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Nucleic Acids Research, 1993, Vol. 21, No. 13 3055-3074
A compilation of large subunit (23S and 23S-like)
ribosomal RNA structures: 1993
Robin R.Gutell*, Michael W.Grayl* and Murray N.Schnare1
Molecular, Cellular, and Developmental Biology, Campus Box 347, University of Colorado, Boulder,
CO 80309-0347, USA and 'Department of Biochemistry, Dalhousie University, Halifax, Nova Scotia
B3H 4H7, Canada
INTRODUCTION
This compilation is part of an on-going effort to maintain a
comprehensive and continually updated collection oflarge subunit
(LSU; 23S and 23S-like) rRNA secondary structures and
associated sequence and citation information. Table 1 gives a
breakdown of the number and phylogenetic distribution of
sequences currently in this LSU rRNA database. A listing of
accession numbers for all complete LSU rRNA sequences now
in the public domain is presented in Table 2. The reference list
is an update ofthe information provided in the 1992 compilation
[1]; here, we include only revised or new citations to LSU rRNA
sequences. The complete bibliography of LSU rRNA sequences
is available electronically, as is the complete listing ofaccession
numbers presented in Table 1 (see below for instructions on how
to obtain this information).
GROWTH OF THE DATABASE
The past year has seen the largest annual increase in the number
of LSU rRNA sequences published and/or released through the
EMBL, GenBank and DDBJ databanks (Table 1). This trend has
also been apparent in each of the previous years we have
monitored, emphasizing the steady increase in the rate at which
LSU rRNA sequences are being determined. The rate ofgrowth
within each of the phylogenetic categories does vary, however.
In the period covered by the present compilation, more than half
(34/66) of the new sequences that appeared were (eu)bacterial
ones. The second largest increase occurred in the Plastids
category, due primarily to the release of 15 new Chlamydomonas
chloroplast sequences. In the previous year, the greatest increases
were in mitochondrial and eucaryotic (nuclear) sequences.
Mitochondrial sequences still constitute the largest single category
in the LSU rRNA database, as they have in every previous
compilation.
MODELS OF HIGHER-ORDER STRUCTURE
As in previous compilations [1-3], each LSU rRNA primary
sequence is presented in a two-dimensional format (the secondary
structure) that underpins the biologically relevant conformation
of an rRNA molecule. When LSU rRNA sequences are
configured in this manner, phylogenetic information becomes
readily apparent, as do patterns of variability and conservation
in sequence and structure. At the same time, the secondary
structure serves as an effective template for relating form to
function. Principles for deducing higher-order structure have been
enunciated in previous compilations [1-3] (see also [4-6]).
Three phylogenetically and structurally distinct examples of
current LSU rRNA secondary structures are presented in this
communication. They are: (i) Escherichia coli, a typical
(eu)bacterial structure (our reference standard, to which other
LSU rRNA structures are compared and against which they are
modelled); (ii) Saccharomyces cerevisiae (yeast), a representative
eucaryotic (nucleocytoplasmic) structure; and (iii) a 'minimalist'
structure, typified by the unusually small mitochondrial LSU
rRNA from the nematode worm, Caenorhabditis elegans. While
the latter two structures exemplify the tpe ofsize variation found
among LSU rRNAs, an even smaller and quite peculiar structure
has been described for the mitochondrial LSU rRNA of
trypanosomatid protozoa (Trypanosoma, Leishumaia, Crithidia).
At the other extreme, LSU rRNA structures larger than the
S.cerevisiae nuclear one can be found; these are primarily
mammalian nucleocytoplasmic ones, which contain large
insertions at the positions of some ofthe variable regions oftheir
S.cerevisiae counterpart.
Due to the extensive sequence and size differences within some
ofthe mitochondrial and eucaryotic variable regions, and the lack
of a sufficient number of phylogenetically close examples from
which to deduce significant primary and secondary structure
homology within these variable regions, some ofthem had been
left unstructured in previous compilations. However, with the
recent large increase in the number of available LSU rRNA
sequences, we have now deduced sequence and structural
homology for many of these variable regions. Because we have
a high degree of confidence in these newly solved structures,
structural variation and evolution in these mitochondrial and
nucleocytoplasmic LSU rRNAs can now be examined critically
and in depth. The results of these analyses will be published in
due course, along with other LSU rRNA structural characteristics
that distinguish the different phylogenetic assemblages.
At the same time that they permit the elucidation ofsecondary
structure pairings, comparative methods allow one to infer teriary
interactions. The three LSU rRNAs presented in this compendium
display all ofthe currendy known secondary and tertary structure
constraints. A small but growing number ofthese newer and more
* To whom correspondence should be addressed
.=/ 1993 Oxford University Press
3056 Nucleic Acids Research, 1993, Vol. 21, No. 13
complex structural elements have been experimentally verified
[4,5], thereby justifying the application of these comparative
methods. New and more powerful correlation analysis algoritms
are now being developed [6,7; R.R. Gutell, unpublished] and
promise to extend our appreciation of the structural (and other)
constraints acting on these LSU rRNAs.
In the immediate future we anticipate a continuing steady
increase in the number of available LSU rRNA sequences (and
thus their structures), in parallel with additional refinements in
each of these structures. The information provided should lead
us to higher-resolution structures and new insights into how they
evolved.
ACCURACY OF THE DATA
As noted previously [1], independently determined versions of
the same primary sequence exist for several LSU rRNAs (see
Table 2 and the List of References). 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
a 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 witiin variable regions [8].
We have also noted that a few published primary sequences differ
at one or more positions from their GenBank/EMBL/DDBJ
listings, without an indication that the database entry represents
a subsequently revised version ofthe original published sequence.
Again, secondary structure modelling may or may not indicate
which version is likely to be correct. This year, the List of
References contains brief [NOTES] on individual sequences,
where discrepancies between different versions of the same
sequence or between published and database entries ofthe same
sequence are noted. In cases ofnon-identical versions ofthe same
sequence, the reader is referred to these notes for information
on which sequence was used for the secondary structures we
present.
AVAILABILITY AND STATUS OF STRUCTURE
FIGURES
As in [1] and [2], the actual 23S and 23S-like rRNA secondary
structures are not published here, except for the three examples
shown. The comprehensive set of LSU rRNA secondary
structures may be obtained in one of two ways. Hardcopy
printouts ofthis set are available directly from us (inquiries
should be referred to M.W.G. at the address listed below).
Release 1.0, which comprised 88 structures, was made available
for distribution in July, 1991, and copies may still be obtained.
Newly modeled and refined LSU rRNA secondary structures are
included in Release 2.0 (January, 1993), which contains 51
structures (13 archaebacterial, 18 eubacterial, 13 plastid, 3
mitochondrial and 4 eucaryotic nuclear). Those structures
available in Release 1.0 and 2.0 are noted in Table 2. The next
release (2.1) will comprise considerably revised and updated
eucaryotic nuclear structures, whereas subsequent releases will
contain revised mitochondial structures (Release 2.2) and models
ofnew prokaryotic (archaebacterial and eubacterial) and plastid
sequences (Release 2.3). Requests for hardcopy printouts,
which will be sent out as soon as they become available, should
state explicitly which Release (1.0,2.1-2.3) is being sought.
Anyone who is on our current mailin ist should already have
received Release 2.0 and will automatically receive future
releases.
Alternatively, individuals with access to the Internet
telecommunications network and a laser printer capable of
processing PostScript.m 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 [9] 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. Currently it includes the set of LSU
rRNA secondary structures (in PostScriptrm format) that are
available in hard copy in Release 2.0, 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).
Finally, we invite comments from readers, and welcome
suggested revisions to and/or alternative interpretations of our
proposed secondary structures, as well as suggestions for
improvement in the content and/or form ofthe database. We also
solicit newly determined LSU rRNA sequences in advance of
publication, in order to accelerate their inclusion in the
compendium.
ACKNOWLEDGEMENTS
We gratefully acknowledge the computer propmming expertise
ofBryn Weiser and Tom Macke in this endeavor. Work on this
compendium has been supported by an operating grant
(MT-11212) from the Medical Research Council of Canada to
M.W.G. and by NIH grant GM48207 to R.R.G., who also
acknowledges a generous donation ofcomputer equipment from
SUN Microsystems. We thank the W.M. Keck Foundation for
their generous support ofRNA science on the Boulder campus,
and the Canadian Institute for Advanced Research (CIAR) for
providing funds in support ofthe 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.
REFERENCES
1. Gutell,R.R., Schnare,M.N. and Gray,M.W. (1992) NucleicAcids Res. 20,
Supplement, 2095-2109.
2. Gutell,R.R., Schnare,M.N. and Gray,M.W. (1990) NucleicAcids Res. 18,
Supplement, 2319-2330.
3. Gutell,R.R. and Fox,G.E. (1988) Nucleic Acids Res. 16, Supplemet,
r175-r269.
4. Gutell,R.R. In Nierhaus,K.H., Subramann,A.R., Erdmann,V.A.,
Franceschi,F., and Wittman-Liebold,B. (eds.). The TrnslationalApparatus.
Plenum, in press.
5. Gutell,R.R., Larsen,N. and Woese,C.R. I Zimmermann,R.A. and
Dahlberg,A.E. (eds.). RibosomalRNA: Strucure, Ewuluion, Gene Epression
and Function in Protein Synthesis. CRC Press, Boca Raton, FL, in press.
6. Gutell,R.R., Power,A., Hertz,G.Z., Putz,E.J. and Stormo,G.D. (1992)
Nucleic Acids Res. 20, 5785-57-95.
7. Gutell,R.R. (1993) Curr. Opin. Struct. BioL 3, in press.
Nucleic Acids Research, 1993, Vol. 21, No. 13 3057
8. Gonzalez,I.L., Gorski,J.L., Campen,T.J., Domey,D.J., Erickson,J.M.,
Sylvester,J.E. and Schmickel,R.D. (1985) Proc. Natl. Acad. Sci. U.S.A.
82, 7666-7670.
9. Olsen,G.J., Overbeek,R., Larsen,N., Marsh,T.L., McCaughey,M.J.,
Maciukenas,M.A., Kuan,W.-M., Macke,T.J., Xing,Y. and Woese,C.R.
(1992) Nucleic Acids Res. 20, Supplement, 2199-2200.
REQUESTS
For hard copies of LSU rRNA secondary structures, either
the complete compilation or selected portions thereof
(please specify Release 1.0. 2.0. 2.1. 2.2 or 2.3):
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: mgray@ac.dal.ca (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 80309-0347, USA.
FAX: (303)492-7744
e-mail: rgutell@boulder.colorado.edu
To obtain PostScriptrm files of LSU rRNA secondary
structures via anonymous ftp on the Internet tele-
communications network:
ftp site: info.mcs.anl.gov
directory: /pub/RDP/LSU_rRNA/sec-struct
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.
3058 Nucleic Acids Research, 1993, Vol. 21, No. 13
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3060 Nucleic Acids Research, 1993, Vol. 21, No. 13
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Nucleic Acids Research, 1993, Vol. 21, No. 13 3061
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Nucleic Acids Research, 1993, Vol. 21, No. 13 3063
Table 1. Growth of the LSU rRNA Database
1988 1990 1992 1993
Archaea 6 7 12 13
Bacteria 5 13 21 55
Plastid 4 8 13 31
Mitochondria 17 27 54 61
Eucarya 10 16 28 34
All 42 71 128 194
Table 2. List of complete LSU rRNA sequences
Organism namel Status2 Accession Number
ARCHAEA3 (ARCHAEBACTERIA)
Euryarchaeota3
Archaeoglobus fulgidus 2.0 M64487
Halobacterinum halobiwn 2.0 X00872;X03407
Halobacterinu marismortui 2.0 X13738
Halococcus morrhuae 2.0 X05481
Methanobacterium thermoautotrophicum 2.0 X15364
Methanococcus vannielii 2.0 X02729
Methanospirillum hungatei 2.0 M61738;M81323
Thermococcus celer 2.0 * M67497
Thernoplasma acidophilum 2.0 M20822;M32298
Crenarchaeota3
Desulfurococcus mobilis 2.0 X05480
Sulfolobus solfataricus 2.0 M67495
Thermofilum pendens 2.0 X14835
Thennoproteus tenax 2.0
BACTERIA3 (EUBACTERIA)
Thermotogales4
Thermotoga maritima
Radio-resistant micrococci and relatives4
7hermus thernophilus
Spirochetes and relatives4
Planctomyces and relatives4
Green sulfur bacteria4
F.lexibacter-cytophaga-bacteroides
Purple bacteria4
Alpha subdivision
Beta subdivision
Gamma subdivision
Cyanobacteria4
Gram-positive phylum4
High G+C subdivision
2.0 *
2.0
2.0
1.0
Borrelia burgdorferi
Leptospira interrogans
Pirellula marina
Chlorobium limicola
phylum4
Flavobacteriwn odoratum
Flexibacterflexilis
1.0
1.0
1.0
Rhodobacter capsulatus
Rhodobacter sphaeroides
Bordetella avium
Bordetella bronchiseptica
Bordetella parapertussis
Bordetella pertussis
Neisseria gonorrhoeae
Neisseria meningitidis
Pseudomonas cepacia
Aeromonas hydrophila
Escherichia coli
Plesiomonas shigelloides
Pseudomonas aeruginosa
Pseudomonas perfectomarina
Ruminobacter amylophilus
Synechococcus sp. 6301 (Anacystis nidulans)
Frankiasp. #1
Frankia sp. #2
2.0
2.0
*
*
*
*
*
2.0
2.0
2.0 *
2.0
*
2.0
M67498
X12612
M88330
X14249
X07408
M31904;M62805
M32365;M62807
M31904;M62806
X06485
X53853 -55
X70370
X70371
X68368
X68323
X67293
X67300
X16368
X67946
J01695
X65487
Y00432
L03788
X06765
X00343;X00512
2.0 M55343
* M88466
3064 Nucleic Acids Research, 1993, Vol. 21, No. 13
Table 2. continued
Organism namel Status2 Accession Number
Micrococcus luteus 2.0 X06484
Mycobacterium kansasji * Z17212
Mycobacterium leprae 2.0 X56657
Streptomyces ambofaciens 2.0 M27245
Streptomyces griseus 2.0 M76388;X55435;X61478
Clostridial subdivision
Clostridium botulinun * X65602
Clostridium tyrobutyricum * L08062
Pectinatus frisingensis * X68423
Peptococcus niger * X68428
Mycoplasmas and relatives
Mycoplasma hyopneumoniae * X68421
Mycoplasma pneumoniae * X68422
Lactobacillus-bacillus-streptococcus phylum
Bacilus sp. (strain PS3) 2.0 X60981
Bacillus alcalophilus * D11459
Bacillus anthracis * X64645
Bacilus cereus * S43429
Bacilus globisporus * X68424
Bacillus licheniformis * X68433
Bacilus stearothermophilus 2.0 # K02663;S43424
Bacills subtilis (rmB) 2.0 K00637;M10606;X00007
Bacillus subtilis (rrn)) D11460
Lactobacilus delbrueckii * X68426
Lactococcus lactis subsp. cremoris * X68434
Lactococcus lactis subsp. klctis (strain EL1403) * X64887
Lactococcus lactis subsp. lactis (strain DSM 20481T) * X68435
Listeria monocytogenes * S46732;X64533;X68420
Staphylococcus aureus * X68425
Staphylococcus camosus * X68419
Streptococcus oralis * X68427
Streptococcus thermophilus * X68429
PLASTIDS
ProtocUsta5
Apicomplexa6
Chlorophyta (green algae)
Plasmodimwfainparum6
Chamydomonas 66.72
Chl(ydomonas eugametos
Chantdomonas frankii
Chamydomonas gelatinosa
Chlamydomonas geitkrii
Chlamydomonas humicola
Chlamydomonas indica
Chlanydomonas iyengarii
Chlamydomonas komma
Chlamydomonas mexicana
Chlamydomonas moewusii
Chlanydomonas pallidostigmatica
Chiamydomonas peterfli
Chlamydomonas pitschmanni
C7amydomonas reinharii
Chiamydomonas starii
Chiamydomonas zebra
Chlorella elipsoidea
Euglenophyta (euglenoid flagellates)
Phaeophyta (brown algae)
Rhodophyta (red algae)
Astasia longa
Euglena gracilis
Pylaiella littoralis
Pabnaria palnata
2.0 #
*
*
*
*
*
*
*
*
*
2.0
*
*
2.0
2.0
2.0 #
X61660
X68923-26
Z17234
X68905 -09
Z15151
X68891-92
X68921-22
X68893 -98
X68885 -86
X68927-29
X68910-12
X68913- 18
X68899-904
X68887-88
Z15152
X15727;X16686-87
X68889-90
X68919-20
M36158
X14386
X12890
X61179
Z18289
Plantae
Angiospermophyta (flowering plants)
Alnus incana (alder)
Conopholis americana
Epifagus Wrgiana (beechdrops)
Nicolia tbacum (tobacco)
2.0
2.0
2.0 *
2.0
M75719;M75722;M76448
X59768
M81884;X62099
J01446;Z00044
Nucleic Acids Research, 1993, Vol. 21, No. 13 3065
Organism name' Status2 Accession Number
Oryza sativa (rice) 2.0 X15901
Pisum sativum (pea) 2.0 M37430
Zea mays (maize) 2.0 X01365
Bryophyta
Marchantia polymorpha (liverwort) 2.0 X01647;X04465
MITOCHONDRIA
Protoctista5
Apicomplexa
Plasmodiwn falciparum
Plasmodium yoelii
Chlorophyta (unicellular green algae)
Chlamydomonas reinhardtii
Ciliophora (ciliates)
Paramecium primaurelia
Paramecium tetraurelia
Tetrahymena pyiformis
Zoomastigina (zooflagellates)
Crithidia fasciculata
Crithidia oncopelti
Leishmania tarentolae
Leptomonas sp.
