Abstract
Chloroplasts are photosynthetic organelles derived from endosymbiotic cyanobacteria during evolution. Dramatic changes occurred during the process of the formation and evolution of chloroplasts, including the large-scale gene transfer from chloroplast to nucleus. However, there are still many essential characters remaining. For the chloroplast division machinery, FtsZ proteins, Ftn2, SulA and part of the division site positioning system—MinD and MinE are still conserved. New or at least partially new proteins, such as FtsZ family proteins FtsZ1 and ARC3, ARC6H, ARC5, PDV1, PDV2 and MCD1, were introduced for the division of chloroplasts during evolution. Some bacterial cell division proteins, such as FtsA, MreB, Ftn6, FtsW and FtsI, probably lost their function or were gradually lost. Thus, the chloroplast division machinery is a dynamically evolving structure with both conservation and innovation.
Similar content being viewed by others
References
Adams D W, Errington J (2009). Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol, 7(9): 642–653
Addinall S G, Lutkenhaus J (1996). FtsA is localized to the septum in an FtsZ-dependent manner. J Bacteriol, 178: 7167–7172
Allard J F, Cytrynbaum E N (2009). Force generation by a dynamic Zring in Escherichia coli cell division. Proc Natl Acad Sci USA, 106(1): 145–150
Amos L A, van den Ent F, Lowe J (2004). Structural/functional homology between the bacterial and eukaryotic cytoskeletons. Curr Opin Cell Biol, 16(1): 24–31
Beech P L, Nheu T, Schultz T, Herbert S, Lithgow T, Gilson P R, McFadden G I (2000). Mitochondrial FtsZ in a chromophyte alga. Science, 287(5456): 1276–1279
Bi E, Lutkenhaus J (1993). Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J Bacteriol, 175: 1118–1125
Bi E F, Lutkenhaus J (1991). FtsZ ring structure associated with division in Escherichia coli. Nature, 354(6349): 161–164
Bleazard W, McCaffery J M, King E J, Bale S, Mozdy A, Tieu Q, Nunnari J, Shaw J M (1999). The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol, 1(5): 298–304
Bork P, Sander C, Valencia A (1992). An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc Natl Acad Sci USA, 89(16): 7290–7294
Bramhill D (1997). Bacterial cell division. Annu Rev Cell Dev Biol, 13(1): 395–424
Carballido-Lopez R (2006). The bacterial actin-like cytoskeleton. Microbiol Mol Biol Rev, 70(4): 888–909
Carr J F, Hinshaw J E (1997). Dynamin assembles into spirals under physiological salt conditions upon the addition of GDP and gammaphosphate analogues. J Biol Chem, 272(44): 28030–28035
Cha J H, Stewart G C (1997). The divIVA minicell locus of Bacillus subtilis. J Bacteriol, 179: 1671–1683
Chen M S, Obar R A, Schroeder C C, Austin T W, Poodry C A, Wadsworth S C, Vallee R B (1991). Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature, 351(6327): 583–586
Chu K H, Qi J, Yu Z G, Anh V (2004). Origin and phylogeny of chloroplasts revealed by a simple correlation analysis of complete genomes. Mol Biol Evol, 21(1): 200–206
Chugh J, Chatterjee A, Kumar A, Mishra R K, Mittal R, Hosur R V (2006). Structural characterization of the large soluble oligomers of the GTPase effector domain of dynamin. FEBS J, 273(2): 388–397
Colletti K S, Tattersall E A, Pyke K A, Froelich J E, Stokes K D, Osteryoung K W (2000). A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol, 10(9): 507–516
Cordell S C, Robinson E J, Lowe J (2003). Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc Natl Acad Sci USA, 100(13): 7889–7894
Cullis C A, Vorster B J, Van Der Vyver C, Kunert K J (2009). Transfer of genetic material between the chloroplast and nucleus: how is it related to stress in plants? Ann Bot (Lond), 103(4): 625–633
Dai K, Lutkenhaus J (1992). The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J Bacteriol, 174: 6145–6151
Dajkovic A, Mukherjee A, Lutkenhaus J (2008). Investigation of regulation of FtsZ assembly by SulA and development of a model for FtsZ polymerization. J Bacteriol, 190(7): 2513–2526
Datta P, Dasgupta A, Bhakta S, Basu J (2002). Interaction between FtsZ and FtsW of Mycobacterium tuberculosis. J Biol Chem, 277(28): 24983–24987
de Boer P, Crossley R, Rothfield L (1992a). The essential bacterial celldivision protein FtsZ is a GTPase. Nature, 359(6392): 254–256
