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The effect of expression levels on codon usage in Plasmodium falciparum

Published online by Cambridge University Press:  03 March 2004

L. PEIXOTO ,
V. FERNÁNDEZ  and
H. MUSTO
L. PEIXOTO
Affiliation:
Laboratorio de Organización y Evolución del Genoma, Facultad de Ciencias, Iguá 4225, Montevideo 11400, Uruguay Departamento de Bioquímica, Instituto de Investigaciones Biológicas Clemente Estable, Montevideo, Uruguay
V. FERNÁNDEZ
Affiliation:
Cátedra de Inmunología, Facultad de Química, Montevideo, Uruguay
H. MUSTO
Affiliation:
Laboratorio de Organización y Evolución del Genoma, Facultad de Ciencias, Iguá 4225, Montevideo 11400, Uruguay
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Abstract

The usage of alternative synonymous codons in the completely sequenced, extremely A+T-rich parasite Plasmodium falciparum was studied. Confirming previous studies obtained with less than 3% of the total genes recently described, we found that A- and U-ending triplets predominate but translational selection increases the frequency of a subset of codons in highly expressed genes. However, some new results come from the analysis of the complete sequence. First, there is more variation in GC3 than previously described; second, the effect of natural selection acting at the level of translation has been analysed with real expression data at 4 different stages and third, we found that highly expressed proteins increment the frequency of energetically less expensive amino acids. The implications of these results are discussed.

Keywords

Plasmodiumcodon usagetranslational selectioncorrespondence analysismutational biasoptimal codonsproteome
Type
Research Article
Information
Parasitology , Volume 128 , Issue 3 , March 2004 , pp. 245 - 251
Copyright
2004 Cambridge University Press

