Plant Molecular Biology

, Volume 41, Issue 6, pp 815–824 | Cite as

The Arabidopsis thaliana RER1 gene family: its potential role in the endoplasmic reticulum localization of membrane proteins

  • Ken Sato
  • Takashi Ueda
  • Akihiko Nakano
Article

Abstract

Many endoplasmic reticulum (ER) proteins are known to be localized to the ER by a mechanism called retrieval, which returns the molecules that are exported from the ER to the Golgi apparatus back to the ER. Signals are required to be recognized by this retrieval system. In the work on yeast Saccharomyces cerevisiae, we have demonstrated that transmembrane domains of a subset of ER membrane proteins including Sec12p, Sec71p and Sec63p contain novel ER retrieval signals. For the retrieval of these proteins, a Golgi membrane protein, Rer1p, is essential (Sato et al., Mol. Biol. Cell 6 (1995) 1459–1477; Proc. Natl. Acad. Sci. USA 94 (1997) 9693–9698). To address the role of Rer1p in higher eukaryotes, we searched for homologues of yeast RER1 from Arabidopsis thaliana. We identified three cDNAs encoding Arabidopsis counterparts of Rer1p with an amino acid sequence identity of 39–46% to yeast Rer1p and named AtRER1A, AtRER1B, and AtRER1C1. AtRer1Ap and AtRer1Bp are homologous to each other (85% identity), whereas AtRer1C1p is less similar to AtRer1Ap and AtRer1Bp (about 50%). Genomic DNA gel blot analysis indicates that there are several other AtRER1-related genes, implying that Arabidopsis RER1 constitutes a large gene family. The expression of these three AtRER1 genes is ubiquitous in various tissues but is significantly higher in roots, floral buds and a suspension culture in which secretory activity is probably high. All the three AtRER1 cDNAs complement the yeast rer1 mutant and remedy the defect of Sec12p mislocalization. However, the degree of complementation differs among the three with that of AtRER1C1 being the lowest, again suggesting a divergent role of AtRer1C1p.

