Storage parenchyma cells of developing legume cotyledons actively transport large amounts of storage proteins to protein storage vacuoles (PSV). These proteins are synthesized on the endoplasmic reticulum and pass through the Golgi apparatus. Clathrin coated vesicles (CCV) and small electron dense vesicles found near the trans-Golgi network (TGN) have both been implicated in the Golgi-to-vacuole transport step. Recent findings that protein storage cells contain more than one type of vacuole have necessitated a re-examination of the role of both types of vesicles in vacuolar protein transport. Immunoblots of highly purified CCV preparations and immunogold labelling with antibodies to the storage proteins vicilin and legumin, indicate that the dense vesicles, but not the CCV, are involved in storage protein transport in pea cotyledons. This result is supported by the finding that alpha-TIP, a protein characteristic of the PSV membrane, is absent from CCV. In addition, complex glycoproteins appear to be carried by CCV but are not detectable in the PSV. We suggest on the basis of these data that storage proteins and other vacuolar proteins such as acid hydrolases are not sorted by the same mechanism and are transported by different types of vesicles to different types of vacuoles.
REFERENCES
Bassham
D. C.
, Gal
S.
, Conceicao
A. D.
, Raikhel
N. V.
(1995
). An Arabidopsis syntaxin homolog isolated by functional complementation of a yeast pep 12 mutant.
Proc. Nat. Acad. Sci. USA
92
, 7262
–7266
Bechtel
D. B.
, Gaines
R. L.
(1982
). The presence of protease digestible material inGolgi vesicles during endosperm development of selected cereals.
Am. J. Bot
69
, 880
–884
Beevers
L.
(1996
). Clathrin-coated vesicles in plants.
Int. Rev. Cytol
167
, 1
–35
Casey
R. D.
(1979
). Immunoaffinity chromatography as a means of purifying leguminfrom Pisum (pea) seeds.
Biochem. J
177
, 509
–520
Chrispeels
M. J.
, Higgins
T. J. V.
, Spencer
D.
(1982
). Assembly of storage proteinoligomers in the endoplasmic reticulum and processing of the polypeptides in the protein bodies of developing pea cotyledons.
J. Cell Biol
93
, 306
–313
Chrispeels
M. J.
(1983
). The Golgi apparatus mediates the transport of phytohemagglutinin to the protein bodies in bean cotyledons.
Planta
158
, 140
–151
Chrispeels
M. J.
, Raikhel
N. V.
(1992
). Short peptide domains target proteins to plant vacuoles.
Cell
68
, 613
–616
Craig
S.
, Goodchild
D. J.
(1984
). Periodate-acid treatment of sections permitson-grid immunogold localization of pea seed vicilin in ER and Golgi.
Protoplasma
122
, 35
–44
Depta
H.
, Robinson
D. G.
(1986
). The isolation and enrichment of coated vesiclesfrom suspension-cultured carrot cells.
Protoplasma
130
, 162
–170
Dittie
A. S.
, Hajibagheri
N.
, Tooze
S. A.
(1996
). The AP-1 adaptor complex bindsto immature secretory granules from PC12 cells and is regulated by ADP-ribosylation factor.
J. Cell Biol
132
, 523
–536
Drucker
M.
, Herkt
B.
, Robinson
D. G.
(1995
). Demonstration of a-type adaptin atthe plant plasma membrane.
Cell Biol. Intern
3
, 191
–201
Geli
M. I.
, Torrent
M.
, Ludevid
D.
(1994
). Two structural domains mediate twosequential events in-zein targeting: protein endoplasmic reticulum retention and protein body formation.
Plant Cell
6
, 1911
–1922
Greenwood
J. S.
, Chrispeels
M. J.
(1985
). Immunocytochemical localization ofphaesolin and phytohemagglutinin in the endoplasmic reticulum and Golgi complex of developing bean cotyledons.
Planta
164
, 295
–302
Griffing
L. R.
(1991
). Comparisons of Golgi structure and dynamics in plant andanimal cells.
J. Electron Microsc. Tech
17
, 179
–199
Harley
S. M.
, Beevers
L.
(1989
). Coated vesicles are involved in the transport ofstorage proteins during seed development in Pisum sativum L.
Plant Physiol
91
, 674
–678
Harris
N.
, Grindley
H.
, Mulchrone
J.
, Croy
R. D.
(1989
). Correlated in situ hybridisation and immunochemical studies of legumin storage protein deposition in pea (Pisum sativum L.).
Cell Biol. Int. Rep
13
, 23
–35
Höfte
H.
, Hubbard
L.
, Reizer
J.
, Ludevid
D.
, Herman
E. M.
, Chrispeels
M. J.
(1992
). Vegetative and seed-specific forms of tonoplast intrinsic protein in the vacuolar membrane of Arabidopsis thaliana.
Plant Physiol
99
, 561
–570
Hoh
B.
, Hinz
G.
, Jeong
B.-K.
, Robinson
D. G.
(1995
). Protein storage vacuolesform de novo during pea cotyledon development.
J. Cell Sci
108
, 299
–310
Holstein
S. E. H.
, Drucker
M.
, Robinson
D. G.
(1994
). Identification of a-typeadaptin in plant clathrin-coated vesicles.
J. Cell Sci
107
, 945
–953
Johnson
K. D.
, Herman
E. M.
, Chrispeels
M. J.
(1989
). An abundant, highlyconserved tonoplast protein in seeds.
Plant Physiol
91
, 1006
–1013
Kim
W. T.
, Franceschi
V. R.
, Krishnan
H. B.
, Okita
T. W.
(1988
). Formation ofwheat protein bodies: involvement of the Golgi apparatus in gliadin transport.
Planta
176
, 173
–182
Kirsch
T.
