Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1997 Jan 15;25(2):438–446. doi: 10.1093/nar/25.2.438

Identification of additional rRNA fragments encoded by the Plasmodium falciparum 6 kb element.

J E Feagin 1, B L Mericle 1, E Werner 1, M Morris 1
PMCID: PMC146428  PMID: 9016576

Abstract

Sequences similar to mitochondrial large and small subunit rRNAs are found as small scattered fragments on a tandemly reiterated 6 kb element in the human malaria parasite Plasmodium falciparum. The rDNA sequences previously identified include strongly conserved portions of rRNA, suggesting that fragmented rRNAs derived from them are able to associate into functional ribosomes. However, sequences corresponding to other expected rRNA regions were not found. We here report that 10 of the 13 previously described rDNA regions have abundant small transcripts. An additional 10 transcripts were found from regions not previously known to contain genes. Five of the latter have been identified as rRNA fragments, including those corresponding to the 5'end and 790 loop sequences of small subunit rRNA and the sarcin/ ricin loop of large subunit rRNA. Demonstration that most of the previously described rDNA regions have abundant transcripts and the identification of new transcripts with other portions of conventional rRNAs provide support for the hypothesis that these small transcripts comprise functional rRNAs.

Full Text

The Full Text of this article is available as a PDF (180.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aldritt S. M., Joseph J. T., Wirth D. F. Sequence identification of cytochrome b in Plasmodium gallinaceum. Mol Cell Biol. 1989 Sep;9(9):3614–3620. doi: 10.1128/mcb.9.9.3614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alksne L. E., Anthony R. A., Liebman S. W., Warner J. R. An accuracy center in the ribosome conserved over 2 billion years. Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9538–9541. doi: 10.1073/pnas.90.20.9538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bakin A., Lane B. G., Ofengand J. Clustering of pseudouridine residues around the peptidyltransferase center of yeast cytoplasmic and mitochondrial ribosomes. Biochemistry. 1994 Nov 15;33(45):13475–13483. doi: 10.1021/bi00249a036. [DOI] [PubMed] [Google Scholar]
  4. Boer P. H., Gray M. W. Scrambled ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA. Cell. 1988 Nov 4;55(3):399–411. doi: 10.1016/0092-8674(88)90026-8. [DOI] [PubMed] [Google Scholar]
  5. Burgin A. B., Parodos K., Lane D. J., Pace N. R. The excision of intervening sequences from Salmonella 23S ribosomal RNA. Cell. 1990 Feb 9;60(3):405–414. doi: 10.1016/0092-8674(90)90592-3. [DOI] [PubMed] [Google Scholar]
  6. Campbell D. A., Kubo K., Clark C. G., Boothroyd J. C. Precise identification of cleavage sites involved in the unusual processing of trypanosome ribosomal RNA. J Mol Biol. 1987 Jul 5;196(1):113–124. doi: 10.1016/0022-2836(87)90514-6. [DOI] [PubMed] [Google Scholar]
  7. Chang D. D., Clayton D. A. Mouse RNAase MRP RNA is encoded by a nuclear gene and contains a decamer sequence complementary to a conserved region of mitochondrial RNA substrate. Cell. 1989 Jan 13;56(1):131–139. doi: 10.1016/0092-8674(89)90991-4. [DOI] [PubMed] [Google Scholar]
  8. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  9. Côté V., Mercier J. P., Lemieux C., Turmel M. The single group-I intron in the chloroplast rrnL gene of Chlamydomonas humicola encodes a site-specific DNA endonuclease (I-ChuI). Gene. 1993 Jul 15;129(1):69–76. doi: 10.1016/0378-1119(93)90697-2. [DOI] [PubMed] [Google Scholar]
  10. Dahlberg A. E. The functional role of ribosomal RNA in protein synthesis. Cell. 1989 May 19;57(4):525–529. doi: 10.1016/0092-8674(89)90122-0. [DOI] [PubMed] [Google Scholar]
