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Programmed Cell Death in Dinoflagellates

  • María Segovia
Part of the Molecular Biology Intelligence Unit book series (MBIU)

Abstract

Dinoflagellates are unicellular flagellated eukaryotes exploiting different nutritional modes although approximately half of them are photosynthetic. They are a monophyletic group, included in the lineage Alveolates. Dinoflagellates are ecologically important as components of the phytoplankton and contribute significantly to CO2 fixation and primary productivity in the oceans. As well, they can form blooms (densities of more than a million cells per millilitre) producing red and brown tides. Recently the possible role of programmed cell death (PCD) in phytoplankton has received much attention because massive cell disappearance of species as a consequence of cell death have important consequences in the ocean dynamics. Several species of phytoplankters undergo PCD, apparently using the same core mechanism as metazoans. However, dinoflagellates show different PCD morphologies (apoptotic, necrotic, necrotic-like and paraptotic) depending on the species and on the triggering factor, probably due to their mesokaryotic condition. Similarly to metazoans, PCD in this group goes through intermediates such as ROS, and the proteins in charge of executing the cell are metacaspases (cysteinyl aspartate proteases from the caspase family, found in yeast, plants, protists and some bacteria). The acquisition of the PCD genes in these organisms goes back to ancient times when the endosymbiotic events took place. However, the intriguing point is the gene persistence through evolution, given that such genes provide the cell with negative selective pressure.

Keywords

Coral Reef Possible Role Ofprogrammed Cell Death Coral Bleaching Cell Death Differ Brown Tide 
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.