Trypanosoma brucei
*
Plantae
Angiospermophyta (flowering plants)
Oenothera berteriana (primrose)
Triticum aestivum (wheat)
Zea mays (maize)
Marchantia polymorpha (liverwort)
Aspergillus nidulans
Neurospora crassa
Penicillium chrysogenum
Podospora anserina
Saccharomyces cerevisiae
Schizosaccharomyces pombe
Aedes albopictus (mosquito)
Apis mellifera (honeybee)
Artemia salina (brine shrimp)
Drosophila melanogaster (fruit fly)
Drosophila yakuba (fruit fly)
Locusta migratoria (locust)
Spodoptera frugiperda
Aepyceros melanmpus
Antilocapra americana
Balaenoptera physalus (fin whale)
Bos taurus (ox)
Boselaphus tragocamelus
Capra hircus (goat)
Carassius auratus
Cephalophus maxwelli
Cervus unicolor (sambar deer)
Crossostoma lacustre (freshwater loach)
Cyprinus carpio (carp)
Damnaliscus dorcas
Gallus gallus domesticus (chicken)
Gazella thomsoni
Homo sapiens (human)
Hydropotes inermis (Chinese water deer)
Kobus ellipsiprymnus
Madoqua kirki
Muntiacus reevesi (Reeves' muntjac)
Mus musculus (mouse)
Mytilus edulis (blue mussel)
M76611;M99416; S87790,/792,/801,/807,/809-10,
/833-34,/836-40
M29000
1.0 M22649;M25123 -25130;X54860
1.0 K00634
1.0 K01749;X15917
1.0 M58010;M58011
1.0 X02548
1.0 X51736
1.0 X02354
1.0 J03814
1.0 X02547
1.0 X02559
1.0 # M37274;Z11889
2.0 K01868
M68929
1.0 X06961
1.0 X55443
* D13859
1.0 M30937;X14735
1.0 J01527
1.0 X06597
1.0 X01078
1.0 # L06178;X05011
1.0 M21833;X12965
1.0 X53506
1.0 X03240
1.0 X05287
M76713
M86496
1.0 M55540
X61145
1.0 J01394
M86494
1.0 M55541
M86498
1.0 M35875
* M91245
X61010
M86499
1.0 X52392
M86501
1.0 J01415;M12548;V00710
1.0 M35876
M86497
M86495
1.0 M35877
1.0 J01420
*
M83756
Bryophyta
Fungi
Ascomycota
Animalia
Arthropoda
Chordata
3066 Nucleic Acids Research, 1993, Vol. 21, No. 13
Table 2. continued
Organism namel
Odocoileus virginianus (white-tailed deer)
Oryx gazeia
Phoca vituina (harbor seal)
Rana catesbeiana (frog)
Rattus norvegicus (rat)
Tragelaphus imberbis
Tragulus napu
Xenopus laevis (toad)
Echinodermata (sea urchins)
Paracentrotus lividus
Strongylocentrotus purpuratus
Nematoda
Ascaris suum
Caenorhabditis elegans
EUCARYA3 (EUCARYOTES, NUCLEOCYTOPLASMIC)
Giardia ardeae
Giardia intestinalis
Giardia muris
protocdSta5
Acrasiomycota (cellular slime molds)
Dictyosteliwn discoideum
Ciliophora (ciliates)
Tetrahymena pyrifonnis
Tetrahymena thermophila
Dinoflagellata (dinoflagellates)
Prorocentrum micans
Euglenophyta (euglenoid flagellates)
Eugena gracilis
Myxomycota (plasmodial slime molds)
Didyiwum iridis
Physarun polycephalum
Rhizopoda (amastigote amoebas)
Entamoeba histolytica
Zoomastigina (zooflagellates)
Crithidia fasciculata
Trypanosoma brucei
FunW
Ascomycota
Candida albicans
Pnewnocystis carinii8
Saccharomyces carlsbergensis
Saccharomyces cerevisiae
Schizosaccharomyces pombe
Zygomycota
Mucor racemosus
Plantae
Angiospermophyta (flowering plants)
Arabidopsis thaliana
Brassica napus (rapeseed)
Citus limon O(emon)
Fragaria ananassa (strawberry)
Lycopersicon escuentum (tomato)
Oryza sativa (rice)
Sinapis alba (mustard)
Animalia
Arthropoda
Status2
1.0
*
1.0
1.0
1.0
1.0
1.0
1.0
2.0
2.0
Accession Number
M35874
M86500
S37044;X63726
X12841
J01438
M86493
M55539
M10217
J04815
X12631
X54253
X54252
2.0 X58290
2.0 X52949
2.0 * X65063
X00601
M10752;X54004
1.0 X54512
X15973;X16108
1.0 X53361
X60210
1.0 V01159
* X65163
1.0 Y00055
X14553
* L07796;X70659
* S41246;M86760
J01352;V01285;V01325
2.0 J01355;K01048
* J01359;V01361;Z19136
M26190
X52320
* D10840;S39880
X05910
X15589;X58118
X07889;X13557
1.0 M11585
X15915;X57137
Drosophila melanogaster 1.0 M21017
Chordata
Herdmania momus X53538
Homo sapiens (human) 1.0 J01866;M11167
Mus musclus (mouse) 1.0 J01871;X00525
Rattus norvegicus (rat) 1.0 J01881;KO1591;X00521;X01069
Xenopus borealis (toad) X59733
Xenopus laeVis (toad) 1.0 K01376;X00136;X59734
Nematoda
Caenorhabditis elegans 1.0 X03680
lEucaryotic organisms are classified according to the scheme of Margulis,L. and Schwartz,K.V. (1988) [Five Kingdoms. An Illustrated Guide to the Phyla ofLife
on Earth (2nd edition). W.H. Freeman and Co., New York].
2New lisings that did not appear in the previous edition [Gutell,R.R., Schnare,M.N. and Gray,M.W. (1992) Nucleic Acids Res. 20, Supplement, 2095-2109]
Nucleic Acids Research, 1993, Vol. 21, No. 13 3067
are denoted by *, whereas previous listings containing revised or additional accession number(s) are indicated by #. The most recently updated secondary structure
now available in hardcopy form is listed as 1.0 (Release 1.0; July, 1991) or 2.0 (Release 2.0; January. 1993). Underlining of organism names in the above table
indicates that an associated [NOTE] concerning the sequence appears with that name in the List of References.
3See 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.
Natl. Acad. Sci. U.S.A. 87, 4576-4579.
4The classification used here follows the taxonomically ordered listing for SSU rRNA sequences on the RDP anonymous server. 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; and Woese,C.R. (1991) The use
of ribosomal RNA in reconstructing evolutionary relationships among bacteria. In Evoution at the Molecular Level (Selander,R.K., Clark,A.G. and Whittman,T.S.,
eds.), pp. 1-24. Sinauer, Sunderland, MA.
5The term 'Protoctista', as defined and used by Margulis and Schwartz (1988), includes but is not limited to the 'Protista' (unicellular eucaryotes, or protists).
6See [NOTE] in List of References, below.
7See Cavalier-Smith,T. (1987) Eukaryotes with no mitochondria. Nature 326, 332-333.
8Placement of Pneumocystis carinii within the Ascomycota is probable but not yet proven; see Bruns,T.D., Vilgalys,R., Barns,S.M., Gonzalez,D., Hibbett,D.S.,
Lane,D.J., Simon,L., Stickel,S., Szaro,T.M., Weisburg,W.G. and Sogin, M.L. (1992) Evolutionary relationships within the fungi: analyses of nuclear small subunit
rRNA sequences. Mol. Phylogent. Evol. 1, 231-241.
List of references to LSU rRNA Sequences (new or revised from 1992 edition)
ARCHAEA (ARCHAEBACTERIA)
Halobactenum maismorhu'
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 Halobacteriwn marismortui.
[NOTE: We used the published sequence, which differs from the database entry (X13738) at Ecoli positions 2506 (U vs. A) and 2523 (G vs. deletion).]
Sulfolobus solfataicus
Woese,C.R. (1991) Unpublished.
Thermococcus celer
Woese,C.R. and Achenbach,L. (1991) Unpublished.
The sequence of Thermococcus celer 23S rRNA.
BACTERIA (EUBACTERIA)
Aeromonas hydrophila
East,A.K. and Collins,M.D. (1993) FEMS Microbiol. Lett. 106, 129-134.
Molecular characterization of DNA encoding 23S rRNA and 16S-23S rRNA intergenic spacer regions of Aeromonas hydrophila.
BaciUus alcalophilus
Sutherland,K.J., Kudo,T. and Horikoshi,K. (1992) Unpublished.
B. alcalophilus 23S ribosomal RNA, partial sequence.
Bacillus anthracis
Ash,C. and Collins,M.D. (1992) FEMS Microbiol. Lett. 94, 75-80.
Comparative analysis of 23S ribosomal RNA gene sequences of Bacillus anthracis and emetic Bacillus cereus determined by PCR-direct sequencing.
Bacillus cereus (see BaciUus anthracis)
Bacillus globisporus
Ludwig,W., Kirchhof,G., Klugbauer,N., Weizenegger,M., Betzl,D., Ehrmann,M., Hertel,C., Jilg,S., Tatzel,R., Zitzelsberger,H., Liebl,S., Hochberger,M., Shah,J.,
Lane,D., Walln6fer,P.R. and Schleifer,K.H. (1992) System. Appl. Microbiol. 15, 487-501
Complete 23S ribosomal RNA sequences of gram-positive bacteria with a low DNA G+C content.
Bacillus licheniformis (see Bacillus globisporus)
Bacilus stearothermophilus (see also Bacillus anthracis)
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 stearothermophilus.
[NOTE: We used the primary sequence presented in Kop et al. (1984). The secondary structure in this paper has an extra G between E.coli positions 11 and 12.
This G is not present in the sequence newly determined by Ash and Collins (1992) (see Bacilus anthracis) which, however, differs at two other positions from
that of Kop et al. (1984).]
Bacilus subdlis (rmB)
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 ribosonal RNA operon, rmB.
BaciUus subtilis (rrnI)
Sutherland,K.J., Kudo,T. and Horikoshi,K. (1992) Unpublished.
BordeteUla avium
Mueller,M. (1993) Unpublished.
B. avum gene for 23S rRNA.
3068 Nucleic Acids Research, 1993, Vol. 21, No. 13
Bordetea bvrnchisepeica
Mueller,M. (1993) Unpublished.
B. bronchiseptica gene for 23S rRNA.
Bonetella panwpeSussis
Mueller,M. (1992) Unpublished.
B. parapernussis gene for 23S ribosomal RNA.
Bonhlia pertussis
Mueller,M. (1992) Unpublished.
B. perussis gene for 23S ribosonal RNA.
Bof,dia bugdorfen
Schwartz,I., Gazumyan,A. and Schwartz,J.J. (1992) Unpublished.
Sequence and structure of the ribosomal RNA genes of Borrelia burgdorferi.
Clostriium botuiEnum
East,A.K., Thompson,D.E. and Collins, M.D. (1992) J. Bacteriol. 174, 8158-8162.
Analysis of operons encoding 23S rRNA of Clostriin botulinwn type A.
Closiium iyrobut)ycum
van der Meer,J.R., Ludwig,W. and de Vos,W.M. (1992) Unpublished.
Characterization of a ribosomal RNA gene cluster from Clostridium tyrobutyricum: phylogenetic positioning based on the 16S and 23S nucleotide sequences.
Fnmkia sp.
Normand,P., Cournoyer,B., Simonet,P. and Nazaret,S. (1992) Gene 111, 119-124.
Analysis of a ribosomal RNA operon in the actinomycete Frankia.
Johnson,D.A. (1992) Thesis, Biology, University of Ottawa.
Analysis of an rRNA operon from Frankia strain AcNl4a.
[NOTE: The two Frankia sequences have many differences and so are listed as separate sequences (#1 and #2) in Table 1.]
Lactobadilus delbrueckl subsp. bulgancus (see Bacislls globisporus)
Lactococcus kacis subsp. cremoris (see Bacillus globisponas)
Lactococcus lacis subsp. lactis (strain 1L1403)
Chiaruttini,C. and Milet,M. (1993) J. Mol. Biol. 230, 57-76.
Gene organization, primary structure and RNA processing analysis of a ribosomal RNA operon in Lactococcus lactis.
Lactococcus lacts subsp. lactis (strain DSM 20481T) (see Bac4us gWoNiipous)
[NOTE: Although the three Lactococcus sequences are very similar, strain DSM 20481T has a different hairpin sequence at E.coli positions -1170-1180.]
