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Synonymous Codon Usage, GC3, and Evolutionary Patterns Across Plastomes of Three Pooid Model Species: Emerging Grass Genome Models for Monocots

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Abstract

We have analyzed factors affecting the codon usage pattern of the chloroplasts genomes of representative species of pooid grass family. Correspondence analysis of relative synonymous codon usages (RSCU) showed that genes on secondary axis were correlated with their GC3S values (all r > 0.3, p < 0.05), indicating mutational bias as an important selective force that shaped the variation in the codon usage among chloroplast genes. The Nc-plot showed that although a majority of the points with low-Nc values were lying below the expected curve, a few genes lied on the expected curve. Nc plot clearly showed that mutational bias plays a major role in codon biology across the monocot plastomes. The hydrophobicity and aromaticity of encoded proteins of each species were found to be other factors of codon usage variation. In the view of above light, besides natural selection, several other factors also likely to be involved in determining the selective constraints on codon bias in plastomes of pooid grass genomes. In addition, five codons (B. distachyon), seven codons (H. vulgare), and four codons (T. aestivum) were identified as optimal codons of the three grass chloroplasts. To identify genes evolving under positive selection, rates of nonsynonymous substitutions (Ka) and synonymous substitutions (Ks) were computed for all groups of orthologous gene pairs.

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References

  1. Sau, K., & Deb, A. (2008). Temperature influences synonymous codon and amino acid usage biases in the phages infecting extremely thermophilic prokaryotes. In Silico Biology, 9, 0001.

    Google Scholar 

  2. Guo, F., & Yuan, J. (2009). Codon usages of genes on chromosome, and surprisingly, genes in plasmid are primarily affected by strand-specific mutational biases in Lawsonia intracellularis. DNA Research, 16, 91–104.

    Article  CAS  Google Scholar 

  3. Liu, Q. P., & Xue, Q. Z. (2005). Comparative studies on codon usage pattern of chloroplasts and their host nuclear genes in four plant species. Journal of Genetics, 84, 55–62.

    Article  CAS  Google Scholar 

  4. Stenico, M., Lloyd, A. T., & Sharp, P. M. (1994). Codon usage in Caenorhabditis elegans: delineation of translational selection and mutational biases. Nucleic Acids Research, 22, 2437–2446.

    Article  CAS  Google Scholar 

  5. Karlin, S., & Mrazek, J. (1996). What drives codon choices in human genes? Journal of Molecular Biology, 262, 459–472.

    Article  CAS  Google Scholar 

  6. Chiapello, H., Lisacek, F., Caboche, M., & Henaut, A. (1998). Codon usage and gene function are related in sequences of Arabidopsis thaliana. Gene, 209, GC1–GC38.

    Article  CAS  Google Scholar 

  7. Morton, B. R., & Wright, S. I. (2007). Selective constraints on codon usage of nuclear genes from Arabidopsis thaliana. Molecular Biology and Evolution, 24, 122–129.

    Article  CAS  Google Scholar 

  8. Wang, H. C., & Hickey, D. A. (2007). Rapid divergence of codon usage patterns within the rice genome. BMC Evolutionary Biology, 7(Suppl 1), S6.

    Article  Google Scholar 

  9. Tatarinova, T., Alexandrov, N., Bouck, J., & Feldman, K. (2010). GC3 biology in corn, rice, sorghum and other grasses. BMC Genomics, 11, 308.

    Article  Google Scholar 

  10. Douzery, E. J. P., Snell, E. A., Bapteste, E., Delsuc, F., & Philippe, H. (2004). The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? Proceedings of the National Academy of Sciences USA, 101, 15386–15391.

    Article  CAS  Google Scholar 

  11. Yoon, H. S., Hackett, J. D., Ciniglia, C., Pinto, G., & Bhattacharya, D. (2004). A molecular timeline for the origin of photosynthetic eukaryotes. Molecular Biology and Evolution, 21, 809–818.

