Phylogeny-Based Comparative Analysis of Venom Proteome Variation in a Clade of Rattlesnakes (Sistrurus sp.)

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Gibbs, H Lisle ^a   Sanz, Libia ^b   Sovic, Michael G ^a   Calvete, Juan J ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME; SNAKE VENOM;

ANIMAL BEHAVIOR; ARTICLE; BIOCHEMICAL COMPOSITION; CLADISTICS; CROTALUS; DIETARY INTAKE; GENE SEQUENCE; LIZARD; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NATURAL SELECTION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SISTRURUS MILARIUS MILARIUS; SISTRURUS MILARIUS STRECKERI; SPECIES DIVERSITY; TOXIN ANALYSIS;

ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, REVERSE-PHASE; CROTALID VENOMS; CROTALUS; DIET; EVOLUTION, MOLECULAR; GENETIC LOCI; LEAST-SQUARES ANALYSIS; PHYLOGENY; PROTEOME; PROTEOMICS;

CROTALUS; MAMMALIA; SERPENTES; SISTRURUS; SQUAMATA;

EID: 84879494960     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067220     Document Type: Article

References (57)

1. Meier J, Stocker KF (1995) Biology and distribution of venomous snakes of medical importance and the composition of snake venoms. In Handbook of Clinical Toxicology of Animal Venoms and Poisons (Meier J, White J, eds), CRC Press Inc, Boca Raton, Florida, USA, p.367-412.
2. Ménez A (ed) (2002) Perspectives in Molecular Toxinology. J Wiley and Sons, UK.
3. Markland FS, (1998) Snake venoms and the hemostatic system. Toxicon 36: 1749-1800.
4. Calvete JJ (2010) Snake venomics, antivenomics, and venom phenotyping: The Ménage à Trois of proteomic tools aimed at understanding the biodiversity of venoms. In Toxins and Hemostasis: from Bench to Bedside (Kini RM, Markland F, McLane MA, Morita T, eds.), Springer, Dordrecht (The Netherlands), p.45-72.
5. Fry BG, Wüster W, (2004) Assembling an arsenal: origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences. Mol. Biol. Evol. 21: 870-83.
6. Fry BG, (2005) From genome to 'venome': Molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins. Genome Res. 15: 403-20.
7. Serrano SM, Shannon JD, Wang D, Camargo AC, Fox JW, (2005) A multifaceted analysis of viperid snake venoms by two-dimensional gel electrophoresis: an approach to understanding venom proteomics. Proteomics 5: 501-10.
8. Calvete JJ, Juárez P, Sanz L, (2007) Snake venomics. Strategy and applications. J. Mass. Spectrom. 42: 1405-14.
9. Mackessy SP, ed (2010) Handbook of Venoms and Toxins of Reptiles. CRC Press, Taylor & Francis Group, Boca Raton, FL.
10. Chippaux J-P, Williams V, White J, (1991) Snake venom variability: methods of study, results and interpretation. Toxicon 29: 1279-303.
11. Mackessy SP (2010)The field of reptile toxinology: snakes, lizards and their venoms. In Handbook of Venoms and Toxins of Reptiles (Mackessy SP, ed). CRC Press, Taylor & Francis Group, Boca Raton, FL, P.3-23.
12. Daltry JC, Wüster W, Thorpe RS, (1996) Diet and snake venom evolution. Nature 379: 537-40.
13. Wüster W, Daltry JC, Thorpe RS, (1999) Can diet explain intraspecific venom variation? Reply to Sasa. Toxicon 37: 253-8.
14. Barlow A, Pook CE, Harrison RA, Wüster W, (2009) Co-evolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution. Proceedings of the Royal Society B 276: 2443-9.
15. Williams V, White J, Schwaner TD, Sparrow A, (1998) Variation in venom proteins from isolated populations of tiger snakes (Notechis ater niger, N. scutatus) in South Australia. Toxicon 26: 1067-75.
16. Sasa M, (1999) Diet and snake venom evolution: can local selection alone explain intraspecific vemon variation? Toxicon 32: 249-52.
17. Mebs D. Toxicity in animals, (2001) Trends in evolution? Toxicon 39: 87-96.
