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EMBO J. May 4, 1999; 18(9): 2621–2630.
PMCID: PMC1171341

Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression.

Abstract

The maize nuclear gene crp1 is required for the translation of the chloroplast petA and petD mRNAs and for the processing of the petD mRNA from a polycistronic precursor. In order to understand the biochemical role of the crp1 gene product and the interconnections between chloroplast translation and RNA metabolism, the crp1 gene and cDNA were cloned. The predicted crp1 gene product (CRP1) is related to nuclear genes in fungi that play an analogous role in mitochondrial gene expression, suggesting an underlying mechanistic similarity. Analysis of double mutants that lack both chloroplast ribosomes and crp1 function indicated that CRP1 activates a site-specific endoribonuclease independently of any role it plays in translation. Antibodies prepared to recombinant CRP1 were used to demonstrate that CRP1 is localized to the chloroplast stroma and that it is a component of a multisubunit complex. The CRP1 complex is not associated detectably with either chloroplast membranes or chloroplast ribosomes. Models for CRP1 function and its relationship to other activators of organellar translation are discussed.

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Selected References

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  • Barkan A. Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs. EMBO J. 1988 Sep;7(9):2637–2644. [PMC free article] [PubMed]
  • 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. 1994 Jul 1;13(13):3170–3181. [PMC free article] [PubMed]
  • Boudreau E, Takahashi Y, Lemieux C, Turmel M, Rochaix JD. The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. EMBO J. 1997 Oct 15;16(20):6095–6104. [PMC free article] [PubMed]
  • Braun F, Le Derout J, Régnier P. Ribosomes inhibit an RNase E cleavage which induces the decay of the rpsO mRNA of Escherichia coli. EMBO J. 1998 Aug 17;17(16):4790–4797. [PMC free article] [PubMed]
  • Brown NG, Costanzo MC, Fox TD. Interactions among three proteins that specifically activate translation of the mitochondrial COX3 mRNA in Saccharomyces cerevisiae. Mol Cell Biol. 1994 Feb;14(2):1045–1053. [PMC free article] [PubMed]
  • Chandler VL, Hardeman KJ. The Mu elements of Zea mays. Adv Genet. 1992;30:77–122. [PubMed]
  • Cline K, Henry R. Import and routing of nucleus-encoded chloroplast proteins. Annu Rev Cell Dev Biol. 1996;12:1–26. [PubMed]
  • Coffin JW, Dhillon R, Ritzel RG, Nargang FE. The Neurospora crassa cya-5 nuclear gene encodes a protein with a region of homology to the Saccharomyces cerevisiae PET309 protein and is required in a post-transcriptional step for the expression of the mitochondrially encoded COXI protein. Curr Genet. 1997 Oct;32(4):273–280. [PubMed]
  • Danon A, Mayfield SP. Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins. EMBO J. 1991 Dec;10(13):3993–4001. [PMC free article] [PubMed]
  • Drapier D, Girard-Bascou J, Wollman FA. Evidence for Nuclear Control of the Expression of the atpA and atpB Chloroplast Genes in Chlamydomonas. Plant Cell. 1992 Mar;4(3):283–295. [PMC free article] [PubMed]
  • Frohman MA, Dush MK, Martin GR. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. [PMC free article] [PubMed]
  • Girard-Bascou J, Pierre Y, Drapier D. A nuclear mutation affects the synthesis of the chloroplast psbA gene production Chlamydomonas reinhardtii. Curr Genet. 1992 Jul;22(1):47–52. [PubMed]
