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Two Types of FtsZ Proteins in Mitochondria and Red-Lineage Chloroplasts: The Duplication of FtsZ Is Implicated in Endosymbiosis

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Abstract

The ancestors of plastids and mitochondria were once free-living bacteria that became organelles as a result of endosymbiosis. According to this theory, a key bacterial division protein, FtsZ, plays a role in plastid division in algae and plants as well as in mitochondrial division in lower eukaryotes. Recent studies have shown that organelle division is a process that combines features derived from the bacterial division system with features contributed by host eukaryotic cells. Two nonredundant versions of FtsZ, FtsZ1 and FtsZ2, have been identified in green-lineage plastids, whereas most bacteria have a single ftsZ gene. To examine whether there is also more than one type of FtsZ in red-lineage chloroplasts (red algal chloroplasts and chloroplasts that originated from the secondary endosymbiosis of red algae) and in mitochondria, we obtained FtsZ sequences from the complete sequence of the primitive red alga Cyanidioschyzon merolae and the draft sequence of the stramenopile (heterokont) Thalassiosira pseudonana. Phylogenetic analyses that included known FtsZ proteins identified two types of chloroplast FtsZ in red algae (FtsZA and FtsZB) and stramenopiles (FtsZA and FtsZC). These analyses also showed that FtsZB emerged after the red and green lineages diverged, while FtsZC arose by the duplication of an ftsZA gene that in turn descended from a red alga engulfed by the ancestor of stramenopiles. A comparison of the predicted proteins showed that like bacterial FtsZ and green-lineage FtsZ2, FtsZA has a short conserved C-termmal sequence (the C-terminal core domain), whereas FtsZB and FtsZC, like the green-lineage FtsZ1, lack this sequence. In addition, the Cyanidioschyzon and Dictyostelium genomes encode two types of mitochondrial FtsZ proteins, one of which lacks the C-terminal variable domain. These results suggest that the acquisition of an additional FtsZ protein with a modified C terminus was common to the primary and secondary endosymbioses that produced plastids and that this also occurred during the establishment of mitochondria, presumably to regulate the multiplication of these organelles.

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References

  1. J Adachi M Hasegawa (1996) ArticleTitleMOLPHY version 2.3: Programs for molecular phylogenetics based on maximum likelihood. Comput Sci Monogr 28 1–150

    Google Scholar 

  2. MB Allen (1959) ArticleTitleStudies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch Microbiol 32 270–277 Occurrence Handle1:STN:280:CyaD2MjmvVI%3D

    CAS  Google Scholar 

  3. Y Araki S Takio K Ono H Takano (2003) ArticleTitleTwo types of plastid ftsZ genes in the liverwort Marchantia polymorpha. Protoplasma 221 163–173 Occurrence Handle1:CAS:528:DC%2BD3sXksFWmsbc%3D Occurrence Handle12802623

    CAS  PubMed  Google Scholar 

  4. PL Beech PR Gilson (2000) ArticleTitleFtsZ and organelle division in Protists. Protist 151 11–16 Occurrence Handle1:CAS:528:DC%2BD3cXnsF2isrs%3D Occurrence Handle10896129

    CAS  PubMed  Google Scholar 

  5. PL Beech T Nheu T Schultz S Herbert T Lithgow PR Gilson GI McFadden (2000) ArticleTitleMitochondrial FtsZ in a chromophyte alga. Science 287 1276–1279 Occurrence Handle10.1126/science.287.5456.1276 Occurrence Handle1:CAS:528:DC%2BD3cXhtlOqsbs%3D Occurrence Handle10678836

    Article  CAS  PubMed  Google Scholar 

  6. D Bramhill (1997) ArticleTitleBacterial cell division. Annu Rev Cell Dev Biol 13 395–424 Occurrence Handle10.1146/annurev.cellbio.13.1.395 Occurrence Handle1:CAS:528:DyaK1cXisFSrsg%3D%3D Occurrence Handle9442879