de Boer P A, Crossley R E, Hand A R, Rothfield L I (1991). The MinD protein is a membrane ATPase required for the correct placement of the Escherichia colidivision site. EMBO J, 10: 4371–4380
de Boer P A, Crossley R E, Rothfield L I (1989). A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell, 56(4): 641–649
de Boer P A, Crossley R E, Rothfield L I (1992b). Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli. J Bacteriol, 174: 63–70
Dewar S J, Begg K J, Donachie W D (1992). Inhibition of cell division initiation by an imbalance in the ratio of FtsA to FtsZ. J Bacteriol, 174: 6314–6316
Dinkins R, Reddy M S, Leng M, Collins G B (2001). Overexpression of the Arabidopsis thaliana MinD1 gene alters chloroplast size and number in transgenic tobacco plants. Planta, 214(2): 180–188
Douce R, Joyard J (1990). Biochemistry and function of the plastid envelope. Annu Rev Cell Biol, 6(1): 173–216
Douglas S E (1998). Plastid evolution: origins, diversity, trends. Curr Opin Genet Dev, 8(6): 655–661
Dyall S D, Brown M T, Johnson P J (2004). Ancient invasions: from endosymbionts to organelles. Science, 304(5668): 253–257
Eberhardt C, Kuerschner L, Weiss D S (2003). Probing the catalytic activity of a cell division-specific transpeptidase in vivo with betalactams. J Bacteriol, 185(13): 3726–3734
Egelman E H (2003). A tale of two polymers: new insights into helical filaments. Nat Rev Mol Cell Biol, 4(8): 621–630
Ellis J L, Leech R M (1985). Cell-size and chloroplast size in relation to chloroplast replication in light-grown wheat leaves. Planta, 165(1): 120–125
Eric Ottesen R Z, Gayle K (2010). Identification of a chloroplast division mutant coding for ARC6H, an ARC6 homolog that plays a nonredundant role. Plant Sci, 178(2): 114–122
Erickson H P (1998). Atomic structures of tubulin and FtsZ. Trends Cell Biol, 8(4): 133–137
Erickson H P (2009). Modeling the physics of FtsZ assembly and force generation. Proc Natl Acad Sci USA, 106(23): 9238–9243
Errington J, Daniel R A, Scheffers D J (2003). Cytokinesis in bacteria. Microbiol Mol Biol Rev, 67(1): 52–65
Fischer-Friedrich E, Meacci G, Lutkenhaus J, Chate H, Kruse K (2010). Intra- and intercellular fluctuations in Min-protein dynamics decrease with cell length. Proc Natl Acad Sci USA, 107(14): 6134–6139
Fraipont C, Alexeeva S, Wolf B, van der Ploeg R, Schloesser M, den Blaauwen T, Nguyen-Disteche M (2011). The integral membrane FtsW protein and peptidoglycan synthase PBP3 form a subcomplex in Escherichia coli. Microbiology, 157(1): 251–259
Fu X, Shih Y L, Zhang Y, Rothfield L I (2001). The MinE ring required for proper placement of the division site is a mobile structure that changes its cellular location during the Escherichia colidivision cycle. Proc Natl Acad Sci USA, 98(3): 980–985
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(3): 345–361
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(11): 2399–2410
Fukushima N H, Brisch E, Keegan B R, Bleazard W, Shaw J M (2001). The GTPase effector domain sequence of the Dnm1p GTPase regulates self-assembly and controls a rate-limiting step in mitochondrial fission. Mol Biol Cell, 12: 2756–2766
Gao H, Kadirjan-Kalbach D, Froehlich J E, Osteryoung K W (2003). ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci USA, 100(7): 4328–4333
Garcia M, Myouga F, Takechi K, Sato H, Nabeshima K, Nagata N, Takio S, Shinozaki K, Takano H (2008). An Arabidopsis homolog of the bacterial peptidoglycan synthesis enzyme MurE has an essential role in chloroplast development. Plant J, 53(6): 924–934
Ghasriani H, Ducat T, Hart C T, Hafizi F, Chang N, Al-Baldawi A, Ayed S H, Lundstrom P, Dillon J A, Goto N K (2010). Appropriation of the MinD protein-interaction motif by the dimeric interface of the bacterial cell division regulator MinE. Proc Natl Acad Sci USA, 107(43): 18416–18421
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(6): 1315–1326
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(9): 2460–2470
Glynn J M, Yang Y, Vitha S, Schmitz A J, Hemmes M, Miyagishima S Y, Osteryoung K W (2009). PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis. Plant J, 59(5): 700–711
Graumann P L (2007). Cytoskeletal elements in bacteria. Annu Rev Microbiol, 61(1): 589–618