  • Glick BS, Von Heijne G. Saccharomyces cerevisiae mitochondria lack a bacterial-type sec machinery. Protein Sci. 1996 Dec;5(12):2651–2652. [PMC free article] [PubMed]
  • Goldschmidt-Clermont M. Coordination of nuclear and chloroplast gene expression in plant cells. Int Rev Cytol. 1998;177:115–180. [PubMed]
  • Hauser CR, Gillham NW, Boynton JE. Translational regulation of chloroplast genes. Proteins binding to the 5'-untranslated regions of chloroplast mRNAs in Chlamydomonas reinhardtii. J Biol Chem. 1996 Jan 19;271(3):1486–1497. [PubMed]
  • Hayes R, Kudla J, Schuster G, Gabay L, Maliga P, Gruissem W. Chloroplast mRNA 3'-end processing by a high molecular weight protein complex is regulated by nuclear encoded RNA binding proteins. EMBO J. 1996 Mar 1;15(5):1132–1141. [PMC free article] [PubMed]
  • Hirose T, Sugiura M. Cis-acting elements and trans-acting factors for accurate translation of chloroplast psbA mRNAs: development of an in vitro translation system from tobacco chloroplasts. EMBO J. 1996 Apr 1;15(7):1687–1695. [PMC free article] [PubMed]
  • Jenkins BD, Kulhanek DJ, Barkan A. Nuclear mutations that block group II RNA splicing in maize chloroplasts reveal several intron classes with distinct requirements for splicing factors. Plant Cell. 1997 Mar;9(3):283–296. [PMC free article] [PubMed]
  • Kuchka MR, Mayfield SP, Rochaix JD. Nuclear mutations specifically affect the synthesis and/or degradation of the chloroplast-encoded D2 polypeptide of photosystem II in Chlamydomonas reinhardtii. EMBO J. 1988 Feb;7(2):319–324. [PMC free article] [PubMed]
  • Kuras R, Wollman FA. The assembly of cytochrome b6/f complexes: an approach using genetic transformation of the green alga Chlamydomonas reinhardtii. EMBO J. 1994 Mar 1;13(5):1019–1027. [PMC free article] [PubMed]
  • Lambowitz AM, Perlman PS. Involvement of aminoacyl-tRNA synthetases and other proteins in group I and group II intron splicing. Trends Biochem Sci. 1990 Nov;15(11):440–444. [PubMed]
  • Leon P, Arroyo A, Mackenzie S. NUCLEAR CONTROL OF PLASTID AND MITOCHONDRIAL DEVELOPMENT IN HIGHER PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49(NaN):453–480. [PubMed]
  • Maier RM, Neckermann K, Igloi GL, Kössel H. Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J Mol Biol. 1995 Sep 1;251(5):614–628. [PubMed]
  • Manthey GM, McEwen JE. The product of the nuclear gene PET309 is required for translation of mature mRNA and stability or production of intron-containing RNAs derived from the mitochondrial COX1 locus of Saccharomyces cerevisiae. EMBO J. 1995 Aug 15;14(16):4031–4043. [PMC free article] [PubMed]
  • Manthey GM, Przybyla-Zawislak BD, McEwen JE. The Saccharomyces cerevisiae Pet309 protein is embedded in the mitochondrial inner membrane. Eur J Biochem. 1998 Jul 1;255(1):156–161. [PubMed]
  • Mullet JE. Dynamic regulation of chloroplast transcription. Plant Physiol. 1993 Oct;103(2):309–313. [PMC free article] [PubMed]
  • Nickelsen J, Link G. The 54 kDa RNA-binding protein from mustard chloroplasts mediates endonucleolytic transcript 3' end formation in vitro. Plant J. 1993 Apr;3(4):537–544. [PubMed]
  • Rochaix JD. Post-transcriptional regulation of chloroplast gene expression in Chlamydomonas reinhardtii. Plant Mol Biol. 1996 Oct;32(1-2):327–341. [PubMed]
