Early events in the evolution of spider silk genes

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Starrett, James ^a   Garb, Jessica E ^b   Kuelbs, Amanda ^a   Azubuike, Ugochi O ^a   Hayashi, Cheryl Y ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Massachusetts Lowell   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTHROPOD PROTEIN; COMPLEMENTARY DNA; EGG CASE PROTEIN; SPIDROIN; UNCLASSIFIED DRUG;

AMINO ACID COMPOSITION; ARTICLE; DNA SYNTHESIS; GENE DUPLICATION; GENETIC VARIABILITY; MESOTHELAE; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPISTHOTHELAE; PHYLOGENY; SILK; SPIDER;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; EVOLUTION, MOLECULAR; FIBROINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; REPETITIVE SEQUENCES, AMINO ACID; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPIDERS;

EID: 84862644865     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038084     Document Type: Article

References (80)

1. Platnick NI, (2011) The world spider catalog, version 12.0. American Museum of Natural History, Available:http://research.amnh.org/iz/spiders/catalog. DOI:10.5531/db.iz.0001. Accessed 2011, August 8.
2. Coddington JA, Levi HW, (1991) Systematics and Evolution of Spiders (Araneae). Annu. Rev. Ecol. Syst. 22: 565-592.
3. Coyle FA, (1986) The Role of Silk in Prey Capture by Nonaraneomorph Spiders. In: Shear WA (Ed) Spiders: webs, behavior, and evolution. Palo Alto, CA: Stanford Univ. Press. P. pp. 310-363.
4. Haupt J, (2003) The Mesothelae - a monograph of an exceptional group of spiders (Araneae: Mesothelae). Zoologica. 154: 1-102.
5. Shear WA, Palmer JM, Coddington JA, Bonamo PM, (1989) A Devonian Spinneret: Early Evidence of Spiders and Silk Use. Science. 246: 479-481.
6. Haupt J, Kovoor J, (1993) Silk-gland system and silk production in Mesothelae (Araneae). Ann. Sci. Nat. Zool.13e. ser. 14: 35-48.
7. Foelix RF, (1996) Biology of Spiders. 2nd Ed. Oxford: Oxford University Press.
8. Vollrath F, Selden P, (2007) The Role of Behavior in the Evolution of Spiders, Silks, and Webs. Annu. Rev. Ecol. Evol. S. 38: 819-846.
9. Ayoub NA, Garb JE, Hedin M, Hayashi CY, (2007) Utility of the nuclear protein-coding gene, elongation factor-1 gamma (Ef-1γ), for spider systematics, emphasizing family level relationships of tarantulas and their kin (Araneae: Mygalomorphae). Mol. Phylogenet. Evol. 42: 394-409.
10. Ayoub NA, Hayashi CY, (2009) Spiders (Araneae). In: Hedges SB, Kumar S (Eds), The Timetree of Life. Oxford: Oxford University Press. pp. 255-259.
11. Blackledge TA, Scharff N, Coddington JA, Szüts T, Wenzel JW, et al. (2009) Reconstructing web evolution and spider diversification in the molecular era. P. Natl. Acad. Sci. USA. 106 (13): 5229-5234.
12. Griffiths JR, Salantiri VR, (1980) The strength of spider silk. J. Mater. Sci. 15: 491-496.
13. Gosline JM, DeMont ME, Denny MW, (1986) The structure and properties of spider silk. Endeavor. 10(1): 37-43.
14. Blackledge TA, Hayashi CY, (2006) Silken toolkits: biomechanics of silk fibers spun by the orb web spider Argiope argentata (Fabricius 1775). J. Exp. Biol. 209: 2452-2461.
15. Agnarsson I, Kuntner M, Blackledge TA, (2010) Bioprospecting Finds the Toughest Biological Material: Extraordinary Silk for a Giant Riverine Orb spider. PloS ONE. 5(9): e11234.
16. Hinman MB, Lewis RV, (1992) Isolation of a Clone Encoding a Second Dragline Silk Fibroin. 1992. J. Biol. Chem. 267(27): 19320-19324.
17. Guerette PA, Ginzinger DG, Weber BH, Gosline JM, (1996) Silk properties determined by gland-specific expression of a spider fibroin gene family. Science. 272: 112-115.
