Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Trafficking to the seed protein storage vacuole

Joanne R. Ashnest A B and Anthony R. Gendall A C
+ Author Affiliations
- Author Affiliations

A Department of Animal, Plant and Soil Sciences, AgriBio, Centre for AgriBiosciences, 5 Ring Road, La Trobe University, Bundoora, Vic. 3086, Australia.

B Global Institute for Food Security, 110 Gymnasium Place, University of Saskatchewan, Saskatoon, SK, Canada.

C Corresponding author. Email: t.gendall@latrobe.edu.au

Functional Plant Biology 45(9) 895-910 https://doi.org/10.1071/FP17318
Submitted: 14 November 2017  Accepted: 17 February 2018   Published: 22 March 2018

Abstract

The processing and subcellular trafficking of seed storage proteins is a critical area of physiological, agricultural and biotechnological research. Trafficking to the lytic vacuole has been extensively discussed in recent years, without substantial distinction from trafficking to the protein storage vacuole (PSV). However, despite some overlap between these pathways, there are several examples of unique processing and machinery in the PSV pathway. Moreover, substantial new data has recently come to light regarding the important players in this pathway, in particular, the intracellular NHX proteins and their role in regulating lumenal pH. In some cases, these new data are limited to genetic evidence, with little mechanistic understanding. As such, the implications of these data in the current paradigm of PSV trafficking is perhaps yet unclear. Although it has generally been assumed that the major classes of storage proteins are trafficked via the same pathway, there is mounting evidence that the 12S globulins and 2S albumins may be trafficked independently. Advances in identification of vacuolar targeting signals, as well as an improved mechanistic understanding of various vacuolar sorting receptors, may reveal the differences in these trafficking pathways.

Additional keywords: Arabidopsis spp., globulins, seed development, seed storage protein, vacuoles.


References

Adachi M, Kanamori J, Masuda T, Yagasaki K, Kitamura K, Mikami B, Utsumi S (2003) Crystal structure of soybean 11S globulin: glycinin A3B4 homohexamer. Proceedings of the National Academy of Sciences of the United States of America 100, 7395–7400.
Crystal structure of soybean 11S globulin: glycinin A3B4 homohexamer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslOmsbs%3D&md5=2c7176455dd500a806f9b87a8a045a71CAS |

Ashnest JR, le Huynh D, Dragwidge JM, Ford BA, Gendall AR (2015) Arabidopsis intracellular NHX-type sodium-proton antiporters are required for seed storage protein processing. Plant & Cell Physiology 56, 2220–2233.
Arabidopsis intracellular NHX-type sodium-proton antiporters are required for seed storage protein processing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht12rtr%2FI&md5=9731faaa39f3c47f6e8ac823abf0aa30CAS |

Bassil E, Ohto MA, Esumi T, Tajima H, Zhu Z, Cagnac O, Belmonte M, Peleg Z, Yamaguchi T, Blumwald E (2011) The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. The Plant Cell 23, 224–239.
The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsFCmsrw%3D&md5=1de83a4498809601d54d628a633dd6e8CAS |

Carter C, Pan S, Zouhar J, Avila EL, Girke T, Raikhel NV (2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. The Plant Cell 16, 3285–3303.
The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVKlsg%3D%3D&md5=fa90ad75d25a5e5e8ccb9ad005256d2dCAS |

Chang HC, Hull M, Mellman I (2004) The J-domain protein Rme-8 interacts with Hsc70 to control clathrin-dependent endocytosis in Drosophila. Journal of Cell Biology 164, 1055–1064.
The J-domain protein Rme-8 interacts with Hsc70 to control clathrin-dependent endocytosis in Drosophila.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivVCht7g%3D&md5=30295d9a9aea2560055a14466de14bb9CAS |

Chrispeels MJ, Higgins TJ, Spencer D (1982) Assembly of storage protein oligomers in the endoplasmic reticulum and processing of the polypeptides in the protein bodies of developing pea cotyledons. Journal of Cell Biology 93, 306–313.
Assembly of storage protein oligomers in the endoplasmic reticulum and processing of the polypeptides in the protein bodies of developing pea cotyledons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XktVeltr0%3D&md5=9c52b637e4b041386dfbef379c79a12aCAS |

