The rice α-amylase glycoprotein is targeted from the golgi apparatus through the secretory pathway to the plastids

Plant Cell

Volumn 21, Issue 9, 2009, Pages 2844-2858

  Kitajima, Aya ^a   Asatsuma, Satoru ^a,d   Okada, Hisao ^a   Hamada, Yuki ^a   Kaneko, Kentaro ^a   Nanjo, Yohei ^a,g   Kawagoe, Yasushi ^b   Toyooka, Kiminori ^c   Matsuoka, Ken ^c,d   Takeuchi, Masaki ^e,f   Nakano, Akihiko ^e,f   Mitsui, Toshiaki ^a  

^a NIIGATA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^c RIKEN Center for Sustainable Resource Science   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

^e RIKEN   (Japan)

^f UNIVERSITY OF TOKYO   (Japan)

^g NATIONAL INSTITUTE OF CROP SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALLIUM CEPA; ARABIDOPSIS; ARABIDOPSIS THALIANA; ORYZA SATIVA;

EID: 70949096336     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.109.068288     Document Type: Article

References (55)

1. Asatsuma, S., Sawada, C., ltoh, K., Okito, M., Kitajima, A., and Mitsui, T. (2005). Involvement of α-amylase I-1 in starch degradation in rice chloroplasts. Plant Cell Physiol. 46: 858-869.
2. Asatsuma, S., Sawada, C., Kitajima, A., Asakura, T., and Mitsui, T. (2006). α-Amylase affects starch accumulation in the rice grain. J. Appl. Glycosci. 53: 187-192.
3. Bennett-Lovsey, R.M., Herbert, A.D., Sternberg, M.J., and Kelley, L.A. (2008). Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins 70: 611-625.
4. Blobel, G. (1980). Intracellular protein topogenesis. Proc. Natl. Acad. Sci. USA 77: 1496-1500.
5. Bruce, B.D. (2000). Chloroplast transit peptides: Structure, function and evolution. Trends Cell Biol. 10: 440-447
6. Chen, M.H., Huang, L.F., Li, H.M., Chen, Y.R., and Yu, S.M. (2004). Signal peptide-dependent targeting of a rice a-amylase and cargo proteins to plastids and extracellular compartments of plant cells. Plant Physiol. 135: 1367-1377.
7. Chen, M.H., Liu, L.F., Chen, Y.R., Wu, H.K., and Yu, S.M. (1994 Expression of a-amylase, carbohydrate metabolism, and autophagy in cultured rice cells is coordinately regulated by sugar nutrient. Plant J. 6: 625-636. (Pubitemid 2159141)
8. Gaikwad, A., Tewari, K.K., Kumar, D., Chen, W., and Mukherjee, S.K. (1999 Isolation and characterization of the cDNA encoding a glycosylated accessory protein of pea chloroplast DNA polymerase. Nucleic Acids Res. 27: 3120-3129. (Pubitemid 29355726)
9. 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.
10. Hayashi, M., Turu, A., Mitsui, T., Takahashi, N., Hanzawa, H., Arata, Y., and Akazawa, T. (1990). Structure and biosynthesis of the xylosecontaining carbohydrate moiety of rice α-amylase. Eur. J. Biochem. 191:287-295.
11. Hiei, Y., Ohta, S., Komari, T., and Kumashiro, T. (1994). Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6: 271-282.
12. Hood, E.E., Helmer, G.L., Fraley, R.T., and Chilton, M.D. (1986). The hyper-virulence of Agrobacterium tumefaciens A281 is encoded in a region of pTiBo542 outside of T-DNA. J. Bacteriol. 168: 1291-1301.
13. Ishida, H., Yoshimoto, K., Izumi, M., Reisen, D., Yano, Y., Makino, A., Ohsumi, Y., Hanson, M.R., and Mae, T. (2008 Mobilization of Rubisco and stromal-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol. 148: 142-155. (Pubitemid 352847588)
14. ltoh, K., Ozaki, H., Okada, K., Hori, H., Takeda, Y., and Mitsui, T. (2003). Introduction of Wx transgene into rice wx mutants leads to both high- and low-amylose rice. Plant Cell Physiol. 44: 473-480.
15. Jarvis, P. (2008). Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol. 179: 257-285.
16. Kim, D.H., Eu, Y.J., Yoo, CM., Kim, Y.W., Pih, K.T., Jin, J.B., Kim, S.J., Stenmark, H., and Hwang, I. (2001 Trafficking of phosphatidylinositol 3-phosphate from the trans-Golgi network to the lumen of the central vacuole in plant cells. Plant Cell 13: 287-301. (Pubitemid 32207684)
