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The trans-spliced intron 1 in the psaA gene of the Chlamydomonas chloroplast: a comparative analysis

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Abstract

In the secondary structure model that has been proposed for the trans-spliced intron 1 in the Chlamydomonas reinhardtii psaA gene, a third RNA species (tscA RNA) interacts with the 5′ and 3′ intron parts flanking the exons to reconstitute a composite structure with several features of group-II introns. To test the validity of this model, we undertook the sequencing and modelling of equivalent introns in the psaA gene from other unicellular green algae belonging to the highly diversified genus Chlamydomonas. Our comparative analysis supports the model reported for the C. reinhardtii psaA intron 1, and also indicates that the 5′ end of the tscA RNA and the region downstream from the psaA exon 1 cannot be folded into a structure typical of domain I as described for most group-II introns. It is possible that a fourth RNA species, yet to be discovered, provides the parts of domain I which are apparently missing.

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References

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA Struhl K (1990) Current protocols in molecular biology. J Wiley and Sons, New York

    Google Scholar 

  • Binder S, Marchfelder A, Brennicke A, Wissinger B (1992) RNA editing in trans-splicing intron sequences of nad2 mRNAs in Oenothera mitochondria. J Biol Chem 276:7615–7623

    Google Scholar 

  • Bonen L (1993) Trans-splicing of pre-mRNA in plants, animals, and protists. FASEB J 7:40–46

    Google Scholar 

  • Boudreau E, Otis C, Turmel M (1994) Conserved gene clusters in the highly rearranged chloroplast genomes of Chlamydomonas moewusii and Chlamydomonas reinhardtii. Plant Mol Biol 24: 585–602

    Google Scholar 

  • Boynton JE, Gillham NW, Harris EH, Hosler JP, Johnson AM, Jones AR, Randolph-Anderson BL, Robertson D, Klein TM, Shark KB, Sanford JC (1988) Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science 240:1534–1538

    Google Scholar 

  • Buchheim MA, Turmel M, Zimmer EA, Chapman RL (1990) Phylogen of Chlamydomonas (Chlorophyta) based on cladistic analysis of nuclear 18S rRNA sequence data. J Phycol 26:689–699

    Google Scholar 

  • Chapdelaine Y, Bonen L (1991) The wheat mitochondrial gene for subunit I of the NADH dehydrogenase complex: a trans-splicing model for this gene-in-pieces. Cell 65:465–472

    Google Scholar 

  • Choquet Y, Goldschmidt-Clermont M, Girard-Bascou J, Kück U, Bennoun P, 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

    Google Scholar 

  • Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395

    Google Scholar 

  • Erickson JM, Rahire M, Rochaix J-D (1984) Chlamydomonas reinhardtii gene for the 32 000 mol. wt. protein of photosystem II contains four large introns and is located entirely within the chloroplast inverted repeat. EMBO J 3:2753–2762

    Google Scholar 

  • Ferat J-L, Michel F (1993) Group-II self-splicing introns in bacteria. Nature 364:358–361

    Google Scholar 

  • Fukuzawa H, Kohchi T, Shirai H, Ohyama K, Umesono K, Inokuchi H, Ozeki H (1986) Coding sequences for chloroplast ribosomal protein S12 from liverwort, Marchantia polymorpha, are separated far apart on different DNA strands. FEBS Lett 198:11–15

    Google Scholar 

  • Goldschmidt-Clermont M, Girard-Bascou J, Choquet Y, Rochaix J-D (1990) Trans-splicing mutants of Chlamydomonas reinhardtii. Mol Gen Genet 223:417–425

    Google Scholar 

  • Goldschmidt-Clermont M, Choquet Y, Girard-Bascou J, Michel M, Schirmer-Rahire M, Rochaix J-D (1991) A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell 65:135–143

    Google Scholar 

  • Hallick RB, Hong L, Drager RG, Favreau MR, Monfort A, Orsat B, Spielmann A, Stutz E (1993) Complete sequence of Euglena gracilis chloroplast DNA. Nucleic Acids Res 21:3537–3544

    Google Scholar 

  • Herrin DL, Schmidt GW (1988) Trans-splicing of transcripts for the chloroplast psaA1 gene. J Biol Chem 263:14601–14604

    Google Scholar 

  • Higgins DG, Sharp PM (1988) CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 79: 237–244

    Google Scholar 

  • Jacquier A (1990) Self-splicing group-II and nuclear pre-mRNA introns: how similar are they? Trends Biochem Sci 15:351–354

