Advertisement

Calreticulin pp 94-104 | Cite as

Calreticulin and the Endoplasmic Reticulum in Plant Cell Biology

  • Paola Mariani
  • Lorella Navazio
  • Anna Zuppini
Part of the Molecular Biology Intelligence Unit book series (MBIU)

Abstract

Calreticulin is ubiquitously expressed in plants. The plant homologue shares with its animal counterpart a similar structural organization and basic functioning. A wide range of developmental and environmental stimuli differentially affect the expression of calreticulin in plant cells, highlighting its importance in cell physiology. Nevertheless, current knowledge on calreticulin’s relevance in plant physiology is rather limited compared with animal systems. The contribution of the endoplasmic reticulum to Ca2+ homeostasis and signalling, and the multifunctional role of calreticulin in plant cellular events are rapidly emerging areas of study in plant biology.

Keywords

Endoplasmic Reticulum Pollen Tube Endoplasmic Reticulum Stress Cyclopiazonic Acid Glycan Chain 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Denecke J, Carlsson LE, Vidal S et al. The tobacco homolog of mammalian calreticulin is present in protein complexes in vivo. Plant cell 1995; 7:391–406.PubMedGoogle Scholar
  2. 2.
    Crofts AJ, Leborgne-Castel N, Hillmer S et al. Saturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow. Plant cell 1999; 11:2233–2247.PubMedGoogle Scholar
  3. 3.
    Michalak M, Corbett EF, Mesaeli N et al. Calreticulin: one protein, one gene, many functions. Biochem J 1999; 344:281–92.PubMedCrossRefGoogle Scholar
  4. 4.
    Chen F, Hayes PM, Mulrooney DM et al. Identification and characterization of cDNA clones encoding plant calreticulin in barley. Plant cell 1994; 6:835–843.PubMedGoogle Scholar
  5. 5.
    Napier RM, Trueman S, Henderson J et al. Purification, sequencing and functions of calreticulin from maize. J Exp Bot 1995; 46:1603–1613.CrossRefGoogle Scholar
  6. 6.
    Coughlan SJ, Hastings C, Winfrey R. Cloning and characterization of the calreticulin gene from Ricinus communis L. Plant Mol Biol 1997; 34:897–911.PubMedCrossRefGoogle Scholar
  7. 7.
    Nelson DE, Glaunsinger B, Bohnert HJ. Abundant accumulation of the calcium-binding molecular chaperone calreticulin in specific floral tissues of Arabidopsis thaliana. Plant Physiol 1997; 114:29–37.PubMedCrossRefGoogle Scholar
  8. 8.
    Li Z, Komatsu S. Molecular cloning and characterization of calreticulin, a calcium-binding protein involved in the regeneration of rice cultured suspension cells. Eur J Biochem 2000; 267:737–745.PubMedCrossRefGoogle Scholar
  9. 9.
    Navazio L, Baldan B, Mariani P et al. Primary structure of N-linked carbohydrate chains of calreticulin from spinach leaves. Glycoconjugate J 1996; 13:977–983.CrossRefGoogle Scholar
  10. 10.
    Pagny S, Cabanes-Macheteau M, Gillikin JW et al. Protein recycling from the Golgi apparatus to the endoplasmic reticulum in plants and its minor contribution to calreticulin retention. Plant cell 2000; 12:739–755.PubMedGoogle Scholar
  11. 11.
    Navazio L, Baldan B, Dainese P et al. Evidence that spinach leaves express calreticulin but not calsequestrin. Plant Physiol 1995; 109:983–990.PubMedCrossRefGoogle Scholar
  12. 12.
    Navazio L, Sponga L, Dainese P et al. The calcium binding protein calreticulin in pollen of Liriodendron tulipifera L. Plant Sci 1998; 131:35–42.CrossRefGoogle Scholar
  13. 13.
    Helenius A, Aebi M. Intracellular functions of N-linked glycans. Science 2001; 291:2364–2369.PubMedCrossRefGoogle Scholar
  14. 14.
    Ellgaard L, Helenius A. ER quality control: towards an understanding at the molecular level. Curt Opin Cell Biol 2001; 13:431–437.CrossRefGoogle Scholar
  15. 15.
    Baldan B, Navazio L, Friso A et al. Plant calreticulin is specifically and efficiently phosphorylated by protein kinase CK2. Biochem Biophys Res Commun 1996; 221:498–502.PubMedCrossRefGoogle Scholar
