© 1992 Oxford University Press Nucleic Acids Research, Vol. 20, Supplement 2095-2109 A compilation of large subunit (23S- and 23S-like) ribosomal RNA structures Robin R.Gutell*, Murray N.Schnare1 and Michael W.Gray1* Molecular, Cellular, and Developmental Biology, Campus Box 347, University of Colorado, Boulder, CO 80309 and department of Biochemistry, Dalhousie University, Halifax, Nova Scotia B3H 4H7, Canada INTRODUCTION The present edition of large subunit (LSU; 23S and 23S-like) rRNA secondary structures updates and refines the collections of 1988 [1] and 1990 [2]. As in [1] and [2], each LSU rRNA sequence is presented as a secondary structure, a two-dimensional format that represents, in part, the biologically relevant conformation of the rRNA molecule. When LSU rRNA sequences are configured in this manner, valuable phylogenetic information is readily extracted, facilitating the identification of conserved and variable regions. At the same time, the secondary structure serves as an effective template for relating form to function. GROWTH OF THE DATABASE The collection of LSU rRNA sequences has continued its steady increase in the twelve years following publication of the first complete and correct 23S rRNA sequence [3]. The growth of this collection is tracked in Table 1, with numbers reflecting those sequences that are in the public domain. Within the past few years, a small but growing number of sequences have been released through the GenBank/EMBL databases prior to formal publication; some of these entries still lack a journal citation. Those sequences new to our collection are appropriately noted in Table 2. MODELS OF HIGHER-ORDER STRUCTURE In deducing higher-order structure, comparative analysis is used to reveal features common to all homologous rRNAs. This approach has resulted in detailed and progressively refined higherorder structures for the 23S and 16S rRNAs of Escherichia coli, the standards to which all other homologous rRNA structures are referred. Initially, with a minimal number of LSU rRNA sequences available for comparison, several alternative secondary structures were proposed [4—6]. As both the number and phylogenetic diversity of LSU rRNA sequences increased, it became possible to test and correct existing models, taking out or adding helices and/or base pairs as appropriate. More recently, expansion of the sequence dataset has made it possible to identify * To whom correspondence should be addressed a number of tertiary pairings. The current version of the E. coli 23S rRNA secondary structure is the culmination of over ten years of analysis [7,8]; all of the secondary structure pairings and proposed tertiary interactions are now strongly supported by comparative data. We anticipate, however, that additional tertiary interactions will continue to be discovered as new LSU rRNA sequences appear. The evolutionary process has affected the size as well as the primary structure of LSU rRNAs. The smallest such RNAs are those found in the kinetoplast (mitochondrion) of the trypanosomatid flagellates, such as Crithidia fasciculata (1141 nt), while the largest are those in the cytoplasmic ribosomes of vertebrates, e.g., humans (5182 nt; 5.8S + 28S). While comparative analysis has defined a core of higher-order structure common to all LSU rRNAs, certain other structures are found only within particular phylogenetic subsets. Elucidation of these phylogenetically restricted structures requires comparison of at least several related LSU rRNA sequences (the number depending on the rate at which such structures are diverging). In the case of those LSU rRNAs comparable in size to E. coli 23S rRNA, secondary structures have been modeled in their entirety. Larger LSU rRNAs (eucaryotic cytoplasmic and some mitochondrial) contain apparent insertions relative to the E. coli structure. Within the past year, a number of these previously unstructured regions have been configured by comparative methods. As additional LSU rRNA sequences are determined, especially within localized phylogenetic divisions, we anticipate that each remaining unstructured region will be resolved. It is of interest that within the eucaryotic nucleocytoplasmic lineage, several of these recently structured regions are common only to a relatively narrow phylogenetic grouping. All secondary structures follow the convention and layout established for the E. coli 23S rRNA model, the de facto reference structure. The majority of homologous primary and secondary structure features are displayed in an analogous graphical manner to emphasize this structural homology. In a small number of cases, due to insertion/deletion events, this graphical representation varies somewhat for structural elements deemed to be homologous. In future editions of this secondary structure compendium, we will begin to incorporate tertiary interactions that satisfy comparative criteria. 2096 Nucleic Acids Research, Vol. 20, Supplement AVAILABILITY AND STATUS OF STRUCTURE FIGURES As in [2], the actual 23S rRNA secondary structures are not published here. Instead, readers will find (i) a table of complete LSU rRNA sequences, grouped according to phylogenetic division and including GenBank/EMBL Accession Numbers (Table 2), and (ii) a publication reference list for these sequences. The comprehensive set of LSU rRNA secondary structures may be obtained in one of two ways. Hardcopy printouts of this set are available directly from us (inquiries should be referred to M.W.G. at the address listed below). Release 1.0, which comprises 88 structures (see Table 2), is immediately available. This release contains virtually finalized archaebacterial, eubacterial and plastid structures. Mitochondrial structures have been extensively revised from those first presented in [1], but a further round of (relatively minor) revision is necessary before these models will be in final form. Eukaryotic cytoplasmic structures in Release 1.0 are largely unchanged from those given in [1]; an exception is the newly modeled Euglena gracilis cytoplasmic secondary structure [9], which does contain revisions that are being incorporated into the secondary structures of other nucleus-encoded LSU rRNAs. Newly modeled and refined LSU rRNA secondary structures will be included in Release 2.0, hardcopies of which should be ready for distribution before the end of 1992. Inquiries about hardcopy printouts should state explicitly which Release (1.0 or 2.0) is being requested. Alternatively, individuals with access to the Internet telecommunications network and a laser printer capable of processing PostScript™ files may elect to obtain files of LSU rRNA secondary structures by anonymous file transfer protocol (ftp). These files are deposited with the Ribosomal RNA Database Project [10] on the RDP computer at the Argonne National Laboratory, and may be accessed as indicated below. Inquiries concerning this on-line service may be directed to R.R.G. (e-mail and postal addresses as noted below). As time and facilities