    Article  CAS  PubMed  Google Scholar 

  7. T Cavalier-Smith (2000) ArticleTitleMembrane heredity and early chloroplast evolution. Trends Plant Sci 5 174–182 Occurrence Handle10.1016/S1360-1385(00)01598-3 Occurrence Handle1:STN:280:DC%2BD3c3gslWntQ%3D%3D Occurrence Handle10740299

    Article  CAS  PubMed  Google Scholar 

  8. KS Colletti EA Tattersall KA Pyke JE Froelich KD Stokes KW Osteryoung (2000) ArticleTitleA homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol 10 507–516 Occurrence Handle10.1016/S0960-9822(00)00466-8 Occurrence Handle1:CAS:528:DC%2BD3cXjt1Cjur0%3D Occurrence Handle10801439

    Article  CAS  PubMed  Google Scholar 

  9. MO Dayhoff RM Schwartz BC Orcutt (1978) A model of evolutionary change in proteins. MO Dayhoff (Eds) Atlas of protein sequence and structure, Vol 5, Suppl 3. National Biomedical Research Foundation Washington, DC 345–352

    Google Scholar 

  10. N Din EM Quardokus MJ Sackett YV Brun (1998) ArticleTitleDominant C-terminal deletions of FtsZ that affect its ability to localize in Caulobacter and its interaction with FtsA. Mol Microbiol 27 1051–1063 Occurrence Handle10.1046/j.1365-2958.1998.00752.x Occurrence Handle1:CAS:528:DyaK1cXhs1ygu7w%3D Occurrence Handle9535094

    Article  CAS  PubMed  Google Scholar 

  11. SE Douglas CA Murphy DF Spencer MW Gray (1991) ArticleTitleCryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350 148–151 Occurrence Handle10.1038/350148a0 Occurrence Handle1:CAS:528:DyaK3MXit1amuro%3D Occurrence Handle2005963

    Article  CAS  PubMed  Google Scholar 

  12. NM Fast JC Kissinger DS Roos PJ Keeling (2001) ArticleTitleNuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol Biol Evol 18 418–426 Occurrence Handle1:CAS:528:DC%2BD3MXhvVKrt78%3D Occurrence Handle11230543

    CAS  PubMed  Google Scholar 

  13. J Felsenstein (1993) PHYLIP (phylogeny inference package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington Seattle

    Google Scholar 

  14. MJ Fraunholz E Moerschel UG Maier (1998) ArticleTitleThe chloroplast division protein FtsZ is encoded by a nucleomorph gene in cryptomonads. Mol Gen Genet 260 207–211 Occurrence Handle10.1007/s004380050887 Occurrence Handle1:CAS:528:DyaK1MXjvFWn Occurrence Handle9862473

    Article  CAS  PubMed  Google Scholar 

  15. H Fulgosi L Gerdes S Westphal C Glockmann J Soll (2002) ArticleTitleCell and chloroplast division requires ARTEMIS. Proc Natl Acad Sci USA 99 11501–11506 Occurrence Handle10.1073/pnas.172032599 Occurrence Handle1:CAS:528:DC%2BD38XmslSls70%3D Occurrence Handle12169665

    Article  CAS  PubMed  Google Scholar 

  16. H Gao D Kadirjan-Kalbach JE Froehlich KW Osteryoung (2003) ArticleTitleARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci USA 100 4328–4333 Occurrence Handle10.1073/pnas.0530206100 Occurrence Handle1:CAS:528:DC%2BD3sXivFWjsbs%3D Occurrence Handle12642673

    Article  CAS  PubMed  Google Scholar 

  17. PR Gilson PL Beech (2001) ArticleTitleCell division protein FtsZ: Running rings around bacteria, chloroplasts and mitochondria. Res Microbiol 152 3–10 Occurrence Handle10.1016/S0923-2508(00)01162-1 Occurrence Handle1:CAS:528:DC%2BD3MXisVCisLg%3D Occurrence Handle11281323

    Article  CAS  PubMed  Google Scholar 

  18. MW Gray (1999) ArticleTitleEvolution of organellar genomes. Curr Opin Genet Dev 9 678–687 Occurrence Handle1:CAS:528:DC%2BD3cXhslOitw%3D%3D Occurrence Handle10607615

