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The riddle of the plant vacuolar sorting receptors

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Summary.

Proteins synthesized on membrane-bound ribosomes are sorted at the Golgi apparatus level for delivery to various cellular destinations: the plasma membrane or the extracellular space, and the lytic vacuole or lysosome. Sorting involves the assembly of vesicles, which preferentially package soluble proteins with a common destination. The selection of proteins for a particular vesicle type involves the recognition of proteins by specific receptors, such as the vacuolar sorting receptors for vacuolar targeting. Most eukaryotic organisms have one or two receptors to target proteins to the lytic vacuole. Surprisingly, plants have several members of the same family, seven in Arabidopsis thaliana. Why do plants have so many proteins to sort soluble proteins to their respective destinations? The presence of at least two types of vacuoles, lytic and storage, seems to be a partial answer. In this review we analyze the last experimental evidence supporting the presence of different subfamilies of plant vacuolar sorting receptors.

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Abbreviations

CCV:

clathrin-coated vesicles

ER:

endoplasmic reticulum

PSV:

protein storage vacuole

TGN:

trans-Golgi network

VSR:

vacuolar sorting receptor

References

  • SV Ahmed M Bar-Peled NV Raikhel (1997) ArticleTitleCloning 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 Occurrence Handle10.1104/pp.114.1.325 Occurrence Handle9159954 Occurrence Handle1:CAS:528:DyaK2sXjtlehs7c%3D

    Article  PubMed  CAS  Google Scholar 

  • InstitutionalAuthorNameArabidopsis Genome Initiative (2000) ArticleTitleAnalysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408 796–815

    Google Scholar 

  • L Beevers NV Raikhel (1998) ArticleTitleTransport to the vacuole: receptors and trans elements. J Exp Bot 49 1271–1279 Occurrence Handle10.1093/jexbot/49.325.1271 Occurrence Handle1:CAS:528:DyaK1cXlsVOktr4%3D

    Article  CAS  Google Scholar 

  • MW Black HRB Pelham (2000) ArticleTitleA selective transport route from Golgi to late endosomes that requires the yeast GGA proteins. J Cell Biol 151 587–600 Occurrence Handle10.1083/jcb.151.3.587 Occurrence Handle11062260 Occurrence Handle1:CAS:528:DC%2BD3cXnsl2lsLg%3D

    Article  PubMed  CAS  Google Scholar 

  • J Bonifacino L Traub (2003) ArticleTitleSignals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72 395–447 Occurrence Handle10.1146/annurev.biochem.72.121801.161800 Occurrence Handle12651740 Occurrence Handle1:CAS:528:DC%2BD3sXntFSgtLc%3D

    Article  PubMed  CAS  Google Scholar 

  • G Boudart E Jamet M Rossignol C Lafitte G Borderies A Jauneau M-T Esquerré-Tugayé R Pont-Lezica (2005) ArticleTitleCell wall proteins in apoplastic fluids of Arabidopsis thaliana rosettes: identification by mass spectrometry and bioinformatics. Proteomics 5 212–221 Occurrence Handle10.1002/pmic.200400882 Occurrence Handle15593128 Occurrence Handle1:CAS:528:DC%2BD2MXhtleis7c%3D

    Article  PubMed  CAS  Google Scholar 

  • MJ Chrispeels EM Herman (2000) ArticleTitleEndoplasmic reticulum-derived compartments function in storage and as mediators of vacuolar remodeling via a new type of organelle, precursor protease vesicles. Plant Physiol 123 1227–1234 Occurrence Handle10938342 Occurrence Handle1:CAS:528:DC%2BD3cXmtVehtbk%3D

    PubMed  CAS  Google Scholar 

  • E Conibear T Stevens (1998) ArticleTitleMultiple sorting pathways between the late Golgi and the vacuole in yeast. Biochim Biophys Acta 1404 211–230 Occurrence Handle9714809 Occurrence Handle1:CAS:528:DyaK1cXltFWktrc%3D

