REVIEW

Evolution of the chloroplast division machinery

  • Hongbo GAO , 1,2,3 ,
  • Fuli GAO 1
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  • 1. College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China
  • 2. National Engineering Laboratory for Tree Breeding, Beijing 100083, China
  • 3. Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants of Ministry of Education, Beijing 100083, China

Received date: 21 Jan 2011

Accepted date: 28 Mar 2011

Published date: 01 Oct 2011

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

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.

Cite this article

Hongbo GAO , Fuli GAO . Evolution of the chloroplast division machinery[J]. Frontiers in Biology, 2011 , 6(5) : 398 -413 . DOI: 10.1007/s11515-011-1139-1

Acknowledgements

This work was partially supported by grants from the Natural Science Foundation of China (Grant No. 30971439), the Beijing Municipal Natural Science Foundation (No. 5102022) and the Fundamental Research Funds for the Central Universities.
1
Adams D W, Errington J (2009). Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol, 7(9): 642–653

DOI

2
Addinall S G, Lutkenhaus J (1996). FtsA is localized to the septum in an FtsZ-dependent manner. J Bacteriol, 178: 7167–7172

3
Allard J F, Cytrynbaum E N (2009). Force generation by a dynamic Z-ring in Escherichia coli cell division. Proc Natl Acad Sci USA, 106(1): 145–150

DOI

4
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

DOI

5
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

DOI

6
Bi E, Lutkenhaus J (1993). Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J Bacteriol, 175: 1118–1125

7
Bi E F, Lutkenhaus J (1991). FtsZ ring structure associated with division in Escherichia coli. Nature, 354(6349): 161–164

DOI

8
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

DOI

9
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

DOI

10
Bramhill D (1997). Bacterial cell division. Annu Rev Cell Dev Biol, 13(1): 395–424

DOI

11
Carballido-Lopez R (2006). The bacterial actin-like cytoskeleton. Microbiol Mol Biol Rev, 70(4): 888–909

DOI

12
Carr J F, Hinshaw J E (1997). Dynamin assembles into spirals under physiological salt conditions upon the addition of GDP and gamma-phosphate analogues. J Biol Chem, 272(44): 28030–28035

DOI

13
Cha J H, Stewart G C (1997). The divIVA minicell locus of Bacillus subtilis. J Bacteriol, 179: 1671–1683

14
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

DOI

15
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

DOI

16
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

DOI

17
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

DOI

18
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

DOI

19
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

DOI

20
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

21
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

DOI

22
Datta P, Dasgupta A, Bhakta S, Basu J (2002). Interaction between FtsZ and FtsW of Mycobacteriumtuberculosis. J Biol Chem, 277(28): 24983–24987

DOI

23
de Boer P, Crossley R, Rothfield L (1992a). The essential bacterial cell-division protein FtsZ is a GTPase. Nature, 359(6392): 254–256

DOI

24
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 coli division site. EMBO J, 10: 4371–4380

25
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

DOI

26
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

27
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

28
Dinkins R, Reddy M S, Leng M, Collins G B (2001). Overexpression of the Arabidopsis thalianaMinD1 gene alters chloroplast size and number in transgenic tobacco plants. Planta, 214(2): 180–188

DOI

29
Douce R, Joyard J (1990). Biochemistry and function of the plastid envelope. Annu Rev Cell Biol, 6(1): 173–216

DOI

30
Douglas S E (1998). Plastid evolution: origins, diversity, trends. Curr Opin Genet Dev, 8(6): 655–661

DOI

31
Dyall S D, Brown M T, Johnson P J (2004). Ancient invasions: from endosymbionts to organelles. Science, 304(5668): 253–257

DOI

32
Eberhardt C, Kuerschner L, Weiss D S (2003). Probing the catalytic activity of a cell division-specific transpeptidase in vivo with beta-lactams. J Bacteriol, 185(13): 3726–3734

DOI

33
Egelman E H (2003). A tale of two polymers: new insights into helical filaments. Nat Rev Mol Cell Biol, 4(8): 621–630

DOI

34
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

DOI

35
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

DOI

36
Erickson H P (1998). Atomic structures of tubulin and FtsZ. Trends Cell Biol, 8(4): 133–137

DOI

37
Erickson H P (2009). Modeling the physics of FtsZ assembly and force generation. Proc Natl Acad Sci USA, 106(23): 9238–9243

