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Euglena gracilis chloroplastpsbB, psbT, psbH andpsbN gene cluster: Regulation ofpsbB-psbT pre-mRNA processing

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Abstract

A 2.4 kb region of theEuglena gracilis chloroplast genome containing the genespsbT, psbH andpsbN was characterized. The mRNAs transcribed frompsbB, psbT, psbH andpsbN were analyzed by northern hybridization, S1 nuclease protection analysis and primer extension RNA sequencing. The gene pairspsbB psbT andpsbH-psbN are cotranscribed from opposite strands. The 5′ end of thepsbN-psbH transcript and the intercistronic cleavage sites betweenpsbB-psbT and psbN-psbH were determined. The extent ofpsbB-psbT intercistronic cleavage is greater during photoautotrophic than heterotrophic growth and thus may be developmentally regulated. Processing is absent in the nonphotosyntheticE. gracilis mutant Y9Z1NaL.

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References

  • Adams CC, Stern DB (1990) Control of mRNA stability in chloroplasts by 3′ inverted repeats: effects of stem loop mutations on degradation ofpsbA mRNAin vitro. Nucleic Acids Res 18:6003–6010

    Google Scholar 

  • Apirion D, Miczak A (1993) RNA processing in prokaryotic cells. BioEssays 15:113–120

    Google Scholar 

  • Barkan A (1988) Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs. EMBO J 7:2637–2644

    Google Scholar 

  • Barkan A (1993) Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell 5:389–402

    Google Scholar 

  • Baumgartner BJ, Rapp JC, Mullet JE (1993) Plastid genes encoding the transcription/translation apparatus are differentially transcribed early in barley (Hordeum vulgare) chloroplast development: evidence for selective stabilization ofpsbA mRNA. Plant Physiol 101:781–791

    Google Scholar 

  • Berends T, Gamble PE, Mullet JE (1987) Characterization of the barley chloroplast transcription units containing psaA-psaB and psbD-psbC. Nucleic Acids Res 15:5217–5240

    Google Scholar 

  • Blowers AD, Klein U, Ellmore GS, Bogorad L (1993) Functional in vivo analyses of the 3′ flanking sequences of theChlamydomonas chloroplastrbcL andpsaB genes. Mot Gen Genet 238:339–349

    Google Scholar 

  • Brand SN, Tan X, Widget WR (1992) Cloning and sequencing of the petBD operon from the cyanobacteriumSynechococcus sp. PCC 7002. Plant Mol Biol 20:481–491

    Google Scholar 

  • Büschlen S, Choquet Y, Kuras R, Wollman F (1991) Nucleotide sequences of the continuous and separatedpetA, petB andpetD chloroplast genes inChlamydomonas reinhardtii. FEBS Lett 284:257–262

    Google Scholar 

  • Chelm BK, Hallick RB, Gray PW (1979) Transcription program of the chloroplast genome ofEuglena gracilis during chloroplast development. Proc Natl Acad Sci USA 76:2258–2262

    Google Scholar 

  • Chen H, Stern DB (1991) Specific ribonuclease activities in spinach chloroplasts promote mRNA maturation and degradation. J Biol Chem 266:24205–24211

    Google Scholar 

  • Christopher DA (1989) Structure and expression of aEuglena gracilis chloroplast transcription unit encoding II ribosomal protein genes, a tRNA gene and a 2.8 kb intergenic region. PhD dissertation, University of Arizona, Tucson, Arizona

    Google Scholar 

  • Christopher DA, Hallick RB (1990) Complex RNA maturation pathway for a chloroplast ribosomal protein operon with an internal tRNA cistron. Plant Cell 2:659–671

    Google Scholar 

  • Copertino DW, Hallick RB (1991) Group 11 twintron: an intron within an intron in a chloroplast cytochromeb-559 gene. EMBO J 10:433–442

    Google Scholar 

  • Deng XW, Gruissem W (1987) Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell 49:379–87

    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 

  • Drager RG (1993) Structure and transcript processing of aEuglena gracilis chloroplast operon encoding genesrps2, atpI, atpH, atpF atpA and rps18. PhD dissertation, University of Arizona, Tucson, Arizona

    Google Scholar 

  • Gingrich JC, Hallick RB (1985) TheEuglena gracilis chloroplast ribulose-1,5-bisphosphate carboxylase gene. I. Complete DNA sequence and analysis of the nine intervening sequences. J Biol Chem 260:16156–16161

