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Origin and evolution of the chloroplast division machinery

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Abstract

Chloroplasts were originally established in eukaryotes by the endosymbiosis of a cyanobacterium; they then spread through diversification of the eukaryotic hosts and subsequent engulfment of eukaryotic algae by previously nonphotosynthetic eukaryotes. The continuity of chloroplasts is maintained by division of preexisting chloroplasts. Like their ancestors, chloroplasts use a bacterial division system based on the FtsZ ring and some associated factors, all of which are now encoded in the host nuclear genome. The majority of bacterial division factors are absent from chloroplasts and several new factors have been added by the eukaryotic host. For example, the ftsZ gene has been duplicated and modified, plastid-dividing (PD) rings were most likely added by the eukaryotic host, and a member of the dynamin family of proteins evolved to regulate chloroplast division. The identification of several additional proteins involved in the division process, along with data from diverse lineages of organisms, our current knowledge of mitochondrial division, and the mining of genomic sequence data have enabled us to begin to understand the universality and evolution of the division system. The principal features of the chloroplast division system thus far identified are conserved across several lineages, including those with secondary chloroplasts, and may reflect primeval features of mitochondrial division.

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References

  • Aldridge C, Maple J, Møller SG (2005) The molecular biology of plastid division in higher plants. J Exp Bot 56:1061–1077

    Article  PubMed  CAS  Google Scholar 

  • Arimura S, 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

    Article  PubMed  CAS  Google Scholar 

  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WW, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86

    Article  PubMed  CAS  Google Scholar 

  • Asano T, Yoshioka Y, Kurei S, Sakamoto W, Sodmergen, Machida Y (2004) A mutation of the CRUMPLED LEAF gene that encodes a protein localized in the outer envelope membrane of plastids affects the pattern of cell division, cell differentiation, and plastid division in Arabidopsis. Plant J 38:448–459

    Article  PubMed  CAS  Google Scholar 

  • Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972–977

    Article  PubMed  CAS  Google Scholar 

  • Beech PL, Gilson PR (2000) FtsZ and organelle division in protists. Protist 151:11–16

    PubMed  CAS  Google Scholar 

  • Beech PL, Nheu T, Schultz T, Herbert S, Lithgow T, Gilson PR, McFadden GI (2000) Mitochondrial FtsZ in a chromophyte alga. Science 287:1276–1279

    Article  PubMed  CAS  Google Scholar 

  • Bhattacharya D, Yoon HS, Hackett JD (2004) Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 26:50–60

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bleazard W, McCaffery JM, King EJ, Bale S, Mozdy A, Tieu Q, Nunnari J, Shaw JM (1999) The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol 1:298–304

    PubMed  CAS  Google Scholar 

  • Boffey SA, Lloyd D (1988) Division and segregation of organelles. Cambridge University Press, Cambridge

    Google Scholar 

  • Brown RC, Lemmon BE (1985) Preprophasic establishment of division polarity in monoplastidic mitosis of hornworts. Protoplasma 124:175–183

    Article  Google Scholar 

  • Cavalier-Smith T (2004) Only six kingdoms of life. Proc Biol Sci 271:1251–1262

    PubMed  CAS  Google Scholar 

  • Chida Y, Ueda K (1991) Division of chloroplasts in a green alga, Trebouxia potteri. Ann Bot 67:435–442

    Google Scholar 

  • Colletti KS, Tattersall EA, Pyke KA, Froelich JE, Stokes KD, Osteryoung KW (2000) A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol 10:507–516

    Article  PubMed  CAS  Google Scholar 

  • Douglas SE, Murphy CA, Spencer DF, Gray MW (1991) Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350:148–151

    Article  PubMed  CAS  Google Scholar 

  • Erickson HP (2000) Dynamin and FtsZ. Missing links in mitochondrial and bacterial division. J Cell Biol 148:1103–1105

    Article  PubMed  CAS  Google Scholar 

  • Errington J, Daniel RA, Scheffers DJ (2003) Cytokinesis in bacteria. Microbiol Mol Biol Rev 67:52–65

