Molecular Biology Reports

, 37:677 | Cite as

Analysis of synonymous codon usage in Zea mays

  • Hanmei Liu
  • Rui He
  • Huaiyu Zhang
  • Yubi Huang
  • Mengliang Tian
  • Junjie Zhang


It is important and meaningful to understand the codon usage pattern and the factors that shape codon usage of maize. In this study, trends in synonymous codon usage in maize have been firstly examined through the multivariate statistical analysis on 7402 cDNA sequences. The results showed that the genes positions on the primary axis were strongly negatively correlated with GC3s, GC content of individual gene and gene expression level assessed by the codon adaptation index (CAI) values, which indicated that nucleotide composition and gene expression level were the main factors in shaping the codon usage of maize, and the variation in codon usage among genes may be due to mutational bias at the DNA level and natural selection acting at the level of mRNA translation. At the same time, CDS length and the hydrophobicity of each protein were, respectively, significantly correlated with the genes locations on the primary axis, GC3s and CAI values. We infer that genes length and the hydrophobicity of the encoded protein may play minor role in shaping codon usage bias. Additional 28 codons ending with a G or C base have been defined as “optimal codons”, which may provide useful information for maize gene-transformation and gene prediction.


Maize Codon usage bias Correspondence analysis Optimal codons 



This work was supported by the National Key Project of Scientific and Technical Supporting Programs Funded by Ministry of Science & Technology of China in the Eleventh Five-year Plan Period (NO.2006BAD01A03), and the key project of Education Bureau of Sichuan Province, China (NO.2006A018).


