Advertisement

Photosynthesis Research

, Volume 16, Issue 1–2, pp 23–39 | Cite as

Introns in chloroplast protein-coding genes of land plants

  • Aine L. Plant
  • John C. Gray
Genes Minireview

Abstract

Several protein-coding genes from land plant chloroplasts have been shown to contain introns. The majority of these introns resemble the fungal mitochondrial group II introns due to considerable nucleotide sequence homology at their 5′ and 3′ ends and they can readily be folded to form six hairpins characteristic of the predicted secondary structure of the mitochondrial group II introns. Recently it has been demonstrated that some mitochondrial group II introns are capable of self-splicing in vitro in the absence of protein co-factors. However evidence presented in this overview suggests that this is probably not the case for chloroplast introns and that trans-acting factors are almost certainly involved in their processing reactions.

Key words

intron splice exon lariat 

Abbreviations

kop

kilobase pairs

ORF

Open Reading Frame

pre-RNA

precursor ribonucleic acid

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abelson J (1979) RNA processing and the intervening sequence problem. Ann Rev Biochem 48: 1035–1069Google Scholar
  2. Anziano PQ, Hanson DL, Mahler HR and Perlman PS (1982) Functional domains in introns: trans-acting and cis-acting regions of intron 4 of the cob gene. Cell 30: 925–932Google Scholar
  3. Been MD and Cech TR (1986) One binding site determines sequence specificity of Tetrahymena pre-rRNA self-splicing, trans-splicing, and RNA enzyme activity. Cell 47: 207–216Google Scholar
  4. Bird CR, Koller B, Auffret AD, Huttly AK, Howe CJ, Dyer TA and Gray JC (1985) The wheat chloroplast gene for CFo subunit 1 of the ATP synthase contains a large intron. EMBO J 4: 1381–1388Google Scholar
  5. Bonitz SG, Coruzzi G, Thalenfeld BE, Tzagoloff A and Macino G (1980) Assembly of the mitochondrial membrane system. Structure and nucleotide sequence of the gene coding for subunit 1 of yeast cytochrome oxidase. J Biol Chem 255: 11925–11941Google Scholar
  6. Bonnard G, Michel F, Weil JH and Steinmetz A (1984) Nucleotide sequence of the split tRNA UAA Leu gene from Vicia faba chloroplasts: evidence for structural homologies of the chloroplast tRNALeu intron with the intron from the autosplicable Tetrahymena ribosomal RNA precursor. Mol Gen Genet 194: 330–336Google Scholar
  7. Breathnach R, Mandel JL and Chambon P (1977) Ovalbumin gene is split in chicken DNA. Nature 270: 314–319Google Scholar
  8. Breathnach R, Benoist C, O'Hare K, Gannon F and Chambon P (1978) Ovalbumin gene: evidence for a leader sequence in mRNA and DNA sequences at the exon-intron boundaries. Proc Natl Acad Sci USA 75: 4853–4857Google Scholar
  9. Brody E and Abelson J (1985) The "spliceosome": yeast pre-messenger RNA associates with a 40S complex in a splicing-dependent reaction. Science 228; 963–967Google Scholar
  10. Burke JM, Irvine KD, Kaneko KJ, Kerker BJ, Oettgen AB, Tierney WM, Williamson CL, Zaug AJ and Cech TR (1986) Role of conserved sequence elements 9L and 2 in self-splicing of the Tetrahymena ribosomal RNA precursor. Cell 45: 167–176Google Scholar
  11. Carignani G, Groudinsky O, Frezza D, Schiaron E, Bergantino E and Slonimski PP (1983) An mRNA maturase is encoded by the first intron of the mitochondrial gene for the subunit 1 of cytochrome oxidase in S. cerevisiae. Cell 35: 733–742Google Scholar
  12. Cech TR (1986) The generality of self-splicing RNA: relationship to nuclear mRNA splicing. Cell 44: 207–210Google Scholar
  13. Collins RA and Lambowitz AM (1985) RNA splicing in Neurospora mitochondria. Defective splicing of mitochondrial mRNA precursors in the nuclear mutant Cyt 18–1. J Mol Biol 184: 413–428Google Scholar
  14. Davies RW, Waring RB, Ray JA, Brown TA and Scazzocchio C. (1982) Making ends meet: a model for RNA splicing in fungal mitochondria. Nature 300: 719–724Google Scholar
  15. De LaSalle H, Jacq C and Slonimski PP (1982) Critical sequences within mitochondrial introns: pleiotropic mRNA maturase and cis-dominant signals of the box intron controlling reductase and oxidase. Cell 28: 721–732Google Scholar
