Sequence and analysis of chromosome 2 of Dictyostelium discoideum

The genome of the lower eukaryote Dictyostelium discoideum comprises six chromosomes. Here we report the sequence of the largest, chromosome 2, which at 8 megabases (Mb) represents about 25% of the genome. Despite an A + T content of nearly 80%, the chromosome codes for 2,799 predicted protein coding genes and 73 transfer RNA genes. This gene density, about 1 gene per 2.6 kilobases (kb), is surpassed only by Saccharomyces cerevisiae (one per 2 kb) and is similar to that of Schizosaccharomyces pombe (one per 2.5 kb). If we assume that the other chromosomes have a similar gene density, we can expect around 11,000 genes in the D. discoideum genome. A significant number of the genes show higher similarities to genes of vertebrates than to those of other fully sequenced eukaryotes. This analysis strengthens the view that the evolutionary position of D. discoideum is located before the branching of metazoa and fungi but after the divergence of the plant kingdom, placing it close to the base of metazoan evolution.

[1]  N. Perrimon,et al.  X-linked female-sterile loci in Drosophila melanogaster. , 1986, Genetics.

[2]  S. Benzer,et al.  Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[3]  D. Bouchon,et al.  Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[4]  Stephen M. Mount,et al.  The genome sequence of Drosophila melanogaster. , 2000, Science.

[5]  E V Koonin,et al.  Chromosome 2 sequence of the human malaria parasite Plasmodium falciparum. , 1998, Science.

[6]  R. Kay,et al.  The Dictyostelium genome project: an invitation to species hopping. , 1999, Trends in genetics : TIG.

[7]  W. Doolittle,et al.  A kingdom-level phylogeny of eukaryotes based on combined protein data. , 2000, Science.

[8]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[9]  B. Meyer,et al.  Vive la différence: males vs females in flies vs worms. , 1996, Annual review of genetics.

[10]  Alex Bateman,et al.  InterPro: An Integrated Documentation Resource for Protein Families, Domains and Functional Sites , 2002, Briefings Bioinform..

[11]  B. Barrell,et al.  The genome sequence of Schizosaccharomyces pombe , 2002, Nature.

[12]  R. Gwilliam,et al.  The complete nucleotide sequence of chromosome 3 of Plasmodium falciparum , 1999, Nature.

[13]  Paul H. Dear,et al.  Genome mapping : a practical approach , 1997 .

[14]  Andrew Smith.  Genome sequence of the nematode C-elegans: A platform for investigating biology , 1998 .

[15]  G. Markakis,et al.  Wolbachia infection and cytoplasmic incompatibility in Drosophila species. , 1996, Genetics.

[16]  J. Werren,et al.  Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia , 2001, Nature.

[17]  T. Cline,et al.  Expression of the Sex-lethal gene is controlled at multiple levels during Drosophila oogenesis. , 1993, Development.

[18]  M. Boguski,et al.  A Survey of Human Disease Gene Counterparts in the Drosophila Genome , 2000, The Journal of cell biology.

[19]  N. Perrimon,et al.  Genetic evidence that the sans fille locus is involved in Drosophila sex determination. , 1988, Genetics.

[20]  P. Dear,et al.  A high-resolution HAPPY map of Dictyostelium discoideum chromosome 6. , 2000, Genome research.

[21]  M. Goebl,et al.  Most of the yeast genomic sequences are not essential for cell growth and division , 1986, Cell.

[22]  R. Giordano,et al.  16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[23]  T. Saito,et al.  The Dictyostelium developmental cDNA project: generation and analysis of expressed sequence tags from the first-finger stage of development. , 1998, DNA research : an international journal for rapid publication of reports on genes and genomes.

[24]  C. Parent,et al.  A cell's sense of direction. , 1999, Science.

[25]  L. Eichinger,et al.  Dictyostelium as model system for studies of the actin cytoskeleton by molecular genetics , 1999, Microscopy research and technique.

[26]  J. Knight.  Meet the Herod bug , 2001, Nature.

[27]  J. Berg.  Genome sequence of the nematode C. elegans: a platform for investigating biology. , 1998, Science.

[28]  H. Robertson,et al.  Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. , 1993, Science.

[29]  J. V. Moran,et al.  Initial sequencing and analysis of the human genome. , 2001, Nature.

[30]  R. Firtel,et al.  Dictyostelium: a model for regulated cell movement during morphogenesis. , 2000, Current opinion in genetics & development.

[31]  E. Blackburn,et al.  Single extrachromosomal ribosomal rna gene copies are synthesized during amplification of the rDNA in tetrahymena , 1981, Cell.

[32]  W. Loomis.  Genetic networks that regulate development in Dictyostelium cells. , 1996, Microbiological reviews.

[33]  G. Glöckner.  Large Scale Sequencing and Analysis of AT Rich Eukaryote Genomes , 2000 .

[34]  S. Eddy,et al.  tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. , 1997, Nucleic acids research.

[35]  M. Quail,et al.  The complex repeats of Dictyostelium discoideum. , 2001, Genome research.

[36]  T. Schüpbach.  Normal female germ cell differentiation requires the female X chromosome to autosome ratio and expression of sex-lethal in Drosophila melanogaster. , 1985, Genetics.

[37]  T. Cline.  A male-specific lethal mutation in Drosophila melanogaster that transforms sex. , 1979, Developmental biology.

[38]  D. Bopp,et al.  Recombination and disjunction in female germ cells of Drosophila depend on the germline activity of the gene sex-lethal. , 1999, Development.

[39]  A. Noegel,et al.  The actin cytoskeleton of Dictyostelium: a story told by mutants. , 2000, Journal of cell science.

[40]  J. Werren.  Biology of Wolbachia. , 2003, Annual review of entomology.

[41]  A. Mahowald,et al.  The role of the ovarian tumor locus in Drosophila melanogaster germ line sex determination. , 1993, Development.

[42]  C. Burge,et al.  A computational analysis of sequence features involved in recognition of short introns , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[43]  M. Steinmann‐Zwicky.  Sex determination in Drosophila: the X‐chromosomal gene liz is required for Sxl activity. , 1988, The EMBO journal.

[44]  Y. Fuyama,et al.  Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. , 2000, Genetics.

[45]  T. Cline,et al.  Induction of female Sex-lethal RNA splicing in male germ cells: implications for Drosophila germline sex determination. , 1997, Development.

[46]  F. Cross,et al.  Growth and division. , 1994, Science.

[47]  The Arabidopsis Genome Initiative.  Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[48]  R. Guigó,et al.  GeneID in Drosophila. , 2000, Genome research.

[49]  B. Barrell,et al.  Life with 6000 Genes , 1996, Science.

[50]  T. Cline,et al.  The Drosophila female-specific sex-determination gene, Sex-lethal, has stage-, tissue-, and sex-specific RNAs suggesting multiple modes of regulation. , 1989, Genes & development.

[51]  T. Cline,et al.  Functional changes associated with structural alterations induced by mobilization of a P element inserted in the Sex-lethal gene of Drosophila. , 1987, Genetics.

[52]  M. Hochberg,et al.  Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp , 2001, Proceedings of the National Academy of Sciences of the United States of America.