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Annual Review of Plant Biology

Volume 69, 2018

Plant Vacuoles

Abstract

Plant vacuoles are multifunctional organelles. On the one hand, most vegetative tissues develop lytic vacuoles that have a role in degradation. On the other hand, seed cells have two types of storage vacuoles: protein storage vacuoles (PSVs) in endosperm and embryonic cells and metabolite storage vacuoles in seed coats. Vacuolar proteins and metabolites are synthesized on the endoplasmic reticulum and then transported to the vacuoles via Golgi-dependent and Golgi-independent pathways. Proprotein precursors delivered to the vacuoles are converted into their respective mature forms by vacuolar processing enzyme, which also regulates various kinds of programmed cell death in plants. We summarize two types of vacuolar membrane dynamics that occur during defense responses: vacuolar membrane collapse to attack viral pathogens and fusion of vacuolar and plasma membranes to attack bacterial pathogens. We also describe the chemical defense against herbivores brought about by the presence of PSVs in the idioblast myrosin cell.

Keyword(s): Golgi-independent pathway, lytic vacuole, metabolite storage vacuole, protein storage vacuole, vacuolar defense, vacuolar processing enzyme, vacuolar sorting receptor, VPE, VSR
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/content/journals/10.1146/annurev-arplant-042817-040508
2018-04-29
2024-04-27
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Literature Cited

  1. Abrahams S, Tanner GJ, Larkin PJ, Ashton AR. 1.  2002. Identification and biochemical characterization of mutants in the proanthocyanidin pathway in Arabidopsis. Plant Physiol 130:561–76 [Google Scholar]
  2. Ahmed SU, Bar-Peled M, Raikhel NV. 2.  1997. Cloning and subcellular location of an Arabidopsis receptor-like protein that shares common features with protein-sorting receptors of eukaryotic cells. Plant Physiol 114:325–36 [Google Scholar]
  3. An Y, Chen CY, Moyer B, Rotkiewicz P, Elsliger MA. 3.  et al. 2009. Structural and functional analysis of the globular head domain of p115 provides insight into membrane tethering. J. Mol. Biol. 391:26–41 [Google Scholar]
  4. Andreasson E, Bolt Jorgensen L, Hoglund AS, Rask L, Meijer J. 4.  2001. Different myrosinase and idioblast distribution in Arabidopsis and Brassicanapus. Plant Physiol 127:1750–63 [Google Scholar]
  5. Appelhagen I, Nordholt N, Seidel T, Spelt K, Koes R. 5.  et al. 2015. TRANSPARENT TESTA 13 is a tonoplast P3A-ATPase required for vacuolar deposition of proanthocyanidins in Arabidopsis thaliana seeds. Plant J 82:840–49 [Google Scholar]
  6. Barlowe CK, Miller EA. 6.  2013. Secretory protein biogenesis and traffic in the early secretory pathway. Genetics 193:383–410 [Google Scholar]
  7. Barth C, Jander G. 7.  2006. Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense. Plant J 46:549–62 [Google Scholar]
  8. Baxter IR, Young JC, Armstrong G, Foster N, Bogenschutz N. 8.  et al. 2005. A plasma membrane H+-ATPase is required for the formation of proanthocyanidins in the seed coat endothelium of Arabidopsis thaliana. PNAS 102:2649–54 [Google Scholar]
  9. Becher B, Hoef-Emden K. 9.  2009. Evolution of vacuolar targeting in algae. Bot. Mar. 52:117–28 [Google Scholar]
  10. Bi X, Corpina RA, Goldberg J. 10.  2002. Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat. Nature 419:271–77 [Google Scholar]
  11. Bi X, Mancias JD, Goldberg J. 11.  2007. Insights into COPII coat nucleation from the structure of Sec23.Sar1 complexed with the active fragment of Sec31. Dev. Cell 13:635–45 [Google Scholar]
  12. Brandizzi F.12.  2017. Transport from the endoplasmic reticulum to the Golgi in plants: Where are we now?. Semin. Cell Dev. Biol. In press
  13. Brandizzi F, Snapp EL, Roberts AG, Lippincott-Schwartz J, Hawes C. 13.  2002. Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching. Plant Cell 141293–309
  14. Bui QT, Golinelli-Cohen MP, Jackson CL. 14.  2009. Large Arf1 guanine nucleotide exchange factors: evolution, domain structure, and roles in membrane trafficking and human disease. Mol. Genet. Genom. 282:329–50 [Google Scholar]