DOI

38
Errington J, Daniel R A, Scheffers D J (2003). Cytokinesis in bacteria. Microbiol Mol Biol Rev, 67(1): 52–65

DOI

39
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

DOI

40
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

DOI

41
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 coli division cycle. Proc Natl Acad Sci USA, 98(3): 980–985

DOI

42
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

DOI

43
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

DOI

44
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

45
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

DOI

46
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

DOI

47
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

DOI

48
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

DOI

49
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

DOI

50
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

DOI

51
Graumann P L (2007). Cytoskeletal elements in bacteria. Annu Rev Microbiol, 61(1): 589–618

DOI

52
Gray J C, Row P E (1995). Protein translocation across chloroplast envelope membranes. Trends Cell Biol, 5(6): 243–247

DOI

53
Gray M W (1999). Evolution of organellar genomes. Curr Opin Genet Dev, 9(6): 678–687

DOI

54
Gross J, Bhattacharya D (2009). Revaluating the evolution of the Toc and Tic protein translocons. Trends Plant Sci, 14(1): 13–20

DOI

55
Gu X, Verma D (1996). Phragmoplastin, a dynamin-like protein associated with cell plate formation in plants. EMBO J, 15: 695–704

56
Harris E H, Boynton J E, Gillham N W (1994). Chloroplast ribosomes and protein synthesis. Microbiol Rev, 58: 700–754

57
Higashitani A, Higashitani N, Horiuchi K (1995). A cell division inhibitor SulA of Escherichia coli directly interacts with FtsZ through GTP hydrolysis. Biochem Biophys Res Commun, 209(1): 198–204

DOI

58
Higashitani A, Ishii Y, Kato Y, Koriuchi K (1997). Functional dissection of a cell-division inhibitor, SulA, of Escherichia coli and its negative regulation by Lon. Mol Gen Genet, 254(4): 351–357

DOI

59
Hinshaw J E (2000). Dynamin and its role in membrane fission. Annu Rev Cell Dev Biol, 16(1): 483–519

DOI

60
Hinshaw J E, Schmid S L (1995). Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature, 374(6518): 190–192

DOI

61
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

DOI

62
Howard M (2004). A mechanism for polar protein localization in bacteria. J Mol Biol, 335(2): 655–663

DOI

63
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

DOI

64
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

DOI

65
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

DOI

66
Hu Z, Lutkenhaus J (1999). Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE. Mol Microbiol, 34(1): 82–90

DOI

67
Hu Z, Mukherjee A, Pichoff S, Lutkenhaus J (1999). The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc Natl Acad Sci USA, 96(26): 14819–14824

DOI

68
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

DOI

69
Huang J, Cao C, Lutkenhaus J (1996). Interaction between FtsZ and inhibitors of cell division. J Bacteriol, 178: 5080–5085

70
Huisman O, D'Ari R, George J (1980). Further characterization of sfiA and sfiB mutations in Escherichia coli. J Bacteriol, 144: 185–191

71
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

DOI

72
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 coli chromosome induce thermosensitive cell growth and division. J Bacteriol, 171: 5523–5530

73
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

DOI

74
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

DOI

75
Jackson-Constan D, Akita M, Keegstra K (2001). Molecular chaperones involved in chloroplast protein import. Biochim Biophys Acta, 1541(1-2): 102–113

DOI

76
Jarvis P, Soll J (2002). Toc, tic, and chloroplast protein import. Biochim Biophys Acta, 1590(1-3): 177–189

DOI

77
Jeong W J, 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

DOI

78
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

DOI

79
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

DOI

80
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

81
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

DOI

82
Kelly R B (1995). Endocytosis. Ringing necks with dynamin. Nature, 374(6518): 116–117

DOI

83
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

84
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

DOI

85
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

DOI

86
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

DOI

87
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

DOI

88
Kruse K, Howard M, Margolin W (2007). An experimentalist’s guide to computational modelling of the Min system. Mol Microbiol, 63(5): 1279–1284

DOI

89
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

DOI

90
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

DOI

91
Lackner L L, Raskin D M, de Boer P A (2003). ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro. J Bacteriol, 185(3): 735–749

DOI

92
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

DOI

93
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

DOI

94
Lara B, Ayala J A (2002). Topological characterization of the essential Escherichia coli cell division protein FtsW. FEMS Microbiol Lett, 216(1): 23–32

