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Plant Vacuoles: from Biogenesis to Function

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Plant Endocytosis

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 1))

Abstract

The plant vacuolar system is far more complex than originally expected and multiple sorting pathways leading to various types of vacuoles can be found depending on the cell type and on the stage of development. In addition, the vacuolar system is highly dynamic and can adjust to environmental signals to meet the changing needs of the plant. Some recent advances have been made in the identification of the molecular mechanisms by which such a complex compartmentation develops and evolves over time. In this review, we present an update of the latest results in this exciting field and propose distinct biogenesis models for the formation of vacuoles in vegetative and seed tissues, taking into account some apparently contradictory results.

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References

  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

    Article  PubMed  Google Scholar 

  2. Avila E, Zouhar J, Agee A, Carter D, Chary S, Raikhel N (2003) Tools to study plant organelle biogenesis. Point mutation lines with disrupted vacuoles and high-speed confocal screening of green fluorescent protein-tagged organelles. Plant Physiol 133:1373–1376

    Article  Google Scholar 

  3. Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166

    Article  PubMed  Google Scholar 

  4. Brown JC, Jolliffe NA, Frigerio L, Roberts LM (2003) Sequence-specific, Golgi dependent targeting of the castor bean 2S albumin to the vacuole in tobacco protoplasts. Plant Journal 36:711–719

    Article  PubMed  Google Scholar 

  5. Cao X, Rogers SW, Butler J, Beevers L, Rogers JC (2000) Structural requirements for ligand binding by a probable plant vacuolar sorting receptor. Plant Cell 12:493–506

    Article  PubMed  Google Scholar 

  6. Carter C, Pan S, Zouhar J, Avila E, Girke T, Raikhel N (2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 16:3285–3303

    Article  PubMed  Google Scholar 

  7. Castelli S, Vitale A (2005) The phaseolin vacuolar sorting signal promotes transient, strong membrane association and aggregation of the bean storage protein in transgenic tobacco. J Exp Bot 56:1379–1387

    Article  PubMed  Google Scholar 

  8. Cosgrove DJ (1997) Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol 13:171–201

    Article  PubMed  Google Scholar 

  9. Cosgrove DJ (1993) How do plant cell walls extend? J Plant Physiol 102:1–6

    Google Scholar 

  10. Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321–326

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  12. Di Sansebastiano G-P, Paris N, Marc-Martin S, Neuhaus J-M (1998) Specific accumulation of GFP in a non-acidic vacuolar compartment via a C-terminal propeptide-mediated sorting pathway. Plant J 15:449–457

    Article  PubMed  Google Scholar 

  13. Di Sansebastiano G-P, Paris N, Marc-Martin S, Neuhaus J-M (2001) Regeneration of a lytic central vacuole and of neutral peripheral vacuoles can be visualised by GFP targeted to either type of vacuoles. Plant Physiol 126:78–86

    Article  PubMed  Google Scholar 

  14. Diwu Z, Chen C-S, Zhang C, Klaubert DH, Haugland RP (1999) A novel acidotropic pH indicator and its potential application in labeling acidic organelles of live cells. Chem Biol 6:411–418

    Article  PubMed  Google Scholar 

  15. Dombrowski JE, Schroeder MR, Bednarek SY, Raikhel NV (1993) Determination of the functional elements within the vacuolar targeting signal of barley lectin. Plant Cell 5:587–596

    Article  PubMed  Google Scholar 

  16. Echeverría E (2000) Vesicle-Mediated Solute Transport between the Vacuole and the Plasma Membrane. Plant Physiol 123:1217–1226

    Article  PubMed  Google Scholar 

  17. Felsenstein J (1988) Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22:521–565

    Article  PubMed  Google Scholar 

  18. Fleurat-Lessard P, Frangne N, Maeshima M, Ratajczak R, Bonnemain JL, Martinoia E (1997) Increased expression of vacuolar aquaporin and H+-ATPase related to motor cell function in Mimosa pudica L. Plant Physiol 114:827–834

    PubMed  Google Scholar 

  19. Flückiger R, De Caroli M, Piro G, Dalessandro G, Neuhaus J-M, Di Sansebastiano G-P (2003) Vacuolar system distribution in Arabidopsis tissues, visualized using GFP fusion proteins. J Exp Bot 54:1577–1584

    Article  PubMed  Google Scholar 

  20. Frigerio L, Foresti O, Hernández Felipe D, Neuhaus J-M, Vitale A (2001) The C-terminal tetrapeptide of phaseolin is sufficient to target green fluorescent protein to the vacuole. J Plant Physiol 158:499–503