  16. Deno H, Kato A, Shinozaki K and Sugiura M (1982) Nucleotide sequences of tobacco chloroplast genes for elongator tRNAMet and tRNAVal (UAC): the tRNAVal (UAC) gene contains a long intron. Nucl Acids Res 10: 7511–7520Google Scholar
  17. Deno H and Sugiura M (1984) Chloroplast tRNAGly gene contains a long intron in the D stem: nucleotide sequences of tobacco chloroplast genes for tRNAGly (UCC) and tRNAArg (UCU). Proc Natl Acad Sci USA 81: 405–408Google Scholar
  18. Erickson JM, Rahire M and Rochaix JD (1984) Chlamydomonas reinhardii gene for the 32000 mol. wt. protein of photosystem II contains four large introns and is located entirely within the chloroplast inverted repeat. EMBO J 3: 2753–2762Google Scholar
  19. Frendewey D and Keller W (1985) Stepwise assembly of a pre-mRNA splicing complex requires U-snRNPs and specific intron sequences. Cell 42: 355–367Google Scholar
  20. Fromm H, Edelman M, Koller B, Goloubinoff P and Galun E (1986) The enigma of the gene coding for ribosomal protein S12 in the chloroplasts of Nicotiana. Nucl Acids Res 14: 883–898Google Scholar
  21. Fukuzawa H, Kohchi T, Shirai H, Ohyama K, Umesono K, Inokuchi H and Ozeki H (1986) Coding sequences for chloroplast ribosomal protein S12 from the liverwort, Marchantia polymorpha, are separated far apart on the different DNA strands. FEBS Lett 198: 11–15Google Scholar
  22. Fukuzawa H, Yoshida T, Kohchi T, Okumura T, Sawano Y and Ohyama K (1987) Splicing of group II introns in mRNAs coding for cytochrome b6 and subunit IV in liverwort Marchantia polymorpha chloroplast genome: exon specifying a region coding for two genes with the spacer region. FEBS Lett 220: 61–66Google Scholar
  23. Garriga G and Lambowitz AM (1984) RNA splicing in Neurospora mitochondria: self-splicing of a mitochondrial intron in vitro. Cell 39: 631–641Google Scholar
  24. Gingrich JC and Hallick RB (1985) The Euglena gracilis chloroplast ribulose-1,5-bisphosphate carboxylase gene 1. Complete DNA sequence and analysis of the nine intervening sequences. J Biol Chem 260: 16156–16116Google Scholar
  25. Grabowski PJ, Padgett RA and Sharp PA (1984) Messenger RNA splicing in vitro: an excised intervening sequence and a potential intermediate. Cell 37: 415–427Google Scholar
  26. Grabowski PJ, Seiler SR and Sharp PA (1985) A multi-component complex is involved in the splicing of messenger RNA precursors. Cell 42: 345–353Google Scholar
  27. Greenberg BM, Narita JO, DeLuca-Flaherty C, Gruissem W, Rushlow KA and Hallick RB (1984) Evidence for two RNA polymerase activities in Englena gracilis chloroplasts. J Biol Chem 259: 14880–14887Google Scholar
  28. Gruissem W, Greenberg BM, Zurawski G, Prescott DM and Hallick RB (1983) Biosynthesis of chloroplast transfer RNA in a spinach chloroplast transcription system. Cell 35: 815–828Google Scholar
  29. Guiso N, Dreyfus M, Siffert O, Danchin A, Spyridakis A, Gargouri A, Claise M and Slonimski PP (1984) Antibodies against synthetic oligopeptides allow identification of the mRNA-maturase encoded by the second intron of the yeast cob-box gene. EMBO J 3: 1769–1772Google Scholar
  30. Hallick RB, Gingrich JC, Johanningmeier U and Passavant CW (1985) Introns in Euglena and Nicotiana chloroplast protein genes. In: Vloten-Doting L, Groot GSP and Hall TC, eds. Molecular Form and Function of the Plant Genome, pp 211–220 NATO ASI series, PlenumGoogle Scholar
  31. Heinemeyer W, Alt J and Herrmann RG (1984) Nucleotide sequence of the clustered genes for apocytochrome b6 and subunit 4 of the cytochrome b/f complex in the spinach plastid genome. Curr Genet 8: 543–549Google Scholar
  32. Hennig J and Herrmann RG (1986) Chloroplast ATP synthase of spinach contains nine non-identical subunit species, six of which are encoded by plastid chromosomes in two operons in a phylogenetically conserved arrangement. Mol Gen Genet 203: 117–128Google Scholar
  33. Hudson GS, Mason JG, Holton TA, Koller B, Cox GR, Whitfeld PR and Bottomley W (1987) A gene cluster in the spinach and pea chloroplast genomes encoding one CF1 and three CFo subunits of the H+-ATP synthase complex and the ribosomal protein S2. J Mol Biol 196: 283–298Google Scholar
