Fragmentation of the large subunit ribosomal RNA gene in oyster mitochondrial genomes

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Milbury, Coren A ^a,c   Lee, Jung C ^b   Cannone, Jamie J ^b   Gaffney, Patrick M ^a   Gutell, Robin R ^b  

^a UNIVERSITY OF DELAWARE   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LARGE SUBUNIT RIBOSOMAL RNA; COMPLEMENTARY DNA; MITOCHONDRIAL DNA;

ARTICLE; CONTROLLED STUDY; CRASSOSTREA GIGAS; CRASSOSTREA HONGKONGENSIS; CRASSOSTREA VIRGINICA; EXPRESSED SEQUENCE TAG; LARGE RIBOSOMAL SUBUNIT; MITOCHONDRIAL GENOME; NONHUMAN; NUCLEOTIDE SEQUENCE; OYSTER; PROTEIN SECONDARY STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CONFORMATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; MOLECULAR GENETICS; PLACOZOA; RNA GENE; X RAY CRYSTALLOGRAPHY;

ANIMALIA; EUKARYOTA; METAZOA; OSTREIDAE;

ANIMALS; BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DNA, COMPLEMENTARY; DNA, MITOCHONDRIAL; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENES, RRNA; GENOME, MITOCHONDRIAL; MODELS, GENETIC; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; OSTREIDAE; PLACOZOA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOME SUBUNITS, LARGE; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 77956456400     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-485     Document Type: Article

References (87)

1. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD. Molecular Biology of the Cell. 1983, New York: Garland Publishing, Inc., 3.
2. Sloof P, Van den Burg J, Voogd A, Benne A, Agostinelli M, Borst P, Gutell R, Noller HF. Further characterization of the extremely small mitochondrial ribosomal RNAs from trypanosomes: a detailed comparison of the 9S and 12S RNAs from Crithidia fasciculata and Trypanosoma brucei with rRNAs from other organisms. Nucl Acids Res 1985, 13:4171-4191. 10.1093/nar/13.11.4171, 341304, 2409531.
3. Chao S, Sederoff R, Levings C. Nucleotide sequence and evolution of the 18S ribosomal RNA gene in maize mitochondria. Nucl Acids Res 1984, 12:6629-6644. 10.1093/nar/12.16.6629, 320101, 6089124.
4. Dale RM, Mendu N, Ginsburg H, Kridl JC. Sequence analysis of the maize mitochondrial 26S rRNA gene and flanking regions. Plasmid 1984, 11:141-150. 10.1016/0147-619X(84)90019-2, 6728934.
5. Spencer DF, Bonen L, Gray MW. Primary sequence of wheat mitochondrial 5S ribosomal ribonucleic acid: functional and evolutionary implications. Biochem 1981, 20:4022-4029.
6. Lang BF, Goff LJ, Gray MW. A 5S rRNA gene is present in the mitochondrial genome of the protist Reclinomonas americana but is absent from red algal mitochondrial DNA. J Mol Biol 1996, 261:607-613.
7. Turmel M, Lemieux C, Burger G, Lang BF, Otis C, Plante I, Gray MW. The complete mitochondrial DNA sequences of Nephroselmis olivacea and Pedinomonas minor: two radically different evolutionary patterns within green algae. Plant Cell 1999, 11:1717-1730. 10.1105/tpc.11.9.1717, 144307, 10488238.
8. Turmel M, Otis C, Lemieux C. The complete mitochondrial DNA sequence of Mesostigma viride identifies this green alga as the earliest green plant divergence and predicts a highly compact mitochondrial genome in the ancestor of all green plants. Mol Biol Evol 2002, 19:24-38.
9. Turmel M, Otis C, Lemieux C. The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: Insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants. Proc Natl Acad Sci USA 2002, 99:11275-11280. 10.1073/pnas.162203299, 123247, 12161560.
