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Volume 141, Issue 11

Small cytoplasmic RNA (scRNA) gene from can replace the gene for the scRNA in both growth and sporulation Free

Abstract

Summary: Small cytoplasmic RNA (scRNA) is a member of an evolutionary conserved signal-recognition-particle-like RNA family. Using a DNA fragment of scRNA gene as a probe, we cloned and characterized a gene encoding the scRNA. Mapping the 5' and 3' ends of scRNA revealed that scRNA consists of 269 nucleotides: the sequence has about 70% primary sequence homology with scRNA. The predicted secondary structure appeared to be similar to that of scRNA, indicating that there are domains I and II in scRNA, in addition to domain IV. Functional analysis showed that scRNA could compensate for vegetative growth and allow the formation of heat-resistant spores in an scRNA-depleted strain, whereas 45S RNA could not maintain sporulation. Since both 45S RNA and scRNA have the same binding specificity to Ffh protein, the difference in complementation activity reflects the function of domains I and II.

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Keyword(s): Clostridium perjringens , small cytoplasmic RNA , sporulation and SRP-like RNA
Society for General Microbiology 1995
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1995-11-01
2024-04-19
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References

  1. Althoff S., Selinger D., Wise J.A. 1994; Molecular evolution of SRP cycle components: functional implications.. Nucleic Acids Res 22:1933–1947
     [Google Scholar]
  2. Altman S. 1989; Ribonuclease P: an enzyme with catalytic RNA subunit.. Adv Enɀymol 62:1–36
     [Google Scholar]
  3. Bernstein H.D., Poritz M.A., Strub K., Hoben P.J., Brenner S., Walter P. 1989; Model for signal sequence recognition from amino acid sequence of 54K subunit of signal recognition particle.. Nature 340:482–486
     [Google Scholar]
  4. Bikoff E., Gefter M.L. 1975; In vitro synthesis of transfer RNA. I. Purification of required components.. J Biol Chem 250:6240–6247
     [Google Scholar]
  5. Bourgaize D.B., Fournier M.J. 1987; Initiation of translation is impaired in E. coli cells deficient in 4·5S RNA.. Nature 325:281–284
     [Google Scholar]
  6. Bovia F., Bui N., Strub K. 1994; The heterodimeric subunit SRP9/14 of the signal recognition particle functions as permuted single polypeptide chain.. Nucleic Acids Res 22:2028–2035
     [Google Scholar]
  7. Brennwald P., Liao X., Holm K., Porter G., Wise J.A. 1988; Identification of an essential Schiɀosaccharomyces pombe RNA homologous to the 7SL component of signal recognition particle.. Mol Cell Biol 8:1580–1590
     [Google Scholar]
  8. Brown S. 1987; Mutations in the gene for EF-G reduce the requirement for 4-5S RNA in the growth of E. coli.. Cell 49:825–833
     [Google Scholar]
  9. Brown S. 1989; Time of action of 4·5S RNA in E. coli translation.. J Mol Biol 209:79–90
     [Google Scholar]
  10. Brown S. 1991; Genes for 7S RNAs can replace the genes for 4·5S RNA in growth of Escherichia coli.. J Bacteriol 173:1835–1837
     [Google Scholar]
  11. Brown S., Fournier M.J. 1984; The 4·5S RNA gene of E. coliis essential for cell growth.. J Mol Biol 178:533–550
     [Google Scholar]
  12. Brown S., Thon G., Tolentino E. 1989; Genetic selection and DNA sequences of 4·5S RNA homologs.. J Bacteriol 171:6517–6520
     [Google Scholar]
