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Origin, Evolution and Division of Plastids

  • Denis Falconet
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 34)

Summary

All living eukaryotic cells with mitochondria, and plastids if any, within their cytoplasm, are the result of two billion years of evolution. Both organelles are the result of two distinct endosymbioses. The increase in oxygen in the atmosphere supports the origin for mitochondria about 2.2 billion years ago, an origin probably due to a single invasion of a host cell by an α-proteobacterium-like organism. Plastids originated between 1.6 and 0.6 billion years ago as a result of a symbiotic association between a cyanobacterium and a mitochondriate eukaryote. This endosymbiotic event generated the green, red and blue algal lineages, which subsequently spread their chloroplasts when the new photosynthetic eukaryotes were, in their turn, engulfed by nonphotosynthetic eukaryotes (between, 1.2 and 0.55 billion years ago) generating more algal divisions. These symbiotic events would have been vain if the continuity of the newly acquired organelles had not been maintained. Since the first observations of chloroplast in the mid ninetieth century, progress made in microscopy techniques, during the first half of the twentieth century, demonstrated without ambiguity that this continuity is the result of division of pre-existing chloroplasts. Moreover, thanks to the completion of sequencing projects and the use of classical and reverse genetic approaches, it was then possible to show that the chloroplast division machinery is an evolutionary hybrid, which has retained the activity of several prokaryotically-derived proteins together with components that have evolved from proteins present in the eukaryotic ancestor.

Keywords

Chloroplast Division Division Site Plastid Division Secondary Endosymbiosis FtsZ Ring 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations:

ARC

– Accumulation and replication of chloroplasts;

BDLP

– Bacterial dynamin-like protein;

CFP

– Cyan fluorescent protein;

DRP

– Dynamin related protein;

Fts

– Filamentous temperature sensitive;

LCA

– Last common ancestor;

LGT

– Lateral gene transfer;

LUCA

– Last universal common ancestor;

MORN

– Membrane occupation and recognition nexus;

PD ring

– Plastid division ring;

TEM

– Transmission electron microscopy;

YFP

– Yellow fluorescent protein

Notes

Acknowledgements

I acknowledge the support of the Centre National de la Recherche Scientifique (CNRS) and the Ministère de l’Education Nationale (MEN) for a research grant (ACI DRAB 03/41, N° 03 5 90). I am grateful to Stéphane Lobreaux, Gabrielle Tichtinsky and Dominique Scheffel-Dunand for critical reading of the manuscript. Special thanks to Romage for his inspiring comments.