    PubMed  CAS  Google Scholar 

  • Fast NM, Kissinger JC, Roos DS, Keeling PJ (2001) Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol Biol Evol 18:418–426

    PubMed  CAS  Google Scholar 

  • Fraunholz MJ, Moerschel E, Maier UG (1998) The chloroplast division protein FtsZ is encoded by a nucleomorph gene in cryptomonads. Mol Gen Genet 260:207–211

    PubMed  CAS  Google Scholar 

  • Fujiwara M, Yoshida S (2001) Chloroplast targeting of chloroplast division FtsZ2 proteins in Arabidopsis. Biochem Biophys Res Commun 287:462–467

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gao H, Kadirjan-Kalbach D, Froehlich JE, Osteryoung KW (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci USA 100:4328–4333

    PubMed  CAS  Google Scholar 

  • Gilson PR, Yu XC, Hereld D, Barth C, Savage A, Kiefel BR, Lay S, Fisher PR, Margolin W, Beech PL (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

    Article  PubMed  CAS  Google Scholar 

  • Gray MW (1999) Evolution of organellar genomes. Curr Opin Genet Dev 9:678–687

    Article  PubMed  CAS  Google Scholar 

  • Harper JT, Keeling PJ (2003) Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol Biol Evol 20:1730–1735

    PubMed  CAS  Google Scholar 

  • Hashimoto H (1986) Double-ring structure around the constricting neck of dividing plastids of Avena sativa. Protoplasma 135:166–172

    Article  Google Scholar 

  • Hashimoto H (1997) Electron-opaque annular structure girdling the constricting isthmus of the dividing chloroplasts of Heterosigma akashiwo (Raphydophyceae, Chromophyta). Protoplasma 197:210–216

    Article  Google Scholar 

  • Hashimoto H (2004) Mitochondrion-dividing ring in an alga Nannochloropsis oculata (Eustigmatophyceae, Heterokonta). Cytologia 69:323–326

    Article  Google Scholar 

  • Hashimoto H (2005) The ultrastructural features and division of secondary plastids. J Plant Res DOI 10.1007/s10265-005-0214-6

  • Hashimoto H, Possingham JV (1989) Division and DNA distribution in ribosome-deficient plastids of the barley mutant “albostrians”. Protoplasma 149:20–23

    Article  Google Scholar 

  • Hinshaw JE, Schmid SL (1995) Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature 374:190–192

    Article  PubMed  CAS  Google Scholar 

  • Hirota Y, Ryter A, Jacob F (1968) Thermosensitive mutants of E. coli affected in the process of DNA synthesis and cellular division. Cold Spring Harbor Symp Quant Biol 33:677–693

    PubMed  CAS  Google Scholar 

  • Hong Z, Bednarek SY, Blumwald E, Hwang I, Jurgens G, Menzel D, Osteryoung KW, Raikhel NV, Shinozaki K, Tsutsumi N, Verma DP (2003) A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions. Plant Mol Biol 53:261–265

    PubMed  CAS  Google Scholar 

  • Iino M, Hashimoto H (2003) Intermediate features of cyanelle division of Cyanophora paradoxa (Glaucocystophyta) between cyanobacterial and plastid division. J Phycol 39:561–569

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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 44:776–781

    Article  PubMed  CAS  Google Scholar 

  • Kiefel BR, Gilson PR, Beech PL (2004) Diverse eukaryotes have retained mitochondrial homologues of the bacterial division protein FtsZ. Protist 155:105–115

    Article  PubMed  CAS  Google Scholar 

  • Kiessling J, Kruse S, Rensing SA, Harter K, Decker EL, Reski R (2000) Visualization of a cytoskeleton-like FtsZ network in chloroplasts. J Cell Biol 151:945–950

    Article  PubMed  CAS  Google Scholar 

  • Koch A, Schneider G, Luers GH, Schrader M (2004) Peroxisome elongation and constriction but not fission can occur independently of dynamin-like protein 1. J Cell Sci 117:3995–4006

    Article  PubMed  CAS  Google Scholar 

  • Koksharova OA, Wolk CP (2002) A novel gene that bears a DnaJ motif influences cyanobacterial cell division. J Bacteriol 184:5524–5528

