Abstract
Seed storage proteins (SSPs) have been studied for more than 250 years because of their nutritional value and their impact on the use of grain in food processing. More recently, the use of seeds for the production of recombinant proteins has rekindled interest in the behavior of SSPs and the question how they are able to accumulate as stable storage reserves. Seed cells produce vast amounts of SSPs with different subcellular destinations creating an enormous logistic challenge for the endomembrane system. Seed cells contain several different storage organelles including the complex and dynamic protein storage vacuoles (PSVs) and other protein bodies (PBs) derived from the endoplasmic reticulum (ER). Storage proteins destined for the PSV may pass through or bypass the Golgi, using different vesicles that follow different routes through the cell. In addition, trafficking may depend on the plant species, tissue and developmental stage, showing that the endomembrane system is capable of massive reorganization. Some SSPs contain sorting signals or interact with membranes or with other proteins en route in order to reach their destination. The ability of SSPs to form aggregates is particularly important in the formation or ER-derived PBs, a mechanism that occurs naturally in response to overloading with proteins that cannot be transported and that can be used to induce artificial storage bodies in vegetative tissues. In this review, we summarize recent findings that provide insight into the formation, function, and fate of storage organelles and describe tools that can be used to study them.
Similar content being viewed by others
Abbreviations
- At-ELP:
-
Arabidopsis thaliana EGF receptor-like protein
- CCV:
-
Clathrin-coated vesicle
- DIP:
-
Dark intrinsic protein
- DV:
-
Dense vesicle
- ER:
-
Endoplasmic reticulum
- ERvt:
-
ER to vacuole trafficking
- GFP:
-
Green fluorescent protein
- GPA1:
-
G-protein alpha subunit 1
- HMW:
-
High molecular weight
- i-ER:
-
Induced ER (body)
- KV:
-
KDEL-tailed cysteine proteinase-accumulating vesicle
- LV:
-
Lytic vacuole
- MBP:
-
Maltose binding protein
- MVB:
-
Multivesicular body
- PAC:
-
Precursor-accumulating (vesicle)
- PB:
-
ER-derived protein bodies
- PCD:
-
Programmed cell death
- PPI:
-
Peptidyl-prolyl cis–trans isomerase
- PSV:
-
Protein storage vacuole
- PVC:
-
Prevacuolar compartment
- rER:
-
Rough endoplasmic reticulum
- RMR:
-
Receptor homology-transmembrane-RING H2
- RNAi:
-
RNA interference
- SBP:
-
Sucrose-binding protein
- SH-EP:
-
Sulfhydryl endopeptidase
- SNARE:
-
Soluble N-ethylmaleimide-sensitive-factor attachment receptor
- SSP:
-
Seed storage protein
- TGN:
-
Trans-Golgi network
- TIP:
-
Tonoplast intrinsic protein
- VAMP:
-
Vesicle associated membrane protein
- VSR:
-
Vacuole sorting receptor
References
Abhary M, Siritunga D, Stevens G, Taylor NJ, Fauquet CM (2011) Transgenic biofortification of the starchy staple cassava (Manihot esculenta) generates a novel sink for protein. PLoS One 6(1):e16256
Abranches R, Arcalis E, Marcel S, Altmann F, Ribeiro-Pedro M, Rodriguez J, Stoger E (2008) Functional specialization of Medicago truncatula leaves and seeds does not affect the subcellular localization of a recombinant protein. Planta 227(3):649–658
Altpeter F, Baisakh N, Beachy R, Bock R, Capell T, Christou P, Daniell H, Datta K, Datta S, Dix PJ, Fauquet C, Huang N, Kohli A, Mooibroek H, Nicholson L, Nguyen TT, Nugent G, Raemakers K, Romano A, Somers DA, Stoger E, Taylor N, Visser R (2005) Particle bombardment and the genetic enhancement of crops: myths and realities. Mol Breed 15:305–327