    PubMed  CAS  Google Scholar 

  • N Geldner J Friml Y Stierhof G Jurgens K Palme (2001) ArticleTitleAuxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413 425–428 Occurrence Handle10.1038/35096571 Occurrence Handle11574889 Occurrence Handle1:CAS:528:DC%2BD3MXntl2gtb0%3D

    Article  PubMed  CAS  Google Scholar 

  • SR Gerrard NJ Bryant TH Stevens (2000a) ArticleTitleVps21 controls entry of endocytosed and biosynthetic proteins into the yeast prevacuolar compartment. Mol Biol Cell 11 613–626 Occurrence Handle1:CAS:528:DC%2BD3cXjsl2itbo%3D

    CAS  Google Scholar 

  • – Levi BP, Stevens TH (2000b) Pep12p is a multifunctional yeast syntaxin that controls entry of biosynthetic, endocytic and retrograde traffic into the prevacuolar compartment. Traffic 1: 259–269

    Google Scholar 

  • P Ghosh NM Dahms S Kornfeld (2003) ArticleTitleMannose-6-phosphate receptors: new twists in the tale. Nat Rev Mol Cell Biol 4 2002–20012 Occurrence Handle10.1038/nrm1050 Occurrence Handle1:CAS:528:DC%2BD3sXhsFajsL0%3D

    Article  CAS  Google Scholar 

  • JL Hadlington J Denecke (2000) ArticleTitleSorting of soluble proteins in the secretory pathway of plants. Curr Opin Plant Biol 3 461–468 Occurrence Handle10.1016/S1369-5266(00)00114-X Occurrence Handle11074376 Occurrence Handle1:CAS:528:DC%2BD3cXovVSiu7c%3D

    Article  PubMed  CAS  Google Scholar 

  • N Happel S Höning JM Neuhaus N Paris DG Robinson EH Holstein (2004) ArticleTitle Arabidopsis μA-adaptin interacts with the tyrosine motif of the vacuolar sorting receptor VSR-PS1. Plant J 37 678–693 Occurrence Handle10.1111/j.1365-313X.2003.01995.x Occurrence Handle14871308 Occurrence Handle1:CAS:528:DC%2BD2cXislyltrg%3D

    Article  PubMed  CAS  Google Scholar 

  • S Hillmer A Movafeghi DG Robinson G Hinz (2001) ArticleTitleVacuolar storage proteins are sorted in the cis-cisternae of the pea cotyledon Golgi apparatus. J Cell Biol 152 41–50 Occurrence Handle10.1083/jcb.152.1.41 Occurrence Handle11149919 Occurrence Handle1:CAS:528:DC%2BD3MXjslyisw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • D Humair D Hernandez Felipe JM Neuhaus N Paris (2001) ArticleTitleDemonstration in yeast of the function of BP-80, a putative plant vacuolar sorting receptor. Plant Cell 13 781–792 Occurrence Handle10.1105/tpc.13.4.781 Occurrence Handle11283336 Occurrence Handle1:CAS:528:DC%2BD3MXjtFWqu7s%3D

    Article  PubMed  CAS  Google Scholar 

  • GY Jauh AM Fisher HD Grimes CA Ryan JC Rogers (1998) ArticleTitleδ-Tonoplast intrinsic protein defines unique plant vacuole functions. Proc Natl Acad Sci USA 95 12995–12999 Occurrence Handle10.1073/pnas.95.22.12995 Occurrence Handle9789029 Occurrence Handle1:CAS:528:DyaK1cXntFWktbw%3D

    Article  PubMed  CAS  Google Scholar 

  • L Jiang TE Phillips CA Hamm YM Drozdowicz PA Rea M Maeshima SW Rogers JC Rogers (2001) ArticleTitleThe protein storage vacuole: a unique compound organelle. J Cell Biol 155 991–1002 Occurrence Handle10.1083/jcb.200107012 Occurrence Handle11739409 Occurrence Handle1:CAS:528:DC%2BD3MXptVejsbo%3D