Gray J C, Row P E (1995). Protein translocation across chloroplast envelope membranes. Trends Cell Biol, 5(6): 243–247
Gray M W (1999). Evolution of organellar genomes. Curr Opin Genet Dev, 9(6): 678–687
Gross J, Bhattacharya D (2009). Revaluating the evolution of the Toc and Tic protein translocons. Trends Plant Sci, 14(1): 13–20
Gu X, Verma D (1996). Phragmoplastin, a dynamin-like protein associated with cell plate formation in plants. EMBO J, 15: 695–704
Harris E H, Boynton J E, Gillham N W (1994). Chloroplast ribosomes and protein synthesis. Microbiol Rev, 58: 700–754
Higashitani A, Higashitani N, Horiuchi K (1995). A cell division inhibitor SulA of Escherichia colidirectly interacts with FtsZ through GTP hydrolysis. Biochem Biophys Res Commun, 209(1): 198–204
Higashitani A, Ishii Y, Kato Y, Koriuchi K (1997). Functional dissection of a cell-division inhibitor, SulA, of Escherichia coliand its negative regulation by Lon. Mol Gen Genet, 254(4): 351–357
Hinshaw J E (2000). Dynamin and its role in membrane fission. Annu Rev Cell Dev Biol, 16(1): 483–519
Hinshaw J E, Schmid S L (1995). Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature, 374(6518): 190–192
Homi S, Takechi K, Tanidokoro K, Sato H, Takio S, Takano H (2009). The peptidoglycan biosynthesis genes MurA and MraY are related to chloroplast division in the moss Physcomitrella patens. Plant Cell Physiol, 50(12): 2047–2056
Howard M (2004). A mechanism for polar protein localization in bacteria. J Mol Biol, 335(2): 655–663
Howe C J, Barbrook A C, Koumandou V L, Nisbet R E, Symington H A, Wightman T F (2003). Evolution of the chloroplast genome. Philos Trans R Soc Lond B Biol Sci, 358(1429): 99–107
Hsieh C W, Lin T Y, Lai H M, Lin C C, Hsieh T S, Shih Y L (2010). Direct MinE-membrane interaction contributes to the proper localization of MinDE in E. coli. Mol Microbiol, 75(2): 499–512
Hu Z, Gogol E P, Lutkenhaus J (2002). Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc Natl Acad Sci USA, 99(10): 6761–6766
Hu Z, Lutkenhaus J (1999). Topological regulation of cell division in Escherichia coliinvolves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE. Mol Microbiol, 34(1): 82–90
Hu Z, Mukherjee A, Pichoff S, Lutkenhaus J (1999). The MinC component of the division site selection system in Escherichia coliinteracts with FtsZ to prevent polymerization. Proc Natl Acad Sci USA, 96(26): 14819–14824
Hu Z, Saez C, Lutkenhaus J (2003). Recruitment of MinC, an inhibitor of Z-ring formation, to the membrane in Escherichia coli: role of MinD and MinE. J Bacteriol, 185(1): 196–203
Huang J, Cao C, Lutkenhaus J (1996). Interaction between FtsZ and inhibitors of cell division. J Bacteriol, 178: 5080–5085
Huisman O, D’Ari R, George J (1980). Further characterization of sfiA and sfiB mutations in Escherichia coli. J Bacteriol, 144: 185–191
Huisman O, D’Ari R, Gottesman S (1984). Cell-division control in Escherichia coli: specific induction of the SOS function SfiA protein is sufficient to block septation. Proc Natl Acad Sci USA, 81(14): 4490–4494
Ishino F, Jung H K, Ikeda M, Doi M, Wachi M, Matsuhashi M (1989). New mutations fts-36, lts-33, and ftsW clustered in the mra region of the Escherichia colichromosome induce thermosensitive cell growth and division. J Bacteriol, 171: 5523–5530
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(4): 1644–1655
Ivanov V, Mizuuchi K (2010). Multiple modes of interconverting dynamic pattern formation by bacterial cell division proteins. Proc Natl Acad Sci USA, 107(18): 8071–8078
Jackson-Constan D, Akita M, Keegstra K (2001). Molecular chaperones involved in chloroplast protein import. Biochim Biophys Acta, 1541(1–2): 102–113
Jarvis P, Soll J (2002). Toc, tic, and chloroplast protein import. Biochim Biophys Acta, 1590(1–3): 177–189
Jeong WJ, Park Y I, Suh K, Raven J A, Yoo O J, Liu J R (2002). A large population of small chloroplasts in tobacco leaf cells allows more effective chloroplast movement than a few enlarged chloroplasts. Plant Physiol, 129(1): 112–121
Jones C, Holland I B (1985). Role of the SulB (FtsZ) protein in division inhibition during the SOS response in Escherichia coli: FtsZ stabilizes the inhibitor SulA in maxicells. Proc Natl Acad Sci USA, 82(18): 6045–6049
Jones L J, Carballido-Lopez R, Errington J (2001). Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell, 104(6): 913–922
