Restriction and recruitment-gene duplication and the origin and evolution of snake venom toxins

Genome Biology and Evolution

Volumn 6, Issue 8, 2014, Pages 2088-2095

  Hargreaves, Adam D ^a   Swain, Martin T ^b   Hegarty, Matthew J ^b   Logan, Darren W ^c   Mulley, John F ^a  

^a BANGOR UNIVERSITY   (United Kingdom)

^b ABERYSTWYTH UNIVERSITY   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Evolution; Gene duplication; Neofunctionalization; Snake venom; Subfunctionalization

Indexed keywords

SNAKE VENOM; TRANSCRIPTOME;

ANIMAL; GENE DUPLICATION; GENETIC SELECTION; GENETICS; GENOME; MOLECULAR EVOLUTION; PHYLOGENY; REPTILE; SNAKE;

ANIMALS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENOME; PHYLOGENY; REPTILES; SELECTION, GENETIC; SNAKE VENOMS; SNAKES; TRANSCRIPTOME;

EID: 84907537182     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu166     Document Type: Article

References (76)

1. Andrews S. 2010. FastQC: A quality control tool for high throughput sequence data, Available from: http://www.bioinformatics.babraham.ac.uk/ projects/fastqc
2. Camacho C, et al. 2009. BLAST+: Architecture and applications. BMC Bioinformatics 10:421
3. Casewell NR, Huttley GA, Wüster W. 2012. Dynamic evolution of venom proteins in squamate reptiles. Nat Commun. 3:1066
4. Casewell NR, Wüster W, Vonk FJ, Harrison RA, Fry BG. 2013. Complex cocktails: The evolutionary novelty of venoms. Trends Ecol Evol. 28: 219-229
5. Castoe TA, et al. 2011. A multi-organ transcriptome resource for the Burmese python (Python molurus bivittatus). BMC Res Notes. 4:310
6. Castoe TA, et al. 2013. The Burmese python genome reveals the molecular basis for extreme adaptation in snakes. Proc Natl Acad Sci U S A. 110: 20645-20650
7. Cotton JA, Page RD. 2005. Rates and patterns of gene duplication and loss in the human genome. Proc Biol Sci. 272:277-283
8. Deng C, Cheng CH, Ye H, He X, Chen L. 2010. Evolution of an antifreeze protein by neofunctionalization under escape from adaptive conflict. Proc Natl Acad Sci U S A. 107:21593-21598
9. Di-Poi N, Montoya-Burgos JI, Duboule D. 2009. Atypical relaxation of structural constraints in Hox gene clusters of the green anole lizard. Genome Res. 19:602-610
10. Durban J, et al. 2011. Profiling the venom gland transcriptomes of Costa Rican snakes by 454 pyrosequencing. BMC Genomics 12:259
11. Escriva H, et al. 2006. Neofunctionalization in vertebrates: The example of retinoic acid receptors. PLOS Genet. 2:e102
12. Fahmi L, et al. 2012. Venomics and antivenomics profiles of North African Cerastes cerastes and C. vipera populations reveals a potentially important therapeutic weakness. J Proteomics. 75:2442-2453
13. Force A, et al. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545
14. Fox JW, Serrano SM. 2008. Exploring snake venom proteomes: multifaceted analyses for complex toxin mixtures. Proteomics 8:909-920
15. Fritzinger DC, Bredehorst R, Vogel CW. 1994. Molecular cloning and derived primary structure of cobra venom factor. Proc Natl Acad Sci U S A. 91:12775-12779
16. Fritzinger DC, Petrella EC, Connelly MB, Bredehorst R, Vogel CW. 1992. Primary structure of cobra complement component C3. J Immunol. 149:3554-3562
17. 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. 15:403-420
18. Fry BG, Casewell NR, et al. 2012. The structural and functional diversification of the Toxicofera reptile venom system. Toxicon 60:434-448
19. Fry BG, et al. 2006. Early evolution of the venom system in lizards and snakes. Nature 439:584-588
20. Fry BG, et al. 2008. Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Mol Cell Proteomics. 7:215-246
21. Fry BG, et al. 2013. Squeezers and leaf-cutters: differential diversification and degeneration of the venom system in Toxicoferan reptiles. Mol Cell Proteomics. 12:1881-1899
22. Fry BG, Roelants K, et al. 2009. The Toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet. 10:483-511