Angelovici R, Galili G, Fernie AR, Fait A (2010) Seed desiccation: a bridge between maturation and germination. Trends Plant Sci 15(4):211–218
Arcalis E, Marcel S, Altmann F, Kolarich D, Drakakaki G, Fischer R, Christou P, Stoger E (2004) Unexpected deposition patterns of recombinant proteins in post-endoplasmic reticulum compartments of wheat endosperm. Plant Physiol 136(3):3457–3466
Arcalis E, Stadlmann J, Marcel S, Drakakaki G, Winter V, Rodriguez J, Fischer R, Altmann F, Stoger E (2010) The changing fate of a secretory glycoprotein in developing maize endosperm. Plant Physiol 153(2):693–702
Avila EL, Zouhar J, Agee AE, Carter DG, Chary SN, Raikhel NV (2003) Tools to study plant organelle biogenesis. Point mutation lines with disrupted vacuoles and high-speed confocal screening of green fluorescent protein-tagged organelles. Plant Physiol 133(4):1673–1676
Bagga S, Adams H, Kemp JD, Sengupta-Gopalan C (1995) Accumulation of 15-kilodalton zein in novel protein bodies in transgenic tobacco. Plant Physiol 107(1):13–23
Bagga S, Adams HP, Rodriguez FD, Kemp JD, Sengupta-Gopalan C (1997) Coexpression of the maize delta-zein and beta-zein genes results in stable accumulation of delta-zein in endoplasmic reticulum-derived protein bodies formed by beta-zein. Plant Cell 9(9):1683–1696
Banc A, Desbat B, Renard D, Popineau Y, Mangavel C, Navailles L (2009) Exploring the interactions of gliadins with model membranes: effect of confined geometry and interfaces. Biopolymers 91(8):610–622
Bassham DC, Raikhel NV (2000) Unique features of the plant vacuolar sorting machinery. Curr Opin Cell Biol 12(4):491–495
Bednarek SY, Raikhel NV (1992) Intracellular trafficking of secretory proteins. Plant Mol Biol 20(1):133–150
Carlson JA, Rogers BB, Sifers RN, Finegold MJ, Clift SM, DeMayo FJ, Bullock DW, Woo SL (1989) Accumulation of PiZ alpha 1-antitrypsin causes liver damage in transgenic mice. J Clin Invest 83(4):1183–1190
Coleman CE, Herman EM, Takasaki K, Larkins BA (1996) The maize gamma-zein sequesters alpha-zein and stabilizes its accumulation in protein bodies of transgenic tobacco endosperm. Plant Cell 8(12):2335–2345
Coleman CE, Yoho PR, Escobar S, Ogawa M (2004) The accumulation of alpha-zein in transgenic tobacco endosperm is stabilized by co-expression of beta-zein. Plant Cell Physiol 45(7):864–871
Conley AJ, Joensuu JJ, Richman A, Menassa R (2011) Protein body-inducing fusions for high-level production and purification of recombinant proteins in plants. Plant Biotechnol J (in press)
Crofts AJ, Washida H, Okita TW, Ogawa M, Kumamaru T, Satoh H (2004) Targeting of proteins to endoplasmic reticulum-derived compartments in plants. The importance of RNA localization. Plant Physiol 136(3):3414–3419
Crofts AJ, Crofts N, Whitelegge JP, Okita TW (2010) Isolation and identification of cytoskeleton-associated prolamine mRNA binding proteins from developing rice seeds. Planta 231(6):1261–1276
Drakakaki G, Marcel S, Arcalis E, Altmann F, Gonzalez-Melendi P, Fischer R, Christou P, Stoger E (2006) The intracellular fate of a recombinant protein is tissue dependent. Plant Physiol 141(2):578–586
Ebine K, Okatani Y, Uemura T, Goh T, Shoda K, Niihama M, Morita MT, Spitzer C, Otegui MS, Nakano A, Ueda T (2008) A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. Plant Cell 20(11):3006–3021
Floss DM, Sack M, Arcalis E, Stadlmann J, Quendler H, Rademacher T, Stoger E, Scheller J, Fischer R, Conrad U (2009) Influence of elastin-like peptide fusions on the quantity and quality of a tobacco-derived human immunodeficiency virus-neutralizing antibody. Plant Biotechnol J 7(9):899–913
