期刊论文详细信息
BMC Evolutionary Biology
Intragenic homogenization and multiple copies of prey-wrapping silk genes in Argiope garden spiders
Cheryl Y Hayashi1  Kirmanj Atrushi1  Ryan Allen1  Nadia A Ayoub3  Jie Wei2  Yonghui Zhao1  R Crystal Chaw1 
[1] Department of Biology, University of California, 900 University Avenue, Riverside 92507, Riverside, CA, USA;Faculty of Life Science, Liaoning University, Province Shenyang, Liaoning 110036, China;Department of Biology, Washington and Lee University, 204 W. Washington St., Lexington, VA 24450, USA
关键词: Spider;    Spidroin;    Silk;    Multiple loci;    Intragenic homogenization;    Concerted evolution;    AcSp1;   
Others  :  857956
DOI  :  10.1186/1471-2148-14-31
 received in 2013-10-25, accepted in 2014-02-14,  发布年份 2014
PDF
【 摘 要 】

Background

Spider silks are spectacular examples of phenotypic diversity arising from adaptive molecular evolution. An individual spider can produce an array of specialized silks, with the majority of constituent silk proteins encoded by members of the spidroin gene family. Spidroins are dominated by tandem repeats flanked by short, non-repetitive N- and C-terminal coding regions. The remarkable mechanical properties of spider silks have been largely attributed to the repeat sequences. However, the molecular evolutionary processes acting on spidroin terminal and repetitive regions remain unclear due to a paucity of complete gene sequences and sampling of genetic variation among individuals. To better understand spider silk evolution, we characterize a complete aciniform spidroin gene from an Argiope orb-weaving spider and survey aciniform gene fragments from congeneric individuals.

Results

We present the complete aciniform spidroin (AcSp1) gene from the silver garden spider Argiope argentata (Aar_AcSp1), and document multiple AcSp1 loci in individual genomes of A. argentata and the congeneric A. trifasciata and A. aurantia. We find that Aar_AcSp1 repeats have >98% pairwise nucleotide identity. By comparing AcSp1 repeat amino acid sequences between Argiope species and with other genera, we identify regions of conservation over vast amounts of evolutionary time. Through a PCR survey of individual A. argentata, A. trifasciata, and A. aurantia genomes, we ascertain that AcSp1 repeats show limited variation between species whereas terminal regions are more divergent. We also find that average dN/dS across codons in the N-terminal, repetitive, and C-terminal encoding regions indicate purifying selection that is strongest in the N-terminal region.

Conclusions

Using the complete A. argentata AcSp1 gene and spidroin genetic variation between individuals, this study clarifies some of the molecular evolutionary processes underlying the spectacular mechanical attributes of aciniform silk. It is likely that intragenic concerted evolution and functional constraints on A. argentata AcSp1 repeats result in extreme repeat homogeneity. The maintenance of multiple AcSp1 encoding loci in Argiope genomes supports the hypothesis that Argiope spiders require rapid and efficient protein production to support their prolific use of aciniform silk for prey-wrapping and web-decorating. In addition, multiple gene copies may represent the early stages of spidroin diversification.

【 授权许可】

   
2014 Chaw et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20140723090127934.pdf 1064KB PDF download
125KB Image download
76KB Image download
43KB Image download
81KB Image download
【 图 表 】