  15. Cai H, Yu S, Menon S, Cai Y, Lazarova D. 15.  et al. 2007. TRAPPI tethers COPII vesicles by binding the coat subunit Sec23. Nature 445:941–44 [Google Scholar]
  16. Cao X, Rogers SW, Butler J, Beevers L, Rogers JC. 16.  2000. Structural requirements for ligand binding by a probable plant vacuolar sorting receptor. Plant Cell 12:493–506 [Google Scholar]
  17. Chan CB, Abe M, Hashimoto N, Hao C, Williams IR. 17.  et al. 2009. Mice lacking asparaginyl endopeptidase develop disorders resembling hemophagocytic syndrome. PNAS 106:468–73 [Google Scholar]
  18. Chanoca A, Kovinich N, Burkel B, Stecha S, Bohorquez-Restrepo A. 18.  et al. 2015. Anthocyanin vacuolar inclusions form by a microautophagy mechanism. Plant Cell 27:2545–59 [Google Scholar]
  19. daSilva LL, Foresti O, Denecke J. 19.  2006. Targeting of the plant vacuolar sorting receptor BP80 is dependent on multiple sorting signals in the cytosolic tail. Plant Cell 18:1477–97 [Google Scholar]
  20. daSilva LL, Snapp EL, Denecke J, Lippincott-Schwartz J, Hawes C, Brandizzi F. 20.  2004. Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell 16:1753–71 [Google Scholar]
  21. De Marchis F, Bellucci M, Pompa A. 21.  2013. Traffic of human α-mannosidase in plant cells suggests the presence of a new endoplasmic reticulum-to-vacuole pathway without involving the Golgi complex. Plant Physiol 161:1769–82 [Google Scholar]
  22. De Marcos Lousa C, Gershlick DC, Denecke J. 22.  2012. Mechanisms and concepts paving the way towards a complete transport cycle of plant vacuolar sorting receptors. Plant Cell 24:1714–32 [Google Scholar]
  23. Debeaujon I, Peeters AJ, Leon-Kloosterziel KM, Koornneef M. 23.  2001. The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell 13:853–71 [Google Scholar]
  24. Edger PP, Heidel-Fischer HM, Bekaert M, Rota J, Glockner G. 24.  et al. 2015. The butterfly plant arms-race escalated by gene and genome duplications. PNAS 112:8362–66 [Google Scholar]
  25. Fan J, Crooks C, Creissen G, Hill L, Fairhurst S. 25.  et al. 2011. Pseudomonas sax genes overcome aliphatic isothiocyanate-mediated non-host resistance in Arabidopsis. Science 331:1185–88 [Google Scholar]
  26. Faraco M, Spelt C, Bliek M, Verweij W, Hoshino A. 26.  et al. 2014. Hyperacidification of vacuoles by the combined action of two different P-ATPases in the tonoplast determines flower color. Cell Rep 6:32–43 [Google Scholar]
  27. Foresti O, Gershlick DC, Bottanelli F, Hummel E, Hawes C, Denecke J. 27.  2010. A recycling-defective vacuolar sorting receptor reveals an intermediate compartment situated between prevacuoles and vacuoles in tobacco. Plant Cell 22:3992–4008 [Google Scholar]
  28. Foster AS.28.  1956. Plant idioblasts: remarkable examples of cell specialization. Protoplasma 46:184–93 [Google Scholar]
  29. Francisco RM, Regalado A, Ageorges A, Burla BJ, Bassin B. 29.  et al. 2013. ABCC1, an ATP binding cassette protein from grape berry, transports anthocyanidin 3-O-glucosides. Plant Cell 25:1840–54 [Google Scholar]
  30. Fuji K, Shimada T, Takahashi H, Tamura K, Koumoto Y. 30.  et al. 2007. Arabidopsis vacuolar sorting mutants (green fluorescent seed) can be identified efficiently by secretion of vacuole-targeted green fluorescent protein in their seeds. Plant Cell 19:597–609 [Google Scholar]
  31. Fuji K, Shirakawa M, Shimono Y, Kunieda T, Fukao Y. 31.  et al. 2016. The adaptor complex AP-4 regulates vacuolar protein sorting at the trans-Golgi network by interacting with VACUOLAR SORTING RECEPTOR1. Plant Physiol 170:211–19 [Google Scholar]
  32. Fukuda H.32.  1996. Xylogenesis: initiation, progression, and cell death. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:299–325 [Google Scholar]
  33. Gershlick DC, de Marcos Lousa C, Foresti O, Lee AJ, Pereira EA. 33.  et al. 2014. Golgi-dependent transport of vacuolar sorting receptors is regulated by COPII, AP1, and AP4 protein complexes in tobacco. Plant Cell 26:1308–29 [Google Scholar]
  34. Gomez C, Conejero G, Torregrosa L, Cheynier V, Terrier N, Ageorges A. 34.  2011. In vivo grapevine anthocyanin transport involves vesicle-mediated trafficking and the contribution of anthoMATE transporters and GST. Plant J 67:960–70 [Google Scholar]