ER membrane protein Golgi apparatus retrieval 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bar-Peled, M. and Raikhel, N.V. 1997. Characterization of AtSEC12 and AtSAR1. Plant Physiol. 114: 315–324.PubMedGoogle Scholar
  2. Bar-Peled, M., Conceição, A.S., Frigerio, L. and Raikhel, N.V. 1995. Expression and regulation of aERD2, a gene encoding the KDEL receptor homolog in plants, and other genes encoding proteins involved in ER-Golgi vesicular trafficking. Plant Cell 7: 667–676.PubMedGoogle Scholar
  3. Barlowe, C. and Schekman, R. 1993. SEC12 encodes a guanine nu-cleotide exchange factor essential for transport vesicle budding from the ER. Nature 365: 347–349.CrossRefPubMedGoogle Scholar
  4. Boehm, J., Ulrich, H.D., Ossig, R. and Schmitt, H.D. 1994. Kex2-dependent invertase secretion as a tool to study the targeting of transmembrane proteins which are involved in ER ! Golgi transport in yeast. EMBO J. 13: 3696–3710.PubMedGoogle Scholar
  5. Boehm, J., Letourneur, F., Ballensiefen, W., Ossipov, D., Démol-lière, C. and Schmitt, H.D. 1997. Sec12p requires Rer1p for sorting to coatomer (COPI)-coated vesicles and retrieval to the ER. J. Cell Sci. 110: 991–1003.PubMedGoogle Scholar
  6. Boevink, P., Oparka, K., Santa Cruz, S., Martin, B., Betteridge, A. and Hawes, C. 1998. Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J. 15: 441–447.PubMedGoogle Scholar
  7. Chan, R.K. and Otte, C.A. 1982. Isolation and genetic analysis of Saccharomyces cerevisiae mutants supersensitive to G1 arrest by a factor and _ factor pheromones. Mol. Cell. Biol. 2: 11–20.PubMedGoogle Scholar
  8. Cosson, P. and Letourneur, F. 1994. Coatomer interaction with di-lysine endoplasmic reticulum motifs. Science 263: 1629–1631.PubMedGoogle Scholar
  9. Cosson, P., Démollière, C., Hennecke, S., Duden, R. and Le-tourneur, F. 1996. _-and_-COP, two coatomer subunits homolo-gous to clathrin-associated proteins, are involved in ER retrieval. EMBO J. 15: 1792–1798.PubMedGoogle Scholar
  10. Denecke, J., De Rycke, R. and Botterman, J. 1992. Plant and mam-malian sorting signals for protein retention in the endoplasmic reticulum contain a conserved epitope. EMBO J. 11: 2345–2355.PubMedGoogle Scholar
  11. d'Enfert, C., Gensse, M. and Gaillardin, C. 1992. Fission yeast and a plant have functional homologues of the Sar1 and Sec12 proteins involved in ER to Golgi traffic in budding yeast. EMBO J. 11: 4205–4211.PubMedGoogle Scholar
  12. Füllekrug, J., Boehm, J., Röttger, S., Nilsson, T., Mieskes, G. and Schmitt, H.D. 1997. Human Rer1 is localized to the Golgi apparatus and complements the deletion of the homologous Rer1 protein of Saccharomyces cerevisiae. Eur. J. Cell. Biol 74: 31–40.PubMedGoogle Scholar
  13. Fuller, R.S., Sterne, R.E. and Thorner, J. 1988. Enzymes required for yeast prohormone processing. Annu. Rev. Physiol. 50: 345–362.PubMedGoogle Scholar
  14. Haseloff, J., Siemering, K., Prasher, D. and Hodge, S. 1997. Re-moval of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl. Acad. Sci. USA. 94: 2122–2127.PubMedGoogle Scholar
  15. Higgins, D.G., Bleasby, A.J. and Fuchs, R. 1992. CLUSTAL V: im-proved software for multiple sequence alignment. Comput. Appl. Biosci. 8: 189–191.PubMedGoogle Scholar
  16. Jackson, M.R., Nillson, T. and Peterson, P.A. 1993. Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. EMBO J. 9: 3153–3162.Google Scholar
  17. Jackson, M.R., Nillson, T. and Peterson, P.A. 1993. Retrieval of transmembrane proteins to the endoplasmic reticulum. J. Cell Biol. 121: 317–333.PubMedGoogle Scholar
  18. Keszenman-Pereyra, D. and Hieda, K. 1988. A colony procedure for transformation of Saccharomyces cerevisiae. Curr. Genet. 13: 21–23.PubMedGoogle Scholar
  19. Kyte, J. and Doolittle, R.F. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157: 105–132.PubMedGoogle Scholar
  20. Lee, H., Gal, S., Newman, T.C. and Raikhel, N.V. 1993. The Ara-bidopsis endoplasmic reticulum retention receptor functions in yeast. Proc. Natl. Acad. Sci. USA 90: 11433–11437.PubMedGoogle Scholar