    PubMed  CAS  Google Scholar 

  • Kuroiwa H, Mori T, Takahara M, Miyagishima S, Kuroiwa T (2002) Chloroplast division machinery as revealed by immunofluorescence and electron microscopy. Planta 215:185–190

    Article  PubMed  CAS  Google Scholar 

  • Kuroiwa T (1982) Mitochondrial nuclei. Int Rev Cytol 75:1–59

    PubMed  CAS  Google Scholar 

  • Kuroiwa T (1986) Mitochondria multiplication with mitochondrial nucleoids division. Kagaku 56:339–348

    Google Scholar 

  • Kuroiwa T (1989) The nuclei of cellular organelles and the formation of daughter organelles by the “plastid-dividing ring”. Bot Mag 102:291–329

    Google Scholar 

  • Kuroiwa T (1991) The replication, differentiation, and inheritance of plastids with emphasis on the concept of organelle nuclei. Int Rev Cytol 128:1–62

    CAS  Google Scholar 

  • Kuroiwa T, Suzuki T, Ogawa K, Kawano S (1981) The chloroplast nucleus: distribution, number, size, and a model for the multiplication of the chloroplast genome during development. Plant Cell Phsiol 22:381–396

    Google Scholar 

  • Kuroiwa T, Suzuki K, Kuroiwa H (1993) Mitochondrial division by an electron-dense ring in Cyanidioschyzon merolae. Protoplasma 175:173–177

    Article  Google Scholar 

  • Kuroiwa T, Suzuki K, Itoh R, Toda K, Okeefe TC, Kawano S (1995) Mitochondria-dividing ring: ultrastructural basis for the mechanisms of mitochondrial division in Chanidioschyzon merolae. Protoplasma 186:12–23

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Labrousse AM, Zappaterra MD, Rude DA, van der Bliek AM (1999) C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol Cell 4:815–826

    Article  PubMed  CAS  Google Scholar 

  • Leech RM, Thomson WW, Platt-Aloia KA (1981) Observations on the mechanism of chloroplast division in higher plants. New Phytol 87:1–9

    Google Scholar 

  • Legesse-Miller A, Massol RH, Kirchhausen T (2003) Constriction and Dnm1p recruitment are distinct processes in mitochondrial fission. Mol Biol Cell 14:1953–1963

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Maple J, Chua NH, Møller SG (2002) The topological specificity factor AtMinE1 is essential for correct plastid division site placement in Arabidopsis. Plant J 31:269–277

    Article  PubMed  CAS  Google Scholar 

  • Maple J, Fujiwara MT, Kitahata N, Lawson T, Baker NR, Yoshida S, Møller SG (2004) GIANT CHLOROPLAST 1 is essential for correct plastid division in Arabidopsis. Curr Biol 14:776–781

    Article  PubMed  CAS  Google Scholar 

  • Margolin W (2000) Self-assembling GTPase caught in the middle. Curr Biol 10:R328–R330

    Article  PubMed  CAS  Google Scholar 

  • Marrison JL, Rutherford SM, Robertson EJ, Lister C, Dean C, Leech RM (1999) The distinctive roles of five different ARC genes in the chloroplast division process in Arabidopsis. Plant J 18:651–662

    Article  PubMed  CAS  Google Scholar 

  • Matsuzaki M, Kikuchi T, Kita K, Kojima S, Kuroiwa T (2001) Large amounts of apicoplast nucleoid DNA and its segregation in Toxoplasma gondii. Protoplasma 218:180–191

    Article  PubMed  CAS  Google Scholar 

  • Matsuzaki M, Misumi O, Shin-I T, Maruyama S, Takahara M, Miyagishima S, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657

    Article  PubMed  CAS  Google Scholar 

  • 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 52:1145–1158

    Article  PubMed  CAS  Google Scholar 

  • McAndrew RS, Froehlich JE, Vitha S, Stokes KD, Osteryoung KW (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

    Article  PubMed  CAS  Google Scholar 

  • McFadden GI (2001) Primary and secondary endosymbiosis and the origin of plastids. J Phycol 37:951–959

