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Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia).
Mol Cell Proteomics 2008; 7(2):215-46MC

Abstract

Venom is a key innovation underlying the evolution of advanced snakes (Caenophidia). Despite this, very little is known about venom system structural diversification, toxin recruitment event timings, or toxin molecular evolution. A multidisciplinary approach was used to examine the diversification of the venom system and associated toxins across the full range of the approximately 100 million-year-old advanced snake clade with a particular emphasis upon families that have not secondarily evolved a front-fanged venom system (approximately 80% of the 2500 species). Analysis of cDNA libraries revealed complex venom transcriptomes containing multiple toxin types including three finger toxins, cobra venom factor, cysteine-rich secretory protein, hyaluronidase, kallikrein, kunitz, lectin, matrix metalloprotease, phospholipase A(2), snake venom metalloprotease/a disintegrin and metalloprotease, and waprin. High levels of sequence diversity were observed, including mutations in structural and functional residues, changes in cysteine spacing, and major deletions/truncations. Morphological analysis comprising gross dissection, histology, and magnetic resonance imaging also demonstrated extensive modification of the venom system architecture in non-front-fanged snakes in contrast to the conserved structure of the venom system within the independently evolved front-fanged elapid or viperid snakes. Further, a reduction in the size and complexity of the venom system was observed in species in which constriction has been secondarily evolved as the preferred method of prey capture or dietary preference has switched from live prey to eggs or to slugs/snails. Investigation of the timing of toxin recruitment events across the entire advanced snake radiation indicates that the evolution of advanced venom systems in three front-fanged lineages is associated with recruitment of new toxin types or explosive diversification of existing toxin types. These results support the role of venom as a key evolutionary innovation in the diversification of advanced snakes and identify a potential role for non-front-fanged venom toxins as a rich source for lead compounds for drug design and development.

Authors+Show Affiliations

Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, Victoria 3010, Australia. bgf@unimelb.edu.auNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

17855442

Citation

Fry, Bryan G., et al. "Evolution of an Arsenal: Structural and Functional Diversification of the Venom System in the Advanced Snakes (Caenophidia)." Molecular & Cellular Proteomics : MCP, vol. 7, no. 2, 2008, pp. 215-46.
Fry BG, Scheib H, van der Weerd L, et al. Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Mol Cell Proteomics. 2008;7(2):215-46.
Fry, B. G., Scheib, H., van der Weerd, L., Young, B., McNaughtan, J., Ramjan, S. F., ... Norman, J. A. (2008). Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Molecular & Cellular Proteomics : MCP, 7(2), pp. 215-46.
Fry BG, et al. Evolution of an Arsenal: Structural and Functional Diversification of the Venom System in the Advanced Snakes (Caenophidia). Mol Cell Proteomics. 2008;7(2):215-46. PubMed PMID: 17855442.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). AU - Fry,Bryan G, AU - Scheib,Holger, AU - van der Weerd,Louise, AU - Young,Bruce, AU - McNaughtan,Judith, AU - Ramjan,S F Ryan, AU - Vidal,Nicolas, AU - Poelmann,Robert E, AU - Norman,Janette A, Y1 - 2007/09/12/ PY - 2007/9/15/pubmed PY - 2008/3/28/medline PY - 2007/9/15/entrez SP - 215 EP - 46 JF - Molecular & cellular proteomics : MCP JO - Mol. Cell Proteomics VL - 7 IS - 2 N2 - Venom is a key innovation underlying the evolution of advanced snakes (Caenophidia). Despite this, very little is known about venom system structural diversification, toxin recruitment event timings, or toxin molecular evolution. A multidisciplinary approach was used to examine the diversification of the venom system and associated toxins across the full range of the approximately 100 million-year-old advanced snake clade with a particular emphasis upon families that have not secondarily evolved a front-fanged venom system (approximately 80% of the 2500 species). Analysis of cDNA libraries revealed complex venom transcriptomes containing multiple toxin types including three finger toxins, cobra venom factor, cysteine-rich secretory protein, hyaluronidase, kallikrein, kunitz, lectin, matrix metalloprotease, phospholipase A(2), snake venom metalloprotease/a disintegrin and metalloprotease, and waprin. High levels of sequence diversity were observed, including mutations in structural and functional residues, changes in cysteine spacing, and major deletions/truncations. Morphological analysis comprising gross dissection, histology, and magnetic resonance imaging also demonstrated extensive modification of the venom system architecture in non-front-fanged snakes in contrast to the conserved structure of the venom system within the independently evolved front-fanged elapid or viperid snakes. Further, a reduction in the size and complexity of the venom system was observed in species in which constriction has been secondarily evolved as the preferred method of prey capture or dietary preference has switched from live prey to eggs or to slugs/snails. Investigation of the timing of toxin recruitment events across the entire advanced snake radiation indicates that the evolution of advanced venom systems in three front-fanged lineages is associated with recruitment of new toxin types or explosive diversification of existing toxin types. These results support the role of venom as a key evolutionary innovation in the diversification of advanced snakes and identify a potential role for non-front-fanged venom toxins as a rich source for lead compounds for drug design and development. SN - 1535-9484 UR - https://www.unboundmedicine.com/medline/citation/17855442/Evolution_of_an_arsenal:_structural_and_functional_diversification_of_the_venom_system_in_the_advanced_snakes__Caenophidia__ L2 - http://www.mcponline.org/cgi/pmidlookup?view=long&pmid=17855442 DB - PRIME DP - Unbound Medicine ER -