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PMID: 19424177 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Site-specific binding of a PPR protein defines and stabilizes 5' and 3' mRNA termini in chloroplasts.

The EMBO journal ·Vol. 28 ·No. 14 ·2009-07-22 ·Pages 2042-52

Pfalz J, Bayraktar OA, Prikryl J, Barkan A

Abstract

Chloroplast mRNA populations are characterized by overlapping transcripts derived by processing from polycistronic precursors. The mechanisms and functional significance of these processing events are poorly understood. We describe a pentatricopeptide repeat (PPR) protein, PPR10, whose binding defines mRNA segments derived from two transcription units in maize chloroplasts. PPR10 interacts in vivo and in vitro with two intergenic RNA regions of similar sequence. The processed 5' and 3' RNA termini in these regions overlap by approximately 25 nucleotides. The PPR10-binding sites map precisely to these overlapping sequences, and PPR10 is required specifically for the accumulation of RNAs with these termini. These findings show that PPR10 serves as a barrier to RNA decay from either the 5' or 3' direction and that a bound protein provides an alternative to an RNA hairpin as a barrier to 3' exonucleases. The results imply that protein 'caps' at both 5' and 3' ends can define the termini of chloroplast mRNA segments. These results, together with recent insights into bacterial RNA decay, suggest a unifying model for the biogenesis of chloroplast transcript populations and for the determinants of chloroplast mRNA stability.