permit, the rRNA information available on-line will be increased. Initially, it will include the complete set of LSU rRNA secondary structures (in PostScript™ format), the table of LSU rRNA sequences and their accession numbers, and the associated publication reference list. Refinements to existing secondary structures as well as newly modeled secondary structures will be released on-line as soon as we have completed our own analysis. From time to time, we will also update the associated table and reference list. Currently we include only those LSU rRNA sequences that are complete (or nearly so). ACCURACY OF THE DATA Ambiguous positions in a published sequence are specified according to the nomenclature recommended by IUPAC (e.g., Y = pyrimidine ; R = purine; etc.). As noted in Table 2 and the List of References, there are independently determined versions of the same primary sequence for several LSU rRNAs. Usually, these alternative versions differ from one another at a number of positions, and at least some of these differences are likely to be sequencing errors. Often, the secondary structure predicts which version of the sequence is likely to be correct at a particular position. On the other hand, it is probable that some of the variation actually reflects genuine inter- or intra-strain sequence heterogeneity, particularly if the differences occur within variable regions [11]. We have also noted that a few published primary sequences differ at one or more positions from their GenBank/EMBL listings, without an indication that the database entry represents a subsequently revised version of the original published sequence. Again, secondary structure modeling may or may not indicate which version is likely to be correct. It is our intent to provide brief annotation in the hardcopy and electronic versions of the secondary structure figures to indicate which version of the primary sequence has been used at discrepant positions. In compiling the reference list, we have checked each of these citations against the original published paper. We note that citation information in the GenBank/EMBL database is occasionally inaccurate, and for that reason we have provided complete references, including titles. Finally, we invite further comments from readers, and welcome suggested revisions/alternative interpretations to the proposed secondary structures, as well as suggestions for improvement in the content and/or form of the database. We also solicit newly determined LSU rRNA sequences in advance of publication, in order to accelerate their inclusion in the compendium. ACKNOWLEDGMENTS We gratefully acknowledge the computer programming expertise of Bryn Weiser and Tom Macke in this endeavor. Work on this compendium by M.N.S. and M.W.G. is supported by an operating grant (MT-11212) from the Medical Research Council of Canada to M.W.G. We thank the Canadian Institute for Advanced Research (CIAR) for providing funds in support of the production and distribution of secondary structure figures. M.W.G. is a Fellow and R.R.G. is an Associate in the Program in Evolutionary Biology of the CIAR. We also thank the W.M.Keck Foundation for their generous support of RNA science on the Boulder campus. REQUESTS For hard copies of LSU rRNA secondary structures, either the complete compilation or selected portions thereof (please specify Release 1.0 or 2.0): M.W. Gray, Department of Biochemistry, Sir Charles Tupper Medical Building, Dalhousie University, Halifax, Nova Scotia B3H 4H7, Canada. FAX: (902)494-1355 e-mail: [email protected] (via Bitnet) For information about on-line availability of LSU rRNA secondary structure files and other information contained in this compendium: R.R. Gutell, Molecular, Cellular, and Developmental Biology, Campus Box 347, University of Colorado, Boulder, Colorado 80309, U.S.A. FAX: (303)492-7744 e-mail: [email protected] Nucleic Acids Research, Vol. 20, Supplement 2097 To obtain PostScript™ files of LSU rRNA secondary structures via anonymous ftp on the Internet telecommunications network: ftp site: info.mcs.anl.gov directory: /pub/RDP/Contrib/RobinGutell REFERENCES 1. Gutell,R.R. and Fox,G.E. (1988) Nucleic Acids Res. 16, Supplement, rl75-r269. 2. Gutell.R.R., Schnare.M.N. and Gray,M.W. (1990) Nucleic Acids Res. 18, Supplement, 2319-2330. 3. Brosius,J., Dull.T.J. and Noller.H.F. (1980) Proc. Nail. Acad. Sci. U.S.A. 77, 201 -204. 4. Glotz.C, Zwieb.C, Brimacombe.R., Edwards, K. and Kossel.H. (1981) Nucleic Acids Res. 9, 3287-3306. 5. Branlant.C, Krol.A., Machatt.M.A., Pouyet,J., Ebel,J.-P., Edwards.K. and K6ssel,H. (1981) Nucleic Acids Res. 9, 4303-4324. 6. Noller.H.F., Kop,J., Wheaton,V., BrosiusJ., Gutell,R.R., Kopylov.A.M., Dohme,F., Herr.W., Stahl.D.A., Gupta.R. and Woese.C.R. (1981) Nucleic Acids Res. 9, 6167-6189. 7. Larsen,N. (1992) Proc. Natl. Acad. Sci. U.S.A., in press. 8. Gutell.R.R., Larsen,N. and Woese.C.R. (1992) In Ribosomal RNA: Structure, Evolution, Gene Expression and Function in Protein Synthesis (Zimmermann,R.A. and Dahlberg,A.E., eds), The Telford Press, Caldwell, N.J., in press. 9. Schnare,M.N. and Gray.M.W. (1990)7. Mol. Biol. 215, 73-83. 10. Olsen.G.J., Larsen,N. and Woese.C.R. (1991) Nucleic Acids Res. 19, Supplement, 2017-2021. 11. Gonzalez,].L., Gorski.J.L., Campen,T.J., Dorney.D.J., Erickson.J.M., Sylvester.J.E. and Schmickel.R.D. (1985) Proc. Natl. Acad. Sci. U.S.A. 82, 7666-7670. The present publication should be quoted as reference for secondary structure data obtained either as hard copies from the authors or from the electronically accessible compilation. 2098 Nucleic Acids Research, Vol. 20, Supplement Table 1. Growth of the LSU rRNA database Archaebactenal Eubacterial Plastid Mitochondria] Eukaryotic (nuclear) All 1988 1990 1992 6 5 4 17 10 42 7 13 12 21 13 54 28 128 8 27 16 71 Table 2. List of complete LSU rRNA sequences Organism name 1 Status2 Accession Number ARCHAEBACTERIA (ARCHAEA 3 ) Euryarchaeota 3 Archaeoglobus fulgidus Halobacterium halobium Halobacterium marismortui Halococcus morrhuae Methanobacterium thermoautotrophicum Methanococcus vannielii Methanospirillum hungatei Thermoplasma acidophilum *# + + + + + *# +# M64487 X00872,X03407 X13738 X05481 X15364 X02729 M61738,M81323 M20822,M32298 Desulfurococcus mobilis Sulfolobus solfataricus Thermofilum pendens Thermoproteus tenax + *# +# + X05480 M67495 X14835 +# M55343 X06484 X56657 M27245 X55435.X61478 Crenarchaeota3 EUBACTERIA (BACTERIA 3 ) Gram positive bacteria 4 High G+C subdivision Frankia sp. Micrococcus luteus Mycobacterium leprae Streptomyces ambofaciens Streptomyces griseus Low G+C subdivision Bacillus sp. Bacillus stearothermophilus Bacillus subtilis Purple photosynthetic bacteria and their relatives 4 Alpha subdivision Rhodobacter capsulatus Rhodobacter sphaeroides Beta subdivision Pseudomonas cepacia Gamma subdivision Escherichia coli Pseudomonas aeruginosa Ruminobacter amylophilus *# *# X60981 K02663 K00637,M10606,X00007 +# X06485 X53853,X53854,X53855 X16368 J01695 Y00432 X06765 Nucleic Acids Research, Vol. 