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Protein trafficking in plant cells: Tools and markers

  • Dongmei Zhu
  • Mengdi Zhang
  • Caiji Gao
  • Jinbo ShenEmail author
Review
  • 1 Downloads

Abstract

Eukaryotic cells consist of numerous membrane-bound organelles, which compartmentalize cellular materials to fulfil a variety of vital functions. In the post-genomic era, it is widely recognized that identification of the subcellular organelle localization and transport mechanisms of the encoded proteins are necessary for a fundamental understanding of their biological functions and the organization of cellular activity. Multiple experimental approaches are now available to determine the subcellular localizations and dynamics of proteins. In this review, we provide an overview of the current methods and organelle markers for protein subcellular localization and trafficking studies in plants, with a focus on the organelles of the endomembrane system. We also discuss the limitations of each method in terms of protein colocalization studies.

Keywords

protein subcellular localization organelle markers endomembrane system 

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Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31970181), the Zhejiang Provincial Natural Science Foundation of China (R20C020001), the National Key Research and Development Program of China (2018YFD1000604) and the Zhejiang Agricultural and Forestry University Starting Funding (2018FR029). We apologize to colleagues whose work could not be included in this review because of space limitations.

Compliance and ethics

The author(s) declare that they have no conflict of interest.

References

  1. Ahmed, S.U., Bar-Peled, M., and Raikhel, N.V. (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.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Ahmed, S.U., Rojo, E., Kovaleva, V., Venkataraman, S., Dombrowski, J.E., Matsuoka, K., and Raikhel, N.V. (2000). The plant vacuolar sorting receptor AtELP is involved in transport of NH2-terminal propeptide-containing vacuolar proteins in Arabidopsis thaliana. J Cell Biol 149, 1335–1344.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Austin, J.R., and Staehelin, L.A. (2011). Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography. Plant Physiol 155, 1601–1611.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Baldwin, T.C., Handford, M.G., Yuseff, M.I., Orellana, A., and Dupree, P. (2001). Identification and characterization of GONST1, a Golgi-localized GDP-mannose transporter in Arabidopsis. Plant Cell 13, 2283–2295.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Banbury, D.N., Oakley, J.D., Sessions, R.B., and Banting, G. (2003). Tyrphostin A23 inhibits internalization of the transferrin receptor by perturbing the interaction between tyrosine motifs and the medium chain subunit of the AP-2 adaptor complex. J Biol Chem 278, 12022–12028.PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bar, M., Leibman, M., Schuster, S., Pitzhadza, H., and Avni, A. (2013). EHD1 functions in endosomal recycling and confers salt tolerance. PLoS ONE 8, e54533.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Barberon, M., Zelazny, E., Robert, S., Conéjéro, G., Curie, C., Friml, J., and Vert, G. (2011). Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc Natl Acad Sci USA 108, E450–E458.PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bassham, D.C., Sanderfoot, A.A., Kovaleva, V., Zheng, H., and Raikhel, N. V. (2000). AtVPS45 complex formation at the trans-Golgi network. Mol Biol Cell 11, 2251–2265.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bayle, V., Arrighi, J.F., Creff, A., Nespoulous, C., Vialaret, J., Rossignol, M., Gonzalez, E., Paz-Ares, J., and Nussaume, L. (2011). Arabidopsis thaliana high-affinity phosphate transporters exhibit multiple levels of posttranslational regulation. Plant Cell 23, 1523–1535.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bell, K., Mitchell, S., Paultre, D., Posch, M., and Oparka, K. (2013). Correlative imaging of fluorescent proteins in resin-embedded plant material. Plant Physiol 161, 1595–1603.PubMedPubMedCentralCrossRefGoogle Scholar
  11. Blommaart, E.F.C., Krause, U., Schellens, J.P.M., Vreeling-Sindelarova, H., and Meijer, A.J. (1997). The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 243, 240–246.PubMedCrossRefGoogle Scholar
  12. Boevink, P., Cruz, S., Hawes, C., Harris, N., and Oparka, K.J. (1996). Virus-mediated delivery of the green fluorescent protein to the endoplasmic reticulum of plant cells. Plant J 10, 935–941.CrossRefGoogle Scholar
  13. Boevink, P., Oparka, K., Cruz, S.S., Martin, B., Betteridge, A., and Hawes, C. (1998). Stacks on tracks: The plant Golgi apparatus traffics on an actin/ER network. Plant J 15, 441–447.PubMedCrossRefGoogle Scholar
  14. Boevink, P., Martin, B., Oparka, K., Santa Cruz, S., and Hawes, C. (1999). Transport of virally expressed green fluorescent protein through the secretory pathway in tobacco leaves is inhibited by cold shock and brefeldin A. Planta 208, 392–400.CrossRefGoogle Scholar
  15. Bottanelli, F., Gershlick, D.C., and Denecke, J. (2012). Evidence for sequential action of Rab5 and Rab7 GTPases in prevacuolar organelle partitioning. Traffic 13, 338–354.PubMedCrossRefGoogle Scholar
  16. Brandizzi, F., Frangne, N., Marc-Martin, S., Hawes, C., Neuhaus, J.M., and Paris, N. (2002a). The destination for single-pass membrane proteins is influenced markedly by the length of the hydrophobic domain. Plant Cell 14, 1077–1092.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Brandizzi, F., Snapp, E.L., Roberts, A.G., Lippincott-Schwartz, J., and Hawes, C. (2002b). Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent. Plant Cell 14, 1293–1309.PubMedPubMedCentralCrossRefGoogle Scholar
  18. Brandizzi, F., Hanton, S., daSilva, L.L.P., Boevink, P., Evans, D., Oparka, K., Denecke, J., and Hawes, C. (2003). ER quality control can lead to retrograde transport from the ER lumen to the cytosol and the nucleoplasm in plants. Plant J 34, 269–281.PubMedCrossRefGoogle Scholar
  19. Brazda, P., Krieger, J., Daniel, B., Jonas, D., Szekeres, T., Langowski, J., Tóth, K., Nagy, L., and Vámosi, G. (2014). Ligand binding shifts highly mobile retinoid X receptor to the chromatin-bound state in a coactivator-dependent manner, as revealed by single-cell imaging. Mol Cell Biol 34, 1234–1245.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Cardona-López, X., Cuyas, L., Marín, E., Rajulu, C., Irigoyen, M.L., Gil, E., Puga, M.I., Bligny, R., Nussaume, L., Geldner, N., et al. (2015). ESCRT-III-associated protein ALIX mediates high-affinity phosphate transporter trafficking to maintain phosphate homeostasis in Arabidopsis. Plant Cell 27, 2560–2581.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Cheng, F., Zamski, E., Guo, W., Pharr, D.M., and Williamson, J.D. (2009). Salicylic acid stimulates secretion of the normally symplastic enzyme mannitol dehydrogenase: A possible defense against mannitol-secreting fungal pathogens. Planta 230, 1093–1103.PubMedCrossRefPubMedCentralGoogle Scholar