    Google Scholar 

  • Graf L, Roux E, Stutz E (1982) Nucleotide sequence of aEuglena gracilis chloroplast gene coding for the 16S ribosomal RNA. Homologies toEscherichia coli andZea mays chloroplast 168 ribosomal RNA. Nucleic Acids Res 10:6369–6381

    Google Scholar 

  • Gruissem W (1989) Chloroplast gene expression: how plants turn their plastids on. Cell 56:161–170

    Google Scholar 

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

    Google Scholar 

  • Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng B-Y, Li Y-Q, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the 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

    Google Scholar 

  • Hird SM, Webber AN, Wilson RJ, Dyer TA, Gray JC (1991) Differential expression of thepsbB andpsbH genes encoding the 47 kDa chlorophyll a-protein and the 10 kDa phosphoprotein of photosystem 11 during chloroplast development in wheat. Curr Genet 19:199–206

    Google Scholar 

  • Hollingsworth MJ, Johanningmeier U, Karabin GD, Stiegler GL, Hallick RB (1984) Detection of multiple, unspliced precursor mRNA transcripts for the Mr 32,000 thylakoid membrane protein fromEuglena gracilis chloroplasts. Nucleic Acids Res 12:2001–2017

    Google Scholar 

  • Hong L, Hallick RB (1994a) Gene structure and expression of a novelEuglena gracilis chloroplast operon encoding cytochromeb6 and the β and ɛ subunits of the H-ATP synthase complex. Curr Genet 25:270–281

    Google Scholar 

  • Hong L, Hallick RB (1994b) A group III intron is formed from domains of two individual group II introns. Genes Dev 8:1589–1599

    Google Scholar 

  • Ikeuchi M, Koike H, Inoue Y (1989) N-terminal sequencing of low-molecular-mass components in cyanobacterial photosystem 11 core complex. Two components correspond to unidentified open reading frames of plant chloroplast DNA. FEBS Lett 253:178–182

    Google Scholar 

  • Johnson CH, Schmidt GW (1993) ThepsbB gene cluster of the Chlamydomonas reinhardtii chloroplast: Sequence and transcriptional analyses of psbN and psbH. Plant Mol Biol 22:645–658

    Google Scholar 

  • Kallas T, Spiller S, Malkin R (1988) Characterization of two operons encoding the cytochromeb6-f complex of the cyanobacteriumNostoc PCC 7906. Highly conserved sequences but different gene organization than in chloroplasts. J Biol Chem 263:14334–14342

    Google Scholar 

  • Karabin GD, Narita JO, Dodd JR, Hallick RB (1983)Euglena gracilis chloroplast ribosomal RNA transcription units. Nucleotide sequence polymorphism in 5 S rRNA genes and 5 S rRNAs. J Biol Chem 258:14790–14796

    Google Scholar 

  • Karabin GD, Farley M, Hallick RB (1984) Chloroplast gene for Mr 32000 polypeptide of photosystem II inEuglena gracilis is interrupted by four introns with conserved boundary sequences. Nucleic Acids Res 12:5801–5812

    Google Scholar 

  • Keller M, Weil JK, Nair CKK (1989) Nucleotide sequence of thepsbB gene ofEuglena gracilis. Plant Mol Biol 13:723–725

    Google Scholar 

  • Kohchi T, Yoshida T, Komano T, Ohyama K (1988) Divergent mRNA transcription in the chloroplastpsbB operon. EMBO J 7:885–891

    Google Scholar 

  • Matsubayashi T, Wakasugi T, Shinozaki K, Yamaguchi SK, Zaita N, Hidaka T, Meng BY, Ohto C, Tanaka M, Kato A (1987) Six chloroplast genes (ndhA-F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: determination of the splice sites in ndhA and ndhB pre-mRNAs. Mol Gen Genet 210:385–393

    Google Scholar 

  • Mayes SR, Barber J (1991) Primary structure of thepsbN-psbH-petC petA gene cluster of the cyanobacteriumSynechocystis PCC 6803. Plant Mol Biol 17:289–293

    Google Scholar 

  • Monod C, Goldschmidt-Clermont M, Rochaix JD (1992) Accumulation of chloroplastpsbB RNA requires a nuclear factor inChlamydomonas reinhardtii. Mol Gen Genet 231:449–459

    Google Scholar 

  • Monod C, Takahashi Y, Goldschmidt-Clermont M, Rochaix JD (1994) The chloroplastycf8 open reading frame encodes a photosystem II polypeptide which maintains photosynthetic activity under adverse growth conditions. EMBO J 13:2747–2754

