Summary
The chloroplast genomes of Chlamydomonas spp. contain introns that belong to the two major classes found in organelles: group I and group II. Some of the members of both classes are ribozymes capable of self-splicing in vitro and, indeed, most of the group I introns studied in Chlamydomonas spp. are autocatalyic. The biochemical characterization of these introns suggests that, in vivo, their splicing must be dependent on protein factors. It is particularly interesting in this respect that light regulates the splicing of the four group I introns in the psbA gene of C. reinhardtii. The two group II introns of the psaA gene are split into two or more pieces which are transcribed separately from different chloroplast loci. The mature psaA RNA is assembled from the separate precursors in two steps of intermolecular trans-splicing. There are many nuclear mutants defective in psaA mRNA maturation, which identify a large number of protein factors that are required, directly or indirectly, for trans-splicing.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
Abbreviations
- LSU:
-
large subunit ribosomal RNA
- ORF:
-
open reading frame
References
Bao Y (1993) Studies of a self-splicing group I ribozyme in the chloroplast psbA gene of Chlamydomonas reinhardtii. PhD Dissertation, University of Texas at Austin
Bao Y and Herrin DL (1993) Nucleotide sequence and secondary structure of the chloroplast group I intron Cr.psbA-2: Novel features of this self-splicing ribozyme. Nucleic Acids Res 21:1667
Bass B and Cech TR (1984) Specific interaction between the self-splicing RNA of Tetrahymena and its guanosine substrate: Implications for biological catalysis by RNA. Nature 308: 820–826
Bonen L (1993) Trans-splicing of pre-mRNA in plants, animals and protists. FASEB J 7:40–46
Cech TR (1990) Self-splicing of group I introns. Annu Rev Biochem 59: 543–568
Cech TR, Damberger SH and Gutell RR (1994) Representation of the secondary and tertiary structure of group I introns. Nature Struct Biol 1:273–280
Choquet Y, Goldschmidt-Clermont M, Girard-Bascou J, KĂ¼ck U, Bennoun P and Rochaix J-D (1988) Mutant phenotypes support a trans-splicing mechanism for the expression of the tripartite psaA gene in the C. reinhardtii chloroplast. Cell 52: 903–913
Costa M, Dème E, Jacquier A and Michel F (1997) Multiple tertiary interactions involving domain II of group II self-splicing introns. J Mol Biol 267:520–536
Côté M-J and Tunnel, M (1995) In vitro self-splicing reactions of chloroplast and mitochondrial group-1 introns in Chlamydomonas eugametos and Chlamydomonas moewusii. Curr Genet 27:177–183.
Côté V, Mercier J-P, Lemieux C and Turmel M (1993) The single group I intron in the chloroplast rrnL gene of Chlamydomonas humicola encodes a site-specific DNA endonuclease. Gene 129:69–76
Curcio MJ and Belfort M (1996) Retrohoming: cDNA-mediated mobility of group II introns requires a catalytic RNA. Cell 84:9–12
DarĂ²s J and Flores R (1996) A group I plant intron accumulates as circular RNA forms with extensive 5′ deletions in vivo. RNA 2:928–936
Deshpande NN, Hollingsworth M and Herrin DL (1995) The atpF group-I I intron-containing gene from spinach chloroplasts is not spliced in transgenic Chlamydomonas chloroplasts. Curr Genet 28:122–127
Deshpande NN, Bao Y and Herrin DL (1997) Evidence for light/redox regulated splicing of the psbA introns in Chlamydomonas chloroplasts. RNA 3:37–48
Dujon B (1989) Group I introns as mobile genetic elements: Facts and mechanistic speculations—a review. Gene 82:91–114
Durocher V, Gauthier A, Bellemare G and Lemieux C (1989) An optional group I intron between the chloroplast small subunit rRNA genes of Chlamydomonas moewusii and C. eugametos. Curr Genet 15: 277–82
DĂ¼rrenberger F and Rochaix J-D (1991) Chloroplast ribosomal intron of Chlamydomonas reinhardtii: In vitro self-splicing, DNA endonuclease activity and in vivo mobility. EMBO J 10: 3495–3501
Gampel A and Tzagoloff A (1987) In vitro splicing of the terminal intervening sequence of Saccharomyces cerevisiae cytochrome b pre-mRNA. Mol Cell Biol 7: 2545–2551
Gampel A, Nishikimi M and Tzagoloff A (1989) CBP2 protein promotes in vitro excision of a yeast mitochondrial group I intron. Mol Cell Biol 9: 5424–5433
