Evolution and Characteristics of the Opossum Genome

The opossum genome sequence furnishes a critical comparator for examining the evolutionary histories of vertebrate genomes in general, and provides the most appropriate outgroup sequence for establishing the relative antiquity or novelty of genetic features among the major lineages of eutherian (‘placental’) mammals. Comparative analyses using the opossum genome have already provided a wealth of evidence regarding the importance of noncoding elements in the evolution of mammalian genomes, the role of transposable elements in driving genomic innovation, and the relationships between recombination rate, nucleotide composition, and the genomic distributions of repetitive elements. This article summarizes key features of the opossum genome and discusses their implications for better understanding the varied processes that contribute to genome evolution and how changes in structural organization, complexity, and molecular functions of mammalian (and other) genomes can lead to differences in gene regulation, expression, and action among and within species. Key concepts: Because the pace of evolutionary change varies for different classes of genomic elements, the power of comparative genomic analysis is dependent on the availability of genomic data from organisms occupying key phylogenetic positions that enable comparisons of both slow and fast evolving genomic features. Metatherian (marsupial) and eutherian (placental) mammals are each other's closest relatives. During divergence from their common ancestor they evolved distinctive morphologic, physiologic, and genetic variations on the elemental mammalian patterns. These distinctions hold great potential for examining relationships between the molecular structures of mammalian genomes and the functional attributes of their components. Representing the Metatheria, the opossum genome furnishes a crucial reference for examining the evolutionary histories of vertebrate genomes in general, and provides the most appropriate outgroup sequence for establishing ancestral versus derived polarity for genomic and genetic features among the major lineages of eutherian mammals. The opossum genome sequence has provided new evidence regarding the importance of noncoding elements in the evolution of mammalian genomes, the role of transposable elements in driving genomic innovation, and the relationships between recombination rate, nucleotide composition, and the genomic distributions of repetitive elements. The opossum genome is comprised of eight very large autosomes and a sex chromosome (X or Y), and exhibits extremely low levels of meiotic recombination relative to other mammalian genomes examined. The opossum genome exhibits the lowest levels of G and C nucleotides known among sequenced amniotes. At least 52% of the opossum genome is composed of interspersed repeat family elements—the highest level known from sequenced amniotes. Low recombination rate may contribute to the unusual nucleotide composition and the high levels of interspersed repeat elements in the opossum genome. The protein-coding gene complement of the opossum genome is very similar to that of eutherian mammals and other vertebrates. Conserved noncoding genomic elements (CNEs) show high levels of novelty between opossum and eutherian genomes and strong lineage specificity among eutherian clades. This finding strengthens the idea that in mammalian evolution alterations in the repertoires of noncoding elements that regulate protein-coding gene function may be more important than changes in the structures or numbers of protein-coding genes. The opossum genome has provided new evidence regarding the structure of the ancestral eutherian karyotype and the evolution of genomic imprinting. It also furnishes new tools to study the evolution and function of the mammalian immune system and the phenomenon of X-chromosome inactivation. Keywords: comparative genomics; marsupials; genome evolution; recombination; phylogeny