10. Burger G, Saint-Louis D, Gray MW, Lang BF. Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea: cyanobacterial introns and shared ancestry of red and green algae. Plant Cell 1999, 11:1675-1694. 10.1105/tpc.11.9.1675, 144311, 10488235.
11. Wolff G, Plante I, Lang BF, Kück U, Burger G. Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii: gene content and genome organization. J Mol Biol 1994, 237:75-86. 10.1006/jmbi.1994.1210, 8133522.
12. Ohta N, Sato N, Kuroiwa T. Structure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence. Nucl Acids Res 1998, 26:5190-5298. 10.1093/nar/26.22.5190, 147977, 9801318.
13. Oudot-Le Secq MP, Fontaine JM, Rousvoal S, Kloareg B, Loiseaux-de Goer S. The complete sequence of a brown algal mitochondrial genome, the ectocarpale Pylaiella littoralis (L.) Kjellm. J Molec Evol 2001, 53:80-88.
14. Oudot-le Secq MP, Kloareg B, Loiseaux-de Goer S. The mitochondrial genome of the brown alga Laminaria digitata: a comparative analysis. European Journal of Phycology 2002, 37:163-172.
15. Gray MW, Lang BF, Burger G. Mitochondria of protists. Annu Rev Gen 2004, 38:477-524.
16. Bullerwell CE, Schnare MN, Gray MW. Discovery and characterization of Acanthamoeba castellanii mitochondrial 5S rRNA. RNA - a Publication of the RNA Society 2003, 9:287-292.
17. Cannone J, Subramanian S, Schnare M, Collett J, D'Souza L, Du Y, Feng B, Lin N, Madabusi L, Muller K, et al. The Comparative RNA Web (CRW) Site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 2002, 3:2. 10.1186/1471-2105-3-2, 65690, 11869452.
18. Gutell RR, Weiser B, Woese CR, Noller HF. Comparative anatomy of 16S-like ribosomal RNA. Progress in Nucleic Acid Research and Molecular Biology 1985, 32:155-216. full_text, 3911275.
19. Kruger K, Grabowski PJ, Zaug AJ, Sands J, Gottschling DE, Cech TR. Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell 1982, 31:147-157. 10.1016/0092-8674(82)90414-7, 6297745.
20. Jackson SA, Cannone JJ, Lee JC, Gutell RR, Woodson SA. Distribution of rRNA introns in the three-dimensional structure of the ribosome. J Mol Biol 2002, 323:35-52. 10.1016/S0022-2836(02)00895-1, 12368097.
21. Trust TJ, Logan SM, Gustafson CE, Romanik PJ, Kim NW, Chan VL, Ragan MA, Guerry P, Gutell RR. Phylogenetic and molecular characterization of a 23S rRNA gene positions the genus Campylobacter in the epsilon subdivision of the Proteobacteria and shows that the presence of transcribed spacers in common in Campylobacter spp. Journal of Bacteriology 1994, 176:4597-4609. 196280, 8045890.
22. Kim NW, Gutell RR, Chan VL. Complete sequences and organization of the rrnA operon from Campylobacter jejuni TGH9011 (ATCC43431). Gene 1995, 164:101-106. 10.1016/0378-1119(95)00471-H, 7590296.
23. Gray MW, Schnare MN. Evolution of rRNA gene organization. Ribosomal RNA: Structure, evolution, processing, and function in protein biosynthesis 1996, 49-69. Boca Raton: CRC Press, Zimmermann R, Dahlberg A.
24. Evguenieva-Hackenberg E. Bacterial ribosomal RNA in pieces. Molec Microbiol 2005, 57:318-325.
25. Forget L, Ustinova J, Wang Z, Huss VAR, Franz Lang B. Hyaloraphidium curvatum: A linear mitochondrial genome, tRNA editing, and an evolutionary link to lower fungi. Mol Biol Evol 2002, 19:310-319.