  34. Jacq C, Banroques J, Becam AM, Slonimski PP, Guiso N and Danchin A (1984) Antibodies against a fused ‘lacZ-yeast mitochondrial intron’ gene product allow identification of the mRNA maturase encoded by the fourth intron of the yeast cob-box gene. EMBO J 3: 1567–1572Google Scholar
  35. Jacquier A and Rosbash M (1986) Efficient trans-splicing of a yeast mitochondrial RNA group II intron implicates a strong 5′ exon-intron interaction. Science 234: 1099–1104.Google Scholar
  36. Jacquier A and Michel F (1987) Multiple exon-binding sites in class II self-splicing introns. Cell 50: 17–29Google Scholar
  37. Jeffreys AJ and Flavell RA (1977) The rabbit β-globin gene contains a large insert in the coding sequence. Cell 12: 1097–1108Google Scholar
  38. Karabin GD, Farley M and Hallick RB (1984) Chloroplast gene for M r32000 polypeptide of photosystem II in Euglena gracilis is interrupted by four introns with conserved boundary sequences. Nucl Acids Res 12: 5801–5812Google Scholar
  39. Keller M and Michel F (1985) The introns of the Euglena gracilis chloroplast gene which codes for the 32-kDa protein of photosystem II. Evidence for structural homologies with Class II introns. FEBS Lett 179: 69–73Google Scholar
  40. Koch W, Edwards K and Kossel H (1981) Sequencing of the 16S–23S spacer in a ribosomal RNA operon of Zea mays chloroplast DNA reveals two split tRNA genes. Cell 25: 203–213Google Scholar
  41. Koller B and Delius H (1984) Intervening sequences in chloroplast genomes. Cell 36: 613–622Google Scholar
  42. Koller B, Gingrich JC, Stiegler GL, Farley MA, Delius H and Hallick RB (1984) Nine introns with conserved boundary sequences in the Euglena gracilis chloroplast ribulose-1,5-bisphosphate carboxylase gene. Cell 36: 545–553Google Scholar
  43. Koller B, Fromm H, Galun E and Edelman M (1987) Evidence for in vivo trans splicing of pre-mRNAs in tobacco chloroplasts. Cell 48: 111–119Google Scholar
  44. Konarska MM, Padgett RA and Sharp PA (1985) Trans splicing of mRNA precursors in vitro. Cell 42: 165–171Google Scholar
  45. Kreike J, Schulze M, Ahne F and Lang BF (1987) A yeast nuclear gene, MRS1, involved in mitochondrial RNA splicing: nucleotide sequence and mutational analysis of two overlapping open reading frames on opposite strands. EMBO J 6: 2123–2129Google Scholar
  46. Kruger K, Grabowski PJ, Zaug AJ, Sands J, Gottschling DE and Cech TR (1982) Self splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequences of Tetrahymena. Cell 31: 147–157Google Scholar
  47. Lazowski J, Jacq C and Slonimski PP (1980) Sequence of introns and flanking exons in wild-type and box 3 mutants of cytochrome b reveals an interlaced splicing protein coded by an intron. Cell 22: 333–348Google Scholar
  48. Melton DA, Krieg PA, Rebagliatti MR, Maniatis T, Zinn K and Green ME (1984) Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucl Acids Res 12: 7035–7056Google Scholar
  49. Michel F and Dujon B (1983) Conservation of RNA secondary structures in two intron families including mitochondrial-, chloroplast-and nuclear-encoded members. EMBO J 2: 33–38Google Scholar
  50. Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H and Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322: 572–574Google Scholar
  51. Orozco EM, Mullet JE and Chua N-H (1985) An in vitro system for accurate transcription initiation of chloroplast protein genes. Nucl Acids Res 13: 1283–1302Google Scholar
  52. Padgett RA, Konarska MM, Grabowski PJ, Hardy SF and Sharp PA (1984) Lariat RNA's as intermediates and products in the splicing of messenger RNA precursors. Science 225: 898–903Google Scholar
  53. Peebles CL, Perlman PS, Mecklenburg KL, Petrillo ML, Tabor JH, Jarrell KA and Cheng H-L (1986) A self-splicing RNA excises an intron lariat. Cell 44: 213–223Google Scholar
  54. Rochaix JD and Malnoe P (1978) Anatomy of the chloroplast ribosomal DNA of Chlamydomonas reinhardii. Cell 15: 661–670Google Scholar
  55. Rochaix JD, Rahire M and Michel F (1985) The chloroplast ribosomal intron of Chlamydomonas reinhardii codes for a polypeptide related to mitochondrial maturases. Nucl Acids Res 13: 975–984Google Scholar