Frame BR, Shou H, Chikwamba RK, Zhang Z, Xiang C, Fonger TM, Pegg SE, Li B, Nettleton DS, Pei D, Wang K (2002) Agrobacterium tumefaciens-mediated transformation of maize embryos using a standard binary vector system. Plant Physiol 129(1):13–22
Frigerio L, de Virgilio M, Prada A, Faoro F, Vitale A (1998) Sorting of phaseolin to the vacuole is saturable and requires a short C-terminal peptide. Plant Cell 10(6):1031–1042
Frigerio L, Hinz G, Robinson DG (2008) Multiple vacuoles in plant cells: rule or exception? Traffic 9(10):1564–1570
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. Plant Cell 19(2):597–609
Galili G (2004) ER-derived compartments are formed by highly regulated processes and have special functions in plants. Plant Physiol 136(3):3411–3413
Gallie DR, Young TE (1994) The regulation of gene expression in transformed maize aleurone and endosperm protoplasts. Analysis of promoter activity, intron enhancement, and mRNA untranslated regions on expression. Plant Physiol 106(3):929–939
Gattolin S, Sorieul M, Frigerio L (2010) 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(1):180–189
Geetha KB, Lending CR, Lopes MA, Wallace JC, Larkins BA (1991) Opaque-2 modifiers increase gamma-zein synthesis and alter its spatial distribution in maize endosperm. Plant Cell 3(11):1207–1219
Geli MI, Torrent M, Ludevid D (1994) Two structural domains mediate two sequential events in [gamma]-Zein targeting: protein endoplasmic reticulum retention and protein body formation. Plant Cell 6(12):1911–1922
Gietl C, Schmid M (2001) Ricinosomes: an organelle for developmentally regulated programmed cell death in senescing plant tissues. Naturwissenschaften 88:49–58
Greenwood JS, Helm M, Gietl C (2005) Ricinosomes and endosperm transfer cell structure in programmed cell death of the nucellus during Ricinus seed development. Proc Natl Acad Sci USA 102(6):2238–2243
Hara-Nishimura II, Shimada T, Hatano K, Takeuchi Y, Nishimura M (1998) Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles. Plant Cell 10(5):825–836
Herman EM (2008) Endoplasmic reticulum bodies: solving the insoluble. Curr Opin Plant Biol 11(6):672–679
Herman EM, Larkins BA (1999) Protein storage bodies and vacuoles. Plant Cell 11(4):601–614
Herman E, Schmidt M (2004) Endoplasmic reticulum to vacuole trafficking of endoplasmic reticulum bodies provides an alternate pathway for protein transfer to the vacuole. Plant Physiol 136(3):3440–3446
Hillmer S, Movafeghi A, Robinson DG, Hinz G (2001) Vacuolar storage proteins are sorted in the cis-cisternae of the pea cotyledon Golgi apparatus. J Cell Biol 152(1):41–50
Hinz G, Hillmer S, Baumer M, Hohl II (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(8):1509–1524
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(10):1452–1464
Hoh B, Hinz G, Jeong BK, Robinson DG (1995) Protein storage vacuoles form de novo during pea cotyledon development. J Cell Sci 108(Pt 1):299–310
Hohl I, Robinson DG, Chrispeels MJ, Hinz G (1996) Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat. J Cell Sci 109(Pt 10):2539–2550
Holding DR, Otegui MS, Li B, Meeley RB, Dam T, Hunter BG, Jung R, Larkins BA (2007) The maize floury1 gene encodes a novel endoplasmic reticulum protein involved in zein protein body formation. Plant Cell 19(8):2569–2582
Holkeri H, Vitale A (2001) Vacuolar sorting determinants within a plant storage protein trimer act cumulatively. Traffic 2(10):737–741