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References

  1. 1.
    Graham LE, Wilcox LW. Algae. Upper Saddle River: Prentice-Hall, 2000.Google Scholar
  2. 2.
    Taylor FJR. The biology of dinoflagellates. In: Taylor FJR, ed. General Group Characteristics. Oxford: Blackwell, 1985:1–24.Google Scholar
  3. 3.
    Bhattacharya D, Yoon HS, Hackett JD. Photosynthetic eukaryotes unite: Endosymbiosis connects the dots. Bioessays 2004; 26:50–60.PubMedGoogle Scholar
  4. 4.
    Murray S, Flø Jørgensen M, Hoc SYW et al. Improving the analysis of dinoflagellate phylogeny based on rDNA. Protist 2005; 156:269–286.PubMedGoogle Scholar
  5. 5.
    Livolant F, Bouligand Y. New observations on the twisted arrangement of dinoflagellate chromosomes. Chromosoma 1978; 8:21–44.Google Scholar
  6. 6.
    Bendich AJ, Drlica K. Prokaryotic and eukaryotic chromosomes: What’s the difference? Bioessays 2000; 2:481–486.Google Scholar
  7. 7.
    Sala-Rovira M, Geraud ML, Caput D et al. Molecular cloning and imunolocalization of two variants of the major basic nuclear protein (HCc) from the histone-less eukaryote Crypthecodinium cohnii (Pyrrhophyta). Chromosoma 1991; 100:510–518.PubMedGoogle Scholar
  8. 8.
    Wong JT, New DC, Wong JC et al. Histone-like proteins of the dinoflagellate Crypthecodinium cohnii have homologies to bacterial DNA-binding proteins. Eukaryot Cell 2003; 2:646–650.PubMedGoogle Scholar
  9. 9.
    Fagan TF, Li JF, Chudnovsky J et al. Cloning, sequencing and expression of a histone-like protein from the photosynthetic dinoflagellate Gonyaulax polyedra. J Phycol 2000; 36:21–22.Google Scholar
  10. 10.
    Chudnovsky Y, Li JF, Rizzo PJ et al. Cloning, expression, and characterization of a histone-like protein from the marine dinoflagellate Lingulodinium polyedrum (Dinophyceae). J Phycol 2002; 38:543–550.Google Scholar
  11. 11.
    Hackett JD, Scheetz TE, Yoon HS et al. Insights into a dinoflagellate genome through expressed sequence tag analysis. BMC Genomics 2005; 6:80.PubMedGoogle Scholar
  12. 12.
    Dodge JD. Dinoflagellate with both a mesocaryotic and a cucaryotic nucleus: Fine structure of nuclei. Protoplasma 1971; 73:145–157.PubMedGoogle Scholar
  13. 13.
    Costas E, Goyanes V. Ultrastructure and division behavior of dinoflagellate chromosomes. Chromosoma 1987; 95:435–441.Google Scholar
  14. 14.
    Wong JTY, Kwok ACM. Proliferation of dinoflagellates: Blooming or bleaching. Bioessays 2005; 27:730–740.PubMedGoogle Scholar
  15. 15.
    Guillebault D, Sasorith S, Derelle E et al. A new class of transcription initiation factors, intermediate between TATA box-binding proteins (TBPs) and TBP-like factors (TLFs), is present in the marine unicellular organism, the dinoflagellate Crypthecodinium cohnii. J Biol Chem 2002; 277:40881–40886.PubMedGoogle Scholar
  16. 16.
    Falkowski PG, Raven JA. Aquatic Photosynthesis. Malden, Massachusetts: Blackwell Science, 1997.Google Scholar
  17. 17.
    Anderson DM. Toxic red tides and harmful algal blooms: A practical challenge in coastal oceanography. Rev Geophys 1995; 33:1189–1200.Google Scholar
  18. 18.
    Richardson K. Harmful or exceptional phytoplankton blooms in the marine ecosystem. Adv Mar Biol 1997; 31:302–385.Google Scholar
  19. 19.
    Sellner KG, Doucette GJ, Kirkpatrick GJ. Harmful algal blooms: Causes, impacts and detection. J Microbiol Biotechnol 2003; 30:383–406.Google Scholar
  20. 20.
    Walsh JJ. Death in the sea: Enigmatic phytoplankton losses. Prog Oceanogr 1983; 12:1–86.Google Scholar
  21. 21.
    Fogg CE, Thake B. Algal cultures and phytoplankton ecology. University of Wisconsin Press, 1987.Google Scholar
  22. 22.
    Vardi A, Berman-Frank I, Rozenberg T et al. Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO2 limitation and oxidative stress. Curr Biol 1999; 9:1061–1064.PubMedGoogle Scholar
