Advertisement

Plant Vacuolar Sorting: An Overview

  • Bruno Peixoto
  • Susana PereiraEmail author
  • José Pissarra
Chapter
Part of the Progress in Botany book series (BOTANY, volume 78)

Abstract

Eukaryotic cells have developed membrane-bound organelles, connected between themselves in a complex and tightly regulated network – the endomembrane system. Despite being less well understood when compared to the animal and yeast models, plant cells have begun to reveal an intricate and dense network of endomembranes. Particularly diverse is the network of pathways revolving around the vacuole, especially when comparing plant and non-plant models. This dynamic, pleiomorphic and multifunctional organelle is essential for correct plant growth and development, compartmentalizing different components, from proteins to secondary metabolites. In this review we will provide an historical perspective of what has been discovered relating vacuolar sorting, and the potential biotech applications of such findings.

Keywords

Cardosin Chemical genomics Plant-specific insert RAB GTPase SNARE Vacuolar sorting Vacuole 

List of Abbreviations

AP

Aspartic proteinase

BFA

Brefeldin A

BP-80

80 kDa proaleurein-binding protein

CCV

Clathrin coated vesicle

CPY

Carboxypeptidase Y

ctVSD

C-terminal vacuolar sorting determinant

Cvt

Cytosol-to-vacuole targeting pathway

DCB

Dichlorobenzonitrile

EM

Electron microscopy

ER

Endoplasmic reticulum

ERvt

ER to the vacuole targeting pathway

EST

Expressed sequence tag

GEF

Guanine nucleotide exchange factor

LV

Lytic vacuole

M6P

Mannose-6-phosphate

PA Domain

Protease associated domain

PB

Protein body

PI3P

Phosphatidylinositol 3-phosphate

PM

Plasma membrane

PSI

Plant-specific insert

PSV

Protein storage vacuole

psVSD

Physical structure vacuolar sorting determinant

PVC

Prevacuolar compartment

RMR

Receptor-homology-region-transmembrane-domain-RING-H2

SAPLIP

Saposin-like protein

SNARE

Soluble NSF attachment protein receptor

ssVSD

Sequence-specific vacuolar sorting determinant

TGN

trans Golgi Network

TIP

Tonoplast intrinsic protein

VSR

Vacuolar sorting receptor

Notes

Acknowledgments

Work developed under the Strategic Project OE/BIA/UI4046/2014 of the BioISI – Biosystems & Integrative Sciences Institute, supported by FCT (Fundação para a Ciência e a Tecnologia) funding.

