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The complete set of Toxoplasma gondii ribosomal protein genes contains two conserved promoter elements

Published online by Cambridge University Press:  04 May 2006

N. F. J. VAN POPPEL ,
J. WELAGEN ,
A. N. VERMEULEN  and
D. SCHAAP
N. F. J. VAN POPPEL
Affiliation:
Department of Parasitology R&D, Intervet International BV, P.O. Box 31, 5830 AA Boxmeer, The Netherlands
J. WELAGEN
Affiliation:
Department of Parasitology R&D, Intervet International BV, P.O. Box 31, 5830 AA Boxmeer, The Netherlands
A. N. VERMEULEN
Affiliation:
Department of Parasitology R&D, Intervet International BV, P.O. Box 31, 5830 AA Boxmeer, The Netherlands
D. SCHAAP
Affiliation:
Department of Parasitology R&D, Intervet International BV, P.O. Box 31, 5830 AA Boxmeer, The Netherlands
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Abstract

Recently we showed that de novo ribosome biosynthesis is transcriptionally regulated in Coccidia, depending on their life-cycle stage. Since the expression of ribosomal protein genes is likely coordinated, the transcriptional control of all Toxoplasma gondii ribosomal protein (RP) genes was analysed. Therefore, the complete set of all cytoplasmic RPs was defined, containing 79 different RPs in T. gondii. RP genes were randomly distributed over the genome, each with a unique upstream region with the exception of 8 RP genes which were paired in a head-to-head orientation. To study if the RP genes share conserved promoter elements, a database was made containing upstream sequences of all T. gondii RP genes. Promoter activity was confirmed for the upstream sequences of 8 RP genes, some of which are comparable in strength to the alpha-tubulin promoter. In the complete set of RP upstream sequences 2 novel and highly conserved elements were identified, named Toxoplasma Ribosomal Protein (TRP)-1 (consensus: TCGGCTTATATTCGG) and TRP-2 ([T/C]GCATGC[G/A]). TRP-1 and/or TRP-2 were present in 95% of all RP upstream sequences and moreover, were specifically localized in a small region near the presumptive transcriptional start site (10–330 bp upstream). Although TRP elements were mostly absent in known T. gondii promoters, they are present elsewhere in the T. gondii genome suggesting that they operate not only in RP genes but in a larger set of genes. The identification of TRP elements creates a basis to further study the underlying mechanism by which RP transcription is controlled in T. gondii.The nucleotide sequence data reported in this paper are available in the Third Party Annotation Section of the DDBJ/EMBL/GenBank databases under the Accession numbers TPA: BK004896-BK004974.

Keywords

ribosome biosynthesistranscriptional regulationpromoterTRP element
Type
Research Article
Information
Parasitology , Volume 133 , Issue 1 , July 2006 , pp. 19 - 31
Copyright
2006 Cambridge University Press