    Article  Google Scholar 

  21. Frigerio L, Jolliffe NA, Di Cola A, Hernández Felipe D, Paris N, Neuhaus J-M, Lord JM, Ceriotti A, Roberts LM (2001) The internal propeptide of the ricin precursor carries a sequence-specific determinant for vacuolar sorting. Plant Physiol 126:167–175

    Article  PubMed  Google Scholar 

  22. Gietl C, Schmid M, Simpson DJ (2000) Ricinosomes and aleurain-containing vacuoles (ACVs): proteases-storing organelles. In: Robinson DG and Rogers JC (eds) Vacuolar compartments, vol 5, pp 90–11

    Google Scholar 

  23. Gomez L, Chrispeels MJ (1993) Tonoplast and soluble vacuolar proteins are targeted by different mechanisms. Plant Cell 5:1113–1124

    Article  PubMed  Google Scholar 

  24. Hara-Nishimura I, Shimada T, Hatano K, Yakeuchi Y, Nishimura M (1998) Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles. Plant Cell 10:825–836

    Article  PubMed  Google Scholar 

  25. Hicks G, Rojo E, Hong S, Carter D, Raikhel N (2004) Germinating pollen has tubular vacuoles, displays highly dynamic vacuole biogenesis, and requires VACUOLESS1 for proper function. Plant Physiol 134:1227–1239

    Article  PubMed  Google Scholar 

  26. Hinz G, Hillmer S, Baumer M, Hohl I (1999) Vacuolar storage proteins and the putative vacuolar sorting receptor BP80 exit the Golgi apparatus of developing pea cotyledons in different transport vesicles. Plant Cell 11:1509–1524

    Article  PubMed  Google Scholar 

  27. Hinz G, Menze A, Hohl I, Vaux D (1997) Isolation of prolegumin from developing pea seeds: its binding to endomembranes and assembly into prolegumin hexamers in the protein storage vacuole. J Exp Botany 48:139–149

    Google Scholar 

  28. Hodel Hernández D, Paris N, Neuhaus J-M, Deloche O (2005) The yeast S. cerevisiae is not an efficient tool for in vivo studies of plant vacuolar sorting receptors. Plant Cell

    Google Scholar 

  29. Holwerda BC, Padgett HS, Rogers JC (1992) Proaleurain vacuolar targeting is mediated by short contiguous peptide interactions. Plant Cell 4:307–318

    Article  PubMed  Google Scholar 

  30. Humair D, Hernández Felipe D, Neuhaus J-M, Paris N (2001) Demonstration in yeast of the function of BP80, a putative plant vacuolar sorting receptor. Plant Cell 13:781–792

    Article  PubMed  Google Scholar 

  31. Jauh G-Y, Phillips TE, Rogers JC (1999) Tonoplast intrinsic protein isoforms as markers for vacuolar functions. Plant Cell 11:1867–1882

    Article  PubMed  Google Scholar 

  32. Jiang L, Erickson A, Rogers JC (2002) Multivesicular bodies: a mechanism to package lytic and storage functions in one organelle? Trends Cell Biol 12:362–367

    Article  PubMed  Google Scholar 

  33. Jiang L, Phillips TE, Hamm CA, Drozdowicz YM, Rea PA, Maeshima M, Rogers SW, Rogers JC (2001) The protein storage vacuole: a unique compound organelle. J Cell Biol 155:991–1002

    Article  PubMed  Google Scholar 

  34. Jiang L, Phillips TE, Rogers SW, Rogers JC (2000) Biogenesis of the protein storage vacuole crystalloid. J Cell Biol 150:755–770

    Article  PubMed  Google Scholar 

  35. Jiang LW, Rogers JC (1998) Integral membrane protein sorting to vacuoles in plant cells: evidence for two pathways. J Cell Biol 143:1183–1199

    Article  PubMed  Google Scholar 

  36. Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjövall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126:1358–1369

    Article  PubMed  Google Scholar 

  37. Johnson KD, Herman EM, Chrispeels MJ (1989) An abundant, highly conserved tonoplast protein in seeds. Plant Physiol 91:1006–1013

    Google Scholar 

  38. Jolliffe N, Brown J, Neumann U, Vicré M, Bachi A, Hawes C, Ceriotti A, Roberts LM, Frigerio L (2004) Transport of ricin and 2S albumin precursors to the storage vacuoles of Ricinus communis endosperm involves the Golgi and VSR-like receptors. Plant Journal 39:821–833