DOI

95
Leech R M, Thomson W W, Platt-Aloia K A (1981). Observations on the mechanism of chloroplast division in higher-plants. New Phytol, 87(1): 1–9

DOI

96
Low H H, Lowe J (2010). Dynamin architecture-from monomer to polymer. Curr Opin Struct Biol, 20(6): 791–798

DOI

97
Lowe J, Amos L A (1998). Crystal structure of the bacterial cell-division protein FtsZ. Nature, 391(6663): 203–206

DOI

98
Lowe J, van den Ent F, Amos L A (2004). Molecules of the bacterial cytoskeleton. Annu Rev Biophys Biomol Struct, 33(1): 177–198

DOI

99
Lutkenhaus J (2002). Dynamic proteins in bacteria. Curr Opin Microbiol, 5(6): 548–552

DOI

100
Lutkenhaus J (2007). Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem, 76(1): 539–562

DOI

101
Ma X, Ehrhardt D W, Margolin W (1996). Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. Proc Natl Acad Sci USA, 93(23): 12998–13003

DOI

102
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

103
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

DOI

104
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

DOI

105
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

DOI

106
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

DOI

107
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

DOI

108
Margolin W (2000). Themes and variations in prokaryotic cell division. FEMS Microbiol Rev, 24(4): 531–548

DOI

109
Margolin W (2001). Bacterial cell division: a moving MinE sweeper boggles the MinD. Curr Biol, 11(10): R395–R398

DOI

110
Marrison J L, Rutherford S M, 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

DOI

111
Martin W (2003). Gene transfer from organelles to the nucleus: Frequent and in big chunks. Proc Natl Acad Sci USA, 100(15): 8612–8614

DOI

112
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

DOI

113
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

DOI

114
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

DOI

115
McFadden G I (1999). Endosymbiosis and evolution of the plant cell. Curr Opin Plant Biol, 2(6): 513–519

DOI

116
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

DOI

117
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

118
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

DOI

119
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

DOI

120
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

DOI

121
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

DOI

122
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

DOI

123
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

DOI

124
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

125
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

DOI

126
Nakanishi H, Suzuki K, Kabeya Y, Miyagishima S Y (2009). Plant-specific protein MCD1 determines the site of chloroplast division in concert with bacteria-derived MinD. Curr Biol, 19(2): 151–156

DOI

127
Nogales E, Wolf S G, Downing K H (1998). Structure of the alpha beta tubulin dimer by electron crystallography. Nature, 391(6663): 199–203

DOI

128
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

DOI

129
Oross J W, Possingham J V (1989). Ultrastructural features of the constricted region of dividing plastids. Protoplasma, 150(2-3): 131–138

DOI

130
Osawa M, Anderson D E, Erickson H P (2008). Reconstitution of contractile FtsZ rings in liposomes. Science, 320(5877): 792–794

DOI

131
Osteryoung K W (2000). Organelle fission. Crossing the evolutionary divide. Plant Physiol, 123(4): 1213–1216

DOI

132
Osteryoung K W, McAndrew R S (2001). The plastid division machine. Annu Rev Plant Physiol Plant Mol Biol, 52(1): 315–333

DOI

133
Osteryoung K W, Nunnari J (2003). The division of endosymbiotic organelles. Science, 302(5651): 1698–1704

DOI

134
Osteryoung K W, Pyke K A (1998). Plastid division: evidence for a prokaryotically derived mechanism. Curr Opin Plant Biol, 1(6): 475–479

DOI

135
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

136
Osteryoung K W, Vierling E (1995). Conserved cell and organelle division. Nature, 376(6540): 473–474

DOI

137
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

DOI

138
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

DOI

139
Pichoff S, Lutkenhaus J (2007). Identification of a region of FtsA required for interaction with FtsZ. Mol Microbiol, 64(4): 1129–1138

DOI

140
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

DOI

141
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

DOI

142
Possingh J S (1969). Changes in chloroplast number per cell during leaf development in spinach. Planta, 86(2): 186–194

DOI

143
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

DOI

144
Pyke K A (1999). Plastid division and development. Plant Cell, 11: 549–556

145
Pyke K A, Leech R M (1994). A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol, 104: 201–207

146
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

147
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 dynamin-catalyzed vesicle scission. Mol Biol Cell, 20(22): 4630–4639