Listeria monocytogenes (see also Bacillus globisponus)
Thompson,D.E., Balsdon,J.T., Cai,J. and Collins,M.D. (1992) FEMS Microbiol. Lett. 96, 219-224.
Studies on the ribosomal RNA operons of Listeria monocytogenes.
Micrococcus luteus
Regensburger,A., Ludwig,W., Frank,R., Bl6cker,H. and Schleifer,K.H. (1988) Nucleic Acids Res. 16, 2344.
Complete nucleotide sequence of a 23S ribosomal RNA gene from Micrococcus luteus.
[NOTE: We used the published sequence, which differs from the database entry (X06484) at the following E.coli positions (published sequence first, database entry
second): 112, A vs. U; between 174 and 175, G vs. U.]
Mycobactenwum kasii
Fleurbaaij,G.A., McNally,M. and Marich,J.E. (1992) Unpublished.
The complete nucleotide sequence of Mycobacterium knsasii 23S ribosomal RNA.
Mycoplasma hyopneumoniae (see Bacillus globisporus)
Mycoplasma pneumoniae (see Bacius globisporus)
Neissena gonon*oeae
Wolff,K., Sperka,S. and Stern,A. (1992) Nucleic Acids Res. 20, 4657.
Phylogeny and nucleotide sequence of a 23S rRNA gene from Neisseria gonorrhoeae and Neiserria meningitidis.
Neisseria meningitdis (see Neisseria gonorioee)
Pecnatus fisigensis (see Bacillus globisporus)
Peptocccus niger (see BaciElus globisporus)
Plesiomonas shigelloides
East, A.K., Allaway,D. and Collins, M.D. (1992) FEMS Microbiol. Lett. 95, 57-62.
Analysis of DNA encoding 23S rRNA and 16S-23S rRNA intergenic spacer regions from Plesiomonas shigelloides.
Nucleic Acids Research, 1993, Vol. 21, No. 13 3069
Pseudomonas cepacia
Hopfl,P., Ludwig,W., Schleifer,K.H. and Larsen,N. (1989) Eur. J. Biochemn. 185, 355-364.
The 23S ribosomal RNA higher-order structure of Pseudomonas cepacia and other prokaryotes.
[NOTE: The position ofthe 3'-terminus is unclear in Hopfl et al. (1989) (there is a discrepancy between the number given in text and the secondary strucure figure).
We have assigned the 3'-terminus by comparison with E.coli 23S rRNA.]
Pseudomonas perfectomanila (= P. stutzen)
Kerkhof,L.J. (1992) Unpublished.
A species-specific probe for the marine bacterium, Pseudomonas perfectomarina (P. stutzeri strain Zobell)
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.
[NOTE: Minor sequence heterogeneity has been noted in the three operons that have been sequenced.]
Staphylococcus aureus (see Bacillus globisporus)
Staphylococcus carnosus (see Bacillus globisporus)
Streptococcus orais (see Bacillus globisporus)
Streptococcus thermophilus (see Bacilus globisporus)
Synechococcus sp. 6301 (formerly Anacystis nidlans)
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.
[NOTE: The Douglas and Doolittle (1984) sequence differs from that of Kumano et al. (1983) at a number of positions. We used the former sequence, which is
better supported by secondary structure comparisons.]
Thermotoga maritia
Achenbach,L. and Woese,C.R. (1991) Unpublished.
Sequence of the ribosomal operon of Thermotoga maritima.
PLASTIDS
Alnus incana
Levesque,M. and Johnson,D.A. (1992). Plant Mol. Biol. 18, 601-602.
Nucleotide sequence of the chloroplast 23S rRNA gene from alder (Alnus incana).
Imbeault,J.-C. and Johnson,D.A. (1991) Unpublished.
Analysis of the 4.5S-5S rRNA intergenic region in rDNA from alder (Alnus incana) chloroplast.
Chiamydomonas sp. 66.72 (see Chkunydomonas fimnkii)
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 Chlamydononas eugametos.
Chlamydomonas fnmnkii
Turmel,M., Gutell,R.R., Mercier,J.-P., Otis,C. and Lemieux,C. (1993) J. Mol. Biol., in press.
Analysis ofthe chloroplast large subunit ribosomal RNA gene from 17 Chlamydomonas taxa. Three internal transcribed spacers and 12 group I intron insertion sites.
Chlamydomonas geitlen (see Chlamydomonas fJankia)
Chlamydomonas gekainosa (see Chlamydomonas frankii)
Chlamydomonas hunicola (see Chlamydomonas ftenkiu)
Chlamydomonas indica (see Chlamydomonas ftankii)
Chiamydomonas iyengani (see Chlamydomonas franki)
Chlamydomonas komma (see Chlamydomonas frankis)
Chiamydomonas mexicana (see Chlamydomonas fnnkii)
Chlamydomonas moewusui (see Chiamydomonas frakia)
Chlamydomonas pallidostigmatica (see Chlamydomonas franAd)
3070 Nucleic Acids Research, 1993, Vol. 21, No. 13
Chlamydomonas peterfii (see Chlamydomonas frankli)
Chlamydomonas pitschmannii (see Chlamydomonas franka)
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.
[NOTE: The 5'-end of the 7S rRNA and the 3'-end of the 23S rRNA have been changed to agree with those of the corresponding species in C. eugametos chloroplast;
see Chlamydomonas eugametos.)]
Chlamydomonas starru (see Chlamydomonas frankii)
Chlamydomonas zebra (see Chlamydomonas frankii)
Chlorella eUipsoidea
Yamada,T. 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.
[NOTE: The putative intron described by Yamada and Shimaji (1987) is probably an internal transcribed spacer that is excised during post-transcriptional processing;
see Turmel et al. (1991), Chlamydomonas eugametos).
Epifagus virginiana (beechdrops)
Wolfe,K.H., Katz-Downie,D.S., Morden,C.W. and Palmer,J.D. (1992) Plant Mol. Biol. 18, 1037-1048.
Evolution of the plastid ribosomal RNA operon in a nongreen parasitic plant: Accelerated sequence evolution, altered promoter structure, and tRNA pseudogenes.
Eugena graciis
Yepiz-Plascencia,G.M., Jenkins,M.E. and Hallick,R.B. (1988) Nucleic Acids Res. 16, 9340.
Nucleotide sequence of the Euglena gracilis chloroplast 23S rRNA gene of the rrnC operon.
Schnare,M.N., Yepiz-Plascencia,G.M., Copertino,D.W., Hallick,R.B. and Gray,M.W. (1992) Nucleic Acids Res. 20, 1421.
5'- and 3'-terminal sequences of the chloroplast 16S and 23S ribosomal RNAs of Euglena gracilis.
[NOTE: The sequence in Schnare et al. (1992) (X12890) revises the original one (X13310) presented in Yepiz-Plascencia et al. (1988).]
Nicotiana tabacum
Takaiwa,F. and Sugiura,M. (1982) Eur. J. Biochem. 124, 13-19.
The complete nucleotide sequence of a 23-S rRNA gene from tobacco chloroplasts.
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,B.Y., Sugita,M., Deno,H., Kamogashira,T., Yamada,K., Kusuda,J., Takaiwa,F., Kato,A., Tohdoh,N., Shimada,H. and Sugiura,M. (1986)
Plant Mol. Biol. Reporter 4, 111-147.
The complete nucleotide sequence of the tobacco chloroplast genome.
[See also: EMBO J. 5, 2043-2049 (1986). The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression.]
[NOTE: The original sequence of Takaiwa and Sugiura (1982) differs from that presented later in Shinozaki et al. (1986). We used the more recent sequence because
it agrees with other plant chloroplast sequences and is supported by the secondary structure.]
Palmari palnata
Singh,R.K. (1993) Unpublished.
The organization and primary structure of the plastid rRNA operon from the red alga Palmaria palmata.
Plasmodium fakiparum
Gardner,M.J., Feagin,J.E., Moore,D.J., Rangachari,K., Williamson,D.H. and Wilson,R.J.M. (1993) Nucleic Acids Res. 21, 1067-1071.
Sequence and organization of large subunit rRNA genes from the extrachromosomal 35 kb circular DNA of the malaria parasite Plasmodium falciparum.
[NOTE: Phylogenetic analysis by Gardner et al. (1993) suggests that the P.falciparun 35-kbp DNA may be a plastid DNA remnant; see also Gardner,M.J., Feagin,J.E.,
Moore,D.J., Spencer,D.F., Gray,M.W., Williamson,D.H. and Wilson,R.J.M. (1991) Mol. Biochem. Parasitol. 48, 77-88.]
PylaeUla littoralis
Somerville,C.C., Jouannic,S., Martin,W.F., Kloareg,B. and Loiseaux-de Goer,S. (1993) Plant Mol. Biol. 21, 779-787.
Secondary structure and phylogeny of the chloroplast 23S rRNA gene from the brown alga Pylaiella littoralis.
Zea mays
Edwards,K. and K6ssel,H. (1981) Nucleic Acids Res. 9, 2853-2869.
The rRNA operon from Zea mays chloroplasts: nucleotide sequence of 23S rDNA and its homology with E.coli 23S rDNA.
[NOTE: The 23S rRNA is thought to be fragmented at two positions as a result of excision of short internal transcribed spacers; see Kossel,H., Natt,E., Strittmatter,G.,
Fritzche,E., Gozdzicka-Jozefiak,A. and Przybyl,D. (1985) Structure and expression of rRNA operons from plastids of higher plants. In Molecular Form and Function
ofthe Plant Genome (van Vloten-Doting,L., Groot,G.S.P. and Hall,T.C., eds.), NATO ASI Series (Series A: Life Sciences), Vol. 83, pp. 183-198, Plenum, New York.]
Nucleic Acids Research, 1993, Vol. 21, No. 13 3071
MITOCHONDRIA
Aepyceros melampus
Allard,M.W., Miyamoto,M.M., Jarecki,L., Kraus,F. and Tennant,M.R. (1992) Proc. Natl. Acad. Sci. U.S.A. 89, 3972-3976.
DNA systematics and evolution of the artiodactyl family Bovidae.
Apis mellifem
Vlasak,I., Burgschwaiger,S. and Kreil,G. (1987) Nucleic Acids Res. 15, 2388.
Nucleotide sequence of the large ribosomal RNA of honeybee mitochondria.
Crozier,R.H. and Crozier,Y.C. (1993) Genetics 133, 97-117.
The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization.
Artemia saUna
Palmero,I., Renart,J. and Sastre,L. (1988) Gene 68, 239-248.
Isolation of cDNA clones coding for mitochondrial 16S ribosomal RNA from the crustacean Artemia.
[NOTE: The partial cDNA sequence of Palmero et al. (1988) shows many differences from the database entry (complete sequence). We used the sequence from
the database.]
Ascaris suum
Okimoto,R., Macfarlane,J.L., Clary,D.O. and Wolsteholme,D.R. (1992) Genetics 130, 471-498.
The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum.
Caenorhabdis elegans (see Ascais suum)
Carassius auratus (goldfish)
Peng,G., Taylor,J.D. and Tchen,T.T. (1992) Biochem. Biophys. Res. Conmunn. 189, 445-449.
Increased mitochondrial activities in pigmented (melanized) fish cells and nucleotide sequence of mitochondrial large rRNA.
Crossostoma lacustre (freshwater loach)
Tzeng,C.-S., Hui,C.-F., Shen,S.-C. and Huang,P.C. (1992) Nucleic Acids Res. 20, 4853 -4858.
The complete nucleotide sequence of the Crossostoma lacustre mitochondrial genome: conservation and variations among vertebrates.
Locusta migratoria
Uhlenbusch,I., McCracken,A. and Gellissen,G. (1987) Curr. Genet. 11, 631-638.
The gene for the large (16S) ribosomal RNA from the Locusta migratoria mitochondrial genome.
[NOTE: The prinmay sequence figure in Uhlenbusch et al. (1987) has the sequence presented backwards and a few positions are not clear. These positions (corresonding
to E.coli 1933 and 2659) are clearly G in the secondary structure presented in the same paper; however, they are C in the database entry (X05287), which also
displays the sequence backwards.]
Marchantia poymorpha
Oda,K., Yamato,K., Ohta,E., Nakamura,Y., Takemura,M., Nozato,N., Akashi,K., Kanegae,T., Ogura,Y., Kohchi,T. and Ohyama,K. (1992) Plant Mol. Biol.
Reporter 10, 105-163.
Complete nucleotide sequence of the mitochondrial DNA from a liverwort, Marchantia polymorpha.
[# See also: J. Mol. Biol. 223, 1 -7 (1992). Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA: a
prnimtive form of plant mitochondrial genome.]
Mytilus edulis
Hoffmann,R.J., Boore,J.L. and Brown,W.M. (1992) Genetics 131, 397-412.
A novel mitochondrial genome organization for the blue mussel, Mytilus edulis.
Paramecium pnmaurelia
Seilhamer,J.J. and Cummings,D.J. (1981) Nucleic Acids Res. 9, 6391-6406.
Structure and sequence of the mitochondrial 20S rRNA and tRNA tyr gene of Paramecium primaurelia.
Seilhamer,J.J., Gutell,R.R. and Cummings,D.J. (1984) J. Biol. Chem. 259, 5173-5181.
Paramecium mitochondrial genes. II. Large subunit rRNA gene sequence and microevolution.
[NOTE: The sequence in Seilhamer and Cummings (1981) differs from that in Seilhamer et al. (1984). We used the latter (more recent) version.]
Penicifium chrysogenum
Naruse,A., Yamamoto,H. and Sekiguchi,J. (1993) Biochim. Biophys. Acta 1172, 353-356.
Nucleotide sequence of the large mitochondrial rRNA gene of Penicillium chrysogenum.
Phoca vitulina
Arnason,U. and Johnsson,E. (1992) J. Mol. Evol. 34, 493-505.
The complete mitochondrial DNA sequence of the harbor seal, Phoca vitulina.
Plasmodium falkqnum
Feagin,J.E., Werner,E., Gardner,M.J., Williamson,D.H. and Wilson,R.J.M. (1992) Nucleic Acids Res. 20, 879-887.
Homologies between the contiguous and fragmented rRNAs of two Plasmodium falciparum extrachromosomal DNAs are limited to core sequences.
3072 Nucleic Acids Research, 1993, Vol. 21, No. 13
Vaidya,A.B., Lashgari,M.S., Pologe,L.G. and Morrisey,J. (1993) Strctuanl features ofPlasodwn cytochrome b that may underlie susceptibility to 8-aminoqinolines
and hydroxynaphthoquinones. Mol. Biochem. Parasitol. 58, 33-42.
Plasmnodiw yoeEli
Vaidya,A.B., Akella,R. and Suplick,K. (1989) Mol. Biochem. Parasitol. 35, 97-108.
Sequences similar to genes for two nitochondrial proteins and portions of ribosomal RNA in tandemly arrayed 6-kilobase-pair DNA of a malarial parasite.
[NOTE: A corrigendum by the same authors (Mol. Biochem. Parasitol. 39, 295 -296 (1990)) contains corrections to their original sequence.]
Suplick,K., Morrisey,J. and Vaidya,A.B. (1990) Mol. Cell. Biol. 10, 6381-6388.
Complex tription from the extrachromosomal DNA encoding mitochondrial functions of Plasmodium yoelii.
