Published online 2 April 2001. doi:10.1083/jcb.153.1.111
© The Rockefeller University Press,
0021-9525/2001//111 $5.00
The Journal of Cell Biology, Volume 153, Number 1,
, 2001 111-120
Ftsz Ring Formation at the Chloroplast Division Site in Plants
Stanislav Vithaa,
Rosemary S. McAndrewa, and
Katherine W. Osteryounga
a Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824
Department of Plant Biology, 166 Plant Biology Building, Michigan State University, East Lansing, MI 48824.(517) 353-1926(517) 355-4685
osteryou{at}msu.edu
Among the events that accompanied the evolution of chloroplasts from their endosymbiotic ancestors was the host cell recruitment of the prokaryotic cell division protein FtsZ to function in chloroplast division. FtsZ, a structural homologue of tubulin, mediates cell division in bacteria by assembling into a ring at the midcell division site. In higher plants, two nuclear-encoded forms of FtsZ, FtsZ1 and FtsZ2, play essential and functionally distinct roles in chloroplast division, but whether this involves ring formation at the division site has not been determined previously. Using immunofluorescence microscopy and expression of green fluorescent protein fusion proteins in Arabidopsis thaliana, we demonstrate here that FtsZ1 and FtsZ2 localize to coaligned rings at the chloroplast midpoint. Antibodies specific for recognition of FtsZ1 or FtsZ2 proteins in Arabidopsis also recognize related polypeptides and detect midplastid rings in pea and tobacco, suggesting that midplastid ring formation by FtsZ1 and FtsZ2 is universal among flowering plants. Perturbation in the level of either protein in transgenic plants is accompanied by plastid division defects and assembly of FtsZ1 and FtsZ2 into filaments and filament networks not observed in wild-type, suggesting that previously described FtsZ-containing cytoskeletal-like networks in chloroplasts may be artifacts of FtsZ overexpression.
Key Words: plastids organelle replication organelle fission cytoskeleton mitochondria
© 2001 The Rockefeller University Press
The online version of this article contains supplemental material.
Abbreviations used in this paper: GFP, green fluorescent protein; CaMV, cauliflower mosaic virus; PD, plastid-dividing.

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Martin, A., Lang, D., Hanke, S. T., Mueller, S. J.X., Sarnighausen, E., Vervliet-Scheebaum, M., Reski, R.
(2009). Targeted Gene Knockouts Reveal Overlapping Functions of the Five Physcomitrella patens FtsZ Isoforms in Chloroplast Division, Chloroplast Shaping, Cell Patterning, Plant Development, and Gravity Sensing. Mol Plant
2: 1359-1372
[Abstract]
[Full Text]
-
Schmitz, A. J., Glynn, J. M., Olson, B. J.S.C., Stokes, K. D., Osteryoung, K. W.
(2009). Arabidopsis FtsZ2-1 and FtsZ2-2 Are Functionally Redundant, But FtsZ-Based Plastid Division Is Not Essential for Chloroplast Partitioning or Plant Growth and Development. Mol Plant
2: 1211-1222
[Abstract]
[Full Text]
-
Fujiwara, M. T., Sekine, K., Yamamoto, Y. Y., Abe, T., Sato, N., Itoh, R. D.
(2009). Live Imaging of Chloroplast FtsZ1 Filaments, Rings, Spirals, and Motile Dot Structures in the AtMinE1 Mutant and Overexpressor of Arabidopsis thaliana. Plant Cell Physiol
50: 1116-1126
[Abstract]
[Full Text]
-
Okazaki, K., Kabeya, Y., Suzuki, K., Mori, T., Ichikawa, T., Matsui, M., Nakanishi, H., Miyagishima, S.-y.
(2009). The PLASTID DIVISION1 and 2 Components of the Chloroplast Division Machinery Determine the Rate of Chloroplast Division in Land Plant Cell Differentiation. Plant Cell
21: 1769-1780
[Abstract]
[Full Text]
-
Glynn, J. M., Froehlich, J. E., Osteryoung, K. W.
(2008). Arabidopsis ARC6 Coordinates the Division Machineries of the Inner and Outer Chloroplast Membranes through Interaction with PDV2 in the Intermembrane Space. Plant Cell
20: 2460-2470
[Abstract]
[Full Text]
-
Fujiwara, M. T., Hashimoto, H., Kazama, Y., Abe, T., Yoshida, S., Sato, N., Itoh, R. D.
(2008). The Assembly of the FtsZ Ring at the Mid-Chloroplast Division Site Depends on a Balance Between the Activities of AtMinE1 and ARC11/AtMinD1. Plant Cell Physiol
49: 345-361
[Abstract]
[Full Text]
-
Maple, J., Moller, S. G.