References

  1. Agarwal PK, Jain P, Jha B, Reddy MK, Sopory SK (2008) Constitutive over-expression of a stress-inducible small GTP binding protein PgRab7 from Pennisetum glaucum enhances abiotic stress tolerance in transgenic tobacco. Plant Cell Rep 27:105–115PubMedCrossRefGoogle Scholar
  2. Banyai W, Mii M, Supaibulwatana K (2011) Enhancement of artemisinin content and biomass in Artemisia annua by exogenous GA3 treatment. Plant Growth Regul 63:45–54CrossRefGoogle Scholar
  3. Bednarek SY, Wilkins TA, Dombrowski JE, Raikhel NV (1990) A carboxyl-terminal propeptide is necessary for proper sorting of barley lectin to vacuoles of tobacco. Plant Cell 2:1145–1155PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bocock J, Carmicle S, Chhotani S, Ruffolo MR, Chu H, Erickson AH (2009) The PA-TM-RING protein RING finger protein 13 is an endosomal integral membrane E3 ubiquitin ligase whose RING finger domain is released to the cytoplasm by proteolysis. FEBS J 276:1860–1877PubMedCrossRefGoogle Scholar
  5. Bolte S, Schiene K, Dietz KJ (2000) Characterization of a small GTP-binding protein of the rab 5 family in Mesembryanthemum crystallinum with increased level of expression during early salt stress. Plant Mol Biol 42:923–936PubMedCrossRefGoogle Scholar
  6. Bolte S, Lanquar V, Soler MN, Beebo A, Satiat-Jeunemaitre B, Bouhidel K, Thomine S (2011) Distinct lytic vacuolar compartments are embedded inside the protein storage vacuole of dry and germinating Arabidopsis thaliana seeds. Plant Cell Physiol 52:1142–1152PubMedCrossRefGoogle Scholar
  7. Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166PubMedCrossRefGoogle Scholar
  8. Bottanelli F, Foresti O, Hanton S, Denecke J (2011) Vacuolar transport in tobacco leaf epidermis cells involves a single route for soluble cargo and multiple routes for membrane cargo. Plant Cell 23:3007–3025PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bottanelli F, Gershlick DC, Denecke J (2012) Evidence for sequential action of Rab5 and Rab7 GTPases in prevacuolar organelle partitioning. Traffic 13:338–354PubMedCrossRefGoogle Scholar
  10. Bowers K, Stevens TH (2005) Protein transport from the late Golgi to the vacuole in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1744:438–454PubMedCrossRefGoogle Scholar
  11. 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 12:493–506PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chen JL, Fang HM, Ji YP, Pu GB, Guo YW, Huang LL, Du ZG, Liu BY, Ye HC, Li GF, Wang H (2011) Artemisinin biosynthesis enhancement in transgenic Artemisia annua plants by downregulation of the β-caryophyllene synthase gene. Planta Med 77:1759–1765PubMedCrossRefGoogle Scholar
  13. Chow CM, Neto H, Foucart C, Moore I (2008) Rab-A2 and Rab-A3 GTPases define a trans-golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate. Plant Cell 20:101–123PubMedPubMedCentralCrossRefGoogle Scholar
  14. Craddock CP, Hunter PR, Szakacs E, Hinz G, Robinson DG, Frigerio L (2008) Lack of a vacuolar sorting receptor leads to non-specific missorting of soluble vacuolar proteins in Arabidopsis seeds. Traffic 9:408–416PubMedCrossRefGoogle Scholar
  15. Cui Y, Zhao Q, Gao C, Ding Y, Zeng Y, Ueda T, Nakano A, Jiang L (2014) Activation of the Rab7 GTPase by the MON1-CCZ1 complex is essential for PVC-to-vacuole trafficking and plant growth in Arabidopsis. Plant Cell 26(5):2080–2097PubMedPubMedCentralCrossRefGoogle Scholar
  16. da Costa DS, Pereira S, Moore I, Pissarra J (2010) Dissecting cardosin B trafficking pathways in heterologous systems. Planta 232(6):1517–1530PubMedCrossRefGoogle Scholar
  17. Dacks JB, Fields MC (2007) Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J Cell Sci 120:2977–2985PubMedCrossRefGoogle Scholar