  22. Chung, K.P., Zeng, Y., Li, Y., Ji, C., Xia, Y., and Jiang, L. (2018). Signal motif-dependent ER export of the Qc-SNARE BET12 interacts with MEMB12 and affects PR1 trafficking in Arabidopsis. J Cell Sci 131, jcs202838.PubMedCrossRefPubMedCentralGoogle Scholar
  23. Clausen, M.P., Sezgin, E., Bernardino de la Serna, J., Waithe, D., Lagerholm, B.C., and Eggeling, C. (2015). A straightforward approach for gated STED-FCS to investigate lipid membrane dynamics. Methods 88, 67–75.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Colinas, J., Schmidler, S.C., Bohrer, G., Iordanov, B., Benfey, P.N., and Valcarcel, J. (2008). Intergenic and genic sequence lengths have opposite relationships with respect to gene expression. PLoS ONE 3, e3670.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Corvera, S., D’Arrigo, A., and Stenmark, H. (1999). Phosphoinositides in membrane traffic. Curr Opin Cell Biol 11, 460–465.PubMedCrossRefPubMedCentralGoogle Scholar
  26. Cui, Y., Cao, W., He, Y., Zhao, Q., Wakazaki, M., Zhuang, X., Gao, J., Zeng, Y., Gao, C., Ding, Y., et al. (2019). A whole-cell electron tomography model of vacuole biogenesis in Arabidopsis root cells. Nat Plants 5, 95–105.PubMedCrossRefPubMedCentralGoogle Scholar
  27. Cutler, S.R., Ehrhardt, D.W., Griffitts, J.S., and Somerville, C.R. (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.PubMedCrossRefPubMedCentralGoogle Scholar
  28. Dangol, S., Singh, R., Chen, Y.F., and Jwa, N.S. (2017). Visualization of multicolored in vivo organelle markers for co-localization studies in Oryza sativa. Mol Cells 40, 828–836.PubMedPubMedCentralGoogle Scholar
  29. daSilva, L.L.P., Taylor, J.P., Hadlington, J.L., Hanton, S.L., Snowden, C.J., Fox, S.J., Foresti, O., Brandizzi, F., and Denecke, J. (2005). Receptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell 17, 132–148.PubMedPubMedCentralCrossRefGoogle Scholar
  30. de Boer, P., Hoogenboom, J.P., and Giepmans, B.N.G. (2015). Correlated light and electron microscopy: Ultrastructure lights up! Nat Methods 12, 503–513.PubMedCrossRefPubMedCentralGoogle Scholar
  31. Dejonghe, W., Kuenen, S., Mylle, E., Vasileva, M., Keech, O., Viotti, C., Swerts, J., Fendrych, M., Ortiz-Morea, F.A., Mishev, K., et al. (2016). Mitochondrial uncouplers inhibit clathrin-mediated endocytosis largely through cytoplasmic acidification. Nat Commun 7, 11710.PubMedPubMedCentralCrossRefGoogle Scholar
  32. Dejonghe, W., and Russinova, E. (2017). Plant chemical genetics: From phenotype-based screens to synthetic biology. Plant Physiol 174, 5–20.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Denecke, J., De Rycke, R., and Botterman, J. (1992). Plant and mammalian sorting signals for protein retention in the endoplasmic reticulum contain a conserved epitope. EMBO J 11, 2345–2355.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Denecke, J., Carlsson, L.E., Vidal, S., Höglund, A.S., Ek, B., van Zeijl, M. J., Sinjorgo, K.M., and Palva, E.T. (1995). The tobacco homolog of mammalian calreticulin is present in protein complexes in vivo. Plant Cell 7, 391–406.PubMedPubMedCentralGoogle Scholar
  35. Denecke, J., Aniento, F., Frigerio, L., Hawes, C., Hwang, I., Mathur, J., Neuhaus, J.M., and Robinson, D.G. (2012). Secretory pathway research: The more experimental systems the better. Plant Cell 24, 1316–1326.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y.D., and Schumacher, K. (2006). Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18, 715–730.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dhonukshe, P., Aniento, F., Hwang, I., Robinson, D.G., Mravec, J., Stierhof, Y.D., and Friml, J. (2007). Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 17, 520–527.PubMedCrossRefPubMedCentralGoogle Scholar
  38. Ding, Y., Wang, J., Chun Lai, J.H., Ling Chan, V.H., Wang, X., Cai, Y., Tan, X., Bao, Y., Xia, J., Robinson, D.G., et al. (2014). Exo70E2 is essential for exocyst subunit recruitment and EXPO formation in both plants and animals. Mol Biol Cell 25, 412–426.PubMedPubMedCentralCrossRefGoogle Scholar
  39. Dirnberger, D., Bencúr, P., Mach, L., and Steinkellner, H. (2002). The Golgi localization of Arabidopsis thaliana β1, 2-xylosyltransferase in plant cells is dependent on its cytoplasmic and transmembrane sequences. Plant Mol Biol 50, 273–281.PubMedCrossRefPubMedCentralGoogle Scholar
  40. Doyle, S.M., Haeger, A., Vain, T., Rigal, A., Viotti, C., Łangowska, M., Ma, Q., Friml, J., Raikhel, N.V., Hicks, G.R., et al. (2015). An early secretory pathway mediated by GNOM-LIKE 1 and GNOM is essential for basal polarity establishment in Arabidopsis thaliana. Proc Natl Acad Sci USA 112, E806–E815.PubMedCrossRefPubMedCentralGoogle Scholar
  41. Drakakaki, G., Robert, S., Szatmari, A.M., Brown, M.Q., Nagawa, S., Van Damme, D., Leonard, M., Yang, Z., Girke, T., Schmid, S.L., et al. (2011). Clusters of bioactive compounds target dynamic endomembrane networks in vivo. Proc Natl Acad Sci USA 108, 17850–17855.PubMedCrossRefPubMedCentralGoogle Scholar
  42. Duby, G., Degand, H., and Boutry, M. (2001). Structure requirement and identification of a cryptic cleavage site in the mitochondrial processing of a plant F1-ATPase β-subunit presequence. FEBS Lett 505, 409–413.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Dunkley, T.P.J., Hester, S., Shadforth, I.P., Runions, J., Weimar, T., Hanton, S.L., Griffin, J.L., Bessant, C., Brandizzi, F., Hawes, C., et al. (2006). Mapping the Arabidopsis organelle proteome. Proc Natl Acad Sci USA 103, 6518–6523.PubMedCrossRefPubMedCentralGoogle Scholar
  44. Fan, L., Hao, H., Xue, Y., Zhang, L., Song, K., Ding, Z., Botella, M.A., Wang, H., and Lin, J. (2013). Dynamic analysis of Arabidopsis AP2 sigma subunit reveals a key role in clathrin-mediated endocytosis and plant development. Development 140, 3826–3837.PubMedCrossRefPubMedCentralGoogle Scholar
  45. Fan, L., Li, R., Pan, J., Ding, Z., and Lin, J. (2015). Endocytosis and its regulation in plants. Trends Plant Sci 20, 388–397.PubMedCrossRefPubMedCentralGoogle Scholar
  46. Flückiger, R., De Caroli, M., Piro, G., Dalessandro, G., Neuhaus, J.M., and Di Sansebastiano, G.P. (2003). Vacuolar system distribution in Arabidopsis tissues, visualized using GFP fusion proteins. J Exp Bot 54, 1577–1584.PubMedCrossRefPubMedCentralGoogle Scholar
  47. Foresti, O., Gershlick, D.C., Bottanelli, F., Hummel, E., Hawes, C., and Denecke, J. (2010). A recycling-defective vacuolar sorting receptor reveals an intermediate compartment situated between prevacuoles and vacuoles in tobacco. Plant Cell 22, 3992–4008.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Fricker, M., Runions, J., and Moore, I. (2006). Quantitative fluorescence microscopy: From art to science. Annu Rev Plant Biol 57, 79–107.PubMedCrossRefPubMedCentralGoogle Scholar