  16. 16.
    Navazio L, Nardi MC, Pancaldi S et al. Functional conservation of calreticulin in Euglena gracilis. J Euk Microbiol 1998; 45:307–313.PubMedCrossRefGoogle Scholar
  17. 17.
    Zuppini A, Barbato R, Bergantino E et al. Ca2+ binding protein calreticulin in Chlamydomonas reinhardtii (Chlorophyta): biochemical characterization, differential expression during sexual reproduction, and phylogenetic analysis. J Phycol 1999; 35:1224–1232.CrossRefGoogle Scholar
  18. 18.
    Cala SE. GRP94 hyperglycosylation and phosphorylation in Sf21 cells. Biochem Biophys Acta 2000; 1496:296–310.PubMedCrossRefGoogle Scholar
  19. 19.
    Droillard MJ, Güclü J, Le Caer J-P et al. Identification of calreticulin-like protein as one of the phosphoproteins modulated in response to oligogalacturonides in tobacco cells. Planta 1997; 202:341–348.PubMedCrossRefGoogle Scholar
  20. 20.
    Sanderfoot AA, Raikhel NV. The specificity of vesicle traffiking: coat proteins and SNAREs. Plant cell 1999; 11:629–641.PubMedGoogle Scholar
  21. 21.
    Pimpl P, Movafeghi A, Coughlan S et al. In situ localization and in vitro induction of plant COPI-coated vesicles. Plant cell 2000; 12:2219–2235.PubMedGoogle Scholar
  22. 22.
    Phillipson BA, Pimpl P, Pinto daSilva LL et al. Secretory bulk flow of soluble proteins is efficient and COPII dependent. Plant cell 2001; 13:2005–2020.PubMedGoogle Scholar
  23. 23.
    Crofts AJ, Leborgne-Castel N, Pesca M et al. BiP and calreticulin form an abundant complex that is independent of endoplasmic reticulum stress. Plant cell 1998; 10:813–823.PubMedGoogle Scholar
  24. 24.
    Baluska F, Samaj J, Napier R et al. Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J 1999; 19:481–488.PubMedCrossRefGoogle Scholar
  25. 25.
    Baluska F, Cvrcková F, Kendrick-Jones J et al. Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiol 2001; 126:39–46.PubMedCrossRefGoogle Scholar
  26. 26.
    Holdaway-Clarke TL, Walker NA, Hepler PK et al. Physiological elevations in cytoplasmic free calcium by cold or iron injection result in transient closure of higher plant plasmodesmata. Planta 2000; 210:329–335.PubMedCrossRefGoogle Scholar
  27. 27.
    Tucker EB, Boss WF. Mastoparan-induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiol 1996; 111:459–467.PubMedGoogle Scholar
  28. 28.
    Baluska F, Salaj J, Mathur J et al. Root hait formation: F-actin-dependent tip growth is initiated by local assembly of ptofilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 2000; 227:618–632.PubMedCrossRefGoogle Scholar
  29. 29.
    Lenartowska M, Karas K, Marshall J et al. Immunocytochemical evidence of calreticulin-like protein in pollen tubes and styles of Petunia hybrida Hort. Protoplasma 2002; 219:23–30.PubMedCrossRefGoogle Scholar
  30. 30.
    Borisjuk N, Sitailo L, Adler K et al. Calreticulin expression in plant cells: developmental regulation, tissue specificity and intracellular distribution. Planta 1998; 206:504–514.PubMedCrossRefGoogle Scholar
  31. 31.
    Torres E, Gonzales-Melendi P, Stöger E et al. Native and artificial reticuloplasmins co-accumulate in distinct domains of the endoplasmic reticulum and in post-endoplasmic reticulum compartments. Plant Physiol 2001; 127:1212–1223.PubMedCrossRefGoogle Scholar
  32. 32.
    Opas M, Tharin S, Milner RE et al. Identification and localization of calreticulin in plant cells. Protoplasma 1996; 191:164–171.CrossRefGoogle Scholar
  33. 33.
    Dresselhaus T, Hagel C, Lörz H et al. Isolation of a full-length cDNA encoding calreticulin from a PCR library of in vitro zygotes of maize. Plant Mol Biol 1996; 31:23–34.PubMedCrossRefGoogle Scholar
  34. 34.
    Williams CM, Zhang G, Michalak M et al. Calcium-induced protein phosphorylation and changes in levels of calmoduiin and calreticulin in maize sperm cells. Sex Plant Reprod 1997; 10:83–88.CrossRefGoogle Scholar