Hsu SM, Hsu PL, McMillan PN, Fanger H (1982) Russell bodies: a light and electron microscopic immunoperoxidase study. Am J Clin Pathol 77(1):26–31
Hunter BG, Beatty MK, Singletary GW, Hamaker BR, Dilkes BP, Larkins BA, Jung R (2002) Maize opaque endosperm mutations create extensive changes in patterns of gene expression. Plant Cell 14(10):2591–2612
Hunter PR, Craddock CP, Di Benedetto S, Roberts LM, Frigerio L (2007) Fluorescent reporter proteins for the tonoplast and the vacuolar lumen identify a single vacuolar compartment in Arabidopsis cells. Plant Physiol 145(4):1371–1382
Jiang L, Phillips TE, Rogers SW, Rogers JC (2000) Biogenesis of the protein storage vacuole crystalloid. J Cell Biol 150(4):755–770
Jiang L, Phillips TE, Hamm CA, Drozdowicz YM, Rea PA, Maeshima M, Rogers SW, Rogers JC (2001) The protein storage vacuole: a unique compound organelle. J Cell Biol 155(6):991–1002
Joensuu JJ, Conley AJ, Lienemann M, Brandle JE, Linder MB, Menassa R (2010) Hydrophobin fusions for high-level transient protein expression and purification in Nicotiana benthamiana. Plant Physiol 152(2):622–633
Jurgens G (2004) Membrane trafficking in plants. Annu Rev Cell Dev Biol 20:481–504
Kaloff CR, Haas IG (1995) Coordination of immunoglobulin chain folding and immunoglobulin chain assembly is essential for the formation of functional IgG. Immunity 2(6):629–637
Kawakatsu T, Hirose S, Yasuda H, Takaiwa F (2010) Reducing rice seed storage protein accumulation leads to changes in nutrient quality and storage organelle formation. Plant Physiol 154(4):1842–1854
Kim CS, Woo Ym YM, Clore AM, Burnett RJ, Carneiro NP, Larkins BA (2002) Zein protein interactions, rather than the asymmetric distribution of zein mRNAs on endoplasmic reticulum membranes, influence protein body formation in maize endosperm. Plant Cell 14(3):655–672
Kim CS, Hunter BG, Kraft J, Boston RS, Yans S, Jung R, Larkins BA (2004) A defective signal peptide in a 19-kD alpha-zein protein causes the unfolded protein response and an opaque endosperm phenotype in the maize De*-B30 mutant. Plant Physiol 134(1):380–387
Kinney AJ, Jung R, Herman EM (2001) Cosuppression of the alpha subunits of beta-conglycinin in transgenic soybean seeds induces the formation of endoplasmic reticulum-derived protein bodies. Plant Cell 13(5):1165–1178
Kirsch T, Paris N, Butler JM, Beevers L, Rogers JC (1994) Purification and initial characterization of a potential plant vacuolar targeting receptor. Proc Natl Acad Sci USA 91(8):3403–3407
Kogan MJ, Lopez O, Cocera M, Lopez-Iglesias C, De La Maza A, Giralt E (2004) Exploring the interaction of the surfactant N-terminal domain of gamma-Zein with soybean phosphatidylcholine liposomes. Biopolymers 73(2):258–268
Larre C, Penninck S, Bouchet B, Lollier V, Tranquet O, Denery-Papini S, Guillon F, Rogniaux H (2010) Brachypodium distachyon grain: identification and subcellular localization of storage proteins. J Exp Bot 61(6):1771–1783
Lending CR, Larkins BA (1989) Changes in the zein composition of protein bodies during maize endosperm development. Plant Cell 1(10):1011–1023
Lending CR, Larkins BA (1992) Effect of the floury-2 locus on protein body formation during maize endosperm development. Protoplasma 171:123–133
Levanony H, Rubin R, Altschuler Y, Galili G (1992) Evidence for a novel route of wheat storage proteins to vacuoles. J Cell Biol 119(5):1117–1128
Li X, Wu Y, Zhang DZ, Gillikin JW, Boston RS, Franceschi VR, Okita TW (1993) Rice prolamine protein body biogenesis: a BiP-mediated process. Science 262(5136):1054–1056
