Ribosomal RNA genes in Euglena gracilis mitochondrial DNA: fragmented genes in a seemingly fragmented genome

Molecular Genetics and Genomics

Volumn 285, Issue 1, 2011, Pages 19-31

  Spencer, David F ^a   Gray, Michael W ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Euglena gracilis; Euglenid Protozoa; Guide RNAs; Kinetoplastid Protozoa; Mitochondrial DNA; Ribosomal RNA

Indexed keywords

GUIDE RNA; MITOCHONDRIAL DNA;

ARTICLE; EUGLENA GRACILIS; EVOLUTION; GENE; GENETICS; GENOME; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; RNA GENE;

BASE SEQUENCE; BIOLOGICAL EVOLUTION; DNA, MITOCHONDRIAL; EUGLENA GRACILIS; GENES, PROTOZOAN; GENES, RRNA; GENOME, PROTOZOAN; MOLECULAR SEQUENCE DATA; RNA, GUIDE;

EID: 79952204281     PISSN: 16174615     EISSN: 16174623     Source Type: Journal    
DOI: 10.1007/s00438-010-0585-9     Document Type: Article

References (61)

1. Avadhani NG, Buetow DE (1972) Isolation of active polyribosomes from the cytoplasm, mitochondria and chloroplasts of Euglena gracilis. Biochem J 128:353–365
2. Bendich AJ (1993) Reaching for the ring: the study of mitochondrial genome structure. Curr Genet 24:279–290 DOI: 10.1007/BF00336777
3. Bendich AJ (1996) Structural analysis of mitochondrial DNA molecules from fungi and plants using moving pictures and pulsed-field gel electrophoresis. J Mol Biol 255:564–588 DOI: 10.1006/jmbi.1996.0048
4. Bendich AJ (2010) The end of the circle for yeast mitochondrial DNA. Mol Cell 39:831–832 DOI: 10.1016/j.molcel.2010.09.005
5. Boer PH, Gray MW (1988) Scrambled ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA. Cell 55:399–411 DOI: 10.1016/0092-8674(88)90026-8
6. Buetow DE (1989) The mitochondrion. In: Buetow DE (ed) The biology of Euglena, vol IV. Academic Press, San Diego, pp 247–314
7. Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes—anything goes. Trends Genet 19:709–716 DOI: 10.1016/j.tig.2003.10.012
8. Cavalier-Smith T (1993) Kingdom Protozoa and its 18 phyla. Microbiol Rev 57:953–994
9. Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev 73:203–266 DOI: 10.1017/S0006323198005167
10. Cook JR, Roxby R (1985) Physical properties of a plasmid-like DNA from Euglena gracilis. Biochim Biophys Acta 824:80–83
11. Covello PS, Gray MW (1991) Sequence analysis of wheat mitochondrial transcripts capped in vitro: definitive identification of transcription initiation sites. Curr Genet 20:245–251 DOI: 10.1007/BF00326239
12. Covello PS, Gray MW (1993) On the evolution of RNA editing. Trends Genet 9:265–268 DOI: 10.1016/0168-9525(93)90011-6
13. Cramer M, Myers J (1952) Growth and photosynthetic characteristics of Euglena gracilis. Arch Mikrobiol 17:384–402 DOI: 10.1007/BF00410835
14. Crouse EJ, Vandrey JP, Stutz E (1974) Hybridization studies with RNA and DNA isolated from Euglena gracilis chloroplasts and mitochondria. FEBS Lett 42:262–266 DOI: 10.1016/0014-5793(74)80741-6
15. Donis-Keller H (1979) Site specific enzymatic cleavage of RNA. Nucleic Acids Res 7:179–192 DOI: 10.1093/nar/7.1.179
16. Donis-Keller H, Maxam AM, Gilbert W (1977) Mapping adenines, guanines, and pyrimidines in RNA. Nucleic Acids Res 4:2527–2538 DOI: 10.1093/nar/4.8.2527
17. 4-methylcytidine. Nucleic Acids Res 5:4385–4397 DOI: 10.1093/nar/5.11.4385
18. Edelman M, Epstein HT, Schiff JA (1966) Isolation and characterization of DNA from the mitochondrial fraction of Euglena. J Mol Biol 17:463–469 DOI: 10.1016/S0022-2836(66)80156-0
19. Eperon IC, Janssen JWG, Hoeijmakers JHJ, Borst P (1983) The major transcripts of the kinetoplast DNA of Trypanosoma brucei are very small ribosomal RNAs. Nucleic Acids Res 11:105–125 DOI: 10.1093/nar/11.1.105