18. Gatesy J, Hayashi CY, Motriuk D, Woods J, Lewis RV, (2001) Extreme Diversity, Conservation, and Convergence of Spider Silk Fibroin Sequences. Science. 291: 2603-2605.
19. Hayashi CY, Blackledge TA, Lewis RV, (2004) Molecular and Mechanical Characterization of Aciniform Silk: Uniformity of Iterated Sequence Modules in a Novel Member of the Spider Silk Fibroin Gene Family. Mol. Biol. Evol. 21(10): 1950-1959.
20. Garb JE, Hayashi CY, (2005) Modular evolution of egg case silk genes across orb-weaving spider superfamilies. P. Natl. Acad. Sci. USA. 102(32): 11379-11384.
21. Garb JE, DiMauro T, Lewis RV, Hayashi CY, (2007) Expansion and Intragenic Homogenization of Spider Silk Genes since the Triassic: Evidence from Mygalomorphae (Tarantulas and Their Kin) Spidroins. Mol. Biol. Evol. 24(11): 2454-2464.
22. Blasingame E, Tuton-Blasingame T, Larkin L, Falick AM, Zhao L, et al. (2009) Pyriform Spidroin 1, a Novel Member of the Silk Gene Family That Anchors Dragline Silk Fibers in Attachment Discs of the Black Widow Spider, Latrodectus hesperus. J. Biol. Chem. 284(42): 29097-29108.
23. Garb JE, Ayoub NA, Hayashi CY, (2010) Untangling spider silk evolution with spidroin terminal domains. BMC Evol. Biol. 10: 243.
24. Xu M, Lewis RV, (1990) Structure of a protein superfiber: Spider dragline silk. P. Natl. Acad. Sci. USA. 87: 7120-7124.
25. Hayashi CY, Lewis RV, (1998) Evidence from Flagelliform Silk cDNA for the Structural Basis of Elasticity and Modular Nature of Spider Silks. J. Mol. Biol. 275: 773-784.
26. Hayashi CY, Lewis RV, (2000) Molecular Architecture and Evolution of a Modular Spider Silk Protein Gene. Science. 287: 1477-1479.
27. Hu X, Lawrence B, Kohler K, Falick AM, Moore AMF, et al. (2005) Araneoid Egg Case Silk: A Fibroin with Novel Ensemble Repeat Units from the Black Widow Spider, Latrodectus hesperus. Biochemistry-US. 44: 10020-10027.
28. Ayoub NA, Garb JE, Tinghitella R, Collin MA, Hayashi CY, (2007) Blueprint for a High-Performance Biomaterial: Full-Length Spider Dragline Silk Genes. PLoS ONE. 6: e514.
29. Hu X, Vasanthavada K, Kohler K, McNary S, Moore AMF, et al. (2006) Molecular mechanisms of spider silk. Cell. Mol. Life Sci. 63: 1986-1999.
30. Hu X, Kohler K, Falick AM, Moore AMF, Jones PR, et al. (2005) Egg Case Protein-1. J. Biol. Chem. 280(22): 21220-21230.
31. Hu X, Kohler K, Falick AM, Moore AMF, Jones PR, et al. (2006) Spider Egg Case Core Fibers: Trimeric Complexes Assembled from TuSp1, ECP-1, and ECP-2. Biochemistry-US. 45: 3506-3516.
32. Glatz L, (1972) Der Spinnapparat haplogyner Spinnen (Arachnida, Araneae). Z. Morphol. Tiere. 72: 1-25.
33. Glatz L, (1973) Der Spinnapparat der Orthognatha (Arachnida, Araneae). Z. Morphol Tiere. 75: 1-50.
34. Palmer JM, Coyle FA, Harrison FW, (1982) Structure and cytochemistry of the silk glands of the mygalomorph spider Antrodiaetus unicolor (Araneae, Antrodiaetidae). J. Morphol. 174: 269-274.
35. Palmer JM, (1985) The silk and silk production of the funnel-web mygalomorph spider Euagrus (Araneae, Dipluridae). J. Morphol. 186: 195-207.