Llop-Tous I, Madurga S, Giralt E, Marzabal P, Torrent M, Ludevid MD (2010) Relevant elements of a maize gamma-zein domain involved in protein body biogenesis. J Biol Chem 285(46):35633–35644
Loos A, Van Droogenbroeck B, Hillmer S, Grass J, Pabst M, Castilho A, Kunert R, Liang M, Arcalis E, Robinson DG, Depicker A, Steinkellner H (2011) Expression of antibody fragments with a controlled N-glycosylation pattern and induction of ER-derived vesicles in seeds of Arabidopsis thaliana. Plant Physiol (in press)
Ludevid Mugica MD, Bastida Virgili M, Llompart Royo B, Marzabal Luna P, Torrent Quetglas M (2007) Production of proteins. European Patent Application. Publication number EP1819725, published on August 22, 2007
Mainieri D, Rossi M, Archinti M, Bellucci M, De Marchis F, Vavassori S, Pompa A, Arcioni S, Vitale A (2004) Zeolin. A new recombinant storage protein constructed using maize gamma-zein and bean phaseolin. Plant Physiol 136(3):3447–3456
Matsushima R, Hayashi Y, Yamada K, Shimada T, Nishimura M, Hara-Nishimura I (2003) The ER body, a novel endoplasmic reticulum-derived structure in Arabidopsis. Plant Cell Physiol 44(7):661–666
Mattioli L, Anelli T, Fagioli C, Tacchetti C, Sitia R, Valetti C (2006) ER storage diseases: a role for ERGIC-53 in controlling the formation and shape of Russell bodies. J Cell Sci 119(Pt 12):2532–2541
Mohanty A, Luo A, DeBlasio S, Ling X, Yang Y, Tuthill DE, Williams KE, Hill D, Zadrozny T, Chan A, Sylvester AW, Jackson D (2009a) Advancing cell biology and functional genomics in maize using fluorescent protein-tagged lines. Plant Physiol 149(2):601–605
Mohanty A, Yang Y, Luo A, Sylvester AW, Jackson D (2009b) Methods for generation and analysis of fluorescent protein-tagged maize lines. Methods Mol Biol 526:71–89
Munro S, Pelham HR (1986) An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46(2):291–300
Muntz K (1998) Deposition of storage proteins. Plant Mol Biol 38(1–2):77–99
Neuhaus, JM, Paris N. (2006) Plant Vacuoles: from Biogenesis to Function. Plant Cell Monographs 1/2006, 63–82. doi:10.1007/7089_005
Nicholson L, Gonzalez-Melendi P, van Dolleweerd C, Tuck H, Perrin Y, Ma JK, Fischer R, Christou P, Stoger E (2005) A recombinant multimeric immunoglobulin expressed in rice shows assembly-dependent subcellular localization in endosperm cells. Plant Biotechnol J 3(1):115–127
Niemes S, Langhans M, Viotti C, Scheuring D, San Wan Yan M, Jiang L, Hillmer S, Robinson DG, Pimpl P (2010a) Retromer recycles vacuolar sorting receptors from the trans-Golgi network. Plant J 61(1):107–121
Niemes S, Labs M, Scheuring D, Krueger F, Langhans M, Jesenofsky B, Robinson DG, Pimpl P (2010b) Sorting of plant vacuolar proteins is initiated in the ER. Plant J 62(4):601–614
Oda Y, Higaki T, Hasezawa S, Kutsuna N (2009) Chapter 3. New insights into plant vacuolar structure and dynamics. Int Rev Cell Mol Biol 277:103–135
Okamoto T, Shimada T, Hara-Nishimura I, Nishimura M, Minamikawa T (2003) C-terminal KDEL sequence of a KDEL-tailed cysteine proteinase (sulfhydryl-endopeptidase) is involved in formation of KDEL vesicle and in efficient vacuolar transport of sulfhydryl-endopeptidase. Plant Physiol 132(4):1892–1900
Olbrich A, Hillmer S, Hinz G, Oliviusson P, Robinson DG (2007) Newly formed vacuoles in root meristems of barley and pea seedlings have characteristics of both protein storage and lytic vacuoles. Plant Physiol 145(4):1383–1394
Onda Y, Kumamaru T, Kawagoe Y (2009) ER membrane-localized oxidoreductase Ero1 is required for disulfide bond formation in the rice endosperm. Proc Natl Acad Sci USA 106(33):14156–14161