MeSH Terms
Chloroplasts/genetics,metabolism Gene Expression Regulation, Plant Molecular Sequence Data Plant Proteins/metabolism RNA Cap-Binding Proteins/metabolism RNA Processing, Post-Transcriptional RNA Stability RNA, Messenger/genetics,metabolism Zea mays/genetics,metabolism
Chemicals
Plant Proteins RNA Cap-Binding Proteins RNA, Messenger
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Pfalz Jeannette
Institute of Molecular Biology, University of Oregon, Eugene, OR 97403, USA.
Bayraktar Omer Ali
Prikryl Jana
Barkan Alice
References (49)
49 references, click to expand
  1. How ribosomes select initiator regions in mRNA: base pair formation between the 3' terminus of 16S rRNA and the mRNA during initiation of protein synthesis in Escherichia coli.
    Proc Natl Acad Sci U S A. 1975 Dec;72(12):4734-8 PMID: 1107998
  2. RNA processing alters open reading frame stoichiometry from the large ATP synthase gene cluster of spinach chloroplasts.
    Plant Mol Biol. 1997 Mar;33(4):635-40 PMID: 9132055
  3. The PPR motif - a TPR-related motif prevalent in plant organellar proteins.
    Trends Biochem Sci. 2000 Feb;25(2):46-7 PMID: 10664580
  4. Lost in translation: the influence of ribosomes on bacterial mRNA decay.
    Genes Dev. 2005 Nov 1;19(21):2526-33 PMID: 16264189
  5. Stability determinants in the chloroplast psbB/T/H mRNAs of Chlamydomonas reinhardtii.
    Plant J. 2000 Mar;21(5):469-82 PMID: 10758498
  6. A ribonuclease III domain protein functions in group II intron splicing in maize chloroplasts.
    Plant Cell. 2007 Aug;19(8):2606-23 PMID: 17693527
  7. RNA-binding properties of HCF152, an Arabidopsis PPR protein involved in the processing of chloroplast RNA.
    Eur J Biochem. 2003 Oct;270(20):4070-81 PMID: 14519118
  8. Nuclear Mutants of Maize with Defects in Chloroplast Polysome Assembly Have Altered Chloroplast RNA Metabolism.
    Plant Cell. 1993 Apr;5(4):389-402 PMID: 12271069
  9. Sequence-specific binding of a chloroplast pentatricopeptide repeat protein to its native group II intron ligand.
    RNA. 2008 Sep;14(9):1930-41 PMID: 18669444
  10. In vivo analysis of plastid psbA, rbcL and rpl32 UTR elements by chloroplast transformation: tobacco plastid gene expression is controlled by modulation of transcript levels and translation efficiency
    Plant J. 1999 Aug;19(3):333-45 PMID: 10476080
  11. 5'-to-3' exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5' stability of mRNA.
    Cell. 2007 May 18;129(4):681-92 PMID: 17512403
  12. Identification of cis-acting RNA leader elements required for chloroplast psbD gene expression in Chlamydomonas.
    Plant Cell. 1999 May;11(5):957-70 PMID: 10330479
  13. A 125 kDa RNase E/G-like protein is present in plastids and is essential for chloroplast development and autotrophic growth in Arabidopsis.
    J Exp Bot. 2008;59(10):2597-610 PMID: 18515828
  14. RNase E: still a wonderfully mysterious enzyme.
    Mol Microbiol. 1997 Mar;23(6):1099-106 PMID: 9106202
  15. RNA immunoprecipitation and microarray analysis show a chloroplast Pentatricopeptide repeat protein to be associated with the 5' region of mRNAs whose translation it activates.
    Plant Cell. 2005 Oct;17(10):2791-804 PMID: 16141451
  16. Transcript analysis of the tobacco plastid operon rps2/atpI/H/F/A reveals the existence of a non-consensus type II (NCII) promoter upstream of the atpI coding sequence.
    Mol Gen Genet. 1998 Feb;257(3):299-307 PMID: 9520264
  17. HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbH-petB-petD RNAs.
    Plant Cell. 2003 Jun;15(6):1480-95 PMID: 12782738
  18. Role of Bacillus subtilis RNase J1 endonuclease and 5'-exonuclease activities in trp leader RNA turnover.
    J Biol Chem. 2008 Jun 20;283(25):17158-67 PMID: 18445592
  19. Altering the 3 UTR endonucleolytic cleavage site of a Chlamydomonas chloroplast mRNA affects 3-end maturation in vitro but not in vivo.
    Plant Mol Biol. 1999 Jul;40(4):679-86 PMID: 10480391
  20. PPR motifs of the nucleus-encoded factor, PGR3, function in the selective and distinct steps of chloroplast gene expression in Arabidopsis.
    Plant J. 2004 Apr;38(1):152-63 PMID: 15053768
  21. Co-transcription pattern of an introgressed operon in the maize chloroplast genome comprising four ATP synthase subunit genes and the ribosomal rps2.
    Plant Mol Biol. 1993 Mar;21(6):1069-76 PMID: 8490127
  22. Characterization of Mbb1, a nucleus-encoded tetratricopeptide-like repeat protein required for expression of the chloroplast psbB/psbT/psbH gene cluster in Chlamydomonas reinhardtii.
    Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14813-8 PMID: 11121080
  23. Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression.
    EMBO J. 1999 May 4;18(9):2621-30 PMID: 10228173