  23. 23.
    Dunn SR, Bythell JC, Le Tissier MDA et al. Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J Exp Mar Biol Ecol 2002; 272:29–53.Google Scholar
  24. 24.
    Franklin DJ, Berges JA. Mortality in cultures of the dinoflagellate Amphidinium carterae during culture senescence and darkness. Proc R Soc Lond B 2004; 271:2099–2107.Google Scholar
  25. 25.
    Cornillon S, Foa C, Davoust J et al. Programmed cell-death in Dictyostelium. J Cell Sci 1994; 107:2691–2704.PubMedGoogle Scholar
  26. 26.
    Ameisen JC. The origin of programmed cell death. Science 1996; 272:1278–1279.PubMedGoogle Scholar
  27. 27.
    Berges JA, Falkowski PG. Physiological stress and cell death in marine phytoplankton: Induction of proteases in response to nitrogen or light limitation. Limnol Oceanogr 1998; 43:129–135.Google Scholar
  28. 28.
    Frohlich KU, Madeo F. Apoptosis in yeast-A monocellular organism exhibits altruistic behaviour. FEBS Lett 2000; 473:6–9.PubMedGoogle Scholar
  29. 29.
    Lewis K. Programmed cell death in bacteria. Microbiol Mol Biol Rev 2000; 64:503–514.PubMedGoogle Scholar
  30. 30.
    Ning SB, Guo HL, Wang L et al. Salt stress induces programmed cell death in prokaryotic organism anabaena. J Appl Microbiol 2002; 93:15–28.PubMedGoogle Scholar
  31. 31.
    Segovia M, Haramaty L, Berges JA et al. Cell death in the unicellular chlorophyte Dunaliella tertiolecta: An hypothesis on the evolution of apoptosis in higher plants and metazoans. Plant Physiol 2003; 132:99–105.PubMedGoogle Scholar
  32. 32.
    Berman-Frank I, Bidle KD, Haramaty L et al. The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol Oceanogr 2004; 49:997–1005.Google Scholar
  33. 33.
    Bidle KD, Falkowski PG. Cell death in planktonic, photosynthetic microorganisms. Nature Rev Microbiol 2004; 2:643–655.Google Scholar
  34. 34.
    Kitanaka C, Kuchino Y. Caspase-independent programmed cell death with necrotic morphology. Cell Death Differ 1999; 6:508–515.PubMedGoogle Scholar
  35. 35.
    Sperandio S, de Belle I, Bredesen DE. An alternative, nonapoptotic form of programmed cell death. Proc Natl Acad Sci USA 2000; 97:14376–14381.PubMedGoogle Scholar
  36. 36.
    Wyllie AH, Golstein P. More than one way to go. Proc Natl Acad Sci USA 2001; 98:11–13.PubMedGoogle Scholar
  37. 37.
    Dunn SR, Thomason JC, Thissler ML et al. Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration. Cell Death Differ 2004; 11:1213–1222.PubMedGoogle Scholar
  38. 38.
    Juhl AR, Latz MI. Mechanisms of fluid shear-induced inhibition of population growth in a red-tide dinoflagellate. J Phycol 2002; 38:683–694.Google Scholar
  39. 39.
    Madeo F, Frohlich E, Ligr M et al. Oxygen stress: A regulator of apoptosis in yeast. J Cell Biol 1999; 145:757–767.PubMedGoogle Scholar
  40. 40.
    Jabs T. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol 1999; 57:231–245.PubMedGoogle Scholar
  41. 41.
    Cohen GM. Caspases: The executioners of apoptosis. Biochemical J 1997; 326:1–16.Google Scholar
  42. 42.
    Leist M, Nicotera P. The shape of cell death. Biochem Biophys Res Com 1997; 236:1–9.PubMedGoogle Scholar
  43. 43.
    Pennell RI, Lamb C. Programmed plant cell in plants. Plant Cell 1997; 9:1157–1168.PubMedGoogle Scholar
  44. 44.
    Lam E, Kato N, Lawton M. Programmed cell death, mitochondria, and the plant hypersensitive response. Nature 2001; 411:848–853.PubMedGoogle Scholar
  45. 45.
    Chichkova NV, Kim SH, Titova ES et al. A plant caspase-like protease activated during the hypersensitive response. Plant Cell 2004; 16:157–171.PubMedGoogle Scholar
  46. 46.
    Ridgley EL, Xiong ZH, Ruben L. Reactive oxygen species activate a Ca2+-dependent cell death pathway in the unicellular organism Trypanosoma brucei. Biochem J 1999; 340:33–40.PubMedGoogle Scholar