Gauthier A, Turmel M and Lemieux C (1991) A Group I intron in the chloroplast large subunit rRNA gene of Chlamydomonas eugametos encodes a double-strand endonuclease that cleaves the homing site of this intron. Curr Genet 19: 43–47
Goldschmidt Clermont M, Girard Bascou J, Choquet Y and Rochaix JD (1990) Trans-splicing mutants of Chlamydomonas reinhardtii. Mol Gen Genet 223: 417–25
Goldschmidt-Clermont M, Choquet Y, Girard-Bascou J, Michel F, Schirmer-Rahire M and Rochaix J-D (1991) A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell 65: 135–143
Grivell LA (1996) Transposition: Mobile introns get into line. Curr Biol 6: 48–51
Guo Q and Lambowitz A (1992) A tyrosyl-tRNA synthetase binds specifically to the Group I intron catalytic core. Genes Dev 6: 1357–1372
Harris EH (1989) The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use. Academic Press, San Diego
Harris EH, Boynton JE and Gillham NW (1974) Chloroplast ribosome biogenesis in Chlamydomonas. Selection and characterization of mutants blocked in ribosome formation. J Cell Biol 63: 160–179
Herdenberger F, Holländer B and KĂ¼ck U (1994) Correct in vivo RNA splicing of a mitochondrial intron in algal chloroplasts. Nucleic Acids Res 22: 2869–2875
Herrin D and Michaels A (1984) Gene Expression during the Cell Cycle of Chlamydomonas reinhardtii. In: Stein G and Stein J (eds) Recombinant DNA and Cell Proliferation, pp 87–106. Academic Press, Orlando
Herrin DL and Schmidt GW (1988) trans-Splicing of transcripts for the chloroplast psaA gene. In vivo requirement for nuclear gene products. J Biol Chem 263: 14601–14604
Herrin DL, Michaels AS and Paul A-P (1986) Regulation of genes encoding the large subunit of ribulose-1,5-bisphosphate carboxylase and the photosystem II polypeptides D-1 and D-2 during the cell cycle of Chlamydomomas reinhardtii. J Cell Biol 103: 1837–1845
Herrin DL, Chen Y-F and Schmidt GW (1990) RNA splicing in Chlamydomonas chloroplasts: Self-splicing of 23S preRNA. J Biol Chem 265: 21134–21140
Herrin DL, Bao Y, Thompson AJ and Chen Y-F (1991) Self-splicing of the Chlamydomonas chloroplast psbA introns. Plant Cell 3: 1095–1107
Hetzer M, Schweyen RJ and Mueller MW (1997) DNA polymerization catalysed by a group II intron RNA in vivo. Nucleic Acids Res 25: 825–1829
Jaeger L, Michel F and Westhof E (1996) The structure of group I ribozymes. In: Eckstein F and Lilley DMJ (eds) Nucleic Acids and Molecular Biology, Vol 10, pp 33–52. Springer-Verlag, Berlin
Jacquier A (1996) Group II introns: Elaborate ribozymes. Biochimie 78: 474–487
Jenkins BD, Kulhanek DJ and Barkan AB (1997) Nuclear mutations that block group II RNA splicing in maize chloroplasts reveal several intron classes with distinct requirements for splicing factors. Plant Cell 9: 283–296
KĂ¼ck U, Choquet Y, Schneider M, Dron M and Bennoun P (1987) Structural and transcriptional analysis of two homologous genes for the P700 chlorophyll a apoproteins in Chlamydomonas reinhardtii: Evidence for trans-splicing. EMBO J 6: 2185–2195
KĂ¼ck U, Godehardt I and Schmidt U (1990) A self-splicing group II intron in the mitochondrial large subunit rRNA (LSUrRNA) gene of the eukaryotic alga Scenedesmus obliquus. Nucleic Acids Res 18: 2691–2697
Laird PW (1989) Trans-splicing in trypanosomes—archaism or adaptation? Trends Genet 5: 204–216
Liu X-Q, Gillham NW and Boynton JE (1989) Chloroplast ribosomal protein gene rps12 of Chlamydomonas reinhardtii. J Biol Chem 27: 16100–16108
Michel F and Dujon B (1983) Conservation of secondary structures in two intron families including mitochondrial-, chloroplast-and nuclear-encoded members. EMBO J 2: 33–38
Michel F and Ferat J-L (1995) Structure and activities of group II introns. Annu Rev Biochem 64: 435–461
Michel F and Westhof E (1990) Modelling of the three-dimensional architecture of Group I catalytic introns based on comparative sequence analysis. J Mol Biol 216: 585–610
Michel F, Umesono K and Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns—a review. Gene 82: 5–30
Mohr G, Zhang A, Gianelos J, Belfort M and Lambowitz A (1992) The Neurospora cyt-18 protein suppresses defects in the phage T4 td intron by stabilizing the catalytically active structure of the intron core. Cell 69: 483–494