References

  1. Abdallah F, Salamini F and Leister D (2000) A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends Plant Sci 5: 141–142PubMedGoogle Scholar
  2. Aldridge C and Moller SG (2005) The plastid division protein AtMinD1 is a Ca2+−ATPase stimulated by AtMinE1. J Biol Chem 280: 31673–31678PubMedGoogle Scholar
  3. Archibald JM and Keeling PJ (2002) Recycled plastids: a ‘green movement’ in eukaryotic evolution. Trends Genet 18: 577–584PubMedGoogle Scholar
  4. Asano T, Yoshioka Y, Kurei S, Sakamoto W and 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: 448–459PubMedGoogle Scholar
  5. Beech PL and Gilson PR (2000) FtsZ and organelle division in Protists. Protist 151: 11–16PubMedGoogle Scholar
  6. Bhattacharya D, Yoon HS and Hackett JD (2004) Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 26: 50–60PubMedGoogle Scholar
  7. Bhattacharya D, Archibald JM, Weber AP and Reyes-Prieto A (2007) How do endosymbionts become organelles? Understanding early events in plastid evolution. Bioessays 29: 1239–1246PubMedGoogle Scholar
  8. Block MA, Douce R, Joyard J and Rolland N (2007) Chloroplast envelope membranes: a dynamic interface between plastids and the cytosol. Photosynth Res 92: 225–244PubMedGoogle Scholar
  9. Boasson R and Laetsch WM (1969) Chloroplast replication and growth in tobacco. Science 166: 749–751PubMedGoogle Scholar
  10. Bouck BJ (1962) Chromatophore development, pits, and other fine structure in the red alga, Lomentaria baileyana (Harv.) Farlow. J Cell Biol 12: 553–569PubMedGoogle Scholar
  11. Brocks JJ, Logan GA, Buick R and Summons RE (1999) Archean molecular fossils and the early rise of eukaryotes. Science 285: 1033–1036PubMedGoogle Scholar
  12. Cavalier-Smith T (2006) Cell evolution and earth history: stasis and revolution. Philos Trans R Soc Lond B Biol Sci 361: 969–1006PubMedGoogle Scholar
  13. Chaly N and Possingham JV (1981) Structure of constricted proplastids in meristematic plant tissues. Biol Cell 41: 203–210Google Scholar
  14. Chaly N, Possingham JV and Thomson WW (1980) Chloroplast division in spinach leaves examined by scanning electron microscopy and freeze-etching. J Cell Sci 46: 87–96PubMedGoogle Scholar
  15. Chida Y and Ueda K (1991) Division of chloroplasts in a green alga, Trebouxia potteri. Ann Bot 67: 435–442Google Scholar
  16. Colletti KS, Tattersall EA, Pyke KA, Froelich JE, Stokes KD and Osteryoung KW (2000) A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol 10: 507–516PubMedGoogle Scholar
  17. Dangeard P (1947) Cytologie Végétale et Cytologie Générale. Paul Lechevalier, ParisGoogle Scholar
  18. Delwiche CF (1999) Tracing the thread of plastid diversity through the tapestry of life. Am Nat 154: S164–S177PubMedGoogle Scholar
  19. Din N, Quardokus EM, Sackett MJ and Brun YV (1998) Dominant C-terminal deletions of FtsZ that affect its ability to localize in Caulobacter and its interaction with FtsA. Mol Microbiol 27: 1051–1063PubMedGoogle Scholar
  20. Dinkins R, Reddy MS, Leng M and Collins GB (2001) Overexpression of the Arabidopsis thaliana MinD1 gene alters chloroplast size and number in transgenic tobacco plants. Planta 214: 180–188PubMedGoogle Scholar
  21. Doolittle WF (2000) The nature of the universal ancestor and the evolution of the proteome. Curr Opin Struct Biol 10: 355–358PubMedGoogle Scholar
  22. Douglas SE (1998) Plastid evolution: origins, diversity, trends. Curr Opin Genet Dev 8: 655–661PubMedGoogle Scholar
  23. Douglas SE and Penny SL (1999) The plastid genome of the cryptophyte alga, Guillardia theta: complete sequence and conserved synteny groups confirm its common ancestry with red algae. J Mol Evol 48: 236–244PubMedGoogle Scholar
  24. Douglas SE, Murphy CA, Spencer DF and Gray MW (1991) Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350: 148–151PubMedGoogle Scholar
  25. Doutreligne J (1935) Note sur la structure des chloroplastes. Porc Akad Wetensch Amsterd 38: 886–896Google Scholar
  26. Duckett JG and Ligrone R (1993a) Plastid-dividing rings in ferns. Ann Bot 72: 619–627Google Scholar
  27. Duckett JG and Ligrone R (1993b) Plastid-dividing rings in the liverwort Odontoschisma denudatum (Mart) Dum. (Jungermanniales, Hepaticae). Gio Bot Ital 127: 318–319Google Scholar
  28. Dyall SD, Brown MT and Johnson PJ (2004) Ancient invasions: from endosymbionts to organelles. Science 304: 253–257PubMedGoogle Scholar
  29. El-Kafafi S, Mukherjee S, El-Shami M, Putaux JL, Block MA, Pignot-Paintrand I, Lerbs-Mache S and Falconet D (2005) The plastid division proteins, FtsZ1 and FtsZ2, differ in their biochemical properties and sub-plastidial localization. Biochem J 387: 669–676Google Scholar
  30. El-Kafafi S, Karamoko M, Pignot-Paintrand I, Grunwald D, Mandaron P, Lerbs-Mache S and Falconet D (2008) Developmentally regulated association of plastid division protein FtsZ1 with thylakoid membranes in Arabidopsis thaliana. Biochem J 409: 87–94Google Scholar
  31. El-Shami M, El-Kafafi S, Falconet D and Lerbs-Mache S (2002) Cell cycle-dependent modulation of FtsZ expression in synchronized tobacco BY2 cells. Mol Genet Genomics 267: 254–261PubMedGoogle Scholar
  32. Esser C and Martin W (2007) Supertrees and symbiosis in eukaryote genome evolution. Trends Microbiol 15: 435–437PubMedGoogle Scholar