  11. Denovan-Wright E. M., Lee R. W. Comparative structure and genomic organization of the discontinuous mitochondrial ribosomal RNA genes of Chlamydomonas eugametos and Chlamydomonas reinhardtii. J Mol Biol. 1994 Aug 12;241(2):298–311. doi: 10.1006/jmbi.1994.1505. [DOI] [PubMed] [Google Scholar]
  12. Feagin J. E., Drew M. E. Plasmodium falciparum: alterations in organelle transcript abundance during the erythrocytic cycle. Exp Parasitol. 1995 May;80(3):430–440. doi: 10.1006/expr.1995.1055. [DOI] [PubMed] [Google Scholar]
  13. Feagin J. E. The 6-kb element of Plasmodium falciparum encodes mitochondrial cytochrome genes. Mol Biochem Parasitol. 1992 May;52(1):145–148. doi: 10.1016/0166-6851(92)90046-m. [DOI] [PubMed] [Google Scholar]
  14. Feagin J. E. The extrachromosomal DNAs of apicomplexan parasites. Annu Rev Microbiol. 1994;48:81–104. doi: 10.1146/annurev.mi.48.100194.000501. [DOI] [PubMed] [Google Scholar]
  15. Feagin J. E., Werner E., Gardner M. J., Williamson D. H., Wilson R. J. Homologies between the contiguous and fragmented rRNAs of the two Plasmodium falciparum extrachromosomal DNAs are limited to core sequences. Nucleic Acids Res. 1992 Feb 25;20(4):879–887. doi: 10.1093/nar/20.4.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gardner M. J., Feagin J. E., Moore D. J., Rangachari K., Williamson D. H., Wilson R. J. Sequence and organization of large subunit rRNA genes from the extrachromosomal 35 kb circular DNA of the malaria parasite Plasmodium falciparum. Nucleic Acids Res. 1993 Mar 11;21(5):1067–1071. doi: 10.1093/nar/21.5.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gardner M. J., Feagin J. E., Moore D. J., Spencer D. F., Gray M. W., Williamson D. H., Wilson R. J. Organisation and expression of small subunit ribosomal RNA genes encoded by a 35-kilobase circular DNA in Plasmodium falciparum. Mol Biochem Parasitol. 1991 Sep;48(1):77–88. doi: 10.1016/0166-6851(91)90166-4. [DOI] [PubMed] [Google Scholar]
  18. Gautheret D., Konings D., Gutell R. R. A major family of motifs involving G.A mismatches in ribosomal RNA. J Mol Biol. 1994 Sep 9;242(1):1–8. doi: 10.1006/jmbi.1994.1552. [DOI] [PubMed] [Google Scholar]
  19. Gray M. W. Origin and evolution of mitochondrial DNA. Annu Rev Cell Biol. 1989;5:25–50. doi: 10.1146/annurev.cb.05.110189.000325. [DOI] [PubMed] [Google Scholar]
  20. Gutell R. R. Collection of small subunit (16S- and 16S-like) ribosomal RNA structures: 1994. Nucleic Acids Res. 1994 Sep;22(17):3502–3507. doi: 10.1093/nar/22.17.3502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gutell R. R., Gray M. W., Schnare M. N. A compilation of large subunit (23S and 23S-like) ribosomal RNA structures: 1993. Nucleic Acids Res. 1993 Jul 1;21(13):3055–3074. doi: 10.1093/nar/21.13.3055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gutell R. R., Larsen N., Woese C. R. Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiol Rev. 1994 Mar;58(1):10–26. doi: 10.1128/mr.58.1.10-26.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Heinonen T. Y., Schnare M. N., Young P. G., Gray M. W. Rearranged coding segments, separated by a transfer RNA gene, specify the two parts of a discontinuous large subunit ribosomal RNA in Tetrahymena pyriformis mitochondria. J Biol Chem. 1987 Feb 25;262(6):2879–2887. [PubMed] [Google Scholar]
  24. Ji Y. E., Mericle B. L., Rehkopf D. H., Anderson J. D., Feagin J. E. The Plasmodium falciparum 6 kb element is polycistronically transcribed. Mol Biochem Parasitol. 1996 Oct 30;81(2):211–223. doi: 10.1016/0166-6851(96)02712-0. [DOI] [PubMed] [Google Scholar]