20, Supplement 2099 Organism name1 Spirochetes and their relatives 4 Leptospira interrogans Bacteroides, flavobacteria and cytophagas and relatives 4 Flavobacterium odoratum Flexibacter flexilis Cyanobacteria 4 Anacystis nidulans Green sulfur bacteria 4 Chlorobium limicola Planctomyces and their relatives 4 Pirellula marina Radio-resistant micrococci4 Thermus thermophilus Status2 Accession Number + X14249 +# +# M32365.M62807 M31904.M62806 + X00343,X00512 +# M31904,M62805 + X07408 + X12612 PLASTIDS Protoctista 5 Apicomplexa6 Plasmodium falciparum6 Euglenophyta (euglenoid flageUates) Astasia longa Euglena gracilis Chlorophyta (unicellular green algae) Chlamydomonas eugametos Chlamydomonas reinhardtii Chlorella ellipsoidea X61660 + + X14386 X13310 *# + + X15727,X16686,X16687 M36158 + X01647.X04465 *# *# + + +# + M76448,M75722,M75719 X59768 J01446.Z00044 X15901 M37430 X01365 + +# + + + X02548 X51736 X02354 J03814 X02547 + M22649,M25123-25130,X54860 + + +# K00634 K01749,X15917 M58010.M58011 Plantae Bryophyta Marchantia polymorpha (liverwort) Angiospermophyta (flowering plants) Alnus incana (alder) Conopholis americana Nicotiana tabacum (tobacco) Oryza sativa (rice) Pisum sativum (pea) Zea mays (maize) MITOCHONDRIA Protoctista 5 Zoomastigina (zooflagellates) Crithidia fasciculata Crithidia oncopelti Leishmania tarentolae Leptomonas sp. Trypanosoma brucei Chlorophyta (unicellular green algae) Chlamydomonas reinhardtii Ciliophora (ciliates) Parameciiim primaurelia Paramecium tetraurelia Tetrahymena pyriformis 2100 Nucleic Acids Research, Vol. 20, Supplement Organism name1 Status2 Accession Number Aspergillus nidulans Neurospora crassa Podospora anserina Saccharomyces cerevisiae Schizosaccharomyces pombe + +# + + + Fungi Ascomycota X06961 X55443 M30937.X14735 J01527 X06597 Plantae Bryophyta Marchantia polymorpha (liverwort) Angiospermophyta (flowering plants) Oenothera berteriana (primrose) Triticum aestivum (wheat) Zea mays (maize) M68929 + + + X02559 M37274 K01868 *# *# X54253 X54252 + + + +# + + *# X01078 X05011 M21833.X12965 X53506 X03240 X05287 M76713 + + J04815 X12631 • # M86496 M55540 X61145 J01394 M86494 M55541 M86498 M35875 X61010 M86499 X52392 M86501 J01415,M12548,V00710 M35876 M86497 M86495 M35877 J01420 M35874 M86500 X12841 Animalia Nematoda Ascaris suum Caenorhabditis elegans Arthropoda Aedes albopictus (mosquito) Apis mellifera (honeybee) Anemia salina (brine shrimp) Drosophila melanogaster (fruit fly) Drosophila yakuba (fruit fly) Locusta migratoria (locust) Spodoptera frugiperda Echinodermata (sea urchins) Paracentrotus Hvidus Strongylocentrotus purpuratus Chordata Aepyceros melampus Antilocapra americana Balaenoptera physalus (fin whale) Bos taurus (ox) Boselaphus tragocamelus Capra hircus (goat) Cephalophus maxwelli Cervus unicolor (sambar deer) Cyprinus carpio (carp) Damaliscus dorcas Gallus gallus domesticus (chicken) Gazella thomsoni Homo sapiens (human) Hydropotes inermis (Chinese water deer) Kobus ellipsiprymnus Madoqua Idrki Muntiacus reevesi (Reeves' muntjac) Mus musculus (mouse) Odocoileus virginianus (white-tailed deer) Oryx gazella Rana catesbeiana (frog) +# *# + *# +# *# +# *# *# +# •# + +# *# *# +# + +# *# + Nucleic Acids Research, Vol. 20, Supplement 2101 Organism name1 Rattus norvegicus (rat) Tragelaphus imberbis Tragulus napu Xenopus laevis (toad) Status2 Accession Number *# +# J01438 M86493 M55539 M10217 EUCARYOTES (EUCARYA3) (NUCLEOCYTOPLASMIC) Archezoa7 Giardia ardeae Giardia intestinalis Protoctista5 Dinoflagellata (dinoflagellates) Prorocentrum micans Euglenophyta (euglenoid flagellates) Euglena gracilis Zoomastigina (zooflagellates) Crithidia fasciculata Trypanosoma brucei Ciliophora (ciliates) Tetrahymena pyriformis Tetrahymena thermophila Acrasiomycota (cellular slime molds) Dictyostelium discoideum Myxomycota (plasmodial slime molds) Didymium iridis Physarum polycephalum *# *# X58290 X52949 * X15973,X16108 +# X53361 + *# Y00055 X14553 *# +# M10752,X54004 X54512 X00601 *# + X60210 V01159 Fungi Zygomycota Mucor racemosus M26190 Ascomycota Saccharomyces carlsbergensis Saccharomyces cerevisiae Plantae Angiospermophyta (flowering plants) Arabidopsis thaliana Citrus limon (lemon) Fragaria ananassa (strawberry) Lycopersicon esculentum (tomato) Oryza sativa (rice) Sinapsis alba (mustard) + * V01285 J01355,K01048 *# * *# * + *# X52320 X05910 X15589.X58118 X07889.X13557 Ml 1585 X15915.X57137 Animalia Nematoda Caenorhabditis elegans X03680 Arthropoda Drosophila melanogaster M21017 Chordata Herdmania momus Homo sapiens (human) Mus musculus (mouse) X53538 J01866.M11167 J01871.X00525 2102 Nucleic Acids Research, Vol. 20, Supplement Organism name 1 Status2 Accession Number Rattus norvegicus (rat) + Xenopus borealis (toad) Xenopus laevis (toad) *# + J01881,K01591,X00521, X01069 X59733 K01376,X00136,X59734 'Eucaryotic organisms are classified according to the scheme of Margulis.L. and Schwartz.K.V. (1988) [Five Kingdoms. An Illustrated Guide to the Phyla of Life on Earth (2nd edition). W.H. Freeman and Co., New York]. 2 New listings that did not appear in the previous edition [Gutell.R.R., Schnare.M.N. and Gray.M.W. (1990) Nucleic Acids Res. 18, Supplement, 2319—2330] are denoted by ' #'. Secondary structures now available inhardcopy form in Release 1.0 are denoted by ' + ', while newly modeled structures that will be included in future releases are indicated by '*'. 3 See Woese.C.R., Kandler.O. and Wheelis,M.L. (1990) Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Nail. Acad. Sci. U.S.A. 87, 4576-4579. 4 See Woese,C.R., Stackebrandt,E., Macke.T.J. and Fox, G.E. (1985) A phylogenetic definition of the major eubacterial taxa. System. Appl. Microbiol. 6, 143-151. 5 The term 'Protoctista', as defined and used by Margulis and Schwartz (1988), includes but is not limited to the 'Protista' (unicellular eucaryotes, or protists). 6 See note in List of References, below. 7 See Cavalier-Smith.T. (1987) Eukaryotes with no mitochondria. Nature 326, 332-333. List of references to LSU rRNA sequences (# = new this edition) ARCHAEBACTERIA Archaeoglobus fulgidus #Woese,C.R., Achenbach.L., Rouviere.P. and Mandelco.L. (1991) System. Appl. Microbiol. 14, 364-371. Archaeal phylogeny: reexamination of the phylogenetic position of Archaeoglobus fulgidus in light of certain composition-induced artifacts. Desulfumcoccus mobUis Leffers.H., Kjems.J., Ostergaard.L., Larsen.N. and Garrett.R.A. (1987) J. Mol. Biol. 195, 4 3 - 6 1 . Evolutionary relationships amongst archaebacteria. A comparative study of 23 S ribosomal RNAs of a sulpur-dependent extreme thermophile, an extreme halophile and a thermophilic methanogen. Halobacterium halobium Mankin.A.S. and Kagramanova.V.K. (1986) Mol. Gen. Genet. 202, 152-161. Complete nucleotide sequence of the single ribosomal RNA operon of Halobacterium halobium: secondary structure of the archaebacterial 23S rRNA. Halobacterium marismortui Brombach.M., Specht.T., Erdmann.V.A. and Ulbrich.N. (1989) Nucleic Acids Res. 17, 3293. Complete nucleotide sequence of a 23S ribosomal RNA gene from Halobacterium marismortui. Halococcus morrhuae (see Desulfumcoccus mobilis) Methanobacterium thermoautotrophicum (see Desulfumcoccus mobilis) Methanococcus vannielii Jarsch.M. and Bock.A. (1985) Mol. Gen. Genet. 