  49. Frigerio, L., Jolliffe, N.A., Di Cola, A., Felipe, D.H., Paris, N., Neuhaus, J. M., Lord, J.M., Ceriotti, A., and Roberts, L.M. (2001). The internal propeptide of the ricin precursor carries a sequence-specific determinant for vacuolar sorting. Plant Physiol 126, 167–175.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Früholz, S., Fäßler, F., Kolukisaoglu, Ü., and Pimpl, P. (2018). Nanobody-triggered lockdown of VSRs reveals ligand reloading in the Golgi. Nat Commun 9, 643.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Fuji, K., Shimada, T., Takahashi, H., Tamura, K., Koumoto, Y., Utsumi, S., Nishizawa, K., Maruyama, N., and Hara-Nishimura, I. (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.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Gao, C., Yu, C.K.Y., Qu, S., San, M.W.Y., Li, K.Y., Lo, S.W., and Jiang, L. (2012). The Golgi-localized Arabidopsis endomembrane protein12 contains both endoplasmic reticulum export and Golgi retention signals at its C terminus. Plant Cell 24, 2086–2104.PubMedPubMedCentralCrossRefGoogle Scholar
  53. Gao, C., Luo, M., Zhao, Q., Yang, R., Cui, Y., Zeng, Y., Xia, J., and Jiang, L. (2014). A unique plant ESCRT component, FREE1, regulates multivesicular body protein sorting and plant growth. Curr Biol 24, 2556–2563.PubMedCrossRefPubMedCentralGoogle Scholar
  54. Gao, C., Zhuang, X., Shen, J., and Jiang, L. (2017). Plant ESCRT complexes: Moving beyond endosomal sorting. Trends Plant Sci 22, 986–998.PubMedCrossRefPubMedCentralGoogle Scholar
  55. Gattolin, S., Sorieul, M., and Frigerio, L. (2011). Mapping of tonoplast intrinsic proteins in maturing and germinating Arabidopsis seeds reveals dual localization of embryonic TIPs to the tonoplast and plasma membrane. Mol Plant 4, 180–189.PubMedCrossRefPubMedCentralGoogle Scholar
  56. Geldner, N., Friml, J., Stierhof, Y.D., Jürgens, G., and Palme, K. (2001). Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425–428.PubMedCrossRefPubMedCentralGoogle Scholar
  57. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A., and Jürgens, G. (2003). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219–230.PubMedCrossRefPubMedCentralGoogle Scholar
  58. Geldner, N. (2004). The plant endosomal system—its structure and role in signal transduction and plant development. Planta 219, 547–560.PubMedCrossRefPubMedCentralGoogle Scholar
  59. Geldner, N., Hyman, D.L., Wang, X., Schumacher, K., and Chory, J. (2007). Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 21, 1598–1602.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Geldner, N., Dénervaud-Tendon, V., Hyman, D.L., Mayer, U., Stierhof, Y. D., and Chory, J. (2009). Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J 59, 169–178.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Grabenbauer, M., Geerts, W.J.C., Fernadez-Rodriguez, J., Hoenger, A., Koster, A.J., and Nilsson, T. (2005). Correlative microscopy and electron tomography of GFP through photooxidation. Nat Methods 2, 857–862.PubMedCrossRefPubMedCentralGoogle Scholar
  62. Graham, J.M. (2001). Isolation of Golgi membranes from tissues and cells by differential and density gradient centrifugation. Curr Protocols Cell Biol 10, 3.9.1-3.9.24.CrossRefGoogle Scholar
  63. Grebenok, R.J., Pierson, E., Lambert, G.M., Gong, F.C., Afonso, C.L., Haldeman-Cahill, R., Carrington, J.C., and Galbraith, D.W. (1997). Green-fluorescent protein fusions for efficient characterization of nuclear targeting. Plant J 11, 573–586.PubMedCrossRefPubMedCentralGoogle Scholar
  64. Hao, H., Fan, L., Chen, T., Li, R., Li, X., He, Q., Botella, M.A., and Lin, J. (2014). Clathrin and membrane microdomains cooperatively regulate RbohD dynamics and activity in Arabidopsis. Plant Cell 26, 1729–1745.PubMedPubMedCentralCrossRefGoogle Scholar
  65. Hatsugai, N., Iwasaki, S., Tamura, K., Kondo, M., Fuji, K., Ogasawara, K., Nishimura, M., and Hara-Nishimura, I. (2009). A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev 23, 2496–2506.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Hawes, C., Saint-Jore, C., Martin, B., and Zheng, H. (2001). ER confirmed as the location of mystery organelles in Arabidopsis plants expressing GFP! Trends Plant Sci 6, 245–246.PubMedCrossRefPubMedCentralGoogle Scholar
  67. Henne, W.M., Buchkovich, N.J., and Emr, S.D. (2011). The ESCRT pathway. Dev Cell 21, 77–91.PubMedCrossRefPubMedCentralGoogle Scholar
  68. Hillmer, S., Movafeghi, A., Robinson, D.G., and Hinz, G. (2001). Vacuolar storage proteins are sorted in the cis-cisternae of the pea cotyledon Golgi apparatus. J Cell Biol 152, 41–50.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Hinz, G., Menze, A., Hohl, I., and 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 Bot 48, 139–149.CrossRefGoogle Scholar
  70. Hinz, G., Hillmer, S., Bäumer, M., and Hohl, I. (1999). Vacuolar storage proteins and the putative vacuolar sorting receptor BP-80 exit the Golgi apparatus of developing pea cotyledons in different transport vesicles. Plant Cell 11, 1509–1524.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Huss, M., Ingenhorst, G., König, S., Gassel, M., Dröse, S., Zeeck, A., Altendorf, K., and Wieczorek, H. (2002). Concanamycin A, the specific inhibitor of V-ATPases, binds to the Vo subunit c. J Biol Chem 277, 40544–40548.PubMedCrossRefPubMedCentralGoogle Scholar
  72. Irons, S.L., Evans, D.E., and Brandizzi, F. (2003). The first 238 amino acids of the human lamin B receptor are targeted to the nuclear envelope in plants. J Exp Bot 54, 943–950.PubMedCrossRefPubMedCentralGoogle Scholar
  73. Ito, Y., Uemura, T., and Nakano, A. (2018). The Golgi entry core compartment functions as a COPII-independent scaffold for ER-to-Golgi transport in plant cells. J Cell Sci 131, jcs203893.PubMedCrossRefPubMedCentralGoogle Scholar
  74. Jackson, C.L., and Casanova, J.E. (2000). Turning on ARF: The Sec7 family of guanine-nucleotide-exchange factors. Trends Cell Biol 10, 60–67.PubMedCrossRefPubMedCentralGoogle Scholar
  75. Jauh, G.Y., Phillips, T.E., and Rogers, J.C. (1999). Tonoplast intrinsic protein isoforms as markers for vacuolar functions. Plant Cell 11, 1867–1882.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Jedd, G., Mulholland, J., and Segev, N. (1997). Two new Ypt GTPases are required for exit from the yeast trans-Golgi compartment. J Cell Biol 137, 563–580.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Jia, T., Gao, C., Cui, Y., Wang, J., Ding, Y., Cai, Y., Ueda, T., Nakano, A., and Jiang, L. (2013). ARA7(Q69L) expression in transgenic Arabidopsis cells induces the formation of enlarged multivesicular bodies. J Exp Bot 64, 2817–2829.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Jiang, L., and Rogers, J.C. (1998). Integral membrane protein sorting to vacuoles in plant cells: Evidence for two pathways. J Cell Biol 143, 1183–1199.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Jiang, L., Phillips, T.E., Rogers, S.W., and Rogers, J.C. (2000). Biogenesis of the protein storage vacuole crystalloid. J Cell Biol 150, 755–770.PubMedPubMedCentralCrossRefGoogle Scholar
