期刊论文详细信息
Particle and Fibre Toxicology
Analysis of codon usage pattern in Taenia saginata based on a transcriptome dataset
Xuepeng Cai1  Xuenong Luo2  Xing Yang1 
[1] College of Veterinary Medicine, Jilin University, Changchun 130000, PR China;State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730046, PR China
关键词: Optimal codon;    Trancriptome;    Codon usage bias;    Taenia saginata;   
Others  :  1148913
DOI  :  10.1186/s13071-014-0527-1
 received in 2014-04-11, accepted in 2014-11-06,  发布年份 2014
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【 摘 要 】

Background

Codon usage bias is an important evolutionary feature in a genome and has been widely documented in many genomes. Analysis of codon usage bias has significance for mRNA translation, design of transgenes, new gene discovery, and studies of molecular biology and evolution, etc. However, the information about synonymous codon usage pattern of T. saginata genome remains unclear. T. saginata is a food-borne zoonotic cestode which infects approximataely 50 million humans worldwide, and causes significant health problems to the host and considerable socio-economic losses as a consequence. In this study, synonymous codon usage in T. saginata were examined.

Methods

Total RNA was isolated from T. saginata cysticerci and 91,487 unigenes were generated using Illumina sequencing technology. After filtering, the final sequence collection containing 11,399 CDSs was used for our analysis.

Results

Neutrality analysis showed that the T. saginata had a wide GC3 distribution and a significant correlation was observed between GC12 and GC3. NC-plot showed most of genes on or close to the expected curve, but only a few points with low-ENC values were below it, suggesting that mutational bias plays a major role in shaping codon usage. The Parity Rule 2 plot (PR2) analysis showed that GC and AT were not used proportionally. We also identified twenty-three optimal codons in the T. saginata genome, all of which were ended with a G or C residue. These results suggest that mutational and selection forces are probably driving factors of codon usage bias in T. saginata genome. Meanwhile, other factors such as protein length, gene expression, GC content of genes, the hydropathicity of each protein also influence codon usage.

Conclusions

Here, we systematically analyzed the codon usage pattern and identified factors shaping in codon usage bias in T. saginata. Currently, no complete nuclear genome is available for codon usage analysis at the genome level in T. saginata. This is the first report to investigate codon biology in T. sagninata. Such information does not only bring about a new perspective for understanding the mechanisms of biased usage of synonymous codons but also provide useful clues for molecular genetic engineering and evolutionary studies.