    Article  PubMed  Google Scholar 

  39. 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

    PubMed  Google Scholar 

  40. Kirsch T, Saalbach G, Raikhel NV, Beevers L (1996) Interaction of a potential vacuolar targeting receptor with amino- and carboxyl-terminal targeting determinants. Plant Physiol 111:469–474

    Article  PubMed  Google Scholar 

  41. Laval V, Chabannes M, Carrière M, Canut H, Barre A, Rougé P, Pont-Lezica R, Galaud J-P (1999) A family of Arabidopsis plasma membrane receptors presenting animalβ-integrin domains. Biochim Biophys Acta 1435:61–70

    PubMed  Google Scholar 

  42. Laval V, Masclaux F, Serin A, Carrière M, Roldan C, Devic M, Pont-Lezica RF, Galaud J-P (2003) Seed germination is blocked in Arabidopsis putative (atbp80) antisense transformants. J Exp Bot 54:213–221

    Article  PubMed  Google Scholar 

  43. Loqué D, Ludewig U, Yuan L, von Wiren N (2005) Tonoplast Intrinsic Proteins AtTIP2;1 and AtTIP2;3 Facilitate NH3 Transport into the Vacuole. Plant Physiol 137:671–678

    Article  PubMed  Google Scholar 

  44. MacRobbie E (1999) Vesicle trafficking: a role in trans-tonoplast ion movements. J Exp Bot 50:925–934

    Article  Google Scholar 

  45. Martinoia E, Massonneau A, Frangne N (2000) Transport processes of solutes across the vacuolar membrane of higher plants. Plant Cell Physiol 41:1175–1186

    Article  Google Scholar 

  46. 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

    Article  PubMed  Google Scholar 

  47. Matsuoka K, Neuhaus J-M (1999) Cis-elements of protein transport to the plant vacuoles. J Exp Bot 50:165–174

    Article  Google Scholar 

  48. Maurel C, Chrispeels M (2001) Aquaporins: a molecular entry into plant water relations. Plant Physiol 125:135–138

    Article  PubMed  Google Scholar 

  49. Montero M, Alvarez J, Scheenen WJJ, Rizzuto R, Meldolesi J, Pozzan T (1997) Ca2+ homeostasis in the endoplasmic reticulum: coexistence of high and low [Ca2+] subcompartments in intact HeLa cells. J Cell Biol 139:601–611

    Article  PubMed  Google Scholar 

  50. Moriyasu Y, Hattori M, Jauh GY, Rogers JC (2003) Alpha tonoplast intrinsic protein is specifically associated with vacuole membrane involved in an autophagic process. Plant Cell Physiol 44:795–802

    Article  Google Scholar 

  51. Murphy KA, Rachel A, Kuhle RA, Fischer AM, Anterola AM, Grimes HD (2005) The functional status of paraveinal mesophyll vacuoles changes in response to altered metabolic conditions in soybean leaves. Funct Plant Biol 32:335–344

    Google Scholar 

  52. Netting AG (2002) pH, abscisic acid and the integration of metabolism in plants under stressed and non-stressed conditions. II. Modifications in modes of metabolism induced by variation in the tension on the water column and by stress. J Exp Bot 53:151–173

    Article  PubMed  Google Scholar 

  53. Neuhaus J, Pietrzak M, Boller T (1994) Mutation analysis of the C-terminal vacuolar targeting peptide of tobacco chitinase: low specificity of the sorting system, and gradual transition between intracellular retention and secretion into the extracellular space. Plant J 5:45–54

    Article  PubMed  Google Scholar 

  54. Neuhaus J-M, Rogers JC (1998) Sorting of proteins to vacuoles in plant cells. Plant Mol Biol 38:127–144

    Article  PubMed  Google Scholar 

  55. Nishizawa K, Maruyama N, Satoh R, Fuchikami Y, Higasa T, Utsumi S (2003) A C-terminal sequence of soybean β-conglycinin α′subunit acts as a vacuolar sorting determinant in seed cells. Plant J 34:647–659

    Article  PubMed  Google Scholar 

  56. Otegui MS, Noh YS, Martinez DE, Vila Petroff MG, Staehelin LA, Amasino RM, Guiamet JJ (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J 41:831–844

    Article  PubMed  Google Scholar 

  57. 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

    Article  PubMed  Google Scholar 

  58. Paris N, Stanley CM, Jones RL, Rogers JC (1996) Plant cells contain two functionally distinct vacuolar compartments. Cell 85:563–572

    Article  PubMed  Google Scholar 

  59. Park M, Kim S, Vitale A, Hwang I (2004) Identification of the protein storage vacuole and protein targeting to the vacuole in leaf cells of three plant species. Plant Physiol 134:625–639