Mueller MW, Hetzer M and Schweyen RJ (1993) Group II intron RNA catalysis of progressive nucleotide insertion: A model for RNA editing. Science 261: 1035–1038
Plant AL and Gray JC (1988) Introns in chloroplast protein-coding genes of land plants. Photosynth Res 16: 23–39
Rochaix J-D (1996) Post-transcriptional regulation of chloroplast gene expression in Chlamydomonas reinhardtii. Plant Mol Biol 32: 327–341
Rochaix J-D, Rahire M and Michel F (1985) The chloroplast ribosomal intron of Chlamydomonas reinhardtii codes for a polypeptide related to mitochondrial maturases. Nucleic Acids Res 13: 975–984
Roitgrund C and Mets LJ (1990) Localization of two novel chloroplast genome functions: Trans-splicing of RNA and protochlorophyllide reduction. Curr Genet 17: 147–153
Saldanha R, Mohr G, Belfort M and Lambowitz A (1993) Group I and Group II introns. FASEB J 7: 15–24
Shaw LC and Lewin AS (1995) Protein induced folding of a Group 1 intron in Cytochrome b pre-mRNA. J Biol Chem 270: 21552–21562
Thompson AJ and Herrin DL (1991) In vitro self-splicing reactions of the chloroplast Group I intron Cr.LSU from Chlamydomonas reinhardtii and in vivo manipulation via gene replacement. Nucleic Acids Res 19: 6611–6618
Thompson AJ and Herrin DL (1994) A chloroplast group I intron undergoes the first step of reverse splicing into host 5.8S rRNA: Implications for intron-mediated RNA recombination, intron transposition and 5.8S rRNA structure. J Mol Biol 236: 455–468
Thompson AJ, Yuan X, Kudlicki W and Herrin DL (1992) Cleavage and recognition pattern of a double-strand-specific endonuclease (l-Crel) encoded by the chloroplast 23S rRNA intron of Chlamydomonas reinhardtii. Gene 119: 247–251
Tunnel M, Boulanger J and Lemieux C (1989) Two group I introns with long internal open reading frames in the chloroplast psbA gene of Chlamydomonas moewusii. Nucleic Acids Res 17:3875–87
Turmel M, Boulanger J, Schnare MN, Gray MW and Lemieux C (1991) 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 218: 293–311
Turmel M, Gutell RR, Mercier JP, Otis C and Lemieux C (1993a) Analysis of the chloroplast large subunit ribosomal RNA gene from 17 Chlamydomonas taxa. Three internal transcribed spacers and 12 group I intron insertion sites. J Mol Biol 232: 446–467
Turmel M, Mercier J-P and Côté M-J (1993b) Group I introns interrupt the chloroplast psaB and psbC genes in Chlamydomonas. Nucleic Acids Res 21: 5242–5250
Turmel M, Choquet Y, Goldschmidt-Clermont, Rochaix J-D, Otis C and Lemieux C (1995a) The trans-spliced intron 1 in the psaA gene of the Chlamydomonas chloroplast: A comparative analysis. Curr Genet 27: 270–279
Turmel M, Côté V, Otis C, Mercier J-P, Gray MW, Lonergan KM, and Lemieux C (1995b) Evolutionary transfer of ORF-containing group I introns between different subcellular compartments (chloroplast and mitochondria). Mol Biol Evol 12: 533–45
Turmel M, Mercier J-P, Côté V, Otis C and Lemieux C (1995c) The site-specific DNA endonuclease encoded by a group I intron in the Chlamydomonas pallidostigmatica chloroplast small subunit rRNA gene introduces a single-strand break at low concentrations of Ma2+. Nucleic Acids Res 23: 2519–2525
Weeks KM and Cech TR (1995) Protein facilitation of group I intron splicing by assembly of the catalytic core and the 5′ splice site domain. Cell 82: 221–230
Woodson SA and Cech TR (1989) Reverse self-splicing of the Tetrahymena group I intron: Implication for the directionality of splicing and for intron transposition. Cell 57: 335–345.
Zimmerly S, Guo H, Eskes R, Yang J, Perlman PS and Lambowitz AM (1995) A group II intron RNA is a catalytic component of a DNA endonuclease involved in intron mobility. Cell 83: 529–538
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1998 Kluwer Academic Publishers
About this chapter
Cite this chapter
Herrin, D.L., Kuo, TC., Goldschmidt-Clermont, M. (1998). RNA Splicing in the Chloroplast. In: Rochaix, J.D., Goldschmidt-Clermont, M., Merchant, S. (eds) The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Advances in Photosynthesis and Respiration, vol 7. Springer, Dordrecht. https://doi.org/10.1007/0-306-48204-5_11
Download citation
DOI: https://doi.org/10.1007/0-306-48204-5_11
Publisher Name: Springer, Dordrecht
Print ISBN: 978-0-7923-5174-0
Online ISBN: 978-0-306-48204-5
eBook Packages: Springer Book Archive