    Article  PubMed  CAS  Google Scholar 

  • NA Jolliffe JC Brown U Neumann M Vicré A Bachi C Hawes A Ceriotti LM Roberts L Frigerio (2004) ArticleTitleTransport of ricin and 2S albumin precursors to the storage vacuoles of Ricinus communis endosperm involves the golgi and VSR-like receptors. Plant J 39 821–833 Occurrence Handle10.1111/j.1365-313X.2004.02167.x Occurrence Handle15341626 Occurrence Handle1:CAS:528:DC%2BD2cXpt1GntLw%3D

    Article  PubMed  CAS  Google Scholar 

  • T Kirsch N Paris JM Butler L Beevers C Rogers (1994) ArticleTitlePurification and initial characterization of a potential plant vacuolar targeting receptor. Proc Natl Acad Sci USA 91 3403–3407 Occurrence Handle8159760 Occurrence Handle1:CAS:528:DyaK2cXltVahtr4%3D

    PubMed  CAS  Google Scholar 

  • S Kornfeld (1992) ArticleTitleStructure and function of the mannose 6-phosphate/insulinlike growth factor II receptors. Annu Rev Biochem 61 307–330 Occurrence Handle10.1146/annurev.bi.61.070192.001515 Occurrence Handle1323236 Occurrence Handle1:CAS:528:DyaK38Xlt1Cmtb8%3D

    Article  PubMed  CAS  Google Scholar 

  • V Laval M Chabannes M Carriere H Canut A Barre P Rouge R Pont-Lezica J Galaud (1999) ArticleTitleA family of Arabidopsis plasma membrane receptors presenting animal beta-integrin domains. Biochim Biophys Acta 1435 61–70 Occurrence Handle10561538 Occurrence Handle1:CAS:528:DyaK1MXotVOqsb4%3D

    PubMed  CAS  Google Scholar 

  • – Masclaux F, Serin A, Carriere M, Roldan C, Devic M, Pont-Lezica RF, Galaud J-P (2003) Seed germination is blocked in Arabidopsis putative vacuolar sorting receptor (AtBP80) antisense transformants. J Exp Bot 54: 213–221

    Google Scholar 

  • E Marcusson B Horazdovsky J Cereghino E Gharakhanian S Emr (1994) ArticleTitleThe sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell 77 579–586 Occurrence Handle10.1016/0092-8674(94)90219-4 Occurrence Handle8187177 Occurrence Handle1:CAS:528:DyaK2cXltVeku7k%3D

    Article  PubMed  CAS  Google Scholar 

  • I Mellman G Warren (2000) ArticleTitleThe road taken: past and future foundations of membrane traffic. Cell 100 99–112 Occurrence Handle10.1016/S0092-8674(00)81687-6 Occurrence Handle10647935 Occurrence Handle1:CAS:528:DC%2BD3cXks1CrsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • K Nakabayashi M Okamoto T Koshiba Y Kamiya E Nambara (2005) ArticleTitleGenome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41 697–709 Occurrence Handle10.1111/j.1365-313X.2005.02337.x Occurrence Handle15703057 Occurrence Handle1:CAS:528:DC%2BD2MXisVWitb8%3D

    Article  PubMed  CAS  Google Scholar 

  • J-M Neuhaus JC Rogers (1998) ArticleTitleSorting of proteins to vacuoles in plant cells. Plant Mol Biol 38 127–144 Occurrence Handle10.1023/A:1006032627036 Occurrence Handle9738964 Occurrence Handle1:CAS:528:DyaK1cXlslegsbY%3D

    Article  PubMed  CAS  Google Scholar 

  • MS Nielsen P Madsen EI Christensen A Nykjaer J Gliemann D Kasper R Pohlmann CM Petersen (2001) ArticleTitleThe sortilin cytoplasmic tail conveys Golgi-endosome transport and binds the VS domain of the GAA2 sorting protein. EMBO J 20 2180–2190 Occurrence Handle10.1093/emboj/20.9.2180 Occurrence Handle11331584 Occurrence Handle1:CAS:528:DC%2BD3MXjsl2gu7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • K Nishizawa N Maruyama R Satoh Y Fuchikami T Higasa S Utsumi (2003) ArticleTitleA C-terminal sequence of soybean β-conglycin α′ subunit acts as a vacuolar sorting determinant in seed cells. Plant J 34 647–659 Occurrence Handle10.1046/j.1365-313X.2003.01754.x Occurrence Handle12787246 Occurrence Handle1:CAS:528:DC%2BD3sXlsFels78%3D