  35. Goodman CD, Casati P, Walbot V. 35.  2004. A multidrug resistance-associated protein involved in anthocyanin transport in Zeamays. Plant Cell 16:1812–26 [Google Scholar]
  36. Grotewold E.36.  2006. The genetics and biochemistry of floral pigments. Annu. Rev. Plant Biol. 57:761–80 [Google Scholar]
  37. Grubb CD, Abel S. 37.  2006. Glucosinolate metabolism and its control. Trends Plant Sci 11:89–100 [Google Scholar]
  38. Halkier BA, Gershenzon J. 38.  2006. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57:303–33 [Google Scholar]
  39. Hara-Nishimura I.39.  2012. Plant legumain, asparaginyl endopeptidase, vacuolar processing enzyme. Handbook of Proteolytic Enzymes AJ Barrett, ND Rawlings, JF Woessner 2314–20 Cambridge, MA: Academic. , 3rd ed.. [Google Scholar]
  40. Hara-Nishimura I, Hatsugai N. 40.  2011. The role of vacuole in plant cell death. Cell Death Differ 18:1298–304 [Google Scholar]
  41. Hara-Nishimura I, Hatsugai N, Kuroyanagi M, Nakaune S, Nishimura M. 41.  2005. Vacuolar processing enzyme: an executor of plant cell death. Curr. Opin. Plant Biol. 8:404–8 [Google Scholar]
  42. Hara-Nishimura I, Inoue K, Nishimura M. 42.  1991. A unique vacuolar processing enzyme responsible for conversion of several proprotein precursors into the mature forms. FEBS Lett 294:89–93 [Google Scholar]
  43. Hara-Nishimura I, Nishimura M. 43.  1987. Proglobulin processing enzyme in vacuoles isolated from developing pumpkin cotyledons. Plant Physiol 85:440–45 [Google Scholar]
  44. Hara-Nishimura I, Nishimura M, Akazawa T. 44.  1985. Biosynthesis and intracellular transport of 11S globulin in developing pumpkin cotyledons. Plant Physiol 77:747–52 [Google Scholar]
  45. Hara-Nishimura I, Shimada T, Hatano K, Takeuchi Y, Nishimura M. 45.  1998. Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles. Plant Cell 10:825–36 [Google Scholar]
  46. Hara-Nishimura I, Takeuchi Y, Nishimura M. 46.  1993. Molecular characterization of a vacuolar processing enzyme related to a putative cysteine proteinase of Schistosomamansoni. Plant Cell 5:1651–59 [Google Scholar]
  47. Harborne JB, Williams CA. 47.  2000. Advances in flavonoid research since 1992. Phytochemistry 55:481–504 [Google Scholar]
  48. Hatsugai N, Hara-Nishimura I. 48.  2010. Two vacuole-mediated defense strategies in plants. Plant Signal. Behav. 5:1568–70 [Google Scholar]
  49. Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K. 49.  et al. 2009. A novel membrane-fusion-mediated plant immunity against bacterial pathogens. Gene. Dev. 23:2496–506 [Google Scholar]
  50. Hatsugai N, Kuroyanagi M, Nishimura M, Hara-Nishimura I. 50.  2006. A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis 11:905–11 [Google Scholar]
  51. Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S. 51.  et al. 2004. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305:855–58 [Google Scholar]
  52. Hatsugai N, Nakatsuji A, Unten O, Ogasawara K, Kondo M. 52.  et al. 2017. Involvement of Adapter Protein Complex 4 in hypersensitive cell death induced by avirulent bacteria. Plant Physiol 176:1824–34 [Google Scholar]
  53. Hatsugai N, Yamada K, Goto-Yamada S, Hara-Nishimura I. 53.  2015. Vacuolar processing enzyme in plant programmed cell death. Front. Plant Sci. 6:234 [Google Scholar]
  54. Hohl I, Robinson DG, Chrispeels MJ, Hinz G. 54.  1996. Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat. J. Cell Sci. 109:2539–50 [Google Scholar]
  55. Honig A, Avin-Wittenberg T, Ufaz S, Galili G. 55.  2012. A new type of compartment, defined by plant-specific Atg8-interacting proteins, is induced upon exposure of Arabidopsis plants to carbon starvation. Plant Cell 24:288–303 [Google Scholar]
  56. Hopkins RJ, van Dam NM, van Loon JJ. 56.  2009. Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu. Rev. Entomol. 54:57–83 [Google Scholar]
  57. Hsieh K, Huang AH. 57.  2007. Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum-derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell 19:582–96 [Google Scholar]
  58. Husebye H, Chadchawan S, Winge P, Thangstad OP, Bones AM. 58.  2002. Guard cell- and phloem idioblast-specific expression of thioglucoside glucohydrolase 1 (myrosinase) in Arabidopsis. Plant Physiol 128:1180–88 [Google Scholar]