  47. 47.
    Sen N, Das BB, Ganguly A et al. Camptothecin-induced imbalance in intracellular cation homeostasis regulates programmed cell death in unicellular hemoflagellate Leishmania donovani. J Biol Chem 2004; 279:52366–5237.PubMedGoogle Scholar
  48. 48.
    Lesser MP. Oxidative stress in marine environments. Biochem Physiol Ecol Annu Rev Physiol 2006; 68:253–78.Google Scholar
  49. 49.
    Lesser MP, Shick JM. Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida: Primary production, photoinhibition, and enzymatic defences against oxygen toxicity. Mar Biol 1989; 102:243–55.Google Scholar
  50. 50.
    Hollnagel HC, di Mascio P, Asano CS et al. The effect of light on the biosynthesis of β-carotene and superoxide dismutase activity in the photosynthetic alga Gonyaulax polyedra. Brazil J Med Biol Res 1996; 29:105–10.Google Scholar
  51. 51.
    Butow BJ, Wynne D, Tel-Or E. Superoxide dismutase activity in Peridinium gatunense in Lake Kinnert: Effect of light regime and carbon dioxide concentration. J Phycol 1997; 33:787–93.Google Scholar
  52. 52.
    Lage OM, Sansonetry F, O’Connor JE et al. Flow cytometric analysis of chronic and acute toxicity of copper (II) on the marine dinoflagellate Amphidinium carterae. Cytometry 2001; 44:226–235.PubMedGoogle Scholar
  53. 53.
    Cardozo KHM, de Oliveira MAL, Tavares MFM et al. Daily oscillation of fatty acids and malondialdehyde in the dinoflagellate Lingulodinium polyedrum. Biol Rhythm Res 2002; 33:371–381.Google Scholar
  54. 54.
    Leitao MAD, Cardozo KHM, Pinto E et al. PCB-induced oxidative stress in the unicellular marine dinoflagellate Lingulodinium polyedrum. Arch Environ Con Tox 2003; 45:59–65.Google Scholar
  55. 55.
    Kroemer G, Petit P, Zamzami N et al The biochemistry of programmed cell-death. FASEB J 1995; 9:1277–1287.PubMedGoogle Scholar
  56. 56.
    Sato T, Hanada M, Bodrug S et al. Interactions among members of the Bcl-2 protein family analyzed with a yeast two-hybrid system. Proc Natl Acad Sci USA 1994; 91:9238–9242.PubMedGoogle Scholar
  57. 57.
    Korsmeyer SJ. Regulators of cell death. Trends Genet 1995; 11:101–105.PubMedGoogle Scholar
  58. 58.
    Watanabe N, Lam E. Recent advance in the study of caspase-like proteases and Bax inhibitor-1 in plants: Their possible roles as regulator of programmed cell death. Mol Plant Pathol 2004; 5:65–70.Google Scholar
  59. 59.
    Deponte M, Becker K. Plasmodium falciparum — do killers, commit suicide? Trends Parasitol 2004; 20:165–169.PubMedGoogle Scholar
  60. 60.
    Nishiyama Y, Yamamoto H, Allakhverdiev SI et al. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 2001; 20:5587–5594.PubMedGoogle Scholar
  61. 61.
    Takahashi S, Nakamura T, Sakamizu M et al. Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef building corals. Plant Cell Physiol 2004; 45:251–255.PubMedGoogle Scholar
  62. 62.
    Gates RD, Baghdasarian G, Muscatine L. Temperature stress causes host cell detachment in symbiotic cnidarians: Implications for coral bleaching. Biol Bull 1992; 182:324–32.Google Scholar
  63. 63.
    Ramanathan V, Collins W. A thermostat in the tropics. Nature 1993; 361:410–411.Google Scholar
  64. 64.
    Hoegh-Guldberg O. Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 1999; 50:839–66.Google Scholar
  65. 65.
    Lesser MP. Experimental coral reef biology. J Exp Mar Biol Ecol 2004; 300:217–52.Google Scholar
  66. 66.
    Rowan R. Coral bleaching—Thermal adaptation in reef coral symbionts. Nature 2004; 430:742–742.PubMedGoogle Scholar
  67. 67.
    Tchernov D, Gorbunov MY, de Vargas C et al. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 2004; 101:13531–13535.PubMedGoogle Scholar
  68. 68.