【 授权许可】

   
2014 Yang et al.; licensee BioMed Central.

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【 参考文献 】
  • [1]Akashi H, Eyre-Walker A: Translational selection and molecular evolution. Curr Opin Genet Dev 1998, 8(6):688-693.
  • [2]Akashi H: Gene expression and molecular evolution. Curr Opin Genet Dev 2001, 11(6):660-666.
  • [3]Duret L: Evolution of synonymous codon usage in metazoans. Curr Opin Genet Dev 2002, 12(6):640-649.
  • [4]Hershberg R, Petrov DA: Selection on codon bias. Annu Rev Genet 2008, 42:287-299.
  • [5]Kane JF: Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr Opin Biotechnol 1995, 6(5):494-500.
  • [6]Ahn I, Jeong B-J, Bae S-E, Jung J, Son HS: Genomic analysis of influenza A viruses, including avian flu (H5N1) strains. Eur J Epidemiol 2006, 21(7):511-519.
  • [7]Zheng Y, Zhao WM, Wang H, Zhou YB, Luan Y, Qi M, Cheng YZ, Tang W, Liu J, Yu H, Yu XP, Fan YZ, Yang X: Codon usage bias in Chlamydia trachomatis and the effect of codon modification in the MOMP gene on immune responses to vaccination. Biochem Cell Biol 2007, 85(2):218-226.
  • [8]Naya H, Romero H, Carels N, Zavala A, Musto H: Translational selection shapes codon usage in the GC-rich genome of Chlamydomonas reinhardtii. FEBS Lett 2001, 501(2):127-130.
  • [9]Gupta S, Bhattacharyya T, Ghosh TC: Synonymous codon usage in Lactococcus lactis: mutational bias versus translational selection. J Biomol Struct Dyn 2004, 21(4):527-535.
  • [10]Lin K, Kuang Y, Joseph JS, Kolatkar PR: Conserved codon composition of ribosomal protein coding genes in Escherichia coli, Mycobacterium tuberculosis and Saccharomyces cerevisiae: lessons from supervised machine learning in functional genomics. Nucleic Acids Res 2002, 30(11):2599-2607.
  • [11]Duret L, Mouchiroud D: Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci U S A 1999, 96(8):4482-4487.
  • [12]Kliman RM, Irving N, Santiago M: Selection conflicts, gene expression, and codon usage trends in yeast. J Mol Evol 2003, 57(1):98-109.
  • [13]Lafay B, Sharp PM: Synonymous codon usage variation among Giardia lamblia genes and isolates. Mol Biol Evol 1999, 16(11):1484-1495.
  • [14]Ghosh TC, Gupta SK, Majumdar S: Studies on codon usage in Entamoeba histolytica. Int J Parasitol 2000, 30(6):715-722.
  • [15]Wright F, Bibb MJ: Codon usage in the G + C-rich Streptomyces genome. Gene 1992, 113(1):55-65.
  • [16]McInerney JO: Replicational and transcriptional selection on codon usage in Borrelia burgdorferi. Proc Natl Acad Sci U S A 1998, 95(18):10698-10703.
  • [17]Sharp PM, Cowe E: Synonymous codon usage in Saccharomyces cerevisiae. Yeast 1991, 7(7):657-678.
  • [18]Stenico M, Lloyd AT, Sharp PM: Codon usage in Caenorhabditis elegans: delineation of translational selection and mutational biases. Nucleic Acids Res 1994, 22(13):2437-2446.
  • [19]Wanzala W, Onyango-Abuje JA, Kang'ethe EK, Zessin KH, Kyule NM, Baumann MP, Ochanda H, Harrison LJ: Control of Taenia saginata by post-mortem examination of carcasses. Afr Health Sci 2003, 3(2):68-76.
  • [20]Dorny P, Vercammen F, Brandt J, Vansteenkiste W, Berkvens D, Geerts S: Sero-epidemiological study of Taenia saginata cysticercosis in Belgian cattle. Vet Parasitol 2000, 88(1):43-49.
  • [21]Lightowlers MW, Rolfe R, Gauci CG: Taenia saginata: Vaccination against Cysticercosis in Cattle with Recombinant Oncosphere Antigens. Exp Parasitol 1996, 84(3):330-338.
  • [22]Matuchansky C, Lenormand Y: Images in clinical medicine. Taenia saginata N Engl J Med 1999, 341(23):1737.
  • [23]Lees W, Nightingale J, Brown D, Scandrett B, Gajadhar A: Outbreak of Cysticercus bovis (Taenia saginata) in feedlot cattle in Alberta. Can Vet J 2002, 43(3):227-228.
  • [24]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402.
  • [25]Journet EP, van Tuinen D, Gouzy J, Crespeau H, Carreau V, Farmer MJ, Niebel A, Schiex T, Jaillon O, Chatagnier O, Godiard L, Micheli F, Kahn D, Gianinazzi-Pearson V, Gamas P: Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Res 2002, 30(24):5579-5592.
  • [26]Fukunishi Y, Hayashizaki Y: Amino acid translation program for full-length cDNA sequences with frameshift errors. Physiol Genomics 2001, 5(2):81-87.
  • [27]Sharp PM, Li W-H: An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 1986, 24(1–2):28-38.
  • [28]Wright F: The 'effective number of codons' used in a gene. Gene 1990, 87(1):23-29.
  • [29]Sueoka N: Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci U S A 1988, 85(8):2653-2657.
  • [30]Sharp PM, Li W-H: The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 1987, 15(3):1281-1295.
  • [31]Wang H-C, Hickey DA: Rapid divergence of codon usage patterns within the rice genome. BMC Evol Biol 2007, 7(Suppl 1):S6. BioMed Central Full Text