  33. Fasse-Franzisket (1955) Die Teilung der Proplastiden und Choroplasten by Agapanthus umbellatus l’hérit. Protoplasma 45: 194–227Google Scholar
  34. Fischer WW (2008) Biogeochemistry: Life before the rise of oxygen. Nature 455: 1051–1052PubMedGoogle Scholar
  35. Forterre P and Gribaldo S (2007) The origin of modern terrestrial life. HFSP Journal 1: 156–168PubMedGoogle Scholar
  36. Forterre P and Philippe H (1999) Where is the root of the universal tree of life? Bioessays 21: 871–879PubMedGoogle Scholar
  37. Fujiwara MT, Nakamura A, Itoh R, Shimada Y, Yoshida S and Moller SG (2004) Chloroplast division site placement requires dimerization of the ARC11/AtMinD1 protein in Arabidopsis. J Cell Sci 117: 2399–2410PubMedGoogle Scholar
  38. Gaikwad A, Babbarwal V, Pant V and Mukherjee SK (2000) Pea chloroplast FtsZ can form multimers and correct the thermosensitive defect of an Escherichia coli ftsZ mutant. Mol Gen Genet 263: 213–221PubMedGoogle Scholar
  39. Gantt E and Arnott HJ (1963) Chloroplast division in the gametophyte of the fern Matteucia struthiopteris (L.) Todaro. J Cell Biol 19: 446–448PubMedGoogle Scholar
  40. Gao H, Kadirjan-Kalbach D, Froehlich JE and Osteryoung KW (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci USA 100: 4328–4333PubMedGoogle Scholar
  41. Gao H, Sage TL and Osteryoung KW (2006) FZL, an FZO-like protein in plants, is a determinant of thylakoid and chloroplast morphology. Proc Natl Acad Sci USA 103: 6759–6764PubMedGoogle Scholar
  42. Garton S, Knight H, Warren GJ, Knight MR and Thorlby GJ (2007) crinkled leaves 8 – a mutation in the large subunit of ribonucleotide reductase – leads to defects in leaf development and chloroplast division in Arabidopsis thaliana. Plant J 50: 118–127PubMedGoogle Scholar
  43. Gibbs SP (1978) The chloroplast of Euglena may have evolved from symbiotic green algae. Can J Bot 56: 2883–2889Google Scholar
  44. Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW and Vitha S (2007) Chloroplast division. Traffic 8: 451–461PubMedGoogle Scholar
  45. Glynn JM, Froehlich JE and Osteryoung KW (2008) Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20: 2460–2470PubMedGoogle Scholar
  46. Glynn JM, Yang Y, Vitha S, Schmitz AJ, Hemmes M, Miyagishima SY and Osteryoung KW (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: 700–711Google Scholar
  47. Gray MW, Burger G and Lang BF (1999) Mitochondrial evolution. Science 283: 1476–1481PubMedGoogle Scholar
  48. Green PB (1964) Cinematic observations on the growth and division of chloroplasts in Nitella. Am J Bot 51: 334–342Google Scholar
  49. Gremillon L, Kiessling J, Hause B, Decker EL, Reski R and Sarnighausen E (2007) Filamentous temperature-sensitive Z (FtsZ) isoforms specifically interact in the chloroplasts and in the cytosol of Physcomitrella patens. New Phytol 176: 299–310PubMedGoogle Scholar
  50. Gris JBA (1857) Recherches microscopiques sur la chlorophylle. Ann Sci Nat Bot Ser IV 7: 179–219Google Scholar
  51. Gunning B, Koenig F and Govindjee (2006) A dedication to pionners of research on chloroplast structure. In: Wise RR and Hoober JK (eds) The Structure and Function of Plastids, Advances in Photosynthesis and Respiration, Vol 23, pp xxiii–xxxi. Springer, DordrechtGoogle Scholar
  52. Hale CA, Rhee AC and de Boer PA (2000) ZipA-induced bundling of FtsZ polymers mediated by an interaction between C-terminal domains. J Bacteriol 182: 5153–5166PubMedGoogle Scholar
  53. Hashimoto H (1986) Double ring structure around the constricting neck of dividing plastids of Avena sativa. Protoplasma 135: 166–172Google Scholar
  54. Hashimoto H (1992) Involvement of actin filaments in chloroplast division of the alga closterium ehrengergii. Protoplasma 167: 88–96Google Scholar
  55. Hashimoto H (1997) Electron-opaque annular structure girdling the constriction isthmus of the dividing chloroplasts of Heterosigma akashiwo (Raphidophyceae, Chromophyta). Protoplasma 197: 210–216Google Scholar
  56. Hashimoto H (2003) Plastid division: its origins and evolution. Int Rev Cytol 222: 63–98PubMedGoogle Scholar
  57. Hashimoto H (2005) The ultrastructural features and division of secondary plastids. J Plant Res 118: 163–172PubMedGoogle Scholar
  58. Hashimoto H and Possingham JV (1989) Division and DNA distribution in ribosome-deficient plastids of the barley mutant “albostrians”. Protoplasma 149: 20–23Google Scholar
  59. Haswell ES and Meyerowitz EM (2006) MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr Biol 16: 1–11PubMedGoogle Scholar
  60. Hayashida A, Takechi K, Sugiyama M, Kubo M, Itoh RD, Takio S, Fujita T, Hiwatashi Y, Hasebe M and Takano H (2005) Isolation of mutant lines with decreased numbers of chloroplasts per cell from a tagged mutant library of the moss Physcomitrella patens. Plant Biol (Stuttg) 7: 300–306Google Scholar
  61. Heitz E (1936) Untersuchungen über den Bau der Plastiden. I. Die Gerichteten Chlorophyllscheiben der Chloroplasten. Planta 26: 134–163Google Scholar
  62. Holland HD (2006) The oxygenation of the atmosphere and oceans. Philos Trans R Soc Lond B Biol Sci 361: 903–915PubMedGoogle Scholar
  63. Hollande AC and Hollande G (1941) La structure des chloroplastes. Cell and Tissue Res 31: 648–652Google Scholar