Kasten B, Reski R (1997). β-Lactam antibiotics inhibit chloroplast division in a moss (Physcomitrella patens) but not in tomato (Lycopersicon esculentum). J Plant Physiol, 150: 137–140
Katayama N, Takano H, Sugiyama M, Takio S, Sakai A, Tanaka K, Kuroiwa H, Ono K (2003). Effects of antibiotics that inhibit the bacterial peptidoglycan synthesis pathway on moss chloroplast division. Plant Cell Physiol, 44(7): 776–781
Kelly R B (1995). Endocytosis. Ringing necks with dynamin. Nature, 374(6518): 116–117
Khattar M M, Begg K J, Donachie W D (1994). Identification of FtsW and characterization of a new ftsW division mutant of Escherichia coli. J Bacteriol, 176: 7140–7147
Kiefel B R, Gilson P R, Beech P L (2004). Diverse eukaryotes have retained mitochondrial homologues of the bacterial division protein FtsZ. Protist, 155(1): 105–115
Koksharova O A, Wolk C P (2002). A novel gene that bears a DnaJ motif influences cyanobacterial cell division. J Bacteriol, 184(19): 5524–5528
Kosaka T, Ikeda K (1983a). Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J Neurobiol, 14(3): 207–225
Kosaka T, Ikeda K (1983b). Reversible blockage of membrane retrieval and endocytosis in the garland cell of the temperature-sensitive mutant of Drosophila melanogaster, shibirets1. J Cell Biol, 97(2): 499–507
Kruse K, Howard M, Margolin W (2007). An experimentalist’s guide to computational modelling of the Min system. Mol Microbiol, 63(5): 1279–1284
Kuroiwa T, Kuroiwa H, Sakai A, Takahashi H, Toda K, Itoh R (1998). The division apparatus of plastids and mitochondria. Int Rev Cytol, 181: 1–41
Kuroiwa T, Misumi O, Nishida K, Yagisawa F, Yoshida Y, Fujiwara T, Kuroiwa H (2008). Vesicle, mitochondrial, and plastid division machineries with emphasis on dynamin and electron-dense rings. Int Rev Cell Mol Biol, 271: 97–152
Lackner L L, Raskin D M, de Boer P A (2003). ATP-dependent interactions between Escherichia coliMin proteins and the phospholipid membrane in vitro. J Bacteriol, 185(3): 735–749
Lan G, Daniels B R, Dobrowsky T M, Wirtz D, Sun S X (2009). Condensation of FtsZ filaments can drive bacterial cell division. Proc Natl Acad Sci USA, 106(1): 121–126
Lan G, Wolgemuth C W, Sun S X (2007). Z-ring force and cell shape during division in rod-like bacteria. Proc Natl Acad Sci USA, 104(41): 16110–16115
Lara B, Ayala J A (2002). Topological characterization of the essential Escherichia colicell division protein FtsW. FEMS Microbiol Lett, 216(1): 23–32
Leech RM, Thomson WW, Platt-Aloia K A (1981). Observations on the mechanism of chloroplast division in higher-plants. New Phytol, 87(1): 1–9
Low H H, Lowe J (2010). Dynamin architecture-from monomer to polymer. Curr Opin Struct Biol, 20(6): 791–798
Lowe J, Amos L A (1998). Crystal structure of the bacterial cell-division protein FtsZ. Nature, 391(6663): 203–206
Lowe J, van den Ent F, Amos L A (2004). Molecules of the bacterial cytoskeleton. Annu Rev Biophys Biomol Struct, 33(1): 177–198
Lutkenhaus J (2002). Dynamic proteins in bacteria. Curr Opin Microbiol, 5(6): 548–552
Lutkenhaus J (2007). Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem, 76(1): 539–562
Ma X, Ehrhardt DW, Margolin W (1996). Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia colicells by using green fluorescent protein. Proc Natl Acad Sci USA, 93(23): 12998–13003
Ma X, Margolin W (1999). Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol, 181: 7531–7544
Machida M, Takechi K, Sato H, Chung S J, Kuroiwa H, Takio S, Seki M, Shinozaki K, Fujita T, Hasebe M, Takano H (2006). Genes for the peptidoglycan synthesis pathway are essential for chloroplast division in moss. Proc Natl Acad Sci USA, 103(17): 6753–6758
Maple J, Chua N H, Moller S G (2002). The topological specificity factor AtMinE1 is essential for correct plastid division site placement in Arabidopsis. Plant J, 31(3): 269–277
Maple J, Fujiwara M T, Kitahata N, Lawson T, Baker N R, Yoshida S, Moller S G (2004). GIANT CHLOROPLAST 1 is essential for correct plastid division in Arabidopsis. Curr Biol, 14(9): 776–781
Maple J, Vojta L, Soll J, Moller S G (2007). ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Rep, 8(3): 293–299