    Article  CAS  Google Scholar 

  12. Waters, M. T., & Langdale, J. A. (2009). The making of a chloroplast. The EMBO Journal, 28, 2861–2873.

    Article  CAS  Google Scholar 

  13. Bendich, A. J. (2004). Circular chloroplast chromosomes: the grand illusion. The Plant Cell, 16, 1661–1666.

    Article  CAS  Google Scholar 

  14. Sugiura, M. (1992). The chloroplast genome. Plant Molecular Biology, 19, 149–168.

    Article  CAS  Google Scholar 

  15. Morton, B. R. (2003). The role of context-dependent mutations in generating compositional and codon usage bias in grass chloroplast DNA. Journal of Molecular Evolution, 56, 616–629.

    Article  CAS  Google Scholar 

  16. Morton, B. R. (1998). Selection on the codon bias of chloroplast and cyanelle genes in different plant and algal lineages. Journal of Molecular Evolution, 46, 449–459.

    Article  CAS  Google Scholar 

  17. Draper, J., Mur, L. A. J., Jenkins, G., Ghosh-Biswas, G. C., Bablak, P., Hasterok, R., et al. (2001). Brachypodium distachyon. A new model system for functional genomics in grasses. Plant Physiology, 127, 155–1539.

    Article  Google Scholar 

  18. Bortiri, E., Coleman-Derr, D., Lazo, G. R., Anderson, O. D., & Gu, Y. Q. (2008). The complete chloroplast genome sequence of Brachypodium distachyon: sequence comparison and phylogenetic analysis of eight grass plastomes. BMC Research Notes, 1, 61.

    Article  Google Scholar 

  19. The International Brachypodium Initiative. (2010). Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature, 463, 763–768.

    Article  Google Scholar 

  20. Zhang, W. J., Zhou, J., Li, Z. F., Wang, L., Gu, X., & Zhong, Y. (2007). Comparative analysis of codon usage patterns among mitochondrion, chloroplast and nuclear genes in Triticum aestivum L. Journal of Integrative Plant Biology, 149, 37–44.

    Google Scholar 

  21. Rosenberg, M. S., Subramanian, S., & Kumar, S. (2003). Patterns of transitional mutation biases within and among mammalian genomes. Molecular Biology and Evolution, 20, 988–993.

    Article  CAS  Google Scholar 

  22. Wright, F. (1990). The ‘effective number of codons’ used in a gene. Gene, 87, 23–29.

    Article  CAS  Google Scholar 

  23. Greenacre, M. J. (1984). Theory and application of correspondence analysis (p. 223). London: Academic Press.

    Google Scholar 

  24. Sharp, P. M., & Li, W. H. (1987). The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Research, 15, 1281–1295.

    Article  CAS  Google Scholar 

  25. Morton, B. R., & Levin, J. A. (1997). The atypical codon usage of the psbA gene may be the remnant of an ancestral bias. Proceedings of the National Academy of Sciences USA, 94, 11434–11438.

    Article  CAS  Google Scholar 

  26. Kyte, J., & Doolittle, R. (1982). A simple method for displaying the hydropathic character of a protein. Journal of Molecular Evolution, 157, 105–132.

    CAS  Google Scholar 

  27. McInerney, J. O. (1998). Replicational and transcriptional selection on codon usage in Borrelia burgdorferi. Proceedings of the National Academy of Sciences USA, 95, 10698–10703.

    Article  CAS  Google Scholar 

  28. Ikemura, T. (1985). Codon usage and tRNA content in unicellular and multicellular organisms. Molecular Biology and Evolution, 2, 13–34.

    CAS  Google Scholar 

  29. Polzin, K. M., Calvo, E. S., & Olsona, T. S. (1998). Identification of homoeologous regions in complex genomes using lambda genomic clones. Plant Science, 131, 161–171.

    Article  CAS  Google Scholar 

  30. Lyons, E., Pedersen, B., Kane, J., Alam, M., Ming, R., Tang, H., et al. (2008). Finding and comparing syntenic regions among arabidopsis and the outgroups papaya, poplar, and grape: CoGe with Rosids. Plant Physiology, 148(4), 1772–1781.

    Article  CAS  Google Scholar 

  31. Popendorf, K., Hachiya, T., Osana, Y., & Sakakibara, Y. (2010). Murasaki: a fast, parallelizable algorithm to find anchors from multiple genomes. PLoS ONE, 5(9), e12651.