20. Estévez AM, Simpson L (1999) Uridine insertion/deletion RNA editing in trypanosome mitochondria—a review. Gene 240:247–260 DOI: 10.1016/S0378-1119(99)00437-0
21. Feagin JE, Werner E, Gardner MJ, Williamson DH, Wilson RJM (1992) Homologies between the continuous and fragmented rRNAs of the two Plasmodium falciparum extrachromosomal DNAs are limited to core sequences. Nucleic Acids Res 20:879–887 DOI: 10.1093/nar/20.4.879
22. Feagin JE, Mericle BL, Werner E, Morris M (1997) Identification of additional rRNA fragments encoded by the Plasmodium falciparum 6 kb element. Nucleic Acids Res 25:438–446 DOI: 10.1093/nar/25.2.438
23. Fonty G, Crouse EJ, Stutz E, Bernardi G (1975) The mitochondrial genome of Euglena gracilis. Eur J Biochem 54:367–372 DOI: 10.1111/j.1432-1033.1975.tb04147.x
24. Gillespie DE, Salazar NA, Rehkopf DH, Feagin JE (1999) The fragmented mitochondrial ribosomal RNAs of Plasmodium falciparaum have short A tails. Nucleic Acids Res 27:2416–2422 DOI: 10.1093/nar/27.11.2416
25. Gray MW (2001) Speculations on the origin and evolution of editing, chap. 8. In: Bass BL (ed) Frontiers in molecular biology 34 (RNA editing). Oxford University Press, Oxford, pp 160–184
26. Gray MW, Schnare MN (1990) Evolution of the modular structure of ribosomal RNA, chap. 52. In: Hill WE, Dahlberg A, Garrett R, Moore PB, Schlessinger D, Warner JR (eds) The ribosome: structure, function, and evolution. American Society for Microbiology, Washington, pp 589–597
27. Gray MW, Schnare MN (1996) Evolution of rRNA gene organization, chap. 3. In: Zimmermann RA, Dahlberg AE (eds) Ribosomal RNA: structure, evolution, processing, and function in protein biosynthesis. CRC Press, Boca Raton, pp 49–69
28. Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283:1476–1481 DOI: 10.1126/science.283.5407.1476
29. Gutell RR, Larsen NL, Woese CR (1994) Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiol Rev 58:10–26
30. Hajduk SL, Harris ME, Pollard VW (1993) RNA editing in kinetoplastid mitochondria. FASEB J 7:54–63
31. Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson AG, Roger AJ (2009) Phylogenetic analyses support the monophyly of Excavata and resolve relationships among eukaryotic “supergroups”. Proc Natl Acad Sci USA 106:3859–3864 DOI: 10.1073/pnas.0807880106
32. Hassur SM, Whitlock HW Jr (1974) UV shadowing—a new and convenient method for the location of ultraviolet-absorbing species in polyacrylamide gels. Anal Biochem 59:162–164 DOI: 10.1016/0003-2697(74)90020-7
33. Jackson CJ, Norman JE, Schnare MN, Gray MW, Keeling PJ, Waller RF (2007) Broad genomic and transcriptional analysis reveals a highly derived genome in dinoflagellate mitochondria. BMC Biol 5:41 DOI: 10.1186/1741-7007-5-41
34. Johnson DA, Gautsch JW, Sportsman JR, Elder JH (1984) Improved technique utilizing nonfat dry milk for analysis of proteins and nucleic acids transferred to nitrocellulose. Gene Anal Tech 1:3–8 DOI: 10.1016/0735-0651(84)90049-9
35. Kajander OA, Rovio AT, Majamaa K, Poulton J, Spelbrink JN, Holt IJ, Karhunen PJ, Jacobs HT (2000) Human mtDNA sublimons resemble rearranged mitochondrial genomes found in pathological states. Hum Mol Genet 9:2821–2835 DOI: 10.1093/hmg/9.19.2821
36. Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, Roger AJ, Gray MW (2005) The tree of eukaryotes. Trends Ecol Evol 20:670–676 DOI: 10.1016/j.tree.2005.09.005
37. Krawiec S, Eisenstadt JM (1970a) Ribonucleic acids from the mitochondria of bleached Euglena gracilis. I. Isolation of mitochondria and extraction of nucleic acids. Biochim Biophys Acta 217:120–131
38. Krawiec S, Eisenstadt JM (1970b) Ribonucleic acids from the mitochondria of bleached Euglena gracilis. II. Characterization of highly polymeric ribonucleic acids. Biochim Biophys Acta 217:132–141