Marbouty M, Saguez C, Cassier-Chauvat C, Chauvat F (2009). ZipN, an FtsA-like orchestrator of divisome assembly in the model cyanobacterium Synechocystis PCC6803. Mol Microbiol, 74(2): 409–420
Margolin W (2000). Themes and variations in prokaryotic cell division. FEMS Microbiol Rev, 24(4): 531–548
Margolin W (2001). Bacterial cell division: a moving MinE sweeper boggles the MinD. Curr Biol, 11(10): R395–R398
Marrison J L, Rutherford SM, Robertson E J, Lister C, Dean C, Leech R M (1999). The distinctive roles of five different ARC genes in the chloroplast division process in Arabidopsis. Plant J, 18(6): 651–662
Martin W (2003). Gene transfer from organelles to the nucleus: Frequent and in big chunks. Proc Natl Acad Sci USA, 100(15): 8612–8614
Mazouni K, Domain F, Cassier-Chauvat C, Chauvat F (2004). Molecular analysis of the key cytokinetic components of cyanobacteria: FtsZ, ZipN and MinCDE. Mol Microbiol, 52(4): 1145–1158
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(4): 1656–1666
McAndrew R S, Olson B J, Kadirjan-Kalbach D K, Chi-Ham C L, Vitha S, Froehlich J E, Osteryoung K W (2008). In vivo quantitative relationship between plastid division proteins FtsZ1 and FtsZ2 and identification of ARC6 and ARC3 in a native FtsZ complex. Biochem J, 412(2): 367–378
McFadden G I (1999). Endosymbiosis and evolution of the plant cell. Curr Opin Plant Biol, 2(6): 513–519
Mercer K L, Weiss D S (2002). The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, FtsI (PBP3), to the division site. J Bacteriol, 184(4): 904–912
Miyagishima S, Takahara M, Kuroiwa T (2001). Novel filaments 5 nm in diameter constitute the cytosolic ring of the plastid division apparatus. Plant Cell, 13: 707–721
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(10): 2517–2530
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(3): 655–665
Mori T, Kuroiwa H, Takahara M, Miyagishima S Y, Kuroiwa T (2001). Visualization of an FtsZ ring in chloroplasts of Lilium longiflorum leaves. Plant Cell Physiol, 42(6): 555–559
Mosyak L, Zhang Y, Glasfeld E, Haney S, Stahl M, Seehra J, Somers W S (2000). The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J, 19(13): 3179–3191
Mukherjee A, Cao C, Lutkenhaus J (1998). Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. Proc Natl Acad Sci USA, 95(6): 2885–2890
Mukherjee A, Saez C, Lutkenhaus J (2001). Assembly of an FtsZ mutant deficient in GTPase activity has implications for FtsZ assembly and the role of the Z ring in cell division. J Bacteriol, 183(24): 7190–7197
Mulder E, Woldringh C L, Tetart F, Bouche J P (1992). New minC mutations suggest different interactions of the same region of division inhibitor MinC with proteins specific for minD and dicB coinhibition pathways. J Bacteriol, 174: 35–39
Nakamura M, Maruyama I N, Soma M, Kato J, Suzuki H, Horota Y (1983). On the process of cellular division in Escherichia coli: nucleotide sequence of the gene for penicillin-binding protein 3. Mol Gen Genet, 191(1): 1–9
Nakanishi H, Suzuki K, Kabeya Y, Miyagishima S Y (2009). Plantspecific protein MCD1 determines the site of chloroplast division in concert with bacteria-derived MinD. Curr Biol, 19(2): 151–156
Nogales E, Wolf S G, Downing K H (1998). Structure of the alpha beta tubulin dimer by electron crystallography. Nature, 391(6663): 199–203
Olson B J, Wang Q, Osteryoung K W (2010). GTP-dependent heteropolymer formation and bundling of chloroplast FtsZ1 and FtsZ2. J Biol Chem, 285(27): 20634–20643
Oross J W, Possingham J V (1989). Ultrastructural features of the constricted region of dividing plastids. Protoplasma, 150(2-3): 131–138
Osawa M, Anderson D E, Erickson H P (2008). Reconstitution of contractile FtsZ rings in liposomes. Science, 320(5877): 792–794
Osteryoung K W (2000). Organelle fission. Crossing the evolutionary divide. Plant Physiol, 123(4): 1213–1216
Osteryoung K W, McAndrew R S (2001). The plastid division machine. Annu Rev Plant Physiol Plant Mol Biol, 52(1): 315–333
Osteryoung K W, Nunnari J (2003). The division of endosymbiotic organelles. Science, 302(5651): 1698–1704
Osteryoung K W, Pyke K A (1998). Plastid division: evidence for a prokaryotically derived mechanism. Curr Opin Plant Biol, 1(6): 475–479
Osteryoung K W, Stokes K D, Rutherford S M, Percival A L, Lee W Y (1998). Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell, 10: 1991–2004