  64. Hong Z, Bednarek SY, Blumwald E, Hwang I, Jurgens G, Menzel D, Osteryoung KW, Raikhel NV, Shinozaki K, Tsutsumi N and Verma DP (2003) A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions. Plant Mol Biol 53: 261–265PubMedGoogle Scholar
  65. Hu Z, Mukherjee A, Pichoff S and 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: 14819–14824PubMedGoogle Scholar
  66. Iino M and Hashimoto H (2003) Intermediate features of cyanelle division of Cyanophora paradoxa (Glaucocystophyta) between cyanobacterial and chloroplast division. J Phycol 39: 561–569Google Scholar
  67. Itoh R, Fujiwara M, Nagata N and Yoshida S (2001) A chloroplast protein homologous to the eubacterial topological specificity factor minE plays a role in chloroplast division. Plant Physiol 127: 1644–1655PubMedGoogle Scholar
  68. Kameya T and Takahashi N (1971) Division of chloroplast in vitro. Jap J Genet 46: 153–157Google Scholar
  69. Kanamaru K, Fujiwara M, Kim M, Nagashima A, Nakazato E, Tanaka K and Takahashi H (2000) Chloroplast targeting, distribution and transcriptional fluctuation of AtMinD1, a Eubacteria-type factor critical for chloroplast division. Plant Cell Physiol 41: 1119–1128PubMedGoogle Scholar
  70. Kausche GA and Ruska H (1940) Zur Frage der Chloroplas­tenstruktur. Naturwiss 28: 303–304Google Scholar
  71. Keeling PJ (2004) Diversity and evolutionary history of plastids and their hosts. Am J Bot 91: 1481–1493PubMedGoogle Scholar
  72. Kiessling J, Kruse S, Rensing SA, Harter K, Decker EL and Reski R (2000) Visualization of a cytoskeleton-like FtsZ network in chloroplasts. J Cell Biol 151: 945–950PubMedGoogle Scholar
  73. Kiessling J, Martin A, Gremillon L, Rensing SA, Nick P, Sarnighausen E, Decker EL and Reski R (2004) Dual targeting of plastid division protein FtsZ to chloroplasts and the cytoplasm. EMBO Rep 5: 889–894PubMedGoogle Scholar
  74. Kirk JTO and Tilney-Bassett RAE (1978) The plastids: Their Chemistry, Structure, Growth and Inheritance. Elsevier/North Holland Biochemical Press, AmsterdamGoogle Scholar
  75. Klint J, Rasmussen U and Bergman B (2007) FtsZ may have dual roles in the filamentous cyanobacterium Nostoc/Anabaena sp. strain PCC 7120. J Plant Physiol 164: 11–18PubMedGoogle Scholar
  76. Koksharova OA and Wolk CP (2002) A novel gene that bears a DnaJ motif influences cyanobacterial cell division. J Bacteriol 184: 5524–5528PubMedGoogle Scholar
  77. Kulandaivelu G and Gnanam A (1985) Scanning electron microscope evidence for a budding mode of chloroplast multiplication in higher plants. Physiol Plant 63: 299–302Google Scholar
  78. Kuroiwa T (1989) The nuclei of cellular organelles and the formation of daughter organelles by the “plastid dividing ring”. Bot Mag 102: 291–329Google Scholar
  79. Kuroiwa T (2000) The discovery of the division apparatus of plastids and mitochondria. J Electron Microsc (Tokyo) 49: 123–134Google Scholar
  80. Kuroiwa T, Kuroiwa H, Sakai A, Takahashi H, Toda K and Itoh R (1998) The division apparatus of plastids and mitochondria. Int Rev Cytol 181: 1–41PubMedGoogle Scholar
  81. Kuroiwa H, Mori T, Takahara M, Miyagishima SY and Kuroiwa T (2002) Chloroplast division machinery as revealed by immunofluorescence and electron microscopy. Planta 215: 185–190PubMedGoogle Scholar
  82. Kusunoki S and Kawasaki Y (1936) Beobachtungen über die Chloroplastenteilung by Einigen Blutenpflanzen. Cytologia 7: 530–534Google Scholar
  83. Larkum AW, Lockhart PJ and Howe CJ (2007) Shopping for plastids. Trends Plant Sci 12: 189–195PubMedGoogle Scholar
  84. Leech RM and Pyke K (1988) Chloroplast division in higher plants with particular reference to wheat. In: Boffey SA and Lloyd D (eds) The division and Segregation of Organelles, pp 31–62. Cambridge University Press, Cambridge, UKGoogle Scholar
  85. Leech RM, Thomson WW and Platt-Aloia KA (1981) Observations of the mechanisms of chloroplast division in higher plants. New Phytol 87: 1–9Google Scholar
  86. Lemieux C, Otis C and Turmel M (2000) Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature 403: 649–652PubMedGoogle Scholar
  87. Lemieux C, Otis C and Turmel M (2007) A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies. BMC Biol 5: 1–17Google Scholar
  88. Lindsay MR, Webb RI, Strous M, Jetten MS, Butler MK, Forde RJ and Fuerst JA (2001) Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch Microbiol 175: 413–429PubMedGoogle Scholar
  89. Liu WZ, Hu Y, Zhang RJ, Zhou WW, Zhu JY, Liu XL and He YK (2007) Transfer of a eubacteria-type cell division site-determining factor CrMinD gene to the nucleus from the chloroplast genome in Chlamydomonas reinhardtii. Chin. Sci. Bull. 52: 2514–2521Google Scholar
  90. Liu Z, Mukherjee A and Lutkenhaus J (1999) Recruitment of ZipA to the division site by interaction with FtsZ. Mol Microbiol 31: 1853–1861PubMedGoogle Scholar
  91. Low HH and Lowe J (2006) A bacterial dynamin-like protein. Nature 444: 766–769PubMedGoogle Scholar
  92. Luck BT and Jordan EG (1980) The mitochondria and plastids during microsporogenesis in Hyacinthoides non-scripta (L.) Chouard. Ann Bot (Lond) 45: 511–514Google Scholar
  93. Lumière A (1919) Le Mythe des Symbiotes. Masson & Cie, ParisGoogle Scholar
  94. Lutkenhaus J (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem 76: 539–562PubMedGoogle Scholar
