Advertisement

Genetica

, Volume 115, Issue 1, pp 13–28 | Cite as

Jam packed genomes – a preliminary, comparative analysis of nucleomorphs

  • Paul R. Gilson
  • Geoffrey I. McFadden
Article

Abstract

There are two ways eukaryotic cells can permanently acquire chloroplasts. They can take up a cyanobacterium and turn it into a chloroplast or they can engulf an alga that already has a chloroplast. The second method is far more common and there are at least seven major groups of protists that have obtained their chloroplasts, this way. In most cases little remains of the engulfed alga apart from its chloroplast, but in two groups, the cryptomonads and chlorarachniophytes, a small remnant nucleus of the engulfed alga is still present. These tiny nuclei, called nucleomorphs, are the smallest and most compact eukaryotic genomes known and recently the nucleomorph of the cryptomonad alga Guillardia theta, was completely sequenced (551 kilobases). The nucleomorph of the chlorarachniophyte Bigellowiella natans (380 kilobases), is also being sequenced and is about half complete. We discuss some of the similarities and differences that are emerging between these two nucleomorph genomes. Both genomes contain just three chromosomes that encode mainly housekeeping genes and a few proteins for chloroplast functions. The bulk of nucleomorph gene coding capacity, therefore, appears to be devoted to self perpetuation and creating gene and protein expression machineries to make a small number of essential chloroplast proteins. We discuss reasons why both nucleomorphs are extraordinarily compact and why their gene sequences are evolving rapidly.

chloroplast chlorarachniophyte cryptomonad C-value enigma endosymbiosis intron mitosis nucleomorph photosynthesis secondary plastid telomere transposable element 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abdallah, F., F. Salamini & D. Leister, 2000. A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends Plant Sci. 5: 141-142.Google Scholar
  2. Archibald, J., T. Cavalier-Smith, U. Maier & S. Douglas, 2001. Molecular chaparones encoded by a reduced nucleus-the cryptomonad nucleomorph. Mol. Biol. Evol. 52: 490-501.Google Scholar
  3. Arkhipova, I. & M. Meselson, 2000. Transposable elements in sexual and ancient asexual taxa. Proc. Natl. Acad. Sci. USA 97: 14473-14477.Google Scholar
  4. Barry, J. & R. McCulloch, 2001. Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite. Adv. Parasitol. 49: 1-70.Google Scholar
  5. Beaton, M. & T. Cavalier-Smith, 1999. Eukaryotic non-coding DNA is functional: evidence from the differential scaling of cryptomonad genomes. Proc. R. Soc. London 266: 2053-2059.Google Scholar
  6. Brugère, J., E. Cornillot, G. Metenier & C. Vivares, 2000a. Occurence of subtelomeric rearrangements in the genome of the microsporidian parasite Encephalitozoon cuniculi, as revealed by a new fingerprinting procedure based on two-dimensional pulsed field gel electrophoresis. Electrophoresis 21: 2576-2581.Google Scholar
  7. Brugère, J.-F., E. Cornillot, G. Mètènier, A. Bensimon & C. Vivarès, 2000b. Encephalitozoon cuniculi (Microspora) genome: physical map and evidence for telomere-associated rDNA units on all chromosomes. Nucl. Acid Res. 28: 2026-2033.Google Scholar
  8. Cavalier-Smith, T., 1995a. Membrane heredity, symbiogenesis, and the multiple origins of algae, pp. 75-114 in Biodiversity and Evolution, edited by R. Arai, M. Kato & Y. Doi. National Science Museum, Tokyo.Google Scholar