  18. De Benedictis M, Bleve G, Faraco M, Stigliano E, Grieco F, Piro G, Dalessandro G, Di Sansebastiano GP (2013) AtSYP51/52 functions diverge in the post-Golgi traffic and differently affect vacuolar sorting. Mol Plant 6:916–930PubMedCrossRefGoogle Scholar
  19. de Graaf BH, Cheung AY, Andreyeva T, Levasseur K, Kieliszewski M, Wu HM (2005) Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell 17:2564–2579PubMedPubMedCentralCrossRefGoogle Scholar
  20. De Marcos Lousa C, Gershlick DC, Denecke J (2012) Mechanisms and concepts paving the way towards a complete transport cycle of plant vacuolar sorting receptors. Plant Cell 24:1714–1732PubMedPubMedCentralCrossRefGoogle Scholar
  21. Di Sansebastiano GP (2013) Defining new SNARE functions: the i-SNARE”. Front Plant Sci 4:99PubMedPubMedCentralCrossRefGoogle Scholar
  22. Di Sansebastiano GP, Rizzello F, Durante M, Caretto S, Nisi R, De Paolis A, Faraco M, Montefusco A, Piro G, Mita G (2014) Subcellular compartmentalization in protoplastos from Artemisia annua cell cultures: engineering attempts using a modified SNARE protein. J Biotechnol 202:146–152PubMedCrossRefGoogle Scholar
  23. Duarte P, Pissarra J, Moore I (2008) Processing and trafficking of a single isoform of the aspartic proteinase cardosin A on the vacuolar pathway. Planta 227:1255–1268PubMedCrossRefGoogle Scholar
  24. Ebine K, Okatani Y, Uemura T, Goh T, Shoda K, Niihama M, Morita MT, Spitzer C, Otegui MS, Nakano A, Ueda T (2008) A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. Plant Cell 20:3006–3021PubMedPubMedCentralCrossRefGoogle Scholar
  25. Ebine K, Fujimoto M, Okatani Y, Nishiyama T, Goh T, Ito E, Dainobu T, Nishitani A, Uemura T, Sato MH, Thordal-Christensen H, Tsutsumi N, Nakano A, Ueda T (2011) A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat Cell Biol 13(7):U853–U859CrossRefGoogle Scholar
  26. Ebine K, Uemura T, Nakano A, Ueda T (2012) Flowering time modulation by a vacuolar SNARE via FLOWERING LOCUS C in Arabidopsis thaliana. PLoS One 7, e42239PubMedPubMedCentralCrossRefGoogle Scholar
  27. Ebine K, Inoue T, Ito J, Ito E, Uemura T, Goh T, Abe H, Sato K, Nakano A, Ueda T (2014) Plant vacuolar trafficking occurs through distinctly regulated pathways. Curr Biol 24:1375–1382PubMedCrossRefGoogle Scholar
  28. Elias M (2010) Patterns and processes in the evolution of the eukaryotic endomembrane system. Mol Membr Biol 27:469–489PubMedCrossRefGoogle Scholar
  29. Fasshauer D, Sutton RB, Brunger AT, Jahn R (1998) Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci U S A 95:15781–15786PubMedPubMedCentralCrossRefGoogle Scholar
  30. Floyd BE, Morriss SC, Macintosh GC, Bassham DC (2012) What to eat: evidence for selective autophagy in plants. J Integr Plant Biol 54:907–920PubMedGoogle Scholar
  31. Foresti O, Da Silva LL, Denecke J (2006) Overexpression of the Arabidopsis syntaxin PEP12/SYP21 inhibits transport from the prevacuolar compartment to the lytic vacuole in vivo. Plant Cell 18:2275–2293PubMedPubMedCentralCrossRefGoogle Scholar
  32. Fujimoto M, Ueda T (2012) Conserved and plant-unique mechanisms regulating plant post-Golgi traffic. Front Plant Sci 3(197):1–10Google Scholar
  33. Galili G, Altschuler Y, Levanony H (1993) Assembly and transport of seed storage proteins. Trends Cell Biol 3:437–442PubMedCrossRefGoogle Scholar
  34. Gillespie JE, Rogers SW, Deery M, Dupree P, Rogers JC (2005) A unique family of proteins associated with internalized membranes in protein storage vacuoles of the Brassicaceae. Plant J 41:429–441PubMedCrossRefGoogle Scholar
  35. Grosshans BL, Ortiz D, Novick P (2006) Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci U S A 103:11821–11827PubMedPubMedCentralCrossRefGoogle Scholar
  36. Gurkan C, Koulov AV, Balch WE (2007) An evolutionary perspective on eukaryotic membrane trafficking. Adv Exp Med Biol 607:73–83PubMedCrossRefGoogle Scholar