    Warner ME, Fitt WK, Schmidt GW. Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc Natl Acad Sci USA 1999; 96:8007–12.PubMedGoogle Scholar
  69. 69.
    Jones RJ, Hoegh-Guldberg O, Larkum AWD et al. Temperature induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 1998; 21:1219–30.Google Scholar
  70. 70.
    Sawyer SJ, Muscatine L. Cellular mechanisms underlying temperature-induced bleaching in the tropical sea anemone Aiptasia pulchella. J Exp Biol 2001; 204:3443–3456.PubMedGoogle Scholar
  71. 71.
    Douglas AE. Coral bleaching—How and why? Mar Pollut Bull 2003; 46:385–392.PubMedGoogle Scholar
  72. 72.
    Trench RK. Microalgal-invertebrate symbioses: A review. Endocyt Cell Res 1993; 9:135–175.Google Scholar
  73. 73.
    Perez SF, Cook CB, Brooks WR. The role of symbiotic dinoflagellates in the temperature-induced bleaching response of the subtropical sea anemone Aiptasia pallida. J Exp Mar Biol Ecol 2001; 256:1–14.PubMedGoogle Scholar
  74. 74.
    Franklin DJ, Hoegh-Guldberg O, Jones RJ et al. Cell death and degeneration in the symbiotic dinofla-gellates of the coral Stylophora pistillata during bleaching. Mar Ecol Prog Ser 2004; 272:117–130.Google Scholar
  75. 75.
    Bibby BT, Dodge JD. Ultrastructure and cytochemistry of microbodies in dinoflagellates. Planta 1973; 112:7–16.Google Scholar
  76. 76.
    Trench RK. Nutritional potentials in Zoanthus sociathus (Coelenterata, Anthozoa). Helgol Wiss Meeresunters 1974; 26:174–216.Google Scholar
  77. 77.
    Trench RK. The biology of dinoflagellates. In: Taylor FJR, ed. Dinoflagellates in Nonparasitic Symbioses. Oxford: Blackwell, 1985:530–570.Google Scholar
  78. 78.
    Lesser MP, Farrell J. Solar radiation increases the damage to both host tissues and algal symbionts of corals exposed to thermal stress. Coral Reefs 2004; 23:367–77.Google Scholar
  79. 79.
    Gutteridge JMC, Halliwell B. Free radicals and antioxidants in the year 2000—A historical look to the future. Ann NY Acad Sci 2000; 899:136–147.PubMedGoogle Scholar
  80. 80.
    Imlay JA. Pathways of oxidative damage. Ann Rev Microbiol 2003; 57:395–418.Google Scholar
  81. 81.
    Lane DP. Cell immortalization and transformation by the p53-gene. Nature 1984; 312:596–597.PubMedGoogle Scholar
  82. 82.
    Costas E, Aguilera A, Gonzalez-Gil S et al. Contact inhibition—Also a control for cell-proliferation in unicellular algae. Biol Bull 1993; 184:1–5.Google Scholar
  83. 83.
    Buddemeier RW, Fautin DG. Coral bleaching as an adaptive mechanism: A testable hypothesis. Bioscience 1993; 43:320–326.Google Scholar
  84. 84.
    Rowan R. Diversity and ecology of zooxanthellae on coral reefs. J Phycol 1998; 34:407–417.Google Scholar
  85. 85.
    Savage AM, Goodson MS, Visram S et al. Molecular diversity of symbiotic algae at the latitudinal margins of their distribution: Dinoflagellates of the genus Symbiodinium in corals and sea anemones. Marine Ecol Prog Ser 2002; 244:17–26.Google Scholar
  86. 86.
    Vierstra RD. Proteolysis in plants: Mechanisms and functions. Plant Mol Biol 1996; (1–2):275–302.Google Scholar
  87. 87.
    Abraham MC, Shaham S. Death without caspases, caspases without death. Trends Cell Biol 2004; 14:184–193.PubMedGoogle Scholar
  88. 88.
    Thornberry NA. Caspases: A decade of death research. Cell Death Diff 1999; 6:1023–1027.Google Scholar
  89. 89.
    Uren AG, O’Rourke K, Aravind LA et al. Identification of paracaspases and metacaspases: Two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell 2000; 6:961–967.PubMedGoogle Scholar
  90. 90.
    Villalobo E, Moch C, Fryd-Versavel G et al. Cysteine proteases and cell differentiation: Excystment of the ciliated protist Sterkiella histriomuscorum. Eukaryot Cell 2003; 2:1234–1245.PubMedGoogle Scholar
  91. 91.