【 参考文献 】
  • [1]Hayashi CY, Blackledge TA, Lewis RV: 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 2004, 21:1950-1959.
  • [2]Vasanthavada K, Hu X, Falick A, Mattina CL, Moore A, Jones P, Yee R, Reza R, Tuton T, Vierra C: Aciniform spidroin, a constituent of egg case sacs and wrapping silk fibers from the black widow spider Latrodectus hesperus. J Biol Chem 2007, 282:35088-35097.
  • [3]Griswold CE, Coddington JA, Hormiga G, Scharff N: Phylogeny of the orb-web building spiders (Araneae, Orbiculariae: Deinopoidea, Araneoidea). Zool J Linn Soc-Lond 1998, 123:1-99.
  • [4]Walter A, Elgar MA, Bliss P, Moritz RFA: Wrap attack activates web-decorating behavior in Argiope spiders. Behav Ecol 2008, 19:799-804.
  • [5]Walter A, Elgar MA: The evolution of novel animal signals: silk decorations as a model system. Biol Rev 2012, 87:686-700.
  • [6]Herberstein ME, Craig CL, Coddington JA, Elgar MA: The function significance of silk decorations of orb-web spiders: a critical review of the empirical evidence. Biol Rev Camb Philos Soc 2000, 75:649-669.
  • [7]Blackledge TA, Hayashi CY: Silken toolkits: biomechanics of silk fibers spun by the orb web spider Argiope argentata (Fabricius 1775). J Exp Biol 2006, 209:2452-2461.
  • [8]Hinman MB, Lewis RV: Isolation of a clone encoding a second dragline silk fibroin. Nephila clavipes dragline silk is a two-protein fiber. J Biol Chem 1992, 267:19320-19324.
  • [9]Gatesy J, Hayashi C, Motriuk D, Woods J, Lewis R: Extreme diversity, conservation, and convergence of spider silk fibroin sequences. Science 2001, 291:2603-2605.
  • [10]Garb JE, DiMauro T, Lewis RV, Hayashi CY: Expansion and intragenic homogenization of spider silk genes since the Triassic: evidence from Mygalomorphae (tarantulas and their kin) spidroins. Mol Biol Evol 2007, 24:2454-2464.
  • [11]Rising A, Hjälm G, Engström W, Johansson J: N-terminal nonrepetitive domain common to dragline, flagelliform, and cylindriform spider silk proteins. Biomacromolecules 2006, 7:3120-3124.
  • [12]Garb JE, Ayoub NA, Hayashi CY: Untangling spider silk evolution with spidroin terminal domains. BMC Evol Biol 2010, 10:243-259. BioMed Central Full Text
  • [13]Xu M, Lewis RV: Structure of a protein superfiber: spider dragline silk. Proc Natl Acad Sci U S A 1990, 87:7120-7124.
  • [14]Jenkins JE, Creager MS, Butler EB, Lewis RV, Yarger JL, Holland GP: Solid-state NMR evidence for elastin-like beta-turn structure in spider dragline silk. Chem Commun (Camb) 2010, 46:6714-6716.
  • [15]Xu L, Tremblay M-L, Orrell KE, Leclerc J, Meng Q, Liu X-Q, Rainey JK: Nanoparticle self-assembly by a highly stable recombinant spider wrapping silk protein subunit. FEBS Lett 2013, 587:3273-3280.
  • [16]Beckwitt R, Arcidiacono S: Sequence conservation in the C-terminal region of spider silk proteins (Spidroin) from Nephila clavipes (Tetragnathidae) and Araneus bicentenarius (Araneidae). J Biol Chem 1994, 269:6661-6663.
  • [17]Sponner A, Unger E, Grosse F, Weisshart K: Conserved C-termini of spidroins are secreted by the major ampullate glands and retained in the silk thread. Biomacromolecules 2004, 5:840-845.
  • [18]Hu X, Kohler K, Falick AM, Moore AMF, Jones PR, Vierra C: Spider egg case core fibers: trimeric complexes assembled from TuSp1, ECP-1, and ECP-2. Biochemistry 2006, 45:3506-3516.
  • [19]Ayoub NA, Garb JE, Kuelbs A, Hayashi CY: Ancient properties of spider silks revealed by the complete gene sequence of the prey-wrapping silk protein (AcSp1). Mol Biol Evol 2012, 30:589-601.
  • [20]Beckwitt R, Arcidiacono S, Stote R: Evolution of repetitive proteins: spider silks from Nephila clavipes (Tetragnathidae) and Araneus bicentenarius (Araneidae). Insect Biochem Mol Biol 1998, 28:121-130.
  • [21]Ganley ARD, Kobayashi T: Highly efficient concerted evolution in the ribosomal DNA repeats: Total rDNA repeat variation revealed by whole-genome shotgun sequence data. Genome Res 2007, 17:184-191.
  • [22]Swanson WJ, Vacquier VD: Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein. Science 1998, 281:710-712.
  • [23]Hayashi CY, Lewis RV: Molecular architecture and evolution of a modular spider silk protein gene. Science 2000, 287:1477-1479.
  • [24]Wang S, Huang W, Yang D: NMR structure note: repetitive domain of aciniform spidroin 1 from Nephila antipodiana. J Biomol NMR 2012, 54:415-420.
  • [25]Xu L, Tremblay ML, Meng Q, Liu XQ: 1H, 13C and 15N NMR assignments of the aciniform spidroin (AcSp1) repetitive domain of Argiope trifasciata wrapping silk. Biomol NMR Assigm 2012, 6:147-151.
  • [26]Hayashi CY, Lewis RV: Evidence from flagelliform silk cDNA for the structural basis of elasticity and modular nature of spider silks. J Mol Biol 1998, 275:773-784.