  13. Campos N., Palau J., Torrent M., Ludevid D. 1988; Signal recognition-like particles are present in maize.. J Biol Chem 263:9646–9650
     [Google Scholar]
  14. Deutscher M.P. 1990; Ribonucleases, tRNA nucleotidyltransferase, and the 3´ processing of tRNA.. Prog Nucleic Acid Res Mol Biol 39:209–240
     [Google Scholar]
  15. Finegold S. 1977 Anaerobic Bacteria in Human Disease. New York:: Academic Press.;
     [Google Scholar]
  16. Fournier M.J., Maxwell E. 1993; The nucleolar snRNAs: catching up with the spliceosomal snRNAs.. Trends Biochem Sci 18:131–135
     [Google Scholar]
  17. Gilmore R. 1993; Protein translocation across the endoplasmic reticulum: a tunnel with toll booths at entry and exit.. Cell 75:589–592
     [Google Scholar]
  18. Gitt M.A., Wang L.F., Doi R.H. 1985; A strong sequence homology exists between RNA polymerase sigma factors of Bacillus subtilis and Escherichia coli.. J Biol Chem 260:7178–7185
     [Google Scholar]
  19. Guthrie C. 1991; Messenger RNA splicing in yeast: clues to why the spliceosome is a ribonucleoprotein.. Science 253:157–163
     [Google Scholar]
  20. Haas E.S., Brown J.W., Daniel C.J., Reeve J.N. 1990; Genes encoding the 7S RNA and tRNAser are linked to one of the two rRNA operons in the genome of the extremely thermophilic archaebacterium Methanothermus fervidus.. Gene 90:51–59
     [Google Scholar]
  21. Hann B.C., Poritz M.A., Walter P. 1989; Saccharomyces cerevisiaeand Schiɀosaccharomyces pombe contain a homologue to the 54 kD subunit of the signal recognition particle that in S. cerevisiae is essential for growth.. J Cell Biol 109:3223–3230
     [Google Scholar]
  22. High S., Dobberstein B. 1991; The signal sequence interacts with the methionine-rich domain of the 54 kD protein of signal recognition particle.. J Cell Biol 113:229–233
     [Google Scholar]
  23. Honda K., Nakamura K., Nishiguchi M., Yamane K. 1993; Cloning and characterization of a Bacillus subtilis gene encoding a homolog of the 54-kilodalton subunit of mammalian signal recognition particle and Escherichia coli Ffh.. J Bacteriol 175:4885–4894
     [Google Scholar]
  24. Hoshino T., Kose K., Uratani Y. 1990; Cloning and nucleotide sequence of the gene braB coding for the sodium-coupled branched- chain amino acids carrier in Pseudomonas aeruginosa PAO.. Mol & Gen Genet 220:461–467
     [Google Scholar]
  25. Inouye M., Delihas N. 1988; Small RNAs in the prokaryotes: a growing list of diverse roles.. Cell 53:5–7
     [Google Scholar]
  26. Kaine B.P. 1990; Structure of the archaebacterial 7S RNA molecule.. Mol & Gen Genet 221:315–321
     [Google Scholar]
  27. Krieg U.C., Walter P., Johnson A.E. 1986; Photocrosslinking of the signal sequence of nascent preprolactin to the 54-kilodalton polypeptide of the signal recognition particle.. Proc Natl Acad Sci USA 838604–8608
     [Google Scholar]
  28. Kurzchalia T.V., Wiedmann M., Girskovich A.S., Bochkareva E.S., Bielka M., Rapoport T.A. 1986; The signal sequence of nascent preprolactin interacts with the 54K polypeptide of signal recognition particle.. Nature 320:634–636
     [Google Scholar]
  29. Larsen N., Zwieb C. 1991; SRP-RNA sequence alignment and secondary structure.. Nucleic Acids Res 19:209–215
     [Google Scholar]
  30. van der Meer J.R., Ludwig W., des Vos W.M. 1993; Characterization of a ribosomal RNA gene cluster from Clostridium tyroboturicum: phylogenetic positioning based on the 16S and 23S nucleotide sequences.. Syst Appl Microbiol 16:201–207
     [Google Scholar]
