Abstract
Analysis of RNA maturation in ribosome-deficient plastids of four non-allelic barley mutants revealed an increased accumulation and altered processing of transcripts of the ribosomal protein gene CS12 (rps12) compared to normal chloroplasts. The three exons of rps12 are part of two different polycistronic transcription units. Generation of mature rps12-mRNA involves both cis-and trans-splicing. In ribosome-deficient plastids, the cis-intron separating exons 2 and 3 remains entirely unspliced whereas the splicing of the bipartite rps12 trans-intron between exon 1 and exon 2 occurs, but at a reduced level. A comparison of the 3′ and 5′ ends of the two RNAs that are generally assumed to interact during trans-splicing showed a difference in the processing pathways of 3′ rps12 transcripts between mutated and normal chloroplasts. Nonetheless, the final products were identical.
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Adams CC, Stern DB: Control of mRNA stability in chloroplasts by 3′ inverted repeats: effects of stem and loop mutations on degradation of psbA mRNA in vitro. Nucl Acids Res 18: 6003–6010 (1990).
Apirion D, Miczak A: RNA processing in procaryotic cells. Bioessays 15: 113–120 (1993).
Arnason TJ, Walker GWR: An irreversible gene-induced plastid mutation. Can J Res 27C: 172–178 (1949).
Attardi G, Schatz G: Biogenesis of mitochondria. Annu Rev Cell Biol 4: 289–333 (1988).
Banta AB, Haas ES, Brown JW, Pace NR: Sequence of the ribonuclease P RNA gene from the cyanobacterium Anacystis nidulans. Nucl Acids Res 20: 911 (1992).
Barkan A, Walker M, Nolasco M, Johnson D: A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms. EMBO J 13: 3170–3181 (1994).
Barkan A: Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell 5: 389–402 (1993).
Barkan A: Proteins encoded by a complex chloroplast transcription unit are translated from both monocistronic and polycistronic mRNAs. EMBO J 7: 2637–2644 (1988).
Barkan A, Miles D, Taylor WC: Chloroplast gene expression in nuclear, photosynthetic mutants of maize. EMBO J 5: 1421–1427 (1985).
Börner T, Sears B: Plastome mutants. Plant Mol Biol Rep 4: 68–92 (1985).
Börner T, Schumann B, Hagemann R: Biochemical studies on a plastid ribosome-deficient mutant of Hordeum vulgare. In: Bücher T, Neupert W, Sebald W, Werner S (eds) Genetic and Biogenesis of Chloroplasts and Mitochondria, p pp. 41–48. Elsevier/North Holland, Amsterdam (1976).
Coetzee T, Herschlag D, Belfort M: Escherichia coli proteins, including ribosomal protein S12, facilitate in vitro splicing of phage T4 introns by acting as RNA chaperones. Genes Devel 8: 1575–1588 (1994).
Deutscher MP: Ribonuclease multiplicity, diversity, and complexity. J Biol Chem 268: 13011–13014 (1993).
Ems SC, Morden CW, Dixon CK, Wolfe KH, dePamphilis CW, Palmer JD: Transcription, splicing and editing of plastid RNAs in the nonphotosynthetic plant Epifagus virginiana. Plant Mol Biol, in press.
Falk J, Schmidt A, Krupinska K: Characterization of plastid DNA transcription in ribosome deficient plastids of heat-bleached barley leaves. J Plant Physiol 141: 176–181 (1993).
Godefroy-Colburn T, Grunberg-Manago M: Polynucleotide phosphorylase. In: Boyer PD (ed) The Enzymes, vol. 7, pp. 533–574, Academic Press, New York (1972).
Goldschmidt-Clermont M, Choquet Y, Girard-Bascou J, Michel F, Schirmer-Rahire M, Rochaix JD: A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell 65: 135–143 (1990).
Goldschmidt-Clermont M, Girard-Bascou J, Choquet Y, Rochaix JD: Trans-splicing mutants of Chlamydomonas reinhardtii. Mol Gen Genet 223: 417–425 (1990).
Gruissem W, Schuster G: Control of mRNA degradation in organelles. In: Belasco JG, Brawerman G (eds) Control of Messenger RNA Stability, pp. 329–365. Academic Press, New York (1993).
Gruissem W, Tonkyn JC: Control mechanisms of plastid gene expression. Crit Rev Plant Sci 10: 525–558 (1993).