Spodoptera fiugqeIa
Pashley,D.P. and Ke,L.D. (1992) Mol. Biol. Evol. 9, 1061-1075.
Sequence evolution in mitochondrial ribosomal and ND-1 genes in Lepidoptera: implications for phylogenetic analyses.
lWdcum aeslivum
Falconet,D., Sevignac,M. and Quetier,F. (1988) Curr. Genet. 13, 75-82.
Nucleotide sequence and determiation ofthe extremities ofthe 26S ribosomal RNA gene in wheat mitochondria: evidence for sequence rearrangements in the ribosomal
genes of higher plants.
Spencer,D.F., Schnare,M.N., Coulthart,M.B. and Gray,M.W. (1992) Plant Mol. Biol. 20, 347-352.
Sequence and organization of a 7.2 kb region of wheat mitochondrial DNA containing the large subunit (26S) rRNA gene.
EUCARYA (EUCARYOTES, NUCLEOCYTOPLASMIC)
Brassica napus
Okumura,S. and Shimada,H. (1992) Nucleic Acids Res. 20, 3510.
Nucleotide sequence of genes for a 5.8S and 25S rRNA from rape seed (Brassica napus).
adia albicans
Mercure,S., Rougeau,N., Montplaisir,S. and Lemay,G. (1993) Nucleic Acids Res. 21, 1490.
The nucleotide sequence of the 25S rRNA-encoding gene from Candida albicans.
Lott,T.J. (1992) Unpublished.
Nucleotide sequence of the 5.8S rDNA from Candida albicans.
Ddymum s
Johansen,S., Johansen,T. and Haugli,F. (1992) Curr. Genet. 22, 305-312.
Extrachromosomal ribosomal DNA of Didyniun iridis: sequence analysis of the large subunit ribosomal RNA gene and sub-telomeric region.
Drosophila melanogaster
Tautz,D., Hancock,J.M., Webb,D.A., Tautz,C. and Dover,G.A. (1988) Mol. Biol. Evol. 5, 366-376.
Complete sequences of the rRNA genes of Drosophila melanogaster.
Linares,A.R., Hancock,J.M. and Dover,G.A. (1991) J. Mol. Biol. 219, 381-390.
Secondary structure constraints on the evolution of Drosophila 28 S ribosomal RNA expansion segments
Rousset,F., P6landadis,M. and Solignac,M. (1991) Proc. Natl. Acad. Sci. U.S.A. 88, 10032-10036.
Evolution of compensatory substitutions through GU intermediate state in Drosophila rRNA.
[NOTE: Minor corrections are presented in Linares et al. (1991) and Rousset et al. (1991). The latter contains a sequence of25 nucleoddes absent in Tautz etal. (1988).]
Entwnoeba histolyfica
Ramachandran,S., Bhattacharya,A. and Bhattacharya,S. (1993) Nucleic Acids Res. 21, 2011.
Nucleotide sequence analysis of the rRNA transcription unit of a pathogenic Entamoeba histolytica strain HM-EIMSS.
Ghada wveae
van Keulen,H., Horvat,S., Erlandsen,S.L. and Jarroll,E.L. (1991) Nucleic Acids Res. 19, 6050.
Nucleotide sequence of the 5.8S and large subunit rRNA genes and the internal transcribed spacer and part of the external spacer from Giardia ardeae.
[NOTE: See van Keulen et al. (1992) (Giarna muris) for primary sequence. The G. ardeae sequence in this paper has several differences from the database entry
(X58290). We used the G. ardeae sequence presented in the G. muns paper, which fits the secondary structure better (the V3 structure shown in the G. ardeae
paper is missing a G).j
Giardia intesuinals (= G. d lis, G. mbia)
Healey,A., Mitchell,R., Upcroft,J.A., Boreham,P.F.L. and Upcroft,P. (1990) Nucleic Acids Res. 18, 4006.
Complete nucleotide sequence of the ribosomal RNA tandem repeat unit from Giardia intestinalis.
[NOTE: A minor correction (insertion of a C) is presented in the G. muris reference. The two ambiguous positions are G according to Edlind,T.D., Sharetzsky,C.
and Cha, M.E. (1990) Ribosomal RNA of the primitive eukaryote Giardia lamblia: large subunit domain I and potential processing signals. Gene 96, 289-293.]
Ciri mums
van Keulen,H., Gutell,R.R., Campbell,S.R., Erlandsen,S.L. and Jarrell,E.L. (1992) J. Mol. Evol. 35, 318-328.
The nucleotide sequence of the entire ribosomal DNA operon and the strucure of the large subunit rRNA of Giardia munris.
Nucleic Acids Research, 1993, Vol. 21, No. 13 3073
Homo sapins
Maden,B.E.H., Dent,C.L., Farrell,T.E., Garde,J., McCallum,F.S. and Wakeman,J.A. (1987) Biochem J. 246, 519-527.
Clones of human ribosomal DNA containing the complete 18 S-rRNA and 28 S-rRNA genes. Characterization, a detailed map of the human ribosomal transcription
unit and diversity among clones.
[NOTE: A correction was made in Maden et al. (1987) to eliminate an extra GC (following position 50) in the original 5.8S rRNA sequence of Khan,M.S.N and
Maden,B.E.H. (1977) Nucleic Acids Res. 4, 2495-2505. Nucleotide sequence relationships between vertebrate 5.8 S ribosomal RNAs.]
Gonzalez,I.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.
Variation among human 28S ribosomal RNA genes.
Pneumocystis carinni
Liu,Y., Rocourt,M., Pan,S., Liu,C. and Leibowitz,M.J.(1992) Nucleic Acids Res. 20, 3763-3772.
Sequence and variability of the 5.8S and 26S rRNA genes of Pneumocystis carinii.
Raltus norvegicus
Subrahmanyam,C.S., Cassidy,B., Busch,H. and Rothblum,L.I. (1982) Nucleic Acids Res. 10, 3667-3680.
Nucleotide sequence of the region between the 18S rRNA sequence and the 28S rRNA sequence of rat ribosomal DNA.
Chan,Y.-L., Olvera,J. and Wool,I.G. (1983) Nucleic Acids Res. 11, 7819-7831.
The structure of rat 28S ribosomal ribonucleic acid inferred from the sequence of nucleotides in a gene.
Hadjiolov,A.A., Georgiev,O.I., Nosikov,V.V. and Yavachev,L.P. (1984) Nucleic Acids Res. 12, 3677-3693.
Primary and secondary structure of rat 28 S ribosomal RNA.
Wool,I.G. (1986) In Hardesty,B. and Kramer,G. (eds.). Structure, Function, and Genetics of Ribosomes. Springer-Verlag, New York, pp. 391-411.
Studies on the structure of eukaryotic (mammalian) ribosomes.
[NOTE: We used the most recent (revised) sequence given in Wool (1986).]
Saccharomyces carlsbergensis
Veldman,G.M., Brand, R.C., Klootwijk,J. and Planta,R.J. (1980) Nucleic Acids Res. 8, 2907-2920.
Some characteristics of processing sites in ribosomal precursor RNA of yeast.
Veldman,G.M., Klootwijk,J., van Heerikhuizen,H. and Planta,R.J. (1981) Nucleic Acids Res. 9, 4847-4862.
The nucleotide sequence of the intergenic region between the 5.8S and 26S rRNA genes of the yeast ribosomal RNA operon. Possible implications for the interaction
between 5.8S and 26S rRNA and the processing of the primary transcript.
Veldman,G.M., Klootwijk,J., de Regt,V.C.H.F., Planta,R.J., Branlant,C., Krol,A. and Ebel,J.-P. (1981) Nucleic Acids Res. 9, 6935-6952.
The primary and secondary structure of yeast 26S rRNA.
Saccharomyces cerevisiae
Rubin,G.M. (1973) J. Biol. Chem. 248, 3860-3875.
The nucleotide sequence of Saccharomyces cerevisiae 5.8 S ribosomal ribonucleic acid.
Georgiev,O.I., Nikolaev,N., Hadjiolov,A.A., Skryabin,K.G., Zakharyev,V.M. and Bayev,A.A. (1981) Nucleic Acids Res. 9, 6953-6958.
The structure of the yeast ribosomal RNA genes. 4. Complete sequence of the 25 S rRNA gene from Saccharomyces cerevisiae.
[NOTE: The S. carlsbergensis and S.cerevisiae sequences are very similar; most of the differences likely reflect errors in the latter sequence. However, we used
the S.cerevisiae sequence because the S. carlsbergensis 5.8S rRNA sequence is not complete.]
Schizosaccharomyces pombe
Schaak,J., Mao,J.I. and S611,D.G. (1982) Nucleic Acids Res. 10, 2851-2864.
The 5.8S RNA gene sequence and the ribosomal repeat of Schizosaccharomyces pombe.
Lapeyre,B.B. and Feliu, J.J. (1992) Unpublished.
Nucleotide sequence of the 25S ribosomal RNA from Schizosaccharomyces pombe.
Sinapis alba
Capesius,I. (1991) Plant Mol. Biol. 16, 1093-1094.
Nucleotide sequence of a 25S rRNA gene from mustard (Sinapis alba).
Rathgeber,J. and Capesius,I. (1989) Nucleic Acids Res. 17, 7522.
Nucleotide sequence of the 18S-25S spacer region from mustard DNA.
Tetrahymena thernophila
Engberg,J., Nielsen,H., Lenaers,G., Murayama,O., Fujitani,H. and Higasagawa,T. (1990) J. Mol. Evol. 30, 514-521.
Comprison ofprimary and secondary 26S rRNA structures in two Tetrhymena species: Evidence for a strong evolutionary and stuctural constraint in expansion segments.
Engberg,J. and Nielsen,H. (1990) Nucleic Acids Res. 18, 6915-6919.
Complete sequence of the extrachromosomal rDNA molecule from the ciliate Tetrahymena thermophila strain B1868VII.
[NOTE: The sequence shown in Engberg and Nielsen (1990) is missing positions 6601-6700 (corresponding to E.coli positions 1599-1698.]
3074 Nucleic Acids Research, 1993, Vol. 21, No. 13
Xenopus lWis
Hall,L.M.C. and Maden,B.E.H. (1980) Nucleic Acids Res. 8, 5993-6005.
Nucleotide sequence through the 18S-28S intergene region of a vertebrate ribosomal transcription unit.
Ware,V.C., Tague,B.W., Clark,C.G., Gourse,R.L., Brand,R.C.and Gerbi,S.A. (1983) Nucleic Acids Res. 11, 7795-7817.
Sequence analysis of 28S ribosomal DNA from the amphibian Xenopus laevis.
Stebbins-Boaz,B. and Gerbi,S.A. (1991) J. Mol. Biol. 217, 93-112.
Structunal analysis of the peptidyl transferase region in ribosomal RNA
Ajuh,P.M., Heeney,P.A. and Maden,B.E.H. (1991) Proc. R. Soc. Lond., B, Biol Sci. 245, 65-71.
Xenopus boreals and Xenopus kwvis 28S ribosomal DNA and the complete 40S ribosomal precursor RNA coding units of both species.
Schnare,M.N. and Gray,M.W. (1992) Nucleic Acids Res. 20, 608.
A new 3'-terminus for Xenopus laevis 28S ribosomal RNA.
[NOTE: Corrections to the sequence of Domain V in Ware et al. (1983) may be found in Stebbins-Boaz and Gerbi (1991). The most recent revisions (Ajuh et
al. (1991); Schnare and Gray (1992)) are being incorporated into the current secondaxy structure model.]