  25. Joseph J. T., Aldritt S. M., Unnasch T., Puijalon O., Wirth D. F. Characterization of a conserved extrachromosomal element isolated from the avian malarial parasite Plasmodium gallinaceum. Mol Cell Biol. 1989 Sep;9(9):3621–3629. doi: 10.1128/mcb.9.9.3621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kairo A., Fairlamb A. H., Gobright E., Nene V. A 7.1 kb linear DNA molecule of Theileria parva has scrambled rDNA sequences and open reading frames for mitochondrially encoded proteins. EMBO J. 1994 Feb 15;13(4):898–905. doi: 10.1002/j.1460-2075.1994.tb06333.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lane B. G., Ofengand J., Gray M. W. Pseudouridine and O2'-methylated nucleosides. Significance of their selective occurrence in rRNA domains that function in ribosome-catalyzed synthesis of the peptide bonds in proteins. Biochimie. 1995;77(1-2):7–15. doi: 10.1016/0300-9084(96)88098-9. [DOI] [PubMed] [Google Scholar]
  28. Lemieux C., Boulanger J., Otis C., Turmel M. Nucleotide sequence of the chloroplast large subunit rRNA gene from Chlamydomonas reinhardtii. Nucleic Acids Res. 1989 Oct 11;17(19):7997–7997. doi: 10.1093/nar/17.19.7997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mahendran R., Spottswood M. S., Ghate A., Ling M. L., Jeng K., Miller D. L. Editing of the mitochondrial small subunit rRNA in Physarum polycephalum. EMBO J. 1994 Jan 1;13(1):232–240. doi: 10.1002/j.1460-2075.1994.tb06253.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. O'Connor M., Göringer H. U., Dahlberg A. E. A ribosomal ambiguity mutation in the 530 loop of E. coli 16S rRNA. Nucleic Acids Res. 1992 Aug 25;20(16):4221–4227. doi: 10.1093/nar/20.16.4221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Powers T., Noller H. F. A functional pseudoknot in 16S ribosomal RNA. EMBO J. 1991 Aug;10(8):2203–2214. doi: 10.1002/j.1460-2075.1991.tb07756.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Powers T., Noller H. F. Dominant lethal mutations in a conserved loop in 16S rRNA. Proc Natl Acad Sci U S A. 1990 Feb;87(3):1042–1046. doi: 10.1073/pnas.87.3.1042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Powers T., Noller H. F. Evidence for functional interaction between elongation factor Tu and 16S ribosomal RNA. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1364–1368. doi: 10.1073/pnas.90.4.1364. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Powers T., Noller H. F. Selective perturbation of G530 of 16 S rRNA by translational miscoding agents and a streptomycin-dependence mutation in protein S12. J Mol Biol. 1994 Jan 7;235(1):156–172. doi: 10.1016/s0022-2836(05)80023-3. [DOI] [PubMed] [Google Scholar]
  35. Raué H. A., Klootwijk J., Musters W. Evolutionary conservation of structure and function of high molecular weight ribosomal RNA. Prog Biophys Mol Biol. 1988;51(2):77–129. doi: 10.1016/0079-6107(88)90011-9. [DOI] [PubMed] [Google Scholar]
  36. Schnare M. N., Gray M. W. Sixteen discrete RNA components in the cytoplasmic ribosome of Euglena gracilis. J Mol Biol. 1990 Sep 5;215(1):73–83. doi: 10.1016/S0022-2836(05)80096-8. [DOI] [PubMed] [Google Scholar]
  37. Schnare M. N., Heinonen T. Y., Young P. G., Gray M. W. A discontinuous small subunit ribosomal RNA in Tetrahymena pyriformis mitochondria. J Biol Chem. 1986 Apr 15;261(11):5187–5193. [PubMed] [Google Scholar]
  38. Simpson A. M., Suyama Y., Dewes H., Campbell D. A., Simpson L. Kinetoplastid mitochondria contain functional tRNAs which are encoded in nuclear DNA and also contain small minicircle and maxicircle transcripts of unknown function. Nucleic Acids Res. 1989 Jul 25;17(14):5427–5445. doi: 10.1093/nar/17.14.5427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Skurnik M., Toivanen P. Intervening sequences (IVSs) in the 23S ribosomal RNA genes of pathogenic Yersinia enterocolitica strains. The IVSs in Y. enterocolitica and Salmonella typhimurium have a common origin. Mol Microbiol. 1991 Mar;5(3):585–593. doi: 10.1111/j.1365-2958.1991.tb00729.x. [DOI] [PubMed] [Google Scholar]
