Comparative sequencing provides insights about the structure and conservation of marsupial and monotreme genomes.

Sequencing and comparative analyses of genomes from multiple vertebrates are providing insights about the genetic basis for biological diversity. To date, these efforts largely have focused on eutherian mammals, chicken, and fish. In this article, we describe the generation and study of genomic sequences from noneutherian mammals, a group of species occupying unusual phylogenetic positions. A large sequence data set (totaling >5 Mb) was generated for the same orthologous region in three marsupial (North American opossum, South American opossum, and Australian tammar wallaby) and one monotreme (platypus) genomes. These ancient mammalian genomes are characterized by unusual architectural features with respect to G + C and repeat content, as well as compression relative to human. Approximately 14% and 34% of the human sequence forms alignments with the orthologous sequence from platypus and the marsupials, respectively; these numbers are distinctly lower than that observed with nonprimate eutherian mammals (45-70%). The alignable sequences between human and each marsupial species are not completely overlapping (only 80% common to all three species) nor are the platypus-alignable sequences completely contained within the marsupial-alignable sequences. Phylogenetic analysis of synonymous coding positions reveals that platypus has a notably long branch length, with the human-platypus substitution rate being on average 55% greater than that seen with human-marsupial pairs. Finally, analyses of the major mammalian lineages reveal distinct patterns with respect to the common presence of evolutionarily conserved vertebrate sequences. Our results confirm that genomic sequence from noneutherian mammals can contribute uniquely to unraveling the functional and evolutionary histories of the mammalian genome.

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

[2]  M. Springer,et al.  The evolution of tribospheny and the antiquity of mammalian clades. , 2003, Molecular phylogenetics and evolution.

[3]  W. Miller,et al.  Distinguishing regulatory DNA from neutral sites. , 2003, Genome research.

[4]  E. Birney,et al.  Comparative genomics: genome-wide analysis in metazoan eukaryotes , 2003, Nature Reviews Genetics.

[5]  Len A Pennacchio,et al.  Comparative genomic analysis as a tool for biological discovery , 2003, The Journal of physiology.

[6]  D. Labuda,et al.  Evolutionary inventions and continuity of CORE-SINEs in mammals. , 2000, Journal of molecular biology.

[7]  Berthold Göttgens,et al.  Comparative and functional analyses of LYL1 loci establish marsupial sequences as a model for phylogenetic footprinting. , 2003, Genomics.

[8]  J. Graves,et al.  Marsupial genetics and genomics. , 2002, Trends in genetics : TIG.

[9]  C. Fizames,et al.  Characterization and repeat analysis of the compact genome of the freshwater pufferfish Tetraodon nigroviridis. , 2000, Genome research.

[10]  Colin N. Dewey,et al.  Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution , 2004, Nature.

[11]  W. Murphy,et al.  Resolution of the Early Placental Mammal Radiation Using Bayesian Phylogenetics , 2001, Science.

[12]  D. Haussler,et al.  Aligning multiple genomic sequences with the threaded blockset aligner. , 2004, Genome research.

[13]  J. Deakin,et al.  The monotreme genome: a patchwork of reptile, mammal and unique features? , 2003, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[14]  Arend Sidow,et al.  Genomic regulatory regions: insights from comparative sequence analysis. , 2003, Current opinion in genetics & development.

[15]  P. Green,et al.  Bayesian Markov chain Monte Carlo sequence analysis reveals varying neutral substitution patterns in mammalian evolution. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[16]  W. D. Jackson,et al.  DNA Content of Monotremes , 1967, Nature.

[17]  Lisa M. D'Souza,et al.  Genome sequence of the Brown Norway rat yields insights into mammalian evolution , 2004, Nature.

[18]  Sudhir Kumar,et al.  Mutation rates in mammalian genomes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Thomas R. Buckley,et al.  Marsupials and Eutherians reunited: genetic evidence for the Theria hypothesis of mammalian evolution , 2001, Mammalian Genome.

[20]  E. H. Margulies,et al.  Detecting highly conserved regions of the human genome by multispecies sequence comparisons. , 2003, Cold Spring Harbor symposia on quantitative biology.

[21]  N. M. Brooke,et al.  A molecular timescale for vertebrate evolution , 1998, Nature.

[22]  C. Groves,et al.  Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence. , 1998, Molecular phylogenetics and evolution.

[23]  Nancy F. Hansen,et al.  Comparative analyses of multi-species sequences from targeted genomic regions , 2003, Nature.

[24]  S. Garagna,et al.  DNA content variability in several species of Australian and South American marsupials , 1981 .

[25]  Paramvir S. Dehal,et al.  Whole-Genome Shotgun Assembly and Analysis of the Genome of Fugu rubripes , 2002, Science.

[26]  P. Green,et al.  Transcription-associated mutational asymmetry in mammalian evolution , 2003, Nature Genetics.

[27]  D. Labuda,et al.  CORE-SINEs: eukaryotic short interspersed retroposing elements with common sequence motifs. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Francesca Chiaromonte,et al.  Regulatory potential scores from genome-wide three-way alignments of human, mouse, and rat. , 2004, Genome research.

[29]  J. Touchman,et al.  Vertebrate genome sequencing: building a backbone for comparative genomics. , 2002, Trends in genetics : TIG.

[30]  D. Haussler,et al.  Article Identification and Characterization of Multi-Species Conserved Sequences , 2022 .

[31]  S. Eddy,et al.  Automated de novo identification of repeat sequence families in sequenced genomes. , 2002, Genome research.

[32]  Matthew J Wakefield,et al.  The kangaroo genome , 2003, EMBO reports.

[33]  D. Haussler,et al.  Phylogenetic estimation of context-dependent substitution rates by maximum likelihood. , 2003, Molecular biology and evolution.

[34]  Axel Janke,et al.  Phylogenetic Analysis of 18S rRNA and the Mitochondrial Genomes of the Wombat, Vombatus ursinus, and the Spiny Anteater, Tachyglossus aculeatus: Increased Support for the Marsupionta Hypothesis , 2002, Journal of Molecular Evolution.

[35]  D. Penny,et al.  The root of the mammalian tree inferred from whole mitochondrial genomes. , 2003, Molecular phylogenetics and evolution.

[36]  S. Batzoglou,et al.  Characterization of evolutionary rates and constraints in three Mammalian genomes. , 2004, Genome research.

[37]  Colin N. Dewey,et al.  Initial sequencing and comparative analysis of the mouse genome. , 2002 .