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References

REFERENCES

AKASHI, H. & EYRE-WALKER, A. (1998). Translational selection and molecular evolution. Current Opinion in Genetics and Development 8, 688–693.CrossRefGoogle Scholar
AKASHI, H. & GOJOBORI, T. (2002). Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proceedings of the National Academy of Sciences, USA 99, 3695–3700.CrossRefGoogle Scholar
AKASHI, H. (2001). Gene expression and molecular evolution. Current Opinion in Genetics and Development 11, 660–666.CrossRefGoogle Scholar
ALVAREZ, F., ROBELLO, C. & VIGNALI, M. (1994). Evolution of codon usage and base contents in kinetoplastid protozoans. Molecular Biology and Evolution 11, 790–802.Google Scholar
ANDERSSON, S. G. & KURLAND, C. G. (1990). Codon preferences in free-living microorganisms. Microbiological Reviews 54, 198–210.Google Scholar
BAHL, A., BRUNK, B., CRABTREE, J., FRAUNHOLZ, M. J., GAJRIA, B., GRANT, G. R., GINSBURG, H., GUPTA, D., KISSINGER, J. C., LABO, P., LI, L., MAILMAN, M. D., MILGRAM, A. J., PEARSON, D. S., ROOS, D. S., SCHUG, J., STOECKERT, C. J. jr. & WHETZEL, P. (2003). PlasmoDB: the Plasmodium genome resource. A database integrating experimental and computational data. Nucleic Acids Research 31, 212–215.Google Scholar
BULMER, M. (1991). The selection-mutation-drift theory of synonymous codon usage. Genetics 129, 897–907.Google Scholar
CARLINI, D. B. & STEPHAN, W. (2003). In vivo introduction of unpreferred synonymous codons into the Drosophila Adh gene results in reduced levels of ADH protein. Genetics 163, 239–243.Google Scholar
COGHLAN, A. & WOLFE, K. H. (2000). Relationship of codon bias to mRNA concentration and protein length in Saccharomyces cerevisiae. Yeast 16, 1131–1145.3.0.CO;2-F>CrossRefGoogle Scholar
CORTAZZO, P., CERVENANSKY, C., MARIN, M., REISS, C., EHRLICH, R. & DEANA, A. (2002). Silent mutations affect in vivo protein folding in Escherichia coli. Biochemical and Biophysical Research Communications 293, 537–541.CrossRefGoogle Scholar
DEANA, A., EHRLICH, R. & REISS, C. (1998). Silent mutations in the Escherichia coli ompA leader peptide region strongly affect transcription and translation in vivo. Nucleic Acids Research 26, 4778–4782.CrossRefGoogle Scholar
DUAN, J., WAINWRIGHT, M. S., COMERON, J. M., SAITOU, N., SANDERS, A. R., GELERNTER, J. & GEJMAN, P. V. (2003). Synonymous mutations in the human dopamine receptor D2 (DRD2) affect mRNA stability and synthesis of the receptor. Human Molecular Genetics 12, 205–216.CrossRefGoogle Scholar
DURET, L. & MOUCHIROUD, D. (1999). Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proceedings of the National Academy of Sciences, USA 96, 4482–4487.CrossRefGoogle Scholar
ERMOLAEVA, M. D. (2001). Synonymous codon usage in bacteria. Current Issues in Molecular Biology 3, 91–97.Google Scholar
FERNÁNDEZ, V., ZAVALA, A. & MUSTO, H. (2001). Evidence for translational selection in codon usage in Echinococcus spp. Parasitology 123, 203–209.CrossRefGoogle Scholar
FLORENS, L., WASHBURN, M. P., RAINE, J. D., ANTHONY, R. M., GRAINGER, M., HAYNES, J. D., MOCH, J. K., MUSTER, N., SACCI, J. B., TABB, D. L., WITNEY, A. A., WOLTERS, D., WU, Y., GARDNER, M. J., HOLDER, A. A., SINDEN, R. E., YATES, J. R. & CARUCCI, D. J. (2002). A proteomic view of the Plasmodium falciparum life cycle. Nature, London 419, 520–526.CrossRefGoogle Scholar
GARDNER, M. J., HALL, N., FUNG, E., WHITE, O., BERRIMAN, M., HYMAN, R. W., CARLTON, J. M., PAIN, A., NELSON, K. E., BOWMAN, S., PAULSEN, I. T., JAMES, K., EISEN, J. A., RUTHERFORD, K., SALZBERG, S. L., CRAIG, A., KYES, S., CHAN, M. S., NENE, V., SHALLOM, S. J., SUH, B., PETERSON, J., ANGIUOLI, S., PERTEA, M., ALLEN, J., SELENGUT, J., HAFT, D., MATHER, M. W., VAIDYA, A. B., MARTIN, D. M., FAIRLAMB, A. H., FRAUNHOLZ, M. J., ROOS, D. S., RALPH, S. A., McFADDEN, G. I., CUMMINGS, L. M., SUBRAMANIAN, G. M., MUNGALL, C., VENTER, J. C., CARUCCI, D. J., HOFFMAN, S. L., NEWBOLD, C., DAVIS, R. W., FRASER, C. M. & BARRELL, B. (2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature, London 419, 498–511.CrossRefGoogle Scholar