  9. Cavalier-Smith, T., 1995b. Membrane heredity, symbogenesis, and the multiple origins of the algae., pp. 75-114 in Biodiversity and Evolution, edited by R. Arai, M. Kato & Y. Doi. The National Science Foundation, Tokyo.Google Scholar
  10. Cavalier-Smith, T., J.A. Couch, K.E. Thorsteinsen, P.R. Gilson, J.A. Deane, D.R.A. Hill & G.I. McFadden, 1996. Cryptomonad nuclear and nucleomorph 18S rRNA phylogeny. Eur. J. Phycol. 31: 315-328.Google Scholar
  11. Cavalier-Smith, T. & E.E. Chao, 1997. Sarcomonad ribosomal RNA sequences, rhizopod phylogeny, and the origin of euglyphid amoebae. Arch. Protistenk. 147: 227-236.Google Scholar
  12. Cavalier-Smith, T., 1998. A revised six-kingdom system of life. Biol. Rev. Camb. Phil. Soc. 73: 227-236.Google Scholar
  13. Cavalier-Smith, T., 1999. Priciples of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryotic family tree. J. Euk. Microbiol. 47: 347-366.Google Scholar
  14. Cavalier-Smith, T.& M. Beaton, 1999. The skeletal function of nongenic nuclear DNA: new evidence from ancient cell chimeras. Genetica 106: 3-13.Google Scholar
  15. Cavalier-Smith, T., 2000. Membrane heredity and early chloroplast evolution. Trends Plant Sci. 5: 174-182.Google Scholar
  16. Cornforth, M. & R. Eberle, 2001. Termini of human chromosomes display elevated rates of mitotic recombination. Mutagenesis 16: 85-89.Google Scholar
  17. Deutsch, M. & M. Long, 1999. Intron-exon structures of eukaryotic model organisms. Nucl. Acids Res. 27: 3219-3228.Google Scholar
  18. Douglas, S., 1998. Plastid evolution: origins, diversity, trends. Curr. Opin. Genet. Devel. 8: 655-661.Google Scholar
  19. Douglas, S., S. Zauner, M. Fraunholz, M. Beaton, S. Penny, L.-T. Deng, X. Wu, M. Reith, T. Cavalier-Smith & U.-G. Maier, 2001. The highly reduced genome of an enslaved algal nucleus. Nature 410: 1091-1096.Google Scholar
  20. Douglas, S.E., C.A. Murphy, D.F. Spencer & M.W. Gray, 1991. Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350: 148-151.Google Scholar
  21. Douglas, S.E. & S.L. Penny, 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: 236-244.Google Scholar
  22. Dunham, M., A. Neumann, C. Fasching & R. Reddel, 2000. Telomere maintenance by recombination in human cells. Nat. Genet. 26: 447-450.Google Scholar
  23. Eschbach, S., C.J.B. Hofmann, U.-G. Maier, P. Sitte & P. Hansmann, 1991. A eukaryotic genome of 660 kb: electrophoretic karyotype of nucleomorph and cell nucleus of the cryptomonad alga, Pyrenomonas salina. Nucl. Acids Res. 19: 1779-1781.Google Scholar
  24. Fast, N.M., J. Kissinger, D. Roos & P. Keeling, 2001. Nuclearencoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol. Biol. Evol. 18: 418-426.Google Scholar
  25. Fraunholz, M.J., E. Moerschel & U.G. Maier, 1998. The chloroplast division protein FtsZ is encoded by a nucleomorph gene in cryptomonads. Mol. Gen. Genet. 260: 207-211.Google Scholar
  26. Gaasterland, T. & C.W. Sensen, 1996. Fully automated genome analysis that reflects user needs and preferences: a detailed introduction to the MAGPIE system architecture. Biochimie 78: 302-310.Google Scholar
  27. Gibbs, S., 1981. The chloroplasts of some algal groups may have evolved from some endosymbiotic eukaryotic algae. Ann. NY Acad. Sci. 361: 193-208.Google Scholar