    CAS  PubMed  Google Scholar 

  19. CA Hale AC Rhee PA de Boer (2000) ArticleTitleZipA-induced bundling of FtsZ polymers mediated by an interaction between C-terminal domains. J Bacteriol 182 5153–5166 Occurrence Handle1:CAS:528:DC%2BD3cXmsVOqurg%3D Occurrence Handle10960100

    CAS  PubMed  Google Scholar 

  20. M Hasegawa H Kishino (1994) ArticleTitleAccuracies of the simple methods for estimating the bootstrap probability of a maximum-likelihood tree. Mol Biol Evol 11 142–145 Occurrence Handle1:CAS:528:DyaK2cXht1yqu7Y%3D

    CAS  Google Scholar 

  21. H Hashimoto (2003) ArticleTitlePlastid division: its origins and evolution. Int Rev Cytol 222 63–98 Occurrence Handle12503847

    PubMed  Google Scholar 

  22. R Itoh M Fujiwara N Nagata S Yoshida (2001) ArticleTitleA chloroplast protein homologous to the eubacterial topological specificity factor minE plays a role in chloroplast division. Plant Physiol 127 1644–1655 Occurrence Handle1:CAS:528:DC%2BD38XjtVWmtg%3D%3D Occurrence Handle11743109

    CAS  PubMed  Google Scholar 

  23. DT Jones WR Taylor JM Thornton (1992) ArticleTitleThe rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8 275–282 Occurrence Handle1:CAS:528:DyaK38Xlt1Okt7w%3D Occurrence Handle1633570

    CAS  PubMed  Google Scholar 

  24. M Kimura (1983) The neutral theory of molecular evolution. Cambridge University Press Cambridge, UK

    Google Scholar 

  25. H Kishino M Hasegawa (1989) ArticleTitleEvaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29 170–179 Occurrence Handle1:CAS:528:DyaL1MXkvFCnsbc%3D Occurrence Handle2509717

    CAS  PubMed  Google Scholar 

  26. H Kishino T Miyata M Hasegawa (1990) ArticleTitleMaximum likelihood inference of protein phylogeny, and the origin of chloroplasts. J Mol Evol 31 151–160 Occurrence Handle1:CAS:528:DyaK3cXlt1yqtLw%3D

    CAS  Google Scholar 

  27. OA Koksharova CP Wolk (2002) ArticleTitleA novel gene that bears a DnaJ motif influences cyanobacterial cell division. J Bacteriol 184 5524–5528 Occurrence Handle1:CAS:528:DC%2BD38Xnt1eht7k%3D Occurrence Handle12218043

    CAS  PubMed  Google Scholar 

  28. H Kuroiwa T Mori M Takahara S Miyagishima T Kuroiwa (2002) ArticleTitleChloroplast division machinery as revealed by immunofluorescence and electron microscopy. Planta 215 185–190 Occurrence Handle1:CAS:528:DC%2BD38Xjsl2rtrs%3D Occurrence Handle12029466

    CAS  PubMed  Google Scholar 

  29. T Kuroiwa H Kuroiwa A Sakai H Takahashi K Toda R Itoh (1998) ArticleTitleThe division apparatus of plastids and mitochondria. Int Rev Cytol 181 1–141 Occurrence Handle1:STN:280:DyaK1c7ot12htw%3D%3D Occurrence Handle9522454

    CAS  PubMed  Google Scholar 

  30. Z Liu A Mukherjee J Lutkenhaus (1999) ArticleTitleRecruitment of ZipA to the division site by interaction with FtsZ. Mol Microbiol 31 1853–1861 Occurrence Handle1:CAS:528:DyaK1MXisVenuro%3D Occurrence Handle10209756

    CAS  PubMed  Google Scholar 

  31. XL Ma W Margolin (1999) ArticleTitleGenetic and Functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol 181 7531–7544 Occurrence Handle1:CAS:528:DyaK1MXotVKjtbc%3D Occurrence Handle10601211

    CAS  PubMed  Google Scholar 

  32. X Ma DW Ehrhardt W Margolin (1996) ArticleTitleColocalization 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 12998–13003 Occurrence Handle1:CAS:528:DyaK28XmvV2ksbY%3D Occurrence Handle8917533

    CAS  PubMed  Google Scholar 

  33. RS McAndrew JE Froehlich S Vitha KD Stokes KW Osteryoung (2001) ArticleTitleColocalization 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 Occurrence Handle1:CAS:528:DC%2BD38XjtVWmtw%3D%3D Occurrence Handle11743110

    CAS  PubMed  Google Scholar 

  34. W Martin B Stoebe V Goremykin S Hapsmann M Hasegawa KV Kowallik (1998) ArticleTitleGene transfer to the nucleus and the evolution of chloroplasts. Nature 393 162–165 Occurrence Handle1:CAS:528:DyaK1cXjt1ahsL0%3D Occurrence Handle11560168

    CAS  PubMed  Google Scholar 

  35. GI McFadden (2001) ArticleTitlePrimary and secondary endosymbiosis and the origin of plastids. J Phycol 37 951–959

    Google Scholar 

  36. S Miyagishima M Takahara T Kuroiwa (2001a) ArticleTitleNovel filaments 5 nm in diameter constitute the cytosolic ring of the plastid division apparatus. Plant Cell 13 707–721 Occurrence Handle1:CAS:528:DC%2BD3MXis1akt7s%3D

    CAS  Google Scholar 

  37. S Miyagishima M Takahara T Mori H Kuroiwa T Higashiyama T Kuroiwa (2001b) ArticleTitlePlastid division is driven by a complex mechanism that involves differential transition of the bacterial and eukaryotic division rings. Plant Cell 13 2257–2268 Occurrence Handle1:CAS:528:DC%2BD3MXotVegsr4%3D

    CAS  Google Scholar 

  38. S Miyagishima K Nishida T Mori M Matsuzaki T Higashiyama H Kuroiwa T Kuroiwa (2003a) ArticleTitleA plant-specific dynamin- related protein forms a ring at the chloroplast division site. Plant Cell 15 655–665 Occurrence Handle1:CAS:528:DC%2BD3sXisVektLs%3D

    CAS  Google Scholar 

  39. S Miyagishima K Nishida T Kuroiwa (2003b) ArticleTitleAn evolutionary puzzle: Chloroplast and mitochondrial division rings. Trends Plant Sci 8 432–438 Occurrence Handle1:CAS:528:DC%2BD3sXnt1alsb4%3D

    CAS  Google Scholar 

  40. D Moreira H Le Guyader H Philippe (2000) ArticleTitleThe origin of red algae and the evolution of chloroplasts. Nature 405 69–72 Occurrence Handle1:STN:280:DC%2BD3c3mvFemtA%3D%3D Occurrence Handle10811219

    CAS  PubMed  Google Scholar 

  41. T Mori H Kuroiwa M Takahara S Miyagishima T Kuroiwa (2001) ArticleTitleVisualization of an FtsZ ring in chloroplasts of Lilium longiflorum leaves. Plant Cell Physiol 42 555–559 Occurrence Handle1:CAS:528:DC%2BD3MXks1CrtbY%3D Occurrence Handle11427673

    CAS  PubMed  Google Scholar 

  42. L Mosyak Y Zhang E Glasfeld S Haney M Stahl J Seehra WS Somers (2000) ArticleTitleThe bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J 19 3179–3191 Occurrence Handle1:CAS:528:DC%2BD3cXlt1ajtb8%3D Occurrence Handle10880432

    CAS  PubMed  Google Scholar 

  43. K Nishida M Takahara S Miyagishima H Kuroiwa M Matsuzaki T Kuroiwa (2003) ArticleTitleDynamic recruitment of dynamin for final mitochondrial severance in a primitive red alga. Proc Natl Acad Sci USA 100 2146–2151 Occurrence Handle1:CAS:528:DC%2BD3sXhsFGrt70%3D Occurrence Handle12566569

    CAS  PubMed  Google Scholar 

  44. N Ohta N Sato T Kuroiwa (1998) ArticleTitleStructure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence. Nucleic Acids Res 26 5190–5198 Occurrence Handle1:CAS:528:DyaK1cXnvF2ju78%3D Occurrence Handle9801318

    CAS  PubMed  Google Scholar 

  45. N Ohta M Matsuzaki O Misumi S Miyagishima H Nozaki K Tanaka T Shin-i Y Kohara T Kuroiwa (2003) ArticleTitleComplete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res 10 67–77 Occurrence Handle1:CAS:528:DC%2BD3sXjsFCqsLs%3D Occurrence Handle12755171

    CAS  PubMed  Google Scholar 

  46. KW Osteryoung (2002) ArticleTitleOrganelle fission in eukaryotes. Curr Opin Microbiol 4 639–646

    Google Scholar 

  47. KW Osteryoung RS McAndrew (2001) ArticleTitleThe plastid division machine. Annu Rev Plant Physiol Plant Mol Biol 52 315–333 Occurrence Handle1:CAS:528:DC%2BD3MXkslWgsLc%3D Occurrence Handle11337401

    CAS  PubMed  Google Scholar 

  48. KW Osteryoung E Vierling (1995) ArticleTitleConserved cell and organelle division. Nature 376 473–474 Occurrence Handle1:CAS:528:DyaK2MXnsVCrs74%3D Occurrence Handle7637778

    CAS  PubMed  Google Scholar 

  49. KW Osteryoung KD Stokes SM Rutherford AL Percival WY Lee (1998) ArticleTitleChloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell 10 1991–2004 Occurrence Handle1:CAS:528:DyaK1MXhvV2ntw%3D%3D Occurrence Handle9836740

    CAS  PubMed  Google Scholar 

  50. H Philippe (2000) ArticleTitleLong branch attraction and protist phylogeny. Protist 151 307–316 Occurrence Handle1:STN:280:DC%2BD3M3jt1Oqtg%3D%3D Occurrence Handle11212891

    CAS  PubMed  Google Scholar 

  51. N Saitou M Nei (1987) ArticleTitleThe neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4 406–425 Occurrence Handle1:STN:280:BieC1cbgtVY%3D Occurrence Handle3447015

    CAS  PubMed  Google Scholar 

  52. H Shimodaira M Hasegawa (1999) ArticleTitleMultiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16 1114–1116 Occurrence Handle1:CAS:528:DyaK1MXltVyksrg%3D

    CAS  Google Scholar 

  53. H Shimodaira M Hasegawa (2001) ArticleTitleCONSEL: For assessing the confidence of phylogenetic tree selection. Bioinformatics 17 1246–1247 Occurrence Handle1:STN:280:DC%2BD38%2FgtFOlsw%3D%3D Occurrence Handle11751242

    CAS  PubMed  Google Scholar 

  54. R Strepp S Scholz S Kruse V Speth R Reski (1998) ArticleTitlePlant 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 Occurrence Handle1:CAS:528:DyaK1cXis1Ohurk%3D Occurrence Handle9539743

    CAS  PubMed  Google Scholar 

  55. K Strimmer A Von Haeseler (1996) ArticleTitleQuartet puzzling: A quartet maximum-likelihood method for reconstructing tree topologies. Mol Biol Evol 13 964–969

    Google Scholar 

  56. DL Swofford (2002) PAUP* 4.0: Phylogenetic analysis using parsimony, version 4.0b 10. Computer program distributed by Sinauer Associates Sunderland, MA

    Google Scholar 

  57. M Takahara H Takahashi S Matsunaga S Miyagishima H Takano A Sakai S Kawano T Kuroiwa (2000) ArticleTitleA putative mitochondrial ftsZ gene is present in the unicellular primitive red alga Cyanidioschyzon merolae. Mol Gen Genet 264 452–460 Occurrence Handle1:CAS:528:DC%2BD3MXhtFWkug%3D%3D Occurrence Handle11129049

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  59. JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25 4876–4882 Occurrence Handle10.1093/nar/25.24.4876 Occurrence Handle1:CAS:528:DyaK1cXntFyntQ%3D%3D Occurrence Handle9396791