  40. Sloof P., Van den Burg J., Voogd A., Benne R., Agostinelli M., Borst P., Gutell R., Noller H. Further characterization of the extremely small mitochondrial ribosomal RNAs from trypanosomes: a detailed comparison of the 9S and 12S RNAs from Crithidia fasciculata and Trypanosoma brucei with rRNAs from other organisms. Nucleic Acids Res. 1985 Jun 11;13(11):4171–4190. doi: 10.1093/nar/13.11.4171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Spencer D. F., Collings J. C., Schnare M. N., Gray M. W. Multiple spacer sequences in the nuclear large subunit ribosomal RNA gene of Crithidia fasciculata. EMBO J. 1987 Apr;6(4):1063–1071. doi: 10.1002/j.1460-2075.1987.tb04859.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Suplick K., Morrisey J., Vaidya A. B. Complex transcription from the extrachromosomal DNA encoding mitochondrial functions of Plasmodium yoelii. Mol Cell Biol. 1990 Dec;10(12):6381–6388. doi: 10.1128/mcb.10.12.6381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Szewczak A. A., Moore P. B., Chang Y. L., Wool I. G. The conformation of the sarcin/ricin loop from 28S ribosomal RNA. Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9581–9585. doi: 10.1073/pnas.90.20.9581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Trager W., Jenson J. B. Cultivation of malarial parasites. Nature. 1978 Jun 22;273(5664):621–622. doi: 10.1038/273621a0. [DOI] [PubMed] [Google Scholar]
  45. Turmel M., Boulanger J., Schnare M. N., Gray M. W., Lemieux C. Six group I introns and three internal transcribed spacers in the chloroplast large subunit ribosomal RNA gene of the green alga Chlamydomonas eugametos. J Mol Biol. 1991 Mar 20;218(2):293–311. doi: 10.1016/0022-2836(91)90713-g. [DOI] [PubMed] [Google Scholar]
  46. Uhlenbeck O. C. Tetraloops and RNA folding. Nature. 1990 Aug 16;346(6285):613–614. doi: 10.1038/346613a0. [DOI] [PubMed] [Google Scholar]
  47. Vaidya A. B., Akella R., Suplick K. Sequences similar to genes for two mitochondrial proteins and portions of ribosomal RNA in tandemly arrayed 6-kilobase-pair DNA of a malarial parasite. Mol Biochem Parasitol. 1989 Jun 15;35(2):97–107. doi: 10.1016/0166-6851(89)90112-6. [DOI] [PubMed] [Google Scholar]
  48. White T. C., Rudenko G., Borst P. Three small RNAs within the 10 kb trypanosome rRNA transcription unit are analogous to domain VII of other eukaryotic 28S rRNAs. Nucleic Acids Res. 1986 Dec 9;14(23):9471–9489. doi: 10.1093/nar/14.23.9471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wool I. G., Glück A., Endo Y. Ribotoxin recognition of ribosomal RNA and a proposal for the mechanism of translocation. Trends Biochem Sci. 1992 Jul;17(7):266–269. doi: 10.1016/0968-0004(92)90407-z. [DOI] [PubMed] [Google Scholar]
  50. de la Cruz V. F., Lake J. A., Simpson A. M., Simpson L. A minimal ribosomal RNA: sequence and secondary structure of the 9S kinetoplast ribosomal RNA from Leishmania tarentolae. Proc Natl Acad Sci U S A. 1985 Mar;82(5):1401–1405. doi: 10.1073/pnas.82.5.1401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. de la Cruz V. F., Simpson A. M., Lake J. A., Simpson L. Primary sequence and partial secondary structure of the 12S kinetoplast (mitochondrial) ribosomal RNA from Leishmania tarentolae: conservation of peptidyl-transferase structural elements. Nucleic Acids Res. 1985 Apr 11;13(7):2337–2356. doi: 10.1093/nar/13.7.2337. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES