Abstract
A multivariate statistical method called correspondence analysis was used to examine the codon usage of one-hundred-and-one nuclear genes of maize (Zea mays L.). Forty percent of the variation in codon usage was due to bias toward G or C-ending versus A or U-ending codons. Differences in levels of G-ending codons showed the weakest correlation with the major codon usage bias. The bias toward C or U versus A or G in the silent third nucleotide position of synonymous codons accounted for approximately 10% of the variation in codon usage. The G+C content of the silent third nucleotide position of coding regions was not strongly correlated with G+C content of introns. Codon usage was strongly biased toward codons ending in G or C for a number of highly expressed genes including most light-regulated chloroplast proteins, ABA-induced proteins, histones, and anthocyanin biosynthetic enzymes. Codon usage of genes encoding storage proteins and regulatory proteins, such as transposases, kinases, phosphatases and transcription factors, was more random than that of genes encoding cytosolic enzymes with similar bias toward G or C-ending codons. Codon usage in maize may reflect both regional bias on nucleotide composition and selection on the silent third nucleotide position.
Full text
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Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Andersson S. G., Kurland C. G. Codon preferences in free-living microorganisms. Microbiol Rev. 1990 Jun;54(2):198–210. doi: 10.1128/mr.54.2.198-210.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Antequera F., Bird A. P. Unmethylated CpG islands associated with genes in higher plant DNA. EMBO J. 1988 Aug;7(8):2295–2299. doi: 10.1002/j.1460-2075.1988.tb03072.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bennetzen J. L., Hall B. D. Codon selection in yeast. J Biol Chem. 1982 Mar 25;257(6):3026–3031. [PubMed] [Google Scholar]
- Bernardi G., Bernardi G. Compositional constraints and genome evolution. J Mol Evol. 1986;24(1-2):1–11. doi: 10.1007/BF02099946. [DOI] [PubMed] [Google Scholar]
- Boyer S. K., Shotwell M. A., Larkins B. A. Evidence for the translational control of storage protein gene expression in oat seeds. J Biol Chem. 1992 Aug 25;267(24):17449–17457. [PubMed] [Google Scholar]
- Brinkmann H., Martinez P., Quigley F., Martin W., Cerff R. Endosymbiotic origin and codon bias of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize. J Mol Evol. 1987;26(4):320–328. doi: 10.1007/BF02101150. [DOI] [PubMed] [Google Scholar]
- Bulmer M. The effect of context on synonymous codon usage in genes with low codon usage bias. Nucleic Acids Res. 1990 May 25;18(10):2869–2873. doi: 10.1093/nar/18.10.2869. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bulmer M. The selection-mutation-drift theory of synonymous codon usage. Genetics. 1991 Nov;129(3):897–907. doi: 10.1093/genetics/129.3.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Campbell W. H., Gowri G. Codon usage in higher plants, green algae, and cyanobacteria. Plant Physiol. 1990 Jan;92(1):1–11. doi: 10.1104/pp.92.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goodall G. J., Filipowicz W. Different effects of intron nucleotide composition and secondary structure on pre-mRNA splicing in monocot and dicot plants. EMBO J. 1991 Sep;10(9):2635–2644. doi: 10.1002/j.1460-2075.1991.tb07806.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gouy M., Gautier C. Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res. 1982 Nov 25;10(22):7055–7074. doi: 10.1093/nar/10.22.7055. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grantham R., Gautier C., Gouy M. Codon frequencies in 119 individual genes confirm consistent choices of degenerate bases according to genome type. Nucleic Acids Res. 1980 May 10;8(9):1893–1912. doi: 10.1093/nar/8.9.1893. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol. 1985 Jan;2(1):13–34. doi: 10.1093/oxfordjournals.molbev.a040335. [DOI] [PubMed] [Google Scholar]
- Ikemura T. Correlation between the abundance 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 translational system. J Mol Biol. 1981 Sep 25;151(3):389–409. doi: 10.1016/0022-2836(81)90003-6. [DOI] [PubMed] [Google Scholar]
- Kinnaird J. H., Burns P. A., Fincham J. R. An apparent rare-codon effect on the rate of translation of a Neurospora gene. J Mol Biol. 1991 Oct 5;221(3):733–736. doi: 10.1016/0022-2836(91)80167-s. [DOI] [PubMed] [Google Scholar]
- Kotula L., Curtis P. J. Evaluation of foreign gene codon optimization in yeast: expression of a mouse IG kappa chain. Biotechnology (N Y) 1991 Dec;9(12):1386–1389. doi: 10.1038/nbt1291-1386. [DOI] [PubMed] [Google Scholar]
- Kurland C. G. Codon bias and gene expression. FEBS Lett. 1991 Jul 22;285(2):165–169. doi: 10.1016/0014-5793(91)80797-7. [DOI] [PubMed] [Google Scholar]
- Lawrence J. G., Hartl D. L. Unusual codon bias occurring within insertion sequences in Escherichia coli. Genetica. 1991;84(1):23–29. doi: 10.1007/BF00123981. [DOI] [PubMed] [Google Scholar]
- Lloyd A. T., Sharp P. M. Codon usage in Aspergillus nidulans. Mol Gen Genet. 1991 Nov;230(1-2):288–294. doi: 10.1007/BF00290679. [DOI] [PubMed] [Google Scholar]