    Article  CAS  PubMed  Google Scholar 

  60. K Toda H Takahashi R Itoh T Kuroiwa (1995) ArticleTitleDNA contents in two Cyanidiophyceae: Cyanidioschyzon merolae and Cyanidium caldarium Forma A. Cytologia 60 183–188

    Google Scholar 

  61. S Vitha RS McAndrew KW Osteryoung (2001) ArticleTitleFtsZ ring formation at the chloroplast division site in plants. J Cell Biol 153 111–120 Occurrence Handle1:CAS:528:DC%2BD3MXisVyhtLY%3D Occurrence Handle11285278

    CAS  PubMed  Google Scholar 

  62. S Vitha JE Froehlich O Koksharova KA Pyke H van Erp KW Osteryoung (2003) ArticleTitleARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15 1918–1933 Occurrence Handle1:CAS:528:DC%2BD3sXms1WlsbY%3D Occurrence Handle12897262

    CAS  PubMed  Google Scholar 

  63. D Wang D Kong Y Wang Y Hu Y He J Sun (2003) ArticleTitleIsolation 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 Occurrence Handle1:CAS:528:DC%2BD3sXivFWmsbg%3D Occurrence Handle12598582

    CAS  PubMed  Google Scholar 

  64. X Wang J Huang A Mukherjee C Cao J Lutkenhaus (1997) ArticleTitleAnalysis of the interaction of FtsZ with itself, GTP, and FtsA. J Bacteriol 179 5551–5559 Occurrence Handle1:CAS:528:DyaK2sXlvFWgt7w%3D Occurrence Handle9287012

    CAS  PubMed  Google Scholar 

  65. K Yan KH Pearce DJ Payne (2000) ArticleTitleA conserved residue at the extreme C-terminus of FtsZ is critical for the FtsA-FtsZ interaction in Staphylococcus aureus. Biochem Biophys Res Commun 270 387–392 Occurrence Handle1:CAS:528:DC%2BD3cXit1CqsbY%3D Occurrence Handle10753635

    CAS  PubMed  Google Scholar 

  66. HS Yoon JD Hackett D Bhattacharya (2002a) ArticleTitleA single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc Natl Acad Sci USA 99 11724–11729 Occurrence Handle1:CAS:528:DC%2BD38XntFWqtrw%3D

    CAS  Google Scholar 

  67. HS Yoon JD Hackett G Pinto D Bhattacharya (2002b) ArticleTitleThe single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99 15507–15512 Occurrence Handle1:CAS:528:DC%2BD3sXjvVOg

    CAS  Google Scholar 

  68. XC Yu W Margolin (1997) ArticleTitleCa2+-mediated GTP-dependent dynamic assembly of bacterial cell division protein FtsZ into asters and polymer networks in vitro. EMBO J 16 5455–5463 Occurrence Handle1:CAS:528:DyaK2sXmsVGlsb4%3D Occurrence Handle9312004

    CAS  PubMed  Google Scholar 

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Acknowledgements

We are deeply indebted to Dr. E. Virginia Armbrust, School of Oceanography, University of Washington, and the U.S. Department of Energy Joint Genome Institute for permission to use the Thalassiosira sequences before publication. This work was supported by a research fellowship from the Japanese Society for the Promotion of Science for Young Scientists (No. 7498 to S.M.) and by grants from the Ministry of Education, Culture, Sports, Science, and Technology, Japan (Nos. 12446222 and 12874111 to T.K.) and from the Program for the Promotion of Basic Research Activities for Innovative Biosciences (to T.K.).

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  1. Department of Life Sciences, College of Science, Rikkyo (St. Paul’s) University, 3-34-1 Nishiikebukuro, Toshima-ku, Tokyo 171-8501, Japan

    Shin-ya Miyagishima, Keishin Nishida & Tsuneyoshi Kuroiwa

  2. Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan

    Hisayoshi Nozaki & Keiji Nishida

  3. Department of Biomedical Chemistry, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan

    Motomichi Matsuzaki

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  1. Shin-ya Miyagishima
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Correspondence to Shin-ya Miyagishima.

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Miyagishima, Sy., Nozaki, H., Nishida, K. et al. 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 (2004). https://doi.org/10.1007/s00239-003-2551-1

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