Cui Y, Zhao Q, Gao C, Ding Y, Zeng Y, Ueda T, Nakano A, Jiang L (2014) Activation of the Rab7 GTPase by the MON1-CCZ1 complex is essential for PVC-to-vacuole trafficking and plant growth in Arabidopsis. The Plant Cell 26, 2080–2097.
Activation of the Rab7 GTPase by the MON1-CCZ1 complex is essential for PVC-to-vacuole trafficking and plant growth in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFOhtr3E&md5=3bdb403b4bbd268dda4eb9ccdbca52ebCAS |

Ebine K, Okatani Y, Uemura T, Goh T, Shoda K, Niihama M, Morita MT, Spitzer C, Otegui MS, Nakano A, Ueda T (2008) A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. The Plant Cell 20, 3006–3021.
A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXns1Gnuw%3D%3D&md5=b80a408d14cb54d153a3a8f02c5e259fCAS |

Ebine K, Inoue T, Ito J, Ito E, Uemura T, Goh T, Abe H, Sato K, Nakano A, Ueda T (2014) Plant vacuolar trafficking occurs through distinctly regulated pathways. Current Biology 24, 1375–1382.
Plant vacuolar trafficking occurs through distinctly regulated pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpslCgsL8%3D&md5=c01d8b5030cb8160bfbcb21e520d1c21CAS |

Franke B, Mylne JS, Rosengren KJ (2018) Buried treasure: biosynthesis, structures and applications of cyclic peptides hidden in seed storage albumins. Natural Product Reports
Buried treasure: biosynthesis, structures and applications of cyclic peptides hidden in seed storage albumins.Crossref | GoogleScholarGoogle Scholar |

Fuji K, Shimada T, Takahashi H, Tamura K, Koumoto Y, Utsumi S, Nishizawa K, Maruyama N, 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. The Plant Cell 19, 597–609.
Arabidopsis vacuolar sorting mutants (green fluorescent seed) can be identified efficiently by secretion of vacuole-targeted green fluorescent protein in their seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktFGns7c%3D&md5=f522d76839e16b44da137d0ae65b1781CAS |

Fuji K, Shirakawa M, Shimono Y, Kunieda T, Fukao Y, Koumoto Y, Takahashi H, Hara-Nishimura I, Shimada T (2016) The adaptor complex AP-4 regulates vacuolar protein sorting at the trans-Golgi network by interacting with VACUOLAR SORTING RECEPTOR1. Plant Physiology 170, 211–219.
The adaptor complex AP-4 regulates vacuolar protein sorting at the trans-Golgi network by interacting with VACUOLAR SORTING RECEPTOR1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsFGmtbvE&md5=45938f5ca82224fa16369509a4bba147CAS |

Gao C, Luo M, Zhao Q, Yang R, Cui Y, Zeng Y, Xia J, Jiang L (2014) A unique plant ESCRT component, FREE1, regulates multivesicular body protein sorting and plant growth. Current Biology 24, 2556–2563.
A unique plant ESCRT component, FREE1, regulates multivesicular body protein sorting and plant growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslOrtL%2FK&md5=6ae75d024654e38a87f027aa6d736bcbCAS |

Gao C, Zhuang X, Cui Y, Fu X, He Y, Zhao Q, Zeng Y, Shen J, Luo M, Jiang L (2015) Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation. Proceedings of the National Academy of Sciences of the United States of America 112, 1886–1891.
Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVehsrw%3D&md5=ffef39013b613c2e84a5ccef1d80d341CAS |

Gershlick DC, Lousa CDM, Foresti O, Lee AJ, Pereira EA, daSilva LL, Bottanelli F, Denecke J (2014) Golgi-dependent transport of vacuolar sorting receptors is regulated by COPII, AP1, and AP4 protein complexes in tobacco. The Plant Cell 26, 1308–1329.
Golgi-dependent transport of vacuolar sorting receptors is regulated by COPII, AP1, and AP4 protein complexes in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXotV2ktbg%3D&md5=6f823b9cc64db5ff0aeea6248b851f4fCAS |