  37. Haas TJ, Sliwinski MK, Martinez DE, Preuss M, Ebine K, Ueda T, Nielsen E, Odorizzi G, Otegui MS (2007) The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 19:1295–1312PubMedPubMedCentralCrossRefGoogle Scholar
  38. Hara-Nishimura I, Shimada T, Hatano K, Takeuchi Y, Nishimura M (1998) Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles. Plant Cell 10:825–836PubMedPubMedCentralCrossRefGoogle Scholar
  39. Harley SM, Beevers L (1989) Coated vesicles are involved in the transport of storage proteins during seed development in Pisum sativum L. Plant Physiol 91:674–678PubMedPubMedCentralCrossRefGoogle Scholar
  40. Hashiguchi Y, Niihama M, Takahashi T, Saito C, Nakano A, Tasaka M, Morita MT (2010) Loss-of-function mutations of retromer large subunit genes suppress the phenotype of an Arabidopsis zig mutant that lacks Qb-SNARE VTI11. Plant Cell 22:159–172PubMedPubMedCentralCrossRefGoogle Scholar
  41. Herman EM (2008) Endoplasmic reticulum bodies: solving the insoluble. Curr Opin Plant Biol 11:672–679PubMedCrossRefGoogle Scholar
  42. Hillmer S, Movafeghi A, Robinson DG, Hinz G (2001) Vacuolar storage proteins are sorted in the cis-cisternae of the pea cotyledon Golgi apparatus. J Cell Biol 152:41–50PubMedPubMedCentralCrossRefGoogle Scholar
  43. Hinz G, Colanesi S, Hillmer S, Rogers JC, Robinson DG (2007) Localization of vacuolar transport receptors and cargo proteins in the Golgi apparatus of developing Arabidopsis embryos. Traffic 8:1452–1464PubMedCrossRefGoogle Scholar
  44. Hoflack B, Kornfeld S (1985) Lysosomal enzyme binding to mouse P388D1 macrophage membranes lacking the 215-kDa mannose 6-phosphate receptor: evidence for the existence of a second mannose 6-phosphate receptor. Proc Natl Acad Sci U S A 82:4428–4432PubMedPubMedCentralCrossRefGoogle Scholar
  45. Holkeri H, Vitale A (2001) Vacuolar sorting determinants within a plant storage protein trimer act cumulatively. Traffic 2:737–741PubMedCrossRefGoogle Scholar
  46. Holwerda BC, Padgett HS, Rogers JC (1992) Proaleurain vacuolar targeting is mediated by short contiguous peptide interactions. Plant Cell 4:307–318PubMedPubMedCentralCrossRefGoogle Scholar
  47. Ibl V, Stoger E (2011) The formation, function and fate of protein storage compartments in seeds. Protoplasma 249:379–392PubMedCrossRefGoogle Scholar
  48. Jiang L, Phillips TE, Rogers SW, Rogers JC (2000) Biogenesis of the protein storage vacuole crystalloid. J Cell Biol 150:755–769PubMedPubMedCentralCrossRefGoogle Scholar
  49. Jolliffe NA, Craddock CP, Frigerio L (2005) Pathways for protein transport to seed storage vacuoles. Biochem Soc Trans 33:1016–1018PubMedCrossRefGoogle Scholar
  50. 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 U S A 91:3403–3407PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kolodziejek I, Van Der Hoorn RA (2010) Mining the active proteome in plant science and biotechnology. Curr Opin Biotechnol 21:225–233PubMedCrossRefGoogle Scholar
  52. Kotzer AM, Brandizzi F, Neuman U, Paris N, More I, Hawes C (2004) AtRabF2b (Ara7) acts on the vacuolar trafficking pathway in tobacco leaf epidermal cells. J Cell Sci 117:6377–6389PubMedCrossRefGoogle Scholar
  53. Kriegel MA, Rathinam C, Flavell RA (2009) E3 ubiquitin ligase GRAIL controls primary T cell activation and oral tolerance. Proc Natl Acad Sci U S A 106:16770–16775PubMedPubMedCentralCrossRefGoogle Scholar
  54. Leshem Y, Golani Y, Kaye Y, Levine A (2010) Reduced expression of the v-SNAREs AtVAMP71/AtVAMP7C gene family in Arabidopsis reduces drought tolerance by suppression of abscisic acid-dependent stomatal closure. J Exp Bot 61:2615–2622PubMedPubMedCentralCrossRefGoogle Scholar
  55. Levanony H, Rubin R, Altschuler Y, Galili G (1992) Evidence for a novel route of wheat storage proteins to vacuoles. J Cell Biol 119:1117–1128PubMedCrossRefGoogle Scholar