  95. Lutkenhaus J and Addinall SG (1997) Bacterial cell division and the Z ring. Ann Rev Biochem 66: 93–116PubMedGoogle Scholar
  96. Ma X and Margolin W (1999) Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol 181: 7531–7544PubMedGoogle Scholar
  97. Maple J and Moller SG (2007a) Plastid division: evolution, mechanism and complexity. Ann Bot (Lond) 99: 565–579Google Scholar
  98. Maple J and Moller SG (2007b) Interdependency of formation and localisation of the Min complex controls symmetric plastid division. J Cell Sci 120: 3446–3456PubMedGoogle Scholar
  99. Maple J and Moller SG (2007c) Plastid division coordination across a double-membraned structure. FEBS Lett 581: 2162–2167PubMedGoogle Scholar
  100. Maple J, Chua NH and Moller SG (2002) The topological specificity factor AtMinE1 is essential for correct plastid division site placement in Arabidopsis. Plant J 31: 269–277PubMedGoogle Scholar
  101. Maple J, Fujiwara MT, Kitahata N, Lawson T, Baker NR, Yoshida S and Moller SG (2004) GIANT CHLOROPLAST 1 is essential for correct plastid division in Arabidopsis. Curr Biol 14: 776–781PubMedGoogle Scholar
  102. Maple J, Aldridge C and Moller SG (2005) Plastid division is mediated by combinatorial assembly of plastid division proteins. Plant J 43: 811–823PubMedGoogle Scholar
  103. Maple J, Vojta L, Soll J and Moller SG (2007) ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Rep 8: 293–299PubMedGoogle Scholar
  104. Margolin W (2005) FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6: 862–871PubMedGoogle Scholar
  105. Marin B, Nowack EC and Melkonian M (2005) A plastid in the making: evidence for a second primary endosymbiosis. Protist 156: 425–432PubMedGoogle Scholar
  106. Marrison JL, Rutherford SM, Robertson EJ, Lister C, Dean C and Leech RM (1999) The distinctive roles of five different ARC genes in the chloroplast division process in Arabidopsis. Plant J 18: 651–662PubMedGoogle Scholar
  107. Martin W and Kowallik KV (1999) Annotated English translation of Mereschkowsky’s 1905 paper ‘Über Natur und Ursprung der Chromatophoren im Pflanzenreiche’. Eur J Phycol 34: 287–295Google Scholar
  108. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M and Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99: 12246–12251PubMedGoogle Scholar
  109. Matsuzaki M, Kikuchi T, Kita K, Kojima S and Kuroiwa T (2001) Large amounts of apicoplast nucleoid DNA and its segregation in Toxoplasma gondii. Protoplasma 218: 180–191PubMedGoogle Scholar
  110. McAndrew RS, Olson BJ, Kadirjan-Kalbach DK, Chi-Ham CL, Vitha S, Froehlich JE and Osteryoung KW (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: 367–378PubMedGoogle Scholar
  111. McFadden GI and Van Dooren GG (2004) Evolution: red algal genome affirms a common origin of all plastids. Curr Biol 14: R514–516PubMedGoogle Scholar
  112. McFadden GI, Gilson PR and Waller RF (1995) Molecular phylogeny of chlorarachniophytes based on plastid rRNA and rbcL sequences. Archiv Protistenk 145: 231–239Google Scholar
  113. Menke W (1940) Untersuchungen über den Feinbau des Protoplasmas mit dem Universal-Elektronenmikroskop. Protoplasma 35: 115–130Google Scholar
  114. Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol. centralblatt 25: 593–604. English translation in Martin W, Kowallik KV (1999) Annotated English translation of Mereschkowsky’s 1905 paper ‘Über Natur und Ursprung der Chromatophoren im Pflanzenreiche’. Eur J Phycol 1934: 1287–1295Google Scholar
  115. Meyer A (1883) Das Chlorophyllkorn in Chemischer, Morphologischer und Biologischer Beziehung. Felix S, LeipzigGoogle Scholar
  116. Misumi O, Yoshida Y, Nishida K, Fujiwara T, Sakajiri T, Hirooka S, Nishimura Y and Kuroiwa T (2008) Genome analysis and its significance in four unicellular algae, Cyanidioshyzon merolae, Ostreococcus tauri, Chlamydomonas reinhardtii, and Thalassiosira pseudonana. J Plant Res 121: 3–17PubMedGoogle Scholar
  117. Mita T and Kuroiwa T (1988) Division of plastids by a plastid-dividing ring in Cyanidium caldarium. Protoplasma Suppl 1: 133–152Google Scholar
  118. Mita T, Kanbe T, Tanaka T and Kuroiwa T (1986) A ring structure around the dividing plane of the Cyanidium calderium chloroplast. Protoplasma 130: 211–213Google Scholar
  119. Miyagishima SY and Kuroiwa T (2006) The mechanism of plastid division: the structure and origin of the plastid division apparatus. In: Wise RR and Hoober JK (eds) The Structure and Function of Plastids, Advances in Photosynthesis and Respiration, Vol 23, pp 103–121. Springer, DordrechtGoogle Scholar
  120. Miyagishima SY, Ito M, Toda K, Takabayashi A, Kuroiwa H and Kuroiwa T (1998) Identification of a triple ring structure involve in plastid division in the primitive red alga Cyanidioschyzon merolae. J Electron Microsc 47: 269–272Google Scholar
  121. Miyagishima SY, Itoh R, Toda K, Kuroiwa H and Kuroiwa T (1999) Real-time analyses of chloroplast and mitochondrial division and differences in the behavior of their dividing rings during contraction. Planta 207: 343–353Google Scholar
  122. Miyagishima SY, Kuroiwa H and 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: 517–528PubMedGoogle Scholar
  123. Miyagishima SY, Takahara M and Kuroiwa T (2001b) Novel filaments 5 nm in diameter constitute the cytosolic ring of the plastid division apparatus. Plant Cell 13: 707–721PubMedGoogle Scholar