18. Mackessy SP (2008) Venom composition in rattlesnakes: trends and biological significance. In The Biology of Rattlesnakes (Hayes WK, Beaman KR, Cardwell MD, Bush SP (eds). Loma Linda University Press, Loma Linda, California, p.495-510.
19. Nunn CL (2011) The comparative approach in evolutionary anthropology and Biology. University of Chicago Press, Chicago.
20. Blomberg SP, Garland T Jr, Ives AR, (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more laible. Evolution 57: 717-745.
21. Campbell JA, Lamar W (2004) The Venomous Reptiles of the Western Hemisphere, Cornell University Press, Ithaca, New York.
22. Kubatko LS, Gibbs HL, Bloomquist EW, (2011) Inferring species-level phylogenies and taxonomic distinctiveness using multilocus data in Sistrurus rattlesnakes. Syst. Biol. 60: 393-409.
23. Sanz L, Gibbs HL, Mackessy SP, Calvete JJ, (2006) Venom proteomes of closely related Sistrurus rattlesnakes with divergent diets. J. Proteome Res. 5: 2098-112.
24. Gibbs HL, Mackessy SP, (2006) Functional basis of a molecular adaptation: Prey-specic toxic effects of venom from Sistrurus rattlesnakes. Toxicon 53: 672-9.
25. Calvete JJ, Fasoli E, Sanz L, Boschetti E, Righetti PG, (2009) Exploring the venom proteome of the western diamondback rattlesnake, Crotalus atrox, via snake venomics and combinatorial peptide ligand library approaches.J. Proteome Res. 8: 3055-67.
26. Gibbs HL, Chiucchi JE, (2011) Deconstructing a complex molecular phenotype: population- level variation in individual venom proteins in eastern massasauga rattlesnakes (Sistrurus c. catenatus). Journal of Molecular Evolution 72: 383-397.
27. Gibbs HL, Sanz L, Chiucchi JE, Farrell TM, Calvete JJ, (2011) Proteomic analysis of ontogenetic and diet-related changes in venom composition of juvenile and adult Dusky Pigmy rattlesnakes (Sistrurus miliarius barbouri). J Proteomics 74: 2169-79.
28. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipmann DJ, (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-402.
29. Murphy RW, Fu J, Lathrop A, Feltham JV, Kovak V (2002) Phylogeny of the rattlesnakes (Crotalus and Sistrurus) inferred from sequences of five mitochondrial DNA genes. In Biology of the Vipers (Schuett GW, Hoggren M, Douglas ME, Greene HW, eds), Eagle Mountain Publishing, LC, Eagle Mountain, Utah, p.69-92.
30. Bryson RW Jr, Murphy RW, Graham MR, Lathrop A, Lazcano-Villareal D, (2011) Ephemeral Pleistocene woodlands connect the dots for highland rattlesnakes of the Crotalus intermedius group. J. Biogeograph. 38: 2299-310.
31. R Development Core Team (2005). R: A language and environment for statistical computing, reference index version 2.2.1. R Foundation for Statistical Computing, Vienna, Austria.
32. Holycross AT, Mackessy SP, (2002) Variation in the diet of Sistrurus catenatus (massasauga) with emphasis on Sistrurus catenatus edwardsii (desert massasauga). Journal of Herpetology 36: 454-464.
33. Beavers RA, (1976) Food habits of the western diamond rattlesnake, Crotalus atrox, in Texas (Viperidae) Southwest. Nat. 20: 503-15.
34. Gloyd HK, Conant R (1990) Snakes of the Agkistrodon Complex: A Monographic Review. Society for the Study of Amphibians and Reptiles. 614 pp.
35. Holder TL (1988) Movement and life history aspects of the pigmy rattlesnake in southwest Missouri. Unpublished M.S. thesis. Southwest Missouri State University.
36. Hamilton WJ, Pollack JA, (1955) The food of some crotalid snakes from Fort Benning, Georgia. Nat. Hist. Misc. 140: 1-4.
37. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO, (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463-1464.
