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Plant Physiol, December 1999, Vol. 121, pp. 1127-1141

Stop-and-Go Movements of Plant Golgi Stacks Are Mediated by the Acto-Myosin System1

Andreas Nebenführ,* Larry A. Gallagher, Terri G. Dunahay, Jennifer A. Frohlick, Anna M. Mazurkiewicz, Janet B. Meehl, and L. Andrew Staehelin

Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, Colorado 80309-0347

The Golgi apparatus in plant cells consists of a large number of independent Golgi stack/trans-Golgi network/Golgi matrix units that appear to be randomly distributed throughout the cytoplasm. To study the dynamic behavior of these Golgi units in living plant cells, we have cloned a cDNA from soybean (Glycine max), GmMan1, encoding the resident Golgi protein alpha -1,2 mannosidase I. The predicted protein of approximately 65 kD shows similarity of general structure and sequence (45% identity) to class I animal and fungal alpha -1,2 mannosidases. Expression of a GmMan1::green fluorescent protein fusion construct in tobacco (Nicotiana tabacum) Bright Yellow 2 suspension-cultured cells revealed the presence of several hundred to thousands of fluorescent spots. Immuno-electron microscopy demonstrates that these spots correspond to individual Golgi stacks and that the fusion protein is largely confined to the cis-side of the stacks. In living cells, the stacks carry out stop-and-go movements, oscillating rapidly between directed movement and random "wiggling." Directed movement (maximal velocity 4.2 µm/s) is related to cytoplasmic streaming, occurs along straight trajectories, and is dependent upon intact actin microfilaments and myosin motors, since treatment with cytochalasin D or butanedione monoxime blocks the streaming motion. In contrast, microtubule-disrupting drugs appear to have a small but reproducible stimulatory effect on streaming behavior. We present a model that postulates that the stop-and-go motion of Golgi-trans-Golgi network units is regulated by "stop signals" produced by endoplasmic reticulum export sites and locally expanding cell wall domains to optimize endoplasmic reticulum to Golgi and Golgi to cell wall trafficking.


1 This work was supported by the National Institutes of Health (grant no. GM18639) to L.A.S.

* Corresponding author; e-mail andreas.nebenfuehr{at}colorado.edu; fax 303-492-7744.

© 1999 American Society of Plant Physiologists



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Plant CellHome page
N. M. Escobar, S. Haupt, G. Thow, P. Boevink, S. Chapman, and K. Oparka
High-Throughput Viral Expression of cDNA-Green Fluorescent Protein Fusions Reveals Novel Subcellular Addresses and Identifies Unique Proteins That Interact with Plasmodesmata
PLANT CELL, July 1, 2003; 15(7): 1507 - 1523.
[Abstract] [Full Text] [PDF]


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Plant CellHome page
S. Romagnoli, G. Cai, and M. Cresti
In Vitro Assays Demonstrate That Pollen Tube Organelles Use Kinesin-Related Motor Proteins to Move along Microtubules
PLANT CELL, January 1, 2003; 15(1): 251 - 269.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
J. Petrasek, A. Cerna, K. Schwarzerova, M. Elckner, D. A. Morris, and E. Zazimalova
Do Phytotropins Inhibit Auxin Efflux by Impairing Vesicle Traffic?
Plant Physiology, January 1, 2003; 131(1): 254 - 263.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
A. Nebenfuhr, C. Ritzenthaler, and D. G. Robinson
Brefeldin A: Deciphering an Enigmatic Inhibitor of Secretion
Plant Physiology, November 1, 2002; 130(3): 1102 - 1108.
[Full Text] [PDF]


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Plant Cell PhysiolHome page
T. Shimada, E. Watanabe, K. Tamura, Y. Hayashi, M. Nishimura, and I. Hara-Nishimura
A Vacuolar Sorting Receptor PV72 on the Membrane of Vesicles that Accumulate Precursors of Seed Storage Proteins (PAC Vesicles)
Plant Cell Physiol., October 15, 2002; 43(10): 1086 - 1095.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
C. Ritzenthaler, C. Laporte, F. Gaire, P. Dunoyer, C. Schmitt, S. Duval, A. Piequet, A. M. Loudes, O. Rohfritsch, C. Stussi-Garaud, et al.
Grapevine Fanleaf Virus Replication Occurs on Endoplasmic Reticulum-Derived Membranes
J. Virol., July 29, 2002; 76(17): 8808 - 8819.
[Abstract] [Full Text] [PDF]