Goh T, Uchida W, Arakawa S, Ito E, Dainobu T, Ebine K, Takeuchi M, Sato K, Ueda T, Nakano A (2007) VPS9a, the common activator for two distinct types of Rab5 GTPases, is essential for the development of Arabidopsis thaliana. The Plant Cell 19, 3504–3515.
VPS9a, the common activator for two distinct types of Rab5 GTPases, is essential for the development of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXns1emsQ%3D%3D&md5=1f0f2015c904e4543bab46acee968a98CAS |

Gruis D, Schulze J, Jung R (2004) Storage protein accumulation in the absence of the vacuolar processing enzyme family of cysteine proteases. The Plant Cell 16, 270–290.
Storage protein accumulation in the absence of the vacuolar processing enzyme family of cysteine proteases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXosVektg%3D%3D&md5=060beefb8817b0da855505da71ef6410CAS |

Hegedus DD, Coutu C, Harrington M, Hope B, Gerbrandt K, Nikolov I (2015) Multiple internal sorting determinants can contribute to the trafficking of cruciferin to protein storage vacuoles. Plant Molecular Biology 88, 3–20.
Multiple internal sorting determinants can contribute to the trafficking of cruciferin to protein storage vacuoles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjt1Sgur4%3D&md5=2418e135113db5d5fc2ddda82cc38a04CAS |

Hinz G, Colanesi S, Hillmer S, Rogers JC, Robinson DG (2007) Localization of vacuolar transport receptors and cargo proteins in the Golgi apparatus of developing Arabidopsis embryos. Traffic 8, 1452–1464.
Localization of vacuolar transport receptors and cargo proteins in the Golgi apparatus of developing Arabidopsis embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFKms7vI&md5=e001d071ab0b3e71446a5c8487855447CAS |

Hou C, Tian W, Kleist T, He K, Garcia V, Bai F, Hao Y, Luan S, Li L (2014) DUF221 proteins are a family of osmosensitive calcium-permeable cation channels conserved across eukaryotes. Cell Research 24, 632–635.
DUF221 proteins are a family of osmosensitive calcium-permeable cation channels conserved across eukaryotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitlSgtL4%3D&md5=5e2d07cd02eebd521aefab8b3b79385eCAS |

Ibl V, Stoger E (2014) Live cell imaging during germination reveals dynamic tubular structures derived from protein storage vacuoles of barley aleurone cells. Plants 3, 442–457.
Live cell imaging during germination reveals dynamic tubular structures derived from protein storage vacuoles of barley aleurone cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFOksrzO&md5=b01ece7c03f1b9a9f1cfee0f512aae1aCAS |

Ichino T, Fuji K, Ueda H, Takahashi H, Koumoto Y, Takagi J, Tamura K, Sasaki R, Aoki K, Shimada T, Hara-Nishimura I (2014) GFS9/TT9 contributes to intracellular membrane trafficking and flavonoid accumulation in Arabidopsis thaliana. The Plant Journal 80, 410–423.
GFS9/TT9 contributes to intracellular membrane trafficking and flavonoid accumulation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslCjtLbO&md5=fcfe411536c48360af07e122a362373eCAS |

Kuroyanagi M, Yamada K, Hatsugai N, Kondo M, Nishimura M, Hara-Nishimura I (2005) Vacuolar processing enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana. Journal of Biological Chemistry 280, 32914–32920.
Vacuolar processing enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWiurrN&md5=29ac7e57c04459bcb4a700dd35901927CAS |

Li L, Shimada T, Takahashi H, Ueda H, Fukao Y, Kondo M, Nishimura M, Hara-Nishimura I (2006) MAIGO2 is involved in exit of seed storage proteins from the endoplasmic reticulum in Arabidopsis thaliana. The Plant Cell 18, 3535–3547.
MAIGO2 is involved in exit of seed storage proteins from the endoplasmic reticulum in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvVKru74%3D&md5=f52826ce315700643698371f4f10b718CAS |

Li L, Shimada T, Takahashi H, Koumoto Y, Shirakawa M, Takagi J, Zhao X, Tu B, Jin H, Shen Z, Han B, Jia M, Kondo M, Nishimura M, Hara-Nishimura I (2013) MAG2 and three MAG2 INTERACTING PROTEINs form an ER-localized complex to facilitate the storage protein transport in Arabidopsis thaliana. The Plant Journal 76, 781–791.
MAG2 and three MAG2 INTERACTING PROTEINs form an ER-localized complex to facilitate the storage protein transport in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVGgsrvN&md5=39d79a6a79a9893adcb47a957a3e1364CAS |