  24. Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa.
    Genome Res. 2008 Apr;18(4):571-84 PMID: 18323537
  25. 5' to 3' exoribonucleolytic activity is a normal component of chloroplast mRNA decay pathways.
    Plant J. 1999 Sep;19(5):521-31 PMID: 10504574
  26. Both RNA editing and RNA cleavage are required for translation of tobacco chloroplast ndhD mRNA: a possible regulatory mechanism for the expression of a chloroplast operon consisting of functionally unrelated genes.
    EMBO J. 1997 Nov 17;16(22):6804-11 PMID: 9362494
  27. Pentatricopeptide repeat proteins: a socket set for organelle gene expression.
    Trends Plant Sci. 2008 Dec;13(12):663-70 PMID: 19004664
  28. Identification of small non-coding RNAs from mitochondria and chloroplasts.
    Nucleic Acids Res. 2006;34(14):3842-52 PMID: 16899451
  29. The nucleus-encoded HCF107 gene of Arabidopsis provides a link between intercistronic RNA processing and the accumulation of translation-competent psbH transcripts in chloroplasts.
    Plant Cell. 2001 Sep;13(9):2127-41 PMID: 11549768
  30. Killer and protective ribosomes.
    Prog Mol Biol Transl Sci. 2009;85:423-66 PMID: 19215779
  31. The pentatricopeptide repeat protein PPR5 stabilizes a specific tRNA precursor in maize chloroplasts.
    Mol Cell Biol. 2008 Sep;28(17):5337-47 PMID: 18591259
  32. On the expansion of the pentatricopeptide repeat gene family in plants.
    Mol Biol Evol. 2008 Jun;25(6):1120-8 PMID: 18343892
  33. A spontaneous tRNA suppressor of a mutation in the Chlamydomonas reinhardtii nuclear MCD1 gene required for stability of the chloroplast petD mRNA.
    Nucleic Acids Res. 2005 Jun 09;33(10):3372-80 PMID: 15947135
  34. Molecular identification and function of cis- and trans-acting determinants for petA transcript stability in Chlamydomonas reinhardtii chloroplasts.
    Mol Cell Biol. 2008 Sep;28(17):5529-42 PMID: 18573878
  35. In vivo evidence for 5'-->3' exoribonuclease degradation of an unstable chloroplast mRNA.
    Plant J. 1998 Jan;13(1):85-96 PMID: 9680967
  36. CRS1 is a novel group II intron splicing factor that was derived from a domain of ancient origin.
    RNA. 2001 Sep;7(9):1227-38 PMID: 11565746
  37. The nuclear gene HCF107 encodes a membrane-associated R-TPR (RNA tetratricopeptide repeat)-containing protein involved in expression of the plastidial psbH gene in Arabidopsis.
    Plant J. 2005 Jun;42(5):720-30 PMID: 15918885
  38. Maturation and degradation of RNA in bacteria.
    Curr Opin Microbiol. 2007 Jun;10(3):271-8 PMID: 17560162
  39. Arabidopsis orthologs of maize chloroplast splicing factors promote splicing of orthologous and species-specific group II introns.
    Plant Physiol. 2006 Dec;142(4):1656-63 PMID: 17071648
  40. fastSCOP: a fast web server for recognizing protein structural domains and SCOP superfamilies.
    Nucleic Acids Res. 2007 Jul;35(Web Server issue):W438-43 PMID: 17485476
  41. A conserved DYW domain of the pentatricopeptide repeat protein possesses a novel endoribonuclease activity.
    FEBS Lett. 2008 Dec 24;582(30):4163-8 PMID: 19041647
  42. The RNase E/G-type endoribonuclease of higher plants is located in the chloroplast and cleaves RNA similarly to the E. coli enzyme.
    RNA. 2008 Jun;14(6):1057-68 PMID: 18441049
  43. The Nac2 gene of Chlamydomonas encodes a chloroplast TPR-like protein involved in psbD mRNA stability.
    EMBO J. 2000 Jul 3;19(13):3366-76 PMID: 10880449
  44. A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis.
    Plant J. 2003 Nov;36(4):541-9 PMID: 14617084
  45. A SecY homologue is required for the elaboration of the chloroplast thylakoid membrane and for normal chloroplast gene expression.
    J Cell Biol. 1998 Apr 20;141(2):385-95 PMID: 9548717
  46. Recruitment of a peptidyl-tRNA hydrolase as a facilitator of group II intron splicing in chloroplasts.
    EMBO J. 2001 Feb 15;20(4):872-9 PMID: 11179231
  47. The nuclear factor HCF145 affects chloroplast psaA-psaB-rps14 transcript abundance in Arabidopsis thaliana.
    Plant J. 2004 Jun;38(5):740-53 PMID: 15144376
  48. A chloroplast-localized PPR protein required for plastid ribosome accumulation.
    Plant J. 2003 Dec;36(5):675-86 PMID: 14617068
  49. 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):3170-81 PMID: 8039510
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
1460-2075
DOI
10.1038/emboj.2009.121
Published
2009-07-22
Epub
2009-00-07
Pages
2042-52
Language
English
Region
England
NLM ID
8208664
PMCID
PMC2718276
Subset
IM
Databases
GENBANK
FJ490677
Corrections
CommentIn
PMID: 19623192
External Links
PubMed source DOI: 10.1038/emboj.2009.121 PMC Full Text View journal details
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