  56. Li F, Vierstra RD (2012) Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17:526–537PubMedCrossRefGoogle Scholar
  57. Lipinski CA, Lombardo F, Dominy BW, Feeney PJ (1997) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 23:3–25CrossRefGoogle Scholar
  58. Lipka V, Kwon C, Panstruga R (2007) SNARE-ware: the role of SNARE-domain proteins in plant biology. Annu Rev Cell Dev Biol 23:147–174PubMedCrossRefGoogle Scholar
  59. Lu X, Zhang L, Zhang F, Jiang W, Shen Q, Zhang L, Lv Z, Wang G, Tang K (2013) AaORA, a trichome-specific AP2/ERF transcription factor of Artemisia annua, is a positive regulator in the artemisinin biosynthetic pathway and in disease resistance to Botrytis cinerea. New Phytol 198:1191–1202PubMedCrossRefGoogle Scholar
  60. Luini A (2011) A brief history of the cisternal progression-maturation model. Cell Logist 1:6–11PubMedPubMedCentralCrossRefGoogle Scholar
  61. Luo F, Fong YH, Zeng Y, Shen J, Jiang L, Wong K (2014) How vacuolar sorting receptor proteins interact with their cargo proteins: crystal structures of Apo and cargo-bound forms of the protease-associated domain from an Arabidopsis vacuolar sorting receptor. Plant Cell 26:3693–3708PubMedPubMedCentralCrossRefGoogle Scholar
  62. Lynch-Day MA, Klionsky DJ (2010) The Cvt pathway as a model for selective autophagy. FEBS Lett 584:1359–1366PubMedPubMedCentralCrossRefGoogle Scholar
  63. Maes L, Goossens A (2010) Hormone-mediated promotion of trichome initiation in plants is conserved but utilizes species and trichome-specific regulatory mechanisms. Plant Signal Behav 5:205–207PubMedPubMedCentralCrossRefGoogle Scholar
  64. Maeshima M, Haranishimura I, Takeuchi Y, Nishimura M (1994) Accumulation of vacuolar H+-pyrophosphatase and H+-ATPase during reformation of the central vacuole in germinating pumpkin seeds. Plant Physiol 106:61–69PubMedPubMedCentralCrossRefGoogle Scholar
  65. Matsuoka K, Nakamura K (1991) Propeptide of a precursor to a plant vacuolar protein required for vacuolar targeting. Proc Natl Acad Sci U S A 88:834–838PubMedPubMedCentralCrossRefGoogle Scholar
  66. Mazel A, Leshem Y, Tiwari BS, Levine A (2004) Induction of salt and osmotic stress tolerance by overexpression of an intracellular vesicle trafficking protein AtRab7 (AtRabG3e). Plant Physiol 134:118–128PubMedPubMedCentralCrossRefGoogle Scholar
  67. Michaeli S, Avin-Wittenberg T, Galili G (2014) Involvement of autophagy in the direct ER to vacuole protein trafficking route in plants. Front Plant Sci 5:134PubMedPubMedCentralCrossRefGoogle Scholar
  68. Morita MT, Kato T, Nagafusa K, Saito C, Ueda T, Nakano A, Tasaka M (2002) Involvement of the vacuoles of the endodermis in the early process of shot gravitropism in Arabidopsis. Plant Cell 14:47–56PubMedPubMedCentralCrossRefGoogle Scholar
  69. Murphy AS, Bandyopadhyay A, Holstein SE, Peer WA (2005) Endocytotic cycling of PM proteins. Annu Rev Plant Biol 56:221–251PubMedCrossRefGoogle Scholar
  70. Nafis T, Akmal M, Ram M, Alam P, Ahlawat S, Mohd A, Abdin MZ (2011) Enhancement of artemisinin content by constitutive expression of the HMG-CoA reductase gene in high-yielding strain of Artemisia annua L. Plant Biotechnol Rep 5:53–60CrossRefGoogle Scholar
  71. Nahm MY, Kim SW, Yun D, Lee SY, Cho MJ, Bahk JD (2003) Molecular and biochemical analyses of OsRAB7, a rice Rab7 homolog. Plant Cell Physiol 44:1341–1349PubMedCrossRefGoogle Scholar
  72. Nakamura K, Matsuoka K (1993) Protein targeting to the vacuole in plant cells. Plant Physiol 101:1–5PubMedPubMedCentralCrossRefGoogle Scholar
  73. Neuhaus JM, Rogers J (1998) Sorting of proteins to vacuoles in plant cells. Plant Mol Biol 38:127–144PubMedCrossRefGoogle Scholar
