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Comparative Study
. 2005 Mar 1;102(9):3354-9.
doi: 10.1073/pnas.0408539102. Epub 2005 Feb 17.

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

Elliott H Margulies  1 ; NISC Comparative Sequencing Program; Valerie V B Maduro, Pamela J Thomas, Jeffery P Tomkins, Chris T Amemiya, Meizhong Luo, Eric D Green
Affiliations
Comparative Study

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

Elliott H Margulies et al. Proc Natl Acad Sci U S A. .

Abstract

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.

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Figures

Fig. 1.
Fig. 1.
Comparison of the content and types of repetitive elements among different species' sequences. Sequences from the orthologous regions of the indicated species' genomes were analyzed by repeatmasker, allowing detection and quantification of the indicated types of repetitive elements. The data for the noneutherian mammals are highlighted for emphasis. SINEs, short interspersed nucleotide elements; LINEs, long interspersed nucleotide elements.
Fig. 2.
Fig. 2.
Patterns of sequence conservation among different vertebrates. (A) The fraction of human sequence forming alignments with sequences from each of the indicated species is shown, broken down for four annotated categories. The additional alignable sequence (indicated in purple, see text for details) found exclusive to the TBA-generated multisequence alignment (20) falls largely within nonexonic regions. For data that include a larger set of vertebrates, see the supporting information. (B) The relationships between the fraction of human sequence aligned and estimated branch length from human (calculated as substitutions per site) are shown for the indicated vertebrate species.
Fig. 3.
Fig. 3.
Phylogenetic tree of vertebrate species. By using the generated 27-species multisequence alignment, branch lengths were calculated based on analysis of synonymous coding positions. The branch lengths (as substitutions per synonymous site) between human and each species are listed (with additional pair-wise branch lengths provided in the supporting information). The last common ancestor among the catarrhine primates (A) is estimated at 25 mya (36, 37), between the rodents and primates (B) at 75 mya (5, 6), between eutherians and metatherians (C) at 185 mya (14), between monotremes and other therians (D) at 200 mya (14), and between mammals and birds (E) at 310 mya (13).
Fig. 4.
Fig. 4.
Lineage specificity of MCSs. The proportion of nonexonic MCSs found in the sequences of species in each category is indicated. Note that virtually all MCSs overlapping known exonic sequences are present in all mammals (data not shown). All Mammals: cat, dog, cow, pig, rat, mouse, N.A. opossum, wallaby, and platypus; Eutherian: cat, dog, cow, pig, rat, and mouse; Marsupials: N.A. opossum and wallaby; and Other: species combinations containing <2% of the analyzed MCSs (see the supporting information for the complete data set). Hashed areas of “All Mammals” reflect portions lacking one or both rodents, and hashed portions of “Eutherian + Marsupials” reflect portions lacking both rodents.
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