    Google Scholar 

  • Knoop V, Schuster W, Wissinger B, Brennicke A (1991) Trans splicing integrates an exon of 22 nucleotides into the nad5 mRNA in higher plant mitochondria. EMBO J 10:3483–3493

    Google Scholar 

  • Kohchi T, Umesono K, Ogura Y, Komine Y, Nakahigashi K, Komano T, Yamada Y, Ozeki H, Ohyama K (1988a) A nicked group-II intron and trans-splicing in liverwort, Marchantia polymorpha, chloroplasts. Nucleic Acids Res 16:10025–10036

    Google Scholar 

  • Kohchi T, Ogura Y, Umesono K, Yamada Y, Komano T, Ozeki H, Ohyama K (1988b) Ordered processing and splicing in a polycistronic transcript in liverwort chloroplasts. Curr Genet 14: 147–154

    Google Scholar 

  • Koller B, Fromm H, Galun E, Edelman M (1987) Evidence for in vivo trans-splicing of pre-mRNAs in tobacco chloroplasts. Cell 48:111–119

    Google Scholar 

  • Kück U, Choquet Y, Schneider M, Dron M, Bennoun P (1987) Structural and transcription analysis of two homologous genes for the P700 chlorophyll a-apoproteins in Chlamydomonas reinhardtii: evidence for in vivo trans-splicing. EMBO J 8:2185–2195

    Google Scholar 

  • Maxam AM, Gilbert W (1980) Sequencing end-labelled DNA with base-specific chemical cleavages. Methods Enzymol 65:499–560

    Google Scholar 

  • Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group-II catalytic introns — a review. Gene 82:5–30

    Google Scholar 

  • Muramatsu T, Nishikawa K, Nemoto F, Kuchino Y, Nishimura S, Miyazawa T, Yokoyama S (1988) Codon and amino-acid specificities of a transfer RNA are both converted by a single posttranscriptional modification. Nature 336:179–181

    Google Scholar 

  • Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha. Nature 322:572–574

    Google Scholar 

  • Rochaix J-D (1992) Post-transcriptional steps in the expression of chloroplast genes. Annu Rev Cell Biol 8:1–28

    Google Scholar 

  • Roitgrund C, Mets LJ (1990) Localization of two novel chloroplast genome functions: trans-splicing of RNA and protochlorophylide reduction. Curr Genet 17:147–153

    Google Scholar 

  • Saldanha R, Mohr G, Belfort M, Lambowitz A (1993) Group-I and group-II introns. FASEB J 7:15–24

    Google Scholar 

  • Sambrook J, Fritch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

  • Sharp PA (1991) “Five easy pieces”. Science 254:663

    Google Scholar 

  • Turmel M, Lemieux B, Lemieux C (1988) The chloroplast genome of the green alga Chlamydomonas moewusii: localization of protein-coding genes and transcriptionally active regions. Mol Gen Genet 214:412–419

    Google Scholar 

  • Turmel M, Gutell RR, Mercier J-P, Otis C, 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

    Google Scholar 

  • Turmel M, Mercier J-P, Côté M-J (1993b) Group-I introns interrupt the chloroplast psaB and psbC and the mitochondrial rrnL gene in Chlamydomonas. Nucleic Acids Res 21:5242–5250

    Google Scholar 

  • Wissinger B, Schuster W, Brennicke A (1991) Trans splicing in Oenothera mitochondria: nad1 mRNAs are edited in exon and trans-splicing group-II intron sequences. Cell 65:473–482

    Google Scholar 

  • Woessner JP, Gillham NW, Boynton JE (1986) The sequence of the chloroplast atpB gene and its flanking regions in Chlamydomonas reinhardtii. Gene 44:17–28

    Google Scholar 

  • Zaita N, Torazawa K, Shinozaki K, Sugiura M (1987) Trans-splicing in vivo: joining of transcripts from the “divided” gene for ribosomal protein S12 in the chloroplasts of tobacco. FEBS Lett 210:153–156

    Google Scholar 

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Communicated by R.W. Lee

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Turmel, M., Choquet, Y., Goldschmidt-Clermont, M. et al. The trans-spliced intron 1 in the psaA gene of the Chlamydomonas chloroplast: a comparative analysis. Curr Genet 27, 270–279 (1995). https://doi.org/10.1007/BF00326160

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  • DOI: https://doi.org/10.1007/BF00326160

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