    Article  Google Scholar 

  32. Pevzner, P. A., & Tesler, G. (2003). Genome rearrangements in mammalian evolution: lessons from human and mouse genomes. Genome Research, 13, 37–45.

    Article  CAS  Google Scholar 

  33. Bourque, G., Pevzner, P. A., & Tesler, G. (2004). Reconstructing the genomic architecture of ancestral mammals: lessons from human, mouse, and rat genomes. Genome Research, 14, 507–516.

    Article  CAS  Google Scholar 

  34. Sakakibara, Y., Osana, Y., & Popendorf, K. (2007). Development of a large-scale comparative genome system and its application to the analysis of mycobacteria genomes. Nihon Hansenbyo Gakkai Zasshi, 76, 251–256.

    Google Scholar 

  35. Hachiya, T., Osana, Y., Popendorf, K., & Sakakibara, Y. (2009). Accurate identification of orthologous segments among multiple genomes. Bioinformatics, 25, 853–860.

    Article  CAS  Google Scholar 

  36. Grigoriev, A. (1998). Analyzing genomes with cumulative skew diagrams. Nucleic Acids Research, 26, 2286–2290.

    Article  CAS  Google Scholar 

  37. Tatarinova, T., Brover, V., Troukhan, M., & Alexandrov, N. (2003). Skew in GC content near the transcription start site in Arabidopsis thaliana. Bioinformatics, 19(Suppl 1), i313–i314.

    Article  Google Scholar 

  38. Wan, X. F., Xu, D., Kleinhofs, A., & Zhou, J. (2004). Quantitative relationship between synonymous bias and GC composition across unicellular genomes. BMC Evolutionary Biology, 4, 19.

    Article  Google Scholar 

  39. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., et al. (2007). Clustal W and clustal X version 2.0. Bioinformatics, 23, 2947–2948.

    Article  CAS  Google Scholar 

  40. Sueoka, N. (1999). Translation-coupled violation of parity rule 2 in human genes is not the case of heterogeneity of the DNA G+C content of third codon position. Gene, 238, 53–58.

    Article  CAS  Google Scholar 

  41. Sharp, P. M., Cowe, E., Higgins, D. G., Shields, D. C., Wolfe, K. H., & Wright, F. (1988). Codon usage in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens; a review of the considerable within-species diversity. Nucleic Acids Research, 16, 8207–8711.

    Article  CAS  Google Scholar 

  42. Knight, R. D., Freeland, S. J., & Landweber, L. F. (2001). A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes. Genome Biology, 2, 0010.1–0010.13.

    Google Scholar 

  43. Coulondre, C., Miller, J. H., Farabaugh, P. J., & Gilbert, W. (1978). Molecular basis of base substitution hotspots in Escherichia coli. Nature, 274, 775–780.

    Article  CAS  Google Scholar 

  44. Hasegawa, M., Cao, Y., & Yang, Z. (1998). Preponderance of slightly deleterious polymorphism in mitochondrial DNA: nonsynonymous/synonymous rate ratio is much higher within species than between species. Molecular Biology and Evolution, 15, 1499–1505.

    CAS  Google Scholar 

  45. Sueoka, N. (1962). On the genetic basis of variation and heterogeneity of DNA base composition. Proceedings of the National Academy of Sciences USA, 48, 582–592.

    Article  CAS  Google Scholar 

  46. Morton, B. R. (1999). Strand asymmetry and codon usage bias in the chloroplast genome of Euglena gracilis. Proceedings of the National Academy of Sciences USA, 96, 5123–5128.

    Article  CAS  Google Scholar 

  47. Meng, Z., Wei, L., & Xia, L. (2008). Analysis of synonymous codon usage in chloroplast genome of Populus alba. Journal of Forestry Research, 19, 293–297.

    Article  Google Scholar 

  48. Pfitzinger, H., Guillemaut, P., Weil, J. H., & Pillay, D. T. N. (1987). Adjustment of the tRNA population to the codon usage of chloroplasts. Nucleic Acids Research, 15, 137.