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Gutell 029.nar.1993.21.03055

  • 1. Nucleic Acids Research, 1993, Vol. 21, No. 13 3055-3074 A compilation of large subunit (23S and 23S-like) ribosomal RNA structures: 1993 Robin R.Gutell*, Michael W.Grayl* and Murray N.Schnare1 Molecular, Cellular, and Developmental Biology, Campus Box 347, University of Colorado, Boulder, CO 80309-0347, USA and 'Department of Biochemistry, Dalhousie University, Halifax, Nova Scotia B3H 4H7, Canada INTRODUCTION This compilation is part of an on-going effort to maintain a comprehensive and continually updated collection oflarge subunit (LSU; 23S and 23S-like) rRNA secondary structures and associated sequence and citation information. Table 1 gives a breakdown of the number and phylogenetic distribution of sequences currently in this LSU rRNA database. A listing of accession numbers for all complete LSU rRNA sequences now in the public domain is presented in Table 2. The reference list is an update ofthe information provided in the 1992 compilation [1]; here, we include only revised or new citations to LSU rRNA sequences. The complete bibliography of LSU rRNA sequences is available electronically, as is the complete listing ofaccession numbers presented in Table 1 (see below for instructions on how to obtain this information). GROWTH OF THE DATABASE The past year has seen the largest annual increase in the number of LSU rRNA sequences published and/or released through the EMBL, GenBank and DDBJ databanks (Table 1). This trend has also been apparent in each of the previous years we have monitored, emphasizing the steady increase in the rate at which LSU rRNA sequences are being determined. The rate ofgrowth within each of the phylogenetic categories does vary, however. In the period covered by the present compilation, more than half (34/66) of the new sequences that appeared were (eu)bacterial ones. The second largest increase occurred in the Plastids category, due primarily to the release of 15 new Chlamydomonas chloroplast sequences. In the previous year, the greatest increases were in mitochondrial and eucaryotic (nuclear) sequences. Mitochondrial sequences still constitute the largest single category in the LSU rRNA database, as they have in every previous compilation. MODELS OF HIGHER-ORDER STRUCTURE As in previous compilations [1-3], each LSU rRNA primary sequence is presented in a two-dimensional format (the secondary structure) that underpins the biologically relevant conformation of an rRNA molecule. When LSU rRNA sequences are configured in this manner, phylogenetic information becomes readily apparent, as do patterns of variability and conservation in sequence and structure. At the same time, the secondary structure serves as an effective template for relating form to function. Principles for deducing higher-order structure have been enunciated in previous compilations [1-3] (see also [4-6]). Three phylogenetically and structurally distinct examples of current LSU rRNA secondary structures are presented in this communication. They are: (i) Escherichia coli, a typical (eu)bacterial structure (our reference standard, to which other LSU rRNA structures are compared and against which they are modelled); (ii) Saccharomyces cerevisiae (yeast), a representative eucaryotic (nucleocytoplasmic) structure; and (iii) a 'minimalist' structure, typified by the unusually small mitochondrial LSU rRNA from the nematode worm, Caenorhabditis elegans. While the latter two structures exemplify the tpe ofsize variation found among LSU rRNAs, an even smaller and quite peculiar structure has been described for the mitochondrial LSU rRNA of trypanosomatid protozoa (Trypanosoma, Leishumaia, Crithidia). At the other extreme, LSU rRNA structures larger than the S.cerevisiae nuclear one can be found; these are primarily mammalian nucleocytoplasmic ones, which contain large insertions at the positions of some ofthe variable regions oftheir S.cerevisiae counterpart. Due to the extensive sequence and size differences within some ofthe mitochondrial and eucaryotic variable regions, and the lack of a sufficient number of phylogenetically close examples from which to deduce significant primary and secondary structure homology within these variable regions, some ofthem had been left unstructured in previous compilations. However, with the recent large increase in the number of available LSU rRNA sequences, we have now deduced sequence and structural homology for many of these variable regions. Because we have a high degree of confidence in these newly solved structures, structural variation and evolution in these mitochondrial and nucleocytoplasmic LSU rRNAs can now be examined critically and in depth. The results of these analyses will be published in due course, along with other LSU rRNA structural characteristics that distinguish the different phylogenetic assemblages. At the same time that they permit the elucidation ofsecondary structure pairings, comparative methods allow one to infer teriary interactions. The three LSU rRNAs presented in this compendium display all ofthe currendy known secondary and tertary structure constraints. A small but growing number ofthese newer and more * To whom correspondence should be addressed .=/ 1993 Oxford University Press
  • 2. 3056 Nucleic Acids Research, 1993, Vol. 21, No. 13 complex structural elements have been experimentally verified [4,5], thereby justifying the application of these comparative methods. New and more powerful correlation analysis algoritms are now being developed [6,7; R.R. Gutell, unpublished] and promise to extend our appreciation of the structural (and other) constraints acting on these LSU rRNAs. In the immediate future we anticipate a continuing steady increase in the number of available LSU rRNA sequences (and thus their structures), in parallel with additional refinements in each of these structures. The information provided should lead us to higher-resolution structures and new insights into how they evolved. ACCURACY OF THE DATA As noted previously [1], independently determined versions of the same primary sequence exist for several LSU rRNAs (see Table 2 and the List of References). 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 a 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 witiin variable regions [8]. We have also noted that a few published primary sequences differ at one or more positions from their GenBank/EMBL/DDBJ listings, without an indication that the database entry represents a subsequently revised version ofthe original published sequence. Again, secondary structure modelling may or may not indicate which version is likely to be correct. This year, the List of References contains brief [NOTES] on individual sequences, where discrepancies between different versions of the same sequence or between published and database entries ofthe same sequence are noted. In cases ofnon-identical versions ofthe same sequence, the reader is referred to these notes for information on which sequence was used for the secondary structures we present. AVAILABILITY AND STATUS OF STRUCTURE FIGURES As in [1] and [2], the actual 23S and 23S-like rRNA secondary structures are not published here, except for the three examples shown. The comprehensive set of LSU rRNA secondary structures may be obtained in one of two ways. Hardcopy printouts ofthis set are available directly from us (inquiries should be referred to M.W.G. at the address listed below). Release 1.0, which comprised 88 structures, was made available for distribution in July, 1991, and copies may still be obtained. Newly modeled and refined LSU rRNA secondary structures are included in Release 2.0 (January, 1993), which contains 51 structures (13 archaebacterial, 18 eubacterial, 13 plastid, 3 mitochondrial and 4 eucaryotic nuclear). Those structures available in Release 1.0 and 2.0 are noted in Table 2. The next release (2.1) will comprise considerably revised and updated eucaryotic nuclear structures, whereas subsequent releases will contain revised mitochondial structures (Release 2.2) and models ofnew prokaryotic (archaebacterial and eubacterial) and plastid sequences (Release 2.3). Requests for hardcopy printouts, which will be sent out as soon as they become available, should state explicitly which Release (1.0,2.1-2.3) is being sought. Anyone who is on our current mailin ist should already have received Release 2.0 and will automatically receive future releases. Alternatively, individuals with access to the Internet telecommunications network and a laser printer capable of processing PostScript.m 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 [9] 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. Currently it includes the set of LSU rRNA secondary structures (in PostScriptrm format) that are available in hard copy in Release 2.0, 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). Finally, we invite comments from readers, and welcome suggested revisions to and/or alternative interpretations of our proposed secondary structures, as well as suggestions for improvement in the content and/or form ofthe database. We also solicit newly determined LSU rRNA sequences in advance of publication, in order to accelerate their inclusion in the compendium. ACKNOWLEDGEMENTS We gratefully acknowledge the computer propmming expertise ofBryn Weiser and Tom Macke in this endeavor. Work on this compendium has been supported by an operating grant (MT-11212) from the Medical Research Council of Canada to M.W.G. and by NIH grant GM48207 to R.R.G., who also acknowledges a generous donation ofcomputer equipment from SUN Microsystems. We thank the W.M. Keck Foundation for their generous support ofRNA science on the Boulder campus, and the Canadian Institute for Advanced Research (CIAR) for providing funds in support ofthe 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. REFERENCES 1. Gutell,R.R., Schnare,M.N. and Gray,M.W. (1992) NucleicAcids Res. 20, Supplement, 2095-2109. 2. Gutell,R.R., Schnare,M.N. and Gray,M.W. (1990) NucleicAcids Res. 18, Supplement, 2319-2330. 3. Gutell,R.R. and Fox,G.E. (1988) Nucleic Acids Res. 16, Supplemet, r175-r269. 4. Gutell,R.R. In Nierhaus,K.H., Subramann,A.R., Erdmann,V.A., Franceschi,F., and Wittman-Liebold,B. (eds.). The TrnslationalApparatus. Plenum, in press. 5. Gutell,R.R., Larsen,N. and Woese,C.R. I Zimmermann,R.A. and Dahlberg,A.E. (eds.). RibosomalRNA: Strucure, Ewuluion, Gene Epression and Function in Protein Synthesis. CRC Press, Boca Raton, FL, in press. 6. Gutell,R.R., Power,A., Hertz,G.Z., Putz,E.J. and Stormo,G.D. (1992) Nucleic Acids Res. 20, 5785-57-95. 7. Gutell,R.R. (1993) Curr. Opin. Struct. BioL 3, in press.
  • 3. Nucleic Acids Research, 1993, Vol. 21, No. 13 3057 8. Gonzalez,I.L., Gorski,J.L., Campen,T.J., Domey,D.J., Erickson,J.M., Sylvester,J.E. and Schmickel,R.D. (1985) Proc. Natl. Acad. Sci. U.S.A. 82, 7666-7670. 9. Olsen,G.J., Overbeek,R., Larsen,N., Marsh,T.L., McCaughey,M.J., Maciukenas,M.A., Kuan,W.-M., Macke,T.J., Xing,Y. and Woese,C.R. (1992) Nucleic Acids Res. 20, Supplement, 2199-2200. REQUESTS For hard copies of LSU rRNA secondary structures, either the complete compilation or selected portions thereof (please specify Release 1.0. 2.0. 2.1. 2.2 or 2.3): 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: mgray@ac.dal.ca (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 80309-0347, USA. FAX: (303)492-7744 e-mail: rgutell@boulder.colorado.edu To obtain PostScriptrm files of LSU rRNA secondary structures via anonymous ftp on the Internet tele- communications network: ftp site: info.mcs.anl.gov directory: /pub/RDP/LSU_rRNA/sec-struct 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.
  • 4. 3058 Nucleic Acids Research, 1993, Vol. 21, No. 13 -ACAUS U AA AA BeU U-A A GAUUCfBGwUBUA% ACUCBAU A-U iu00 *,60C-ia c-o CA. C- AcAg.uc 0A ccc-o B a A -A 0 G-C BN-Ca-Ca *U U * B- u-C A O a O-C A AA A A U- ~~~U U A BA c Auu A Fgure 1. Higher-order structure model for a typical (eu)bacterial LSU rRNA (Escherichia coli 23S; accession no. J01695). A, 5'-half; B, 3'-half. C:G and U:A base pairs are connected by lines, G:U pairs by dots, A:G pairs by open circles, and other, non-canonical pairings by closed circles. Proposed terdary interactions connected with thicker, continuous lines are characterized by a sufficient number of compensatory base changes to make their identification firm; more tentative asssignments are connected by thinner, dashed lines. Every 10th position in the sequence is indicated by a tick mark, while every 50th position is numbered.
  • 5. GCAAC-B B-C G AA UGIB B-C B-C u. u Au OBA - U@ C A-U A A A aB B- C-216 B A- A A -B.U C-B U A- U B A-U U-BB3-C C-B 1so-B-C U-A AaB AB-C AAU A A AB..C B A C B-C U B law-c- GUc -a 1900 ~UU-A B . UA G-IAACUA B-C-C-As UAA BBlAU AB-CUCBB-~UAAUA Al B B C C U.B BBC B~~AAU-!BBUBBACC-B - C CCC- B-jI__II-?-L C C-B A-U CBCaB .U CCACC'flU U-A B-CB.:u - BB-UBa ~ AB-UB U C UA U UAAABA a Al C 'AB B.UIB AA~~~~AAACAC CBCABU U-A -U A U or1 ii B U-A Go-cG_u G~~~~~CBB0 A'cB.CUAUUUBU UUUCAC-A-U * C uc UA - au. a ~A A-UAA-A BUa- U A ~~~~~AG- I A-UU C-Bc 2100-B-U A-U %ABCCB#.%,mU-B- -C ~~~~C-B'l A-U 1 -B- C76 B-C A C-B B' CB /BMAA - UA A-U 2200AGA B.UC-BAUACCABG:t---- A-UAAIBUUBCC BBBe ABBOCAC B U l-hl_CACUCCUA UICAUB A A cAUBCIBBAUCAA C~~~~~~~~~~~~~~~~~~~~~~~-B-UAA IO-C ~~~~~~~A-U A A-U O~~~~~~~~~-CA A A C U U A A O-C U - Gu~~~CBmBUC 'a 0 CC-6~~U-U~B GI- c U ~~~~~-BUo U C GU- A A-Uq=A G C~~~A- U=Q 1650-A- U U-AA C 5' half GI U-A A CBCC ABUA C-B UC BaU1260-127'4-u BA ~~~~~~~~~~~~~~~~~~~~~~C-GBU,U -B0A B AU CBA AC.... U A UB~~~~~~~~~~_=C BaUACA UGIAA ~ C-B B-cu C%GCBUA C-B 4 U.. A C A %A A A V 1iiiiII CUB3AUAC BBBUBCCBUCU cc II- I-Il I AU ~ CBBa UBUEC ~~~~~UA UU I C C U2UOO uu U 2A0BUa A U VIB I C,CA U U 28oo-A ,C OfBI B CU B A B BSC C UB B-CA G ~U-GBIBA UU UAB%%B -C UA~% UCABUGCBGAABU - u C -C-U %UC-A GdB U ACBC5!-4BB%%A AC A AC'B% A A- AO0 A CBUUBAA BAC-cU.-U -B-U UC BIlla A -B U-A U U BCABCABC A AB-CAUCUBBBBCUBAA U U 0 C AAUCC AU AUB,Ba A II III I10 A-=UAB AAACB'AABC UUBBACCCUBBAUBU Aa G * CAUU-A U GA,I/JC U- C A A Uc -A-U B-=C- ,"aA UU',G4 C-B-B-c U AA%'U AII BB % C-B CIB C U- AC-a U UB A , UU AOB ~A a BBe U U C A UBI ac~B BuAA ICu - A-2 -CB AI 2700 =C- %A-IC,B-CC AC U-A -A Bl t413AIM B1C BOA c c- u A a - U B- C U-A C-B c200-C - B - GU.A-U U U-A BI =C-E uB-C UA U-A- U Ba -B-C a * U B^-UoA-U B aAAC CU I3I I I UO GOA, a A-U I k -C-BB-C A B AA CAAI BUoCBCC BA U III ! II C OIBCBB CU AUCAB; A Nucleic Acids Research, 1993, Vol. 21, No. 13 3059 B
  • 6. 3060 Nucleic Acids Research, 1993, Vol. 21, No. 13 8 UaAA A UG A UC AUAOU CC ou u o ~ ~ O -U "° O t U A CU ~ ~ ^GUCC AU2CA CCa C ¢ AQU U ac A A O-C A-U A A A-U U C a C A a 0U CCOQ"to~~~AUOOGc^C A A-U a. Ca U U A Ca U U ASCOU CACU C C CA C, A A 0-C U A C A a AU a A -A eQUAAQU UAUA CCU0U000 AUA A 1 1 l- U A UCCSUUC0 AUGU0OOAUACCU A AA A-U QA A A A a lUU-A U-A A-U A-UU( A 3GA a a A a u A C C o CCGCUOAACu Al 11 AAC~U U a Q A PA A A A GA CA U-A C-O a CA 10M- FIgure 2. Higher-order structure model for a representative eucaryotic nucleocytoplasmic LSU rRNA (Saccharomyces cerevisiae 5.8S + 26S; accession nos. J01355, K01048). A, 5'-half; B, 3'-half. Secondary and tertiary interactions are denoted as in Fig. 1. A Sk CAAA- ' A-U A-U A-U S-C U-A U -AS-c U-AU-A A C A A a u 528S