  59. Ichino T, Fuji K, Ueda H, Takahashi H, Koumoto Y. 59.  et al. 2014. GFS9/TT9 contributes to intracellular membrane trafficking and flavonoid accumulation in Arabidopsis thaliana. Plant J 80:410–23 [Google Scholar]
  60. Islam MM, Tani C, Watanabe-Sugimoto M, Uraji M, Jahan MS. 60.  et al. 2009. Myrosinases, TGG1 and TGG2, redundantly function in ABA and MeJA signaling in Arabidopsis guard cells. Plant Cell Physiol 50:1171–75 [Google Scholar]
  61. Ito Y, Uemura T, Nakano A. 61.  2014. Formation and maintenance of the Golgi apparatus in plant cells. Int. Rev. Cell Mol. Biol. 310:221–87 [Google Scholar]
  62. Ito Y, Uemura T, Shoda K, Fujimoto M, Ueda T, Nakano A. 62.  2012. cis-Golgi proteins accumulate near the ER exit sites and act as the scaffold for Golgi regeneration after brefeldin A treatment in tobacco BY-2 cells. Mol. Biol. Cell 23:3203–14 [Google Scholar]
  63. Kanaoka MM, Pillitteri LJ, Fujii H, Yoshida Y, Bogenschutz NL. 63.  et al. 2008. SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell 20:1775–85 [Google Scholar]
  64. Kang BH, Staehelin LA. 64.  2008. ER-to-Golgi transport by COPII vesicles in Arabidopsis involves a ribosome-excluding scaffold that is transferred with the vesicles to the Golgi matrix. Protoplasma 234:51–64 [Google Scholar]
  65. Kang H, Hwang I. 65.  2014. Vacuolar sorting receptor-mediated trafficking of soluble vacuolar proteins in plant cells. Plants 3:392–408 [Google Scholar]
  66. Kang H, Kim SY, Song K, Sohn EJ, Lee Y. 66.  et al. 2012. Trafficking of vacuolar proteins: the crucial role of Arabidopsis vacuolar protein sorting 29 in recycling vacuolar sorting receptor. Plant Cell 24:5058–73 [Google Scholar]
  67. Kim H, Kang H, Jang M, Chang JH, Miao Y. 67.  et al. 2010. Homomeric interaction of AtVSR1 is essential for its function as a vacuolar sorting receptor. Plant Physiol 154:134–48 [Google Scholar]
  68. Kinoshita T, Yamada K, Hiraiwa N, Kondo M, Nishimura M, Hara-Nishimura I. 68.  1999. Vacuolar processing enzyme is up-regulated in the lytic vacuoles of vegetative tissues during senescence and under various stressed conditions. Plant J 19:43–53 [Google Scholar]
  69. Kissen R, Rossiter JT, Bones AM. 69.  2009. The ‘mustard oil bomb’: not so easy to assemble?! Localization, expression and distribution of the components of the myrosinase enzyme system. Phytochem. Rev. 8:69–86 [Google Scholar]
  70. Koornneef M.70.  1990. Mutations affecting the testa colour in Arabidopsis. Arabidopsis Inf. Serv. 27:1–4 [Google Scholar]
  71. Koroleva OA, Davies A, Deeken R, Thorpe MR, Tomos AD, Hedrich R. 71.  2000. Identification of a new glucosinolate-rich cell type in Arabidopsis flower stalk. Plant Physiol 124:599–608 [Google Scholar]
  72. Kulich I, Pecenkova T, Sekeres J, Smetana O, Fendrych M. 72.  et al. 2013. Arabidopsis exocyst subcomplex containing subunit EXO70B1 is involved in autophagy-related transport to the vacuole. Traffic 14:1155–65 [Google Scholar]
  73. Künzl F, Früholz S, Fäßler F, Li B, Pimpl P. 73.  2016. Receptor-mediated sorting of soluble vacuolar proteins ends at the trans-Golgi network/early endosome. Nat. Plants 2:16017 [Google Scholar]
  74. Kurokawa K, Okamoto M, Nakano A. 74.  2014. Contact of cis-Golgi with ER exit sites executes cargo capture and delivery from the ER. Nat. Commun. 5:3653 [Google Scholar]
  75. Kuroyanagi M, Nishimura M, Hara-Nishimura I. 75.  2002. Activation of Arabidopsis vacuolar processing enzyme by self-catalytic removal of an auto-inhibitory domain of the C-terminal propeptide. Plant Cell Physiol 43:143–51 [Google Scholar]
  76. Kuroyanagi M, Yamada K, Hatsugai N, Kondo M, Nishimura M, Hara-Nishimura I. 76.  2005. Vacuolar processing enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana. J. Biol. Chem 280:32914–20 [Google Scholar]
  77. Langhans M, Marcote MJ, Pimpl P, Virgili-Lopez G, Robinson DG, Aniento F. 77.  2008. In vivo trafficking and localization of p24 proteins in plant cells. Traffic 9:770–85 [Google Scholar]
  78. Lepiniec L, Debeaujon I, Routaboul JM, Baudry A, Pourcel L. 78.  et al. 2006. Genetics and biochemistry of seed flavonoids. Annu. Rev. Plant Biol. 57:405–30 [Google Scholar]