GOMAN, M., LANGSLEY, G., HYDE, J. E., YANKOVSKY, N. K., ZOLG, J. W. & SCAIFE, J. G. (1982). The establishment of genomic DNA libraries for the human malaria parasite Plasmodium falciparum and identification of individual clones by hybridisation. Molecular and Biochemical Parasitology 5, 391–400.CrossRefGoogle Scholar
GRANTHAM, R., GAUTIER, C., GOUY, M., JACOBZONE, M. & MERCIER, R. (1981). Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Research 9, r43–r74.CrossRefGoogle Scholar
GREENACRE, M. (1984). Theory and Application of Correspondence Analysis. London, Academic Press.
HYDE, J. E. & SIMS, P. F. (1987). Anomalous dinucleotide frequencies in both coding and non-coding regions from the genome of the human malaria parasite Plasmodium falciparum. Gene 61, 177–187.CrossRefGoogle Scholar
KANAYA, S., YAMADA, Y., KUDO, Y. & IKEMURA, T. (1999). Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. Gene 238, 143–155.CrossRefGoogle Scholar
McCUTCHAN, T. F., DAME, J. B., MILLER, L. H. & BARNWELL, J. (1984). Evolutionary relatedness of Plasmodium species as determined by the structure of DNA. Science 225, 808–811.CrossRefGoogle Scholar
MUSTO, H., CACCIÒ, S., RODRIGUEZ-MASEDA, H. & BERNARDI, G. (1997). Compositional constraints in the extremely GC-poor genome of Plasmodium falciparum. Memorias do Instituto Oswaldo Cruz 92, 835–841.CrossRefGoogle Scholar
MUSTO, H., ROMERO, H., ZAVALA, A., JABBARI, K. & BERNARDI, G. (1999). Synonymous codon choices in the extremely GC-poor genome of Plasmodium falciparum: compositional constraints and translational selection. Journal of Molecular Evolution 49, 27–35.CrossRefGoogle Scholar
MUSTO, H., RODRIGUEZ-MASEDA, H. & BERNARDI, G. (1995). Compositional properties of nuclear genes from Plasmodium falciparum. Gene 152, 127–132.CrossRefGoogle Scholar
MUSTO, H., ROMERO, H. & ZAVALA, A. (2003). Translational selection is operative for synonymous codon usage in Clostridium perfringens and Clostridium acetobutylicum. Microbiology 149, 855–863.CrossRefGoogle Scholar
PERRIÈRE, G. & THIOULOUSE, J. (2001). Use and misuse of correspondence analysis in codon usage studies. Nucleic Acids Research 30, 4548–4555.Google Scholar
POLLACK, Y., KATZEN, A. L., SPIRA, D. T. & GOLENSER, J. (1982). The genome of Plasmodium falciparum. I: DNA base composition. Nucleic Acids Research 10, 539–546.Google Scholar
ROMERO, H., ZAVALA, A. & MUSTO, H. (2000). Compositional pressure and translational selection determine codon usage in the extremely GC-poor unicellular eukaryote Entamoeba histolytica. Gene 242, 307–311.CrossRefGoogle Scholar
SAUL, A. & BATTISTUTTA, D. (1988). Codon usage in Plasmodium falciparum. Molecular and Biochemical Parasitology 27, 35–42.CrossRefGoogle Scholar
SHARP, P. M. & DEVINE, K. M. (1989). Codon usage and gene expression level in Dictyostelium discoideum: highly expressed genes do ‘prefer’ optimal codons. Nucleic Acids Research 17, 5029–5039.CrossRefGoogle Scholar
SHARP, P. M. & LI, W. H. (1986). An evolutionary perspective on synonymous codon usage in unicellular organisms. Journal of Molecular Evolution 24, 28–38.CrossRefGoogle Scholar
SHARP, P. M. & MATASSI, G. (1994). Codon usage and genome evolution. Current Opinion in Genetics and Development 4, 851–860.CrossRefGoogle Scholar
SHARP, P. M., TUOHY, T. M. & MOSURSKI, K. R. (1986). Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Research 14, 5125–5143.CrossRefGoogle Scholar
SHARP, P. M., AVEROF, M., LLOYD, A. T., MATASSI, G. & PEDEN, J. F. (1995). DNA sequence evolution: the sounds of silence. Philosophical Transactions of the Royal Society of London, B 349, 241–247.CrossRefGoogle Scholar
SHIELDS, D. C. & SHARP, P. M. (1987). Synonymous codon usage in Bacillus subtilis reflects both translational selection and mutational biases. Nucleic Acids Research 15, 8023–8040.CrossRefGoogle Scholar
SLIMKO, E. M. & LESTER, H. A. (2003). Codon optimization of Caenorhabditis elegans GluCl ion channel genes for mammalian cells dramatically improves expression levels. Journal of Neuroscience Methods 124, 75–81.CrossRefGoogle Scholar
WEBER, J. L. (1987). Analysis of sequences from the extremely A+T-rich genome of Plasmodium falciparum. Gene 52, 103–109.CrossRefGoogle Scholar