  124. Miyagishima SY, Takahara M, Mori T, Kuroiwa H, Higashiyama T and 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: 2257–2268Google Scholar
  125. Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H and Kuroiwa T (2003) A plant-specific dynamin-related protein forms a ring at the chloroplast division site. Plant Cell 15: 655–665PubMedGoogle Scholar
  126. Miyagishima SY, Nozaki H, Nishida K, Nishida K, Matsuzaki M and 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: 291–303PubMedGoogle Scholar
  127. Miyagishima SY, Froehlich JE and Osteryoung KW (2006) PDV1 and PDV2 mediate recruitment of the dynamin-related protein ARC5 to the plastid division site. Plant Cell 18: 2517–2530PubMedGoogle Scholar
  128. Miyagishima SY, Kuwayama H, Urushihara H and Nakanishi H (2008) Evolutionary linkage between eukaryotic cytokinesis and chloroplast division by dynamin proteins. Proc Natl Acad Sci U S A 105: 15202–15207PubMedGoogle Scholar
  129. Miyake NH and Taniguchi T (1995) Ultrastructural changes of chloroplasts in peanut mesophyll protoplasts treated with electric fields. Jpn J Crop Sci 64: 131–138Google Scholar
  130. Modrusan Z and Wrischer M (1990) Studies on chloroplast division in young leaf tissues of some higher plants. Protoplasma 154: 1–7Google Scholar
  131. Moehs CP, Tian L, Osteryoung KW and Dellapenna D (2001) Analysis of carotenoid biosynthetic gene expression during marigold petal development. Plant Mol Biol 45: 281–293PubMedGoogle Scholar
  132. Moreira D, Le Guyader H and Philippe H (2000) The origin of red algae and the evolution of chloroplasts. Nature 405: 69–72PubMedGoogle Scholar
  133. Morlot C, Noirclerc-Savoye M, Zapun A, Dideberg O and Vernet T (2004) The D,D-carboxypeptidase PBP3 organizes the division process of Streptococcus pneumoniae. Mol Microbiol 51: 1641–1648PubMedGoogle Scholar
  134. Mosyak L, Zhang Y, Glasfeld E, Haney S, Stahl M, Seehra J and Somers WS (2000) The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J 19: 3179–3191PubMedGoogle Scholar
  135. Mühlethaler K (1960) Die Struktur der Grana- und Stroma-Lamellen in Chloroplasten. Z Wissensch Mikroskopie 8: 444–452Google Scholar
  136. Nakanishi H, Suzuki K, Kabeya Y and Miyagishima SY (2009) Plant-specific protein MCD1 determines the site of chloroplast division in concert with bacteria-derived MinD. Curr Biol 19: 151–156Google Scholar
  137. Nass S and Nass MMK (1963) Intramitochondrial fibers with DNA characteristics. J Cell Biol 19: 613–628PubMedGoogle Scholar
  138. Nisbet EG and Sleep NH (2001) The habitat and nature of early life. Science 409: 1083–1091Google Scholar
  139. Nogales E, Wolf SG and Downing KH (1998) Structure of the alpha beta tubulin dimer by electron crystallography. Nature 391: 199–203PubMedGoogle Scholar
  140. Nägeli C (1846) Bläschenförmige Gebilde im Inhalte der Pflanzenzelle. Z Wiss Bot 3/4: 94–128Google Scholar
  141. Ogawa S, Ueda K and Noguchi T (1995) Division apparatus of the chloroplast in Nannochloris Bacillaris (Chlorophyta). J Phycol 31: 132–137Google Scholar
  142. Oross JW and Possingham JV (1989) Ultrastructural features of the constricted region of dividing plastids. Protoplasma 150: 131–138Google Scholar
  143. Osteryoung KW and Vierling E (1995) Conserved cell and organelle division. Nature 376: 473–474PubMedGoogle Scholar
  144. Osteryoung KW and McAndrew RS (2001) The plastid division machine. Annu Rev Plant Physiol Plant Mol Biol 52: 315–333PubMedGoogle Scholar
  145. Osteryoung KW, Stokes KD, Rutherford SM, Percival AL and Lee WY (1998) Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell 10: 1991–2004PubMedGoogle Scholar
  146. Palmer JD (2003) The symbiotic birth and spread of plastids: how many times and whodunit? J Phycol 39: 4–11Google Scholar
  147. Poole AM and Penny D (2007a) Evaluating hypotheses for the origin of eukaryotes. Bioessays 29: 74–84PubMedGoogle Scholar
  148. Poole AM and Penny D (2007b) Eukaryote evolution: engulfed by speculation. Nature 447: 913PubMedGoogle Scholar
  149. Portier P (1918) Les Symbiotes. Masson et Cie, ParisGoogle Scholar
  150. Possingham JV and Lawrence ME (1983) Controls to plastid division. Int Rev Cytol 84: 1–56Google Scholar
  151. Possingham JV and Rose RJ (1976) Chloroplast replication and chloroplast DNA synthesis in spinach leaves. Proc. Roy. Soc. London B 193: 295–305Google Scholar
  152. Possingham JV and Saurer W (1969) Change in chloroplast number per cell during leaf development in spinach. Planta 86: 186–194Google Scholar
  153. Praefcke GJ and McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5: 133–147PubMedGoogle Scholar
  154. Pyke KA (1999) Plastid division and development. Plant Cell 11: 549–556PubMedGoogle Scholar
  155. Pyke KA and Leech RM (1991) Rapid image analysis screening procedure for identifying chloroplast number mutants in mesophyll cells of Arabidopsis thaliana (L.) Heynh. Plant Physiol 96: 1193–1195PubMedGoogle Scholar
  156. Pyke KA and Leech RM (1992) Chloroplast division and expansion is radically altered by nuclear mutations in Arabidopsis thaliana. Plant Physiol 99: 1005–1008PubMedGoogle Scholar
  157. Pyke KA and Leech RM (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol 104: 201–207PubMedGoogle Scholar
