgne-Castel N., Hillmer S., Robinson D.G., Phillipson B., Carlsson L.E., Ashford D.A., Denecke J. Saturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow. Plant Cell 1999, 11(11):2233-2247.
29. Frigerio L., De Virgilio M., Prada A., Faoro F., Vitale A. Sorting of phaseolin to the vacuole is saturable and requires a short C-terminal peptide. Plant Cell 1998, 10(6):1031-1042.
30. Frigerio L., Foresti O., Hernández Felipe D., Paris N., Neuhaus J.-M., Vitale A. The C-terminal tetrapeptide of phaseolin is sufficient to target green fluorescent protein to the vacuole. J.Plant Physiol. 2001, 158(4):499-503.
31. Nebenfuhr A., Ritzenthaler C., Robinson D.G. Brefeldin A: deciphering an enigmatic inhibitor of secretion. Plant Physiol. 2002, 130(3):1102-1108.
32. Teh O.K., Moore I. An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 2007, 448(7152):493-496.
33. Andreeva A.V., Zheng H., Saint-Jore C.M., Kutuzov M.A., Evans D.E., Hawes C.R. Organization of transport from endoplasmic reticulum to Golgi in higher plants. Biochem. Soc. Trans. 2000, 28(4):505-512.
34. Baldwin T.C., Handford M.G., Yuseff M.I., Orellana A., Dupree P. Identification and characterization of GONST1, a Golgi-localized GDP-mannose transporter in Arabidopsis. Plant Cell 2001, 13(10):2283-2295.
35. Faraco M., Di Sansebastiano G.P., Spelt K., Koes R.E., Quattrocchio F.M. One protoplast is not the other!. Plant Physiol. 2011, 156(2):474-478.
36. Dupree P., Sherrier D.J. The plant Golgi apparatus. Biochim. Biophys. Acta 1998, 1404(1-2):259-270.
37. Staehelin L.A., Moore I. The plant golgi-apparatus - structure, functional-organization and trafficking mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1995, 46:261-288.
38. Ruiz-May E., Kim S.J., Brandizzi F., Rose J.K. The secreted plant N-glycoproteome and associated secretory pathways. Front Plant Sci. 2012, 3:117.
39. Peyroche A., Antonny B., Robineau S., Acker J., Cherfils J., Jackson C.L. Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex: involvement of specific residues of the Sec7 domain. Mol. Cell 1999, 3(3):275-285.
40. Robineau S., Chabre M., Antonny B. Binding site of brefeldin A at the interface between the small G protein ADP-ribosylation factor 1 (ARF1) and the nucleotide-exchange factor Sec7 domain. Proc. Natl. Acad. Sci. 2000, 97(18):9913-9918.
41. Saint-Jore-Dupas C., Nebenfuhr A., Boulaflous A., Follet-Gueye M.L., Plasson C., Hawes C., Driouich A., Faye L., Gomord V. Plant N-glycan processing enzymes employ different targeting mechanisms for their spatial arrangement along the secretory pathway. Plant Cell 2006, 18:3182-3200.
42. Batoko H., Zheng H.Q., Hawes C., Moore I. Arab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell 2000, 12(11):2201-2218.
43. Tse Y.C., Lo S.W., Hillmer S., Dupree P., Jiang L. Dynamic response of prevacuolar compartments to brefeldin a in plant cells. Plant Physiol. 2006, 142(4):1442-1459.
44. Dettmer J., Hong-Hermesdorf A., Stierhof Y.D., Schumacher K. Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 2006, 18(3):715-730.
45. Tse Y.C., Mo B.X., Hillmer S., Zhao M., Lo S.W., Robinson D.G., Jiang L.W. Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 2004, 16(3):672-693.
46. Viotti C., Bubeck J., Stierhof Y.D., Krebs M., Langhans M., van den Berg W., van Dongen W., Richter S., Geldner N., Takano J., Jürgens G., de Vries S.C., Robinson D.G., Schumacher K. Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 2010, 22(4):1344-1357.
47. Rivera-Serrano E.E., Rodriguez-Welsh M.F., Hicks G.R., Rojas-Pierce M. Asmall molecule inhibitor partitions two distinct pathways for trafficking of tonoplast intrinsic proteins in Arabidopsis. PLoS One 2012, 7(9):e44735.
48. Gomez L., Chrispeels M.J. Tonoplast and soluble vacuolar proteins are targeted by different mechanisms. Plant Cell 1993, 5(9):1113-1124.
49. Honig A., Avin-Wittenberg T., Ufaz S., Galili G. Anew type of compartment, defined by plant-specific Atg8-interacting proteins, is induced upon exposure of Arabidopsis plants to carbon starvation. Plant Cell 2012, 24(1):288-303.
50. Leucci M.R., Di Sansebastiano G.P., Gigante M., Dalessandro G., Piro G. Secretion marker proteins and cell-wall polysaccharides move through different secretory pathways. Planta 2007, 225(4):1001-1017.
51. De Domenico S., Bonsegna S., Lenucci M.S., Poltronieri P., Di Sansebastiano G.P., Santino A. Localisation of seed oil body proteins in tobacco protoplasts reveals specific mechanisms of protein targeting to leaf lipid droplets. J.Integr. Plant Biol. 2011, 53(11):858-868.