Onda Y, Nagamine A, Sakurai M, Kumamaru T, Ogawa M, Kawagoe Y (2011) Distinct roles of protein disulfide isomerase and p5 sulfhydryl oxidoreductases in multiple pathways for oxidation of structurally diverse storage proteins in rice. Plant Cell 23(1):210–223
Otegui MS, Mastronarde DN, Kang BH, Bednarek SY, Staehelin LA (2001) Three-dimensional analysis of syncytial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell 13(9):2033–2051
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. Plant Cell 18(10):2567–2581
Paris N, Neuhaus JM (2002) BP-80 as a vacuolar sorting receptor. Plant Mol Biol 50(6):903–914
Park M, Lee D, Lee GJ, Hwang I (2005) AtRMR1 functions as a cargo receptor for protein trafficking to the protein storage vacuole. J Cell Biol 170(5):757–767
Park JH, Oufattole M, Rogers JC (2007) Golgi-mediated vacuolar sorting in plant cells: RMR proteins are sorting receptors for the protein aggregation/membrane internalization pathway. Plant Sci 172:728–745
Pompa A, Vitale A (2006) Retention of a bean phaseolin/maize gamma-zein fusion in the endoplasmic reticulum depends on disulfide bond formation. Plant Cell 18(10):2608–2621
Rechinger KB, Simpson DJ, Svendsen I, Cameron-Mills V (1993) A role for gamma 3 hordein in the transport and targeting of prolamin polypeptides to the vacuole of developing barley endosperm. Plant J 4(5):841–853
Reyes FC, Sun B, Guo H, Gruis DF, Otegui MS (2010) Agrobacterium tumefaciens-mediated transformation of maize endosperm as a tool to study endosperm cell biology. Plant Physiol 153(2):624–631
Reyes FC, Chung T, Holding D, Jung R, Vierstra R, Otegui MS (2011) Delivery of prolamins to the protein storage vacuole in maize aleurone cells. Plant Cell 23(2):769–784
Robinson DG, Hinz G (1997) Vacuole biogenesis and protein transport to the plant vacuole: a comparison with the yeast vacuole and mammalian lysosome. Protoplasma 197:1–25
Robinson DG, Hinz G (1999) Golgi-mediated transport of seed storage proteins. Seed Sci Res 9:267–283
Robinson DG, Bäumer M, Hinz G, Hohl I (1997) Ultrastructure of the pea cotyledon Golgi apparatus: origin of dense vesicles and the action of brefeldin A. Protoplasma 200:198–209
Robinson DG, Bäumer M, Hinz G, Hohl I (1998) Vesicle transfer of storage proteins to the vacuole: The role of the Golgi apparatus and multivesicular bodies. Annual Gatersleben Research Conference No. 2, Gatersleben, ALLEMAGNE (1997) 1998, vol. 152, no 6 (118 p.) (39 ref.), pp. 659–667
Rubin R, Levanony H, Galili G (1992) Evidence for the presence of two different types of protein bodies in wheat endosperm. Plant Physiol 99(2):718–724
Russell W (1890) An address on a characteristic organism of cancer. Br Med J 2(1563):1356–1360
Saint-Jean B, Seveno-Carpentier E, Alcon C, Neuhaus JM, Paris N (2010) The cytosolic tail dipeptide Ile-Met of the pea receptor BP80 is required for recycling from the prevacuole and for endocytosis. Plant Cell 22(8):2825–2837
Saito Y, Kishida K, Takata K, Takahashi H, Shimada T, Tanaka K, Morita S, Satoh S, Masumura T (2009) A green fluorescent protein fused to rice prolamin forms protein body-like structures in transgenic rice. J Exp Bot 60(2):615–627
Samuels AL, Giddings TH Jr, Staehelin LA (1995) Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 130(6):1345–1357
Saumonneau A, Rottier K, Conrad U, Popineau Y, Gueguen J, Francin-Allami M (2011) Expression of a new chimeric protein with a highly repeated sequence in tobacco cells. Plant Cell Rep (in press)
Schmid M, Simpson D, Kalousek F, Gietl C (1998) A cysteine endopeptidase with a C-terminal KDEL motif isolated from castor bean endosperm is a marker enzyme for the ricinosome, a putative lytic compartment. Planta 206(3):466–475
