Abstract

The evolutionary pathway of highly toxic proteins expressed in snake venom glands from proteins without toxic function and expressed in non-parotid tissues remains poorly understood. Here we examine gene structure of a representative of a venom protein with an ADAMs metalloproteinase evolutionary origin. The structure of the 15,652 bp Echis ocellatus pre-pro EOC00089-like PIII-SVMP gene was assembled from PCR-amplified sequences of overlapping genomic fragments. The gene comprises 12 exons interrupted by 11 introns. In a homology model of the EOC00089-like protein, the insertion of introns interrupting coding regions lie just after or between secondary structure elements. Long interspersed nuclear retroelements (LINE) L2/CR1 and RTE/Bov-B, short interspersed nuclear retroelements SINE/Sauria, and a hobo-activator DNA (Charlie, hAT) transposon were identified within introns 1, 3, 7 and 8. Pairwise amino acid sequence comparisons between EOC00089-like PIII-SVMP and its closest orthologs, ADAM28, from a mammal, Homo sapiens, and the lizard, Anolis carolinensis, showed that the ORFs of these three proteins share 42%/59%, 49%/69%, and 48%/65% (identity/similarity), respectively. The protein-coding positions interrupted by each of the 11 introns of the Echis PIII-SVMP gene are entirely conserved in the A. carolinensis and human ADAM28 genes. However, the lizard and the human ADAM28 genes contain 5 introns not present in the E. ocellatus gene. Furthermore, Echis and Anolis introns exhibit quantitatively and qualitatively distinctions in their inserted retroelements. These findings identify introns as possible key elements in the recruitment and amplification process of SVMPs into the venom gland of extant snakes. Ongoing reptile genome sequencing projects may shed light on this intriguing aspect of the emergence and evolution of venom toxin genes. Furthermore, the organization of the PIII-SVMP reported here provides a genomic explanation for the emergence of dimeric disintegrin subunits encoded by short messengers.

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