  80. Jiang, L., Phillips, T.E., Hamm, C.A., Drozdowicz, Y.M., Rea, P.A., Maeshima, M., Rogers, S.W., and Rogers, J.C. (2001). The protein storage vacuole. J Cell Biol 155, 991–1002.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Jiang, L., and Rogers, J.C. (2003). Sorting of lytic enzymes in the plant Golgi apparatus. Annual Plant Review 9, 114–140.Google Scholar
  82. Köhler, S., Delwiche, C.F., Denny, P.W., Tilney, L.G., Webster, P., Wilson, R.J., Palmer, J.D., and Roos, D.S. (1997). A plastid of probable green algal origin in apicomplexan parasites. Science 275, 1485–1489.PubMedCrossRefPubMedCentralGoogle Scholar
  83. Kalinowska, K., Nagel, M.K., Goodman, K., Cuyas, L., Anzenberger, F., Alkofer, A., Paz-Ares, J., Braun, P., Rubio, V., Otegui, M.S., et al. (2015). Arabidopsis ALIX is required for the endosomal localization of the deubiquitinating enzyme AMSH3. Proc Natl Acad Sci USA 112, E5543–E5551.PubMedCrossRefPubMedCentralGoogle Scholar
  84. Kang, B.H., Nielsen, E., Preuss, M.L., Mastronarde, D., and Staehelin, L.A. (2011). Electron tomography of RabA4b- and PI-4Kβ1-labeled trans Golgi network compartments in Arabidopsis. Traffic 12, 313–329.PubMedCrossRefPubMedCentralGoogle Scholar
  85. Kasai, K., Takano, J., Miwa, K., Toyoda, A., and Fujiwara, T. (2011). High boron-induced ubiquitination regulates vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana. J Biol Chem 286, 6175–6183.PubMedCrossRefPubMedCentralGoogle Scholar
  86. Kay, J.G., Koivusalo, M., Ma, X., Wohland, T., and Grinstein, S. (2012). Phosphatidylserine dynamics in cellular membranes. Mol Biol Cell 23, 2198–2212.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Kiernan, J.A. (1999). Histological and histochemical methods: Theory and practice. Shock 12, 479.Google Scholar
  88. Kim, D.H., Eu, Y.J., Yoo, C.M., Kim, Y.W., Pih, K.T., Jin, J.B., Kim, S.J., Stenmark, H., and Hwang, I. (2001). Trafficking of phosphatidylinositol 3-phosphate from the trans-Golgi network to the lumen of the central vacuole in plant cells. Plant Cell 13, 287–301.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Kirsch, T., Paris, N., Butler, J.M., Beevers, L., and Rogers, J.C. (1994). Purification and initial characterization of a potential plant vacuolar targeting receptor. Proc Natl Acad Sci USA 91, 3403–3407.PubMedCrossRefPubMedCentralGoogle Scholar
  90. Kleine-Vehn, J., Dhonukshe, P., Swarup, R., Bennett, M., and Friml, J. (2006). Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1. Plant Cell 18, 3171–3181.PubMedPubMedCentralCrossRefGoogle Scholar
  91. Kleine-Vehn, J., and Friml, J. (2008). Polar targeting and endocytic recycling in auxin-dependent plant development. Annu Rev Cell Dev Biol 24, 447–473.PubMedCrossRefPubMedCentralGoogle Scholar
  92. Kluge, C., Lamkemeyer, P., Tavakoli, N., Golldack, D., Kandlbinder, A., and Dietz, K.J. (2003). cDNA cloning of 12 subunits of the V-type ATPase from Mesembryanthemum crystallinum and their expression under stress. Mol Membrane Biol 20, 171–183.CrossRefGoogle Scholar
  93. Komis, G., Mistrik, M., Šamajová O., Ovečka, M., Bartek, J., and Šamaj, J. (2015). Superresolution live imaging of plant cells using structured illumination microscopy. Nat Protoc 10, 1248–1263.PubMedCrossRefPubMedCentralGoogle Scholar
  94. Komis, G., Novčk, D., Ovečka, M., Šamajová, O., and Šamaj, J. (2018). Advances in imaging plant cell dynamics. Plant Physiol 176, 80–93.PubMedCrossRefPubMedCentralGoogle Scholar
  95. Konopka, C.A., and Bednarek, S.Y. (2008). Variable-angle epifluorescence microscopy: A new way to look at protein dynamics in the plant cell cortex. Plant J 53, 186–196.PubMedCrossRefPubMedCentralGoogle Scholar
  96. Kopek, B.G., Paez-Segala, M.G., Shtengel, G., Sochacki, K.A., Sun, M.G., Wang, Y., Xu, C.S., van Engelenburg, S.B., Taraska, J.W., Looger, L.L., et al. (2017). Diverse protocols for correlative super-resolution fluorescence imaging and electron microscopy of chemically fixed samples. Nat Protoc 12, 916–946.PubMedPubMedCentralCrossRefGoogle Scholar
  97. Künzl, F., Früholz, S., Fäßler, F., Li, B., and Pimpl, P. (2016). Receptor-mediated sorting of soluble vacuolar proteins ends at the trans-Golgi network/early endosome. Nat Plants 2, 16017.PubMedCrossRefPubMedCentralGoogle Scholar
  98. Lam, S.K., Siu, C.L., Hillmer, S., Jang, S., An, G., Robinson, D.G., and Jiang, L. (2007). Rice SCAMP1 defines clathrin-coated, trans-Golgi-located tubular-vesicular structures as an early endosome in tobacco BY-2 Cells. Plant Cell 19, 296–319.PubMedPubMedCentralCrossRefGoogle Scholar
  99. Le Bars, R., Marion, J., Le Borgne, R., Satiat-Jeunemaitre, B., and Bianchi, M.W. (2014). ATG5 defines a phagophore domain connected to the endoplasmic reticulum during autophagosome formation in plants. Nat Commun 5, 4121.PubMedCrossRefPubMedCentralGoogle Scholar
  100. Lee, G.J., Sohn, E.J., Lee, M.H., and Hwang, I. (2004). The Arabidopsis Rab5 homologs Rha1 and Ara7 localize to the prevacuolar compartment. Plant Cell Physiol 45, 1211–1220.PubMedCrossRefPubMedCentralGoogle Scholar
  101. Lee, H.I., Gal, S., Newman, T.C., and Raikhel, N.V. (1993). The Arabidopsis endoplasmic reticulum retention receptor functions in yeast. Proc Natl Acad Sci USA 90, 11433–11437.PubMedCrossRefPubMedCentralGoogle Scholar
  102. Lee, M.H., Min, M.K., Lee, Y.J., Jin, J.B., Shin, D.H., Kim, D.H., Lee, K. H., and Hwang, I. (2002). ADP-ribosylation factor 1 of Arabidopsis plays a critical role in intracellular trafficking and maintenance of endoplasmic reticulum morphology in Arabidopsis. Plant Physiol 129, 1507–1520.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Levanony, H., Rubin, R., Altschuler, Y., and Galili, G. (1992). Evidence for a novel route of wheat storage proteins to vacuoles. J Cell Biol 119, 1117–1128.PubMedCrossRefPubMedCentralGoogle Scholar
  104. Li, H., Li, Y., Zhao, Q., Li, T., Wei, J., Li, B., Shen, W., Yang, C., Zeng, Y., Rodriguez, P.L., et al. (2019). The plant ESCRT component FREE1 shuttles to the nucleus to attenuate abscisic acid signalling. Nat Plants 5, 512–524.PubMedCrossRefPubMedCentralGoogle Scholar
  105. Li, R., Liu, P., Wan, Y., Chen, T., Wang, Q., Mettbach, U., Baluška, F., Šamaj, J., Fang, X., Lucas, W.J., et al. (2012). A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a clathrin-independent endocytic pathway and is required for seedling development. Plant Cell 24, 2105–2122.PubMedPubMedCentralCrossRefGoogle Scholar
  106. Li, R., Rodriguez-Furlan, C., Wang, J., van de Ven, W., Gao, T., Raikhel, N. V., and Hicks, G.R. (2017). Different endomembrane trafficking pathways establish apical and basal polarities. Plant Cell 29, 90–108.PubMedCrossRefPubMedCentralGoogle Scholar
  107. Li, X., Wu, Y., Zhang, D.Z., Gillikin, J.W., Boston, R.S., Franceschi, V.R., and Okita, T.W. (1993). Rice prolamine protein body biogenesis: A BiP-mediated process. Science 262, 1054–1056.PubMedCrossRefPubMedCentralGoogle Scholar
  108. Li, X., Xing, J., Qiu, Z., He, Q., and Lin, J. (2016). Quantification of membrane protein dynamics and interactions in plant cells by fluorescence correlation spectroscopy. Mol Plant 9, 1229–1239.PubMedCrossRefPubMedCentralGoogle Scholar