(2007). Interdependency of formation and localisation of the Min complex controls symmetric plastid division. J. Cell Sci.
120: 3446-3456
[Abstract]
[Full Text]
-
Yoder, D. W., Kadirjan-Kalbach, D., Olson, B. J. S. C., Miyagishima, S.-y., DeBlasio, S. L., Hangarter, R. P., Osteryoung, K. W.
(2007). Effects of Mutations in Arabidopsis FtsZ1 on Plastid Division, FtsZ Ring Formation and Positioning, and FtsZ Filament Morphology in Vivo. Plant Cell Physiol
48: 775-791
[Abstract]
[Full Text]
-
Maple, J., Moller, S. G.
(2007). Plastid Division: Evolution, Mechanism and Complexity. ANN BOT (LOND)
99: 565-579
[Abstract]
[Full Text]
-
Lopez-Juez, E.
(2007). Plastid biogenesis, between light and shadows. J Exp Bot
58: 11-26
[Abstract]
[Full Text]
-
Miyagishima, S.-y., Froehlich, J. E., Osteryoung, K. W.
(2006). PDV1 and PDV2 Mediate Recruitment of the Dynamin-Related Protein ARC5 to the Plastid Division Site. Plant Cell
18: 2517-2530
[Abstract]
[Full Text]
-
Lohse, S., Hause, B., Hause, G., Fester, T.
(2006). FtsZ Characterization and Immunolocalization in the Two Phases of Plastid Reorganization in Arbuscular Mycorrhizal Roots of Medicago truncatula. Plant Cell Physiol
47: 1124-1134
[Abstract]
[Full Text]
-
Balmer, Y., Vensel, W. H, DuPont, F. M, Buchanan, B. B, Hurkman, W. J
(2006). Proteome of amyloplasts isolated from developing wheat endosperm presents evidence of broad metabolic capability. J Exp Bot
57: 1591-1602
[Abstract]
[Full Text]
-
Aldridge, C., Moller, S. G.
(2005). The Plastid Division Protein AtMinD1 Is a Ca2+-ATPase Stimulated by AtMinE1. J. Biol. Chem.
280: 31673-31678
[Abstract]
[Full Text]
-
Vaishnava, S., Morrison, D. P., Gaji, R. Y., Murray, J. M., Entzeroth, R., Howe, D. K., Striepen, B.
(2005). Plastid segregation and cell division in the apicomplexan parasite Sarcocystis neurona. J. Cell Sci.
118: 3397-3407
[Abstract]
[Full Text]
-
Aldridge, C., Maple, J., Moller, S. G.
(2005). The molecular biology of plastid division in higher plants. J Exp Bot
56: 1061-1077
[Abstract]
[Full Text]
-
Natesan, S. K. A., Sullivan, J. A., Gray, J. C.
(2005). Stromules: a characteristic cell-specific feature of plastid morphology. J Exp Bot
56: 787-797
[Abstract]
[Full Text]
-
Shimada, H., Koizumi, M., Kuroki, K., Mochizuki, M., Fujimoto, H., Ohta, H., Masuda, T., Takamiya, K.-i.
(2004). ARC3, a Chloroplast Division Factor, is a Chimera of Prokaryotic FtsZ and Part of Eukaryotic Phosphatidylinositol-4-phosphate 5-kinase. Plant Cell Physiol
45: 960-967
[Abstract]
[Full Text]
-
Nishida, K., Misumi, O., Yagisawa, F., Kuroiwa, H., Nagata, T., Kuroiwa, T.
(2004). Triple Immunofluorescent Labeling of FtsZ, Dynamin, and EF-Tu Reveals a Loose Association Between the Inner and Outer Membrane Mitochondrial Division Machinery in the Red Alga Cyanidioschyzon merolae. J. Histochem. Cytochem.
52: 843-849
[Abstract]
[Full Text]
-
Raynaud, C., Cassier-Chauvat, C., Perennes, C., Bergounioux, C.
(2004). An Arabidopsis Homolog of the Bacterial Cell Division Inhibitor SulA Is Involved in Plastid Division. Plant Cell
16: 1801-1811
[Abstract]
[Full Text]
-
Fujiwara, M. T., Nakamura, A., Itoh, R., Shimada, Y., Yoshida, S., Moller, S. G.
(2004). Chloroplast division site placement requires dimerization of the ARC11/AtMinD1 protein in Arabidopsis. J. Cell Sci.