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Plant Cell PhysiolHome page
Y.-B. Li, S. W. Rogers, Y. C. Tse, S. W. Lo, S. S. M. Sun, G.-Y. Jauh, and L. Jiang
BP-80 and Homologs are Concentrated on Post-Golgi, Probable Lytic Prevacuolar Compartments
Plant Cell Physiol., July 15, 2002; 43(7): 726 - 742.
[Abstract] [Full Text] [PDF]


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Plant CellHome page
F. Brandizzi, E. L. Snapp, A. G. Roberts, J. Lippincott-Schwartz, and C. Hawes
Membrane Protein Transport between the Endoplasmic Reticulum and the Golgi in Tobacco Leaves Is Energy Dependent but Cytoskeleton Independent: Evidence from Selective Photobleaching
PLANT CELL, June 1, 2002; 14(6): 1293 - 1309.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
J. E. Carette, K. Guhl, J. Wellink, and A. Van Kammen
Coalescence of the Sites of Cowpea Mosaic Virus RNA Replication into a Cytopathic Structure
J. Virol., May 13, 2002; 76(12): 6235 - 6243.
[Abstract] [Full Text] [PDF]


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Plant Cell PhysiolHome page
G. Jedd and N.-H. Chua
Visualization of Peroxisomes in Living Plant Cells Reveals Acto-Myosin-Dependent Cytoplasmic Streaming and Peroxisome Budding
Plant Cell Physiol., April 15, 2002; 43(4): 384 - 392.
[Abstract] [Full Text] [PDF]


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J Exp BotHome page
K. Van Gestel, R.H. Kohler, and J-P. Verbelen
Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules
J. Exp. Bot., April 1, 2002; 53(369): 659 - 667.
[Abstract] [Full Text] [PDF]


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Plant CellHome page
A. Y. Cheung, C. Y.-h. Chen, R. H. Glaven, B. H. J. de Graaf, L. Vidali, P. K. Hepler, and H.-m. Wu
Rab2 GTPase Regulates Vesicle Trafficking between the Endoplasmic Reticulum and the Golgi Bodies and Is Important to Pollen Tube Growth
PLANT CELL, April 1, 2002; 14(4): 945 - 962.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
T. Inaba, Y. Nagano, T. Nagasaki, and Y. Sasaki
Distinct Localization of Two Closely Related Ypt3/Rab11 Proteins on the Trafficking Pathway in Higher Plants
J. Biol. Chem., March 8, 2002; 277(11): 9183 - 9188.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
J. Mathur, N. Mathur, and M. Hulskamp
Simultaneous Visualization of Peroxisomes and Cytoskeletal Elements Reveals Actin and Not Microtubule-Based Peroxisome Motility in Plants
Plant Physiology, March 1, 2002; 128(3): 1031 - 1045.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
P. Dunoyer, C. Ritzenthaler, O. Hemmer, P. Michler, and C. Fritsch
Intracellular Localization of the Peanut Clump Virus Replication Complex in Tobacco BY-2 Protoplasts Containing Green Fluorescent Protein-Labeled Endoplasmic Reticulum or Golgi Apparatus
J. Virol., January 15, 2002; 76(2): 865 - 874.
[Abstract] [Full Text] [PDF]


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Plant CellHome page
J.-L. Qiu, R. Jilk, M. D. Marks, and D. B. Szymanski
The Arabidopsis SPIKE1 Gene Is Required for Normal Cell Shape Control and Tissue Development
PLANT CELL, January 1, 2002; 14(1): 101 - 118.
[Abstract] [Full Text] [PDF]


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Plant CellHome page
C. Ritzenthaler, A. Nebenfuhr, A. Movafeghi, C. Stussi-Garaud, L. Behnia, P. Pimpl, L. A. Staehelin, and D. G. Robinson
Reevaluation of the Effects of Brefeldin A on Plant Cells Using Tobacco Bright Yellow 2 Cells Expressing Golgi-Targeted Green Fluorescent Protein and COPI Antisera
PLANT CELL, January 1, 2002; 14(1): 237 - 261.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
D. N.V. Geelen and D. G. Inze
A Bright Future for the Bright Yellow-2 Cell Culture
Plant Physiology, December 1, 2001; 127(4): 1375 - 1379.
[Full Text] [PDF]