  79. Levanony H, Rubin R, Altschuler Y, Galili G. 79.  1992. Evidence for a novel route of wheat storage proteins to vacuoles. J. Cell Biol. 119:1117–28 [Google Scholar]
  80. Li L, Shimada T, Takahashi H, Koumoto Y, Shirakawa M. 80.  et al. 2013. MAG2 and three MAG2-INTERACTING PROTEINs form an ER-localized complex to facilitate storage protein transport in Arabidopsis thaliana. Plant J 76:781–91 [Google Scholar]
  81. Li L, Shimada T, Takahashi H, Ueda H, Fukao Y. 81.  et al. 2006. MAIGO2 is involved in exit of seed storage proteins from the endoplasmic reticulum in Arabidopsis thaliana. Plant Cell 18:3535–47 [Google Scholar]
  82. Li M, Sack FD. 82.  2014. Myrosin idioblast cell fate and development are regulated by the Arabidopsis transcription factor FAMA, the auxin pathway, and vesicular trafficking. Plant Cell 26:4053–66 [Google Scholar]
  83. Liu Y, Burgos JS, Deng Y, Srivastava R, Howell SH, Bassham DC. 83.  2012. Degradation of the endoplasmic reticulum by autophagy during endoplasmic reticulum stress in Arabidopsis. Plant Cell 24:4635–51 [Google Scholar]
  84. Liu Z, Jang S-W, Liu X, Cheng D, Peng J. 84.  et al. 2008. Neuroprotective actions of PIKE-L by inhibition of SET proteolytic degradation by asparagine endopeptidase. Mol. Cell 29:665–78 [Google Scholar]
  85. Lord C, Ferro-Novick S, Miller EA. 85.  2013. The highly conserved COPII coat complex sorts cargo from the endoplasmic reticulum and targets it to the Golgi. Cold Spring Harb. Perspect. Biol. 5:a013367 [Google Scholar]
  86. Luo F, Fong YH, Zeng Y, Shen J, Jiang L, Wong KB. 86.  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 26:3693–708 [Google Scholar]
  87. Maehr R, Hang HC, Mintern JD, Kim Y-M, Culvillier A. 87.  et al. 2005. Asparagine endopeptidase is not essential for class II MHC antigen presentation but is required for processing of cathepsin L in murine primary antigen presenting cells. J. Immunol. 174:7066–74 [Google Scholar]
  88. Marinova K, Pourcel L, Weder B, Schwarz M, Barron D. 88.  et al. 2007. The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 19:2023–38 [Google Scholar]
  89. Michaeli S, Avin-Wittenberg T, Galili G. 89.  2014. Involvement of autophagy in the direct ER to vacuole protein trafficking route in plants. Front. Plant Sci. 5:134 [Google Scholar]
  90. Miller EA, Beilharz TH, Malkus PN, Lee MC, Hamamoto S. 90.  et al. 2003. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114:497–509 [Google Scholar]
  91. Mori T, Maruyama N, Nishizawa K, Higasa T, Yagasaki K. 91.  et al. 2004. The composition of newly synthesized proteins in the endoplasmic reticulum determines the transport pathways of soybean seed storage proteins. Plant J 40:238–49 [Google Scholar]
  92. Morita Y, Araki H, Sugimoto T, Takeuchi K, Yamane T. 92.  et al. 2007. Legumain/asparaginyl endopeptidase controls extracellular matrix remodeling through the degradation of fibronectin in mouse renal proximal tubular cells. FEBS Lett 581:1417–24 [Google Scholar]
  93. Nakaune S, Yamada K, Kondo M, Kato T, Tabata S. 93.  et al. 2005. A vacuolar processing enzyme, δVPE, is involved in seed coat formation at the early stage of seed development. Plant Cell 17:876–87 [Google Scholar]
  94. Nebenfuhr A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM. 94.  et al. 1999. Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121:1127–42 [Google Scholar]
  95. Ohashi-Ito K, Bergmann DC. 95.  2006. Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell 18:2493–505 [Google Scholar]
  96. Paris N, Rogers SW, Jiang L, Kirsch T, Beevers L. 96.  et al. 1997. Molecular cloning and further characterization of a probable plant vacuolar sorting receptor. Plant Physiol 115:29–39 [Google Scholar]
  97. Pereira C, Pereira S, Satiat-Jeunemaitre B, Pissarra J. 97.  2013. Cardosin A contains two vacuolar sorting signals using different vacuolar routes in tobacco epidermal cells. Plant J 76:87–100 [Google Scholar]
  98. Pinheiro H, Samalova M, Geldner N, Chory J, Martinez A, Moore I. 98.  2009. Genetic evidence that the higher plant Rab-D1 and Rab-D2 GTPases exhibit distinct but overlapping interactions in the early secretory pathway. J. Cell Sci. 122:3749–58 [Google Scholar]