38. Orme D (2012) The Caper package: comparative analysis of phylogenetics and evolution in R. Available: http://cran.r-project.org/web/packages/caper.
39. Felsenstein J, (1995) Phylogenies and the comparative method. Am. Nat. 125: 1-15.
40. Narum SR, (2006) Beyond Bonferroni: Less conservative analyses for conservation genetics. Conservation Genetics 7: 783-787.
41. Juárez P, Sanz L, Calvete JJ, (2004) Snake venomics: characterization of protein families in Sistrurus barbouri venom by cysteine mapping, N-terminal sequencing, and tandem mass spectrometry analysis. Proteomics 4: 327-38.
42. Lomonte B, Angulo Y, Sasa M, Gutiérrez JM, (2009) The phospholipase A2 homologues of snake venoms: biological activities and their possible adaptive roles. Protein Pept Lett. 16: 860-76.
43. Escalante T, Rucavado A, Fox JW, Gutiérrez JM, (2011) Key events in microvascular damage induced by snake venom hemorrhagic metalloproteinases. J. Proteomics 74: 1781-94.
44. Gutiérrez JM, Lomonte B, (1995) Phospholipase A2 myotoxins from Bothrops snake venoms. Toxicon 33: 1405-24.
45. Ferreira SH, Bartelt DC, Greene LJ, (1970) Isolation of bradykinin-potentiating peptides from Bothrops jararaca venom. Biochemistry 9: 2583-93.
46. Greene L-J, Camargo AC, Krieger EM, Stewart JM, Ferreira SH, (1972) Inhibition of the conversion of angiotensin I to II and potentiation of bradykinin by small peptides present in Bothrops jararaca venom. Circ. Res. 31(suppl 2): 62-71.
47. Luft FC, (2008) The Bothrops legacy: Vasoactive peptides from Brazil. Renin Rep. 10: 57-64.
48. Rodrigues RS, Boldrini-França J, Fonseca FP, de la Torre P, Henrique-Silva F, Sanz L, Calvete JJ, Rodrigues VM, (2012) Combined snake venomics and venom gland transcriptomic analysis of Bothropoides pauloensis. J. Proteomics 75: 2707-20.
49. Gibbs HL, Sanz L, Calvete JJ, (2009) Snake population venomics: proteomics-based analyses of individual variation reveals significant gene regulation effects on venom protein expression in Sistrurus rattlesnakes. J. Mol. Evol. 68: 113-25.
50. Gibbs HL, Rossiter W, (2008) Rapid evolution by positive selection and gene gain and loss: PLA2 venom genes in closely related Sistrurus rattlesnakes with divergent diets. J. Mol. Evol. 66: 151-66.
51. Ranganathan Y, Borges RM, (2011) To transform or not to transform: that is the dilemma in the statistical analysis of plant volatiles. Plant Signaling & Behaviour 6: 113-116.
52. Sunagar K, Johnson WE, O'Brien SJ, Vasconcelos V, Antunes A, (2012) Evolution of CRISPs associated with toxicoferan-reptilian venom and mammalian reproduction. Molecular Biology and Evolution 29: 1807-22.
53. Calvete JJ, (2011) Proteomic tools against the neglected pathology of snake bite envenoming. Expert Rev. Proteomics 8: 739-58.
54. Vidal N, Hedges SB, (2002) Higher-level relationships of snakes inferred from four nuclear and mitochondrial genes. C. R. Biologies 325: 977-85.
55. Pyron RA, Burbrink FT, Colli GR, de Oca AN, Vitt LJ, Kuczynski CA, Wiens JJ, (2011) The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Molecular Phylogenetics and Evolution 58: 329-42.
56. Casewell NR, Harrison RA, Wüster W, Wagstaff SC (2009) Comparative venom gland transcriptome surveys of the saw-scaled vipers (Viperidae: Echis) reveal substantial intra-family gene diversity and novel venom transcripts. BMC Genomics 10, 564.
57. Douglas ME, Douglas MR, Schuett Gw, Porra LW (2006) Evolution of rattlesnakes (Viperidae: Crotalus) in the warm deserts of western North America shaped by Neogen vicariance and Quaternary climate change. Molecular Ecology 15, 3353-3374.