Luo F, Fong YHYH, Zeng Y, Shen J, Jiang L, Wong K-BK-B (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. The Plant Cell 26, 3693–3708.
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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFGhsLzE&md5=16b745c93823d9913316fa8f6c7d29f0CAS |

Martinière A, Desbrosses G, Sentenac H, Paris N (2013) Development and properties of genetically encoded pH sensors in plants. Frontiers in Plant Science 4, 1–6.
Development and properties of genetically encoded pH sensors in plants.Crossref | GoogleScholarGoogle Scholar |

Mazorra-Manzano MA, Tanaka T, Dee DR, Yada RY (2010) Structure-function characterization of the recombinant aspartic proteinase A1 from Arabidopsis thaliana. Phytochemistry 71, 515–523.
Structure-function characterization of the recombinant aspartic proteinase A1 from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvF2ltbk%3D&md5=784672ebd02ba080fc8c1cec467f9d51CAS |

Misas-Villamil JC, Toenges G, Kolodziejek I, Sadaghiani AM, Kaschani F, Colby T, Bogyo M, van der Hoorn RAL (2013) Activity profiling of vacuolar processing enzymes reveals a role for VPE during oomycete infection. The Plant Journal 73, 689–700.
Activity profiling of vacuolar processing enzymes reveals a role for VPE during oomycete infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXislOmurs%3D&md5=cdfc393f1ab4de069f429df7711b0d05CAS |

Mylne JS, Hara-Nishimura I, Rosengren JK (2014) Seed storage albumins: biosynthesis, trafficking and structures. Functional Plant Biology 41, 671–677.
Seed storage albumins: biosynthesis, trafficking and structures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpvV2kuro%3D&md5=1669db96a0f305e6bec256a00384704dCAS |

Nguyen T-P, Cueff G, Hegedus DD, Rajjou L, Bentsink L (2015) A role for seed storage proteins in Arabidopsis seed longevity. Journal of Experimental Botany 66, 6399–6413.
A role for seed storage proteins in Arabidopsis seed longevity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVOgtbvL&md5=663cf9f0d2f73e4273c335994de0ed73CAS |

Occhialini A, Marc-Martin S, Gouzerh G, Hillmer S, Neuhaus J-M (2018) RMR (receptor membrane RING-H2) type 1 and 2 show different promoter activities and subcellular localizations in Arabidopsis thaliana. Plant Science 266, 9–18.
RMR (receptor membrane RING-H2) type 1 and 2 show different promoter activities and subcellular localizations in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhslenurrJ&md5=9645db82db9c2f566af90ec410beb08fCAS |

Otegui MS, Herder R, Schulze J, Jung R, Staehelin LA (2006) The proteolytic processing of seed storage proteins in Arabidopsis embryo cells starts in the multivesicular bodies. The Plant Cell 18, 2567–2581.
The proteolytic processing of seed storage proteins in Arabidopsis embryo cells starts in the multivesicular bodies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1ejurvO&md5=dda1e87a72be59c2da50f4728c11648bCAS |

Park M, Lee D, Lee G-J, Hwang I (2005) AtRMR1 functions as a cargo receptor for protein trafficking to the protein storage vacuole. Journal of Cell Biology 170, 757–767.
AtRMR1 functions as a cargo receptor for protein trafficking to the protein storage vacuole.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXps1yqu7o%3D&md5=ab08e670eb0b9f96826a332ce8dfd482CAS |

Pereira C, Pereira S, Satiat-Jeunemaitre B, Pissarra J (2013) Cardosin A contains two vacuolar sorting signals using different vacuolar routes in tobacco epidermal cells. The Plant Journal 76, 87–100.
Cardosin A contains two vacuolar sorting signals using different vacuolar routes in tobacco epidermal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFalu7rP&md5=fe95b1772ac00510c1df0ef6294b748eCAS |