Schmid M, Simpson DJ, Sarioglu H, Lottspeich F, Gietl C (2001) The ricinosomes of senescing plant tissue bud from the endoplasmic reticulum. Proc Natl Acad Sci USA 98(9):5353–5358
Segal G, Song R, Messing J (2003) A new opaque variant of maize by a single dominant RNA-interference-inducing transgene. Genetics 165(1):387–397
Segui-Simarro JM, Staehelin LA (2006) Cell cycle-dependent changes in Golgi stacks, vacuoles, clathrin-coated vesicles and multivesicular bodies in meristematic cells of Arabidopsis thaliana: a quantitative and spatial analysis. Planta 223(2):223–236
Segui-Simarro JM, Austin JR 2nd, White EA, Staehelin LA (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16(4):836–856
Sherameti I, Venus Y, Drzewiecki C, Tripathi S, Dan VM, Nitz I, Varma A, Grundler FM, Oelmuller R (2008) PYK10, a beta-glucosidase located in the endoplasmatic reticulum, is crucial for the beneficial interaction between Arabidopsis thaliana and the endophytic fungus Piriformospora indica. Plant J 54(3):428–439
Shewry PR, Napier JA, Tatham AS (1995) Seed storage proteins: structures and biosynthesis. Plant Cell 7(7):945–956
Shimada T, Kuroyanagi M, Nishimura M, 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(12):1414–1420
Shimada T, Watanabe E, Tamura K, Hayashi Y, Nishimura M, 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(10):1086–1095
Shy G, Ehler L, Herman E, Galili G (2001) Expression patterns of genes encoding endomembrane proteins support a reduced function of the Golgi in wheat endosperm during the onset of storage protein deposition. J Exp Bot 52(365):2387–2388
Sparkes IA, Frigerio L, Tolley N, Hawes C (2009) The plant endoplasmic reticulum: a cell-wide web. Biochem J 423(2):145–155
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 Physiol 46(1):245–249
Takemoto Y, Coughlan SJ, Okita TW, Satoh H, Ogawa M, Kumamaru T (2002) The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase. Plant Physiol 128(4):1212–1222
Tanchak MA, Fowke LC (1987) The morphology of multivesicular bodies in soybean protoplasts and their role in endocytosis. Protoplasma 138:173–182
Torrent M, Llop-Tous I, Ludevid MD (2009) Protein body induction: a new tool to produce and recover recombinant proteins in plants. Methods Mol Biol 483:193–208
Tosi P, Parker M, Gritsch CS, Carzaniga R, Martin B, Shewry PR (2009) Trafficking of storage proteins in developing grain of wheat. J Exp Bot 60(3):979–991
Toyooka K, Okamoto T, Minamikawa T (2000) Mass transport of proform of a KDEL-tailed cysteine proteinase (SH-EP) to protein storage vacuoles by endoplasmic reticulum-derived vesicle is involved in protein mobilization in germinating seeds. J Cell Biol 148(3):453–464
Valetti C, Grossi CE, Milstein C, Sitia R (1991) Russell bodies: a general response of secretory cells to synthesis of a mutant immunoglobulin which can neither exit from, nor be degraded in, the endoplasmic reticulum. J Cell Biol 115(4):983–994
Van Droogenbroeck B, Cao J, Stadlmann J, Altmann F, Colanesi S, Hillmer S, Robinson DG, Van Lerberge E, Terryn N, Van Montagu M, Liang M, Depicker A, De Jaeger G (2007) Aberrant localization and underglycosylation of highly accumulating single-chain Fv-Fc antibodies in transgenic Arabidopsis seeds. Proc Natl Acad Sci USA 104(4):1430–1435
Verwoerd TC, van Paridon PA, van Ooyen AJ, van Lent JW, Hoekema A, Pen J (1995) Stable accumulation of Aspergillus niger phytase in transgenic tobacco leaves. Plant Physiol 109(4):1199–1205