  158. Pyke KA and Page AM (1998) Plastid ontogeny during petal development in Arabidopsis. Plant Physiol 116: 797–803PubMedGoogle Scholar
  159. Pyke KA, Rutherford SM, Robertson EJ and Leech RM (1994) arc6, a fertile Arabidopsis mutant with only two mesophyll cell chloroplasts. Plant Physiol 106: 1169–1177PubMedGoogle Scholar
  160. Randolf LF (1922) Cytology of chlorophyll type of maize. Bot Gaz 73: 337–375Google Scholar
  161. Raskin DM and de Boer PA (1999) Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc Natl Acad Sci USA 96: 4971–4976PubMedGoogle Scholar
  162. Rasmussen B, Fletcher IR, Brocks JJ and Kilburn MR (2008) Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455: 1101–1104PubMedGoogle Scholar
  163. RayChaudhuri D (1999) ZipA is a MAP-Tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division. EMBO J 18: 2372–2383PubMedGoogle Scholar
  164. Raynaud C, Cassier-Chauvat C, Perennes C and Bergounioux C (2004) An Arabidopsis homolog of the bacterial cell division inhibitor SulA is involved in plastid division. Plant Cell 16: 1801–1811PubMedGoogle Scholar
  165. Raynaud C, Perennes C, Reuzeau C, Catrice O, Brown S and Bergounioux C (2005) Cell and plastid division are coordinated through the prereplication factor AtCDT1. Proc Natl Acad Sci USA 102: 8216–8221PubMedGoogle Scholar
  166. Reddy MS, Dinkins R and 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: 167–176PubMedGoogle Scholar
  167. Reski R (2002) Rings and networks: the amazing complexity of FtsZ in chloroplasts. Trends Plant Sci 7: 103–105PubMedGoogle Scholar
  168. Reumann S, Inoue K and Keegstra K (2005) Evolution of the general protein import pathway of plastids (review). Mol Membr Biol 22: 73–86PubMedGoogle Scholar
  169. Reyes-Prieto A, Weber APM and Bhattacharya D (2007) The origin and establishment of the plastid in algae and plants. Annu Rev Genet 41: 147–168PubMedGoogle Scholar
  170. Ridley SM and Leech RM (1970) Division of chloroplasts in an artificial environment. Nature 227: 463–465PubMedGoogle Scholar
  171. Ris H and Plaut W (1962) Ultrastructure of DNA-containing areas in the chloroplast of Chlamydomonas. J Cell Biol 19: 383–391Google Scholar
  172. Ris H and Singh RN (1961) Electron microscope studies on blue-green algae. J Biophys Biochem Cytol 9: 63–80PubMedGoogle Scholar
  173. Robertson EJ, Pyke KA and Leech RM (1995) arc6, an extreme chloroplast division mutant of Arabidopsis also alters proplastid proliferation and morphology in shoot and root apices. J Cell Sci 108: 2937–2944PubMedGoogle Scholar
  174. Robertson EJ, Rutherford SM and Leech RM (1996) Characterization of chloroplast division using the Arabidopsis mutant arc5. Plant Physiol 112: 149–159PubMedGoogle Scholar
  175. Romberg L and Levin PA (2003) Assembly dynamics of the bacterial cell division protein FtsZ: poised at the edge of stability. Annu Rev Microbiol 57: 125–154PubMedGoogle Scholar
  176. Rutherford SM (1996) The genetic and physical analysis of mutants of chloroplast number and size in Arabidopsis thaliana. PhD Thesis. Department of biology, University of York, York, UKGoogle Scholar
  177. Sagan L (L Margulis) (1967) On the origin of mitosing cells. J Theor Biol 14: 225–275Google Scholar
  178. Sakr S, Jeanjean R, Zhang CC and Arcondeguy T (2006) Inhibition of cell division suppresses heterocyst development in Anabaena sp. strain PCC 7120. J Bacteriol 188: 1396–1404PubMedGoogle Scholar
  179. Sapp J (1994) Evolution by Association: A History of Symbiosis. Oxford University Press, New York and OxfordGoogle Scholar
  180. Sato N (2006) Origin and evolution of plastids: genomic view on the unification and diversity of plastids. In: Wise RR and Hoober JK (eds) The Structure and Function of Plastids, Advances in Photosynthesis and Respiration, Vol 23, pp 75–102. Springer, DordrechtGoogle Scholar
  181. Schimper AFW (1883) Über die Entwickelung der Chlorophyllkörner und Farbkörper. Bot Zeit 41: 105–112Google Scholar
  182. Schimper AFW (1885) Untersuchungen über die Chlorophyllkörner und die ihnen Homologen Gebilde. Jb Wiss Botan 16: 1–247Google Scholar
  183. Schmitz FKJ (1883) Die Chromatophoren der Algen. Verh Naturhist Ver preuß Rheinland und Westfalen 40: 1–180Google Scholar
  184. Schopf JW (2006) Fossil evidence of Archaean life. Philos Trans R Soc Lond B Biol Sci 361: 869–885PubMedGoogle Scholar
  185. Scott NS, Cain P and Possingham JV (1982) Plastid DNA levels in albino and green leaves of the “albostrians” mutant of Hordeum vulgare. Z Pflanzenphysiol 108: 187–191Google Scholar
  186. Sharp LW (1934) Introduction to Cytology. McGraw-Hill book company, New YorkGoogle Scholar
  187. Shimada H, Koizumi M, Kuroki K, Mochizuki M, Fujimoto H, Ohta H, Masuda T and 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: 960–967PubMedGoogle Scholar
  188. Simpson CL and Stern DB (2002) The treasure trove of algal chloroplast genomes. Surprises in architecture and gene content, and their functional implications. Plant Physiol 129: 957–966PubMedGoogle Scholar
  189. Staff IA and Parthasarathy MV (1984) The possibility of cell plate-induced plastid division in a flowering plant. New Phytol 97: 77–82Google Scholar
  190. Steahelin LA (2003) Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynth Res 76: 185–196Google Scholar