  • 7. Nucleic Acids Research, 1993, Vol. 21, No. 13 3061 A A A-U A-U O-C U-A 6 * A A c uuo A c C U AAA A A U-A B B A C-B A-U C A U-^ C-O U . B B-C U-A O-C C BBCCUUBBU AO-CO B U AU B0 A I Hit. U B B AB..C B- C U UU- eC. '.B CUBUUCBBcBa A-UB U-A A .- A-U A-AA C-B ACUA U*BUUQB C-B B*UA A A B-C B-C O-C UAAU U U-A A-U U-AAUC B,AB U-B AU- U-A C= A,%C B - C B-A CCB B U AAUUA-UaC-B -A 8-C ~~ ~ U AAAACAU AUUUC UAABUCU-A U i C a ~ ~~~~~~~~~a . cv U c C- BGBCA AAUCUBU UUABB cc A O-C a-CA AC AQUB- OCABCAAIU U~~~~-UUB A C-B - B ACBC" CA U-A U-A ACCA-U C-B1 A- uIU-B U-A A-U B U A A B-~~~CBA A A C-B -C A B- UU B-C BBBa'AABBAUU BG-CBBACAAB:=C'. -- Q C1U6 AU A B-C% C CUABA U A-U CA AAAACBBICUBAAB.-UBa C-B B-CB*U A C U-Ba A-U C-B U-AU .B A-UC-B B-CB C A-U UU U-A B-C A~U UA.A UAA -U Whaif B-CA-U -0-A U-AIiA %a CQaH!!2!6Qu_ ~~~AC-%- BBCBUUCACBUG"AACBAUCei 1.-- HlllA I lII loI--.I I I I I. I ABOCCUUBgBUBC UUOCUBBCB A A U C A UOcBBUO C 1.11. U A AOCOUCCU A U A A B C A U A B C 0 B-C AUUUBUAU U A AUUCABaC C B U U-A O-C U-A U-A o-C U U.B C C-B C BC-B CO U a AUU- A B B A U C -oBA B-C U * Q U-A C- a A-U U-A U Ba O-C U C U U A U B A C AA U C U B C-B BAAU ABlCB UA A B C B I I I I 1 I U uB U UAAAB A-U B-U A-U U-A A-U A-U B-U A-U B-C A-U A-U A UAU UAUUCAAU U &ABUUG a A-UuACA A=U ACBAUB-C A A U-A A A U-B A:O rr*Oo-u A * BCU :C BO- C-BU U O a U°A A-U B U- AA -C BU .CC BU=A U-A 11 UA CA~U B CC C-CC U-^ B-CC a U a B'a- UC UA L =lU. _c C-B _ -C C-B IUL BA °AUA uC AU U U A=U UC U A C- UCA c - c B AACU B3A% BBUCCC A ' BUCBB1B111 U 1%CU A O UC°oCu C U B CAA l BCUU BUBOCAOU AC BUU * 11I I* I I C UAB1 UUUCBUUA CB A u UU CAB AU C U U C B A IA C-B B-CBA - U Um C0ACe AA-U a * U B-C B-C AUA AUCA UACCOAAa C A I lil I Ie A U UBC AUBBCUUA ACA-U B C-B C-B C A A-U UC U UUO Ba B
  • 8. 3062 Nucleic Acids Research, 1993, Vol. 21, No. 13 oA <., <1 v o < a a, 6.1 < I. II I I -c o V 4 ., D. 44.>,i<>zt.> z<44 4444:> 4< 0 < a- < <= -C " 42 - 2 A < < < < ~4.>4~ 0 u6 It) 4it .2 0s U U cC c) 0 ._ CO 0 0 B4 00 . .~ OC ff .~ *1f
  • 9. Nucleic Acids Research, 1993, Vol. 21, No. 13 3063 Table 1. Growth of the LSU rRNA Database 1988 1990 1992 1993 Archaea 6 7 12 13 Bacteria 5 13 21 55 Plastid 4 8 13 31 Mitochondria 17 27 54 61 Eucarya 10 16 28 34 All 42 71 128 194 Table 2. List of complete LSU rRNA sequences Organism namel Status2 Accession Number ARCHAEA3 (ARCHAEBACTERIA) Euryarchaeota3 Archaeoglobus fulgidus 2.0 M64487 Halobacterinum halobiwn 2.0 X00872;X03407 Halobacterinu marismortui 2.0 X13738 Halococcus morrhuae 2.0 X05481 Methanobacterium thermoautotrophicum 2.0 X15364 Methanococcus vannielii 2.0 X02729 Methanospirillum hungatei 2.0 M61738;M81323 Thermococcus celer 2.0 * M67497 Thernoplasma acidophilum 2.0 M20822;M32298 Crenarchaeota3 Desulfurococcus mobilis 2.0 X05480 Sulfolobus solfataricus 2.0 M67495 Thermofilum pendens 2.0 X14835 Thennoproteus tenax 2.0 BACTERIA3 (EUBACTERIA) Thermotogales4 Thermotoga maritima Radio-resistant micrococci and relatives4 7hermus thernophilus Spirochetes and relatives4 Planctomyces and relatives4 Green sulfur bacteria4 F.lexibacter-cytophaga-bacteroides Purple bacteria4 Alpha subdivision Beta subdivision Gamma subdivision Cyanobacteria4 Gram-positive phylum4 High G+C subdivision 2.0 * 2.0 2.0 1.0 Borrelia burgdorferi Leptospira interrogans Pirellula marina Chlorobium limicola phylum4 Flavobacteriwn odoratum Flexibacterflexilis 1.0 1.0 1.0 Rhodobacter capsulatus Rhodobacter sphaeroides Bordetella avium Bordetella bronchiseptica Bordetella parapertussis Bordetella pertussis Neisseria gonorrhoeae Neisseria meningitidis Pseudomonas cepacia Aeromonas hydrophila Escherichia coli Plesiomonas shigelloides Pseudomonas aeruginosa Pseudomonas perfectomarina Ruminobacter amylophilus Synechococcus sp. 6301 (Anacystis nidulans) Frankiasp. #1 Frankia sp. #2 2.0 2.0 * * * * * 2.0 2.0 2.0 * 2.0 * 2.0 M67498 X12612 M88330 X14249 X07408 M31904;M62805 M32365;M62807 M31904;M62806 X06485 X53853 -55 X70370 X70371 X68368 X68323 X67293 X67300 X16368 X67946 J01695 X65487 Y00432 L03788 X06765 X00343;X00512 2.0 M55343 * M88466
  • 10. 3064 Nucleic Acids Research, 1993, Vol. 21, No. 13 Table 2. continued Organism namel Status2 Accession Number Micrococcus luteus 2.0 X06484 Mycobacterium kansasji * Z17212 Mycobacterium leprae 2.0 X56657 Streptomyces ambofaciens 2.0 M27245 Streptomyces griseus 2.0 M76388;X55435;X61478 Clostridial subdivision Clostridium botulinun * X65602 Clostridium tyrobutyricum * L08062 Pectinatus frisingensis * X68423 Peptococcus niger * X68428 Mycoplasmas and relatives Mycoplasma hyopneumoniae * X68421 Mycoplasma pneumoniae * X68422 Lactobacillus-bacillus-streptococcus phylum Bacilus sp. (strain PS3) 2.0 X60981 Bacillus alcalophilus * D11459 Bacillus anthracis * X64645 Bacilus cereus * S43429 Bacilus globisporus * X68424 Bacillus licheniformis * X68433 Bacilus stearothermophilus 2.0 # K02663;S43424 Bacills subtilis (rmB) 2.0 K00637;M10606;X00007 Bacillus subtilis (rrn)) D11460 Lactobacilus delbrueckii * X68426 Lactococcus lactis subsp. cremoris * X68434 Lactococcus lactis subsp. klctis (strain EL1403) * X64887 Lactococcus lactis subsp. lactis (strain DSM 20481T) * X68435 Listeria monocytogenes * S46732;X64533;X68420 Staphylococcus aureus * X68425 Staphylococcus camosus * X68419 Streptococcus oralis * X68427 Streptococcus thermophilus * X68429 PLASTIDS ProtocUsta5 Apicomplexa6 Chlorophyta (green algae) Plasmodimwfainparum6 Chamydomonas 66.72 Chl(ydomonas eugametos Chantdomonas frankii Chamydomonas gelatinosa Chlamydomonas geitkrii Chlamydomonas humicola Chlamydomonas indica Chlanydomonas iyengarii Chlamydomonas komma Chlamydomonas mexicana Chlamydomonas moewusii Chlanydomonas pallidostigmatica Chiamydomonas peterfli Chlamydomonas pitschmanni C7amydomonas reinharii Chiamydomonas starii Chiamydomonas zebra Chlorella elipsoidea Euglenophyta (euglenoid flagellates) Phaeophyta (brown algae) Rhodophyta (red algae) Astasia longa Euglena gracilis Pylaiella littoralis Pabnaria palnata 2.0 # * * * * * * * * * 2.0 * * 2.0 2.0 2.0 # X61660 X68923-26 Z17234 X68905 -09 Z15151 X68891-92 X68921-22 X68893 -98 X68885 -86 X68927-29 X68910-12 X68913- 18 X68899-904 X68887-88 Z15152 X15727;X16686-87 X68889-90 X68919-20 M36158 X14386 X12890 X61179 Z18289 Plantae Angiospermophyta (flowering plants) Alnus incana (alder) Conopholis americana Epifagus Wrgiana (beechdrops) Nicolia tbacum (tobacco) 2.0 2.0 2.0 * 2.0 M75719;M75722;M76448 X59768 M81884;X62099 J01446;Z00044
  • 11. Nucleic Acids Research, 1993, Vol. 21, No. 13 3065 Organism name' Status2 Accession Number Oryza sativa (rice) 2.0 X15901 Pisum sativum (pea) 2.0 M37430 Zea mays (maize) 2.0 X01365 Bryophyta Marchantia polymorpha (liverwort) 2.0 X01647;X04465 MITOCHONDRIA Protoctista5 Apicomplexa Plasmodiwn falciparum Plasmodium yoelii Chlorophyta (unicellular green algae) Chlamydomonas reinhardtii Ciliophora (ciliates) Paramecium primaurelia Paramecium tetraurelia Tetrahymena pyiformis Zoomastigina (zooflagellates) Crithidia fasciculata Crithidia oncopelti Leishmania tarentolae Leptomonas sp. Trypanosoma brucei * Plantae Angiospermophyta (flowering plants) Oenothera berteriana (primrose) Triticum aestivum (wheat) Zea mays (maize) Marchantia polymorpha (liverwort) Aspergillus nidulans Neurospora crassa Penicillium chrysogenum Podospora anserina Saccharomyces cerevisiae Schizosaccharomyces pombe Aedes albopictus (mosquito) Apis mellifera (honeybee) Artemia salina (brine shrimp) Drosophila melanogaster (fruit fly) Drosophila yakuba (fruit fly) Locusta migratoria (locust) Spodoptera frugiperda Aepyceros melanmpus Antilocapra americana Balaenoptera physalus (fin whale) Bos taurus (ox) Boselaphus tragocamelus Capra hircus (goat) Carassius auratus Cephalophus maxwelli Cervus unicolor (sambar deer) Crossostoma lacustre (freshwater loach) Cyprinus carpio (carp) Damnaliscus dorcas Gallus gallus domesticus (chicken) Gazella thomsoni Homo sapiens (human) Hydropotes inermis (Chinese water deer) Kobus ellipsiprymnus Madoqua kirki Muntiacus reevesi (Reeves' muntjac) Mus musculus (mouse) Mytilus edulis (blue mussel) M76611;M99416; S87790,/792,/801,/807,/809-10, /833-34,/836-40 M29000 1.0 M22649;M25123 -25130;X54860 1.0 K00634 1.0 K01749;X15917 1.0 M58010;M58011 1.0 X02548 1.0 X51736 1.0 X02354 1.0 J03814 1.0 X02547 1.0 X02559 1.0 # M37274;Z11889 2.0 K01868 M68929 1.0 X06961 1.0 X55443 * D13859 1.0 M30937;X14735 1.0 J01527 1.0 X06597 1.0 X01078 1.0 # L06178;X05011 1.0 M21833;X12965 1.0 X53506 1.0 X03240 1.0 X05287 M76713 M86496 1.0 M55540 X61145 1.0 J01394 M86494 1.0 M55541 M86498 1.0 M35875 * M91245 X61010 M86499 1.0 X52392 M86501 1.0 J01415;M12548;V00710 1.0 M35876 M86497 M86495 1.0 M35877 1.0 J01420 * M83756 Bryophyta Fungi Ascomycota Animalia Arthropoda Chordata
  • 12. 3066 Nucleic Acids Research, 1993, Vol. 21, No. 13 Table 2. continued Organism namel Odocoileus virginianus (white-tailed deer) Oryx gazeia Phoca vituina (harbor seal) Rana catesbeiana (frog) Rattus norvegicus (rat) Tragelaphus imberbis Tragulus napu Xenopus laevis (toad) Echinodermata (sea urchins) Paracentrotus lividus Strongylocentrotus purpuratus Nematoda Ascaris suum Caenorhabditis elegans EUCARYA3 (EUCARYOTES, NUCLEOCYTOPLASMIC) Giardia ardeae Giardia intestinalis Giardia muris protocdSta5 Acrasiomycota (cellular slime molds) Dictyosteliwn discoideum Ciliophora (ciliates) Tetrahymena pyrifonnis Tetrahymena thermophila Dinoflagellata (dinoflagellates) Prorocentrum micans Euglenophyta (euglenoid flagellates) Eugena gracilis Myxomycota (plasmodial slime molds) Didyiwum iridis Physarun polycephalum Rhizopoda (amastigote amoebas) Entamoeba histolytica Zoomastigina (zooflagellates) Crithidia fasciculata Trypanosoma brucei FunW Ascomycota Candida albicans Pnewnocystis carinii8 Saccharomyces carlsbergensis Saccharomyces cerevisiae Schizosaccharomyces pombe Zygomycota Mucor racemosus Plantae Angiospermophyta (flowering plants) Arabidopsis thaliana Brassica napus (rapeseed) Citus limon O(emon) Fragaria ananassa (strawberry) Lycopersicon escuentum (tomato) Oryza sativa (rice) Sinapis alba (mustard) Animalia Arthropoda Status2 1.0 * 1.0 1.0 1.0 1.0 1.0 1.0 2.0 2.0 Accession Number M35874 M86500 S37044;X63726 X12841 J01438 M86493 M55539 M10217 J04815 X12631 X54253 X54252 2.0 X58290 2.0 X52949 2.0 * X65063 X00601 M10752;X54004 1.0 X54512 X15973;X16108 1.0 X53361 X60210 1.0 V01159 * X65163 1.0 Y00055 X14553 * L07796;X70659 * S41246;M86760 J01352;V01285;V01325 2.0 J01355;K01048 * J01359;V01361;Z19136 M26190 X52320 * D10840;S39880 X05910 X15589;X58118 X07889;X13557 1.0 M11585 X15915;X57137 Drosophila melanogaster 1.0 M21017 Chordata Herdmania momus X53538 Homo sapiens (human) 1.0 J01866;M11167 Mus musclus (mouse) 1.0 J01871;X00525 Rattus norvegicus (rat) 1.0 J01881;KO1591;X00521;X01069 Xenopus borealis (toad) X59733 Xenopus laeVis (toad) 1.0 K01376;X00136;X59734 Nematoda Caenorhabditis elegans 1.0 X03680 lEucaryotic organisms are classified according to the scheme of Margulis,L. and Schwartz,K.V. (1988) [Five Kingdoms. An Illustrated Guide to the Phyla ofLife on Earth (2nd edition). W.H. Freeman and Co., New York]. 2New lisings that did not appear in the previous edition [Gutell,R.R., Schnare,M.N. and Gray,M.W. (1992) Nucleic Acids Res. 20, Supplement, 2095-2109]
  • 13. Nucleic Acids Research, 1993, Vol. 21, No. 13 3067 are denoted by *, whereas previous listings containing revised or additional accession number(s) are indicated by #. The most recently updated secondary structure now available in hardcopy form is listed as 1.0 (Release 1.0; July, 1991) or 2.0 (Release 2.0; January. 1993). Underlining of organism names in the above table indicates that an associated [NOTE] concerning the sequence appears with that name in the List of References. 3See 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. Natl. Acad. Sci. U.S.A. 87, 4576-4579. 4The classification used here follows the taxonomically ordered listing for SSU rRNA sequences on the RDP anonymous server. 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; and Woese,C.R. (1991) The use of ribosomal RNA in reconstructing evolutionary relationships among bacteria. In Evoution at the Molecular Level (Selander,R.K., Clark,A.G. and Whittman,T.S., eds.), pp. 1-24. Sinauer, Sunderland, MA. 5The term 'Protoctista', as defined and used by Margulis and Schwartz (1988), includes but is not limited to the 'Protista' (unicellular eucaryotes, or protists). 6See [NOTE] in List of References, below. 7See Cavalier-Smith,T. (1987) Eukaryotes with no mitochondria. Nature 326, 332-333. 8Placement of Pneumocystis carinii within the Ascomycota is probable but not yet proven; see Bruns,T.D., Vilgalys,R., Barns,S.M., Gonzalez,D., Hibbett,D.S., Lane,D.J., Simon,L., Stickel,S., Szaro,T.M., Weisburg,W.G. and Sogin, M.L. (1992) Evolutionary relationships within the fungi: analyses of nuclear small subunit rRNA sequences. Mol. Phylogent. Evol. 1, 231-241. List of references to LSU rRNA Sequences (new or revised from 1992 edition) ARCHAEA (ARCHAEBACTERIA) Halobactenum maismorhu' 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 Halobacteriwn marismortui. [NOTE: We used the published sequence, which differs from the database entry (X13738) at Ecoli positions 2506 (U vs. A) and 2523 (G vs. deletion).] Sulfolobus solfataicus Woese,C.R. (1991) Unpublished. Thermococcus celer Woese,C.R. and Achenbach,L. (1991) Unpublished. The sequence of Thermococcus celer 23S rRNA. BACTERIA (EUBACTERIA) Aeromonas hydrophila East,A.K. and Collins,M.D. (1993) FEMS Microbiol. Lett. 106, 129-134. Molecular characterization of DNA encoding 23S rRNA and 16S-23S rRNA intergenic spacer regions of Aeromonas hydrophila. BaciUus alcalophilus Sutherland,K.J., Kudo,T. and Horikoshi,K. (1992) Unpublished. B. alcalophilus 23S ribosomal RNA, partial sequence. Bacillus anthracis Ash,C. and Collins,M.D. (1992) FEMS Microbiol. Lett. 94, 75-80. Comparative analysis of 23S ribosomal RNA gene sequences of Bacillus anthracis and emetic Bacillus cereus determined by PCR-direct sequencing. Bacillus cereus (see BaciUus anthracis) Bacillus globisporus Ludwig,W., Kirchhof,G., Klugbauer,N., Weizenegger,M., Betzl,D., Ehrmann,M., Hertel,C., Jilg,S., Tatzel,R., Zitzelsberger,H., Liebl,S., Hochberger,M., Shah,J., Lane,D., Walln6fer,P.R. and Schleifer,K.H. (1992) System. Appl. Microbiol. 15, 487-501 Complete 23S ribosomal RNA sequences of gram-positive bacteria with a low DNA G+C content. Bacillus licheniformis (see Bacillus globisporus) Bacilus stearothermophilus (see also Bacillus anthracis) 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 stearothermophilus. [NOTE: We used the primary sequence presented in Kop et al. (1984). The secondary structure in this paper has an extra G between E.coli positions 11 and 12. This G is not present in the sequence newly determined by Ash and Collins (1992) (see Bacilus anthracis) which, however, differs at two other positions from that of Kop et al. (1984).] Bacilus subdlis (rmB) 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 ribosonal RNA operon, rmB. BaciUus subtilis (rrnI) Sutherland,K.J., Kudo,T. and Horikoshi,K. (1992) Unpublished. BordeteUla avium Mueller,M. (1993) Unpublished. B. avum gene for 23S rRNA.
  • 14. 3068 Nucleic Acids Research, 1993, Vol. 21, No. 13 Bordetea bvrnchisepeica Mueller,M. (1993) Unpublished. B. bronchiseptica gene for 23S rRNA. Bonetella panwpeSussis Mueller,M. (1992) Unpublished. B. parapernussis gene for 23S ribosomal RNA. Bonhlia pertussis Mueller,M. (1992) Unpublished. B. perussis gene for 23S ribosonal RNA. Bof,dia bugdorfen Schwartz,I., Gazumyan,A. and Schwartz,J.J. (1992) Unpublished. Sequence and structure of the ribosomal RNA genes of Borrelia burgdorferi. Clostriium botuiEnum East,A.K., Thompson,D.E. and Collins, M.D. (1992) J. Bacteriol. 174, 8158-8162. Analysis of operons encoding 23S rRNA of Clostriin botulinwn type A. Closiium iyrobut)ycum van der Meer,J.R., Ludwig,W. and de Vos,W.M. (1992) Unpublished. Characterization of a ribosomal RNA gene cluster from Clostridium tyrobutyricum: phylogenetic positioning based on the 16S and 23S nucleotide sequences. Fnmkia sp. Normand,P., Cournoyer,B., Simonet,P. and Nazaret,S. (1992) Gene 111, 119-124. Analysis of a ribosomal RNA operon in the actinomycete Frankia. Johnson,D.A. (1992) Thesis, Biology, University of Ottawa. Analysis of an rRNA operon from Frankia strain AcNl4a. [NOTE: The two Frankia sequences have many differences and so are listed as separate sequences (#1 and #2) in Table 1.] Lactobadilus delbrueckl subsp. bulgancus (see Bacislls globisporus) Lactococcus kacis subsp. cremoris (see Bacillus globisponas) Lactococcus lacis subsp. lactis (strain 1L1403) Chiaruttini,C. and Milet,M. (1993) J. Mol. Biol. 230, 57-76. Gene organization, primary structure and RNA processing analysis of a ribosomal RNA operon in Lactococcus lactis. Lactococcus lacts subsp. lactis (strain DSM 20481T) (see Bac4us gWoNiipous) [NOTE: Although the three Lactococcus sequences are very similar, strain DSM 20481T has a different hairpin sequence at E.coli positions -1170-1180.] Listeria monocytogenes (see also Bacillus globisponus) Thompson,D.E., Balsdon,J.T., Cai,J. and Collins,M.D. (1992) FEMS Microbiol. Lett. 96, 219-224. Studies on the ribosomal RNA operons of Listeria monocytogenes. Micrococcus luteus Regensburger,A., Ludwig,W., Frank,R., Bl6cker,H. and Schleifer,K.H. (1988) Nucleic Acids Res. 16, 2344. Complete nucleotide sequence of a 23S ribosomal RNA gene from Micrococcus luteus. [NOTE: We used the published sequence, which differs from the database entry (X06484) at the following E.coli positions (published sequence first, database entry second): 112, A vs. U; between 174 and 175, G vs. U.] Mycobactenwum kasii Fleurbaaij,G.A., McNally,M. and Marich,J.E. (1992) Unpublished. The complete nucleotide sequence of Mycobacterium knsasii 23S ribosomal RNA. Mycoplasma hyopneumoniae (see Bacillus globisporus) Mycoplasma pneumoniae (see Bacius globisporus) Neissena gonon*oeae Wolff,K., Sperka,S. and Stern,A. (1992) Nucleic Acids Res. 20, 4657. Phylogeny and nucleotide sequence of a 23S rRNA gene from Neisseria gonorrhoeae and Neiserria meningitidis. Neisseria meningitdis (see Neisseria gonorioee) Pecnatus fisigensis (see Bacillus globisporus) Peptocccus niger (see BaciElus globisporus) Plesiomonas shigelloides East, A.K., Allaway,D. and Collins, M.D. (1992) FEMS Microbiol. Lett. 95, 57-62. Analysis of DNA encoding 23S rRNA and 16S-23S rRNA intergenic spacer regions from Plesiomonas shigelloides.
  • 15. Nucleic Acids Research, 1993, Vol. 21, No. 13 3069 Pseudomonas cepacia Hopfl,P., Ludwig,W., Schleifer,K.H. and Larsen,N. (1989) Eur. J. Biochemn. 185, 355-364. The 23S ribosomal RNA higher-order structure of Pseudomonas cepacia and other prokaryotes. [NOTE: The position ofthe 3'-terminus is unclear in Hopfl et al. (1989) (there is a discrepancy between the number given in text and the secondary strucure figure). We have assigned the 3'-terminus by comparison with E.coli 23S rRNA.] Pseudomonas perfectomanila (= P. stutzen) Kerkhof,L.J. (1992) Unpublished. A species-specific probe for the marine bacterium, Pseudomonas perfectomarina (P. stutzeri strain Zobell) 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. [NOTE: Minor sequence heterogeneity has been noted in the three operons that have been sequenced.] Staphylococcus aureus (see Bacillus globisporus) Staphylococcus carnosus (see Bacillus globisporus) Streptococcus orais (see Bacillus globisporus) Streptococcus thermophilus (see Bacilus globisporus) Synechococcus sp. 6301 (formerly Anacystis nidlans) 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. [NOTE: The Douglas and Doolittle (1984) sequence differs from that of Kumano et al. (1983) at a number of positions. We used the former sequence, which is better supported by secondary structure comparisons.] Thermotoga maritia Achenbach,L. and Woese,C.R. (1991) Unpublished. Sequence of the ribosomal operon of Thermotoga maritima. PLASTIDS Alnus incana Levesque,M. and Johnson,D.A. (1992). Plant Mol. Biol. 18, 601-602. Nucleotide sequence of the chloroplast 23S rRNA gene from alder (Alnus incana). Imbeault,J.-C. and Johnson,D.A. (1991) Unpublished. Analysis of the 4.5S-5S rRNA intergenic region in rDNA from alder (Alnus incana) chloroplast. Chiamydomonas sp. 66.72 (see Chkunydomonas fimnkii) 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 Chlamydononas eugametos. Chlamydomonas fnmnkii Turmel,M., Gutell,R.R., Mercier,J.-P., Otis,C. and Lemieux,C. (1993) J. Mol. Biol., in press. Analysis ofthe chloroplast large subunit ribosomal RNA gene from 17 Chlamydomonas taxa. Three internal transcribed spacers and 12 group I intron insertion sites. Chlamydomonas geitlen (see Chlamydomonas fJankia) Chlamydomonas gekainosa (see Chlamydomonas frankii) Chlamydomonas hunicola (see Chlamydomonas ftenkiu) Chlamydomonas indica (see Chlamydomonas ftankii) Chiamydomonas iyengani (see Chlamydomonas franki) Chlamydomonas komma (see Chlamydomonas frankis) Chiamydomonas mexicana (see Chlamydomonas fnnkii) Chlamydomonas moewusui (see Chiamydomonas frakia) Chlamydomonas pallidostigmatica (see Chlamydomonas franAd)
  • 16. 3070 Nucleic Acids Research, 1993, Vol. 21, No. 13 Chlamydomonas peterfii (see Chlamydomonas frankli) Chlamydomonas pitschmannii (see Chlamydomonas franka) 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. [NOTE: The 5'-end of the 7S rRNA and the 3'-end of the 23S rRNA have been changed to agree with those of the corresponding species in C. eugametos chloroplast; see Chlamydomonas eugametos.)] Chlamydomonas starru (see Chlamydomonas frankii) Chlamydomonas zebra (see Chlamydomonas frankii) Chlorella eUipsoidea Yamada,T. 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. [NOTE: The putative intron described by Yamada and Shimaji (1987) is probably an internal transcribed spacer that is excised during post-transcriptional processing; see Turmel et al. (1991), Chlamydomonas eugametos). Epifagus virginiana (beechdrops) Wolfe,K.H., Katz-Downie,D.S., Morden,C.W. and Palmer,J.D. (1992) Plant Mol. Biol. 18, 1037-1048. Evolution of the plastid ribosomal RNA operon in a nongreen parasitic plant: Accelerated sequence evolution, altered promoter structure, and tRNA pseudogenes. Eugena graciis Yepiz-Plascencia,G.M., Jenkins,M.E. and Hallick,R.B. (1988) Nucleic Acids Res. 16, 9340. Nucleotide sequence of the Euglena gracilis chloroplast 23S rRNA gene of the rrnC operon. Schnare,M.N., Yepiz-Plascencia,G.M., Copertino,D.W., Hallick,R.B. and Gray,M.W. (1992) Nucleic Acids Res. 20, 1421. 5'- and 3'-terminal sequences of the chloroplast 16S and 23S ribosomal RNAs of Euglena gracilis. [NOTE: The sequence in Schnare et al. (1992) (X12890) revises the original one (X13310) presented in Yepiz-Plascencia et al. (1988).] Nicotiana tabacum Takaiwa,F. and Sugiura,M. (1982) Eur. J. Biochem. 124, 13-19. The complete nucleotide sequence of a 23-S rRNA gene from tobacco chloroplasts. 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,B.Y., Sugita,M., Deno,H., Kamogashira,T., Yamada,K., Kusuda,J., Takaiwa,F., Kato,A., Tohdoh,N., Shimada,H. and Sugiura,M. (1986) Plant Mol. Biol. Reporter 4, 111-147. The complete nucleotide sequence of the tobacco chloroplast genome. [See also: EMBO J. 5, 2043-2049 (1986). The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression.] [NOTE: The original sequence of Takaiwa and Sugiura (1982) differs from that presented later in Shinozaki et al. (1986). We used the more recent sequence because it agrees with other plant chloroplast sequences and is supported by the secondary structure.] Palmari palnata Singh,R.K. (1993) Unpublished. The organization and primary structure of the plastid rRNA operon from the red alga Palmaria palmata. Plasmodium fakiparum Gardner,M.J., Feagin,J.E., Moore,D.J., Rangachari,K., Williamson,D.H. and Wilson,R.J.M. (1993) Nucleic Acids Res. 21, 1067-1071. Sequence and organization of large subunit rRNA genes from the extrachromosomal 35 kb circular DNA of the malaria parasite Plasmodium falciparum. [NOTE: Phylogenetic analysis by Gardner et al. (1993) suggests that the P.falciparun 35-kbp DNA may be a plastid DNA remnant; see also Gardner,M.J., Feagin,J.E., Moore,D.J., Spencer,D.F., Gray,M.W., Williamson,D.H. and Wilson,R.J.M. (1991) Mol. Biochem. Parasitol. 48, 77-88.] PylaeUla littoralis Somerville,C.C., Jouannic,S., Martin,W.F., Kloareg,B. and Loiseaux-de Goer,S. (1993) Plant Mol. Biol. 21, 779-787. Secondary structure and phylogeny of the chloroplast 23S rRNA gene from the brown alga Pylaiella littoralis. Zea mays Edwards,K. and K6ssel,H. (1981) Nucleic Acids Res. 9, 2853-2869. The rRNA operon from Zea mays chloroplasts: nucleotide sequence of 23S rDNA and its homology with E.coli 23S rDNA. [NOTE: The 23S rRNA is thought to be fragmented at two positions as a result of excision of short internal transcribed spacers; see Kossel,H., Natt,E., Strittmatter,G., Fritzche,E., Gozdzicka-Jozefiak,A. and Przybyl,D. (1985) Structure and expression of rRNA operons from plastids of higher plants. In Molecular Form and Function ofthe Plant Genome (van Vloten-Doting,L., Groot,G.S.P. and Hall,T.C., eds.), NATO ASI Series (Series A: Life Sciences), Vol. 83, pp. 183-198, Plenum, New York.]