200, 305-312. Sequence of the 23S rRNA gene from the archaebacterium Methanococcus vannielii: evolutionary and functional implications. Methanospirillum hungatei #Burggraf,S., Ching.A., Stetter,K.O. and Woese.C.R. (1991) System. Appl. Microbiol. 14, 358-363. The sequence of Methanospirillum hungatei 23S rRNA confirms the specific relationship between the extreme halophiles and the Methanomicrobiales. Sulfolobus solfalaricus # Woese.C.R. Unpublished. ThermofUum pendens #Kjems,J., Leffers.H., Olesen.T., Holz,I. and Garrett.R.A. (1990) System. Appl. Microbiol. 13, 117-127. Sequence, organization and transcription of the ribosomal RNA operon and the downstream tRNA and protein genes in the archaebacterium Thermofilum pendens. Thermoplasma acidophilum tfRee.H.K. and Zimmermann,R.A. (1990) Nucleic Acids Res. 18, 4471-4478. Organization and expression of the 16S, 23S and 5S ribosomal RNA genes from the archaebacterium Thermoplasma acidophilum. Thermopmteus tenax Kjems,J., Leffers.H., Garrett.R.A., Wich.G., Leinfelder.W. and Bock A. (1987) Nucleic Acids Res. 15, 4821-4835. Gene organization, transcription signals and processing of the single ribosomal RNA operon of the archaebacterium Thermoproteus tenax. EUBACTERIA Anacystis nidulans Kumano.M., Tomioka,N. and Sugiura.M. (1983) Gene 24, 219-225. The complete nucleotide sequence of a 23S rRNA gene from a blue-green alga, Anacystis nidulans. Douglas.S.E. and Doolittle.W.F. (1984) Nucleic Acids Res. 12, 3373-3386. Complete nucleotide sequence of the 23S rRNA gene of the Cyanobacterium, Anacystis nidulans. Nucleic Acids Research, Vol. 20, Supplement 2103 Bacillus sp. #Fink,P.S., Zhao.Y., Prochaska.L.J. and Leffak.M. (1991) Nucleic Acids Res. 19, 5437. Nucleotide sequence of a 23S and a 5S-like rRNA gene from the thermophilic Bacillus sp.strain PS3. Bacillus stearothermophiius Kop,J., Wheaton,V., Gupta.R., Woese.C.R. and Noller.H.F. (1984) DNA 3, 347-357. Complete nucleotide sequence of a 23S ribosomal RNA gene from Bacillus stearolhermophilus. Bacillus subtilis Green.C.J., Stewart.G.C, Hollis.M.A., Vold.B.S. and Bott,K.F. (1985) Gene 37, 261-266. Nucleotide sequence of the Bacillus subtilis ribosomal RNA operon, rmB. Chlorobium limicola #Woese,C.R., Mandelco.L., Yang,D., Gherna,R. and Madigan,M.T. (1990) System. Appl. Microbiol. 13, 258-262. The case for relationship of the Flavobacteria and their relatives to the green sulfur bacteria. Escherichia coli Brosius,J., Dull.T.J. and Noller.H.F. (1980) Proc. Natl. Acad. Sci. U.S.A. 77, 201-204. Complete nucleotide sequence of a 23S ribosomal RNA gene from Escherichia coli. Branlant,C, Krol,A., Machatt.M.A., Pouyet.J., Ebel,J.-P., Edwards.K. and Kossel.H. (1981) Nucleic Acids Res. 9, 4303-4324. Primary and secondary structures of Escherichia coli MRE 600 23S ribosomal RNA. Comparison with models of secondary structure for maize chloroplast 23S rRNA and for large portions of mouse and human 16S mitochondrial rRNAs. Flavobacterium odoratum (see Chlorobium limicola) Flexibacter flexilis (see Chlorobium limicola) Frankia sp. # Normand.P. Unpublished. Leptospira interrogans Fukunaga,M., Horie,!. and Mifuchi.I. (1989) Nucleic Acids Res. 17, 2123. Nucleotide sequence of a 23S ribosomal RNA gene from Leptospira interrogans serovar canicola strain Moulton. Micrococcus luteus