117: 2399-2410
[Abstract]
[Full Text]
-
Ferguson, P. L., Shaw, G. S.
(2004). Human S100B Protein Interacts with the Escherichia coli Division Protein FtsZ in a Calcium-sensitive Manner. J. Biol. Chem.
279: 18806-18813
[Abstract]
[Full Text]
-
Osteryoung, K. W., Nunnari, J.
(2003). The Division of Endosymbiotic Organelles. Science
302: 1698-1704
[Abstract]
[Full Text]
-
Gilson, P. R., Yu, X.-C., Hereld, D., Barth, C., Savage, A., Kiefel, B. R., Lay, S., Fisher, P. R., Margolin, W., Beech, P. L.
(2003). Two Dictyostelium Orthologs of the Prokaryotic Cell Division Protein FtsZ Localize to Mitochondria and Are Required for the Maintenance of Normal Mitochondrial Morphology. Eukaryot Cell
2: 1315-1326
[Abstract]
[Full Text]
-
Gonzalez, J. M., Jimenez, M., Velez, M., Mingorance, J., Andreu, J. M., Vicente, M., Rivas, G.
(2003). Essential Cell Division Protein FtsZ Assembles into One Monomer-thick Ribbons under Conditions Resembling the Crowded Intracellular Environment. J. Biol. Chem.
278: 37664-37671
[Abstract]
[Full Text]
-
Small, E., Addinall, S. G.
(2003). Dynamic FtsZ polymerization is sensitive to the GTP to GDP ratio and can be maintained at steady state using a GTP-regeneration system. Microbiology
149: 2235-2242
[Abstract]
[Full Text]
-
Vitha, S., Froehlich, J. E., Koksharova, O., Pyke, K. A., van Erp, H., Osteryoung, K. W.
(2003). ARC6 Is a J-Domain Plastid Division Protein and an Evolutionary Descendant of the Cyanobacterial Cell Division Protein Ftn2. Plant Cell
15: 1918-1933
[Abstract]
[Full Text]
-
Gao, H., Kadirjan-Kalbach, D., Froehlich, J. E., Osteryoung, K. W.
(2003). From the Cover: ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc. Natl. Acad. Sci. USA
100: 4328-4333
[Abstract]
[Full Text]
-
Miyagishima, S.-y., Nishida, K., Mori, T., Matsuzaki, M., Higashiyama, T., Kuroiwa, H., Kuroiwa, T.
(2003). A Plant-Specific Dynamin-Related Protein Forms a Ring at the Chloroplast Division Site. Plant Cell
15: 655-665
[Abstract]
[Full Text]
-
Ding, Z., Zhao, Z., Jakubowski, S. J., Krishnamohan, A., Margolin, W., Christie, P. J.
(2002). A Novel Cytology-Based, Two-Hybrid Screen for Bacteria Applied to Protein-Protein Interaction Studies of a Type IV Secretion System. J. Bacteriol.
184: 5572-5582
[Abstract]
[Full Text]
-
Fulgosi, H., Gerdes, L., Westphal, S., Glockmann, C., Soll, J.
(2002). Cell and chloroplast division requires ARTEMIS. Proc. Natl. Acad. Sci. USA
99: 11501-11506
[Abstract]
[Full Text]
-
Arimura, S.-i., Tsutsumi, N.
(2002). A dynamin-like protein (ADL2b), rather than FtsZ, is involved in Arabidopsis mitochondrial division. Proc. Natl. Acad. Sci. USA
99: 5727-5731
[Abstract]
[Full Text]
-
Itoh, R., Fujiwara, M., Nagata, N., Yoshida, S.
(2001). A Chloroplast Protein Homologous to the Eubacterial Topological Specificity Factor MinE Plays a Role in Chloroplast Division. Plant Physiol.
127: 1644-1655
[Abstract]
[Full Text]
-
McAndrew, R. S., Froehlich, J. E., Vitha, S., Stokes, K. D., Osteryoung, K. W.
(2001). Colocalization of Plastid Division Proteins in the Chloroplast Stromal Compartment Establishes a New Functional Relationship between FtsZ1 and FtsZ2 in Higher Plants. Plant Physiol.
127: 1656-1666
[Abstract]
[Full Text]
-
Miyagishima, S.-y., Takahara, M., Mori, T., Kuroiwa, H., Higashiyama, T., Kuroiwa, T.
(2001). Plastid Division Is Driven by a Complex Mechanism That Involves Differential Transition of the Bacterial and Eukaryotic Division Rings. Plant Cell
13: 2257-2268
[Abstract]
[Full Text]