Osteryoung K W, Vierling E (1995). Conserved cell and organelle division. Nature, 376(6540): 473–474
Pelloquin L, Belenguer P, Menon Y, Ducommun B (1998). Identification of a fission yeast dynamin-related protein involved in mitochondrial DNA maintenance. Biochem Biophys Res Commun, 251(3): 720–726
Pichoff S, Lutkenhaus J (2005). Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol Microbiol, 55(6): 1722–1734
Pichoff S, Lutkenhaus J (2007). Identification of a region of FtsA required for interaction with FtsZ. Mol Microbiol, 64(4): 1129–1138
Pogliano J, Pogliano K, Weiss D S, Losick R, Beckwith J (1997). Inactivation of FtsI inhibits constriction of the FtsZ cytokinetic ring and delays the assembly of FtsZ rings at potential division sites. Proc Natl Acad Sci USA, 94(2): 559–564
Popp D, Narita A, Maeda K, Fujisawa T, Ghoshdastider U, Iwasa M, Maeda Y, Robinson R C (2010). Filament structure, organization, and dynamics in MreB sheets. J Biol Chem, 285(21): 15858–15865
Possingh J S (1969). Changes in chloroplast number per cell during leaf development in spinach. Planta, 86(2): 186–194
Praefcke G J, McMahon H T (2004). The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol, 5(2): 133–147
Pyke K A (1999). Plastid division and development. Plant Cell, 11: 549–556
Pyke K A, Leech R M (1994). A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol, 104: 201–207
Pyke K A, Rutherford S M, Robertson E J, Leech R M (1994). arc6, a fertile Arabidopsis mutant with only two mesophyll cell chloroplasts. Plant Physiol, 106: 1169–1177
Ramachandran R, Pucadyil T J, Liu Y W, Acharya S, Leonard M, Lukiyanchuk V, Schmid S L (2009). Membrane insertion of the pleckstrin homology domain variable loop 1 is critical for dynamincatalyzed vesicle scission. Mol Biol Cell, 20(22): 4630–4639
Ramachandran R, Surka M, Chappie J S, Fowler DM, Foss T R, Song B D, Schmid S L (2007). The dynamin middle domain is critical for tetramerization and higher-order self-assembly. EMBO J, 26(2): 559–566
Raskin D M, de Boer P A (1999a). MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J Bacteriol, 181: 6419–6424
Raskin D M, de Boer P A (1999b). Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc Natl Acad Sci USA, 96(9): 4971–4976
Raven J A, Allen J F (2003). Genomics and chloroplast evolution: what did cyanobacteria do for plants? Genome Biol, 4(3): 209
RayChaudhuri D, Park J T, and the RayChaudhuri (1992). Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature, 359(6392): 251–254
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(7): 1801–1811
Reddy M S, Dinkins R, Collins G B (2002). Overexpression of the Arabidopsis thaliana MinE1 bacterial division inhibitor homologue gene alters chloroplast size and morphology in transgenic Arabidopsis and tobacco plants. Planta, 215(2): 167–176
Rensing S A, Kiessling J, Reski R, Decker E L (2004). Diversification of ftsZ during early land plant evolution. J Mol Evol, 58(2): 154–162
Rensing S A, Lang D, Zimmer A D, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud P F, Lindquist E A, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin I T, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk W B, Barker E, Bennetzen J L, Blankenship R, Cho S H, Dutcher S K, Estelle M, Fawcett J A, Gundlach H, Hanada K, Heyl A, Hicks K A, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson D R, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton P J, Sanderfoot A, Schween G, Shiu S H, Stueber K, Theodoulou F L, Tu H, Van de Peer Y, Verrier P J, Waters E, Wood A, Yang L, Cove D, Cuming A C, Hasebe M, Lucas S, Mishler B D, Reski R, Grigoriev I V, Quatrano R S, Boore J L (2008). The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science, 319(5859): 64–69
Reumann S, Davila-Aponte J, Keegstra K (1999). The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: identification of a cyanobacterial homolog. Proc Natl Acad Sci USA, 96(2): 784–789
Rico A I, Garcia-Ovalle M, Mingorance J, Vicente M (2004). Role of two essential domains of Escherichia coli FtsA in localization and progression of the division ring. Mol Microbiol, 53(5): 1359–1371
Robertson E J, Pyke K A, Leech R M (1995). arc6, an extreme chloroplast division mutant of Arabidopsis also alters proplastid proliferation and morphology in shoot and root apices. J Cell Sci, 108(Pt 9): 2937–2944
