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Intragenic homogenization and multiple copies of prey-wrapping silk genes in Argiope garden spiders.
BMC Evol Biol 2014; 14:31BE

Abstract

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.

Authors+Show Affiliations

Department of Biology, University of California, 900 University Avenue, Riverside 92507, Riverside, CA, USA. rcrystal@ucr.edu.No 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, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

24552485

Citation

Chaw, R Crystal, et al. "Intragenic Homogenization and Multiple Copies of Prey-wrapping Silk Genes in Argiope Garden Spiders." BMC Evolutionary Biology, vol. 14, 2014, p. 31.
Chaw RC, Zhao Y, Wei J, et al. Intragenic homogenization and multiple copies of prey-wrapping silk genes in Argiope garden spiders. BMC Evol Biol. 2014;14:31.
Chaw, R. C., Zhao, Y., Wei, J., Ayoub, N. A., Allen, R., Atrushi, K., & Hayashi, C. Y. (2014). Intragenic homogenization and multiple copies of prey-wrapping silk genes in Argiope garden spiders. BMC Evolutionary Biology, 14, p. 31. doi:10.1186/1471-2148-14-31.
Chaw RC, et al. Intragenic Homogenization and Multiple Copies of Prey-wrapping Silk Genes in Argiope Garden Spiders. BMC Evol Biol. 2014 Feb 20;14:31. PubMed PMID: 24552485.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Intragenic homogenization and multiple copies of prey-wrapping silk genes in Argiope garden spiders. AU - Chaw,R Crystal, AU - Zhao,Yonghui, AU - Wei,Jie, AU - Ayoub,Nadia A, AU - Allen,Ryan, AU - Atrushi,Kirmanj, AU - Hayashi,Cheryl Y, Y1 - 2014/02/20/ PY - 2013/10/25/received PY - 2014/02/14/accepted PY - 2014/2/21/entrez PY - 2014/2/21/pubmed PY - 2014/5/17/medline SP - 31 EP - 31 JF - BMC evolutionary biology JO - BMC Evol. Biol. VL - 14 N2 - 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. SN - 1471-2148 UR - https://www.unboundmedicine.com/medline/citation/24552485/Intragenic_homogenization_and_multiple_copies_of_prey_wrapping_silk_genes_in_Argiope_garden_spiders_ L2 - https://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-14-31 DB - PRIME DP - Unbound Medicine ER -