36. Kovoor J, (1987) Comparative structure and histochemistry of silk-producing organs in arachnids. In: Nentwig W (Ed) Ecophysiology of Arachnids. Berlin: Springer-Verlag. pp. 160-186.
37. Ubick D, Paquin P, Cushing PE, Roth V, eds. (2005) Spiders of North America: an identification manual. American Arachnological Society. 377 pages (Eds) (.
38. Shultz JW, (1987) The Origin of the Spinning Apparatus in Spiders. Biol. Rev. 62: 89-113.
39. Bittencourt D, Dittmar K, Lewis RV, Rech EL, (2010) A MaSp2-like gene found in the Amazon mygalomorph spider Avicularia juruensis. Comp. Biochem. Phys., B. 155: 419-426.
40. Prosdocimi F, Bittencourt D, da Silva FR, Kirst M, Motta PC, et al. (2011) Spinning Gland Transcriptomics from Two Main Clades of Spiders (Order: Araneae) - Insights on Their Molecular, Anatomical and Behavioral Evolution. PLoS ONE. 6(6): e21634.
41. Gorb SN, Niederegger S, Hayashi CY, Summers AP, Votsch W, et al. (2006) Silk-like secretion from tarantula feet. Nature. 443: 407.
42. Rind FC, Birkett CL, Duncan B-JA, Ranken AJ, (2011) Tarantulas cling to smooth vertical surfaces by secreting silk from their feet. J. Exp. Biol. 214: 1874-1879.
43. Peattie AM, Dirks J-H, Henriques S, Federle W, (2011) Arachnids Secrete a Fluid over Their Adhesive Pads. PLoS ONE. 6(5): e20485.
44. Pérez-Miles F, Panzera A, Ortiz-Villatoro D, Perdomo C, (2009) Silk production from tarantula feet questioned. Nature. 461: E9.
45. Foelix RF, Rast B, Peattie AM, (2012) Silk secretion from tarantula feet revisited: alleged spigots are probably chemoreceptors. J. Exp. Biol. 215: 1084-1089.
46. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
47. Shimodaira H, Hasegawa M, (1999) Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference. Mol. Biol. Evol. 16: 1114-1116.
48. Hedin M, Bond JE, (2006) Molecular phylogenetics of the spider infraorder Mygalomorphae using nuclear rRNA genes (18 S and 28 S): Conflict and agreement with the current system of classification. Mol. Phylogenet. Evol. 41: 454-471.
49. Newman AM, Cooper JB, (2007) XSTREAM: A practical algorithm for identification and architecture modeling of tandem repeats in protein sequences. BMC Bioinformatics. 8: 382.
50. Savage KN, Gosline JM, (2008) The role of proline in the elastic mechanism of hydrated spider silks. J. Exp. Biol. 211: 1948-1957.
51. Lee C, Blay S, Mooers AO, Singh A, Oakley TH, (2006) CoMET: A Mesquite package for comparing models of continuous character evolution on phylogenies. Evol. Bioinform. 2: 193-196.
52. Oakley TH, Gu Z, Abouheif E, Patel NH, Li W-H, (2005) Comparative Methods for the Analysis of Gene-Expression Evolution: An Example Using Yeast Functional Genomic Data. Mol. Biol. Evol. 22(1): 40-50.
53. Akaike H, (1973) Information theory as an extension of the maximum likelihood principle. 267-281 In: Petrov BN, Csaki F (Eds) Second International Symposium on Information theory. Akademiai Kiado, Budapest. Proceeding of the 2nd International Symposium on Information Theory, Supplement. Problems of control and information theory.
54. Platnick NI, Coddington J, Forster RR, Griswold CE, (1991) Spinneret Morphology and the Phylogeny of Haplogyne Spiders (Araneae, Araneomorphae). Am. Mus. Novit. 3016: 1-73.
55. Coddington JA, (1989) Spinneret Silk Spigot Morphology: Evidence for the Monophyly of Orbweaving Spiders, Cyrtophorinae (Araneidae), and the Group Theridiidae Plus Nesticidae. J. Arachnol. 17: 71-95.