Pourcher M, Santambrogio M, Thazar N, Thierry A-MM, Fobis-Loisy I, Miège C, Jaillais Y, Gaude T, Miege C (2010) Analyses of sorting nexins reveal distinct retromer-subcomplex functions in development and protein sorting in Arabidopsis thaliana. The Plant Cell 22, 3980–3991.
Analyses of sorting nexins reveal distinct retromer-subcomplex functions in development and protein sorting in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFGrt74%3D&md5=db0c7f9b787e0916376f891a44ae5b96CAS |

Ramalho-Santos M, Pissarra J, Veríssimo P, Pereira S, Salema R, Pires E, Faro CJ (1997) Cardosin A, an abundant aspartic proteinase, accumulates in protein storage vacuoles in the stigmatic papillae of Cynara cardunculus L. Planta 203, 204–212.
Cardosin A, an abundant aspartic proteinase, accumulates in protein storage vacuoles in the stigmatic papillae of Cynara cardunculus L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmvVams7w%3D&md5=7d0397a66fe6bb1aef82a15983cafdc2CAS |

Reguera M, Bassil E, Tajima H, Wimmer M, Chanoca A, Otegui MS, Paris N, Blumwald E (2015) pH regulation by NHX-type antiporters is required for receptor-mediated protein trafficking to the vacuole in Arabidopsis. The Plant Cell 27, 1200–1217.
pH regulation by NHX-type antiporters is required for receptor-mediated protein trafficking to the vacuole in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXosFSjtbc%3D&md5=02fa35c2e396ae1ea4d97be08d609f3cCAS |

Robinson MS (2015) Forty years of clathrin-coated vesicles. Traffic 16, 1210–1238.
Forty years of clathrin-coated vesicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhslOrs7jJ&md5=4ec53b189d9e0cd5eca3ac6b95d0b388CAS |

Robinson DG, Neuhaus J-MM (2016) Receptor-mediated sorting of soluble vacuolar proteins: myths, facts, and a new model. Journal of Experimental Botany 67, 4435–4449.
Receptor-mediated sorting of soluble vacuolar proteins: myths, facts, and a new model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXjs1yqt7g%3D&md5=b58478706ace456fcb427cfe18614381CAS |

Sakurai HT, Inoue T, Nakano A, Ueda T (2016) ENDOSOMAL RAB EFFECTOR WITH PX-DOMAIN, an interacting partner of RAB5 GTPases, regulates membrane trafficking to protein storage vacuoles in Arabidopsis. The Plant Cell 28, 1490–1503.
ENDOSOMAL RAB EFFECTOR WITH PX-DOMAIN, an interacting partner of RAB5 GTPases, regulates membrane trafficking to protein storage vacuoles in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhslCqurnO&md5=d856419029156eb35e9816d763705f87CAS |

Sanmartín M, Ordóñez A, Sohn EJ, Robert S, Sánchez-Serrano JJ, Surpin M, Raikhel NV, Rojo E (2007) Divergent functions of VTI12 and VTI11 in trafficking to storage and lytic vacuoles in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 104, 3645–3650.
Divergent functions of VTI12 and VTI11 in trafficking to storage and lytic vacuoles in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Shimada T, Fuji K, Tamura K, Kondo M, Nishimura M, Hara-Nishimura I (2003) Vacuolar sorting receptor for seed storage proteins in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 100, 16095–16100.
Vacuolar sorting receptor for seed storage proteins in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVGjtQ%3D%3D&md5=15f17e137fccef9e60c76b7bee98a4d5CAS |

Shimada T, Koumoto Y, Li L, Yamazaki M, Kondo M, Nishimura M, Hara-Nishimura I (2006) AtVPS29, a putative component of a retromer complex, is required for the efficient sorting of seed storage proteins. Plant & Cell Physiology 47, 1187–1194.
AtVPS29, a putative component of a retromer complex, is required for the efficient sorting of seed storage proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFCgur7L&md5=0ba83d72277a0ca1faba8456c0bb6696CAS |

Shirakawa M, Ueda H, Shimada TLT, Koumoto Y, Kondo M, Takahashi T, Okuyama Y, Nishimura M, Hara-Nishimura I (2010) Arabidopsis Qa-SNARE SYP2 proteins localized to different subcellular regions function redundantly in vacuolar protein sorting and plant development. The Plant Journal 64, 924–935.
Arabidopsis Qa-SNARE SYP2 proteins localized to different subcellular regions function redundantly in vacuolar protein sorting and plant development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisFGrtA%3D%3D&md5=a03de957c351d0f82f412611a44bd392CAS |