39. Leaver CJ, Harmey MA (1976) Higher-plant mitochondrial ribosomes contain a 5S ribosomal ribonucleic acid component. Biochem J 157:275–277
40. Lis JT, Schleif R (1975) Size fractionation of double-stranded DNA by precipitation with polyethylene glycol. Nucleic Acids Res 2:383–389 DOI: 10.1093/nar/2.3.383
41. Lukeš J, Leander BS, Keeling PJ (2009) Cascades of convergent evolution: the corresponding evolutionary histories of euglenozoans and dinoflagellates. Proc Natl Acad Sci USA 106:9963–9970 DOI: 10.1073/pnas.0901004106
42. Manning JE, Wolstenholme DR, Ryan RS, Hunter JA, Richards OC (1971) Circular chloroplast DNA from Euglena gracilis. Proc Natl Acad Sci USA 68:1169–1173 DOI: 10.1073/pnas.68.6.1169
43. Marande W, Burger G (2007) Mitochondrial DNA as a genomic jigsaw puzzle. Science 318:415 DOI: 10.1126/science.1148033
44. Marande W, Lukeš J, Burger G (2005) Unique mitochondrial genome structure in diplonemids, the sister group of kinetoplastids. Eukaryot Cell 4:1137–1146 DOI: 10.1128/EC.4.6.1137-1146.2005
45. Maxam AM, Gilbert W (1977) A new method for sequencing DNA. Proc Natl Acad Sci USA 74:560–564 DOI: 10.1073/pnas.74.2.560
46. Nash EA, Nisbet RE, Barbrook AC, Howe CJ (2008) Dinoflagellates: a mitochondrial genome all at sea. Trends Genet 24:328–335 DOI: 10.1016/j.tig.2008.04.001
47. Nass MMK, Schori L, Ben-Shaul Y, Edelman M (1974) Size and configuration of mitochondrial DNA in Euglena gracilis. Biochim Biophys Acta 374:283–291
48. Peattie DA (1979) Direct chemical method for sequencing RNA. Proc Natl Acad Sci USA 76:1760–1764 DOI: 10.1073/pnas.76.4.1760
49. Ray DS, Hanawalt PC (1965) Satellite DNA components in Euglena gracilis cells lacking chloroplasts. J Mol Biol 11:760–768
50. Schnare MN, Gray MW (1990) Sixteen discrete RNA components in the cytoplasmic ribosome of Euglena gracilis. J Mol Biol 215:73–83 DOI: 10.1016/S0022-2836(05)80096-8
51. Sloof P, Van den Burg J, Voogd A, Benne R, Agostinelli M, Borst P, Gutell R, Noller H (1985) 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. Nucleic Acids Res 13:4171–4190 DOI: 10.1093/nar/13.11.4171
52. Small I, Suffolk R, Leaver CJ (1989) Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell 58:69–76 DOI: 10.1016/0092-8674(89)90403-0
53. Spencer DF, Gray MW, Schnare MN (1992) The isolation of wheat mitochondrial DNA and RNA. In: Linskens HF, Jackson JF (eds) Seed analysis. Modern methods of plant analysis, new series, vol 14, Springer, Berlin, pp 347–360
54. Stoltzfus A (1999) On the possibility of constructive neutral evolution. J Mol Evol 49:169–181 DOI: 10.1007/PL00006540
55. Stuart K, Feagin JE (1992) Mitochondrial DNA of kinetoplastids. Int Rev Cytol 141:65–88 DOI: 10.1016/S0074-7696(08)62063-X
56. Stuart KD, Schnaufer A, Ernst NL, Panigrahi AK (2005) Complex management: RNA editing in trypanosomes. Trends Biochem Sci 30:97–105 DOI: 10.1016/j.tibs.2004.12.006
57. Talen JL, Sanders JPM, Flavell RA (1974) Genetic complexity of mitochondrial DNA from Euglena gracilis. Biochim Biophys Acta 374:129–135
58. Tessier LH, van der Speck H, Gualberto JM, Grienenberger JM (1997) The cox1 gene from Euglena gracilis: a protist mitochondrial gene without introns and genetic code modifications. Curr Genet 31:208–213 DOI: 10.1007/s002940050197
59. Wahl GM, Stern M, Stark GR (1979) Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci USA 76:3683–3687 DOI: 10.1073/pnas.76.8.3683
60. Waller RF, Jackson CJ (2009) Dinoflagellate mitochondrial genomes: stretching the rules of molecular biology. Bioessays 31:237–245 DOI: 10.1002/bies.200800164
61. Yasuhira S, Simpson L (1997) Phylogenetic affinity of mitochondria of Euglena gracilis and kinetoplastids using cytochrome oxidase I and hsp60. J Mol Evol 44:341–347 DOI: 10.1007/PL00006152