Abstract
Using all currently predicted coding regions in the honeybee genome, a novel form of synonymous codon bias is presented that affects the usage of particular codons dependent on the surrounding nucleotides in the coding region. Nucleotides at the third codon site are correlated, dependent on their weak (adenine [A] or thyamine [T]) versus strong (guanine [G] or cytosine [C]) status, to nucleotides on the first codon site which are dependent on their purine (A/G) versus pyrimidine (C/T) status. In particular, for adjacent third and first site nucleotides, weak–pyrimidine and strong–purine nucleotide combinations occur much more frequently than the underabundant weak–purine and strong–pyrimidine nucleotide combinations. Since a similar effect is also found in the noncoding regions, but is present for all adjacent nucleotides, this coding effect is most likely due to a genome-wide context-dependent mutation error correcting mechanism in combination with selective constraints on adjacent first and second nucleotide pairs within codons. The position-dependent relationship of synonymous codon usage is evidence for a novel form of codon position bias which utilizes the redundancy in the genetic code to minimize the effect of nucleotide mutations within coding regions.









Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Akashi H, Eyre-Walker A (1998) Translational selection and molecular evolution. Curr Opin Genet Dev 8:688–693
Amdan GV, Omholt SW (2002) The regulatory anatomy of honeybee lifespan. J Theor Biol 216:209–228
Beye M, Hasselmann M, Fondrk MK, Page RE, Omholt SW (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114:419–429
Blake RD, Hess ST, Nicholson-Tuell J (1992) The influence of nearest neighbors on the rate and pattern of spontaneous point mutations. J Mol Evol 34:189–200
Berg OG, Silva PJN (1997) Codon bias in Escherichia coli:the influence of codon context on mutation and selection. Nucleic Acids Res 25(7):1397–1404
Bulmer M (1991) The selection-mutation-drift theory of synonymous codon usage. Genetics 129:897–907
Crick FHC (1966) Codon-anticodon pairing:the wobble hypothesis. J Mol Biol 19:548–555
Duret L (2000) tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes. Trends Genet 16:287–289
Evans JD (2004) Transcriptional immune responses by honey bee larvae during invasion by the bacterial pathogen, Paenibacillus larvae. J Invertebr Pathol 85:105–111
Evans JD, Gundersen-Rindal D (2003) Beenomes to Bombyx:future directions in applied insect genomics. Genome Biol 4:107
Francino MP, Chao L, Riley MA, Ochman H (1996) Asymetries generated by transcription-coupled repair in enterobacterial genes. Science 272:107–109
Fryxell KJ, Moon WJ (2005) CpG mutation rates in the human genome are highly dependent on local GC content. Mol Biol Evol 22(3):650–658
Fedorov A, Saxonov S, Gilbert W (2002) Regularities of context-dependent codon bias in eukaryotic genes. Nucleic Acids Res 30(5):1192–1197
Gouy M (1987) Condon contexts in Enterobacterial and Coliphage genes. Mol Biol Evol 4(4):426–444
Grantham R, Gautier C, Gouy M, Mercier R, Pave A (1980) Codon catalog usage and the genome hypothesis. Nucleic Acids Res 8:49–62
Gregory PG, Evans JD, Rinderer T, De Guzman L (2005) Conditional immune-gene suppression of honeybees parasitized by Varroa mites. J Insect Sci 5:1–5
Grosjean H, Fiers W (1982) Preferential codon usage in prokaryotic genes:the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed gene. Gene 18:199–209
Hambuch TM, Parsch J (2005) Patterns of synonymous codon usage in Drosophila melanogaster genes with sex-biased expression. Genetics 170:1691–1700
Hanai R, Wada A (1990) Doublet preference and gene evolution. J Mol Evol 30:109–115
Heisenberg M (2004) Mushroombody memoir: from maps to models. Nature 4:266–275
Honey bee genome sequencing consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931–949
Ikemura T (1981) Correlation between the abundances of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes:a proposal for a synonymous codon choice that is optimal for the E. coli translation system. J Mol Biol 151:573–597
Ikehara K, Omori Y, Arai R, Hirose A (2002) A novel theory on the origin of the genetic code: a GNC-SNS hypothesis. J Mol Evol 54:530–538
Macdónaill DA, Manktelow M (2004) Molecular informatics: quantifying information patterns in the genetic code. Mol Simul 30(5):267–272
Merkl R (2003) A survey of codon and amino acid frequency bias in microbial genomes focusing on translational efficiency. J Mol Evol 57:453–466
Morton BR (1998) Selection on the codon bias of chloroplast and cyanelle genes in different plant and algal lineage. J Mol Evol 46:449–459
Morton BR, So BG (2000) Codon usage in plastid gene is correlated with context, position within gene, and amino acid content. J Mol Evol 50(2):184–193
Munshaw S, Cutler RW, Wongsiri S, Chantawannakul P (2004) A Genomic-wide analysis of Apis mellifera: insights into diverse high copy number ORFs. J Apic Res 43(4):172–175
Page RE, Peng CYS (2001) Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Exp Geronotol 36:695–711
Petruska J, Goodman MF (1985) Influence of neighboring bases on DNA polymerase insertion and proofreading fidelity. J Biol Chem 260:7533–7539
Radman M (1998) DNA replication: one strand may be more equal. Proc Natl Acad Sci USA 95:9718–9719
Radman M, Wagner R (1986) Mismatch repair in Escherichia coli. Ann Rev Genet 20:523–538
Sancar A (1996) DNA excision repair. Annu Rev Biochem 65:43–81
Singer B, Hang B (2000) Nucleic acid sequence and repair: role of adduct, neighbor bases and enzyme specificity. Carcinogenesis 21(6):1071–1078
Sueoka N, Kawanishi Y (2000) DNA G+C content of the third codon position and codon usage biases of human gene. Gene 261:53–62
Watson JD, Crick FH (1953) Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid. Nature 171:737–738
Whitfield CW, Cziko AM, Robinson GE (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science 302:296–299
Wolfe KH, Sharp PM, Li W-H (1989) Mutation rates differ among regions of the mammalian genome. Nature 337:283–285
Acknowledgments
This research was conducted using funding from a Bard College Research and Travel Grant and the Thailand Research Fund (RMU4980010).We would also like to thank Walker Pett for his efforts in developing PERL routines and Dr. Wanchai Sonthichai and all staff of Department of Biology, Faculty of Science, Chiang Mai University, for providing the facilities used to conduct this research.
Author information
Authors and Affiliations
Corresponding author
Additional information
[Reviewing Editor: Dr. Brian Morton]
Rights and permissions
About this article
Cite this article
Cutler, R.W., Chantawannakul, P. The Effect of Local Nucleotides on Synonymous Codon Usage in the Honeybee (Apis mellifera L.) Genome. J Mol Evol 64, 637–645 (2007). https://doi.org/10.1007/s00239-006-0198-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-006-0198-4