26. Heinonen T, Schnare M, Young P, Gray M. Rearranged coding segments, separated by a transfer RNA gene, specify the two parts of a discontinuous large subunit ribosomal RNA in Tetrahymena pyriformis mitochondria. J Biol Chem 1987, 262:2879-2887.
27. Burger G, Zhu Y, Littlejohn TG, Greenwood SJ, Schnare MN, Lang BF, Gray MW. Complete sequence of the mitochondrial genome of Tetrahymena pyriformis and comparison with Paramecium aurelia mitochondrial DNA. J Mol Biol 2000, 297:365-380. 10.1006/jmbi.2000.3529, 10715207.
28. Boer PH, Gray MW. Scrambled ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA. Cell 1988, 55:399-411. 10.1016/0092-8674(88)90026-8, 2846180.
29. Denovan-Wright EM, Lee RW. Comparative structure and genomic organization of the discontinuous mitochondrial ribosomal RNA genes of Chlamydomonas eugametos and Chlamydomonas reinhardtii. J Mol Biol 1994, 241:298-311. 10.1006/jmbi.1994.1505, 7520083.
30. Denovan-Wright EM, Sankoff D, Spencer DF, Lee RW. Evolution of fragmented mitochondrial ribosomal RNA genes in Chlamydomonas. Journal of Molecular Evolution 1996, 42:382-391. 10.1007/BF02498632, 8642607.
31. Nedelcu AM, Spencer DF, DenovanWright EM, Lee RW. Discontinuous mitochondrial and chloroplast large subunit ribosomal RNAs among green algae: Phylogenetic implications. Journal of Phycology 1996, 32:103-111.
32. Kroymann J, Zetsche K. The mitochondrial genome of Chlorogonium elongatum inferred from the complete sequence. J Molec Evol 1998, 47:431-440. 10.1007/PL00006400, 9767688.
33. Kairo A, Fairlamb AH, Gobright E, Nene V. A 7.1 kb linear DNA molecule of Theileria parva has scrambled rDNA sequences and open reading frames for mitochondrially encoded proteins. EMBO J 1994, 13:898-905. 394889, 8112303.
34. Feagin JE, Gardner MJ, Williamson DH, Wilson RJM. The putative mitochondrial genome of Plasmodium-Falciparum. J Protozool 1991, 38:243-245.
35. Gillespie D, Salazar N, Rehkopf D, Feagin J. The fragmented mitochondrial ribosomal RNAs of Plasmodium falciparum have short A tails. Nucl Acids Res 1999, 27:2416-2422. 10.1093/nar/27.11.2416, 148810, 10325433.
36. Feagin JE. Mitochondrial genome diversity in parasites. Intl J Parasitol 2000, 30:371-390.
37. Nash EA, Nisbet RER, Barbrook AC, Howe CJ. Dinoflagellates: a mitochondrial genome all at sea. Trends in Genetics 2008, 24:328-335. 10.1016/j.tig.2008.04.001, 18514360.
38. Waller RF, Jackson CJ. Dinoflagellate mitochondrial genomes: stretching the rules of molecular biology. BioEssays 2009, 31:237-245. 10.1002/bies.200800164, 19204978.
39. Jackson C, Norman J, Schnare M, Gray M, Keeling P, Waller R. Broad genomic and transcriptional analysis reveals a highly derived genome in dinoflagellate mitochondria. BMC Biology 2007, 5:41. 10.1186/1741-7007-5-41, 2151934, 17897476.
40. Slamovits CH, Saldarriaga JF, Larocque A, Keeling PJ. The Highly Reduced and Fragmented Mitochondrial Genome of the Early-branching Dinoflagellate Oxyrrhis marina Shares Characteristics with both Apicomplexan and Dinoflagellate Mitochondrial Genomes. Journal of Molecular Biology 2007, 372:356-368. 10.1016/j.jmb.2007.06.085, 17655860.
41. Kamikawa R, Inagaki Y, Sako Y. Fragmentation of Mitochondrial Large Subunit rRNA in the Dinoflagellate Alexandrium catenella and the Evolution of rRNA structure in Alveolate Mitochondria. Protist 2007, 158:239-245. 10.1016/j.protis.2006.12.002, 17291829.
42. Milbury CA, Gaffney PM. Complete mitochondrial DNA sequence of the eastern oyster Crassostrea virginica. Marine Biotechnology 2005, 7:697-712. 10.1007/s10126-005-0004-0, 16132463.
43. Yu Z, Wei Z, Kong X, Shi W. Complete mitochondrial DNA sequence of oyster Crassostrea hongkongensis - a case of "Tandem duplication-random loss" for genome rearrangement in Crassostrea?. BMC Genomics 2008, 9:477. 10.1186/1471-2164-9-477, 2576254, 18847502.
44. Ren J, Liua X, Zhanga G, Liu B, Guo X. "Tandem duplication-random loss" is not a real feature of oyster mitochondrial genomes: comment. BMC Genomics 2009, 10:1-6. 10.1186/1471-2164-10-84, 2671524, 19121221.
45. Dellaporta SL, Xu A, Sagasser S, Jakob W, Moreno MA, Buss LW, Schierwater B. Mitochondrial genome of Trichoplax adhaerens supports Placozoa as the basal lower metazoan phylum. Proceedings of the National Academy of Sciences 2006, 103:8751-8756.
46. Signorovitch AY, Buss LW, Dellaporta SL. Comparative genomics of large mitochondria in Placozoans. PLoS Genetics 2007, 3:e13. 10.1371/journal.pgen.0030013, 1781491, 17222063.
47. Ren J, Shen X, Jiang F, Liu B. The mitochondrial genomes of two scallops, Argopecten irradians and Chlamys farreri (Mollusca: Bivalvia): the most highly rearranged gene order in the Family Pectinidae. Journal of Molecular Evolution 2010, 70:57-68. 10.1007/s00239-009-9308-4, 20013337.
48. Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, Lindgreen S, Wilkinson AC, Finn RD, Griffiths-Jones S, Eddy SR, Bateman A. Rfam: updates to the RNA families database. Nucl Acids Res 2009, 37:D136-140. 10.1093/nar/gkn766, 2686503, 18953034.
49. Gutell RR, Fox GE. A compilation of large subunit RNA sequences presented in a structural format. Nucl Acids Res 1988, 16:R175-R269. 340912, 3368328.
50. Gutell RR, Larsen N, Woese CR. Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Micro Rev 1994, 58:10-26.
51. Lydeard C, Holznagel WE, Schnare MN, Gutell RR. Phylogenetic analysis of molluscan mitochondrial LSU rDNA sequences and secondary structures. Molecular Phylogenetics and Evolution 2000, 15:83-102. 10.1006/mpev.1999.0719, 10764537.
52. Salvi D, Bellavia G, Cervelli M, Mariottini P. The analysis of rRNA sequence-structure in phylogenetics: An application to the family Pectinidae (Mollusca: Bivalvia). Molecular Phylogenetics and Evolution 2010, 56:1059-1067. 10.1016/j.ympev.2010.04.025, 20416386.
53. Gillespie JJ, Johnston JS, Cannone JJ, Gutell RR. Characteristics of the nuclear (18 S, 5.8 S, 28S and 5S) and mitochondrial (12S and 16S) rRNA genes of Apis mellifera (Insecta:Hymenoptera): structure, organization, and retrotransposable elements. Insect Molecular Biology 2006, 15:657-686. 10.1111/j.1365-2583.2006.00689.x, 2048585, 17069639.
54. Gray MW, Schnare MN. Evolution of the Modular Structure of rRNA. The Ribosome: Structure, Function, & Evolution 1990, 589-597. Washington DC: American Society for Microbiology, Warner JR.
55. Michot B, Qu L, Bachellerie J. Evolution of large-subunit rRNA structure: The diversification of divergent D3 domain among major phylogenetic groups. European Journal of Biochemistry 1990, 188:219-229. 10.1111/j.1432-1033.1990.tb15393.x, 2138538.
56. Frank J, Zhu J, Penczek P, Li Y, Srivastava S, Verschoor A, Radermacher M, Grassucci R, Lata RK, Agrawal RK. A model of protein synthesis based on cryo-electron microscopy of the E. coli ribosome. Nature 1995, 376:441-444. 10.1038/376441a0, 7630422.
57. Nissen P, Hansen J, Ban N, Moore PB, Steitz TA. The Structural Basis of Ribosome Activity in Peptide Bond Synthesis. Science 2000, 289:920-930. 10.1126/science.289.5481.920, 10937990.
58. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. The complete atomic structure of the large ribosomal subunit at 2.4 angstrom resolution. Science 2000, 289:905-920. 10.1126/science.289.5481.905, 10937989.
59. Sharma MR, Koc EC, Datta PP, Booth TM, Spremulli LL, Agrawal RK. Structure of the Mammalian Mitochondrial Ribosome Reveals an Expanded Functional Role for Its Component Proteins. Cell 2003, 115:97-108. 10.1016/S0092-8674(03)00762-1, 14532006.
60. Gutell RR, Lee JC, Cannone JJ. The accuracy of ribosomal RNA comparative structure models. Current Opinion in Structural Biology 2002, 12:301-310. 10.1016/S0959-440X(02)00339-1, 12127448.
61. Nedelcu A. Fragmented and scrambled mitochondrial ribosomal RNA coding regions among green algae: a model for their origin and evolution. Mol Biol Evol 1997, 14:506-517.
62. Turmel M, Boulanger J, Schnare MN, Gray MW, Lemieux C. Six group I introns and three internal transcribed spacers in the chloroplast large subunit ribosomal RNA gene of the green alga Chlamydomonas eugametos. J Mol Biol 1991, 218:293-311. 10.1016/0022-2836(91)90713-G, 1849178.
63. Colleaux L, Michel-Wolwertz M-R, Matagne RF, Dujon B. The apocytochrome b gene of Chlamydomonas smithii contains a mobile intron related to both Saccharomyces and Neurospora introns. Mol Gen Genom 1990, 223:288-296.
64. Schnare M, Heinonen T, Young P, Gray M. A discontinuous small subunit ribosomal RNA in Tetrahymena pyriformis mitochondria. J Biol Chem 1986, 261:5187-5193.
65. Burger G, Yan Y, Javadi P, Lang BF. Group I-intron trans-splicing and mRNA editing in the mitochondria of placozoan animals. Trends Gen 2009, 25:381-386.
66. Lavrov DV. Key transitions in animal evolution: a mitochondrial DNA perspective. Integr Comp Biol 2007, 47:734-743.
67. Mallatt J, Craig CW, Yoder MJ. Nearly complete rRNA genes assembled from across the metazoan animals: Effects of more taxa, a structure-based alignment, and paired-sites evolutionary models on phylogeny reconstruction. Mol Phyl Evol 2010, 55:1-17.
68. Gissi C, Iannelli F, Pesole G. Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity 2008, 101:301-320. 10.1038/hdy.2008.62, 18612321.
69. Rasmussen S. SEQtools - a program suite for sequence analysis. Book SEQtools - a program suite for sequence analysis (Editor ed.^eds.). City 2002,
70. Holley RW, Apgar J, Everett GA, Madison JT, Merrill SH, Penswick JR, Zamir A. Structure of a ribonucleic acid. Science 1965, 147:1462. 10.1126/science.147.3664.1462, 14263761.
71. Rajbhandary UL, Stuart A, Faulkner RD, Chang SH, Khorana HG. Nucleotide sequence studies on yeast phenylalanine sRNA. Cold Spring Harbor Symposia on Quantitative Biology 1966, 31:425.