    Vardi A, Schatz D, Beeri K et al. Dinoflagellate-cyanobacterium communication may determine the composition of phytoplankton assemblage in a mesotrophic lake. Curr Biol 2002; 12:1767–1772.PubMedGoogle Scholar
  92. 92.
    Okamoto OK, Hastings JW. Genome-wide analysis of redox regulated genes in a dinoflagellate. Gene 2003; 321:73–81.PubMedGoogle Scholar
  93. 93.
    Battinelli E, Loscalzo J. Nitric oxide induces apoptosis in megakaryocytic cell lines. Blood 2000; 95:3451–3459.PubMedGoogle Scholar
  94. 94.
    Mur LAJ, Carver TLW, Prats E. NO way to live; the various roles of nitric oxide in plant-pathogen interactions. J Exp Bot 2006; 57:489–505.PubMedGoogle Scholar
  95. 95.
    Vacca RA, Valenti D, Bobba A et al. Cytochrome c is released in a reactive oxygen species-dependent manner and is degraded via caspase-like proteases in tobacco bright-yellow 2 cells en route to heat shock-induced cell death. Plant Physiol 2006; 141:208–219.PubMedGoogle Scholar
  96. 96.
    Segovia M, Berges JA. Effect of inhibitors of protein synthesis and DNA replication on the induction of proteolytic activities, caspase-like activities and cell death in the unicellular chlorophyte Dunaliella tertiolecta. Eur J Phycol 2005; 40:21–30.Google Scholar
  97. 97.
    Tai V, Lawrence JE, Lang AS et al. Characterization of HaRNAV, a single-stranded RNA virus causing lysis of Heterosigma akashiwo (Raphidophyceae). J Phycol 2003; 39:343–352.Google Scholar
  98. 98.
    Nagasaki K, Shirai Y, Takao Y et al. Comparison of genome sequences of single-stranded RNA viruses infecting the bivalve-killing dinoflagellate Heterocapsa circularisquama. Appl Env Microbiol 2005; 71:8888–8894.Google Scholar
  99. 99.
    Wilson WH, Schroeder DC, Allen MJ et al. Complete genome sequencing and lytic phase transcription profile of a coccolithovirus. Science 2005; 309:1090–1092.PubMedGoogle Scholar
  100. 100.
    Margulis L. Symbiosis in cell evolution: Life and its environment on the early earth. San Francisco: WH Freeman, 1981.Google Scholar
  101. 101.
    Kroemer G. Mitochondrial implication in apoptosis. Towards an endosymbiont hypothesis of apoptosis evolution. Cell Death Differ 1997; 4:443–456.PubMedGoogle Scholar
  102. 102.
    Huettenbrenner S, Maier S, Christina Leisser C et al. The evolution of cell death programs as prerequisites of multicellularity. Mut Res 2003; 543:235–249.Google Scholar
  103. 103.
    Ameisen JC. When cells die. In: Lockshin R, Zakeri Z, Tilly J, eds. The Evolutionary Origin and Role of Programmed Cell Death in Single Celled Organisms: A new view of executioners, mitochondria, host-pathogen interactions, and the role of death in the process of natural selection. New York: Wiley-Liss, 1998:3–56.Google Scholar
  104. 104.
    Falkowski PG, Katz ME, Knoll AH et al. The evolution of modern eukaryotic phytoplankton. Science 2004; 305:354–360.PubMedGoogle Scholar
  105. 105.
    Knoll A. The geological consequences of evolution. Geobiology 2003; 1:3–15.Google Scholar
  106. 106.
    Delwiche CF, Kuhsel M, Palmer JD. Phylogenetic analysis of tufA sequences indicates a cyanobacterial origin of all plastids. Mol Phylogenet Evol 1995; 4:110–128.PubMedGoogle Scholar
  107. 107.
    Delwiche CF. Tracing the thread of plastid diversity through the tapestry of life. Am Nat 1999; 154:164–177.Google Scholar
  108. 108.
    Jain R, Rivera MC, Lake JA. Horizontal gene transfer among genomes: The complexity hypothesis. Proc Natl Acad Sci USA 1999; 96:3801–3806.PubMedGoogle Scholar

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© Landes Bioscience and Springer Science+Business Media 2008

Authors and Affiliations

  1. 1.Departamento de EcologíaFacultad de Ciencias-Universidad de MálagaMálagaSpain

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