23. Fry BG, Scheib H, Junqueira de Azevedo ILM, Silva DA, Casewell NR. 2012. Novel transcripts in the maxillary venom glands of advanced snakes. Toxicon 59:696-708
24. Fry BG, Vidal N, Van der Weerd L, Kochva E, Renjifo C. 2009. Evolution and diversification of the Toxicofera reptile venom system. J Proteomics. 72:127-136
25. 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. 21:870-883
26. Grabherr MG, et al. 2011. Full-length transcriptome assembly from RNAseq data without a reference genome. Nat Biotechnol. 29:644-652
27. Han X, Kwong S, Ge R, Kolatkar P, Kini RM. 2013. Transcriptional regulation of trocarin D, a prothrombin activator from Tropidechis carinatus. FASEB J. 27:550; 6
28. Hayashi MA, Camargo A. 2005. The bradykinin-potentiating peptides from venom gland and brain of Bothrops jararaca contain highly site specific inhibitors of the somatic angiotensin-converting enzyme. Toxicon 45:1163-1170
29. HayashiMA, et al. 2003. The C-type natriuretic peptide precursor of snake brain contains highly specific inhibitors of the angiotensin-converting enzyme. J Neurochem. 85:969-977
30. Hurles M. 2004. Gene duplication: The genomic trade in spare parts. PLOS Biol. 2:e206
31. Ikeda N, et al. 2010. Unique structural characteristics and evolution of a cluster of venom phospholipase A2 isozyme genes of Protobothrops flavoviridis snake. Gene 461:15-25
32. Jiang Y, et al. 2011. Venom gland transcriptomes of two elapid snakes (Bungarus multicinctus and Naja atra) and evolution of toxin genes. BMC Genomics 12:1
33. Kini RM. 2002. Molecular moulds with multiple missions: functional sites in three-finger toxins. Clin Exp Pharmacol Physiol. 29:815-822
34. Kini RM. 2003. Excitement ahead: structure, function and mechanism of snake venom phospholipase A2 enzymes. Toxicon 42:827-840
35. Kini RM, Doley R. 2010. Structure, function and evolution of three-finger toxins: mini proteins with multiple targets. Toxicon 56:855-867
36. Koh D, Armugam A, Jeyaseelan K. 2004. Sputa nerve growth factor forms a preferable substitute to mouse 7S-beta nerve growth factor. Biochem J. 383:149-158
37. Kordiš D, Gubenšek F. 2000. Adaptive evolution of animal toxin multigene families. Gene 261:43-52
38. Kulkeaw K, Chaicumpa W, Sakolvaree Y, Tongtawe P, Tapchaisri P. 2007. Proteome and immunome of the venom of the Thai cobra, Naja kaouthia. Toxicon 49:1026-1041
39. Kwong S, Kini RM. 2011. Duplication of coagulation factor genes and evolution of snake venom prothrombin activators. In: Friedberg F, editor. Gene duplication. InTech. p. 257-278
40. Kwong S, Woods AE, Mirtschin PJ, Ge R, Kini RM. 2009. The recruitment of blood coagulation factor X into snake venom gland as a toxin: The role of promoter cis-elements in its expression. Thromb Haemost. 102(3):469-478
41. Lakatos I. 1980. The methodology of scientific research programmes: Volume 1: Philosophical papers. Cambridge: Cambridge University Press
42. Le TNM, Reza A, Swarup S, Kini RM. 2005. Gene duplication of coagulation factor V and origin of venom prothrombin activator in Pseudonaja textilis snake. Thromb Haemost. 93:420
43. Lipps BV. 2000. Isolation of nerve growth factor (NGF) from human body fluids; saliva, serum and urine: comparison between cobra venom and cobra serum NGF. J Nat Toxins. 9:349-356
44. Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290:1151-1155
45. Lynch M, Conery JS. 2003. The evolutionary demography of duplicate genes. J Struct Funct Genomics. 3:35-44
46. Lynch M, Force A. 2000. The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459-473
47. Lynch VJ. 2007. Inventing an arsenal: Adaptive evolution and neofunctionalization of snake venom phospholipase A2 genes. BMC Evol Biol. 7:2
48. Mable B. 2004. "Why polyploidy is rarer in animals than in plants": myths and mechanisms. Biol J Linn Soc. 82:453-466
49. Margres MJ, Aronow K, Loyacano J, Rokyta DR. 2013. The venom-gland transcriptome of the Eastern coral snake (Micrurus fulvius) reveals high venom complexity in the intragenomic evolution of venoms. BMC Genomics 14:1-18