  35. 35.
    Harris HH. The Chlamydomonas sourcebook: a comprehensive guide to biology and laboratory use. Harcourt Brace Jovanovich, eds. Academic Press Inc. S. Diego, 1989.Google Scholar
  36. 36.
    Faure J-E. Double fertilization in flowering plants: discovery, study methods and mechanisms. Life Sci 2001; 324:551–558.Google Scholar
  37. 37.
    Heilmann I, Shin J, Huang J et al. Transient dissociation of polyribosomes and concurrent recruitment of calreticulin and calmoduiin transcripts in gravistimulated maize pulvini. Plant Physiol 2001; 127: 1193–1203.PubMedCrossRefGoogle Scholar
  38. 38.
    Jelitto-Van Dooren EPWM, Viadl S, Denecke J. Anticipating endoplasmic reticulum stress: a novel early response before pathogenesis-related gene induction. Plant cell 1999; 11:1935–1943.Google Scholar
  39. 39.
    Sinclair W, Trewavas AJ. Calcium in gravitropism: a re-examination. Planta 1997; 203:S85–S90.PubMedCrossRefGoogle Scholar
  40. 40.
    John M, Röhring H, Shmidt J ef al. Cell signalling by oligosaccharides. Trends Plant Sci 1997; 2:111–115.CrossRefGoogle Scholar
  41. 41.
    Sivaguru M, Fujiwara T, Samaj J et al. Aluminum-induced 1→3-β-D-gIucan inhibits cell-to-cell traffiking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol 2000; 124:991–1005.PubMedCrossRefGoogle Scholar
  42. 42.
    Pedrazzini E, Giovinazzo G, Bielli A et al. Protein quality control along the route to the plant vacuole. Plant cell 1997; 9:1869–1880.PubMedGoogle Scholar
  43. 43.
    Kermode AR, Fisher SA, Polishchuk E et al. Accumulation and proteolytic processing of vicilin deletion-mutant proteins in the leaf and seed of transgenic tobacco. Planta 1995; 197:501–513.PubMedCrossRefGoogle Scholar
  44. 44.
    Coleman CE, Herman EM, Takasaki K et al. The maize γ-zein sequesters a-zein and stabilizes its accumulation in protein bodies of transgenic tobacco endosperm. Plant cell 1996; 8:2335–2345.PubMedGoogle Scholar
  45. 45.
    Leborgne-Castel N, Jelitto-Van Dooren EPWM, Crofts AJ et al. Overexpression of BiP in tobacco alleviates endoplasmic reticulum stress. Plant cell 1999; 11:459–469.PubMedGoogle Scholar
  46. 46.
    Pedrazzini E, Vitale A. The binding protein (BiP) and the synthesis of secretory proteins. Plant Physiol Biochem 1996; 34:207–216.Google Scholar
  47. 47.
    Chevet E, Cameron PH, Pelletier MF et al. The endoplasmic reticulum: integration of protein folding, quality control, signaling and degradation. Cutr Opin Struct Biol 2001; 11:120–124.CrossRefGoogle Scholar
  48. 48.
    Lupattelli F, Pedrazzini E, Bollini R et al. The rate of phaseolin assembly is controlled by the glucosylation state of its N-linked oligosaccharide chains. Plant cell 1997; 9:597–609.PubMedGoogle Scholar
  49. 49.
    Trewavas AJ, Malho R. Ca2+ signalling in plant cells: the big network! Curr Opin Plant Biol 1998; 1:428–433.PubMedCrossRefGoogle Scholar
  50. 50.
    Johnson CH, Knight MR, Kondo T et al. Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 1995; 269:1863–1865.PubMedCrossRefGoogle Scholar
  51. 51.
    van der Luit AH, Olivari C, Haley A et al. Distinct calcium signaling pathways regulate calmoduiin gene expression in tobacco. Plant Phys 1999; 121:705–714.CrossRefGoogle Scholar
  52. 52.
    Pauly N, Knight MR, Thuleau P et al. Control of free calcium in plant cell nuclei. Nature 2000; 405:754–755.PubMedCrossRefGoogle Scholar
  53. 53.
    Rizzuto R, Pinton P, Carrington W et al. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 1998; 280:1763–1766.PubMedCrossRefGoogle Scholar
  54. 54.
    Sanders D, Brownlee C, Harper JF. Communicating with calcium. Plant cell 1999; 11:691–706.PubMedGoogle Scholar
  55. 55.
    Yuasa K, Maeshima M. Purification, properties, and molecular cloning of a novel Ca2+-binding protein in radish vacuoles. Plant Physiol 2000; 124:1069–1078.PubMedCrossRefGoogle Scholar
  56. 56.