  28. Gilson, P. & G. McFadden, 1999. Molecular and morphological characterization of six chlorarachniophyte strains. Phycol. Res. 47: 7-19.Google Scholar
  29. Gilson, P. & G. McFadden, 2001. A grin without a cat. Nature 410: 1040-1041.Google Scholar
  30. Gilson, P.R. & G.I. McFadden, 1995. The chlorarachniophyte: a cell with two different nuclei and two different telomeres. Chromosoma 103: 635-641.Google Scholar
  31. Gilson, P.R. & G.I. McFadden, 1996. The miniaturised nuclear genome of a eukaryotic endosymbiont contains genes that overlap, genes that are contranscribed, and smallest known spliceosomal introns. Proc. Natl. Acad. Sci. USA 93: 7737-7742.Google Scholar
  32. Gilson, P.R., U.G. Maier & G.I. McFadden, 1997. Size isn't everything-lessons in genetic miniaturisation from nucleomorphs. Curr. Opin. Genet. Dev. 7: 800-806.Google Scholar
  33. Grant, P., 2001. A tale of histone modifications. Genome Biol. 2: 3.1-3.6.Google Scholar
  34. Greenwood, A., 1974. The Cryptophyta in relation to phylogeny and photosynthesis, pp. 566-567 in 8th International Congress of Electron Microscopy, edited by J. Sanders & D. Goodchild. Australian Academy of Sciences, Canberra.Google Scholar
  35. Greenwood, A., H. Griffiths & U. Santore, 1977. Chloroplasts and cell compartments in Cryptophyceae. Br. Phycol. J. 12: 119.Google Scholar
  36. Gregory, T., 2000. Nucleotypic effects without nuclei: genome size and erythrocyte size in mammals. Genome 43: 895-901.Google Scholar
  37. Gregory, T., 2001. Coincidence, coevolution, or causation? DNA content, cell size and the C-value enigma. Biol. Rev. 76: 65-101.Google Scholar
  38. Grell, K., 1990. Indications of sexual reproduction in the plasmodial protist Chlorarachnion reptans Geitler. Z. Naturforsch. 45c: 112-114.Google Scholar
  39. Hansmann, P., H. Falk, U. Sheer & P. Sitte, 1986. Ultrastructural localization of DNA in two Cryptomonad species by use of a monoclonal DNA antibody. Eur. J. Cell Biol. 42: 152-160.Google Scholar
  40. Hansmann, P. & S. Eschbach, 1990. Isolation and preliminary characterization of the nucleus and the nucleomorph of a cryptomonad, Pyrenomonas salina. Eur. J. Cell Biol. 52: 373-378.Google Scholar
  41. Heslop-Harrison, J., M. Murata, Y. Ogura, T. Schwarzacher & F. Motoyoshi, 1999. Polymorphisms and genomic organization of repetitive DNA from centromeric regions of Arabidopsis chromosomes. Plant Cell 11: 31-42.Google Scholar
  42. Hibberd, D.J. & R.E. Norris, 1984. Cytology and ultrastructure of Chlorarachnion reptans (Chlorarachniophyta Divisio Nova, Chlorarachniophyceae Classis Nova). J. Phycol. 20: 310-330.Google Scholar
  43. Hill, D.R.A. & R. Wetherbee, 1986. Proteomonas sulcata gen. et sp. nov. (Cryptophyceae), a cryptomonad with two morphologically distinct and alternating forms. Phycologia 25: 521-543.Google Scholar
  44. International Human Genome Sequencing Consortium, 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921.Google Scholar
  45. Ishida, K., Y. Cao, M. Hasegawa, N. Okada & Y. Hara, 1997. The origin of chlorarachniophyte plastids, as inferred from phylogenetic comparisons of amino acid sequences of ef-tu. J. Mol. Evol. 45: 682-687.Google Scholar
  46. Ishida, K., B. Green & T. Cavalier-Smith, 1999. Diversification of a chimeric algal group, the Chlorarachniophytes: phylogeny of nuclear and nucleomorph small-subunit rRNA genes. Mol. Biol. Evol. 16: 321-331.Google Scholar