Regensburger.A., Ludwig,W., Frank.R., Blocker.H. and Schleifer.K.H. (1988) Nucleic Acids Res. 16, 2344. Complete nucleotide sequence of a 23S ribosomal RNA gene from Micrococcus luteus. Mycobacterium leprae #Liesack,W., Sela,S., Bercovier.H., Pitulle.C. and Stackebrandt,E. (1991) FEBS Lett. 281, 114-118. Complete nucleotide sequence of the Mycobacterium leprae 23 S and 5 S rRNA genes plus flanking regions and their potential in designing diagnostic oligonucleotide probes. Pirellula marina Liesack.W., Hopfl.P. and Stackebrandt.E. (1988) Nucleic Acids Res. 16, 5194. Complete nucleotide sequence of a 23S ribosomal RNA gene from Pirellula marina. Pseudomonas aeruginosa Toschka.H.Y., Hopfl.P., Ludwig.W., Schleifer.K.H., Ulbrich.N. and Erdmann.V.A. (1987) Nucleic Acids Res. 15, 7182. Complete nucleotide sequence of a 23S ribosomal RNA gene from Pseudomonas aeruginosa. Pseudomonas cepacia Hopfl.P., Ludwig.W., Schleifer.K.H. and Larsen.N. (1989) Eur. J. Biochem. 185, 355-364. The 23S ribosomal RNA higher-order structure of Pseudomonas cepacia and other prokaryotes. Rhodobacter capsulatus Hopfl.P., Ludwig.W. and Schleifer.K.H. (1988) Nucleic Acids Res. 16, 2343. Complete nucleotide sequence of a 23S ribosomal RNA gene from Rhodobacter capsulatus. Rhodobacter sphaeroides #Dryden,S.C. and Kaplan.S. (1990) Nucleic Acids Res. 18, 7267-7277. Localization and structural analysis of the ribosomal RNA operons of Rhodobacter sphaeroides. Ruminobacter amylophilus Spiegl.H., Ludwig.W., Schleifer.K.H. and Stackebrandt.E. (1988) Nucleic Acids Res. 16, 2345. Complete nucleotide sequence of a 23S ribosomal RNA gene from Ruminobacter amylophilus. Streptomyces ambofaciens Pernodet,J.-L., Boccard.F., Alegre,M.-T., Gagnat.J. and Guerineau.M. (1989) Gene 79, 33-46. Organization and nucleotide sequence analysis of a ribosomal RNA gene cluster from Streptomyces ambofaciens. Streptomyces griseus #Kim,E. Unpublished. Thermus thermophUus H6pfl,P., Ulrich.N., Hartmann,R.K., Ludwig.W. and Schleifer.K.H. (1988) Nucleic Acids Res. 16, 9043. Complete nucleotide sequence of a 23S ribosomal RNA gene from Thermus thermophUus HB8. PLASTIDS Alnus incana #Levesque,M. and Johnson,D.A. Unpublished. Sequence of the chloroplast 23S rRNA gene from the alder Alnus incana. Astasia longa #Siemeister,G. and Hachtel.W. (1990) Curr. Genet. 17, 433-438. Organization and nucleotide sequence of ribosomal RNA genes on a circular 73 kbp DNA from the colourless flagellate, Astasia longa. 2104 Nucleic Acids Research, Vol. 20, Supplement Chlamydomonas eugametos #Turmel,M., Boulanger.J., Schnare.M.N., Gray.M.W. and Lemieux.C. (1991) J. Mol. Biol. 218, 293-311. Six group I introns and three internal transcribed spacers in the chloroplast large subunit ribosomal RNA gene of the green alga Chlamydomonas eugametos. Chlamydomonas reinhardtii Lemieux,C, Boulanger.J., Otis.C, and Turmel.M. (1989) Nucleic Acids Res. 17, 7997. Nucleotide sequence of the chloroplast large subunit rRNA gene from Chlamydomonas reinhardtii. Chlorella ellipsoidea YamadaX and Shimaji.M. (1987) Curr. Genet. 11, 347-352. An intron in the 23S rRNA gene of the Chlorella chloroplasts: Complete nucleotide sequence of the 23S rRNA gene. Conopholis americana. #Wimpee,C.F., Morgan,R. and Wrobel.R. (1992) Plant Mol. Biol. 18, 275-285. An aberrant plastid ribosomal RNA gene cluster in the root parasite Conopholis americana. Euglena gracilis Yepiz-Plascencia.G.M., Jenkins.M.E. and Hallick.R.B. (1988) Nucleic Acids Res. 16, 9340. 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