  109. Li, Y.B., Rogers, S.W., Tse, Y.C., Lo, S.W., Sun, S.S.M., Jauh, G.Y., and Jiang, L. (2002). BP-80 and homologs are concentrated on post-Golgi, probable lytic prevacuolar compartments. Plant Cell Physiol 43, 726–742.PubMedCrossRefPubMedCentralGoogle Scholar
  110. Lin, Y., Ding, Y., Wang, J., Shen, J., Kung, C.H., Zhuang, X., Cui, Y., Yin, Z., Xia, Y., Lin, H., et al. (2015). Exocyst-positive organelles and autophagosomes are distinct organelles in plants. Plant Physiol 169, 1917–1932.PubMedPubMedCentralGoogle Scholar
  111. Liu, Y., and Bassham, D.C. (2012). Autophagy: Pathways for self-eating in plant cells. Annu Rev Plant Biol 63, 215–237.PubMedCrossRefGoogle Scholar
  112. Luo, Y., Scholl, S., Doering, A., Zhang, Y., Irani, N.G., Di Rubbo, S., Neumetzler, L., Krishnamoorthy, P., Van Houtte, I., Mylle, E., et al. (2015). V-ATPase activity in the TGN/EE is required for exocytosis and recycling in Arabidopsis. Nat Plants 1, 15094.PubMedPubMedCentralCrossRefGoogle Scholar
  113. Malchus, N., and Weiss, M. (2010). Anomalous diffusion reports on the interaction of misfolded proteins with the quality control machinery in the endoplasmic reticulum. Biophys J 99, 1321–1328.PubMedPubMedCentralCrossRefGoogle Scholar
  114. Mano, H. (1999). Tec family of protein-tyrosine kinases: An overview of their structure and function. Cytokine Growth Factor Rev 10, 267–280.PubMedCrossRefGoogle Scholar
  115. Martinière, A., Lavagi, I., Nageswaran, G., Rolfe, D.J., Maneta-Peyret, L., Luu, D.T., Botchway, S.W., Webb, S.E.D., Mongrand, S., Maurel, C., et al. (2012). Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc Natl Acad Sci USA 109, 12805–12810.PubMedCrossRefGoogle Scholar
  116. Matsushima, R., Hayashi, Y., Kondo, M., Shimada, T., Nishimura, M., and Hara-Nishimura, I. (2002). An endoplasmic reticulum-derived structure that is induced under stress conditions in Arabidopsis. Plant Physiol 130, 1807–1814.PubMedPubMedCentralCrossRefGoogle Scholar
  117. Matsushima, R., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2003). A novel ER-derived compartment, the ER body, selectively accumulates a β-glucosidase with an ER-retention signal in Arabidopsis. Plant J 33, 493–502.PubMedCrossRefGoogle Scholar
  118. Miao, Y., Yan, P.K., Kim, H., Hwang, I., and Jiang, L. (2006). Localization of green fluorescent protein fusions with the seven Arabidopsis vacuolar sorting receptors to prevacuolar compartments in tobacco BY-2 cells. Plant Physiol 142, 945–962.PubMedPubMedCentralCrossRefGoogle Scholar
  119. Miao, Y., and Jiang, L. (2007). Transient expression of fluorescent fusion proteins in protoplasts of suspension cultured cells. Nat Protoc 2, 2348–2353.PubMedCrossRefGoogle Scholar
  120. Morita, M.T., and Shimada, T. (2014). The plant endomembrane system—a complex network supporting plant development and physiology. Plant Cell Physiol 55, 667–671.PubMedCrossRefGoogle Scholar
  121. Murphy, A.S., Bandyopadhyay, A., Holstein, S.E., and Peer, W.A. (2005). Endocytotic cycling of PM proteins. Annu Rev Plant Biol 56, 221–251.PubMedCrossRefGoogle Scholar
  122. Nakano, R.T., Yamada, K., Bednarek, P.Å., Nishimura, M., and Hara-Nishimura, I. (2014). ER bodies in plants of the Brassicales order: Biogenesis and association with innate immunity. Front Plant Sci 5, 73.PubMedPubMedCentralGoogle Scholar
  123. Naramoto, S., Otegui, M.S., Kutsuna, N., de Rycke, R., Dainobu, T., Karampelias, M., Fujimoto, M., Feraru, E., Miki, D., Fukuda, H., et al. (2014). Insights into the localization and function of the membrane trafficking regulator GNOM ARF-GEF at the Golgi apparatus in Arabidopsis. Plant Cell 26, 3062–3076.PubMedPubMedCentralCrossRefGoogle Scholar
  124. Nebenführ, A., Ritzenthaler, C., and Robinson, D.G. (2002). Brefeldin A: Deciphering an enigmatic inhibitor of secretion. Plant Physiol 130, 1102–1108.PubMedPubMedCentralCrossRefGoogle Scholar
  125. Nelson, B.K., Cai, X., and Nebenführ, A. (2007). A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51, 1126–1136.PubMedCrossRefGoogle Scholar
  126. Neuhaus, J.M., and Rogers, J.C. (1998). Sorting of proteins to vacuoles in plant cells. Plant Mol Biol 38, 127–144.PubMedCrossRefGoogle Scholar
  127. Nielsen, M.E., Feechan, A., Böhlenius, H., Ueda, T., and Thordal-Christensen, H. (2012). Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc Natl Acad Sci USA 109, 11443–11448.PubMedCrossRefGoogle Scholar
  128. Nielsen, M.E., and Thordal-Christensen, H. (2013). Transcytosis shuts the door for an unwanted guest. Trends Plant Sci 18, 611–616.PubMedCrossRefGoogle Scholar
  129. Niemes, S., Labs, M., Scheuring, D., Krueger, F., Langhans, M., Jesenofsky, B., Robinson, D.G., and Pimpl, P. (2010a). Sorting of plant vacuolar proteins is initiated in the ER. Plant J 62, 601–614.PubMedCrossRefGoogle Scholar
  130. Niemes, S., Langhans, M., Viotti, C., Scheuring, D., San Wan Yan, M., Jiang, L., Hillmer, S., Robinson, D.G., and Pimpl, P. (2010b). Retromer recycles vacuolar sorting receptors from the trans-Golgi network. Plant J 61, 107–121.PubMedCrossRefGoogle Scholar
  131. Oliviusson, P., Heinzerling, O., Hillmer, S., Hinz, G., Tse, Y.C., Jiang, L., and Robinson, D.G. (2006). Plant retromer, localized to the prevacuolar compartment and microvesicles in Arabidopsis, may interact with vacuolar sorting receptors. Plant Cell 18, 1239–1252.PubMedPubMedCentralCrossRefGoogle Scholar
  132. Oreopoulos, J., Berman, R., and Browne, M. (2014). Spinning-disk confocal microscopy: Present technology and future trends. Quant Imag Cell Biol 123, 153–175.CrossRefGoogle Scholar
  133. Otegui, M.S., Mastronarde, D.N., Kang, B.H., Bednarek, S.Y., and Staehelin, L.A. (2001). Three-dimensional analysis of syncytial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell 13, 2033–2051.PubMedPubMedCentralCrossRefGoogle Scholar
  134. Otegui, M.S., Herder, R., Schulze, J., Jung, R., and Staehelin, L.A. (2006). The proteolytic processing of seed storage proteins in Arabidopsis embryo cells starts in the multivesicular bodies. Plant Cell 18, 2567–2581.PubMedPubMedCentralCrossRefGoogle Scholar
  135. Otegui, M.S., and Pennington, J.G. (2019). Electron tomography in plant cell biology. Microscopy 68, 69–79.PubMedCrossRefGoogle Scholar
  136. Ovečka, M., von Wangenheim, D., Tomančák, P., Šamajová, O., Komis, G., and Šamaj, J. (2018). Multiscale imaging of plant development by light-sheet fluorescence microscopy. Nat Plants 4, 639–650.PubMedCrossRefGoogle Scholar
  137. Paciorek, T., Sauer, M., Balla, J., Wiśniewska, J., and Friml, J. (2006). Immunocytochemical technique for protein localization in sections of plant tissues. Nat Protoc 1, 104–107.PubMedCrossRefGoogle Scholar
  138. Paris, N., and Rogers, J.C. (1996). The role of receptors in targeting soluble proteins from the secretory pathway to the vacuole. Plant Physiol Biochem 34, 223–227.Google Scholar
  139. Paris, N., Stanley, C.M., Jones, R.L., and Rogers, J.C. (1996). Plant cells contain two functionally distinct vacuolar compartments. Cell 85, 563–572.PubMedCrossRefGoogle Scholar