    Google Scholar 

  • Montandon PE, Knuchel AC, Stutz E (1987)Euglena gracilis chloroplast DNA: the untranslated leader of tufA-ORF206 gene contains an intron. Nucleic Acids Res 15:7809–7822

    Google Scholar 

  • Mullet JE (1988) Chloroplast development and gene expression. Annu Rev Plant Physiol Plant Mol Biol 39:475–502

    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 sequence deduced from the complete sequence of liverwortMarchantia polymorpha chloroplast DNA. Nature 322:572–574

    Google Scholar 

  • Palmer JD (1991) Plastid chromosomes: structure and evolution. In: Boqorad L, Vasil IK (eds) Molecular biology of plastids. Academic Press, San Diego, pp 5–53

    Google Scholar 

  • Radebaugh CA (1990) Characterization of the structure and expression of theEuglena gracilis chloroplastrpoC1 andrpoC2 gene loci. PhD dissertation, University of Arizona, Tucson, Arizona

    Google Scholar 

  • Reith M, Munholland J (1993) A high-resolution gene map of the chloroplast genome of the red algaPorphyra purpurea. Plant Cell 5:465–475

    Google Scholar 

  • Rochaix JD, Kuchka M, Mayfield S, Schirmer RM, Girard BJ, Bennoun P (1989) Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplastpsbC gene product inChlamydomonas reinhardtii. EMBO J 8:1013–1021

    Google Scholar 

  • Rosen KM, Lamperti ED, Villa-Komaroff L (1990) Optimizing the Northern blot procedure. BioTechniques 8:398–403

    Google Scholar 

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

    Google Scholar 

  • 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, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049

    Google Scholar 

  • Srivinas U, Lyman H (1980) Photomorphogenetic regulation of chloroplast replication inEuglena. Plant Physiol 66:295–361

    Google Scholar 

  • Stern DB, Kindle KL (1993) 3′ end maturation of theChlamydomonas reinhardtii chloroplastatpB mRNA is a two-step process. Mol Cell Biol 13:2277–2285

    Google Scholar 

  • Stevenson JK, Hallick RB (1994) ThepsaA operon pre-mRNA of theEuglena gracilis chloroplast is processed into photosystem I and photosystem II mRNAs that accumulate differentially depending on the conditions of cell growth. Plant J 5:247–1260

    Google Scholar 

  • Stevenson JK (1994) Transcription and intercistronic RNA processing of polycistronic operons ofEuglena gracilis chloroplast. PhD dissertation, University of Arizona, Tucson, Arizona

    Google Scholar 

  • Sugiura M (1991) Transcript processing in plastids: trimming, cutting, splicing. In: Boqorad L (ed) Cell culture and somatic cell genetics of plants. Academic Press, San Diego, pp 125–137

    Google Scholar 

  • Tanaka M, Obokata J, Chunwongse J, Shinozaki K, Sugiura M (1987) Rapid slicing and stepwise processing of a transcript from thepsbB operon in tobacco chloroplasts: determination of the intron sites inpetB andpetD. Mol Gen Genet 209:427–431

    Google Scholar 

  • Vermaas WF, Williams JG, Arntzen CJ (1987) Sequencing and modification ofpsbB the gene encoding the CP-47 protein of photosystem II, in the cyanobacteriumSynechocystis 6803. Plant Mol Biol 8:317–326

    Google Scholar 

  • Westhoff P, Herrmann RG (1988) Complex RNA maturation in chloroplasts. ThepsbB operon from spinach. Eur J Biochem 171:551–564

    Google Scholar 

  • Yepiz-Plascencia GM, Jenkins ME, Hallick RB (1988) Nucleotide sequence of theEuglena gracilis chloroplast 23S rRNA gene of therrnC operon. Nucleic Acids Res 16:9340

    Google Scholar 

  • Yepiz-Plascencia GM, Radebaugh CA, Hallick RB (1990) TheEuglena gracilis chloroplastrpoB gene — novel gene organization and transcription of the RNA polymerase subunit operon. Nucleic Acids Res 18:1869–1878

    Google Scholar 

  • Zuker M, Stiegler P (1981) Optimal computer folding of large RNA sequences using thermodynamics and auxillary information. Nucleic Acids Res 9:133–148

    Google Scholar 

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Communicated by R. Herrmann

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Hong, L., Stevenson, J.K., Roth, W.B. et al. Euglena gracilis chloroplastpsbB, psbT, psbH andpsbN gene cluster: Regulation ofpsbB-psbT pre-mRNA processing. Molec. Gen. Genet. 247, 180–188 (1995). https://doi.org/10.1007/BF00705648

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