  47. Keeling, P., 2001. Foraminifera and Cercozoa are related in actin phylogeny: two orphans find a home? Mol. Biol. Evol. 18: 1551-1557.Google Scholar
  48. Keeling, P.J., J.A. Deane, C. Hink-Schauer, S.E. Douglas, U.-G. Maier & G.I. McFadden, 1999. The secondary endosymbiont of the cryptomonad Guillardia theta contains alpha-, beta-, and gamma-tubulin genes. Mol. Biol. Evol. 16: 1308-1313.Google Scholar
  49. Liao, D., 1999. Concerted evolution: molecular mechanism and biological implications. Am. J. Hum. Genet. 64: 24-30.Google Scholar
  50. Ludwig, M. & S. Gibbs, 1985. DNA is present in the nucleomorph of cryptomonads: further evidence that the chloroplast evolved from a eukaryotic endosymbiont. Protoplasma 127: 9-20.Google Scholar
  51. Maier, U., M. Fraunholz, S. Zauner, S. Penny & S. Douglas, 2000. A nucleomorph-encoded CbbX and the phylogeny of RuBisCo regulators. Mol. Biol. Evol. 17: 576-583.Google Scholar
  52. Maier, U.-G., C. Hofmann, S. Eschbach, J. Wolters & G. Igloi, 1991. Demonstration of nucleomorph-encoded eukaryotic small subunit RNA in Cryptomonads. Mol. Gen. Genet. 230: 155-160.Google Scholar
  53. Margulis, L. & M. Chapman, 1998. Endosymbioses: cyclical and permanent in evolution. Trends Microbiol. 6: 342-346.Google Scholar
  54. Marquardt, J., S. Wans, E. Rhiel, A. Randolf & W. Krumbein, 2000. Intron-exon structure and gene copy number of a gene encoding for a membrane-intrinsic light-harvesting polypeptide of the red alga Galdieria sulphuraria. Gene 255: 257-265.Google Scholar
  55. Martin, W., B. Stoebe, V. Goremykin, S. Hansmann, M. Hasegawa & K. Kowallik, 1998. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393: 162-165.Google Scholar
  56. McFadden, G., P. Gilson & I. Sims, 1997a. Preliminary characterization of carbohydrate stores from chlorarachniophytes (Division: Chlorarachniophyta). Phycol. Res. 45: 145-151.Google Scholar
  57. McFadden, G.I., P.R. Gilson, C.J. Hofmann, G.J. Adcock & U.-G. Maier, 1994. Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga. Proc. Natl. Acad. Sci. USA 91: 3690-3694.Google Scholar
  58. McFadden, G.I., P.R. Gilson, S.E. Douglas, C.J.B. Hofmann & U.-G. Maier, 1997b. Bonsai genomics: sequencing the smallest eukaryotic genomes. Trends Genet. 13: 46-49.Google Scholar
  59. McFadden, G.I. & D.S. Roos, 1999. Apicomplexan plastids as drug targets. Trends Microbiol. 6: 328-333.Google Scholar
  60. Moestrup, Ø. & M. Sengco, 2001. Ultrastructural studies on Bigelowiella natans, gen. et sp. nov., a chlorarachniophyte flagellate. J. Phycol. 37: 624-646.Google Scholar
  61. Moran, N.A., 1996. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 93: 2873-2878.Google Scholar
  62. Moreira, D., H. LeGuyader & H. Philipe, 2000. The origin of red algae: implications for the evolution of chloroplasts. Nature 405: 69-72.Google Scholar
  63. Murray, A. & J. Szostak, 1985. Chromosome segregation in mitosis and meiosis. Annu. Rev. Cell Biol. 1: 289-315.Google Scholar
  64. Palmer, J.D. & C.F. Delwiche, 1996. Second-hand chloroplasts and the case of the disappearing nucleus. Proc. Natl. Acad. Sci. USA 93: 7432-7435.Google Scholar
  65. Palmer, J.D. & C.F. Delwiche, 1998. The origin and evolution of plastids and their genomes, pp. 375-409 in Molecular Systematics of Plants II, edited by D.E. Soltis, P.S. Soltis & J.J. Doyle. Chapman Hall, New York.Google Scholar