  74. Neuhaus JM, Sticher L, Meins F Jr, Boller T (1991) A short C-terminal sequence is necessary and sufficient for the targeting of chitinases to the plant vacuole. Proc Natl Acad Sci U S A 88:10362–10366PubMedPubMedCentralCrossRefGoogle Scholar
  75. Nishizawa K, Maruyama N, Utsumi S (2006) The C-terminal region of α’ subunit of soybean β-conglycinin contains two types of vacuolar sorting determinants. Plant Mol Biol 62:111–125PubMedCrossRefGoogle Scholar
  76. Ohtomo I, Ueda H, Shimada T, Nishiyama C, Komoto Y, Hara-Nishimura I, Takahashi T (2005) Identification of na allele of VAM3/SYP22 that confers a semi-dwarf phenotype in Arabidopsis thaliana. Plant Cell Physiol 46:1358–1365PubMedCrossRefGoogle Scholar
  77. Olbrich A, Hillmer S, Hinz G, Oliviusson P, Robinson DG (2007) Newly formed vacuoles in root meristems of barley and pea seedlings have characteristics of both protein storage and lytic vacuoles. Plant Physiol 145:1383–1394PubMedPubMedCentralCrossRefGoogle Scholar
  78. Paris N, Stanley CM, Jones RL, Rogers JC (1996) Plant cells contain two functionally distinct vacuolar compartments. Cell 85:563–572PubMedCrossRefGoogle Scholar
  79. Park M, Lee D, Lee G-J, Hwang I (2005) AtRMR1 functions as a cargo receptor for protein trafficking to the protein storage vacuole. J Cell Biol 170:757–767PubMedPubMedCentralCrossRefGoogle Scholar
  80. Park JH, Oufattole M, Rogers JC (2007) Golgi-mediated vacuolar sorting in plant cells: RMR proteins are sorting receptors for the protein aggregation/membrane internalization pathway. Plant Sci 172:728–745CrossRefGoogle Scholar
  81. Peng L, Xiang F, Roberts E, Kawagoe Y, Greve LC, Kreuz K, Delmer DP (2001) The experimental herbicide CGA 325’615 inhibits synthesis of crystalline cellulose and causes accumulation of non-crystalline beta-1,4-glucan associated with CesA protein. Plant Physiol 126:981–992PubMedPubMedCentralCrossRefGoogle Scholar
  82. Pereira C, Pereira S, Satiat-Jeunemaitre B, Pissarra J (2013) Cardosin A contains two vacuolar sorting signals using different vacuolar routes in tobacco epidermal cells. Plant J 76:87–100PubMedGoogle Scholar
  83. Pereira C, Pereira S, Pissarra J (2014) Delivering of proteins to the plant vacuole – an update. Int J Mol Sci 15:7611–7623PubMedPubMedCentralCrossRefGoogle Scholar
  84. Pompa A, de Marchis F, Vitale A, Arcioni S, Bellucci M (2010) An engineered C-terminal disulphide bond can partially replace the phaseolin vacuolar sorting signal. Plant J 61:782–791PubMedCrossRefGoogle Scholar
  85. Preuss ML, Serna J, Falbel TG, Bednarek SY, Nielsen E (2004) The Arabidopsis RabGTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16:1589–1603PubMedPubMedCentralCrossRefGoogle Scholar
  86. Ramalho-Santos M, Pissarra J, Veríssimo P, Pereira S, Salema R, Pires E, Faro CJ (1997) Cardosin A, na abundant aspartic proteinase, accumulates in protein storage vacuoles in the stigmatic papillae of Cynara cardunculus L. Planta 203:204–212PubMedCrossRefGoogle Scholar
  87. Rehman RU, Stigliano E, Lycett G, Sticher L, Franchesca S, Dalessandro G, Di Sansebastiano GP (2008) Tomato Rab11a characterization evidenced a difference between SYP121 dependent and SYP122-dependent exocytosis. Plant Cell Physiol 49(5):751–766PubMedCrossRefGoogle Scholar
  88. Robert S, Raikhel NV, Hicks GR (2009) Powerful partners: Arabidopsis and chemical genomics. Arabidopsis Book 7, e0109, http://doi.org/10.1199/tab.0109 PubMedPubMedCentralCrossRefGoogle Scholar
  89. Robinson DG, Oliviusson P, Hinz G (2005) Protein sorting to the storage vacuoles of plants: a critical appraisal. Traffic 6:615–625PubMedCrossRefGoogle Scholar
  90. Rosado A, Hicks GR, Norambuena L, Rogachev I, Meir S, Pourcel L, Zouhar J, Brown MQ, Boirsdore MP, Puckrin RS, Cutler SR, Rojo E, Aharoni A, Raikhel NV (2011) Sortin1-hypersensitive mutants link vacuolar-trafficking defects and flavonoid metabolism in Arabidopsis vegetative tissues. Chem Biol 18:187–197PubMedCrossRefGoogle Scholar