- Makoff A. J., Oxer M. D., Romanos M. A., Fairweather N. F., Ballantine S. Expression of tetanus toxin fragment C in E. coli: high level expression by removing rare codons. Nucleic Acids Res. 1989 Dec 25;17(24):10191–10202. doi: 10.1093/nar/17.24.10191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martinez P., Martin W., Cerff R. Structure, evolution and anaerobic regulation of a nuclear gene encoding cytosolic glyceraldehyde-3-phosphate dehydrogenase from maize. J Mol Biol. 1989 Aug 20;208(4):551–565. doi: 10.1016/0022-2836(89)90147-2. [DOI] [PubMed] [Google Scholar]
- Matassi G., Montero L. M., Salinas J., Bernardi G. The isochore organization and the compositional distribution of homologous coding sequences in the nuclear genome of plants. Nucleic Acids Res. 1989 Jul 11;17(13):5273–5290. doi: 10.1093/nar/17.13.5273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Montero L. M., Salinas J., Matassi G., Bernardi G. Gene distribution and isochore organization in the nuclear genome of plants. Nucleic Acids Res. 1990 Apr 11;18(7):1859–1867. doi: 10.1093/nar/18.7.1859. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Murray E. E., Lotzer J., Eberle M. Codon usage in plant genes. Nucleic Acids Res. 1989 Jan 25;17(2):477–498. doi: 10.1093/nar/17.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohama T., Muto A., Osawa S. Role of GC-biased mutation pressure on synonymous codon choice in Micrococcus luteus, a bacterium with a high genomic GC-content. Nucleic Acids Res. 1990 Mar 25;18(6):1565–1569. doi: 10.1093/nar/18.6.1565. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oliver J. L., Marín A., Martínez-Zapater J. M. Chloroplast genes transferred to the nuclear plant genome have adjusted to nuclear base composition and codon usage. Nucleic Acids Res. 1990 Jan 11;18(1):65–73. doi: 10.1093/nar/18.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Perlak F. J., Fuchs R. L., Dean D. A., McPherson S. L., Fischhoff D. A. Modification of the coding sequence enhances plant expression of insect control protein genes. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3324–3328. doi: 10.1073/pnas.88.8.3324. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quigley F., Brinkmann H., Martin W. F., Cerff R. Strong functional GC pressure in a light-regulated maize gene encoding subunit GAPA of chloroplast glyceraldehyde-3-phosphate dehydrogenase: implications for the evolution of GAPA pseudogenes. J Mol Evol. 1989 Nov;29(5):412–421. doi: 10.1007/BF02602911. [DOI] [PubMed] [Google Scholar]
- Quigley F., Martin W. F., Cerff R. Intron conservation across the prokaryote-eukaryote boundary: structure of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2672–2676. doi: 10.1073/pnas.85.8.2672. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sharp P. M., Devine K. M. Codon usage and gene expression level in Dictyostelium discoideum: highly expressed genes do 'prefer' optimal codons. Nucleic Acids Res. 1989 Jul 11;17(13):5029–5039. doi: 10.1093/nar/17.13.5029. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sharp P. M., Li W. H. Codon usage in regulatory genes in Escherichia coli does not reflect selection for 'rare' codons. Nucleic Acids Res. 1986 Oct 10;14(19):7737–7749. doi: 10.1093/nar/14.19.7737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sharp P. M., Tuohy T. M., Mosurski K. R. Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res. 1986 Jul 11;14(13):5125–5143. doi: 10.1093/nar/14.13.5125. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shields D. C., Sharp P. M., Higgins D. G., Wright F. "Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol. 1988 Nov;5(6):704–716. doi: 10.1093/oxfordjournals.molbev.a040525. [DOI] [PubMed] [Google Scholar]
- Shields D. C., Sharp P. M. Synonymous codon usage in Bacillus subtilis reflects both translational selection and mutational biases. Nucleic Acids Res. 1987 Oct 12;15(19):8023–8040. doi: 10.1093/nar/15.19.8023. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shotwell M. A., Boyer S. K., Chesnut R. S., Larkins B. A. Analysis of seed storage protein genes of oats. J Biol Chem. 1990 Jun 15;265(17):9652–9658. [PubMed] [Google Scholar]
- Springer B. A., Sligar S. G. High-level expression of sperm whale myoglobin in Escherichia coli. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8961–8965. doi: 10.1073/pnas.84.24.8961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sørensen M. A., Kurland C. G., Pedersen S. Codon usage determines translation rate in Escherichia coli. J Mol Biol. 1989 May 20;207(2):365–377. doi: 10.1016/0022-2836(89)90260-x. [DOI] [PubMed] [Google Scholar]
- Viotti A., Balducci C., Weil J. H. Adaptation of the tRNA population of maize endosperm for zein synthesis. Biochim Biophys Acta. 1978 Jan 26;517(1):125–132. doi: 10.1016/0005-2787(78)90040-0. [DOI] [PubMed] [Google Scholar]
- Williams D. P., Regier D., Akiyoshi D., Genbauffe F., Murphy J. R. Design, synthesis and expression of a human interleukin-2 gene incorporating the codon usage bias found in highly expressed Escherichia coli genes. Nucleic Acids Res. 1988 Nov 25;16(22):10453–10467. doi: 10.1093/nar/16.22.10453. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wolfe K. H., Sharp P. M., Li W. H. Mutation rates differ among regions of the mammalian genome. Nature. 1989 Jan 19;337(6204):283–285. doi: 10.1038/337283a0. [DOI] [PubMed] [Google Scholar]
- Wright F., Bibb M. J. Codon usage in the G+C-rich Streptomyces genome. Gene. 1992 Apr 1;113(1):55–65. doi: 10.1016/0378-1119(92)90669-g. [DOI] [PubMed] [Google Scholar]
- Wright F. The 'effective number of codons' used in a gene. Gene. 1990 Mar 1;87(1):23–29. doi: 10.1016/0378-1119(90)90491-9. [DOI] [PubMed] [Google Scholar]