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Plant CellHome page
T. C. Baldwin, M. G. Handford, M.-I. Yuseff, A. Orellana, and P. Dupree
Identification and Characterization of GONST1, a Golgi-Localized GDP-Mannose Transporter in Arabidopsis
PLANT CELL, October 1, 2001; 13(10): 2283 - 2295.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
B.-H. Kang, J. S. Busse, C. Dickey, D. M. Rancour, and S. Y. Bednarek
The Arabidopsis Cell Plate-Associated Dynamin-Like Protein, ADL1Ap, Is Required for Multiple Stages of Plant Growth and Development
Plant Physiology, May 1, 2001; 126(1): 47 - 68.
[Abstract] [Full Text]


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Plant Physiol.Home page
D. K. Ro, N. Mah, B. E. Ellis, and C. J. Douglas
Functional Characterization and Subcellular Localization of Poplar (Populus trichocarpa x Populus deltoides) Cinnamate 4-Hydroxylase
Plant Physiology, May 1, 2001; 126(1): 317 - 329.
[Abstract] [Full Text]


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Plant CellHome page
Z. Hong, Z. Zhang, J. M. Olson, and D. P. S. Verma
A Novel UDP-Glucose Transferase Is Part of the Callose Synthase Complex and Interacts with Phragmoplastin at the Forming Cell Plate
PLANT CELL, April 1, 2001; 13(4): 769 - 780.
[Abstract] [Full Text]


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Plant Physiol.Home page
A. Vitale and G. Galili
The Endomembrane System and the Problem of Protein Sorting
Plant Physiology, January 1, 2001; 125(1): 115 - 118.
[Full Text]


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Plant Physiol.Home page
C. R. Hawes and B. Satiat-Jeunemaitre
Trekking along the Cytoskeleton
Plant Physiology, January 1, 2001; 125(1): 119 - 122.
[Full Text]


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Plant CellHome page
N. A. Eckardt
Green Light for Traffic in the Early Secretory Pathway
PLANT CELL, November 1, 2000; 12(11): 2009 - 2011.
[Full Text]


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Plant CellHome page
H. Batoko, H.-Q. Zheng, C. Hawes, and I. Moore
A Rab1 GTPase Is Required for Transport between the Endoplasmic Reticulum and Golgi Apparatus and for Normal Golgi Movement in Plants
PLANT CELL, November 1, 2000; 12(11): 2201 - 2218.
[Abstract] [Full Text]


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Plant Cell PhysiolHome page
N. Mitsuhashi, T. Shimada, S. Mano, M. Nishimura, and I. Hara-Nishimura
Characterization of Organelles in the Vacuolar-Sorting Pathway by Visualization with GFP in Tobacco BY-2 Cells
Plant Cell Physiol., September 1, 2000; 41(9): 993 - 1001.
[Abstract] [Full Text] [PDF]


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Plant CellHome page
V. Gomord and L. Faye
Reply: Glycobiology and the Plant Cell--A World of Information
PLANT CELL, September 1, 2000; 12(9): 1519 - 1521.
[Full Text]


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Plant Physiol.Home page
A. Nebenführ, J. A. Frohlick, and L. A. Staehelin
Redistribution of Golgi Stacks and Other Organelles during Mitosis and Cytokinesis in Plant Cells
Plant Physiology, September 1, 2000; 124(1): 135 - 152.
[Abstract] [Full Text]


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Plant CellHome page
S. Pagny, M. Cabanes-Macheteau, J. W. Gillikin, N. Leborgne-Castel, P. Lerouge, R. S. Boston, L. Faye, and V. Gomord
Protein Recycling from the Golgi Apparatus to the Endoplasmic Reticulum in Plants and Its Minor Contribution to Calreticulin Retention
PLANT CELL, May 1, 2000; 12(5): 739 - 756.
[Abstract] [Full Text]




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