The opossum genome: insights and opportunities from an alternative mammal

Abstract

The strategic importance of the genome sequence of the gray, short-tailed opossum, Monodelphis domestica, accrues from both the unique phylogenetic position of metatherian (marsupial) mammals and the fundamental biologic characteristics of metatherians that distinguish them from other mammalian species. Metatherian and eutherian (placental) mammals are more closely related to one another than to other vertebrate groups, and owing to this close relationship they share fundamentally similar genetic structures and molecular processes. However, during their long evolutionary separation these alternative mammals have developed distinctive anatomical, physiologic, and genetic features that hold tremendous potential for examining relationships between the molecular structures of mammalian genomes and the functional attributes of their components. Comparative analyses using the opossum genome have already provided a wealth of 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 genome sequence is also beginning to enlarge our understanding of the evolution and function of the vertebrate immune system, and it provides an alternative model for investigating mechanisms of genomic imprinting. Equally important, availability of the genome sequence is fostering the development of new research tools for physical and functional genomic analyses of M. domestica that are expanding its versatility as an experimental system for a broad range of research applications in basic biology and biomedically oriented research.

Figure 1.

Phylogenetic splitting topology and approximate ages for mammalian divergences discussed in this article. Shaded boxes indicate approximate ranges for divergence date estimates extracted from multiple literature sources cited in the main text and footnote 2. Approximate dates for the earliest (deepest) divergences among extant species within the eutherian and metatherian lineages are indicated by arrowheads. As for the branching points, the shaded boxes associated with arrowheads indicate approximate range estimates for these basal divergence dates.

Figure 2.

Monodelphis domestica. (A) Adult female. (B) Female with a litter of 10 pups. The newborns are ∼36 h postpartum age. Note that M. domestica does not possess a pouch. (C) Detail of litter seen in panel B. (D) Newborn, <12 h postpartum age. Scale is 1 mm between marks. (Photos: Larry Wadsworth, TAMU Media Resources.)

Figure 3.

Sex-specific linkage maps for chromosomes 1 and 2 (linkage groups 1 and 3) of Monodelphis domestica. For each pair of maps, the female map is to the left. Scale is in centiMorgans (cM) with zero corresponding to the p terminus of the chromosome. Information for individual map markers may be found in Samollow et al. (2007).

Figure 4.

Comparison of MHC organization in representative mammals (figure and legend adapted from Belov et al. 2006, with permission). Of particular note in the opossum MHC is the arrangement of the Class I and II genes into a single interspersed cluster and the absence of Class I genes from the Framework region. These characteristics are reminiscent of arrangements seen in the MHCs of nonmammalian vertebrates. Lines between MHCs of different species indicate the positions of orthologous genes. The asterisk indicates the presence of a duplicated DMB locus (H2-DMb2) in mouse, but not in rat. Dashed lines and question marks represent missing or uncertain data for the particular gene or portion of the genome. Numbers within boxes indicate the number of predicted genes identified within that segment (pseudogenes not included). Unless otherwise indicated, the small boxes indicate individual genes. Map not drawn to scale. Additional details regarding this diagram and implications for the evolution of the mammalian MHC may be found in Belov et al. (2006).