  • [27]Ayoub NA, Hayashi CY: Spiders (Araneae). In The Timetree of Life. Edited by Hedges SB, Kumar S. Oxford University Press; 2009:255-259.
  • [28]Tian M, Lewis RV: Molecular characterization and evolutionary study of spider Tubuliform (eggcase) silk protein. Biochemistry 2005, 44:8006-8012.
  • [29]McAllister BF, Werren JH: Evolution of tandemly repeated sequences: what happens at the end of an array? J Mol Evol 1999, 48:469-481.
  • [30]Hayashi CY, Lewis RV: Spider flagelliform silk: lessons in protein design, gene structure, and molecular evolution. Bioessays 2001, 23:750-756.
  • [31]Su YC, Chang YH, Smith D, Zhu MS, Kuntner M, Tso IM: Biogeography and speciation patterns of the golden orb spider genus Nephila (Araneae:Nephilidae) in Asia. Zool Sci 2011, 28(1):47-55.
  • [32]Elices M, Plaza GR, Arnedo MA, Perez-Riguerio J, Torres FG, Guinea GV: Mechanical behavior of silk during the evolution of orb-web spinning spiders. Biomacromolecules 2009, 10(7):1904-1910.
  • [33]Lefèvre T, Boudreault S, Cloutier C, Pézolet M: Diversity of molecular transformations involved in the formation of spider silks. J Mol Biol 2011, 405:238-253.
  • [34]Gosline JM, Guerette PA, Ortlepp CS, Savage KN: The mechanical design of spider silks: from fibroin sequence to mechanical function. J Exp Biol 1999, 202:3295-3303.
  • [35]Anisimova M, Nielsen R, Yang Z: Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 2002, 164:1229-1236.
  • [36]Ohno S: Evolution by Gene Duplication. New York: Springer-Verlag; 1970.
  • [37]Guehrs K-H, Schlott B, Grosse F, Weisshart K: Environmental conditions impinge on dragline silk protein composition. Insect Mol Biol 2008, 17:553-564.
  • [38]Blamires SJ, Wu C-L, Tso I-M: Variation in protein intake induces variation in spider silk expression. PLoS ONE 2012, 7:e31626.
  • [39]Tso IM: The effect of food and silk reserve manipulation on decoration-building of Argiope aetheroides. Behaviour 2004, 141(5):603-616.
  • [40]Craig CL, Wolf SG, Davis JLD, Hauber ME, Maas JL: Signal polymorphism in the web-decorating spider Argiope argentata is correlated with reduced survivorship and the presence of stingless bees, its primary prey. Evolution 2001, 55(5):986-993.
  • [41]Condon C, Liveris D, Squires C, Schwartz I, Squires CL: rRNA operon multiplicity in Escherichia coli and the physiological implications of rrn inactivation. J Bacteriol 1995, 177:4152-4156.
  • [42]Stevenson BS, Schmidt TM: Life history implications of rRNA gene copy number in Escherichia coli. Appl Environ Microb 2004, 70:6670-6677.
  • [43]Guerette PA, Ginzinger DG, Weber BH, Gosline JM: Silk properties determined by gland-specific expression of a spider fibroin gene family. Science 1996, 272:112-115.
  • [44]Colgin MA, Lewis RV: Spider minor ampullate silk proteins contain new repetitive sequences and highly conserved non-silk-like “spacer regions”. Protein Sci 1998, 7:667-672.
  • [45]Garb JE, DiMauro T, Vo V, Hayashi CY: Silk genes support the single origin of orb webs. Science 2006, 312:1762.
  • [46]Higgins LE, White S, Nuñez-Farfán J, Vargas J: Patterns of variation among distinct alleles of the Flag silk gene from Nephila clavipes. Int J Biol Macromol 2007, 40:201-216.
  • [47]Ayoub NA, Hayashi CY: Multiple recombining loci encode MaSp1, the primary constituent of dragline silk, in widow spiders (Latrodectus: Theridiidae). Mol Biol Evol 2008, 25:277-286.
  • [48]Gaines WA IV, Marcotte WR Jr: Identification and characterization of multiple Spidroin 1 genes encoding major ampullate silk proteins in Nephila clavipes. Insect Mol Biol 2008, 17:465-474.
  • [49]Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680.
  • [50]Stamatakis A: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
  • [51]Stamatakis A, Hoover P, Rougemont J: A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 2008, 57:758-771.
  • [52]Miller MA, Pfeiffer W, Schwartz T: The CIPRES science gateway. In Proceedings of the Gateway Computing Environments Workshop (GCE). New Orleans, LA: ACM Press; 2010:1-8.
  • [53]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739.
  • [54]Delport W, Scheffler K, Botha G, Gravenor MB, Muse SV, Pond SLK: CodonTest: modeling amino acid substitution preferences in coding sequences. PLoS Comput Biol 2010, 6(8):e1000885.
  • [55]Pond SLK, Frost SD: Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 2005, 21(10):2531-2533.
  • [56]Delport W, Poon AF, Frost SD, Pond SLK: Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 2010, 26(19):2455-2457.
  • [57]Felsenstein J: Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981, 17:368-376.
  文献评价指标  
  下载次数:29次 浏览次数:5次