  191. Strepp R, Scholz S, Kruse S, Speth V and 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: 4368–4373PubMedGoogle Scholar
  192. Striepen B, Crawford MJ, Shaw MK, Tilney LG, Seeber F and Roos DS (2000) The plastid of Toxoplasma gondii is divided by association with the centrosomes. J Cell Biol 151: 1423–1434PubMedGoogle Scholar
  193. Strugger S (1950) Über den Bau der Proplastiden und Chloroplasten. Naturwissenschaften 37: 166–167Google Scholar
  194. Strugger S (1957) Elektronenmikroskopische Beobachtungen über die Teilung der Proplastiden im Urmeristem der Wurzelspitze von Allium cepa. Z Naturforsch 12b: 280–283Google Scholar
  195. Summons RE, Jahnke LL, Hope JM and Logan GA (1999) 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400: 554–557PubMedGoogle Scholar
  196. Suzuki KI and Ueda R (1975) Electron microscope observations on plastid division in root meristematic cells of Pisum sativum L. Bot Mag Tokyo 88: 319–321Google Scholar
  197. Tavva VS, Collins GB and Dinkins RD (2006) Targeted overexpression of the Escherichia coli MinC protein in higher plants results in abnormal chloroplasts. Plant Cell Rep 25: 341–348PubMedGoogle Scholar
  198. Tewinkel M and Volkmann D (1987) Observations on dividing plastids in the protonema of the moss Funaria hygrometrica. Planta 172: 309–320Google Scholar
  199. Trécul AAL (1858) Des formations vésiculaires dans les cellules végétales. Ann Sci Nat Bot Ser IV 8: 20 –163, 205–382Google Scholar
  200. Ueda R, Tominga S and Tanuma T (1970) Cinematographic observations on the chloroplast division in Mnium leaf cells. Science Report of the Tokyo Daigaku, Section B 14: 129–137Google Scholar
  201. Vaughan S, Wickstead B, Gull K and Addinall SG (2004) Molecular evolution of FtsZ protein sequences encoded within the genomes of archaea, bacteria, and eukaryota. J Mol Evol 58: 19–29PubMedGoogle Scholar
  202. Ventura GT, Kenig F, Reddy CM, Schieber J, Frysinger GS, Nelson RK, Dinel E, Gaines RB and Schaeffer P (2007) Molecular evidence of Late Archean archaea and the presence of a subsurface hydrothermal biosphere. Proc Natl Acad Sci USA 104: 14260–14265PubMedGoogle Scholar
  203. Vicente M, Rico AI, Martinez-Arteaga R and Mingorance J (2006) Septum enlightenment: assembly of bacterial division proteins. J Bacteriol 188: 19–27PubMedGoogle Scholar
  204. Vitha S, Froehlich JE, Koksharova O, Pyke KA, Van Erp H and 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: 1918–1933PubMedGoogle Scholar
  205. von Wettstein D (1954) Formwechsel und Teilung der Chromatophoren von Fucus vesiculosus. Z Naturforsch 9B: 476–481Google Scholar
  206. 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 and 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: 5967–5972PubMedGoogle Scholar
  207. Wallin IE (1927) Symbionticism and the Origin of Species. Williams and Wilkins, BaltimoreGoogle Scholar
  208. Wang X, Huang J, Mukherjee A, Cao C and Lutkenhaus J (1997) Analysis of the interaction of FtsZ with itself, GTP, and FtsA. J Bacteriol 179: 5551–5559PubMedGoogle Scholar
  209. Weatherill K, Lambiris I, Pickett-Heaps J, Deane JA and Beech PL (2007) Plastid division in Mallomonas (Synurophyceae, Heterokonta). J Phycol 43: 535–541Google Scholar
  210. Whatley JM (1988) Mechanism and morphology of plastid divison. In: Boffey SA and Lloyd D (eds) The Division and Segregation of Organelles, pp 63–83. Cambridge University Press, Cambridge, UKGoogle Scholar
  211. Woese C (1998) The universal ancestor. Proc Natl Acad Sci USA 95: 6854–6859PubMedGoogle Scholar
  212. Woese CR and Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74: 5088–5090PubMedGoogle Scholar
  213. Yan K, Pearce KH and Payne DJ (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: 387–392PubMedGoogle Scholar
  214. Yang Y, Glynn JM, Olson BJ, Schmitz AJ and Osteryoung KW (2008) Plastid division: across time and space. Curr Opin Plant Biol 11: 577–584PubMedGoogle Scholar
  215. Yoder DW, Kadirjan-Kalbach D, Olson BJ, Miyagishima SY, Deblasio SL, Hangarter RP and Osteryoung KW (2007) Effects of mutations in Arabidopsis FtsZ1 on plastid division, FtsZ ring formation and positioning, and FtsZ filament morphology in vivo. Plant Cell Physiol 48: 775–791PubMedGoogle Scholar
  216. Yoon HS, Hackett JD, Ciniglia C, Pinto G and Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21: 809–818PubMedGoogle Scholar
  217. Yoshida Y, Kuroiwa H, Misumi O, Nishida K, Yagisawa F, Fujiwara T, Nanamiya H, Kawamura F and Kuroiwa T (2006) Isolated chloroplast division machinery can actively constrict after stretching. Science 313: 1435–1438PubMedGoogle Scholar
  218. Yuasa A (1949) Studies in the cytology of Pteridophyta. Jpn J Genet 24: 166–173Google Scholar
  219. Zhang M, Hu Y, Jia J, Li D, Zhang R, Gao H and He Y (2009) CDP1, A novel component of chloroplast division site positioning system in Arabidopsis. Cell Res 19: 877–886Google Scholar

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© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Laboratoire de Physiologie Cellulaire VégétaleUMR 5168 CNRS-CEA-INRA-Université Joseph Fourier Grenoble, iRTSV-LPCV, CEA-GrenobleGrenoble Cedex 9France

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