  66. Petrov D.A., E.R. Lozovskaya & D.L. Hartl. 1996. High intrinsic rate of DNA loss in Drosophila. Nature 384: 346-349.Google Scholar
  67. Race, H., R. Herrmann & W. Martin, 1999. Why have organelles retained genomes? Trends Genet. 15: 364-370.Google Scholar
  68. Rensing, S., M. Goddemeier, C. Hofmann & U.-G. Maier, 1994. The presence of a nucleomorph hsp70 gene is a common feature of Cryptophyta and Chloraracnhiophyta. Curr. Genet. 26: 451-455.Google Scholar
  69. Russell, C.B., D. Fraga & R.D. Hinrichsen, 1994. Extremely short 20-33 nucleotide introns are the standard length in Paramecium tetraurelia. Nucl. Acids Res. 22: 1221-1225.Google Scholar
  70. Selosse, M., B. Albert & B. Godelle, 2001. Reducing the genome size of organelles favours gene transfer to the nucleus. Trends Ecol. Evol. 16: 135-141.Google Scholar
  71. Small, I., K. Akashi, A. Chapron, A. Dietrich, A.-M. Duchene, D. Lancelin, L. Maréchal-Drouard, B. Menand, H. Mireau, Y. Moudden, J. Ovesna, N. Peeters, W. Sakamoto, G. Souciet & H. Wintz, 1999. The strange evolutionary history of plant mitochondrial tRNAs and their aminoacyl-tRNA synthetases. J. Hered. 90: 333-337.Google Scholar
  72. Sulli, C., Z. W. Fang, U. Muchal & S.D. Schwartzbach, 1999. Topology of Euglena chloroplast protein precursors within the endoplasmic reticulum to Golgi to chloroplast transport vesicles. J. Biol. Chem. 274: 457-463.Google Scholar
  73. The Arabidopsis Genome Initiative, 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.Google Scholar
  74. Van de Peer, Y., S.A. Rensing, U.-G. Maier & R. de Wachter, 1996. Substitution rate calibration of small subunit rRNA identifies chlorarachniophyte endosymbionts as remnants of green algae. Proc. Natl. Acad. Sci. USA 93: 7732-7736.Google Scholar
  75. van Dooren, G.G., R.F. Waller, K.A. Joiner, D.S. Roos & G.I. McFadden, 2000. Protein transport in Plasmodium falciparum: traffic jams. Parasitol. Today 16: 421-427.Google Scholar
  76. Waller, R.F., P.J. Keeling, R.G.K. Donald, B. Striepen, E. Handman, N. Lang-Unnasch, A.F. Cowman, G.S. Besra, D.S. Roos & G.I. McFadden, 1998. Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 95: 12352-12357.Google Scholar
  77. Wastl, J. & U.-G. Maier, 2000. Transport of proteins into cryptomonads complex plastids. J. Biol. Chem. 275: 23194-23198.Google Scholar
  78. Wastl, J., H. Sticht, U.G. Maier, P. Rosch & S. Hoffmann, 2000. Identification and characterization of a eukaryotically encoded rubredoxin in a cryptomonad alga. FEBS Lett. 471: 191-196.Google Scholar
  79. Whatley, J., 1981. Chloroplast evolution-ancient and modern. Ann. NY Acad. Sci. 361: 154-165.Google Scholar
  80. Wolters, J., 1991. The troublesome parasites: molecular and morphological evidence that Apicomplexa belong to the dinoflagellate-ciliate clade. Biosystems 25: 75-84.Google Scholar
  81. Zauner, S., M. Fraunholz, J. Wastl, S. Penny, M. Beaton, T. Cavalier-Smith, U.-G. Maier & S. Douglas, 2000. Chloropast protein and centrosomal genes, a tRNA intron, and odd telomeres in an unusually compact eukaryotic genome, the cryptomonad nucleomorph. Proc. Natl. Acad. Sci. USA 97: 200-205.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  1. 1.Centre for Cellular and Molecular Biology, School of Biological and Chemical SciencesDeakin UniversityAustralia
  2. 2.Plant Cell Biology Research Centre, School of BotanyUniversity of MelbourneAustralia

Personalised recommendations