  99. Pourcel L, Irani NG, Lu Y, Riedl K, Schwartz S, Grotewold E. 99.  2010. The formation of anthocyanic vacuolar inclusions in Arabidopsis thaliana and implications for the sequestration of anthocyanin pigments. Mol. Plant 3:78–90 [Google Scholar]
  100. Pourcher M, Santambrogio M, Thazar N, Thierry AM, Fobis-Loisy I. 100.  et al. 2010. Analyses of sorting nexins reveal distinct retromer-subcomplex functions in development and protein sorting in Arabidopsis thaliana. Plant Cell 22:3980–91 [Google Scholar]
  101. Poustka F, Irani NG, Feller A, Lu Y, Pourcel L. 101.  et al. 2007. A trafficking pathway for anthocyanins overlaps with the endoplasmic reticulum-to-vacuole protein-sorting route in Arabidopsis and contributes to the formation of vacuolar inclusions. Plant Physiol 145:1323–35 [Google Scholar]
  102. Rask L, Andreasson E, Ekbom B, Eriksson S, Pontoppidan B, Meijer J. 102.  2000. Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol. Biol. 42:93–113 [Google Scholar]
  103. Ratzka A, Vogel H, Kliebenstein DJ, Mitchell-Olds T, Kroymann J. 103.  2002. Disarming the mustard oil bomb. PNAS 99:11223–28 [Google Scholar]
  104. Ren Y, Yip CK, Tripathi A, Huie D, Jeffrey PD. 104.  et al. 2009. A structure-based mechanism for vesicle capture by the multisubunit tethering complex Dsl1. Cell 139:1119–29 [Google Scholar]
  105. Rizo J, Sudhof TC. 105.  2012. The membrane fusion enigma: SNAREs, Sec1/Munc18 proteins, and their accomplices—guilty as charged?. Annu. Rev. Cell Dev. Biol. 28:279–308 [Google Scholar]
  106. Robinson DG, Herranz MC, Bubeck J, Pepperkok R, Ritzenthaler C. 106.  2007. Membrane dynamics in the early secretory pathway. Crit. Rev. Plant Sci. 26:199–225 [Google Scholar]
  107. Robinson DG, Neuhaus JM. 107.  2016. Receptor-mediated sorting of soluble vacuolar proteins: myths, facts, and a new model. J. Exp. Bot. 67:4435–49 [Google Scholar]
  108. Robinson DG, Pimpl P. 108.  2014. Receptor-mediated transport of vacuolar proteins: a critical analysis and a new model. Protoplasma 251:247–64 [Google Scholar]
  109. Rosado A, Hicks GR, Norambuena L, Rogachev I, Meir S. 109.  et al. 2011. Sortin1-hypersensitive mutants link vacuolar-trafficking defects and flavonoid metabolism in Arabidopsis vegetative tissues. Chem. Biol. 18:187–97 [Google Scholar]
  110. Shahriari M, Hulskamp M, Schellmann S. 110.  2010. Seeds of Arabidopsis plants expressing dominant-negative AtSKD1 under control of the GL2 promoter show a transparenttesta phenotype and a mucilage defect. Plant Signal. Behav. 5:1308–10 [Google Scholar]
  111. Shahriari M, Keshavaiah C, Scheuring D, Sabovljevic A, Pimpl P. 111.  et al. 2010. The AAA-type ATPase AtSKD1 contributes to vacuolar maintenance of Arabidopsis thaliana. Plant J 64:71–85 [Google Scholar]
  112. Shen J, Ding Y, Gao C, Rojo E, Jiang L. 112.  2014. N-linked glycosylation of AtVSR1 is important for vacuolar protein sorting in Arabidopsis. Plant J 80:977–92 [Google Scholar]
  113. Shimada T, Fuji K, Tamura K, Kondo M, Nishimura M, Hara-Nishimura I. 113.  2003. Vacuolar sorting receptor for seed storage proteins in Arabidopsis thaliana. PNAS 100:16095–100 [Google Scholar]
  114. Shimada T, Koumoto Y, Li L, Yamazaki M, Kondo M. 114.  et al. 2006. AtVPS29, a putative component of a retromer complex, is required for the efficient sorting of seed storage proteins. Plant Cell Physiol 47:1187–94 [Google Scholar]
  115. Shimada T, Kuroyanagi M, Nishimura M, Hara-Nishimura I. 115.  1997. A pumpkin 72-kDa membrane protein of precursor-accumulating vesicles has characteristics of a vacuolar sorting receptor. Plant Cell Physiol 38:1414–20 [Google Scholar]
  116. Shimada T, Watanabe E, Tamura K, Hayashi Y, Nishimura M, Hara-Nishimura I. 116.  2002. A vacuolar sorting receptor PV72 on the membrane of vesicles that accumulate precursors of seed storage proteins (PAC vesicles). Plant Cell Physiol 43:1086–95 [Google Scholar]
  117. Shimada T, Yamada K, Kataoka M, Nakaune S, Koumoto Y. 117.  et al. 2003. Vacuolar processing enzymes are essential for proper processing of seed storage proteins in Arabidopsis thaliana. J. Biol. Chem 278:32292–99 [Google Scholar]
  118. Shirahama-Noda K, Yamamoto A, Sugihara K, Hashimoto N, Asano M. 118.  et al. 2003. Biosynthetic processing of cathepsins and lysosomal degradation are abolished in asparaginyl endopeptidase-deficient mice. J. Biol. Chem. 278:33194–99 [Google Scholar]