, Paris
N.
, Bulter
J. M.
, Beevers
L.
, Rogers
J. C.
(1994
). Purificationand initial characterization of a potential plant vacuolar targeting receptor.
Proc. Nat. Acad. Sci. USA
91
, 3403
–3407
Kirsch
T.
, Saalbach
G.
, Raikhel
N. V.
, Beevers
L.
(1996
). Interaction of apotential vacuolar targeting receptor with amino-and carboxy-terminal targeting determinants.
Plant Physiol
111
, 469
–474
Kornfeld
S.
, Mellman
I.
(1989
). The biogenesis of lysosomes.
Annu. Rev. Cell Biol
5
, 483
–525
Krishnan
H. B.
, Franceschi
V. R.
, Okita
T. W.
(1986
). Immunochemical studies onthe role of the Golgi complex in protein-body formation in rice seeds.
Planta
169
, 471
–480
Kuliawat
R.
, Arvan
P.
(1994
). Distinct molecular mechanisms for protein sortingwithin immature secretory granules of pancreatic-cells.
J. Cell Biol
126
, 77
–86
Lauriere
M.
, Lauriere
C.
, Chrispeels
M. J.
, Johnson
K. D.
, Sturm
A.
(1989
). Characterization of a xylose-specific antiserum that reacts with the complex asparagine-linked glycans of extracellular and vacuolar glycoproteins.
Plant Physiol
90
, 1182
–1188
Levanony
H.
, Rubin
R.
, Altschuler
Y.
, Galili
G.
(1992
). Evidence for a novel routeof wheat storage proteins to vacuoles.
J. Cell Biol
119
, 1117
–1128
Lycett
G. W.
, Delauney
A. J.
, Gatehouse
J. A.
, Gilroy
J.
, Croy
R. R. D.
, Boulter
D.
(1983
). The vicilin gene family of pea (Pisum sativum L.): a complete cDNA coding sequence for provicilin.
Nucl. Acids Res
11
, 2367
–2380
Lycett
G. W.
, Croy
R. R. D.
, Shirsat
A. H.
, Boulter
D.
(1984
). The completenucleotide sequence of a legumin gene from pea (Pisum sativum L.).
Nucl. Acids Res
12
, 4493
–4506
Mäder
M.
, Chrispeels
M. J.
(1984
). Synthesis of an integral protein of the proteinbody membrane in Phaseolus vulgaris cotyledons.
Planta
160
, 330
–340
Marty-Mazars
D.
, Clemencet
M.-C.
, Dozolme
P.
, Marty
F.
(1995
). Antibodies tothe tonoplast from the storage parenchyma cells of beetroot recognize a major intrinsic protein related to TIPs.
Eur. J. Cell Biol
66
, 106
–118
Matsuoka
K.
, Bassham
D. C.
, Raikhel
N. V.
, Kakamura
K.
(1995
). Differentsensitivity to wortmannin of two vacuolar sorting signals indicates the presence of distinct sorting machineries in tobacco cells.
J. Cell Biol
130
, 1307
–1318
Moore
P. J.
, Swords
K. M. M.
, Lynch
M. A.
, Staehelin
L. A.
(1991
). Spatialorgniaztion of the assembly pathways of glycoproteins and complex polysaccharides in the Golgi apparatus of plants.
J. Cell Biol
112
, 589
–602
Paris
N.
, Stanley
C. M.
, Jones
R. L.
, Rogers
J. C.
(1996
). Plant cells contain twofunctionally distinct vacuolar compartments.
Cell
85
, 563
–572
Qi
X.
, Tai
C.-Y.
, Wasserman
B. P.
(1995
). Plasma membrane intrinsic proteins of Beta vulgaris L.
Plant Physiol
108
, 387
–392
Record
R. D.
, Griffing
L. R.
(1988
). Convergence of the endocytic and lysosomalpathways in soybean protoplasts.
Planta
176
, 425
–432
Robinson
D. G.
, Kristen
U.
(1982
). Membrane flow via the Golgi apparatus ofhigher plant cells.
Int. Rev. Cytol
77
, 89
–127
Robinson
D. G.
, Balusek
K.
, Freundt
H.
(1989
). Legumin antibodies recognizepolypeptides in coated vesicles from developing pea cotyledons.
Protoplasma
150
, 79
–82
Robinson
M. S.
(1994
). The role of clathrin, adaptors and dynamin in endocytosis.
Curr.Opin. Cell Biol
6
, 538
–544
Rothman
J. E.
(1994
). Mechanisms of intracellular protein transport.
Nature
372
, 55
–63
Schekman
R.
, Orci
L.
(1996
). Coat proteins and vesicle budding.
Science
271
, 1526
–1533
Schmid
S. L.
, Damke
H.
(1995
). Coated vesicles: a diversity of form and function.
FASEB J
9
, 1445
–1453
Sturm
A.
, Johnson
K. D.
, Szumilo
T.
, Elbein
A. D.
, Chrispeels
M. J.
(1987
). Subcellular localization of glycosidases and glycosyl-transferases involved in the processing of N-linked oligosaccharides.
Plant Physiol
85
, 741
–745
Tooze
J.
, Tooze
S. A. C.
(1986
). Clathrin-caoted vesicular transport ofsecretoryproteins during the formation of ACTH-containing secretory granules in AtT20cells.
J. Cell Biol
103
, 839
–850
zur Nieden
U.
, Manteuffel
R.
, Weber
E.
, Neumann
D.
(1984
). Dictyosomesparticipate in the intracellular pathway of storage proteins in developing Vicia faba cotyledons.
Eur. J. Cell Biol
34
, 9
–17
This content is only available via PDF.
© 1996 by Company of Biologists
1996