  1. 1.
    Powell JR, Moriyama EN (1997) Evolution of codon usage bias in Drosophila. Proc Natl Acad Sci USA 94(15):7784–7790. doi:10.1073/pnas.94.15.7784 CrossRefPubMedGoogle Scholar
  2. 2.
    Zheng Y, Zhao WM, Wang H et al (2007) Codon usage bias in Chlamydia trachomatis and the effect of codon modification in the MOMP gene on immune responses to vaccination. Biochem Cell Biol 85(2):218–226. doi:10.1139/O06-211 CrossRefPubMedGoogle Scholar
  3. 3.
    Rogic S, Mackworth AK, Ouellette FB (2001) Evaluation of gene-finding programs on mammalian sequences. Genome Res 11(5):817–832. doi:10.1101/gr.147901 CrossRefPubMedGoogle Scholar
  4. 4.
    Salamov AA, Solovyev VV (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res 10(4):516–522. doi:10.1101/gr.10.4.516 CrossRefPubMedGoogle Scholar
  5. 5.
    Lin K, Kuang Y, Joseph JS, Kolatkar PR (2002) 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 30(11):2599–2607. doi:10.1093/nar/30.11.2599 CrossRefPubMedGoogle Scholar
  6. 6.
    Sharp PM, Stenico M, Peden JF et al (1993) Codon usage: mutational bias, translational selection, or both? Biochem Soc Trans 21(4):835–841PubMedGoogle Scholar
  7. 7.
    Shields DC, Sharp PM (1987) Synonymous codon usage in Bacillus subtilis reflects both translational selection and mutational biases. Nucleic Acids Res 15(19):8023–8040. doi:10.1093/nar/15.19.8023 CrossRefPubMedGoogle Scholar
  8. 8.
    Sharp PM, Li WH (1986) An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24(1–2):28–38. doi:10.1007/BF02099948 CrossRefPubMedGoogle Scholar
  9. 9.
    Shields DC, Sharp PM, Higgins DG et al (1988) “Silent” sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol 5(6):704–716PubMedGoogle Scholar
  10. 10.
    Stenico M, Lloyd AT, Sharp PM (1994) Codon usage in Caenorhabditis elegans: delineation of translational selection and mutational biases. Nucleic Acids Res 22(13):2437–2446. doi:10.1093/nar/22.13.2437 CrossRefPubMedGoogle Scholar
  11. 11.
    Eyre-Walker AC (1991) An analysis of codon usage in mammals: selection or mutation bias? J Mol Evol 33(5):442–449. doi:10.1007/BF02103136 CrossRefPubMedGoogle Scholar
  12. 12.
    Chiapello H, Lisacek F, Caboche M et al (1998) Codon usage and gene function are related in sequences of Arabidopsis thaliana. Gene 209(1–2):GC1–GC38. doi:10.1016/S0378-1119(97)00671-9 CrossRefPubMedGoogle Scholar
  13. 13.
    Morton BR, Wright SI (2007) Selective constraints on codon usage of nuclear genes from Arabidopsis thaliana. Mol Biol Evol 24(1):122–129. doi:10.1093/molbev/msl139 CrossRefPubMedGoogle Scholar
  14. 14.
    Mukhopadhyay P, Basak S, Ghosh TC (2007) Nature of selective constraints on synonymous codon usage of rice differs in GC-poor and GC-rich genes. Gene 400(1–2):71–81. doi:10.1016/j.gene.2007.05.027 CrossRefPubMedGoogle Scholar
  15. 15.
    Wang HC, Hickey DA (2007) Rapid divergence of codon usage patterns within the rice genome. BMC Evol Biol 7(Suppl 1):S6. doi:10.1186/1471-2148-7-S1-S6 CrossRefPubMedGoogle Scholar
  16. 16.
    Liu Q, Feng Y, Zhao X et al (2004) Synonymous codon usage bias in Oryza sativa. Plant Sci 167:101–105. doi:10.1016/j.plantsci.2004.03.003 CrossRefGoogle Scholar
  17. 17.
    Chan AP, Pertea G, Cheung F et al (2006) The TIGR maize database. Nucleic Acids Res 34(Database issue):D771–D776. doi:10.1093/nar/gkj072 CrossRefPubMedGoogle Scholar
  18. 18.
    Frank W (1990) The “effective number of codons” used in a gene. Gene 87(1):23–29. doi:10.1016/0378-1119(90)90491-9 CrossRefGoogle Scholar
  19. 19.
    Sharp PM, Li WH (1987) The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15(3):1281–1295. doi:10.1093/nar/15.3.1281 CrossRefPubMedGoogle Scholar
  20. 20.
    Liu Q (2006) Analysis of codon usage pattern in the radioresistant bacterium Deinococcus radiodurans. Biosystems 85(2):99–106. doi:10.1016/j.biosystems.2005.12.003 CrossRefPubMedGoogle Scholar
  21. 21.
    Carels N, Bernardi G (2000) Two classes of genes in plants. Genetics 154(4):1819–1825PubMedGoogle Scholar
  22. 22.
    Jiang P, Sun X, Lu Z (2007) Analysis of synonymous codon usage in Aeropyrum pernix K1 and other Crenarchaeota microorganisms. J Genet Genomics 34(3):275–284. doi:10.1016/S1673-8527(07)60029-0 CrossRefPubMedGoogle Scholar
  23. 23.
    Zhao S, Zhang Q, Chen Z et al (2007) The factors shaping synonymous codon usage in the genome of Burkholderia mallei. J Genet Genomics 34(4):362–372. doi:10.1016/S1673-8527(07)60039-3 CrossRefPubMedGoogle Scholar
  24. 24.