  • Rochaix JD, Kuchka M, Mayfield S, Schirmer-Rahire M, Girard-Bascou J, Bennoun P. Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplast psbC gene product in Chlamydomonas reinhardtii. EMBO J. 1989 Apr;8(4):1013–1021. [PMC free article] [PubMed]
  • Ruf S, Kössel H, Bock R. Targeted inactivation of a tobacco intron-containing open reading frame reveals a novel chloroplast-encoded photosystem I-related gene. J Cell Biol. 1997 Oct 6;139(1):95–102. [PMC free article] [PubMed]
  • Sanchirico ME, Fox TD, Mason TL. Accumulation of mitochondrially synthesized Saccharomyces cerevisiae Cox2p and Cox3p depends on targeting information in untranslated portions of their mRNAs. EMBO J. 1998 Oct 1;17(19):5796–5804. [PMC free article] [PubMed]
  • Schnell Danny J. PROTEIN TARGETING TO THE THYLAKOID MEMBRANE. Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49(NaN):97–126. [PubMed]
  • Schuster G, Gruissem W. Chloroplast mRNA 3' end processing requires a nuclear-encoded RNA-binding protein. EMBO J. 1991 Jun;10(6):1493–1502. [PMC free article] [PubMed]
  • Semrad K, Schroeder R. A ribosomal function is necessary for efficient splicing of the T4 phage thymidylate synthase intron in vivo. Genes Dev. 1998 May 1;12(9):1327–1337. [PMC free article] [PubMed]
  • Stampacchia O, Girard-Bascou J, Zanasco JL, Zerges W, Bennoun P, Rochaix JD. A nuclear-encoded function essential for translation of the chloroplast psaB mRNA in chlamydomonas. Plant Cell. 1997 May;9(5):773–782. [PMC free article] [PubMed]
  • Sugita M, Sugiura M. Regulation of gene expression in chloroplasts of higher plants. Plant Mol Biol. 1996 Oct;32(1-2):315–326. [PubMed]
  • Tatusov RL, Koonin EV, Lipman DJ. A genomic perspective on protein families. Science. 1997 Oct 24;278(5338):631–637. [PubMed]
  • Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. [PMC free article] [PubMed]
  • Valencik ML, Kloeckener-Gruissem B, Poyton RO, McEwen JE. Disruption of the yeast nuclear PET54 gene blocks excision of mitochondrial intron aI5 beta from pre-mRNA for cytochrome c oxidase subunit I. EMBO J. 1989 Dec 1;8(12):3899–3904. [PMC free article] [PubMed]
  • Voelker R, Barkan A. Two nuclear mutations disrupt distinct pathways for targeting proteins to the chloroplast thylakoid. EMBO J. 1995 Aug 15;14(16):3905–3914. [PMC free article] [PubMed]
  • Voelker R, Mendel-Hartvig J, Barkan A. Transposon-disruption of a maize nuclear gene, tha1, encoding a chloroplast SecA homologue: in vivo role of cp-SecA in thylakoid protein targeting. Genetics. 1997 Feb;145(2):467–478. [PMC free article] [PubMed]
  • Yang J, Schuster G, Stern DB. CSP41, a sequence-specific chloroplast mRNA binding protein, is an endoribonuclease. Plant Cell. 1996 Aug;8(8):1409–1420. [PMC free article] [PubMed]
  • Yohn CB, Cohen A, Rosch C, Kuchka MR, Mayfield SP. Translation of the chloroplast psbA mRNA requires the nuclear-encoded poly(A)-binding protein, RB47. J Cell Biol. 1998 Jul 27;142(2):435–442. [PMC free article] [PubMed]
  • Zerges W, Rochaix JD. The 5' leader of a chloroplast mRNA mediates the translational requirements for two nucleus-encoded functions in Chlamydomonas reinhardtii. Mol Cell Biol. 1994 Aug;14(8):5268–5277. [PMC free article] [PubMed]
  • Zerges W, Rochaix JD. Low density membranes are associated with RNA-binding proteins and thylakoids in the chloroplast of Chlamydomonas reinhardtii. J Cell Biol. 1998 Jan 12;140(1):101–110. [PMC free article] [PubMed]

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