  119. Shirakawa M, Ueda H, Koumoto Y, Fuji K, Nishiyama C. 119.  et al. 2014. CONTINUOUS VASCULAR RING (COV1) is a trans-Golgi network-localized membrane protein required for Golgi morphology and vacuolar protein sorting. Plant Cell Physiol 55:764–72 [Google Scholar]
  120. Shirakawa M, Ueda H, Nagano AJ, Shimada T, Kohchi T, Hara-Nishimura I. 120.  2014. FAMA is an essential component for the differentiation of two distinct cell types, myrosin cells and guard cells, in Arabidopsis. Plant Cell 26:4039–52 [Google Scholar]
  121. Shirakawa M, Ueda H, Shimada T, Hara-Nishimura I. 121.  2016. Myrosin cells are differentiated directly from ground meristem cells and are developmentally independent of the vasculature in Arabidopsis leaves. Plant Signal. Behav. 11:e1150403 [Google Scholar]
  122. Shirakawa M, Ueda H, Shimada T, Kohchi T, Hara-Nishimura I. 122.  2014. Myrosin cell development is regulated by endocytosis machinery and PIN1 polarity in leaf primordia of Arabidopsis thaliana. Plant Cell 26:4448–61 [Google Scholar]
  123. Shirakawa M, Ueda H, Shimada T, Koumoto Y, Shimada TL. 123.  et al. 2010. Arabidopsis Qa-SNARE SYP2 proteins localized to different subcellular regions function redundantly in vacuolar protein sorting and plant development. Plant J 64:924–35 [Google Scholar]
  124. Shirakawa M, Ueda H, Shimada T, Nishiyama C, Hara-Nishimura I. 124.  2009. Vacuolar SNAREs function in the formation of the leaf vascular network by regulating auxin distribution. Plant Cell Physiol 50:1319–28 [Google Scholar]
  125. Shroff R, Vergara F, Muck A, Svatos A, Gershenzon J. 125.  2008. Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. PNAS 105:6196–201 [Google Scholar]
  126. Szul T, Sztul E. 126.  2011. COPII and COPI traffic at the ER-Golgi interface. Physiology 26:348–64 [Google Scholar]
  127. Takagi J, Renna L, Takahashi H, Koumoto Y, Tamura K. 127.  et al. 2013. MAIGO5 functions in protein export from Golgi-associated endoplasmic reticulum exit sites in Arabidopsis. Plant Cell 25:4658–75 [Google Scholar]
  128. Takahashi H, Saito Y, Kitagawa T, Morita S, Masumura T, Tanaka K. 128.  2005. A novel vesicle derived directly from endoplasmic reticulum is involved in the transport of vacuolar storage proteins in rice endosperm. Plant Cell Physiol 46:245–49 [Google Scholar]
  129. Takahashi H, Tamura K, Takagi J, Koumoto Y, Hara-Nishimura I, Shimada T. 129.  2010. MAG4/Atp115 is a Golgi-localized tethering factor that mediates efficient anterograde transport in Arabidopsis. Plant Cell Physiol 51:1777–87 [Google Scholar]
  130. Takeuchi M, Ueda T, Sato K, Abe H, Nagata T, Nakano A. 130.  2000. A dominant negative mutant of Sar1 GTPase inhibits protein transport from the endoplasmic reticulum to the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J 23:517–25 [Google Scholar]
  131. Takeuchi M, Ueda T, Yahara N, Nakano A. 131.  2002. Arf1 GTPase plays roles in the protein traffic between the endoplasmic reticulum and the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J 31:499–515 [Google Scholar]
  132. Taylor LP, Grotewold E. 132.  2005. Flavonoids as developmental regulators. Curr. Opin. Plant Biol. 8:317–23 [Google Scholar]
  133. Teh OK, Moore I. 133.  2007. An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 448:493–96 [Google Scholar]
  134. Ueda H, Nishiyama C, Shimada T, Koumoto Y, Hayashi Y. 134.  et al. 2006. AtVAM3 is required for normal specification of idioblasts, myrosin cells. Plant Cell Physiol 47:164–75 [Google Scholar]
  135. Verweij W, Spelt C, Di Sansebastiano GP, Vermeer J, Reale L. 135.  et al. 2008. An H+ P-ATPase on the tonoplast determines vacuolar pH and flower colour. Nat. Cell Biol. 10:1456–62 [Google Scholar]
  136. Wang T, Grabski R, Sztul E, Hay JC. 136.  2015. p115-SNARE interactions: a dynamic cycle of p115 binding monomeric SNARE motifs and releasing assembled bundles. Traffic 16:148–71 [Google Scholar]
  137. Watanabe E, Shimada T, Kuroyanagi M, Nishimura M, Hara-Nishimura I. 137.  2002. Calcium-mediated association of a putative vacuolar sorting receptor PV72 with a propeptide of 2S albumin. J. Biol. Chem. 277:8708–15 [Google Scholar]