  140. Paris, N., Rogers, S.W., Jiang, L., Kirsch, T., Beevers, L., Phillips, T.E., and Rogers, J.C. (1997). Molecular cloning and further characterization of a probable plant vacuolar sorting receptor. Plant Physiol 115, 29–39.PubMedPubMedCentralCrossRefGoogle Scholar
  141. Park, M., Kim, S.J., Vitale, A., and 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.PubMedPubMedCentralCrossRefGoogle Scholar
  142. Park, M., Lee, D., Lee, G.J., and Hwang, I. (2005). AtRMR1 functions as a cargo receptor for protein trafficking to the protein storage vacuole. J Cell Biol 170, 757–767.PubMedPubMedCentralCrossRefGoogle Scholar
  143. Parsons, H.T., Stevens, T.J., McFarlane, H.E., Vidal-Melgosa, S., Griss, J., Lawrence, N., Butler, R., Sousa, M.M.L., Salemi, M., Willats, W.G.T., et al. (2019). Separating Golgi proteins from cis to trans reveals underlying properties of cisternal localization. Plant Cell tpc.00081.2019.Google Scholar
  144. Peddie, C.J., Domart, M.C., Snetkov, X., O’Toole, P., Larijani, B., Way, M., Cox, S., and Collinson, L.M. (2017). Correlative super-resolution fluorescence and electron microscopy using conventional fluorescent proteins in vacuo. J Struct Biol 199, 120–131.PubMedPubMedCentralCrossRefGoogle Scholar
  145. Pendin, D., Greotti, E., Lefkimmiatis, K., and Pozzan, T. (2017). Exploring cells with targeted biosensors. J Gen Physiol 149, 1–36.PubMedPubMedCentralCrossRefGoogle Scholar
  146. Phillipson, B.A., Pimpl, P., daSilva, L.L.P., Crofts, A.J., Taylor, J.P., Movafeghi, A., Robinson, D.G., and Denecke, J. (2001). Secretory bulk flow of soluble proteins is efficient and COPII dependent. PlantCell 13, 2005–2020.Google Scholar
  147. Pimpl, P., Hanton, S.L., Taylor, J.P., daSilva, L.L.P., and Denecke, J. (2003). The GTPase ARF1p controls the sequence-specific vacuolar sorting route to the lytic vacuole. Plant Cell 15, 1242–1256.PubMedPubMedCentralCrossRefGoogle Scholar
  148. Raffaele, S., Bayer, E., Lafarge, D., Cluzet, S., German Retana, S., Boubekeur, T., Leborgne-Castel, N., Carde, J.P., Lherminier, J., Noirot, E., et al. (2009). Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs Potato virus X movement. Plant Cell 21, 1541–1555.PubMedPubMedCentralCrossRefGoogle Scholar
  149. Reisen, D., Leborgne-Castel, N., Özalp, C., Chaumont, F., and 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.PubMedCrossRefGoogle Scholar
  150. Renna, L., Hanton, S.L., Stefano, G., Bortolotti, L., Misra, V., and Brandizzi, F. (2005). Identification and characterization of AtCASP, a plant transmembrane Golgi matrix protein. Plant Mol Biol 58, 109–122.PubMedCrossRefGoogle Scholar
  151. Robert, S., Narasimha Chary, S., Drakakaki, G., Li, S., Yang, Z., Raikhel, N.V., and Hicks, G.R. (2008). Endosidin1 defines a compartment involved in endocytosis of the brassinosteroid receptor BRI1 and the auxin transporters PIN2 and AUX1. Proc Natl Acad Sci USA 105, 8464–8469.PubMedCrossRefGoogle Scholar
  152. Robinson, D.G., Bäumer, M., Hinz, G., and Hohl, I. (1998). Vesicle transfer of storage proteins to the vacuole: The role of the Golgi apparatus and multivesicular bodies. J Plant Physiol 152, 659–667.CrossRefGoogle Scholar
  153. Robinson, D.G., Albrecht, S., and Moriysu, Y. (2004). The V-ATPase inhibitors concanamycin A and bafilomycin A lead to Golgi swelling in tobacco BY-2 cells. Protoplasma 224, 255–260.PubMedCrossRefGoogle Scholar
  154. Robinson, D.G., Jiang, L., and Schumacher, K. (2008a). The endosomal system of plants: Charting new and familiar territories. Plant Physiol 147, 1482–1492.PubMedPubMedCentralCrossRefGoogle Scholar
  155. Robinson, D.G., Langhans, M., Saint-Jore-Dupas, C., and Hawes, C. (2008b). BFA effects are tissue and not just plant specific. Trends Plant Sci 13, 405–408.PubMedCrossRefPubMedCentralGoogle Scholar
  156. Robinson, D.G., Pimpl, P., Scheuring, D., Stierhof, Y.D., Sturm, S., and Viotti, C. (2012). Trying to make sense of retromer. Trends Plant Sci 17, 431–439.PubMedCrossRefPubMedCentralGoogle Scholar
  157. Robinson, D.G. (2014). Trafficking of vacuolar sorting receptors: New data and new problems. Plant Physiol 165, 1417–1423.PubMedPubMedCentralCrossRefGoogle Scholar
  158. Robinson, D.G., and Neuhaus, J.M. (2016). Receptor-mediated sorting of soluble vacuolar proteins: Myths, facts, and a new model. J Exp Bot 67, 4435–4449.PubMedCrossRefPubMedCentralGoogle Scholar
  159. Robinson, D.G. (2018). Retromer and VSR recycling: A red herring? Plant Physiol 176, 483–484.PubMedPubMedCentralCrossRefGoogle Scholar
  160. Rojo, E., and Denecke, J. (2008). What is moving in the secretory pathway of plants? Plant Physiol 147, 1493–1503.CrossRefGoogle Scholar
  161. Rubin, R., Levanony, H., and Galili, G. (1992). Evidence for the presence of two different types of protein bodies in wheat endosperm. Plant Physiol 99, 718–724.PubMedPubMedCentralCrossRefGoogle Scholar
  162. Saint-Jore-Dupas, C., Nebenführ, A., Boulaflous, A., Follet-Gueye, M.L., Plasson, C., Hawes, C., Driouich, A., Faye, L., and Gomord, V. (2006). Plant N-glycan processing enzymes employ different targeting mechanisms for their spatial arrangement along the secretory pathway. Plant Cell 18, 3182–3200.PubMedPubMedCentralCrossRefGoogle Scholar
  163. Sanderfoot, A.A., Ahmed, S.U., Marty-Mazars, D., Rapoport, I., Kirchhausen, T., Marty, F., and Raikhel, N.V. (1998). A putative vacuolar cargo receptor partially colocalizes with AtPEP12p on a prevacuolar compartment in Arabidopsis roots. Proc Natl Acad Sci USA 95, 9920–9925.PubMedCrossRefPubMedCentralGoogle Scholar
  164. Sanderfoot, A.A., Kovaleva, V., Bassham, D.C., and Raikhel, N.V. (2001). Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell. Mol Biol Cell 12, 3733–3743.PubMedPubMedCentralCrossRefGoogle Scholar
  165. Satiat-Jeunemaitre, B., and Hawes, C. (1992). Redistribution of a Golgi glycoprotein in plant cells treated with brefeldin A. J Cell Sci 103, 1153–1166.Google Scholar
  166. Sato, K., Nishikawa, S., and Nakano, A. (1995). Membrane protein retrieval from the Golgi apparatus to the endoplasmic reticulum (ER): Characterization of the RER1 gene product as a component involved in ER localization of Sec12p. Mol Biol Cell 6, 1459–1477.PubMedPubMedCentralCrossRefGoogle Scholar
  167. Sato, M.H., Nakamura, N., Ohsumi, Y., Kouchi, H., Kondo, M., Hara-Nishimura, I., Nishimura, M., and Wada, Y. (1997). The AtVAM3 encodes a syntaxin-related molecule implicated in the vacuolar assembly in Arabidopsis thaliana. J Biol Chem 272, 24530–24535.PubMedCrossRefGoogle Scholar
  168. Sauer, M., Paciorek, T., Benková, E., and Friml, J. (2006). Immunocytochemical techniques for whole-mount in situ protein localization in plants. Nat Protoc 1, 98–103.PubMedCrossRefGoogle Scholar
  169. Scheuring, D., Viotti, C., Krüger, F., Künzl, F., Sturm, S., Bubeck, J., Hillmer, S., Frigerio, L., Robinson, D.G., Pimpl, P., et al. (2011). Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 23, 3463–3481.PubMedPubMedCentralCrossRefGoogle Scholar