    Naya H, Romero H, Carels N et al (2001) Translational selection shapes codon usage in the GC-rich genomes of Chlamydomonas reinhardtii. FEBS Lett 501(2–3):127–130. doi:10.1016/S0014-5793(01)02644-8 CrossRefPubMedGoogle Scholar
  25. 25.
    Gupta SK, Bhattacharyya TK, Ghosh TC (2004) Synonymous codon usage in Lactococcus lactis: mutational bias versus translational selection. J Biomol Struct Dyn 21(4):527–536PubMedGoogle Scholar
  26. 26.
    Peixoto L, Zavala A, Romero H et al (2003) The strength of translational selection for codon usage varies in the three replicons of Sinorhizobium meliloti. Gene 320:109–116. doi:10.1016/S0378-1119(03)00815-1 CrossRefPubMedGoogle Scholar
  27. 27.
    Kawabe A, Miyashita NT (2003) Patterns of codon usage bias in three dicot and four monocot plant species. Genes Genet Syst 78(5):343–352. doi:10.1266/ggs.78.343 CrossRefPubMedGoogle Scholar
  28. 28.
    Guo X, Bao J, Fan L (2007) Evidence of selectively driven codon usage in rice: implications for GC content evolution of Gramineae genes. FEBS Lett 581(5):1015–1021. doi:10.1016/j.febslet.2007.01.088 CrossRefPubMedGoogle Scholar
  29. 29.
    Bulmer M (1988) Are codon usage patterns in unicellular organisms determined by selection-mutation balance? J Mol Biol 1:15–26Google Scholar
  30. 30.
    Bulmer M (1991) The selection-mutation-drift theory of synonymous codon usage. Genetics 129(3):897–907PubMedGoogle Scholar
  31. 31.
    Mitreva M, Wendl MC, Martin J et al (2006) Codon usage patterns in Nematoda: analysis based on over 25 million codons in thirty-two species. Genome Biol 7(8):R75. doi:10.1186/gb-2006-7-8-r75 CrossRefPubMedGoogle Scholar
  32. 32.
    Sueoka N, Kawanishi Y (2000) DNA G + C content of the third codon position and codon usage biases of human genes. Gene 261(1):53–62. doi:10.1016/S0378-1119(00)00480-7 CrossRefPubMedGoogle Scholar
  33. 33.
    Fennoy SL, Bailey-Serres J (1993) Synonymous codon usage in Zea mays L. nuclear genes is varied by levels of C and G-ending codons. Nucleic Acids Res 21(23):5294–5300. doi:10.1093/nar/21.23.5294 CrossRefPubMedGoogle Scholar
  34. 34.
    Moriyama EN, Powell JR (1998) Gene length and codon usage bias in Drosophila melanogaster, Saccharomyces cerevisiae and Escherichia coli. Nucleic Acids Res 26(13):3188–3193. doi:10.1093/nar/26.13.3188 CrossRefPubMedGoogle Scholar
  35. 35.
    Das S, Paul S, Dutta C (2006) Synonymous codon usage in adenoviruses: influence of mutation, selection and protein hydropathy. Virus Res 117(2):227–236. doi:10.1016/j.virusres.2005.10.007 CrossRefPubMedGoogle Scholar
  36. 36.
    Duret L, Mouchiroud D (1999) Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci USA 96(8):4482–4487. doi:10.1073/pnas.96.8.4482 CrossRefPubMedGoogle Scholar
  37. 37.
    Karlin S, Mrázek J (1996) What drives codon choices in human genes? J Mol Biol 262(4):459–472. doi:10.1006/jmbi.1996.0528 CrossRefPubMedGoogle Scholar
  38. 38.
    Wang L, Roossinck MJ (2006) Comparative analysis of expressed sequences reveals a conserved pattern of optimal codon usage in plants. Plant Mol Biol 61(4–5):699–710. doi:10.1007/s11103-006-0041-8 CrossRefPubMedGoogle Scholar
  39. 39.
    Frelin L, Ahlén G, Alheim M et al (2004) Codon optimization and mRNA amplification effectively enhances the immunogenicity of the hepatitis C virus nonstructural 3/4A gene. Gene Ther 11(6):522–533. doi:10.1038/ CrossRefPubMedGoogle Scholar
  40. 40.
    Ko HJ, Ko SY, Kim YJ et al (2005) Optimization of codon usage enhances the immunogenicity of a DNA vaccine encoding mycobacterial antigen Ag85B. Infect Immun 73(9):5666–5674. doi:10.1128/IAI.73.9.5666-5674.2005 CrossRefPubMedGoogle Scholar
  41. 41.
    Peng RH, Yao QH, Xiong AS et al (2006) Codon-modifications and an endoplasmic reticulum-targeting sequence additively enhance expression of an Aspergillus phytase gene in transgenic canola. Plant Cell Rep 25(2):124–132. doi:10.1007/s00299-005-0036-y CrossRefPubMedGoogle Scholar
  42. 42.
    Rouwendal GJ, Mendes O, Wolbert EJ et al (1997) Enhanced expression in tobacco of the gene encoding green fluorescent protein by modification of its codon usage. Plant Mol Biol 33(6):989–999. doi:10.1023/A:1005740823703 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Hanmei Liu
    • 1
    • 2
  • Rui He
    • 2
  • Huaiyu Zhang
    • 2
  • Yubi Huang
    • 1
  • Mengliang Tian
    • 1
  • Junjie Zhang
    • 2
  1. 1.Maize Research InstituteSichuan Agricultural UniversityYaanPeople’s Republic of China
  2. 2.College of Life SciencesSichuan Agricultural UniversityYaanPeople’s Republic of China

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