  21. Letourneur, F., Gaynor, E.C., Hennecke, S., Démollière, C., Duden, R., Emr, S.D., Riezman, H, and Cosson, P. 1994. Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79: 1199–1207.PubMedGoogle Scholar
  22. Lewis, M.J. and Pelham, H.R.B. 1990. A human homologue of the yeast HDEL receptor. Nature 348: 162–163.PubMedGoogle Scholar
  23. Lewis, M.J., Sweet, D.J. and Pelham, H.R.B. 1990. The ERD2 gene determines the specificity of the luminal ER protein retention system. Cell 61: 1359–1363.CrossRefPubMedGoogle Scholar
  24. Matsuda, N. and Nakano, A. 1998. RMA1,anArabidopsis thaliana gene whose cDNA suppresses the yeast sec15 mutation, encodes a novel protein with a RING finger motif and a membrane anchor. Plant Cell Physiol. 39: 545–554.Google Scholar
  25. Munro, S. and Pelham, H.R.B. 1987. A C-terminal signal prevents secretion of luminal ER proteins. Cell 48: 899–907.CrossRefPubMedGoogle Scholar
  26. Nakano, A. and Muramatsu, M. 1989. A novel GTP-binding protein, SAR1, is involved in transport from the endoplasmic reticulum to the Golgi apparatus. J. Cell. Biol. 109: 2677–2691.PubMedGoogle Scholar
  27. Nakano, A., Brada, D. and Schekman, R. 1988. A membrane glycoprotein, Sec12p, required for protein transport from the endoplasmic reticulum to the Golgi apparatus in yeast. J. Cell Biol. 107: 851–863.PubMedGoogle Scholar
  28. Nishikawa, S. and Nakano, A. 1993. Identification of a gene re-quired for membrane protein retention in the early secretory pathway. Proc. Natl. Acad. Sci. USA 90: 8179–8183.PubMedGoogle Scholar
  29. Palmiter, R. 1974. Magnesium precipitation of ribonucleoprotein complexes. Expedient techniques for the isolation of under-graded polysomes and messenger ribonucleic acid. Biochemistry 13: 3606–3615.PubMedGoogle Scholar
  30. Pelham, H.R.B. 1989. Control of protein exit from the endoplasmic reticulum. Annu. Rev. Cell Biol. 5: 1–23.PubMedGoogle Scholar
  31. Pelham, H.R.B., Hardwick, K.G. and Lewis, M.J. 1988. Sorting of soluble ER proteins in yeast. EMBO J. 7: 1757–1762.PubMedGoogle Scholar
  32. Pih, K.T., Jang, H.J., Kang, S.G., Piao, H.L. and Hwang, I. 1997. Isolation of molecular markers for salt stress responses in Arabidopsis thaliana. Mol. Cell 7: 567–571.Google Scholar
  33. Sato, K., Nishikawa, S. and Nakano, A. 1995. Membrane protein retrieval from the Golgi apparatus to the endoplasmic reticulum (ER): characterization of the RER1 gene product as a component involved in ER localization of Sec12p. Mol. Biol. Cell 6: 1459–1477.PubMedGoogle Scholar
  34. Sato, M., Sato, K. and Nakano, A. 1996. Endoplasmic reticulum localization of Sec12p is achieved by two mechanisms: Rer1p-dependent retrieval that requires the transmembrane domain and Rer1p-independent retention that involves the cytoplasmic domain. J. Cell Biol. 134: 279–293.PubMedGoogle Scholar
  35. Sato, K., Sato, M. and Nakano, A. 1997. Rer1p as common ma-chinery for the endoplasmic reticulum localization of membrane proteins. Proc. Natl. Acad. Sci. USA 94: 9693–9698.PubMedGoogle Scholar
  36. Semenza, J.C., Hardwick, K.G., Dean, N. and Pelham, H.R.B. 1990. ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell 61: 1349–1357.PubMedGoogle Scholar
  37. Staehelin, L.A. 1997. The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J. 11: 1151–1165.PubMedGoogle Scholar
  38. Ueda, T., Matsuda, N., Anai, T., Tsukaya, H., Uchimiya, H. and Nakano, A. 1996. An Arabidopsis gene isolated by a novel method for detecting genetic interaction in yeast encodes the GDP dissociation inhibitor of Ara4 GTPase. Plant Cell 8: 2079–2091.PubMedGoogle Scholar
  39. Ueda, T., Yoshizumi, T., Anai, T., Matsui, M., Uchimiya, H. and Nakano, A. 1998. AtGDI2, a novel Arabidopsis gene encoding a Rab GDP dissociation inhibitor. Gene 206: 137–143.PubMedGoogle Scholar
  40. Vitale, A., Ceriotti, A. and Denecke, J. 1993. The role of the endoplasmic reticulum in protein synthesis, modification and intracellular transport. J. Exp. Bot. 44: 1417–1444.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Ken Sato
    • 1
  • Takashi Ueda
    • 1
  • Akihiko Nakano
    • 1
  1. 1.Molecular Membrane Biology Laboratory, RIKENWako, SaitamaJapan

Personalised recommendations