DOI

148
Ramachandran R, Surka M, Chappie J S, Fowler D M, 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

DOI

149
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

150
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

DOI

151
Raven J A, Allen J F (2003). Genomics and chloroplast evolution: what did cyanobacteria do for plants? Genome Biol, 4(3): 209

DOI

152
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

DOI

153
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

DOI

154
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

DOI

155
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

DOI

156
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

DOI

157
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

DOI

158
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

DOI

159
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

160
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

DOI

161
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

DOI

162
Rothfield L, Justice S, Garcia-Lara J (1999). Bacterial cell division. Annu Rev Genet, 33(1): 423–448

DOI

163
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

164
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

165
Saurer W, Possingham J V (1970). Studies on the growth of spinach leaves (Spinacea oleracea). J Exp Biol, 21: 151–158

166
Scheffers D, Driessen A J (2001). The polymerization mechanism of the bacterial cell division protein FtsZ. FEBS Lett, 506(1): 6–10

DOI

167
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

DOI

168
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

DOI

169
Scheffers D J, Driessen A J (2002). Immediate GTP hydrolysis upon FtsZ polymerization. Mol Microbiol, 43(6): 1517–1521

DOI

170
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

DOI

171
Sesaki H, Jensen R E (1999). Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J Cell Biol, 147(4): 699–706

DOI

172
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

DOI

173
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

DOI

174
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

DOI

175
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

DOI

176
Stokes K D, Osteryoung K W (2003). Early divergence of the FtsZ1 and FtsZ2 plastid division gene families in photosynthetic eukaryotes. Gene, 320: 97–108

DOI

177
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

DOI

178
Stricker J, Maddox P, Salmon E D, Erickson H P (2002). Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc Natl Acad Sci USA, 99(5): 3171–3175

DOI

179
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

DOI

180
Sun Q, Margolin W (1998). FtsZ dynamics during the division cycle of live Escherichia coli cells. J Bacteriol, 180: 2050–2056

181
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

DOI

182
Sweitzer S M, Hinshaw J E (1998). Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell, 93(6): 1021–1029

DOI

183
Taghbalout A, Ma L, Rothfield L (2006). Role of MinD-membrane association in Min protein interactions. J Bacteriol, 188(8): 2993–3001

DOI

184
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

DOI

185
Takano H, Takechi K (2010). Plastid peptidoglycan. Biochim Biophys Acta, 1800: 144–151

186
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

DOI

187
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

DOI

188
Tavva V S, Collins G B, Dinkins R D (2006). Targeted overexpression of the Escherichia coli MinC protein in higher plants results in abnormal chloroplasts. Plant Cell Rep, 25(4): 341–348

DOI

189
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

DOI

190
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

191
van den Ent F, Amos L, Lowe J (2001a). Bacterial ancestry of actin and tubulin. Curr Opin Microbiol, 4(6): 634–638

DOI

192
van den Ent F, Amos L A, Lowe J (2001b). Prokaryotic origin of the actin cytoskeleton. Nature, 413(6851): 39–44

DOI

193
van den Ent F, Moller-Jensen J, Amos L A, Gerdes K, Lowe J (2002). F-actin-like filaments formed by plasmid segregation protein ParM. EMBO J, 21(24): 6935–6943

DOI

194
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

DOI

195
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

DOI

196
Vitha S, McAndrew R S, Osteryoung K W (2001). FtsZ ring formation at the chloroplast division site in plants. J Cell Biol, 153(1): 111–120

DOI

197
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

DOI

198
Wang S, Arellano-Santoyo H, Combs P A, Shaevitz J W (2010). Actin-like cytoskeleton filaments contribute to cell mechanics in bacteria. Proc Natl Acad Sci USA, 107(20): 9182–9185

DOI

199
Warnock D E, Schmid S L (1996). Dynamin GTPase, a force-generating molecular switch. Bioessays, 18(11): 885–893

DOI

200
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

201
Weiss D S, Pogliano K, Carson M, Guzman L M, Fraipont C, Nguyen-Disteche M, Losick R, Beckwith J (1997). Localization of the Escherichia coli cell division protein Ftsl (PBP3) to the division site and cell pole. Mol Microbiol, 25(04): 671–681

DOI

202
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

DOI

203
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

204
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

DOI

205
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

DOI

206
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

DOI

207
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

DOI

208
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

DOI

209
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

DOI

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