17. Kirsch, T., Saalbach, G., Raikhel, N.V., and Beevers, L. (1996 Interaction of a potential vacuolar targeting receptor with aminoand carboxyl-terminal targeting determinants. Plant Physiol. 111: 469-474. (Pubitemid 126640491)
18. Kleffmann, T., Russenberger, D., von Zychlinski, A., Christopher, W., Sjolander, K., Gruissem, W., and Baginsky, S. (2004). The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 14: 354-362.
19. Klösgen, R.B., and Weil, J.H. (1991). Subcellular location and expression level of a chimeric protein consisting of the maize waxy transit peptide and the beta-glucuronidase of Escherichia coli in transgenic potato plants. Mol. Gen. Genet. 225: 297-304.
20. Kornfeld, R., and Kornfeld, S. (1985). Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54: 631-664.
21. Latijnhouwers, M., Hawes, C., Carvalho, C., Oparka, K., Gillingham, A.K., and Boevink, P. (2005 An Arabidopsis GRIP domain protein locates to the trans-Golgi and binds the small GTPase ARL1. Plant J. 44: 459-470. (Pubitemid 43919874)
22. Lee, D.W., Kim, J.K., Lee, S., Choi, S., Kim, S., and Hwang, I. (2008). Arabidopsis nuclear-encoded plastid transit peptides contain multiple sequence subgroups with distinctive chloroplast-targeting sequence motifs. Plant Cell 20: 1603-1622.
23. Losev, E., Reinke, C.A., Jellen, J., Strongin, D.E., Bevis, B.J., and Glick, B.S. (2006). Golgi maturation visualized in living yeast. Nature 441: 1002-1006. (Pubitemid 43980356)
24. Mano, S., Nakamori, C., Hayashi, M., Kato, A., Kondo, M., and Nishimura, M. (2002). Distribution and characterization of peroxisomes in Arabidopsis by visualization with GFP: Dynamic morphology and actin-dependent movement. Plant Cell Physiol. 43: 331-341.
25. Matsuoka, K., and Neuhaus, J. (1999). Cis-elements of protein transport to the plant vacuoles. J. Exp. Bot. 50: 165-174.
26. Matsuura-Tokita, K., Takeuchi, M., Ichihara, A., Mikuriya, K., and Nakano, A. (2006). Live imaging of yeast Golgi cisternal maturation. Nature 441: 1007-1010. (Pubitemid 43980357)
27. Mitsui, T., Loboda, T., Kamimura, I., Hori, H., ltoh, K., and Mitsunaga, S. (1999). Sucrose-controlled transport and turnover of a-amylase in rice (Ofyza sativa L.) cells. Plant Cell Physiol. 40: 884-893.
28. Mitsui, T., Yamaguchi, J., and Akazawa, T. (1996). Physicochemical and serological characterization of rice a-amylase isoforms and identification of their corresponding genes. Plant Physiol. 110: 1395-1404. (Pubitemid 126630751)
29. Nanjo, Y., Asatsuma, S., ltoh, K., Hori, H., and Mitsui, T. (2004). Proteomic identification of a-amylase isoforms encoded by RAmy3B/ 3C from germinating rice seeds. Biosci. Biotechnol. Biochem. 68: 112-118.
30. Nanjo, Y., Oka, H., Ikarashi, N., Kaneko, K., Kitajima, A., Mitsui, T., Muñoz, F.J., Rodríguez-López, M., Baroja-Fernández, E., and Pozueta-Romero, J. (2006). Rice plastidial N-glycosylated nucleotide yrophosphatase/phosphodiesterase is transported from the ERGolgi to the chloroplast through the secretory pathway. Plant Cell 18: 2582-2592. (Pubitemid 44749891)
31. Nebenführ, A., Frohlick, J.A., and Staehelin, L.A. (2000). Redistribution of Golgi stacks and other organelles during mitosis and cytokinesis in plant cells. Plant Physiol. 124: 135-151.
32. Nebenführ, A., Gallagher, L.A., Dunahay, T.G., Frohlick, J.A., Mazurkiewicz, A.M., Meehl, J.B., and Staehelin, L.A. (1999). Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol. 121: 1127-1142. (Pubitemid 30018499)
33. Niwa, Y., Hirano, T., Yoshimoto, K., Shimizu, M., and Kobayashi, H. (1999). Non-invasive quantitative detection and applications of nontoxic, S65T-type green fluorescent protein in living plants. Plant J. 18: 455-463. (Pubitemid 129515065)
34. Palade, G. (1975). Intracellular aspects of the process of protein synthesis. Science 189: 347-358.