    Article  Google Scholar 

  • Misumi O, Matsuzaki M, Nozaki H, Miyagishima S, Mori T, Nishida K, Yagisawa F, Yoshida Y, Kuroiwa H, Kuroiwa T (2005) Cyanidioschyzon merolae genome. A tool for facilitating comparable studies on organelle biogenesis in photosynthetic eukaryotes. Plant Physiol 137:567–585

    Article  PubMed  CAS  Google Scholar 

  • Mita T, Kuroiwa T (1988) Division of plastids by a plastid-dividing ring in Cyanidium caldarium. Protoplasma 146(Suppl 1):133–152

    Google Scholar 

  • Mita T, Kanbe T, Tanaka K, Kuroiwa T (1986) A ring structure around the dividing plane of the Cyanidium caldarium chloroplast. Protoplasma 130:211–213

    Article  Google Scholar 

  • Miyagishima S, Itoh R, Toda K, Takahashi H, Kuroiwa H, Kuroiwa T (1998a) Identification of a triple ring structure involved in plastid division in the primitive red alga Cyanidioschyzon merolae. J Electron Microsc 47:269–272

    Google Scholar 

  • Miyagishima S, Itoh R, Toda K, Takahashi H, Kuroiwa H, Kuroiwa T (1998b) Orderly formation of the double ring structures for plastid and mitochondrial division in the unicellular red alga Cyanidioschyzon merolae. Planta 206:551–560

    Article  CAS  Google Scholar 

  • Miyagishima S, Itoh R, Toda K, Kuroiwa H, Kuroiwa T (1999a) Real-time analyses of chloroplast and mitochondrial division and differences in the behaviour of their dividing rings during contraction. Planta 207:343–353

    Article  CAS  Google Scholar 

  • Miyagishima S, Itoh R, Toda K, Kuroiwa H, Nishimura M, Kuroiwa T (1999b) Microbody proliferation and segregation cycle in the single-microbody alga Cyanidioschyzon merolae. Planta 208:326–336

    Article  CAS  Google Scholar 

  • Miyagishima S, Kuroiwa H, Kuroiwa T (2001a) The timing and manner of disassembly of the apparatuses for chloroplast and mitochondrial division in the red alga Cyanidioschyzon merolae. Planta 212:517–528

    Article  PubMed  CAS  Google Scholar 

  • Miyagishima S, Takahara M, Kuroiwa T (2001b) Novel filaments 5 nm in diameter constitute the cytosolic ring of the plastid division apparatus. Plant Cell 13:707–721

    PubMed  CAS  Google Scholar 

  • Miyagishima S, Takahara M, Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2001c) Plastid division is driven by a complex mechanism that involves differential transition of the bacterial and eukaryotic division rings. Plant Cell 13:2257–2268

    CAS  Google Scholar 

  • Miyagishima S, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (2003a) A plant-specific dynamin-related protein forms a ring at the chloroplast division site. Plant Cell 15:655–665

    Article  PubMed  CAS  Google Scholar 

  • Miyagishima S, Nishida K, Kuroiwa T (2003b) An evolutionary puzzle: chloroplast and mitochondrial division rings. Trends Plant Sci 8:432–438

    Article  PubMed  CAS  Google Scholar 

  • Miyagishima S, Nozaki H, Nishida K, Nishida K, Matsuzaki M, Kuroiwa T (2004) Two types of FtsZ proteins in mitochondria and red-lineage chloroplasts: the duplication of FtsZ is implicated in endosymbiosis. J Mol Evol 58:291–303

    Article  PubMed  CAS  Google Scholar 

  • Miyagishima S, Wolk CP, Osteryoung KW (2005) Identification of cyanobacterial cell division genes by comparative and mutational analyses. Mol Microbiol 56:126–143

    Article  PubMed  CAS  Google Scholar 

  • Morgan GW, Goulding D, Field MC (2004) The single dynamin-like protein of Trypanosoma brucei regulates mitochondrial division and is not required for endocytosis. J Biol Chem 279:10692–10701