    Article  Google Scholar 

  49. Shi, X. F., Huang, J. F., Liang, C. R., Liu, S. Q., Xie, J., & Liu, C. Q. (2001). Is there a close relationship between synonymous codon bias and codon-anticodon binding strength in human genes? Chinese Science Bulletin, 12, 1015–1019.

    Article  Google Scholar 

  50. Xia, X. (1998). How optimized is the translational machinery in Escherichia coli, Salmonella typhimurium and Saccharomyces cerevisiae? Genetics, 149, 37–44.

    CAS  Google Scholar 

  51. Lynn, D. J., Singer, G. A., & Hickey, D. A. (2002). Synonymous codon usage is subject to selection in thermophilic bacteria. Nucleic Acids Research, 30, 4272–4277.

    Article  CAS  Google Scholar 

  52. Wolfe, K. H., & Sharp, P. M. (1988). Identification of functional open reading frames in chloroplast genomes. Gene, 66, 215–222.

    Article  CAS  Google Scholar 

  53. Morton, B. R. (1993). Chloroplast DNA codon use: evidence for selection at the psbA locus based on tRNA availability. Journal of Molecular Evolution, 37, 273–280.

    Article  CAS  Google Scholar 

  54. Zhao, S., Zhang, Q., Chen, Z., et al. (2007). The factors shaping synonymous codon usage in the genome of Burkholderia mallei. Journal of Genetics and Genomics, 34, 362–372.

    Article  CAS  Google Scholar 

  55. Hausner, G., Olson, R., Simon, D., Johnson, I., Sanders, E. R., Karol, K. G., et al. (2006). Origin and evolution of the chloroplast trnK (matK) intron: a model for evolution of group II intron RNA structures. Molecular Biology and Evolution, 23, 380–391.

    Article  CAS  Google Scholar 

  56. Selvaraj, D., Sarma, R. K., & Sathishkumar, R. (2008). Phylogenetic analysis of chloroplast matK gene from Zingiberaceae for plant DNA barcoding. Bioinformation, 3, 24–27.

    Google Scholar 

  57. Wolfe, K. H., Morden, C. W., Ems, S. C., & Palmer, J. D. (1992). Rapid evolution of the plastid translational apparatus in a non-photosynthetic plant: loss of accelerated sequence evolution of tRNA and ribosomal protein genes. Journal of Molecular Evolution, 35, 304–317.

    Article  CAS  Google Scholar 

  58. Boudreau, E., Takahashi, Y., Lemieux, C., Turmel, M., & Rochaix, J. D. (1997). The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. The EMBO Journal, 16, 6095–6104.

    Article  CAS  Google Scholar 

  59. Magee, A. M., Aspinall, S., Rice, D. W., Cusack, B. P., Sémon, M., Perry, A. S., et al. (2010). Localized hypermutation and associated gene losses in legume chloroplast genomes. Genome Research, 20, 1700–1710.

    Article  CAS  Google Scholar 

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Acknowledgments

Gaurav Sablok thanks Key Lab of Horticultural Plant Biology (MOE), Huazhong Agricultural University. Tsuyoshi Hachiya and Yasubumi Sakakibara of Department of Biosciences and Informatics, Faculty of Science and Technology, Keio University, Japan are gratefully acknowledged for chrom-link visualization of the genomes. We gratefully acknowledge Professor Hans K. Stenoien, Systematics & Evolution Group, Norwegian University of Science and Technology, Norway for providing the peer review eye during the manuscript preparation. This work was supported by the Department of Biotechnology, Ministry of Science and Technology, Government of India. Research work of F. Vazquez is supported by an Ambizione Grant (PZ00P3_126329/1 to F.V.) of the Swiss National Science Foundation. Tatiana Tatarinova would like to thank the University of Glamorgan’s Research Investment Scheme for supporting this project.

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Correspondence to Gaurav Sablok or Tatiana V. Tatarinova.

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Sablok, G., Nayak, K.C., Vazquez, F. et al. Synonymous Codon Usage, GC3, and Evolutionary Patterns Across Plastomes of Three Pooid Model Species: Emerging Grass Genome Models for Monocots. Mol Biotechnol 49, 116–128 (2011). https://doi.org/10.1007/s12033-011-9383-9

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