72. Madison JT, Everett GA, Kung H. Nucleotide sequence of a yeast tyrosine transfer RNA. Science 1966, 153:531. 10.1126/science.153.3735.531, 5938777.
73. Zachau HG, Dutting D, Feldmann H, Melchers F, Karau W. SERINE SPECIFIC TRANSFER RIBONUCLEIC ACIDS .14. COMPARISON OF NUCLEOTIDE SEQUENCES AND SECONDARY STRUCTURE MODELS. Cold Spring Harbor Symposia on Quantitative Biology 1966, 31:417.
74. Levitt M. DETAILED MOLECULAR MODEL FOR TRANSFER RIBONUCLEIC ACID. Nature 1969, 224:759. 10.1038/224759a0, 5361649.
75. Kim SH, Suddath FL, Quigley GJ, Sussman JL, Wang AHJ, Seeman NC, Rich A. Three-dimensional tertiary structure of yeast phenylalanine transfer RNA. Science 1974, 185:435-440. 10.1126/science.185.4149.435, 4601792.
76. Robertus JD, Ladner JE, Finch JT, Rhodes D, Brown RS, Clark BFC, Klug A. Structure of yeast phenylalanine tRNA at 3Å resolution. Nature 1974, 250:546-551. 10.1038/250546a0, 4602655.
77. Fox GE, Woese CR. The architecture of 5S rRNA and its relation to function. J Molec Evol 1975, 6:61-76. 10.1007/BF01732674, 1185796.
78. Fox GE, Woese CR. 5S RNA secondary structure. Nature 1975, 256:505-507. 10.1038/256505a0, 808733.
79. Woese CR, Magrum LJ, Gupta R, Siegel RB, Stahl DA, Kop J, Crawford N, Brosius R, Gutell R, Hogan JJ, Noller HF. Secondary structure model for bacterial 16S ribosomal RNA: phylogenetic, enzymatic and chemical evidence. Nucl Acids Res 1980, 8:2275-2294. 10.1093/nar/8.10.2275, 324077, 6159576.
80. Noller HF, Kop J, Wheaton V, Brosius J, Gutell RR, Kopylov AM, Dohme F, Herr W, Stahl DA, Gupta R, Woese CR. Secondary structure model for 23S ribosomal RNA. Nucl Acids Res 1981, 9:6167-6189. 10.1093/nar/9.22.6167, 327592, 7031608.
81. Gutell RR, Power A, Hertz GZ, Putz EJ, Stormo GD. Identifying constraints on the higher-order structure of RNA: continued development and application of comparative sequence-analysis methods. Nucl Acids Res 1992, 20:5785-5795. 10.1093/nar/20.21.5785, 334417, 1454539.
82. Gautheret D, Damberger SH, Gutell RR. Identification of base-triples in RNA using comparative sequence-analysis. J Mol Biol 1995, 248:27-43. 10.1006/jmbi.1995.0200, 7537339.
83. Olsen G. Comparative analysis of nucleotide sequence data. Ph.D. dissertation 1983, University of Colorado, Health Sciences Center.
84. Chiu DKY, Kolodziejczak T. Inferring consensus structure from nucleic acid sequences. Computer Applications in the Biosciences 1991, 7:347-352.
85. Gardner PP, Giegerich R. A comprehensive comparison of comparative RNA structure prediction approaches. BMC Bioinformatics 2004, 30:5-140.
86. Krogh A, Brown M, Mian IS, Sjolander K, Haussler D. Hidden Markov Models in Computational Biology - Applications to protein modeling. J Mol Biol 1994, 235:1501-1531. 10.1006/jmbi.1994.1104, 8107089.
87. Eddy SR, Mitchison G, Durbin R. Maximum discrimination hidden Markov models of sequence consensus. Journal of Computational Biology 1995, 2:9-23. 10.1089/cmb.1995.2.9, 7497123.