Home LiteratureArticle Details
PMID: 16453848 Published · ppublish English Journal Article

Novel mechanisms for maturation of chloroplast transfer RNA precursors.

The EMBO journal ·Vol. 7 ·No. 6 ·1988-06-00 ·Pages 1567-74

Wang MJ, Davis NW, Gegenheimer P

Abstract

Despite the prokaryotic origins of chloroplasts, a plant chloroplast tRNA precursor is processed in a homologous in vitro system by a pathway distinct from that observed in Escherichia coli, but identical to that utilized for maturation of nuclear pre-tRNAs. The mature tRNA 5' terminus is generated by the site-specific endonucleolytic cleavage of an RNase P (or P-type) activity. The 3' end is likewise produced by a single precise endonucleolytic cut at the 3' terminus of the encoded tRNA domain. This is the first complete structural characterization of an organellar tRNA processing system using a homologous substrate. In contrast to eubacterial RNase P, chloroplast RNase P does not appear to contain an RNA subunit. The chloroplast activity bands with bulk protein at 1.28 g/ml in CsCI density gradients, whereas E.coli RNase P bands as ribonucleoprotein at 1.73 g/ml. Chloroplast RNase P activity survives treatment with micrococcal nuclease (MN) at levels 10- to 100-fold higher than those required to totally inactivate the E.coli enzyme. The chloroplast system is sensitive to a suppression of tRNA processing, caused by binding of inactive MN to pre-tRNA substrate, which is readily overcome by addition of carrier RNA to the assay.

Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Wang M J
Department of Biochemistry, University of Kansas, Lawrence, KS 66045, USA.
Davis N W
Gegenheimer P
References (51)
51 references, click to expand
  1. Conservation of genes and their organization in the chromosomal replication origin region of Bacillus subtilis and Escherichia coli.
    EMBO J. 1985 Dec 1;4(12):3345-50 PMID: 3004954
  2. A small nuclear ribonucleoprotein associates with the AAUAAA polyadenylation signal in vitro.
    Cell. 1986 May 23;45(4):581-91 PMID: 2423249
  3. Supercoil sequencing: a fast and simple method for sequencing plasmid DNA.
    DNA. 1985 Apr;4(2):165-70 PMID: 3996185
  4. Nucleotide sequences of five maize chloroplast transfer RNA genes and their flanking regions.
    J Biol Chem. 1983 May 10;258(9):5503-11 PMID: 6853530
  5. Two RNA species co-purify with RNase P from the fission yeast Schizosaccharomyces pombe.
    EMBO J. 1986 Jul;5(7):1697-703 PMID: 3743551
  6. Apparent involvement of ribonuclease D in the 3' processing of tRNA precursors.
    Proc Natl Acad Sci U S A. 1980 Feb;77(2):837-41 PMID: 6153805
  7. Purification and characterization of an endonuclease from Xenopus laevis ovaries which accurately processes the 3' terminus of human pre-tRNA-Met(i) (3' pre-tRNase).
    J Biol Chem. 1985 Jul 25;260(15):9002-8 PMID: 3848432
  8. An RNA ligase from wheat germ which participates in transfer RNA splicing in vitro.
    J Biol Chem. 1983 Jul 10;258(13):8365-73 PMID: 6863293
  9. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme.
    Cell. 1983 Dec;35(3 Pt 2):849-57 PMID: 6197186
  10. Structure and organization of genes for transfer ribonucleic acid in Bacillus subtilis.
    Microbiol Rev. 1985 Mar;49(1):71-80 PMID: 2580221
  11. The primary transcription product of a silkworm alanine tRNA gene: identification of in vitro sites of initiation, termination and processing.
    Cell. 1979 Dec;18(4):1217-29 PMID: 519766
  12. Processing of tRNA in prokaryotes and eukaryotes.
    CRC Crit Rev Biochem. 1984;17(1):45-71 PMID: 6094100
  13. In vitro synthesis of transfer RNA. II. Identification of required enzymatic activities.
    J Biol Chem. 1975 Aug 25;250(16):6248-55 PMID: 1099090
  14. Dimeric transfer RNA precursors in S. pombe.
    Cell. 1980 Sep;21(2):509-16 PMID: 7407924
  15. Eukaryotic pre-tRNA 5' processing nuclease: copurification with a complex cylindrical particle.
    Cell. 1986 Aug 1;46(3):377-85 PMID: 3637121
  16. The RNA component of the Bacillus subtilis RNase P. Sequence, activity, and partial secondary structure.
    J Biol Chem. 1986 Jun 15;261(17):7888-93 PMID: 2423526
  17. Bacterial evolution.
    Microbiol Rev. 1987 Jun;51(2):221-71 PMID: 2439888
  18. Processing of procaryotic ribonucleic acid.
    Microbiol Rev. 1981 Dec;45(4):502-41 PMID: 6173734
  19. Nucleotide sequence of the gene encoding the RNA subunit (M1 RNA) of ribonuclease P from Escherichia coli.
    Cell. 1982 Sep;30(2):627-36 PMID: 6183002
  20. Has the endosymbiont hypothesis been proven?
    Microbiol Rev. 1982 Mar;46(1):1-42 PMID: 6178009
  21. RNase P activity in the mitochondria of Saccharomyces cerevisiae depends on both mitochondrion and nucleus-encoded components.
    Mol Cell Biol. 1986 Apr;6(4):1058-64 PMID: 3537697
  22. Biosynthesis of chloroplast transfer RNA in a spinach chloroplast transcription system.
    Cell. 1983 Dec;35(3 Pt 2):815-28 PMID: 6652686
  23. Characterization of an RNase P activity from HeLa cell mitochondria. Comparison with the cytosol RNase P activity.
    J Biol Chem. 1985 May 25;260(10):5942-9 PMID: 2581945
  24. DNA sequence of a T4 transfer RNA gene cluster.
    J Mol Biol. 1980 May 25;139(3):377-91 PMID: 6255163
  25. 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. 1979 Jul 10;254(13):5802-16 PMID: 109442
  26. Partial purification of RNase P from Schizosaccharomyces pombe.
    J Biol Chem. 1981 May 25;256(10):5058-63 PMID: 6262315
  27. Purification and properties of a specific Escherichia coli ribonuclease which cleaves a tyrosine transfer ribonucleic acid presursor.
    J Biol Chem. 1972 Aug 25;247(16):5243-51 PMID: 4560501
  28. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression.
    EMBO J. 1986 Sep;5(9):2043-2049 PMID: 16453699
  29. The secondary structure of ribonuclease P RNA, the catalytic element of a ribonucleoprotein enzyme.
    Cell. 1988 Jan 15;52(1):19-26 PMID: 2449969
  30. Processing of precursor tRNAs in Drosophila. Processing of the 3' end involves an endonucleolytic cleavage and occurs after 5' end maturation.
    J Biol Chem. 1985 Jan 10;260(1):449-54 PMID: 3843841
  31. Veal heart ribonuclease P has an essential RNA component.
    Biochem Biophys Res Commun. 1980 Sep 30;96(2):831-7 PMID: 6158945
  32. Role of the protein moiety of ribonuclease P, a ribonucleoprotein enzyme.
    Science. 1988 Jan 8;239(4836):178-81 PMID: 3122322
  33. Structural alterations in mutant precursors of the yeast tRNALeu3 gene which behave as defective substrates for a highly purified splicing endoribonuclease.
    EMBO J. 1985 Dec 1;4(12):3289-97 PMID: 3937725
  34. Heterologous enzyme function in Escherichia coli and the selection of genes encoding the catalytic RNA subunit of RNase P.
    Proc Natl Acad Sci U S A. 1987 Oct;84(19):6825-9 PMID: 2443911
  35. The synthesis of infectious RNA with a replicase purified according to its size and density.
    Proc Natl Acad Sci U S A. 1966 Jun;55(6):1608-15 PMID: 5227679
  36. Requirements for accurate and efficient mRNA 3' end cleavage and polyadenylation of a simian virus 40 early pre-RNA in vitro.
    Mol Cell Biol. 1987 Jan;7(1):495-503 PMID: 3031477
  37. Separation and characterization of 5'- and 3'-tRNA processing nucleases from rat liver mitochondria.
    J Biol Chem. 1987 Jul 25;262(21):10272-9 PMID: 3301831
  38. Nucleolytic processing of ribonucleic acid transcripts in procaryotes.
    Microbiol Rev. 1986 Dec;50(4):428-51 PMID: 2432388
  39. Transcription of a cloned Bombyx mori tRNA2Ala gene: nucleotide sequence of the tRNA precursor and its processing in vitro.
    Cell. 1979 Nov;18(3):817-28 PMID: 260697
  40. A subpopulation of spinach chloroplast tRNA genes does not require upstream promoter elements for transcription.
    Nucleic Acids Res. 1986 Oct 10;14(19):7541-56 PMID: 3774537
  41. E. coli RNAase P has a required RNA component.
    Cell. 1980 Apr;19(4):881-7 PMID: 6155215
  42. Structure and organization of the transfer ribonucleic acid genes of Escherichia coli K-12.
    Microbiol Rev. 1985 Dec;49(4):379-97 PMID: 2419743
  43. Electronic fingerprinting of RNA.
    Nucleic Acids Res. 1988 Mar 11;16(5):1799-800 PMID: 2451220
  44. Nucleolytic processing of a tRNAArg-tRNAAsp dimeric precursor by a homologous component from Saccharomyces cerevisiae.
    J Biol Chem. 1985 Jan 25;260(2):1271-9 PMID: 2981839
  45. RNase P of Bacillus subtilis has a RNA component.
    J Biol Chem. 1980 Aug 25;255(16):7507-9 PMID: 6156938
  46. Structural characterization and in vitro processing of Escherichia coli ribosomal RNA transcripts containing 5- triphosphates, leader sequences, 16 S rRNA, and spacer tRNAs.
    J Mol Biol. 1980 Nov 5;143(3):227-57 PMID: 6163863
  47. Reconstitution of RNAase P activity using inactive subunits from E. coli and HeLa cells.
    Cell. 1986 Jan 31;44(2):243-9 PMID: 2417727
  48. Ribonuclease P: an enzyme with an essential RNA component.
    Proc Natl Acad Sci U S A. 1978 Aug;75(8):3717-21 PMID: 358197
  49. Chloroplast gene expression and promoter identification in chloroplast extracts.
    Methods Enzymol. 1986;118:253-70 PMID: 2419734
  50. Ion dependence of the Bacillus subtilis RNase P reaction.
    J Biol Chem. 1985 May 10;260(9):5415-9 PMID: 3921545
  51. In vitro transcription of chloroplast protein genes.
    Methods Enzymol. 1986;118:232-53 PMID: 2419733
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1988-06-00
Pages
1567-74
Language
English
Region
England
NLM ID
8208664
PMCID
PMC457138
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]