Silady RA, Ehrhardt DW, Jackson K, Faulkner C, Oparka K, Somerville CR (2008) The GRV2/RME-8 protein of Arabidopsis functions in the late endocytic pathway and is required for vacuolar membrane flow. The Plant Journal 53, 29–41.
The GRV2/RME-8 protein of Arabidopsis functions in the late endocytic pathway and is required for vacuolar membrane flow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXns1GmsQ%3D%3D&md5=5c83f4c7b7c94ef729b62a6f1db0177bCAS |

Sohn EJ, Rojas-pierce M, Pan S, Carter C, Serrano-mislata A, Maduen F, Rojo E, Surpin M, Raikhel NV (2007) The shoot meristem identity gene TFL1 is involved in flower development and trafficking to the protein storage vacuole. Proceedings of the National Academy of Sciences of the United States of America 104, 18801–18806.
The shoot meristem identity gene TFL1 is involved in flower development and trafficking to the protein storage vacuole.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtl2lu73L&md5=2b764e52bdf5f7092747ea8f049fbdf8CAS |

Takagi J, Renna L, Takahashi H, Koumoto Y, Tamura K, Stefano G, Fukao Y, Kondo M, Nishimura M, Shimada T, Brandizzi F, Hara-Nishimura I (2013) MAIGO5 functions in protein export from Golgi-associated endoplasmic reticulum axit sites in Arabidopsis. The Plant Cell 25, 4658–4675.
MAIGO5 functions in protein export from Golgi-associated endoplasmic reticulum axit sites in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVOqsrs%3D&md5=714061662352cd2b0eaa2176ae71d1f3CAS |

Takahashi H, Saito Y, Kitagawa T, Morita S, Masumura T, 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 Physiology 46, 245–249.
A novel vesicle derived directly from endoplasmic reticulum is involved in the transport of vacuolar storage proteins in rice endosperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1eqtb8%3D&md5=22193bf1f036cdc27dc6dceb43682684CAS |

Takahashi H, Tamura K, Takagi J, Koumoto Y, Hara-Nishimura I, Shimada T (2010) MAG4/Atp115 is a Golgi-localized tethering factor that mediates efficient anterograde transport in Arabidopsis. Plant & Cell Physiology 51, 1777–1787.
MAG4/Atp115 is a Golgi-localized tethering factor that mediates efficient anterograde transport in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1OgsrfK&md5=e5e6eb30aa817c2cf5b42d494776cecaCAS |

Tamura K, Takahashi H, Kunieda T, Fuji K, Shimada T, Hara-Nishimura I (2007) Arabidopsis KAM2/GRV2 is required for proper endosome formation and functions in vacuolar sorting and determination of the embryo growth axis. The Plant Cell 19, 320–332.
Arabidopsis KAM2/GRV2 is required for proper endosome formation and functions in vacuolar sorting and determination of the embryo growth axis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtFyntLs%3D&md5=f359ce007b80a84242ad15b3a1325b3bCAS |

Teh OK, Hatsugai N, Tamura K, Fuji K, Tabata R, Yamaguchi K, Shingenobu S, Yamada M, Hasebe M, Sawa S, Shimada T, Hara-Nishimura I (2015) BEACH-domain proteins act together in a cascade to mediate vacuolar protein trafficking and disease resistance in Arabidopsis. Molecular Plant 8, 389–398.
BEACH-domain proteins act together in a cascade to mediate vacuolar protein trafficking and disease resistance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmtValtro%3D&md5=f2e9cd8223a6c08ee83fe0560f61f826CAS |

Tse YC, Wang J, Miao Y, Jiang L (2007) Biogenesis of the compound seed protein storage vacuole. In ‘Seeds: biology, development and ecology’. (Eds SW Adkins, S Ashmore, S Navre) pp. 112–119. (CABI: Wallingford, UK)