  31. Nakaar V., Dare A.O., Hong D., Ullu E., Tschudi C. 1994; Upstream tRNA genes are essential for expression of small nuclear and cytoplasmic RNA genes in Trypanosomes.. Mol Cell Biol 14:6736–6742
     [Google Scholar]
  32. Nakamura K., Nakamura A., Takamatsu H., Yamane K. 1990; Cloning and characterization of a Bacillus subtilis gene homologous to Escherichia coli secY.. J Biochem 107:603–607
     [Google Scholar]
  33. Nakamura K., Imai Y., Nakamura A., Yamane K. 1992a; Small cytoplasmic RNA of Bacillus subtilis: functional relationship with human signal recognition particle 7S RNA and Escherichia coli 4·5S RNA.. J Bacteriol 174:2185–2192
     [Google Scholar]
  34. Nakamura K., Minemura M., Nishiguchi M., Honda K., Yamane K. 1992b; Conserved residues and secondary structure found in small cytoplasmic RNAs from Bacillus species.. Nucleic Acids Res 20:5227–5228
     [Google Scholar]
  35. Nakamura K., Nishiguchi M., Honda K., Yamane K. 1994; The Bacillus subtilis SRP54 homologue, Ffh, has an intrinsic GTPase activity and forms a ribonucleoprotein complex with small cytoplasmic RNA in vivo.. Biochem Biophys Res Commun 199:1394–1399
     [Google Scholar]
  36. Nishiguchi M., Honda K., Amikura R., Nakamura K., Yamane K. 1994; Structural requirements of Bacillus subtilis small cytoplasmic RNA for cell growth, sporulation, and extracellular enzyme production.. J Bacteriol 176:157–165
     [Google Scholar]
  37. Normanly J., Ogden R.C., Horvath S.J., Abelson J. 1986; Changing the identity of a transfer RNA.. Nature 321:213–219
     [Google Scholar]
  38. Nunnari J., Walter P. 1992; Protein targeting to and translocation across the membrane of the endoplasmic reticulum.. Curr Opin Cell Biol 4:573–580
     [Google Scholar]
  39. Poritz M.A., Strub K., Walter P. 1988; Human SRP RNA and E. coli 4·5S RNA contain a highly homologous structural domain.. Cell 55:4–6
     [Google Scholar]
  40. Rapoport T.A. 1991; Protein transport across the endoplasmic reticulum membrane: facts, models, mysteries.. FASEB J 5:2792–2798
     [Google Scholar]
  41. Rapoport T.A. 1992; Transport of proteins across the endoplasmic reticulum membrane.. Science 258:931–936
     [Google Scholar]
  42. Romish K., Webb J., Lingelbach K., Gausepohl H., Dobberstein B. 1990; The 54-kD protein of the signal recognition particle contains a methionine-rich RNA binding domain.. J Cell Biol 111:1793–1802
     [Google Scholar]
  43. Saito H., Miura K. 1963; Preparation of transforming deoxyribonucleic acid by phenol treatment.. Biochim Biophys Acta 72:619–629
     [Google Scholar]
  44. Samuelsson T. 1992; Mycoplasma protein homologous to mammalian SRP54 recognizes a highly conserved domain of SRP RNA.. Nucleic Acids Res 20:5763–5770
     [Google Scholar]
  45. Samuelsson T., Guindy Y. 1990; Nucleotide sequence of a Mycoplasma mycoides RNA which is homologous to E. coli 4·5S RNA.. Nucleic Acids Res 18:4938
     [Google Scholar]
  46. Samuelsson T., Olsson M. 1993; GTPase activity of a bacterial SRP-like complex.. Nucleic Acids Res 21:847–853
     [Google Scholar]
  47. Sanders S.L., Schekman R. 1992; Polypeptide translocation across the endoplasmic reticulum membrane.. J Biol Chem 267:13791–13794
     [Google Scholar]
  48. Sekiya T., Contreras R., Takeya T., Khorana H.G. 1979; Total synthesis of a tyrosine suppressor transfer RNA gene. XVII. Transcription in vitro of the synthetic gene and processing of the primary transcript to transfer RNA.. J Biol Chem 254:5802–5816
     [Google Scholar]