    Article  PubMed  CAS  Google Scholar 

  • A Nykjaer R Lee KK Teng P Jansen P Madsen MS Nielsen C Jacobsen M Kliemannel E Schwarz TE Willnow BL Hempstead CM Petersen (2004) ArticleTitleSortilin is essential for proNGF-induced neuronal cell death. Nature 427 843–848 Occurrence Handle10.1038/nature02319 Occurrence Handle14985763 Occurrence Handle1:CAS:528:DC%2BD2cXhsFCis7s%3D

    Article  PubMed  CAS  Google Scholar 

  • K Palme L Galweiler (1999) ArticleTitlePin-pointing the molecular basis of auxin transport. Curr Opin Plant Biol 2 375–381 Occurrence Handle10.1016/S1369-5266(99)00008-4 Occurrence Handle10508762 Occurrence Handle1:CAS:528:DyaK1MXmvFSis7w%3D

    Article  PubMed  CAS  Google Scholar 

  • N Paris J-M Neuhaus (2002) ArticleTitleBP-80 as a vacuolar sorting receptor. Plant Mol Biol 50 903–914 Occurrence Handle10.1023/A:1021205715324 Occurrence Handle12516861 Occurrence Handle1:CAS:528:DC%2BD38XptFejtb4%3D

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • – 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

    Google Scholar 

  • J Petrasek A Cerna K Schwarzerova M Elckner DA Morris E Zazimalova (2003) ArticleTitleDo phytotropins inhibit auxin efflux by impairing vesicle traffic? Plant Physiol 131 254–263 Occurrence Handle10.1104/pp.012740 Occurrence Handle12529533 Occurrence Handle1:CAS:528:DC%2BD3sXnvVGnsg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • R Puertollano PA Randazzo JF Presley LM Hartnell JS Bonifacino (2001a) ArticleTitleThe GGAs promote ARF-dependent recruitment of clathrin to the TGN. Cell 105 93–102 Occurrence Handle10.1016/S0092-8674(01)00299-9 Occurrence Handle1:CAS:528:DC%2BD3MXivFOjtr8%3D

    Article  CAS  Google Scholar 

  • – Aguilar RC, Gorshkova I, Crouch RJ, Bonifacino JS (2001b) Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science 292: 1712–1716

    Google Scholar 

  • L Rajjou K Gallardo I Debeaujon J Vandekerckhove C Job D Job (2004) ArticleTitleThe effect of α-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 134 1598–1613 Occurrence Handle10.1104/pp.103.036293 Occurrence Handle15047896 Occurrence Handle1:CAS:528:DC%2BD2cXjsFKmsLk%3D

    Article  PubMed  CAS  Google Scholar 

  • D Robinson G Hinz (1997) ArticleTitleVacuole biogenesis and protein transport to the plant vacuole: a comparison with the yeast and mammalian lysosome. Protoplasma 197 1–25 Occurrence Handle10.1007/BF01279880 Occurrence Handle1:CAS:528:DyaK2sXktVCntbo%3D

    Article  CAS  Google Scholar 

  • F Servant C Bru S Carrère E Courcelle J Gouzy D Peyruc D Kahn (2002) ArticleTitleProdom: automated clustering of homologous domains. Briefings Bioinformatics 3 246–251 Occurrence Handle1:CAS:528:DC%2BD38XnsFOhtbk%3D

    CAS  Google Scholar 

  • T Shimada M Kuroyanagi M Nishimura I Hara-Nishimura (1997) ArticleTitleA pumpkin 72-kDa membrane protein of precursor-accumulating vesicles has characteristics of a vacuolar sorting receptor. Plant Cell Physiol 38 1414–1420 Occurrence Handle9522472 Occurrence Handle1:CAS:528:DyaK1cXlsVem

