Identification of small non-coding RNAs from mitochondria and chloroplasts

Small non-protein-coding RNAs (ncRNAs) have been identified in a wide spectrum of organisms ranging from bacteria to humans. In eukarya, systematic searches for ncRNAs have so far been restricted to the nuclear or cytosolic compartments of cells. Whether or not small stable non-coding RNA species also exist in cell organelles, in addition to tRNAs or ribosomal RNAs, is unknown. We have thus generated cDNA libraries from size-selected mammalian mitochondrial RNA and plant chloroplast RNA and searched for small ncRNA species in these two types of DNA-containing cell organelles. In total, we have identified 18 novel candidates for organellar ncRNAs in these two cellular compartments and confirmed expression of six of them by northern blot analysis or RNase A protection assays. Most candidate ncRNA genes map to intergenic regions of the organellar genomes. As found previously in bacteria, the presumptive ancestors of present-day chloroplasts and mitochondria, we also observed examples of antisense ncRNAs that potentially could target organelle-encoded mRNAs. The structural features of the identified ncRNAs as well as their possible cellular functions are discussed. The absence from our libraries of abundant small RNA species that are not encoded by the organellar genomes suggests that the import of RNAs into cell organelles is of very limited significance or does not occur at all.

[1]  R. Bock,et al.  Constancy of organellar genome copy numbers during leaf development and senescence in higher plants , 2006, Molecular Genetics and Genomics.

[2]  Jörg Vogel,et al.  Experimental approaches to identify non-coding RNAs , 2006, Nucleic acids research.

[3]  A. Marchfelder,et al.  The tRNase Z family of proteins: physiological functions, substrate specificity and structural properties , 2005, Biological chemistry.

[4]  D. Baulcombe,et al.  Identification of new small non-coding RNAs from tobacco and Arabidopsis. , 2005, Biochimie.

[5]  Ilka M. Axmann,et al.  Identification of cyanobacterial non-coding RNAs by comparative genome analysis , 2005, Genome Biology.

[6]  D. Geiger,et al.  Polyadenylation and Degradation of Human Mitochondrial RNA: the Prokaryotic Past Leaves Its Mark , 2005, Molecular and Cellular Biology.

[7]  J. Xie,et al.  A two‐dimensional electrophoretic map of human mitochondrial proteins from immortalized lymphoblastoid cell lines: A prerequisite to study mitochondrial disorders in patients , 2005, Proteomics.

[8]  K. Bräutigam,et al.  Photosynthetic redox control of nuclear gene expression. , 2005, Journal of experimental botany.

[9]  S. Holtgrefe,et al.  Strategies to maintain redox homeostasis during photosynthesis under changing conditions. , 2005, Journal of experimental botany.

[10]  A. Hüttenhofer,et al.  Non-coding RNAs: hope or hype? , 2005, Trends in genetics : TIG.

[11]  J. Mattick,et al.  Small regulatory RNAs in mammals. , 2005, Human molecular genetics.

[12]  A. Hüttenhofer,et al.  Experimental RNomics in Aquifex aeolicus: identification of small non-coding RNAs and the putative 6S RNA homolog , 2005, Nucleic acids research.

[13]  G. Storz,et al.  Detection of 5′- and 3′-UTR-derived small RNAs and cis-encoded antisense RNAs in Escherichia coli , 2005, Nucleic acids research.

[14]  J. Vogel,et al.  The Small RNA IstR Inhibits Synthesis of an SOS-Induced Toxic Peptide , 2004, Current Biology.

[15]  G. Storz,et al.  GadY, a Small-RNA Regulator of Acid Response Genes in Escherichia coli , 2004, Journal of bacteriology.

[16]  R. Bock,et al.  Taming plastids for a green future. , 2004, Trends in biotechnology.

[17]  Graham R Fleming,et al.  Toward an understanding of the mechanism of nonphotochemical quenching in green plants. , 2004, Biochemistry.

[18]  D. Bartel,et al.  Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs , 2004, Nature Reviews Genetics.

[19]  P. Maliga.  Plastid transformation in higher plants. , 2004, Annual review of plant biology.

[20]  J. Mattick.  RNA regulation: a new genetics? , 2004, Nature Reviews Genetics.

[21]  R. Bungard,et al.  Photosynthetic evolution in parasitic plants: insight from the chloroplast genome , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[22]  W. Martin,et al.  Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes , 2004, Nature Reviews Genetics.