    Article  PubMed  Google Scholar 

  60. Pinton P, Pozzan T, Rizzuto R (1998) The Golgi apparatus is an inositol 1,4,5-trisphosphate-sensitive Ca2+ store, with functional properties distinct from those of the endoplasmic reticulum. EMBO J 17:5298–5308

    Article  PubMed  Google Scholar 

  61. Reisen D, Leborgne-Castel N, Özalp C, Chaumont F, Marty F (2003) Expression of a cauliflower tonoplast aquaporin tagged with GFP in tobacco suspension cells correlates with an increase in cell size. Plant Mol Biol 52:387–400

    Article  PubMed  Google Scholar 

  62. Robinson DG, Rogers JC (2000) Vacuolar compartments. Sheffield Academic Press and CRC Press, London, Sheffield, p 314

    Google Scholar 

  63. Sanderfoot AA, Raikhel N (2003) The secretory system of Arabidopsis. American Society of Plant Biologists, Rockville, MD

    Google Scholar 

  64. Lam SK, Tse YC, Jiang L, Oliviusson P, Heinzerling O, Robinson DG (2005) Plant prevacuolar compartments and endocytosis (in this volume). Springer, Berlin Heidelberg New York

    Google Scholar 

  65. Shimada T, Kuroyanagi M, Nishimura M, Hara-Nishimura I (1997) A pumpkin 72-kDa membrane protein of precursor-accumulating vesicles has characteristics of a vacuolar sorting receptor. Plant Cell Physiol 38:1414–1420

    Google Scholar 

  66. Shimada T, Fuji K, Tamura K, Kondo M, Nishimura M, Hara-Nishimura I (2003) Vacuolar sorting receptor for seed storage proteins in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:16 095–16 100

    Article  Google Scholar 

  67. Shimada T, Yamada K, Kataoka M, Nakaune S, Koumoto Y, Kuroyanagi M, Tabata S, Kato T, Shinozaki K, Seki M, Kobayashi M, Kondo M, Nishimura M, Hara-Nishimura I (2003) Vacuolar processing enzymes are essential for proper processing of seed storage proteins in Arabidopsis thaliana. J Biol Chem 278:32 292–32 299

    Article  Google Scholar 

  68. Smart LB, Vojdani F, Maeshima M, Wilkins TA (1998) Genes involved in osmoregulation during turgor-driven cell expansion of developing cotton fibers are differentially regulated. Plant Physiol 116:1539–1549

    Article  PubMed  Google Scholar 

  69. Surpin M, Rojas-Pierce M, Carter C, Hicks GR, Vasquez J, Raikhel NV (2005) The power of chemical genomics to study the link between endomembrane system components and the gravitropic response. Proc Natl Acad Sci USA 102:4902–4907

    Article  PubMed  Google Scholar 

  70. Swanson S, Bethke P, Jones R (1998) Barley aleurone cells contain two types of vacuoles. Characterization of lytic organelles by use of fluorescent probes. Plant Cell 10:685–698

    Article  PubMed  Google Scholar 

  71. Watanabe E, Shimada T, Kuroyanagi M, Nishimura M, Hara-Nishimura I (2002) Calcium-mediated association of a putative vacuolar sorting receptor PV72 with a propeptide of 2S albumin. J Biol Chem 277:8708–8715

    Article  PubMed  Google Scholar 

  72. Wenzel D, Schauermann G, von Lupke A, Hinz G (2005) The cargo in vacuolar storage protein transport vesicles is stratified. Traffic 6:45–55

    Article  PubMed  Google Scholar 

  73. Zeiger E, Zhu J (1998) Role of zeaxanthin in blue light photoreception and the modulation of light-CO2 interactions in guard cells. J Exp Bot 49:433–442

    Article  Google Scholar 

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Authors and Affiliations

  1. Laboratoire de Biochimie, rue E. Argand 9, BP2, 2007, Neuchâtel, Switzerland

    Jean-Marc Neuhaus

  2. CNRS-UMR 6037, IFRMP23, Université de Rouen, 76821, Mont Saint Aignan, France

    Nadine Paris

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  1. Jean-Marc Neuhaus
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  2. Nadine Paris
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Correspondence to Nadine Paris .

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Jozef Šamaj František Baluška Diedrik Menzel

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Neuhaus, JM., Paris, N. Plant Vacuoles: from Biogenesis to Function. In: Šamaj, J., Baluška, F., Menzel, D. (eds) Plant Endocytosis. Plant Cell Monographs, vol 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_005

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