Vitale A, Denecke J (1999) The endoplasmic reticulum-gateway of the secretory pathway. Plant Cell 11(4):615–628
Vitale A, Hinz G (2005) Sorting of proteins to storage vacuoles: how many mechanisms? Trends Plant Sci 10(7):316–323
Vitale A, Raikhel NV (1999) What do proteins need to reach different vacuoles? Trends Plant Sci 4(4):149–155
Wakasa Y, Yang L, Hirose S, Takaiwa F (2009) Expression of unprocessed glutelin precursor alters polymerization without affecting trafficking and accumulation. J Exp Bot 60(12):3503–3511
Wakasa Y, Yasuda H, Oono Y, Kawakatsu T, Hirose S, Takahashi H, Hayashi S, Yang L, Takaiwa F (2011) Expression of ER quality control-related genes in response to changes in BiP1 levels in developing rice endosperm. Plant J 65(5):675–689
Wang J, Li Y, Lo SW, Hillmer S, Sun SS, Robinson DG, Jiang L (2007) Protein mobilization in germinating mung bean seeds involves vacuolar sorting receptors and multivesicular bodies. Plant Physiol 143(4):1628–1639
Wang Y, Ren Y, Liu X, Jiang L, Chen L, Han X, Jin M, Liu S, Liu F, Lv J, Zhou K, Su N, Bao Y, Wan J (2010) OsRab5a regulates endomembrane organization and storage protein trafficking in rice endosperm cells. Plant J 64(5):812–824
Watanabe E, Shimada T, Tamura K, Matsushima R, Koumoto Y, Nishimura M, Hara-Nishimura I (2004) An ER-localized form of PV72, a seed-specific vacuolar sorting receptor, interferes the transport of an NPIR-containing proteinase in Arabidopsis leaves. Plant Cell Physiol 45(1):9–17
Weiss S, Burrows PD, Meyer J, Wabl MR (1984) A Mott cell hybridoma. Eur J Immunol 14(8):744–748
Wenzel D, Schauermann G, von Lupke A, Hinz G (2005) The cargo in vacuolar storage protein transport vesicles is stratified. Traffic 6(1):45–55
Woo YM, Hu DW, Larkins BA, Jung R (2001) Genomics analysis of genes expressed in maize endosperm identifies novel seed proteins and clarifies patterns of zein gene expression. Plant Cell 13(10):2297–2317
Wu Y, Messing J (2010) RNA interference-mediated change in protein body morphology and seed opacity through loss of different zein proteins. Plant Physiol 153(1):337–347
Wudick MM, Luu DT, Maurel C (2009) A look inside: localization patterns and functions of intracellular plant aquaporins. New Phytol 184(2):289–302
Yamada K, Nagano AJ, Ogasawara K, Hara-Nishimura I, Nishimura M (2009) The ER body, a new organelle in Arabidopsis thaliana, requires NAI2 for its formation and accumulates specific beta-glucosidases. Plant Signal Behav 4(9):849–852
Yang D, Guo F, Liu B, Huang N, Watkins SC (2003) Expression and localization of human lysozyme in the endosperm of transgenic rice. Planta 216(4):597–603
Yasuda H, Hirose S, Kawakatsu T, Wakasa Y, Takaiwa F (2009) Overexpression of BiP has inhibitory effects on the accumulation of seed storage proteins in endosperm cells of rice. Plant Cell Physiol 50(8):1532–1543
Zheng HQ, Staehelin A (2011) Protein storage vacuoles are transformed into lytic vacuoles in root meristematic cells of germinating seedlings by multiple, cell type-specific mechanisms. Plant Physiol (in press)
Zouhar J, Hicks GR, Raikhel NV (2004) Sorting inhibitors (Sortins): chemical compounds to study vacuolar sorting in Arabidopsis. Proc Natl Acad Sci USA 101(25):9497–9501
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: David Robinson
Rights and permissions
About this article
Cite this article
Ibl, V., Stoger, E. The formation, function and fate of protein storage compartments in seeds. Protoplasma 249, 379–392 (2012). https://doi.org/10.1007/s00709-011-0288-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-011-0288-z