[23]  D. Bartel.  MicroRNAs Genomics, Biogenesis, Mechanism, and Function , 2004, Cell.

[24]  W. Duan,et al.  The function of chloroplastic NAD(P)H dehydrogenase in tobacco during chilling stress under low irradiance. , 2004, Plant & cell physiology.

[25]  J. Vogel,et al.  RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. , 2003, Nucleic acids research.

[26]  J. Mullikin,et al.  Revisiting the mouse mitochondrial DNA sequence. , 2003, Nucleic acids research.

[27]  Jürgen Brosius,et al.  Experimental RNomics Identification of 140 Candidates for Small Non-Messenger RNAs in the Plant Arabidopsis thaliana , 2002, Current Biology.

[28]  A. Hüttenhofer,et al.  RNomics: identification and function of small, non-messenger RNAs. , 2002, Current opinion in chemical biology.

[29]  R. Martin,et al.  5 S rRNA and tRNA Import into Human Mitochondria , 2001, The Journal of Biological Chemistry.

[30]  S. Eddy.  Non–coding RNA genes and the modern RNA world , 2001, Nature Reviews Genetics.

[31]  R. Bock.  Transgenic plastids in basic research and plant biotechnology. , 2001, Journal of molecular biology.

[32]  A. Hüttenhofer,et al.  RNomics: an experimental approach that identifies 201 candidates for novel, small, non‐messenger RNAs in mouse , 2001, The EMBO journal.

[33]  G. Peltier,et al.  Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around photosystem I. , 2001, Plant physiology.

[34]  R. Garesse,et al.  Animal mitochondrial biogenesis and function: a regulatory cross-talk between two genomes. , 2001, Gene.

[35]  G. Peltier,et al.  Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure. , 2000, Plant physiology.

[36]  A. Barkan,et al.  Participation of nuclear genes in chloroplast gene expression. , 2000, Biochimie.

[37]  S. Lerbs-Mache.  Regulation of rDNA transcription in plastids of higher plants. , 2000, Biochimie.

[38]  D. Leister,et al.  A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. , 2000, Trends in plant science.

[39]  F. Sato,et al.  The role of chloroplastic NAD(P)H dehydrogenase in photoprotection , 1999, FEBS letters.

[40]  J. Taanman,et al.  The mitochondrial genome: structure, transcription, translation and replication. , 1999, Biochimica et biophysica acta.

[41]  M. Sugiura,et al.  Updated Gene Map of Tobacco Chloroplast DNA , 1998, Plant Molecular Biology Reporter.

[42]  Yasuyuki Yamada,et al.  Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[43]  R. Bock.  Analysis of RNA editing in plastids. , 1998, Methods.

[44]  D. Turnbull,et al.  Mammalian mitochondrial genetics: heredity, heteroplasmy and disease. , 1997, Trends in genetics : TIG.

[45]  T. Börner,et al.  Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. , 1997, Science.

[46]  M. Sugiura,et al.  Regulation of gene expression in chloroplasts of higher plants , 1996, Plant Molecular Biology.

[47]  A. Brennicke,et al.  Molecular biology of plant mitochondria , 1996, Naturwissenschaften.

[48]  John Maynard Smith,et al.  The major evolutionary transitions , 1995, Nature.

[49]  M. Sugiura,et al.  A novel RNA gene in the tobacco plastid genome: its possible role in the maturation of 16S rRNA. , 1994, The EMBO journal.

[50]  W. Gruissem,et al.  Control mechanisms of plastid gene expression , 1993 .

[51]  R. Gutell,et al.  Collection of small subunit (16S- and 16S-like) ribosomal RNA structures: 1994. , 1993, Nucleic acids research.

[52]  J. Mullet,et al.  Quantitative analysis of transcription and RNA levels of 15 barley chloroplast genes. Transcription rates and mRNA levels vary over 300-fold; predicted mRNA stabilities vary 30-fold. , 1992, The Journal of biological chemistry.

[53]  J. Palmer,et al.  Rapid evolution of the plastid translational apparatus in a nonphotosynthetic plant: Loss or accelerated sequence evolution of tRNA and ribosomal protein genes , 1992, Journal of Molecular Evolution.

[54]  K. Oda,et al.  Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome. , 1992, Journal of molecular biology.