  91. Rutherford S, Moore I (2002) The Arabidopsis Rab GTPase family: another enigma variation. Curr Opin Plant Biol 5:518–528PubMedCrossRefGoogle Scholar
  92. Saito C, Ueda T (2009) Chapter 4: Functions of RAB and SNARE proteins in plant life. Int Rev Cell Mol Biol 274:183–233PubMedCrossRefGoogle Scholar
  93. Saito C, Uemura T, Awai C, Tominaga M, Ebine K, Ito J, Ueda T, Abe H, Morita MT, Tasaka M et al (2011) The occurrence of ‘bulbs’, a complex configuration of the vacuolar membrane, is affected by mutations of vacuolar SNARE and phospholipase in Arabidopsis. Plant J 68:64–73PubMedCrossRefGoogle Scholar
  94. Samaj J, Muller J, Beck M, Bohm N, Menzel D (2006) Vesicular trafficking, cytoskeleton and signalling in root hairs and pollen tubes. Trends Plant Sci 11:594–600PubMedCrossRefGoogle Scholar
  95. Sanderfoot A (2007) Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol 144:6–17PubMedPubMedCentralCrossRefGoogle Scholar
  96. Sanderfoot AA, Kovaleva V, Bassham DC, Raikhel NV (2001) Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell. Mol Biol Cell 12:3733–3743PubMedPubMedCentralCrossRefGoogle Scholar
  97. Sansebastiano GD, Piro G (2014) The SNARE proteins (in plants) beyond the Noble Prize. J Plant Biochem Physiol 2:2Google Scholar
  98. Scott SV, Hefner-Gravink A, Morano KA, Noda T, Ohsumi Y, Klionsky DJ (1996) Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc Natl Acad Sci U S A 93:12304–12308PubMedPubMedCentralCrossRefGoogle Scholar
  99. Serrano M, Kombrink E, Meesters C (2015) Considerations for designing chemical screening strategies in plant biology. Front Plant Sci 6:131PubMedPubMedCentralCrossRefGoogle Scholar
  100. 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 U S A 100:16095–16100PubMedPubMedCentralCrossRefGoogle Scholar
  101. Shinshi H, Wenzler H, Neuhaus JM, Felix G, Hofsteenge J, Meins F (1988) Evidence for N- and C-terminal processing of a plant defense-related enzyme: primary structure of tobacco prepro-beta-1,3-glucanase. Proc Natl Acad Sci U S A 85:5541–5545PubMedPubMedCentralCrossRefGoogle Scholar
  102. Shirakawa M, Ueda H, Shimada T, Nishiyama C, Hara-Nishimura I (2009) Vacuolar SNAREs function in the formation of the leaf vascuolar network by regulating auxin distribution. Plant Cell Physiol 50:1319–1328PubMedCrossRefGoogle Scholar
  103. Shirakawa M, Ueda H, Shimada T, Koumoto Y, Shimada TL, Kondo M, Takahashi T, Okuyama Y, Nishimura M, Hara-Nishimura I (2010) Arabidopsis Qa-SNARE SYP2 proteins localized to different subcellular regions function redundantly in vacuolar protein sorting and plant development. Plant J 64:924–935PubMedCrossRefGoogle Scholar
  104. Simões I, Faro C (2004) Structure and function of plant aspartic proteinases. Eur J Biochem 271:2067–2075PubMedCrossRefGoogle Scholar
  105. Stenmark H, Olkkonen VM (2001) The Rab GTPase family. Genome Biol 2, Reviews 3007. doi: 10.1186/gb-2001-2-5-reviews3007
  106. Suen PK, Shen J, Sun SSM, Jiang L (2010) Expression and characterization of two functional vacuolar sorting receptor (VSR) proteins, BP-80 and AtVSR4 from culture media of transgenic tobacco BY-2 cells. Plant Sci 179:68–76CrossRefGoogle Scholar
  107. Sutter JU, Campanoni P, Blatt MR, Paneque M (2006) Setting SNAREs in a different wood. Traffic 7:627–638PubMedCrossRefGoogle Scholar
  108. Szumlanski AL, Nielsen E (2009) The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana. Plant Cell 21:526–544PubMedPubMedCentralCrossRefGoogle Scholar
  109. Tang K, Shen Q, Yan T, Fu X (2014) Transgenic approach to increase artemisinin content in Artemisia annua L. Plant Cell Rep 33:605–615PubMedCrossRefGoogle Scholar
  110. Ueda T, Matsuda N, Anai T, Tsukaya H, Uchimiya H, 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 8:2079–2091PubMedPubMedCentralCrossRefGoogle Scholar