Hagemann R, Scholz F: Ein Fall Gen-induzierter Mutationen des Plasmotyps bei Gerste. Züchter 32: 50–59 (1962).
Henningsen KW, Boynton JE, von Wettstein D: Mutants at xantha and albina loci in relation to chloroplast biogenesis in barley (Hordeum vulgare L.). Copenhagen, Denmark: The Royal Danish Academy of Sciences and Letters. Munksgaard, Copenhagen (1993).
Hess WR, Hoch B, Zeltz P, Hübschmann T, Kössel H, Börner T: Inefficient rpl2 splicing in barley mutants with ribosome-deficient plastids. Plant Cell 6: 1455–1465 (1994).
Hess WR, Müller A, Nagy F, Börner T: Ribosome-deficient plastids affect transcription of light-induced nuclear genes: genetic evidence for a plastid-derived signal. Mol Gen Genet 242: 305–312 (1994).
Hess WR, Prombona A, Fieder B, Subramanian AR, Börner T: Chloroplast rps15 and rpoB/C1/C2 gene cluster are strongly transcribed in ribosome-deficient plastids: evidence for a functioning non-chloroplast-encoded RNA polymerase. EMBO J 12: 563–571 (1993).
Hess WR, Schendel R, Rüdiger W, Fieder B, Börner T: Components of chlorophyll biosynthesis in a barley albina mutant unable to synthesize δ-aminolevulinic acid by utilizing the transfer RNA for glutamic acid. Planta 188: 19–27 (1992).
Hildebrand M, Hallick RB, Passavant CW, Bourque DP: Trans-splicing in chloroplasts: The rps12 loci of Nicotiana tabacum. Proc Natl Acad Sci USA 85: 372–376 (1986).
Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M: The complete sequence of rice (Oryza sativa) chloroplast genome: Intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217: 185–194 (1989).
Iratni R, Baeza L, Andreeva A, Mache R, Lerbs-Mache S: Regulation of rDNA transcription in chloroplasts: promoter exclusion by constitutive repression. Genes Devel 8: 2928–2938 (1994).
Kanno A, Hirai A: A transcription map of the chloroplast genome from rice (Oryza sativa). Curr Genet 23: 166–174 (1993).
Kohchi T, Umesono K, Ogura Y, Komine Y, Nakahigashi K, Komano T, Yamada Y, Ozeki H, Ohyama K: A nicked group II intron and trans-splicing in liverwort, Marchantia polymorpha, chloroplasts. Nucl Acids Res 16: 10025–10036 (1988).
Lambowitz AM, Belfort M: Introns as mobile genetic elements. Annu Rev Biochem 62: 587–622 (1993).
Liere K, Link G: RNA-binding activity of the matK protein encoded by the chloroplast trnK intron from mustard (Sinapis alba L.) Nucl Acids Res 23: 917–921 (1995).
Maurizi MR, William PC, Seung-Ho K, Gottesman S: ClpP represents a unique family of serine proteases. J Biol Chem 265: 12546–12552 (1990).
Michel F, Umesono K, Ozeki H: Comparative and functional anatomy of group II catalytic introns: a review. Gene 82: 5–30 (1989).
Mohr G, Perlman PS, Lambowitz AM: Evolutionary relationship among group II intron-encoded proteins and identification of a conserved domain that may be related to maturase function. Nucl Acids Res 21: 4991–4997 (1993).
Moran JV, Mecklenburg KL, Sass P, Belcher SM, Mahnke D, Lewin A, Perlman P: Splicing defective mutants of the COXI gene of yeast mitochondrial DNA: initial definition of the maturase domain of the group II intron A12. Nucl Acids Res 22: 2057–2064 (1994).
Mullet JE: Dynamic regulation of chloroplast transcription. Plant Physiol 103: 309–313 (1994).
Nickelsen J, Dillewijn JV, Rahire M, Rochaix JD: Determinants for stability of the chloroplast psbD RNA are located within its short leader region in Chlamydomonas reinhardtii. EMBO J 13: 3182–3191 (1994).
Nickelsen J, Link G: The 54 kDa RNA-binding protein from mustard chloroplasts mediates endonucleolytic transcript 3′ end formation in vitro. Plant J 3: 537–544 (1993).
Nilsen TW: RNA-RNA interactions in the spliceosome: unraveling the ties that bind. Cell 78: 1–4 (1994).