50. Mighell A, Smith N, Robinson P, Markham A. 2000. Vertebrate pseudogenes. FEBS Lett. 468:109-114
51. Murayama N, et al. 1997. Cloning and sequence analysis of a Bothrops jararaca cDNA encoding a precursor of seven bradykinin-potentiating peptides and a C-type natriuretic peptide. Proc Natl Acad Sci U S A. 94: 1189-1193
52. Ohno S. 1970. Evolution by gene duplication. London: George Alien & Unwin Ltd
53. Otto SP, Whitton J. 2000. Polyploid incidence and evolution. Annu Rev Genet. 34:401-437
54. Popper KR. 1959. The logic of scientific discovery. New York: Routledge.
55. Presgraves DC. 2005. Evolutionary genomics: new genes for new jobs. Curr Biol. 15:R52-R53
56. Rádis-Baptista G, et al. 2003. Structure and chromosomal localization of the gene for crotamine, a toxin from the South American rattlesnake, Crotalus durissus terrificus. Toxicon 42:747-752.
57. Rádis-Baptista G, et al. 2004. Identification of crotasin, a crotamine-related gene of Crotalus durissus terrificus. Toxicon 43:751-759.
58. Reza M, Swarup S, Kini R. 2007. Structure of two genes encoding parallel prothrombin activators in Tropidechis carinatus snake: gene duplication and recruitment of factor X gene to the venom gland. J Thromb Haemost. 5:117-126
59. Kipling R. 1902. Just so stories. London: Macmillan and Co. Limited.
60. Schwartz TS, Bronikowski AM. 2013. Dissecting molecular stress networks: identifying nodes of divergence between life-history phenotypes. Mol Ecol. 22:739-756
61. Schwartz TS, et al. 2010. A garter snake transcriptome: pyrosequencing, de novo assembly, and sex-specific differences. BMC Genomics 11: 694
62. Shedlock AM, et al. 2007. Phylogenomics of nonavian reptiles and the structure of the ancestral amniote genome. Proc Natl Acad Sci U S A. 104:2767-2772
63. Stewart AJ, Hannenhalli S, Plotkin JB. 2012. Why transcription factor binding sites are ten nucleotides long. Genetics 192:973-985
64. Sunagar K, et al. 2013. Molecular evolution of vertebrate neurotrophins: co-option of the highly conserved nerve growth factor gene into the advanced snake venom arsenal. PLOS One 8:e81827
65. Sunagar K, Johnson WE, O'Brien SJ, Vasconcelos V, Antunes A. 2012. Evolution of CRISPs associated with Toxicoferan-reptilian venom and mammalian reproduction. Mol Biol Evol. 29:1807-1822
66. Tzika AC, Helaers R, Schramm G, Milinkovitch MC. 2011. Reptilian-transcriptome v1. 0, a glimpse in the brain transcriptome of five divergent Sauropsida lineages and the phylogenetic position of turtles. EvoDevo. 2:1-18
67. Van Damme EJ, et al. 2007. A novel family of lectins evolutionarily related to class V chitinases: An example of neofunctionalization in legumes. Plant Physiol. 144:662-672
68. Vidal N, Hedges SB. 2005. The phylogeny of squamate reptiles (lizards, snakes, and amphisbaenians) inferred from nine nuclear proteincoding genes. C R Biol. 328:1000-1008
69. Vonk FJ, et al. 2013. The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc Natl Acad Sci U S A. 110:20651-20656
70. Wagstaff SC, Laing GD, Theakston RDG, Papaspyridis C, Harrison RA. 2006. Bioinformatics and multiepitope DNA immunization to design rational snake antivenom. PLOS Med 3:e184
71. Wagstaff SC, Sanz L, Juárez P, Harrison RA, Calvete JJ. 2009. Combined snake venomics and venom gland transcriptomic analysis of the ocellated carpet viper, Echis ocellatus. J Proteomics. 71:609-623
72. Wall CE, et al. 2011. Whole transcriptome analysis of the fasting and fed Burmese python heart: insights into extreme physiological cardiac adaptation. Physiol Genomics. 43:69-76
73. Warrell DA. 2010. Snake bite. Lancet 375:77-88
74. Wong ES, Belov K. 2012. Venom evolution through gene duplications. Gene 496:1-7
75. Wray GA, et al. 2003. The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol. 20:1377-1419
76. Zhang J. 2003. Evolution by gene duplication: An update. Trends Ecol Evol. 18:292-298