  56. Ruskin B, Krainer AR, Maniatis T and Green MR (1984) Excision of an intact intron as a novel lariat structure during pre-mRNA splicing in vitro. Cell 38: 317–331Google Scholar
  57. Schmelzer C, Haid A, Grosch G, Schweyen RJ and Kaudewitz F (1981) Pathways of transcript splicing in yeast mitochondria. Mutations in intervening sequences of the split gene cob reveal a requirement for intervening sequence-encoded products. J Biol Chem 256: 7610–7619Google Scholar
  58. Schmelzer C and Schweyen RJ (1986) Self-splicing of group II introns in vitro: mapping of the branch point and mutational inhibition of lariat formation. Cell 46: 557–565Google Scholar
  59. Schmelzer C, Schmidt C, May K and Schweyen RJ (1983) Determination of functional domains in intron b/1 of yeast mitochondrial RNA by studies of mitochondrial mutations and a nuclear suppressor. EMBO J 2: 2047–2052Google Scholar
  60. Shinozaki K, Deno H, Wakasugi T and Sugiura M (1986a) Tobacco chloroplast gene coding for subunit 1 of proton-translocating ATPase: comparison with the wheat subunit 1 and E. coli subunit b. Curr Genet 10: 421–423Google Scholar
  61. Shinozaki K, Deno H, Sugita M, Kuramitsu S and Sugiura M (1986b) Intron in the gene for the ribosomal protein S16 of tobacco chloroplast and its conserved boundary sequences. Mol Gen Genet 202: 1–5Google Scholar
  62. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H and Suguira M (1986c) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5: 2043–2049Google Scholar
  63. Solnick D (1985) Trans splicing of mRNA precursors. Cell 42: 157–164Google Scholar
  64. Steinmentz A, Gubbins EJ and Bogorad L (1982) The anticodon of the maize chloroplast gene for tRNAUAA leu is split by a large intron. Nucl Acid Res 10: 3027–3037Google Scholar
  65. Torazawa K, Hayashida N, Obokata J, Shinozaki K and Sugiura M (1986) The 5′ part of the gene for ribosomal protein S12 is located 30 kbp down-stream from its 3′ part in tobacco chloroplast genome. Nucl Acids Res 14: 3143Google Scholar
  66. Van DerHorst G and Tabak HF (1985) Self-splicing of yeast mitochondrial ribosomal and messenger RNA precursors. Cell 40: 759–766Google Scholar
  67. Van DerVeen R, Arnberg AC, Van DerHorst G, Bonen L, Tabak HF and Grivell LA (1986) Excised group II introns in yeast mitochondria are lariats and can be formed by self-splicing in vitro. Cell 44: 225–234Google Scholar
  68. Van DerVeen R, Arnberg AC and Grivell LA (1987) Self-splicing of a group II intron in yeast mitochondria: dependence on 5′ exon sequences. EMBO J 6: 1079–1084Google Scholar
  69. Wallace JC and Edmonds M (1983) Polyadenylated nuclear RNA contains branches. Proc Natl Acad Sci USA 80: 950–954Google Scholar
  70. Waring RB, Towner P, Minter SJ and Davies RW (1986) Splice-site selection by a self-splicing RNA of Tetrahymena. Nature 321: 133–139Google Scholar
  71. Weiss-Brummer B, Rodel G, Schweyen RJ and Kaudewitz F (1982) Expression of the split gene cob in yeast: evidence for a precursor of a "maturase" protein translated from intron 4 and preceding exon. Cell 29: 527–536Google Scholar
  72. Westhoff P, Farchaus JW and Herrmann RG (1986) The gene for the M r10,000 phosphoprotein associated with photosystem II is part of the psb B operon of the spinach plastid chromosome. Curr Genet 11: 165–169Google Scholar
  73. Zaita N, Torazawa K, Shinozaki K and Suguira M (1987) Trans-splicing in vivo: joining of transcripts from the ‘divided’ gene for ribosomal protein S12 in the chloroplasts of tobacco. FEBS Lett 210: 153–156Google Scholar
  74. Zurawski G, Bottomley W and Whitfeld PR (1984) Junctions of the large single copy region and the inverted repeats in Spinacia oleracea and Nicotiana debneyi chloroplast DNA: sequence of the genes for tRNAHis and the ribosomal proteins S19 and L2. Nucl Acids Res 12: 6547–6558Google Scholar

Copyright information

© Kluwer Academic Publishers 1988

Authors and Affiliations

  • Aine L. Plant
    • 1
  • John C. Gray
    • 1
  1. 1.Botany SchoolUniversity of CambridgeCambridgeUK

Personalised recommendations