Ohta M, Sugita M, Sugiura M: Three types of nuclear genes encoding chloroplast RNA-binding proteins (cp29, cp31 and cp33) are present in Arabidopsis thaliana: presence of cp31 in chloroplasts and its homologue in nuclei/cytoplasm. Plant Mol Biol 27: 529–539 (1995).
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: Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322: 572–574 (1986).
Pace NR, Brown JW: Evolutionary perspective on structure and function of ribonuclease P, a ribozyme. J Bact 17: 1919–1928 (1995).
Paulsen H, Bogorad L: Diurnal and circadian rhythm in the accumulation and synthesis of mRNA for the light-harvesting chlorophyll a/b binding protein in tobacco. Plant Physiol 88: 1104–1109 (1988).
Post LE, Nomura M: DNA sequences from the str operon of Escherichia coli. J Biol Chem 255: 4660–4666 (1980).
Rochaix JD: Post-transcriptional steps in the expression of chloroplast genes. Annu Rev Cell Biol 8: 1–28 (1992).
Rogers SO, Bendich AI: Extraction of DNA from milligram amounts of fresh, herbarium, and mummified plant tissues. Plant Mol Biol 5: 69–76 (1985).
Saldanha R, Mohr G, Belfort M, Lambowitz AM: Group I and group II introns. FASEB J 7: 15–24 (1993).
Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
Schuster G, Gruissem W: Chloroplast mRNA 3′ end processing requires a nuclear-encoded RNA-binding protein. EMBO J 10: 1493–1502 (1991).
Sexton TB, Jones JT, Mullet JE: Sequence and trancriptional analysis of the barley cDNA region upstream of psbD-psbC encoding trnK(UUU), rps16, trnQ(UUG), psbK, psbI and trnS(GCU). Curr Genet 17: 445–454 (1990).
Shimada H, Sugiura M: Fine structural features of the chloroplast genome: comparison of the sequenced chloroplast genomes. Nucl Acids Res 19: 983–995 (1991).
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 H, Yamada K, Kusuda J, Takaiwa F, Kato A, Shimada A, Sugiura M: The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5: 2043–2049 (1986).
Stern DB, Kindle KL: 3′ end maturation of the Chlamydomonas reinhardtii chloroplast atpB mRNA is a two-step process. Mol Cel Biol 13: 2277–2285 (1993).
Stern DB, Gruissem W: Chloroplast mRNA 3′ end maturation is biochemical distinct from prolaryotic mRNA processing. Plant Mol Biol 13: 615–625 (1989).
Sugiura M: The chloroplast genome. Plant Mol Biol 19: 149–168 (1992).
Turmel M, Choquet Y, Goldschmidt-Clermont M, Rochaix JD, Otis C, Lemieux C: The trans-spliced intron 1 in the psaA gene of the Chlamydomonas chloroplast: a comparative analysis. Curr Genet 27: 270–279 (1995).
Vera A, Sugiura M: A novel RNA gene in the tobacco plastid genome: its possible role in the maturation of 16S rRNA. EMBO J 13: 2211–2217 (1994).
Wang MJ, Davis NW, Gegenheimer P: Novel mechanisms for maturation of chloroplast transfer RNA precursors. EMBO J: 1567–1574 (1988).
Weglöhner W, Subramanian AR: Nucleotide sequence of a region of maize chloroplast DNA containing the 3′ end of clpP, exon 1 of rps12 and rpl20 and their cotranscription. Plant Mol Biol 18: 415–418 (1992).
Westhoff P, Herrmann RG: Complex RNA maturation in chloroplasts: the psbB operon from spinach. Eur J Biochem 171: 551–564 (1988).
Ye L, Li Y, Fukami-Kobayashi K, Go M, Konishi T, Watanabe A, Sugiura M: Diversity of a ribonucleoprotein family in tobacco chloroplasts: two new chloroplast ribonucleoproteins and a phylogenetic tree of ten chloroplast RNA-binding domains. Nucl Acids Res 19: 6485–6490 (1991).
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Hübschmann, T., Hess, W.R. & Börner, T. Impaired splicing of the rps 12 transcript in ribosome-deficient plastids. Plant Mol Biol 30, 109–123 (1996). https://doi.org/10.1007/BF00017806
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DOI: https://doi.org/10.1007/BF00017806