    PubMed  CAS  Google Scholar 

  • – 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: 16095–16100

    Google Scholar 

  • K Takegawa T Iwaki Y Fujita T Morita A Hosomi N Tanaka (2003) ArticleTitleVesicle-mediated protein transport pathways to the vacuole in Schizosaccharomyces pombe. Cell Struct Funct 28 399–417 Occurrence Handle10.1247/csf.28.399 Occurrence Handle14745133 Occurrence Handle1:CAS:528:DC%2BD2cXhvVGlu74%3D

    Article  PubMed  CAS  Google Scholar 

  • LM Traub S Kornfeld (1997) ArticleTitleThe trans-Golgi network: a late secretory sorting station. Curr Opin Cell Biol 9 527–533 Occurrence Handle10.1016/S0955-0674(97)80029-4 Occurrence Handle9261049 Occurrence Handle1:CAS:528:DyaK2sXltVWhtL0%3D

    Article  PubMed  CAS  Google Scholar 

  • TH Ward F Brandizzi (2004) ArticleTitleDynamics of proteins in Golgi membranes: comparison between mammalian and plant cells highlighted by photobleaching techniques. Cell Mol Life Sci 61 172–185 Occurrence Handle14745496 Occurrence Handle1:CAS:528:DC%2BD2cXjt1yht7c%3D Occurrence Handle10.1007/s00018-003-3355-6

    Article  PubMed  CAS  Google Scholar 

  • E Watanabe T Shimada K Tamura R Matsushima Y Koumoto M Nishimura I Hara-Nishimura (2004) ArticleTitleAn ER-localized form of PV72, a seed-specific vacuolar sorting receptor, interferes the transport of an NPIR-containing proteinase in Arabidopsis leaves. Plant Cell Physiol 45 9–17 Occurrence Handle10.1093/pcp/pch012 Occurrence Handle14749481 Occurrence Handle1:CAS:528:DC%2BD2cXpsVajtQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • J Whyte S Munro (2001) ArticleTitleA yeast homolog of the mammalian mannose 6-phosphate receptors contributes to the sorting of vacuolar hydrolases. Curr Biol 11 1074–1078 Occurrence Handle10.1016/S0960-9822(01)00273-1 Occurrence Handle11470415 Occurrence Handle1:CAS:528:DC%2BD3MXltlOgsLo%3D

    Article  PubMed  CAS  Google Scholar 

  • J Zouhar GR Hicks NV Raikhel (2004) ArticleTitleSorting inhibitors (Sortins): chemical compounds to study vacuolar sorting in Arabidopsis. Proc Natl Acad Sci USA 101 9497–9501 Occurrence Handle10.1073/pnas.0402121101 Occurrence Handle15190181 Occurrence Handle1:CAS:528:DC%2BD2cXltlKjsbY%3D

    Article  PubMed  CAS  Google Scholar 

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  1. Surfaces Cellulaires et Signalisation chez les Végétaux, Unité Mixte de Recherche 5546 de Centre National de la Recherche Scientifique, Université Paul Sabatier, Castanet-Tolosan

    F. G. Masclaux, J.-P. Galaud & R. Pont-Lezica

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  1. F. G. Masclaux
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  2. J.-P. Galaud
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  3. R. Pont-Lezica
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Correspondence to R. Pont-Lezica.

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Correspondence and reprints: Surfaces Cellulaires et Signalisation chez les Végétaux, UMR 5546 de CNRS, Université Paul Sabatier, BP 42617 Auzeville, 31326 Castanet-Tolosan, France.

Present address: Laboratoire de Génétique Végétale, Sciences III 30, Université de Genève, Genève, Switzerland.

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Masclaux, F., Galaud, JP. & Pont-Lezica, R. The riddle of the plant vacuolar sorting receptors. Protoplasma 226, 103–108 (2005). https://doi.org/10.1007/s00709-005-0117-3

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