56. Griswold CE, Coddington JA, Platnick NI, Foster RR, (1999) Towards a Phylogeny of Entelegyne Spiders (Araneae, Araneomorphae, Entelegynae). J. Arachnol. 27: 53-63.
57. Perry DJ, Bittencourt D, Siltberg-Liberles J, Rech EL, Lewis RV, (2010) Piriform Spider Silk Sequences Reveal Unique Repetitive Elements. Biomacromolecules. 11: 3000-3006.
58. Brooks AE, Stricker SM, Joshi SB, Kamerzell TJ, Middaugh CR, et al. (2008) Properties of Synthetic Spider Silk Fibers Based on Argiope aurantia MaSp2. Biomacromolecules. 9: 1506-1510.
59. An B, Hinman MB, Holland GP, Yarger JL, Lewis RV, (2011) Inducing β-Sheets Formation in Synthetic Spider Silk Fibers by Aqueous Post-Spin Stretching. Biomacromolecules. 12: 2375-2381.
60. Sutherland TD, Young JH, Weisman S, Hayashi CY, Merritt DJ, (2010) Insect Silk: One Name, Many Materials. Annu. Rev. Entomol. 55: 171-188.
61. Swanson BO, Blackledge TA, Summers AP, Hayashi CY, (2006) Spider Dragline Silk: Correlated and Mosaic Evolution in High-Performance Biological Materials. Evolution. 60(12): 2539-2551.
62. Boutry C, Blackledge TA, (2010) Evolution of supercontraction in spider silk: structure-function relationship from tarantulas to orb-weavers. J. Exp. Biol. 213: 3505-3514.
63. Swanson BO, Anderson SP, DiGiovine C, Ross RN, Dorsey JP, (2009) The evolution of complex biomaterial performance: The case of spider silk. Integr. Comp. Biol. 49(1): 21-31.
64. Beuken E, Vink C, Bruggeman C, (1998) One-step procedure for screening recombinant plasmids by size. BioTechniques. 24: 748-750.
65. Garb JE, Dimauro T, Vo V, Hayashi CY, (2006) Silk genes support the single origin of orb webs. Science. 312(5781): 1762.
66. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5): 1792-1797.
67. Nicholas KB, Nicholas Jr HB, (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by the author.
68. Suyama M, Torrents D, Bork P, (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34: W609-W612.
69. Simmons MP, Ochoterena H, (2000) Gaps as Characters in Sequence-Based Phylogenetic Analyses. Syst. Biol. 49(2): 369-381.
70. Miller MA, Pfeiffer W, Schwartz T, (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA 1-8.
71. Stamatakis A, (2006) Phylogenetic Models of Rate Heterogeneity: A High Performance Computing Perspective. In Proceedings of 20th IEEE/ACM International Parallel and Distributed Processing Symposium (IPDPS2006), High Performance Computational Biology Workshop, Rhodos, Greece.
72. Stamatakis A, (2006) RAxML-VI-HPC: Maximum Likelihood-based Phylogenetic Analyses with Thousands of Taxa and Mixed Models. Bioinformatics. 22(21): 2688-2690.
73. Stamatakis A, Hoover P, Rougemont J, (2008) A Rapid Bootstrap Algorithm for the RAxML Web Servers. Syst. Biol. 57(5): 758-771.
74. Huelsenbeck JP, Ronquist F, (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 17: 754-755.
75. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 19: 1572-1574.
76. Nylander JAA, (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
77. Ronquist F, Huelsenbeck JP, van der Mark P, (2005) mrbayes 3.1 manual, draft 5/26/2005, MrBayes website. Available:http://mrbayes.csit.fsu.edu/manual.php. Accessed 2010, October 14.
78. Coddington JA, Giribet G, Harvey MS, Prendini L, Walter DE, (2004) Arachnida. In: Cracraft J, Donoghue M (Eds) Assembling the Tree of Life. New York: Oxford University Press. P. pp. 296-318.
79. Page RDM, (1998) GeneTree: comparing genes and species phylogenies using reconciled trees. Bioinformatics. 14: 819-820.
80. Maddison WP, Maddison DR, (2010) Mesquite: a modular system for evolutionary analysis. Version 2.74. Mesquite website. Available:http://mesquiteproject.org. Accessed 2011, June 12.