    Liang F, Sze H. A high affinity Ca2+ pump, ECA1, from the endoplasmic reticulum is inhibited by cyclopiazonic acid but not by thapsigargin. Plant Physiol 1998; 817–825.Google Scholar
  57. 57.
    Hong BA, Ichida S, Wang Y et al. Identification of a calmodulin-regulated Ca2+ ATPase in the ER. Plant Physiol 1999; 119; 1165–1176.PubMedCrossRefGoogle Scholar
  58. 58.
    Klüsener B, Boheim G, Liss H et al. Gadolinium-sensitive, voltage-dependent calcium release channels in the endoplasmic reticulum of a highet plant mechanoreceptor organ. EMBO J 1995; 14:2708–2714.PubMedGoogle Scholar
  59. 59.
    Klüsener B, Weiler EW. A calcium-selective channel from root-tip endomembranes of garden cress. Plant Phys 1999 119:1399–1405.CrossRefGoogle Scholar
  60. 60.
    Navazio L, Bewell MA, Siddiqua A et al. Calcium release from the endoplasrmc reticulum of higher plants elicited by the NADP metabolite nicotinic acid adenine dinucleotide phosphate. Proc Natl Acad Sci USA 2000; 8693–8698.Google Scholar
  61. 61.
    Navazio L, Mariani P, Sanders D. Mobilization of Ca2+ by cyclic ADP-ribose from the endoplasmic reticulum of cauliflower florets. Plant Physiol 2001; 125:2129–2138.PubMedCrossRefGoogle Scholar
  62. 62.
    Muir SR, Sanders D. Inositol 1,4,5-trisphosphate-sensitive Ca2+ release across nonvacuolar membranes in cauliflower. Plant Physiol 1997; 11:1511–1521.CrossRefGoogle Scholar
  63. 63.
    Boevink P, Oparka K, Santa Cruz S et al. Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 1998; 15:441–447.PubMedCrossRefGoogle Scholar
  64. 64.
    Reuzeau C, McNally JG, Pickard B. The endomembrane sheath: a key structure for understanding the plant cell? Protoplasma 1997; 200:1–9.PubMedCrossRefGoogle Scholar
  65. 65.
    Knight H, Trewavas AJ, Knight MR. Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant cell 1996; 8:489–503PubMedGoogle Scholar
  66. 66.
    Knight MR, Smith SM, Trewavas AJ. Wind-induced plant motion immediately increases cytosolic calcium. Proc Natl Acad Sci 1992; 89:4967–4971.PubMedCrossRefGoogle Scholar
  67. 67.
    Evans NH, McAinsh MR, Hetherington AM. Calcium oscillations in higher plants. Curr Opin Plant Biol 2001; 4:415–420.PubMedCrossRefGoogle Scholar
  68. 68.
    Bauer CS, Plieth C, Hansen U-P et al. Repetitive Ca2+ spikes in a unicellular green alga. FEBS Lett 1997; 405:390–393.PubMedCrossRefGoogle Scholar
  69. 69.
    Bauer CS, Plieth C, Bethmann B et al. Strontium-induced repetitive calcium spikes in a unicellular green alga. Plant Physiol 1998; 117:545–557.PubMedCrossRefGoogle Scholar
  70. 70.
    Malhó R, Moutinho A, van der Luit A et al. Spatial characteristics of calcium signalling: the calcium wave as a basic unit in plant cell calcium signalling. Phil Trans R Soc Lond 1998; 353:1463–1473.CrossRefGoogle Scholar
  71. 71.
    Corbett EF, Michalak M. Calcium, a signalling molecule in the endoplasmic reticulum? Trends Biol Sci 2000; 25:307–311.CrossRefGoogle Scholar
  72. 72.
    Persson S, Wyatt SE, Love J et al. The Ca2+ status of the endoplasmic reticulum is altered by induction of calreticulin expression in transgenic plants. Plant Physiol 2001; 126:1092–1104.PubMedCrossRefGoogle Scholar
  73. 73.
    Camacho P, Lechleiter JD. Calreticulin inhibits repetitive intracellular Ca2+ waves. Cell 1995; 82:765–771.PubMedCrossRefGoogle Scholar
  74. 74.
    John LM, Lechleiter JD, Camacho P. Differential modulation of SERCA2 isoforms by calreticulin. J Cell Biol 1998; 142:963–973.PubMedCrossRefGoogle Scholar
  75. 75.
    Wyatt SE, Tsou PL, Robertson D. Expression of the high capacity calcium-binding domain of calreticulin increases bioavailable calcium stores in plants. Transgenic Res 2002; 11:1–10.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2003

Authors and Affiliations

  • Paola Mariani
  • Lorella Navazio
  • Anna Zuppini

There are no affiliations available

Personalised recommendations