  138. Watanabe E, Shimada T, Tamura K, Matsushima R, Koumoto Y. 138.  et al. 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 45:9–17 [Google Scholar]
  139. Winkel BS.139.  2004. Metabolic channeling in plants. Annu. Rev. Plant Biol. 55:85–107 [Google Scholar]
  140. Wittstock U, Halkier BA. 140.  2002. Glucosinolate research in the Arabidopsis era. Trends Plant Sci 7:263–70 [Google Scholar]
  141. Yamada K, Shimada T, Kondo M, Nishimura M, Hara-Nishimura I. 141.  1999. Multiple functional proteins are produced by cleaving Asn-Gln bonds of a single precursor by vacuolar processing enzyme. J. Biol. Chem. 274:2563–70 [Google Scholar]
  142. Yamaoka S, Shimono Y, Shirakawa M, Fukao Y, Kawase T. 142.  et al. 2013. Identification and dynamics of Arabidopsis adaptor protein-2 complex and its involvement in floral organ development. Plant Cell 25:2958–69 [Google Scholar]
  143. Yamazaki M, Shimada T, Takahashi H, Tamura K, Kondo M. 143.  et al. 2008. Arabidopsis VPS35, a retromer component, is required for vacuolar protein sorting and involved in plant growth and leaf senescence. Plant Cell Physiol 49:142–56 [Google Scholar]
  144. Yang YD, Elamawi R, Bubeck J, Pepperkok R, Ritzenthaler C, Robinson DG. 144.  2005. Dynamics of COPII vesicles and the Golgi apparatus in cultured Nicotianatabacum BY-2 cells provides evidence for transient association of Golgi stacks with endoplasmic reticulum exit sites. Plant Cell 17:1513–31 [Google Scholar]
  145. Yorimitsu T, Sato K. 145.  2012. Insights into structural and regulatory roles of Sec16 in COPII vesicle formation at ER exit sites. Mol. Biol. Cell 23:2930–42 [Google Scholar]
  146. Zeeuwen PL, van Vlijmen-Willems IM, Cheng T, Rodijk-Olthuis D, Hitomi K. 146.  et al. 2010. The cystatin M/E-cathepsin L balance is essential for tissue homeostasis in epidermis, hair follicles and cornea. FASEB J 24:3744–55 [Google Scholar]
  147. Zeeuwen PLJM, van Vlijmen-Willems IMJJ, Olthuis D, Johansen HT, Hitomi K. 147.  et al. 2004. Identification of legumain and cystatin M/E as a functional dyad in skin: Evidence for a role in stratum corneum and skin barrier formation. Hum. Mol. Genet. 13:1069–79 [Google Scholar]
  148. Zeng Y, Chung KP, Li B, Lai CM, Lam SK. 148.  et al. 2015. Unique COPII component AtSar1a/AtSec23a pair is required for the distinct function of protein ER export in Arabidopsis thaliana. PNAS 112:14360–65 [Google Scholar]
  149. Zhang H, Wang L, Deroles S, Bennett R, Davies K. 149.  2006. New insight into the structures and formation of anthocyanic vacuolar inclusions in flower petals. BMC Plant Biol 6:29 [Google Scholar]
  150. Zhao J.150.  2015. Flavonoid transport mechanisms: how to go, and with whom. Trends Plant Sci 20:576–85 [Google Scholar]
  151. Zhao J, Dixon RA. 151.  2009. MATE transporters facilitate vacuolar uptake of epicatechin 3′-O-glucoside for proanthocyanidin biosynthesis in Medicagotruncatula and Arabidopsis. Plant Cell 21:2323–40 [Google Scholar]
  152. Zhao J, Dixon RA. 152.  2010. The ‘ins’ and ‘outs’ of flavonoid transport. Trends Plant Sci 15:72–80 [Google Scholar]
  153. Zhao Z, Zhang W, Stanley BA, Assmann SM. 153.  2008. Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways. Plant Cell 20:3210–26 [Google Scholar]
  154. Zink S, Wenzel D, Wurm CA, Schmitt HD. 154.  2009. A link between ER tethering and COP-I vesicle uncoating. Dev. Cell 17:403–16 [Google Scholar]
  155. Zouhar J, Munoz A, Rojo E. 155.  2010. Functional specialization within the vacuolar sorting receptor family: VSR1, VSR3 and VSR4 sort vacuolar storage cargo in seeds and vegetative tissues. Plant J 64:577–88 [Google Scholar]
  156. Shirakawa M, Ueda H, Shimada T, Hara-Nishimura I. 156.  2016. FAMA: a molecular link between stomata and myrosin cells. Trends Plant Sci. 21:861–71 [Google Scholar]
/content/journals/10.1146/annurev-arplant-042817-040508
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Plant Vacuoles
Annual Review of Plant Biology 69, 123 (2018); https://doi.org/10.1146/annurev-arplant-042817-040508
/content/journals/10.1146/annurev-arplant-042817-040508
/content/journals/10.1146/annurev-arplant-042817-040508
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