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References

REFERENCES

Ajioka, J. W., Boothroyd, J. C., Brunk, B. P., Hehl, A., Hillier, L., Manger, I. D., Marra, M., Overton, G. C., Roos, D. S., Wan, K. L., Waterston, R. and Sibley, L. D. ( 1998). Gene discovery by EST sequencing in Toxoplasma gondii reveals sequences restricted to the Apicomplexa. Genome Research 8, 18–28.CrossRefGoogle Scholar
Donald, R. G., Carter, D., Ullman, B. and Roos, D. S. ( 1996). Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthine-xanthine-guanine phosphoribosyltransferase gene. Use as a selectable marker for stable transformation. Journal of Biological Chemistry 271, 14010–14019.Google Scholar
Gagnon, S., Bourbeau, D. and Levesque, R. C. ( 1996). Secondary structures and features of the 18S, 5.8S and 26S ribosomal RNAs from the Apicomplexan parasite Toxoplasma gondii. Gene 173, 129–135.Google Scholar
Guay, J. M., Huot, A., Gagnon, S., Tremblay, A. and Levesque, R. C. ( 1992). Physical and genetic mapping of cloned ribosomal DNA from Toxoplasma gondii: primary and secondary structure of the 5S gene. Gene 114, 165–171.CrossRefGoogle Scholar
Horn, P. J. and Peterson, C. L. ( 2002). Molecular biology. Chromatin higher order folding--wrapping up transcription. Science 297, 1824–1827.Google Scholar
Ju, Q. and Warner, J. R. ( 1994). Ribosome synthesis during the growth cycle of Saccharomyces cerevisiae. Yeast 10, 151–157.CrossRefGoogle Scholar
Kenmochi, N., Kawaguchi, T., Rozen, S., Davis, E., Goodman, N., Hudson, T. J., Tanaka, T. and Page, D. C. ( 1998). A map of 75 human ribosomal protein genes. Genome Research 8, 509–523.CrossRefGoogle Scholar
Lee, T. I., Rinaldi, N. J., Robert, F., Odom, D. T., Bar-Joseph, Z., Gerber, G. K., Hannett, N. M., Harbison, C. T., Thompson, C. M., Simon, I., Zeitlinger, J., Jennings, E. G., Murray, H. L., Gordon, D. B., Ren, B., Wyrick, J. J., Tagne, J. B., Volkert, T. L., Fraenkel, E., Gifford, D. K. and Young, R. A. ( 2002). Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298, 799–804.CrossRefGoogle Scholar
Li, L., Brunk, B. P., Kissinger, J. C., Pape, D., Tang, K., Cole, R. H., Martin, J., Wylie, T., Dante, M., Fogarty, S. J., Howe, D. K., Liberator, P., Diaz, C., Anderson, J., White, M., Jerome, M. E., Johnson, E. A., Radke, J. A., Stoeckert, C. J. Jr, Waterston, R. H., Clifton, S. W., Roos, D. S. and Sibley, L. D. ( 2003). Gene discovery in the apicomplexa as revealed by EST sequencing and assembly of a comparative gene database. Genome Research 13, 443–454.CrossRefGoogle Scholar
Mager, W. H., Planta, R. J., Ballesta, J. G., Lee, J. C., Mizuta, K., Suzuki, K., Warner, J. R. and Woolford, J. ( 1997). A new nomenclature for the cytoplasmic ribosomal proteins of Saccharomyces cerevisiae. Nucleic Acids Research 25, 4872–4875.CrossRefGoogle Scholar
Martin, D. E., Soulard, A. and Hall, M. N. ( 2004). TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 119, 969–979.CrossRefGoogle Scholar
Meyuhas, O. ( 2000). Synthesis of the translational apparatus is regulated at the translational level. European Journal of Biochemistry 267, 6321–6330.CrossRefGoogle Scholar
Pearson, N. J. and Haber, J. E. ( 1980). Changes in regulation of ribosomal protein synthesis during vegetative growth and sporulation of Saccharomyces cerevisiae. Journal of Bacteriology 143, 1411–1419.Google Scholar
Planta, R. J. and Mager, W. H. ( 1998). The list of cytoplasmic ribosomal proteins of Saccharomyces cerevisiae. Yeast 14, 471–477.3.0.CO;2-U>CrossRefGoogle Scholar
Schaap, D., Arts, G., van Poppel, N. F. J. and Vermeulen, A. N. ( 2005). De novo ribosome biosynthesis is transcriptionally regulated in Eimeria tenella, dependent on its life cycle stage. Molecular and Biochemical Parasitology 139, 239–248.CrossRefGoogle Scholar
Seeber, F. ( 1997). Consensus sequence of translational initiation sites from Toxoplasma gondii genes. Parasitology Research 83, 309–311.CrossRefGoogle Scholar
Seeber, F. and Boothroyd, J. C. ( 1996). Escherichia coli beta-galactosidase as an in vitro and in vivo reporter enzyme and stable transfection marker in the intracellular protozoan parasite Toxoplasma gondii. Gene 169, 39–45.Google Scholar
Soldati, D. and Boothroyd, J. C. ( 1993). Transient transfection and expression in the obligate intracellular parasite Toxoplasma gondii. Science 260, 349–352.CrossRefGoogle Scholar
Striepen, B., He, C. Y., Matrajt, M., Soldati, D. and Roos, D. S. ( 1998). Expression, selection, and organellar targeting of the green fluorescent protein in Toxoplasma gondii. Molecular and Biochemical Parasitology 92, 325–338.CrossRefGoogle Scholar
van Driel, R., Fransz, P. F. and Verschure, P. J. ( 2003). The eukaryotic genome: a system regulated at different hierarchical levels. Journal of Cell Science 116, 4067–4075.CrossRefGoogle Scholar
Wade, J. T., Hall, D. B. and Struhl, K. ( 2004). The transcription factor Ifh1 is a key regulator of yeast ribosomal protein genes. Nature, London 432, 1054–1058.CrossRefGoogle Scholar
Warner, J. R., Mitra, G., Schwindinger, W. F., Studeny, M. and Fried, H. M. ( 1985). Saccharomyces cerevisiae coordinates accumulation of yeast ribosomal proteins by modulating mRNA splicing, translational initiation, and protein turnover. Molecular and Cellular Biology 5, 1512–1521.CrossRefGoogle Scholar
Warner, J. R. ( 1999). The economics of ribosome biosynthesis in yeast. Trends in Biochemical Sciences 24, 437–440.CrossRefGoogle Scholar
Yoshihama, M., Uechi, T., Asakawa, S., Kawasaki, K., Kato, S., Higa, S., Maeda, N., Minoshima, S., Tanaka, T., Shimizu, N. and Kenmochi, N. ( 2002). The human ribosomal protein genes: sequencing and comparative analysis of 73 genes. Genome Research 12, 379–390.CrossRefGoogle Scholar