[55]  J. Palmer,et al.  Plastid translation and transcription genes in a non‐photosynthetic plant: intact, missing and pseudo genes. , 1991, The EMBO journal.

[56]  M. Sugiura,et al.  Fine structural features of the chloroplast genome: comparison of the sequenced chloroplast genomes. , 1991, Nucleic acids research.

[57]  L. Krinke,et al.  RNase III-dependent hydrolysis of lambda cII-O gene mRNA mediated by lambda OOP antisense RNA. , 1990, Genes & development.

[58]  J. Haley,et al.  Alternative promoters are used for genes within maize chloroplast polycistronic transcription units. , 1990, The Plant cell.

[59]  J. Mullet,et al.  Transcription and RNA stability are important determinants of higher plant chloroplast RNA levels , 1987, The EMBO journal.

[60]  A. J. Bendich.  Why do chloroplasts and mitochondria contain so many copies of their genome? , 1987, BioEssays : news and reviews in molecular, cellular and developmental biology.

[61]  J. Mullet,et al.  Control of gene expression during higher plant chloroplast biogenesis. Protein synthesis and transcript levels of psbA, psaA-psaB, and rbcL in dark-grown and illuminated barley seedlings. , 1987, The Journal of biological chemistry.

[62]  F. Takaiwa,et al.  The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression , 1986, The EMBO journal.

[63]  W. Hauswirth,et al.  Replication priming and transcription initiate from precisely the same site in mouse mitochondrial DNA. , 1985, The EMBO journal.

[64]  H. Kössel,et al.  Identification of an rRNA operon promoter from Zea mays chloroplasts which excludes the proximal tRNAValGAC from the primary transcript , 1985, The EMBO journal.

[65]  M. Rabinowitz,et al.  Identification of initiation sites for heavy-strand and light-strand transcription in human mitochondrial DNA. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[66]  D. A. Clayton,et al.  Replication of animal mitochondrial DNA , 1982, Cell.

[67]  J. Montoya,et al.  A small polyadenylated RNA (7 S RNA), containing a putative ribosome attachment site, maps near the origin of human mitochondrial DNA replication. , 1981, Journal of molecular biology.

[68]  F. Sanger,et al.  Sequence and organization of the human mitochondrial genome , 1981, Nature.

[69]  R. Bock.  Extranuclear inheritance: Gene transfer out of plastids , 2006 .

[70]  W. Bottomley,et al.  Comparison of chloroplast DNAs by specific fragmentation with EcoRI endonuclease , 2004, Molecular and General Genetics MGG.

[71]  Alexander Hüttenhofer,et al.  Experimental RNomics: a global approach to identifying small nuclear RNAs and their targets in different model organisms. , 2004, Methods in molecular biology.

[72]  M. Sugiura,et al.  The genomics of land plant chloroplasts: Gene content and alteration of genomic information by RNA editing , 2004, Photosynthesis Research.

[73]  Dmitri A. Nusinow,et al.  Xist RNA and the mechanism of X chromosome inactivation. , 2002, Annual review of genetics.

[74]  R. Bock,et al.  Extranuclear Inheritance: Functional Genomics in Chloroplasts , 2002 .

[75]  E..  Dynamic Regulation of Chloroplast Transcription’ , 2002 .

[76]  E. Wagner,et al.  Antisense RNAs in bacteria and their genetic elements. , 2002, Advances in genetics.

[77]  W. Hess,et al.  Organellar RNA polymerases of higher plants. , 1999, International review of cytology.

[78]  B. Lang,et al.  Mitochondrial evolution. , 1999, Science.

[79]  B. Lang,et al.  Mitochondrial Evolution , 1999 .

[80]  M. W. Gray,et al.  Origin and evolution of organelle genomes. , 1993, Current opinion in genetics & development.

[81]  M. Sugiura,et al.  The chloroplast genome. , 1992, Plant molecular biology.

[82]  H. Kössel,et al.  The transcriptional apparatus of chloroplasts , 1992 .

[83]  C. Sigmund,et al.  Antibiotic resistance mutations in ribosomal RNA genes of Escherichia coli. , 1988, Methods in enzymology.

[84]  D. Chang,et al.  Priming of human mitochondrial DNA replication occurs at the light-strand promoter. , 1985, Proceedings of the National Academy of Sciences of the United States of America.