  170. Schubert, V. (2017). Super-resolution microscopy-applications in plant cell research. Front Plant Sci 8, 531.PubMedPubMedCentralCrossRefGoogle Scholar
  171. Segui-Simarro, J.M., Austin Ii, J.R., White, E.A., and Staehelin, L.A. (2004). Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16, 836–856.PubMedPubMedCentralCrossRefGoogle Scholar
  172. Semenza, J.C., Hardwick, K.G., Dean, N., and Pelham, H.R.B. (1990). ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell 61, 1349–1357.PubMedCrossRefGoogle Scholar
  173. Shen, J., Suen, P.K., Wang, X., Lin, Y., Lo, S.W., Rojo, E., and Jiang, L. (2013a). An in vivo expression system for the identification of cargo proteins of vacuolar sorting receptors in Arabidopsis culture cells. Plant J 75, 1003–1017.PubMedCrossRefGoogle Scholar
  174. Shen, J., Zeng, Y., Zhuang, X., Sun, L., Yao, X., Pimpl, P., and Jiang, L. (2013b). Organelle pH in the Arabidopsis endomembrane system. Mol Plant 6, 1419–1437.PubMedCrossRefPubMedCentralGoogle Scholar
  175. Shen, J., Wang, X., and Jiang, L. (2018a). Seeds as bioreactors. In: Molecular Pharming: Applications, Challenges and Emerging Areas. Kermode, A., ed. (New York, Wiley Blackwell), pp. 91–118.CrossRefGoogle Scholar
  176. Shen, J., Zhao, Q., Wang, X., Gao, C., Zhu, Y., Zeng, Y., and Jiang, L. (2018b). A plant Bro1 domain protein BRAF regulates multivesicular body biogenesis and membrane protein homeostasis. Nat Commun 9, 3784.PubMedPubMedCentralCrossRefGoogle Scholar
  177. Shen, Y., Wang, J., Ding, Y., Lo, S.W., Gouzerh, G., Neuhaus, J.M., and Jiang, L. (2011). The rice RMR1 associates with a distinct prevacuolar compartment for the protein storage vacuole pathway. Mol Plant 4, 854–868.PubMedCrossRefPubMedCentralGoogle Scholar
  178. Shimada, T., Kuroyanagi, M., Nishimura, M., and 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.PubMedCrossRefPubMedCentralGoogle Scholar
  179. Shimada, T., Watanabe, E., Tamura, K., Hayashi, Y., Nishimura, M., and Hara-Nishimura, I. (2002). A vacuolar sorting receptor PV72 on the membrane of vesicles that accumulate precursors of seed storage proteins (PAC vesicles). Plant Cell Physiol 43, 1086–1095.PubMedCrossRefPubMedCentralGoogle Scholar
  180. Shimada, T., Fuji, K., Tamura, K., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2003). Vacuolar sorting receptor for seed storage proteins in Arabidopsis thaliana. Proc Natl Acad Sci USA 100, 16095–16100.PubMedCrossRefPubMedCentralGoogle Scholar
  181. Simon, M.L.A., Platre, M.P., Assil, S., van Wijk, R., Chen, W.Y., Chory, J., Dreux, M., Munnik, T., and Jaillais, Y. (2014). A multi-colour/multi-affinity marker set to visualize phosphoinositide dynamics in Arabidopsis. Plant J 77, 322–337.PubMedCrossRefPubMedCentralGoogle Scholar
  182. Smith, J.M., Leslie, M.E., Robinson, S.J., Korasick, D.A., Zhang, T., Backues, S.K., Cornish, P.V., Koo, A.J., Bednarek, S.Y., and Heese, A. (2014a). Loss of Arabidopsis thaliana dynamin-related protein 2B reveals separation of innate immune signaling pathways. PLoS Pathog 10, e1004578.PubMedPubMedCentralCrossRefGoogle Scholar
  183. Smith, J.M., Salamango, D.J., Leslie, M.E., Collins, C.A., and Heese, A. (2014b). Sensitivity to Flg22 is modulated by ligand-induced degradation and de novo synthesis of the endogenous flagellin-receptor FLAGELLIN-SENSING2. Plant Physiol 164, 440–454.PubMedCrossRefPubMedCentralGoogle Scholar
  184. Sohn, E.J., Kim, E.S., Zhao, M., Kim, S.J., Kim, H., Kim, Y.W., Lee, Y.J., Hillmer, S., Sohn, U., Jiang, L., et al. (2003). Rha1, an Arabidopsis Rab5 homolog, plays a critical role in the vacuolar trafficking of soluble cargo proteins. Plant Cell 15, 1057–1070.PubMedPubMedCentralCrossRefGoogle Scholar
  185. Sosinsky, G.E., Giepmans, B.N., Deerinck, T.J., Gaietta, G.M., and Ellisman, M.H. (2007). Markers for correlated light and electron microscopy. Method Cell Biol 79, 575–591.CrossRefGoogle Scholar
  186. Soto-Burgos, J., Zhuang, X., Jiang, L., and Bassham, D.C. (2018). Dynamics of autophagosome formation. Plant Physiol 176, 219–229.PubMedCrossRefPubMedCentralGoogle Scholar
  187. Spallek, T., Beck, M., Ben Khaled, S., Salomon, S., Bourdais, G., Schellmann, S., and Robatzek, S. (2013). ESCRT-I mediates FLS2 endosomal sorting and plant immunity. PLoS Genet 9, e1004035.PubMedPubMedCentralCrossRefGoogle Scholar
  188. Sparkes, I.A., Runions, J., Kearns, A., and Hawes, C. (2006). Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1, 2019–2025.PubMedCrossRefPubMedCentralGoogle Scholar
  189. Spitzer, C., Reyes, F.C., Buono, R., Sliwinski, M.K., Haas, T.J., and Otegui, M.S. (2009). The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. Plant Cell 21, 749–766.PubMedPubMedCentralCrossRefGoogle Scholar
  190. Sze, H., Li, X., and Palmgren, M.G. (1999). Energization of plant cell membranes by H -pumping ATPases: Regulation and biosynthesis. Plant Cell 11, 677–689.PubMedPubMedCentralGoogle Scholar
  191. Takahashi, H., Saito, Y., Kitagawa, T., Morita, S., Masumura, T., and Tanaka, K. (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, 245–249.PubMedCrossRefPubMedCentralGoogle Scholar
  192. Tse, Y.C., Mo, B., Hillmer, S., Zhao, M., Lo, S.W., Robinson, D.G., and Jiang, L. (2004). Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 16, 672–693.PubMedPubMedCentralCrossRefGoogle Scholar
  193. Tse, Y.C., Lo, S.W., Hillmer, S., Dupree, P., and Jiang, L. (2006). Dynamic response of prevacuolar compartments to brefeldin A in plant cells. Plant Physiol 142, 1442–1459.PubMedPubMedCentralCrossRefGoogle Scholar
  194. Ueki, S., Lacroix, B., Krichevsky, A., Lazarowitz, S.G., and Citovsky, V. (2009). Functional transient genetic transformation of Arabidopsis leaves by biolistic bombardment. Nat Protoc 4, 71–77.PubMedCrossRefPubMedCentralGoogle Scholar
  195. Uemura, T., Yoshimura, S.H., Takeyasu, K., and Sato, M.H. (2002). Vacuolar membrane dynamics revealed by GFP-AtVam3 fusion protein. Genes Cells 7, 743–753.PubMedCrossRefPubMedCentralGoogle Scholar
  196. Uemura, T., Ueda, T., Ohniwa, R.L., Nakano, A., Takeyasu, K., and Sato, M.H. (2004). Systematic analysis of SNARE molecules in Arabidopsis: Dissection of the post-Golgi network in plant cells. Cell Struct Funct 29, 49–65.PubMedCrossRefPubMedCentralGoogle Scholar
  197. Uemura, T., Suda, Y., Ueda, T., and Nakano, A. (2014). Dynamic behavior of the trans-Golgi network in root tissues of Arabidopsis revealed by super-resolution live imaging. Plant Cell Physiol 55, 694–703.PubMedCrossRefPubMedCentralGoogle Scholar
  198. Uemura, T., Nakano, R.T., Takagi, J., Wang, Y., Kramer, K., Finkemeier, I., Nakagami, H., Tsuda, K., Ueda, T., Schulze-Lefert, P., et al. (2019). A Golgi-released subpopulation of the trans-Golgi network mediates protein secretion in Arabidopsis. Plant Physiol 179, 519–532.PubMedCrossRefPubMedCentralGoogle Scholar
  199. Ullrich, O., Reinsch, S., Urbé, S., Zerial, M., and Parton, R.G. (1996). Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135, 913–924.PubMedCrossRefPubMedCentralGoogle Scholar