    PubMed  CAS  Google Scholar 

  • Mori T, Kuroiwa H, Takahara M, Miyagishima S, Kuroiwa T (2001) Visualization of an FtsZ ring in chloroplasts of Lilium longiflorum leaves. Plant Cell Physiol 42:555–559

    PubMed  CAS  Google Scholar 

  • 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 95:2885–2890

    Article  PubMed  CAS  Google Scholar 

  • Nishida K, Takahara M, Miyagishima S, Kuroiwa H, Matsuzaki M, Kuroiwa T (2003) Dynamic recruitment of dynamin for final mitochondrial severance in a primitive red alga. Proc Natl Acad Sci USA 100:2146–2151

    Article  PubMed  CAS  Google Scholar 

  • Nozaki H, Matsuzaki M, Takahara M, Misumi O, Kuroiwa H, Hasegawa M, Shin-i T, Kohara Y, Ogasawara N, Kuroiwa T (2003) The phylogenetic position of red algae revealed by multiple nuclear genes from mitochondria-containing eukaryotes and an alternative hypothesis on the origin of plastids. J Mol Evol 56:485–497

    Article  PubMed  CAS  Google Scholar 

  • Ogawa S, Ueda K, Noguchi T (1995) Division apparatus of chloroplast in Nannochloris bacillaris. J Phycol 31:132–137

    Article  Google Scholar 

  • Oross JW, Possingham JV (1989) Ultrastructural features of the constricted region of dividing plastids. Protoplasma 150:131–138

    Article  Google Scholar 

  • Osteryoung KW, McAndrew RS (2001) The plastid division machine. Annu Rev Plant Physiol Plant Mol Biol 52:315–333

    Article  PubMed  CAS  Google Scholar 

  • Osteryoung KW, Nunnari J (2003) The division of endosymbiotic organelles. Science 302:1698–1704

    Article  PubMed  CAS  Google Scholar 

  • Osteryoung KW, Vierling E (1995) Conserved cell and organelle division. Nature 376:473–474

    Article  PubMed  CAS  Google Scholar 

  • Osteryoung KW, Stokes KD, Rutherford SM, Percival AL, Lee WY (1998) Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell 10:1991–2004

    Article  PubMed  CAS  Google Scholar 

  • Possingham JV, Lawrence ME (1983) Controls to plastid division. Int Rev Cytol 84:1–56

    CAS  Google Scholar 

  • Praefcke GJ, McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5:133–147

    Article  PubMed  CAS  Google Scholar 

  • Pyke KA, Leech RM (1992) Nuclear mutations radically alter chloroplast division and expansion in A. thaliana. Plant Physiol 99:1005–1008

    Article  CAS  PubMed  Google Scholar 

  • Pyke KA, Leech RM (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol 104:201–207

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Reddy MS, Dinkins R, Collins GB (2002) Overexpression of the Arabidopsis thaliana MinE1 bacterial division inhibitor homologue gene alters chloroplast size and morphology in transgenic Arabidopsis and tobacco plants. Planta 215:167–176

    Article  PubMed  CAS  Google Scholar 

  • Robertson EJ, Rutherford SM, Leech RM (1996) Characterization of chloroplast division using the Arabidopsis mutant arc5. Plant Physiol 112:149–159

    Article  PubMed  CAS  Google Scholar 

  • Schimper AFW (1883) Über die Entwicklung der Chlorophyllkörner und Farbkörper. Bot Zeit 41:105–112

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sever S, Damke H, Schmid SL (2000) Dynamin: GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J Cell Biol 150:1137–1148

    Article  PubMed  CAS  Google Scholar 

  • 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 45:960–967

    PubMed  CAS  Google Scholar 

  • Stiller JW, Riley J, Hall BD (2001) Are red algae plants? A critical evaluation of three key molecular data sets. J Mol Evol 52:527–539

    PubMed  CAS  Google Scholar 

  • Stokes KD, Osteryoung KW (2003) Early divergence of the FtsZ1 and FtsZ2 plastid division gene families in photosynthetic eukaryotes. Gene 320:97–108

