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, 18 (6), 986-94

Defensins and the Convergent Evolution of Platypus and Reptile Venom Genes

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Defensins and the Convergent Evolution of Platypus and Reptile Venom Genes

Camilla M Whittington et al. Genome Res.

Abstract

When the platypus (Ornithorhynchus anatinus) was first discovered, it was thought to be a taxidermist's hoax, as it has a blend of mammalian and reptilian features. It is a most remarkable mammal, not only because it lays eggs but also because it is venomous. Rather than delivering venom through a bite, as do snakes and shrews, male platypuses have venomous spurs on each hind leg. The platypus genome sequence provides a unique opportunity to unravel the evolutionary history of many of these interesting features. While searching the platypus genome for the sequences of antimicrobial defensin genes, we identified three Ornithorhynchus venom defensin-like peptide (OvDLP) genes, which produce the major components of platypus venom. We show that gene duplication and subsequent functional diversification of beta-defensins gave rise to these platypus OvDLPs. The OvDLP genes are located adjacent to the beta-defensins and share similar gene organization and peptide structures. Intriguingly, some species of snakes and lizards also produce venoms containing similar molecules called crotamines and crotamine-like peptides. This led us to trace the evolutionary origins of other components of platypus and reptile venom. Here we show that several venom components have evolved separately in the platypus and reptiles. Convergent evolution has repeatedly selected genes coding for proteins containing specific structural motifs as templates for venom molecules.

Figures

Figure 1.
Figure 1.
We identified six beta-defensin and four alpha-defensin genes in the platypus genome, shown in alignment. Alternating text color denotes exons, and the first amino acid of the mature peptide is highlighted in orange. Conserved cysteine residues are highlighted in pink. It can be seen that DEFA4 (boxed) has a cysteine spacing that is intermediate between the alpha- and beta-defensins: Like the alpha-defensins, its first two cysteine residues are separated by one amino acid, but the fourth and fifth residues are separated by six rather than nine amino acids. However, DEFA4 does possess an anionic propiece, the net charge of which counterbalances that of its mature defensin domain, which are clear characteristics of alpha-defensins (Liu and Ganz 1995; Hughes and Yeager 1997).
Figure 2.
Figure 2.
Neighbor joining tree of therian and platypus beta-defensins (DEFB1–6), in red, with chicken beta-defensins (Chick AvBD1–13) and platypus and reptile venom peptides. Chicken and therian sequences are shaded based on whether they belong to synteny groups A (yellow), B (blue), C (green), or D (pink). These synteny groups were determined by Patil et al. (2004) and Belov et al. (2007) based on genomic localization and phylogeny. Platypus DEFB1–5, which we have mapped to chromosome X2, belong to synteny group A, while platypus DEFB6, mapped to chromosome X1, belongs to synteny group D. Similar topologies were recreated using Baysian phylogenetics approaches.
Figure 3.
Figure 3.
Genomic organization of regions of conserved synteny between alpha- and beta-defensins in eutherians, the platypus, and the chicken, based on previously published data (Belov et al. 2007; Patil et al. 2005). Synteny group A, the most ancient beta-defensin synteny group, contains most of the platypus beta-defensins, with synteny group D, containing DEFB6, arising next. Subsequent duplications and translocations have given rise to synteny groups B and C in the later vertebrate lineage. Eutherian genes with labels containing numbers only are beta-defensins. Chicken beta-defensins are labeled as “AvBD,” and mouse alpha-defensins (cryptidins) are labeled as ‘”Defcr.” Solid lines link orthologs based on the phylogenetic tree (Fig. 2), and broken lines connect paralogs; pseudogenes are indicated by white arrows; slanted lines indicate breaks in the group; slanted dotted lines indicate a mouse beta-defensin cluster that is not mapped on chromosome 8. An asterisk indicates the putative early alpha-defensin. The fragmented nature of the platypus genome sequence (Warren et al. 2008) meant that, although the platypus alpha- and beta-defensins and the OvDLPs were localized to chromosomes using FISH mapping and phylogenetic analysis, contig order could not be determined and is instead inferred based on synteny.
Figure 4.
Figure 4.
Overlain structural predictions of identified platypus beta-defensin and OvDLP peptides produced using LALIGN and MODELLER. The structures of DEFB1 (green), OvDLP-B (pink), and DEFB-VL (blue) peptides show notable similarities, supporting the idea that beta-defensins and OvDLPs are evolutionarily related.
Figure 5.
Figure 5.
Syntenic relationships of platypus and reptile venom peptides, based on previously published therian synteny (Patil et al. 2005; Belov et al. 2007) and our phylogenetic analysis (Fig. 2). This shows that the platypus OvDLPs and sauropsid reptile vCLPs and crotamines have evolved from different beta-defensin paralogs belonging to the ancestral synteny group A. Genome arrangements of reptile sequences are unknown, so these are inferred based on synteny and connected by dotted lines.

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