  • 17. Nucleic Acids Research, 1993, Vol. 21, No. 13 3071 MITOCHONDRIA Aepyceros melampus Allard,M.W., Miyamoto,M.M., Jarecki,L., Kraus,F. and Tennant,M.R. (1992) Proc. Natl. Acad. Sci. U.S.A. 89, 3972-3976. DNA systematics and evolution of the artiodactyl family Bovidae. Apis mellifem Vlasak,I., Burgschwaiger,S. and Kreil,G. (1987) Nucleic Acids Res. 15, 2388. Nucleotide sequence of the large ribosomal RNA of honeybee mitochondria. Crozier,R.H. and Crozier,Y.C. (1993) Genetics 133, 97-117. The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Artemia saUna Palmero,I., Renart,J. and Sastre,L. (1988) Gene 68, 239-248. Isolation of cDNA clones coding for mitochondrial 16S ribosomal RNA from the crustacean Artemia. [NOTE: The partial cDNA sequence of Palmero et al. (1988) shows many differences from the database entry (complete sequence). We used the sequence from the database.] Ascaris suum Okimoto,R., Macfarlane,J.L., Clary,D.O. and Wolsteholme,D.R. (1992) Genetics 130, 471-498. The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Caenorhabdis elegans (see Ascais suum) Carassius auratus (goldfish) Peng,G., Taylor,J.D. and Tchen,T.T. (1992) Biochem. Biophys. Res. Conmunn. 189, 445-449. Increased mitochondrial activities in pigmented (melanized) fish cells and nucleotide sequence of mitochondrial large rRNA. Crossostoma lacustre (freshwater loach) Tzeng,C.-S., Hui,C.-F., Shen,S.-C. and Huang,P.C. (1992) Nucleic Acids Res. 20, 4853 -4858. The complete nucleotide sequence of the Crossostoma lacustre mitochondrial genome: conservation and variations among vertebrates. Locusta migratoria Uhlenbusch,I., McCracken,A. and Gellissen,G. (1987) Curr. Genet. 11, 631-638. The gene for the large (16S) ribosomal RNA from the Locusta migratoria mitochondrial genome. [NOTE: The prinmay sequence figure in Uhlenbusch et al. (1987) has the sequence presented backwards and a few positions are not clear. These positions (corresonding to E.coli 1933 and 2659) are clearly G in the secondary structure presented in the same paper; however, they are C in the database entry (X05287), which also displays the sequence backwards.] Marchantia poymorpha Oda,K., Yamato,K., Ohta,E., Nakamura,Y., Takemura,M., Nozato,N., Akashi,K., Kanegae,T., Ogura,Y., Kohchi,T. and Ohyama,K. (1992) Plant Mol. Biol. Reporter 10, 105-163. Complete nucleotide sequence of the mitochondrial DNA from a liverwort, Marchantia polymorpha. [# See also: J. Mol. Biol. 223, 1 -7 (1992). Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA: a prnimtive form of plant mitochondrial genome.] Mytilus edulis Hoffmann,R.J., Boore,J.L. and Brown,W.M. (1992) Genetics 131, 397-412. A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Paramecium pnmaurelia Seilhamer,J.J. and Cummings,D.J. (1981) Nucleic Acids Res. 9, 6391-6406. Structure and sequence of the mitochondrial 20S rRNA and tRNA tyr gene of Paramecium primaurelia. Seilhamer,J.J., Gutell,R.R. and Cummings,D.J. (1984) J. Biol. Chem. 259, 5173-5181. Paramecium mitochondrial genes. II. Large subunit rRNA gene sequence and microevolution. [NOTE: The sequence in Seilhamer and Cummings (1981) differs from that in Seilhamer et al. (1984). We used the latter (more recent) version.] Penicifium chrysogenum Naruse,A., Yamamoto,H. and Sekiguchi,J. (1993) Biochim. Biophys. Acta 1172, 353-356. Nucleotide sequence of the large mitochondrial rRNA gene of Penicillium chrysogenum. Phoca vitulina Arnason,U. and Johnsson,E. (1992) J. Mol. Evol. 34, 493-505. The complete mitochondrial DNA sequence of the harbor seal, Phoca vitulina. Plasmodium falkqnum Feagin,J.E., Werner,E., Gardner,M.J., Williamson,D.H. and Wilson,R.J.M. (1992) Nucleic Acids Res. 20, 879-887. Homologies between the contiguous and fragmented rRNAs of two Plasmodium falciparum extrachromosomal DNAs are limited to core sequences.
  • 18. 3072 Nucleic Acids Research, 1993, Vol. 21, No. 13 Vaidya,A.B., Lashgari,M.S., Pologe,L.G. and Morrisey,J. (1993) Strctuanl features ofPlasodwn cytochrome b that may underlie susceptibility to 8-aminoqinolines and hydroxynaphthoquinones. Mol. Biochem. Parasitol. 58, 33-42. Plasmnodiw yoeEli Vaidya,A.B., Akella,R. and Suplick,K. (1989) Mol. Biochem. Parasitol. 35, 97-108. Sequences similar to genes for two nitochondrial proteins and portions of ribosomal RNA in tandemly arrayed 6-kilobase-pair DNA of a malarial parasite. [NOTE: A corrigendum by the same authors (Mol. Biochem. Parasitol. 39, 295 -296 (1990)) contains corrections to their original sequence.] Suplick,K., Morrisey,J. and Vaidya,A.B. (1990) Mol. Cell. Biol. 10, 6381-6388. Complex tription from the extrachromosomal DNA encoding mitochondrial functions of Plasmodium yoelii. Spodoptera fiugqeIa Pashley,D.P. and Ke,L.D. (1992) Mol. Biol. Evol. 9, 1061-1075. Sequence evolution in mitochondrial ribosomal and ND-1 genes in Lepidoptera: implications for phylogenetic analyses. lWdcum aeslivum Falconet,D., Sevignac,M. and Quetier,F. (1988) Curr. Genet. 13, 75-82. Nucleotide sequence and determiation ofthe extremities ofthe 26S ribosomal RNA gene in wheat mitochondria: evidence for sequence rearrangements in the ribosomal genes of higher plants. Spencer,D.F., Schnare,M.N., Coulthart,M.B. and Gray,M.W. (1992) Plant Mol. Biol. 20, 347-352. Sequence and organization of a 7.2 kb region of wheat mitochondrial DNA containing the large subunit (26S) rRNA gene. EUCARYA (EUCARYOTES, NUCLEOCYTOPLASMIC) Brassica napus Okumura,S. and Shimada,H. (1992) Nucleic Acids Res. 20, 3510. Nucleotide sequence of genes for a 5.8S and 25S rRNA from rape seed (Brassica napus). adia albicans Mercure,S., Rougeau,N., Montplaisir,S. and Lemay,G. (1993) Nucleic Acids Res. 21, 1490. The nucleotide sequence of the 25S rRNA-encoding gene from Candida albicans. Lott,T.J. (1992) Unpublished. Nucleotide sequence of the 5.8S rDNA from Candida albicans. Ddymum s Johansen,S., Johansen,T. and Haugli,F. (1992) Curr. Genet. 22, 305-312. Extrachromosomal ribosomal DNA of Didyniun iridis: sequence analysis of the large subunit ribosomal RNA gene and sub-telomeric region. Drosophila melanogaster Tautz,D., Hancock,J.M., Webb,D.A., Tautz,C. and Dover,G.A. (1988) Mol. Biol. Evol. 5, 366-376. Complete sequences of the rRNA genes of Drosophila melanogaster. Linares,A.R., Hancock,J.M. and Dover,G.A. (1991) J. Mol. Biol. 219, 381-390. Secondary structure constraints on the evolution of Drosophila 28 S ribosomal RNA expansion segments Rousset,F., P6landadis,M. and Solignac,M. (1991) Proc. Natl. Acad. Sci. U.S.A. 88, 10032-10036. Evolution of compensatory substitutions through GU intermediate state in Drosophila rRNA. [NOTE: Minor corrections are presented in Linares et al. (1991) and Rousset et al. (1991). The latter contains a sequence of25 nucleoddes absent in Tautz etal. (1988).] Entwnoeba histolyfica Ramachandran,S., Bhattacharya,A. and Bhattacharya,S. (1993) Nucleic Acids Res. 21, 2011. Nucleotide sequence analysis of the rRNA transcription unit of a pathogenic Entamoeba histolytica strain HM-EIMSS. Ghada wveae van Keulen,H., Horvat,S., Erlandsen,S.L. and Jarroll,E.L. (1991) Nucleic Acids Res. 19, 6050. Nucleotide sequence of the 5.8S and large subunit rRNA genes and the internal transcribed spacer and part of the external spacer from Giardia ardeae. [NOTE: See van Keulen et al. (1992) (Giarna muris) for primary sequence. The G. ardeae sequence in this paper has several differences from the database entry (X58290). We used the G. ardeae sequence presented in the G. muns paper, which fits the secondary structure better (the V3 structure shown in the G. ardeae paper is missing a G).j Giardia intesuinals (= G. d lis, G. mbia) Healey,A., Mitchell,R., Upcroft,J.A., Boreham,P.F.L. and Upcroft,P. (1990) Nucleic Acids Res. 18, 4006. Complete nucleotide sequence of the ribosomal RNA tandem repeat unit from Giardia intestinalis. [NOTE: A minor correction (insertion of a C) is presented in the G. muris reference. The two ambiguous positions are G according to Edlind,T.D., Sharetzsky,C. and Cha, M.E. (1990) Ribosomal RNA of the primitive eukaryote Giardia lamblia: large subunit domain I and potential processing signals. Gene 96, 289-293.] Ciri mums van Keulen,H., Gutell,R.R., Campbell,S.R., Erlandsen,S.L. and Jarrell,E.L. (1992) J. Mol. Evol. 35, 318-328. The nucleotide sequence of the entire ribosomal DNA operon and the strucure of the large subunit rRNA of Giardia munris.
  • 19. Nucleic Acids Research, 1993, Vol. 21, No. 13 3073 Homo sapins Maden,B.E.H., Dent,C.L., Farrell,T.E., Garde,J., McCallum,F.S. and Wakeman,J.A. (1987) Biochem J. 246, 519-527. Clones of human ribosomal DNA containing the complete 18 S-rRNA and 28 S-rRNA genes. Characterization, a detailed map of the human ribosomal transcription unit and diversity among clones. [NOTE: A correction was made in Maden et al. (1987) to eliminate an extra GC (following position 50) in the original 5.8S rRNA sequence of Khan,M.S.N and Maden,B.E.H. (1977) Nucleic Acids Res. 4, 2495-2505. Nucleotide sequence relationships between vertebrate 5.8 S ribosomal RNAs.] Gonzalez,I.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. Variation among human 28S ribosomal RNA genes. Pneumocystis carinni Liu,Y., Rocourt,M., Pan,S., Liu,C. and Leibowitz,M.J.(1992) Nucleic Acids Res. 20, 3763-3772. Sequence and variability of the 5.8S and 26S rRNA genes of Pneumocystis carinii. Raltus norvegicus Subrahmanyam,C.S., Cassidy,B., Busch,H. and Rothblum,L.I. (1982) Nucleic Acids Res. 10, 3667-3680. Nucleotide sequence of the region between the 18S rRNA sequence and the 28S rRNA sequence of rat ribosomal DNA. Chan,Y.-L., Olvera,J. and Wool,I.G. (1983) Nucleic Acids Res. 11, 7819-7831. The structure of rat 28S ribosomal ribonucleic acid inferred from the sequence of nucleotides in a gene. Hadjiolov,A.A., Georgiev,O.I., Nosikov,V.V. and Yavachev,L.P. (1984) Nucleic Acids Res. 12, 3677-3693. Primary and secondary structure of rat 28 S ribosomal RNA. Wool,I.G. (1986) In Hardesty,B. and Kramer,G. (eds.). Structure, Function, and Genetics of Ribosomes. Springer-Verlag, New York, pp. 391-411. Studies on the structure of eukaryotic (mammalian) ribosomes. [NOTE: We used the most recent (revised) sequence given in Wool (1986).] Saccharomyces carlsbergensis Veldman,G.M., Brand, R.C., Klootwijk,J. and Planta,R.J. (1980) Nucleic Acids Res. 8, 2907-2920. Some characteristics of processing sites in ribosomal precursor RNA of yeast. Veldman,G.M., Klootwijk,J., van Heerikhuizen,H. and Planta,R.J. (1981) Nucleic Acids Res. 9, 4847-4862. The nucleotide sequence of the intergenic region between the 5.8S and 26S rRNA genes of the yeast ribosomal RNA operon. Possible implications for the interaction between 5.8S and 26S rRNA and the processing of the primary transcript. Veldman,G.M., Klootwijk,J., de Regt,V.C.H.F., Planta,R.J., Branlant,C., Krol,A. and Ebel,J.-P. (1981) Nucleic Acids Res. 9, 6935-6952. The primary and secondary structure of yeast 26S rRNA. Saccharomyces cerevisiae Rubin,G.M. (1973) J. Biol. Chem. 248, 3860-3875. The nucleotide sequence of Saccharomyces cerevisiae 5.8 S ribosomal ribonucleic acid. Georgiev,O.I., Nikolaev,N., Hadjiolov,A.A., Skryabin,K.G., Zakharyev,V.M. and Bayev,A.A. (1981) Nucleic Acids Res. 9, 6953-6958. The structure of the yeast ribosomal RNA genes. 4. Complete sequence of the 25 S rRNA gene from Saccharomyces cerevisiae. [NOTE: The S. carlsbergensis and S.cerevisiae sequences are very similar; most of the differences likely reflect errors in the latter sequence. However, we used the S.cerevisiae sequence because the S. carlsbergensis 5.8S rRNA sequence is not complete.] Schizosaccharomyces pombe Schaak,J., Mao,J.I. and S611,D.G. (1982) Nucleic Acids Res. 10, 2851-2864. The 5.8S RNA gene sequence and the ribosomal repeat of Schizosaccharomyces pombe. Lapeyre,B.B. and Feliu, J.J. (1992) Unpublished. Nucleotide sequence of the 25S ribosomal RNA from Schizosaccharomyces pombe. Sinapis alba Capesius,I. (1991) Plant Mol. Biol. 16, 1093-1094. Nucleotide sequence of a 25S rRNA gene from mustard (Sinapis alba). Rathgeber,J. and Capesius,I. (1989) Nucleic Acids Res. 17, 7522. Nucleotide sequence of the 18S-25S spacer region from mustard DNA. Tetrahymena thernophila Engberg,J., Nielsen,H., Lenaers,G., Murayama,O., Fujitani,H. and Higasagawa,T. (1990) J. Mol. Evol. 30, 514-521. Comprison ofprimary and secondary 26S rRNA structures in two Tetrhymena species: Evidence for a strong evolutionary and stuctural constraint in expansion segments. Engberg,J. and Nielsen,H. (1990) Nucleic Acids Res. 18, 6915-6919. Complete sequence of the extrachromosomal rDNA molecule from the ciliate Tetrahymena thermophila strain B1868VII. [NOTE: The sequence shown in Engberg and Nielsen (1990) is missing positions 6601-6700 (corresponding to E.coli positions 1599-1698.]
  • 20. 3074 Nucleic Acids Research, 1993, Vol. 21, No. 13 Xenopus lWis Hall,L.M.C. and Maden,B.E.H. (1980) Nucleic Acids Res. 8, 5993-6005. Nucleotide sequence through the 18S-28S intergene region of a vertebrate ribosomal transcription unit. Ware,V.C., Tague,B.W., Clark,C.G., Gourse,R.L., Brand,R.C.and Gerbi,S.A. (1983) Nucleic Acids Res. 11, 7795-7817. Sequence analysis of 28S ribosomal DNA from the amphibian Xenopus laevis. Stebbins-Boaz,B. and Gerbi,S.A. (1991) J. Mol. Biol. 217, 93-112. Structunal analysis of the peptidyl transferase region in ribosomal RNA Ajuh,P.M., Heeney,P.A. and Maden,B.E.H. (1991) Proc. R. Soc. Lond., B, Biol Sci. 245, 65-71. Xenopus boreals and Xenopus kwvis 28S ribosomal DNA and the complete 40S ribosomal precursor RNA coding units of both species. Schnare,M.N. and Gray,M.W. (1992) Nucleic Acids Res. 20, 608. A new 3'-terminus for Xenopus laevis 28S ribosomal RNA. [NOTE: Corrections to the sequence of Domain V in Ware et al. (1983) may be found in Stebbins-Boaz and Gerbi (1991). The most recent revisions (Ajuh et al. (1991); Schnare and Gray (1992)) are being incorporated into the current secondaxy structure model.]