  200. Valencia, J.P., Goodman, K., and Otegui, M.S. (2016). Endocytosis and endosomal trafficking in plants. Annu Rev Plant Biol 67, 309–335.CrossRefGoogle Scholar
  201. Van Damme, D., Gadeyne, A., Vanstraelen, M., Inzé, D., Van Montagu, M. C.E., De Jaeger, G., Russinova, E., and Geelen, D. (2011). Adaptin-like protein TPLATE and clathrin recruitment during plant somatic cytokinesis occurs via two distinct pathways. Proc Natl Acad Sci USA 108, 615–620.PubMedCrossRefPubMedCentralGoogle Scholar
  202. Vermeer, J.E.M., van Leeuwen, W., Tobeña-Santamaria, R., Laxalt, A.M., Jones, D.R., Divecha, N., Gadella Jr, T.W.J., and Munnik, T. (2006). Visualization of PtdIns3P dynamics in living plant cells. Plant J 47, 687–700.PubMedCrossRefPubMedCentralGoogle Scholar
  203. Vitale, A., and Hinz, G. (2005). Sorting of proteins to storage vacuoles: How many mechanisms? Trends Plant Sci 10, 316–323.PubMedCrossRefPubMedCentralGoogle Scholar
  204. Wang, H., and Jiang, L. (2011). Transient expression and analysis of fluorescent reporter proteins in plant pollen tubes. Nat Protoc 6, 419–426.PubMedCrossRefPubMedCentralGoogle Scholar
  205. Wang, H. (2016). Visualizing plant cells in a brand new way. Mol Plant 9, 633–635.PubMedCrossRefPubMedCentralGoogle Scholar
  206. Wang, H.J., Hsu, Y.W., Guo, C.L., Jane, W.N., Wang, H., Jiang, L., and Jauh, G.Y. (2017). VPS36-dependent multivesicular bodies are critical for plasmamembrane protein turnover and vacuolar biogenesis. Plant Physiol 173, 566–581.PubMedCrossRefPubMedCentralGoogle Scholar
  207. Wang, J., Li, Y., Lo, S.W., Hillmer, S., Sun, S.S.M., Robinson, D.G., and Jiang, L. (2007). Protein mobilization in germinating mung bean seeds involves vacuolar sorting receptors and multivesicular bodies. Plant Physiol 143, 1628–1639.PubMedPubMedCentralCrossRefGoogle Scholar
  208. Wang, J., Cai, Y., Miao, Y., Lam, S.K., and Jiang, L. (2009). Wortmannin induces homotypic fusion of plant prevacuolar compartments. J Exp Bot 60, 3075–3083.PubMedPubMedCentralCrossRefGoogle Scholar
  209. Wang, J., Ding, Y., Wang, J., Hillmer, S., Miao, Y., Lo, S.W., Wang, X., Robinson, D.G., and Jiang, L. (2010). EXPO, an exocyst-positive organelle distinct from multivesicular endosomes and autophagosomes, mediates cytosol to cell wall exocytosis in Arabidopsis and tobacco cells. Plant Cell 22, 4009–4030.PubMedPubMedCentralCrossRefGoogle Scholar
  210. Wang, J., Tse, Y.C., Hinz, G., Robinson, D.G., and Jiang, L. (2012). Storage globulins pass through the Golgi apparatus and multivesicular bodies in the absence of dense vesicle formation during early stages of cotyledon development in mung bean. J Exp Bot 63, 1367–1380.PubMedCrossRefGoogle Scholar
  211. Wang, J., Ding, Y., Zhuang, X., Hu, S., and Jiang, L. (2016). Protein co-localization studies: Issues and considerations. Mol Plant 9, 1221–1223.PubMedCrossRefGoogle Scholar
  212. Wang, L., Li, H., Lv, X., Chen, T., Li, R., Xue, Y., Jiang, J., Jin, B., Baluška, F., Šamaj, J., et al. (2015). Spatiotemporal dynamics of the BRI1 receptor and its regulation by membrane microdomains in living Arabidopsis cells. Mol Plant 8, 1334–1349.PubMedCrossRefGoogle Scholar
  213. Wang, P., Liang, Z., and Kang, B.H. (2019). Electron tomography of plant organelles and the outlook for correlative microscopic approaches. New Phytol 118, nph.15882.Google Scholar
  214. Wang, Q., Zhao, Y., Luo, W., Li, R., He, Q., Fang, X., Michele, R.D., Ast, C., von Wirén, N., and Lin, J. (2013). Single-particle analysis reveals shutoff control of the Arabidopsis ammonium transporter AMT1;3 by clustering and internalization. Proc Natl Acad Sci USA 110, 13204–13209.PubMedCrossRefGoogle Scholar
  215. Wang, X., Cai, Y., Wang, H., Zeng, Y., Zhuang, X., Li, B., and Jiang, L. (2014). Trans-Golgi network-located AP1 gamma adaptins mediate dileucine motif-directed vacuolar targeting in Arabidopsis. Plant Cell 26, 4102–4118.PubMedPubMedCentralCrossRefGoogle Scholar
  216. Wang, Y., Inoue, T., and Forgac, M. (2005). Subunit a of the yeast V-ATPase participates in binding of bafilomycin. J Biol Chem 280, 40481–40488.PubMedCrossRefGoogle Scholar
  217. Wu, T.M., Lin, K.C., Liau, W.S., Chao, Y.Y., Yang, L.H., Chen, S.Y., Lu, C. A., and Hong, C.Y. (2016). A set of GFP-based organelle marker lines combined with DsRed-based gateway vectors for subcellular localization study in rice (Oryza sativa L.). Plant Mol Biol 90, 107–115.PubMedCrossRefPubMedCentralGoogle Scholar
  218. Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat Protoc 2, 1565–1572.PubMedCrossRefGoogle Scholar
  219. Zhang, C., Brown, M.Q., van de Ven, W., Zhang, Z.M., Wu, B., Young, M. C., Synek, L., Borchardt, D., Harrison, R., Pan, S., et al. (2016). Endosidin2 targets conserved exocyst complex subunit EXO70 to inhibit exocytosis. Proc Natl Acad Sci USA 113, E41–E50.PubMedCrossRefGoogle Scholar
  220. Zhang, H., Zhang, L., Gao, B., Fan, H., Jin, J., Botella, M.A., Jiang, L., and Lin, J. (2011). Golgi apparatus-localized synaptotagmin 2 is required for unconventional secretion in Arabidopsis. PLoS ONE 6, e26477.PubMedPubMedCentralCrossRefGoogle Scholar
  221. Zhang, L., Zhang, H., Liu, P., Hao, H., Jin, J.B., Lin, J., and Yang, H. (2011). Arabidopsis R-SNARE proteins VAMP721 and VAMP722 are required for cell plate formation. PLoS ONE 6, e26129.PubMedPubMedCentralCrossRefGoogle Scholar
  222. Zheng, H., Kunst, L., Hawes, C., and Moore, I. (2004). A GFP-based assay reveals a role for RHD3 in transport between the endoplasmic reticulum and Golgi apparatus. Plant J 37, 398–414.PubMedCrossRefPubMedCentralGoogle Scholar
  223. Zhuang, X., Wang, H., Lam, S.K., Gao, C., Wang, X., Cai, Y., and Jiang, L. (2013). A BAR-domain protein SH3P2, which binds to phosphatidylinositol 3-phosphate and ATG8, regulates autophagosome formation in Arabidopsis. Plant Cell 25, 4596–4615.PubMedPubMedCentralCrossRefGoogle Scholar
  224. Zhuang, X., and Jiang, L. (2014). Autophagosome biogenesis in plants. Autophagy 10, 704–705.PubMedPubMedCentralCrossRefGoogle Scholar
  225. Zhuang, X., Chung, K.P., Cui, Y., Lin, W., Gao, C., Kang, B.H., and Jiang, L. (2017). ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis. Proc Natl Acad Sci USA 114, E426–E435.PubMedCrossRefPubMedCentralGoogle Scholar
  226. Zhuang, X., Chung, K.P., Luo, M., and Jiang, L. (2018). Autophagosome biogenesis and the endoplasmic reticulum: A plant perspective. Trends Plant Sci 23, 677–692.PubMedCrossRefPubMedCentralGoogle Scholar
  227. Zouhar, J., Rojo, E., and Bassham, D.C. (2009). AtVPS45 is a positive regulator of the SYP41/SYP61/VTI12 SNARE complex involved in trafficking of vacuolar cargo. Plant Physiol 149, 1668–1678.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Dongmei Zhu
    • 1
  • Mengdi Zhang
    • 1
  • Caiji Gao
    • 2
  • Jinbo Shen
    • 1
    Email author
  1. 1.State Key Laboratory of Subtropical SilvicultureZhejiang Aamp;F UniversityHangzhouChina
  2. 2.Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life SciencesSouth China Normal University (SCNU)GuangzhouChina

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