Robertson E J, Rutherford S M, Leech R M (1996). Characterization of chloroplast division using the Arabidopsis mutant arc5. Plant Physiol, 112(1): 149–159
Romberg L, Levin P A (2003). Assembly dynamics of the bacterial cell division protein FTSZ: poised at the edge of stability. Annu Rev Microbiol, 57(1): 125–154
Rothfield L, Justice S, Garcia-Lara J (1999). Bacterial cell division. Annu Rev Genet, 33(1): 423–448
Salim K, Bottomley M J, Querfurth E, Zvelebil M J, Gout I, Scaife R, Margolis R L, Gigg R, Smith C I, Driscoll P C, Waterfield M D, Panayotou G (1996). Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton’s tyrosine kinase. EMBO J, 15: 6241–6250
Sanchez M, Valencia A, Ferrandiz M J, Sander C, Vicente M (1994). Correlation between the structure and biochemical activities of FtsA, an essential cell division protein of the actin family. EMBO J, 13: 4919–4925
Saurer W, Possingham J V (1970). Studies on the growth of spinach leaves (Spinacea oleracea). J Exp Biol, 21: 151–158
Scheffers D, Driessen A J (2001). The polymerization mechanism of the bacterial cell division protein FtsZ. FEBS Lett, 506(1): 6–10
Scheffers D J, de Wit J G, den Blaauwen T, Driessen A J (2002). GTP hydrolysis of cell division protein FtsZ: evidence that the active site is formed by the association of monomers. Biochemistry, 41(2): 521–529
Scheffers D J, den Blaauwen T, Driessen A J (2000). Non-hydrolysable GTP-gamma-S stabilizes the FtsZ polymer in a GDP-bound state. Mol Microbiol, 35(5): 1211–1219
Scheffers D J, Driessen A J (2002). Immediate GTP hydrolysis upon FtsZ polymerization. Mol Microbiol, 43(6): 1517–1521
Schmitz A J, Glynn J M, Olson B J, 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(6): 1211–1222
Sesaki H, Jensen R E (1999). Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J Cell Biol, 147(4): 699–706
Shimada H, Koizumi M, Kuroki K, Mochizuki M, Fujimoto H, Ohta H, Masuda T, Takamiya K (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(8): 960–967
Shiomi D, Margolin W (2007). The C-terminal domain of MinC inhibits assembly of the Z ring in Escherichia coli. J Bacteriol, 189(1): 236–243
Smirnova E, Shurland D L, Newman-Smith E D, Pishvaee B, van der Bliek A M (1999). A model for dynamin self-assembly based on binding between three different protein domains. J Biol Chem, 274(21): 14942–14947
Stokes K D, McAndrew R S, Figueroa R, Vitha S, Osteryoung K W (2000). Chloroplast division and morphology are differentially affected by overexpression of FtsZ1 and FtsZ2 genes in Arabidopsis. Plant Physiol, 124(4): 1668–1677
Stokes K D, Osteryoung KW (2003). Early divergence of the FtsZ1 and FtsZ2 plastid division gene families in photosynthetic eukaryotes. Gene, 320: 97–108
Strepp R, Scholz S, Kruse S, Speth V, Reski R (1998). Plant nuclear gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin. Proc Natl Acad Sci USA, 95(8): 4368–4373
Stricker J, Maddox P, Salmon E D, Erickson H P (2002). Rapid assembly dynamics of the Escherichia coliFtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc Natl Acad Sci USA, 99(5): 3171–3175
Suefuji K, Valluzzi R (2002). Dynamic assembly of MinD into filament bundles modulated by ATP, phospholipids, and MinE. Proc Natl Acad Sci USA, 99(26): 16776–16781
Sun Q, Margolin W (1998). FtsZ dynamics during the division cycle of live Escherichia colicells. J Bacteriol, 180: 2050–2056
Sun Q, Yu X C, Margolin W (1998). Assembly of the FtsZ ring at the central division site in the absence of the chromosome. Mol Microbiol, 29(2): 491–503
Sweitzer S M, Hinshaw J E (1998). Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell, 93(6): 1021–1029
Taghbalout A, Ma L, Rothfield L (2006). Role of MinD-membrane association in Min protein interactions. J Bacteriol, 188(8): 2993–3001
Takahara M, Takahashi H, Matsunaga S, Miyagishima S, Takano H, Sakai A, Kawano S, Kuroiwa T (2000). A putative mitochondrial ftsZ gene is present in the unicellular primitive red alga Cyanidioschyzon merolae. Mol Gen Genet, 264(4): 452–460
Takano H, Takechi K (2010). Plastid peptidoglycan. Biochim Biophys Acta, 1800: 144–151