  111. Ueda T, Uemura T, Sato MH, Nakano A (2004) Functional differentiation of endosomes in Arabidopsis cells. Plant J 40:783–789PubMedCrossRefGoogle Scholar
  112. Ueda H, Nishiyama C, Shimada T, Koumoto Y, Hayashi Y, Kondo M, Takahashi T, Ohtomo I, Nishimura M, Hara-Nishimura I (2006) AtVAM3 is required for normal specification of idioblasts, myrosin cells. Plant Cell Physiol 47:164–175PubMedCrossRefGoogle Scholar
  113. Uemura T, Ueda T, Ohniwa RL, Nakano A, Takeyasu K, Sato MH (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct Funct 29:49–65PubMedCrossRefGoogle Scholar
  114. Uemura T, Sato MH, Takeyasu K (2005) The longin domain regulates subcellular targeting of VAMP7 in Arabidopsis thaliana. FEBS Lett 579:2842–2846PubMedCrossRefGoogle Scholar
  115. Uemura T, Morita MT, Ebine K, Okatani Y, Yano D, Saito C, Ueda T, Nakano A (2010) Vacuolar/pre-vacuolar compartment Qa-SNAREs VAM3/SYP22 and PEP12/SYP21 have interchangeable functions in Arabidopsis. Plant J 64:864–873PubMedCrossRefGoogle Scholar
  116. Vernoud V, Horton AC, Yang Z, Nielsen E (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 131:1191–1208PubMedPubMedCentralCrossRefGoogle Scholar
  117. Vieira M, Pissarra J, Veríssimo P, Castanheira P, Costa Y, Pires E, Faro C (2001) Molecular cloning and characterization of cDNA encoding cardosin B, na aspartic proteinase accumulating extracellularly in the transmitting tissue of Cynara cardunculus L. Plant Mol Biol 45:529–539PubMedCrossRefGoogle Scholar
  118. Viotti C, Bubeck J, Stierhof YD, Krebs M, Langhans M, van den Berg W, van Dongen W, Richter S, Geldener N, Takano J et al (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22:1344–1357PubMedPubMedCentralCrossRefGoogle Scholar
  119. Vitale A, Raikhel NV (1999) What do proteins need to reach different vacuoles? Trends Plant Sci 4:149–155PubMedCrossRefGoogle Scholar
  120. Voelker TA, Herman EM, Chrispeels MJ (1989) In vitro mutated phytohemagglutinin genes expressed in tobacco seeds: role of glycans in protein targeting and stability. Plant Cell 1:95–104PubMedPubMedCentralCrossRefGoogle Scholar
  121. Wang H, Rogers JC, Jiang L (2011) Plant RMR proteins: unique vacuolar sorting receptors that couple ligand sorting with membrane internalization. FEBS J 278:59–68PubMedCrossRefGoogle Scholar
  122. Wasternack C, Kombrink E (2010) Jasmonates: structural requirements for lipid-derived signals active in plant stress responses and development. ACS Chem Biol 5:63–77PubMedCrossRefGoogle Scholar
  123. 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 277:8708–8715PubMedCrossRefGoogle Scholar
  124. Watanabe E, Shimada T, Tamura K, Matsushima R, Koumoto Y, Nishimura M, Hara-Nishimura I (2004) An 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 45:9–17PubMedCrossRefGoogle Scholar
  125. Xiang L, Etxeberria E, van den Ende W (2013) Vacuolar protein sorting mechanisms in plants. FEBS J 280:979–993PubMedCrossRefGoogle Scholar
  126. Zerial M, McBride H (2001) Rab proteins as membrane organisers. Nat Rev Mol Cell Biol 2:107–117PubMedCrossRefGoogle Scholar
  127. Zhang C, Hicks GR, Raikhel NV (2014) Plant vacuole morphology and vacuolar trafficking. Front Plant Sci 5:476–485PubMedPubMedCentralGoogle Scholar
  128. Zouhar J, Rojo E (2009) Plant vacuoles: where did they come from and where are they heading? Curr Opin Plant Biol 12:677–684Google Scholar
  129. Zouhar J, Hicks GR, Raikhel NV (2004) Sorting inhibitors (Sortins): chemical compounds to study vacuolar sorting in Arabidopsis. Proc Natl Acad Sci U S A 101:9497–9501PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Faculty of Sciences, Department of BiologyBioISI – Biosystems & Integrative Sciences Institute, University of PortoPortoPortugal

Personalised recommendations