35. Ritzenthaler, C., Nebenfuhr, A., Movafeghi, A., Stussi-Garaud, C., Behnia, L., Pimpl, P., Staehelin, L.A., and Robinson, D.G. (2002). Reevaluation of the effects of Brefeldin A on plant cells using tobacco Bright Yellow 2 cells expressing Golgi-targeted green fluorescent protein and COPI antisera. Plant Cell 14: 237-261. (Pubitemid 34140409)
36. Radhamony, R.N., and Theg, S.M. (2006). Evidence for an ER to Golgi to chloroplast protein transport pathway. Trends Cell Biol. 16: 385-387.
37. Robert, X., Haser, R., Mori, H., Svensson, B., and Aghajari, N. (2005). Oligosaccharide binding to barley a-amylase 1. J. Biol. Chem. 280: 32968-32978.
38. Rothman, J.E., and Wieland, F.T. (1996). Protein sorting by transport vesicles. Science 272: 227-234.
39. Saalbach, G., Jung, R., Kunze, G., Saalbach, I., Adler, K., and Muntz, K. (1991). Different legumin protein domains act as vacuolar targeting signals. Plant Cell 3: 695-708. (Pubitemid 21913734)
40. Schnell, DJ., and Hebert, D.N. (2003). Protein translocons: Multifunctional mediators of protein translocation across membranes. Cell 112: 491-505. (Pubitemid 36263082)
41. Søgaard, M., Kadziola, A., Haser, R., and Svensson, B. (1993). Site-directed mutagenesis of histidine 93, aspartic acid 180, glutamic acid 205, histidine 290, and aspartic acid 291 at the active site and tryptophan 279 at the raw starch binding site in barley a-amylase 1. J. Biol. Chem. 268: 22480-22484.
42. Soil, J., and Schleiff, E. (2004). Protein import into chloroplasts. Nat. Rev. Mol. Cell Biol. 5: 198-208.
43. Staehelin, L.A., and Moore, I. (1995). The plant Golgi apparatus: Structure, functional organization and trafficking mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 261-288.
44. Takeuchi, M., Ueda, T., Sato, K., Abe, H., Nagata, T., and Nakano, A. (2000). A dominant negative mutant of sari GTPase inhibits protein transport from the endoplasmic reticulum to the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J. 23: 517-525. (Pubitemid 30661280)
45. Takeuchi, M., Ueda, T., Yahara, N., and Nakano, A. (2002). Arf1 GTPase plays roles in the protein traffic between the endoplasmic reticulum and the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J. 31: 499-515. (Pubitemid 34989856)
46. Terashima, M., Kubo, A., Suzawa, M., ltoh, Y., and Katoh, S. (1994). The roles of the N-linked carbohydrate chain of rice a-amylase in thermostability and enzyme kinetics. Eur. J. Biochem. 226: 249-254.
47. Törmäkangas, K., Hadlington, J.L., Pimpl, P., Hillmer, S., Brandizzi, F., Teeri, T.H., and Denecke, J. (2001). A vacuolar sorting domain may also influence the way in which proteins leave the endoplasmic reticulum. Plant Cell 13: 2021-2032. (Pubitemid 32919018)
48. Toyooka, K., Goto, Y., Asatsuma, S., Koizumi, M., Mitsui, T., and Matsuoka, K. (2009). A mobile secretory vesicle cluster involved in mass transport from the Golgi to plant cell exterior. Plant Cell 21: 1212-1229.
49. Toyooka, K., Moriyasu, Y., Goto, Y., Takeuchi, M., Fukuda, H., and Matsuoka, K. (2006). Protein aggregates are transported to vacuoles by a macroautophagic mechanism in nutrient-starved plant cells. Autophagy 2: 96-106.
50. van Dooren, G.G., Schwartzbach, S.D., Osafune, T., and McFadden, G.I. (2001). Translocation of proteins across the multiple membranes of complex plastids. Biochim. Biophys. Acta 1541: 34-53.
51. von Schaewen, A., and Chrispeels, M.J. (1993). Identification of vacuolar sorting information in phytohemagglutinin, an unprocessed vacuolar protein. J. Exp. Bot. 44: 339-342.
52. Villarejo, A., et al. (2005). Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat. Cell Biol. 7: 1224-1231.
53. Vitale, A., and Hinz, G. (2005). Sorting of proteins to storage vacuoles: how many mechanisms? Trends Plant Sci. 10: 316-323.
54. Yu, T.S., et al. (2005). a-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J. Biol. Chem. 280: 9773-9779.
55. Zhang, X.P., and Glaser, E. (2002). Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends Plant Sci. 7: 14-21.