Takei K, Haucke V, Slepnev V, Farsad K, Salazar M, Chen H, De Camilli P (1998). Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell, 94(1): 131–141
Takei K, McPherson P S, Schmid S L, De Camilli P (1995). Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature, 374: 186–190
Tavva V S, Collins G B, Dinkins R D (2006). Targeted overexpression of the Escherichia coliMinC protein in higher plants results in abnormal chloroplasts. Plant Cell Rep, 25(4): 341–348
Timmis J N, Ayliffe M A, Huang C Y, Martin W (2004). Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet, 5(2): 123–135
Trusca D, Scott S, Thompson C, Bramhill D (1998). Bacterial SOS checkpoint protein SulA inhibits polymerization of purified FtsZ cell division protein. J Bacteriol, 180: 3946–3953
van den Ent F, Amos L, Lowe J (2001a). Bacterial ancestry of actin and tubulin. Curr Opin Microbiol, 4(6): 634–638
van den Ent F, Amos L A, Lowe J (2001b). Prokaryotic origin of the actin cytoskeleton. Nature, 413(6851): 39–44
van den Ent F, Moller-Jensen J, Amos L A, Gerdes K, Lowe J (2002). Factin-like filaments formed by plasmid segregation protein ParM. EMBO J, 21(24): 6935–6943
Vesteg M, Vacula R, Krajcovic J (2009). On the origin of chloroplasts, import mechanisms of chloroplast-targeted proteins, and loss of photosynthetic ability - review. Folia Microbiol (Praha), 54(4): 303–321
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(8): 1918–1933
Vitha S, McAndrew R S, Osteryoung KW (2001). FtsZ ring formation at the chloroplast division site in plants. J Cell Biol, 153(1): 111–120
Wakasugi T, Nagai T, Kapoor M, Sugita M, Ito M, Ito S, Tsudzuki J, Nakashima K, Tsudzuki T, Suzuki Y, Hamada A, Ohta T, Inamura A, Yoshinaga K, Sugiura M (1997). Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division. Proc Natl Acad Sci USA, 94(11): 5967–5972
Wang S, Arellano-Santoyo H, Combs P A, Shaevitz J W (2010). Actinlike cytoskeleton filaments contribute to cell mechanics in bacteria. Proc Natl Acad Sci USA, 107(20): 9182–9185
Warnock D E, Schmid S L (1996). Dynamin GTPase, a force-generating molecular switch. Bioessays, 18(11): 885–893
Weiss D S, Chen J C, Ghigo J M, Boyd D, Beckwith J (1999). Localization of FtsI (PBP3) to the septal ring requires its membrane anchor, the Z ring, FtsA, FtsQ, and FtsL. J Bacteriol, 181: 508–520
Weiss D S, Pogliano K, Carson M, Guzman L M, Fraipont C, Nguyen-Disteche M, Losick R, Beckwith J (1997). Localization of the Escherichia colicell division protein Ftsl (PBP3) to the division site and cell pole. Mol Microbiol, 25(04): 671–681
Wijsman H J, Koopman C R (1976). The relation of the genes envA and ftsA in Escherichia coli. Mol Gen Genet, 147(1): 99–102
Wilsbach K, Payne G S (1993). Vps1p, a member of the dynamin GTPase family, is necessary for Golgi membrane protein retention in Saccharomyces cerevisiae. EMBO J, 12: 3049–3059
Wissel M C, Weiss D S (2004). Genetic analysis of the cell division protein FtsI (PBP3): amino acid substitutions that impair septal localization of FtsI and recruitment of FtsN. J Bacteriol, 186(2): 490–502
Xiong A S, Peng R H, Zhuang J, Gao F, Zhu B, Fu X Y, Xue Y, Jin X F, Tian Y S, Zhao W, Yao Q H (2009). Gene duplication, transfer, and evolution in the chloroplast genome. Biotechnol Adv, 27(4): 340–347
Yamamoto K, Pyke K A, Kiss J Z (2002). Reduced gravitropism in inflorescence stems and hypocotyls, but not roots, of Arabidopsis mutants with large plastids. Physiol Plant, 114(4): 627–636
Yan K, Pearce K H, Payne D J (2000). A conserved residue at the extreme C-terminus of FtsZ is critical for the FtsA-FtsZ interaction in Staphylococcus aureus. Biochem Biophys Res Commun, 270(2): 387–392
Zhang M, Hu Y, Jia J, Li D, Zhang R, Gao H, He Y (2009). CDP1, a novel component of chloroplast division site positioning system in Arabidopsis. Cell Res, 19(7): 877–886
Zheng J, Cahill S M, Lemmon M A, Fushman D, Schlessinger J, Cowburn D (1996). Identification of the binding site for acidic phospholipids on the pH domain of dynamin: implications for stimulation of GTPase activity. J Mol Biol, 255(1): 14–21
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gao, H., Gao, F. Evolution of the chloroplast division machinery. Front. Biol. 6, 398–413 (2011). https://doi.org/10.1007/s11515-011-1139-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11515-011-1139-1