  • [32]Liu Q, Feng Y, Zhao X, Dong H, Xue Q: Synonymous codon usage bias in Oryza sativa. Plant Sci 2004, 167(1):101-105.
  • [33]Liu Q: Analysis of codon usage pattern in the radioresistant bacterium Deinococcus radiodurans. Biosystems 2006, 85(2):99-106.
  • [34]Sharp PM, Cowe E, Higgins DG, Shields DC, Wolfe KH, Wright F: Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens; a review of the considerable within-species diversity. Nucleic Acids Res 1988, 16(17):8207-8211.
  • [35]Chen L, Liu T, Yang D, Nong X, Xie Y, Fu Y, Wu X, Huang X, Gu X, Wang S, Peng X, Yang G: Analysis of codon usage patterns in Taenia pisiformis through annotated transcriptome data. Biochem Biophys Res Commun 2013, 430(4):1344-1348.
  • [36]Kawabe A, Miyashita NT: Patterns of codon usage bias in three dicot and four monocot plant species. Genes Genet Syst 2003, 78(5):343-352.
  • [37]Sueoka N, Kawanishi Y: DNA G+ C content of the third codon position and codon usage biases of human genes. Gene 2000, 261(1):53-62.
  • [38]Nakamura Y, Gojobori T, Ikemura T: Codon usage tabulated from the international DNA sequence databases. Nucleic Acids Res 1997, 25(1):244-245.
  • [39]Bulmer M: Are codon usage patterns in unicellular organisms determined by selection‐mutation balance? J Evol Biol 1988, 1(1):15-26.
  • [40]Comeron JM, Kreitman M, Aguade M: Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics 1999, 151(1):239-249.
  • [41]Marais G, Mouchiroud D, Duret L: Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc Natl Acad Sci U S A 2001, 98(10):5688-5692.
  • [42]Hey J, Kliman RM: Interactions between natural selection, recombination and gene density in the genes of Drosophila. Genetics 2002, 160(2):595-608.
  • [43]Kliman RM, Hey J: Hill-Robertson interference in Drosophila melanogaster: reply to Marais, Mouchiroud and Duret. Genet Res 2003, 81(2):89-90.
  • [44]Hartl DL, Moriyama EN, Sawyer SA: Selection intensity for codon bias. Genetics 1994, 138(1):227-234.
  • [45]Chen Y, Carlini DB, Baines JF, Parsch J, Braverman JM, Tanda S, Stephan W: RNA secondary structure and compensatory evolution. Genes Genet Syst 1999, 74(6):271-286.
  • [46]Carlini DB, Chen Y, Stephan W: The relationship between third-codon position nucleotide content, codon bias, mRNA secondary structure and gene expression in the drosophilid alcohol dehydrogenase genes Adh and Adhr. Genetics 2001, 159(2):623-633.
  • [47]Oresic M, Dehn M, Korenblum D, Shalloway D: Tracing specific synonymous codon-secondary structure correlations through evolution. J Mol Evol 2003, 56(4):473-484.
  • [48]Vinogradov AE: Intron length and codon usage. J Mol Evol 2001, 52(1):2-5.
  • [49]Berg OG: Selection intensity for codon bias and the effective population size of Escherichia coli. Genetics 1996, 142(4):1379-1382.
  • [50]Prat Y, Fromer M, Linial N, Linial M: Codon usage is associated with the evolutionary age of genes in metazoan genomes. BMC Evol Biol 2009, 9:285. BioMed Central Full Text
  • [51]Goodarzi H, Torabi N, Najafabadi HS, Archetti M: Amino acid and codon usage profiles: adaptive changes in the frequency of amino acids and codons. Gene 2008, 407(1–2):30-41.
  • [52]Romero H, Zavala A, Musto H: Codon usage in Chlamydia trachomatis is the result of strand-specific mutational biases and a complex pattern of selective forces. Nucleic Acids Res 2000, 28(10):2084-2090.
  • [53]Rispe C, Delmotte F, van Ham RC, Moya A: Mutational and selective pressures on codon and amino acid usage in Buchnera, endosymbiotic bacteria of aphids. Genome Res 2004, 14(1):44-53.
  • [54]Hershberg R, Petrov DA: General rules for optimal codon choice. PLoS Genet 2009, 5(7):e1000556.
  • [55]Saul A, Battistutta D: Codon usage in Plasmodium falciparum. Mol Biochem Parasitol 1988, 27(1):35-42.
  • [56]Milhon JL, Tracy JW: Updated codon usage in Schistosoma. Exp Parasitol 1995, 80(2):353-356.
  • [57]Muto A, Yamao F, Osawa S: The genome of Mycoplasma capricolum. Prog Nucleic Acid Res Mol Biol 1987, 34:29-58.
  • [58]Ingvarsson PK: Gene expression and protein length influence codon usage and rates of sequence evolution in Populus tremula. Mol Biol Evol 2007, 24(3):836-844.
  • [59]Qiu S, Bergero R, Zeng K, Charlesworth D: Patterns of codon usage bias in Silene latifolia. Mol Biol Evol 2011, 28(1):771-780.
  • [60]Moriyama EN, Powell JR: Codon usage bias and tRNA abundance in Drosophila. J Mol Evol 1997, 45(5):514-523.
  • [61]Sharp PM, Li W-H: On the rate of DNA sequence evolution in Drosophila. J Mol Evol 1989, 28(5):398-402.
  • [62]Shields DC, Sharp PM, Higgins DG, Wright F: " Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol 1988, 5(6):704-716.
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