    Article  PubMed  CAS  Google Scholar 

  • Strepp R, Scholz S, Kruse S, Speth V, Reski R (1998) Plant molecular 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 95:4368–4373

    Article  PubMed  CAS  Google Scholar 

  • Striepen B, Crawford MJ, Shaw MK, Tilney LG, Seeber F, Roos DS (2000) The plastid of Toxoplasma gondii is divided by association with the centrosomes. J Cell Biol 151:1423–1434

    Article  PubMed  CAS  Google Scholar 

  • Suzuki K, Ueda R (1975) Electron microscope observations on plastid division in root meristematic cells of Pisum sativum L. Bot Mag 88:319–321

    Article  Google Scholar 

  • Suzuki K, Ehara T, Osafune T, Kuroiwa H, Kawano S, Kuroiwa T (1994) Behavior of mitochondria, chloroplasts and their nuclei during the mitotic cycle in the ultramicroalga Cyanidioschyzon merolae. Eur J Cell Biol 63:280–288

    PubMed  CAS  Google Scholar 

  • Takahara M, Takahashi H, Matsunaga S, Miyagishima S, Sakai A, Kawano S, Kuroiwa T (2000) A putative mitochondrial ftsZ gene is encoded in the unicellular primitive red alga Cyanidioschyzon merolae. Mol Gen Genet 264:452–460

    PubMed  CAS  Google Scholar 

  • Takahara M, Kuroiwa H, Miyagishima S, Mori T, Kuroiwa T (2001) Localization of the mitochondrial FtsZ protein in a dividing mitochondrion. Cytologia 66:421–425

    Google Scholar 

  • Takei K, McPherson PS, Schmid SL, De Camilli P (1995) Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature 374:186–190

    Article  PubMed  CAS  Google Scholar 

  • Terui S, Suzuki K, Takahashi H, Itoh R, Kuroiwa T (1995) Synchronization of chloroplast division in the ultramicroalga Cyanidioschyzon merolae (Rhodophyta) by treatment with light and aphidicolin. J Phycol 31:958–961

    Article  Google Scholar 

  • Van de Peer Y, De Wachter R (1997) Evolutionary relationships among the eukaryotic crown taxa taking into account site-to-site rate variation in 18S rRNA. J Mol Evol 45:619–630

    PubMed  Google Scholar 

  • Vitha S, McAndrew RS, Osteryoung KW (2001) FtsZ ring formation at the chloroplast division site in plants. J Cell Biol 153:111–119

    Article  PubMed  CAS  Google Scholar 

  • Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW (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

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Kong D, Wang Y, Hu Y, He Y, Sun J (2003) Isolation of two plastid division ftsZ genes from Chlamydomonas reinhardtii and its evolutionary implication for the role of FtsZ in plastid division. J Exp Bot 54:1115–1116

    PubMed  CAS  Google Scholar 

  • Weiss DS (2004) Bacterial cell division and the septal ring. Mol Microbiol 54:588–597

    Article  PubMed  CAS  Google Scholar 

  • Yoon HS, Hackett JD, Pinto G, Bhattacharya D (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99:15507–15512

    PubMed  CAS  Google Scholar 

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Acknowledgements

I am deeply indebted to Dr. Tsuneyoshi Kuroiwa (Rikkyo University) and past and present members of his laboratory for their guidance. I am also grateful to Dr. Katherine W. Osteryoung (Michigan State University) and past and present members of her laboratory for the opportunity to pursue further studies. I also thank Dr. C. Peter Wolk (Michigan State University) and members of his laboratory for helpful discussions about cyanobacteria. I also thank Mary Fantacone for editorial help. A portion of my study is supported by a JSPS (Japan Society for the Promotion of Science) Postdoctoral Research Fellowship for Research Abroad to S.M.

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Correspondence to Shin-ya Miyagishima.

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Shin-ya Miyagishima is the recipient of the Botanical Society Award for Young Scientists, 2004.

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Miyagishima, Sy. Origin and evolution of the chloroplast division machinery. J Plant Res 118, 295–306 (2005). https://doi.org/10.1007/s10265-005-0226-2

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