  49. Simoneau P., Hu P.-C. 1992; The 4·5S RNA homolog from Mycoplasma pneumoniae: genetic selection, sequence, and transcription analysis.. J Bacteriol 174:627–629
     [Google Scholar]
  50. Smith L.D.S., Hobbs G. 1974; Clostridium.. In Sergey̓s Manual of Determinative Bacteriology pp. 551–572 Buchanan R.E., Gibbons N.E. Edited by Baltimore:: Williams & Wilkins.;
     [Google Scholar]
  51. Strub K., Walter P. 1990; Assembly of the Alu domain of the signal recognition particle (SRP): dimerization of the two protein components is required for efficient binding to SRP RNA.. Mol Cell Biol 10:777–784
     [Google Scholar]
  52. Strub K., Moss J.C.B., Walter P. 1991; Binding sites of the 9 and 14 kD heterodimeric protein subunit of the signal recognition particle (SRP) are contained exclusively in the Alu domain of SRP RNA and contain a sequence motif that is conserved in evolution.. Mol Cell Biol 11:3949–3959
     [Google Scholar]
  53. Struck J.C.R., Erdmannn V.A. 1990; Phylogenetic and biochemical evidence for a secondary structure model of a small cytoplasmic RNA from Bacilli.. Eur J Biochem 192:17–24
     [Google Scholar]
  54. Struck J.C.R., Toschka H.Y., Erdmann V.A. 1988a; Nucleotide sequence of the 4·5S RNA gene from Thermus thermophilusHB8.. Nucleic Acids Res 16:9042
     [Google Scholar]
  55. Struck J.C.R., Vogel D.W., Ulbrich N., Erdmann V.A. 1988b; The Bacillus subtilis scRNA is related to the 4·5S RNA from Escherichia coli.. Nucleic Acids Res 16:2719
     [Google Scholar]
  56. Struck J.C.R., Hartmann R.K., Toschka H.Y., Erdmann V.A. 1989; Transcription and processing of Bacillus subtilis small cytoplasmic RNA.. Mol & Gen Genet 215:478–482
     [Google Scholar]
  57. Tinoco I., Borer P.N., Dengler B., Levine M.D. 1973; Improved estimation of secondary structure in ribonucleic acids.. Nat New Biol 246:40–41
     [Google Scholar]
  58. Ullu E., Weiner A.M. 1984; Human genes and pseudogenes for the 7SL RNA component of signal recognition particle.. EMBO J 3:3303–3310
     [Google Scholar]
  59. Walter P., Blobel G. 1980; Purification of a membrane-associated protein complex required for protein translocation across the endoplasmic reticulum.. Proc Natl Acad Sci USA 777112–7116
     [Google Scholar]
  60. Walter P., Blobel G. 1982; 7SL RNA small cytoplasmic RNA is an integral component of the signal recognition particle.. Nature 299:691–698
     [Google Scholar]
  61. Walter P., Lingappa V. 1986; Mechanism of protein translocation across the endoplasmic reticulum membrane.. Annu Rev Cell Biol 2:499–516
     [Google Scholar]
  62. Woese C.R. 1987; Bacterial evolution.. Microbiol Rev 51:221–271
     [Google Scholar]
  63. Zopf D., Bernstein H.D., Johnson A.E., Walter P. 1990; The methionine-rich domain of the 54 kd protein subunit of the signal recognition particle contains an RNA binding site and can be crosslinked to a signal sequence.. EMBO J 9:4511–4517
     [Google Scholar]
  64. Zucker M. 1989; Computer prediction of RNA structure.. Methods Enɀymol 180:262–288
     [Google Scholar]
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Small cytoplasmic RNA (scRNA) gene from Clostridium perfringens can replace the gene for the Bacillus subtilis scRNA in both growth and sporulation
Microbiology 141, 2965 (1995); https://doi.org/10.1099/13500872-141-11-2965
/content/journal/micro/10.1099/13500872-141-11-2965
/content/journal/micro/10.1099/13500872-141-11-2965
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