Uemura T, Ueda T (2014) Plant vacuolar trafficking driven by RAB and SNARE proteins. Current Opinion in Plant Biology 22, 116–121.
Plant vacuolar trafficking driven by RAB and SNARE proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsl2hurrE&md5=9a6d0bd12f0a4e0a8bd2be1aa5321b8bCAS |

Watanabe E, Shimada T, Tamura K, Matsushima R, Koumoto Y, Nishimura M, Hara-Nishimura I (2004) An ER-localized form of PV72, a seed-specific vacuolar sorting receptor, interferes the transport of an NPIR-containing proteinase in Arabidopsis leaves. Plant & Cell Physiology 45, 9–17.
An ER-localized form of PV72, a seed-specific vacuolar sorting receptor, interferes the transport of an NPIR-containing proteinase in Arabidopsis leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsVajtQ%3D%3D&md5=981575fc4560879a71e851a106136e2eCAS |

Wen L, Fukuda M, Sunada M, Ishino S, Ishino Y, Okita TW, Ogawa M, Ueda T, Kumamaru T (2015) Guanine nucleotide exchange factor 2 for Rab5 proteins coordinated with GLUP6/GEF regulates the intracellular transport of the proglutelin from the Golgi apparatus to the protein storage vacuole in rice endosperm. Journal of Experimental Botany 66, 6137–6147.
Guanine nucleotide exchange factor 2 for Rab5 proteins coordinated with GLUP6/GEF regulates the intracellular transport of the proglutelin from the Golgi apparatus to the protein storage vacuole in rice endosperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVOgtL3O&md5=fa0f5391462f6d91ff39ae2ddd9ce20fCAS |

Wu X, Ebine K, Ueda T, Qiu Q-S (2016) AtNHX5 and AtNHX6 are required for the subcellular localization of the SNARE complex that mediates the trafficking of seed storage proteins in Arabidopsis. PLoS One 11, e0151658
AtNHX5 and AtNHX6 are required for the subcellular localization of the SNARE complex that mediates the trafficking of seed storage proteins in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Xiang L, Etxeberria E, Van den Ende W (2013) Vacuolar protein sorting mechanisms in plants. The FEBS Journal 280, 979–993.
Vacuolar protein sorting mechanisms in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXis1Wmtb4%3D&md5=457b85033007c1b7e57b176fff65b997CAS |

Yamazaki M, Shimada T, Takahashi H, Tamura K, Kondo M, Nishimura M, Hara-Nishimura I (2008) Arabidopsis VPS35, a retromer component, is required for vacuolar protein sorting and involved in plant growth and leaf senescence. Plant & Cell Physiology 49, 142–156.
Arabidopsis VPS35, a retromer component, is required for vacuolar protein sorting and involved in plant growth and leaf senescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVWltbc%3D&md5=cfd060970218ccebe89e4f49c9668209CAS |

Zelazny E, Santambrogio M, Pourcher M, Chambrier P, Berne-Dedieu A, Fobis-Loisy I, Miège C, Jaillais Y, Gaude T (2013) Mechanisms governing the endosomal membrane recruitment of the core retromer in Arabidopsis. Journal of Biological Chemistry 288, 8815–8825.
Mechanisms governing the endosomal membrane recruitment of the core retromer in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXkvF2rsLc%3D&md5=a4162306fe94e077295c5b4c59b08c26CAS |

Zouhar J, Muñoz A, Rojo E, Munoz A, Rojo E (2010) Functional specialization within the vacuolar sorting receptor family: VSR1, VSR3 and VSR4 sort vacuolar storage cargo in seeds and vegetative tissues. The Plant Journal 64, 577–588.
Functional specialization within the vacuolar sorting receptor family: VSR1, VSR3 and VSR4 sort vacuolar storage cargo in seeds and vegetative tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFygsbrK&md5=2f969d81194f83815d1cbeb599224adcCAS |

Zwiewka M, Feraru E, Möller B, Hwang I, Feraru MI, Kleine-Vehn J, Weijers D, Friml J (2011) The AP-3 adaptor complex is required for vacuolar function in Arabidopsis. Cell Research 21, 1711–1722.
The AP-3 adaptor complex is required for vacuolar function in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKms7nF&md5=753d4fc734ea62328c875c4b6f27db65CAS |