Purification and characterization of organellar DNA polymerases in the red alga Cyanidioschyzon merolae

FEBS Journal

Volumn 275, Issue 11, 2008, Pages 2899-2918

  Moriyama, Takashi ^a   Terasawa, Kimihiro ^a   Fujiwara, Makoto ^a   Sato, Naoki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Cyanidioschyzon merolae; DNA polymerase; Organelle; POP; Replication

Indexed keywords

DNA DIRECTED DNA POLYMERASE BETA; GREEN FLUORESCENT PROTEIN; POL PROTEIN; PROTEIN POLA; PROTEIN POLB;

ARTICLE; CONTROLLED STUDY; CYANIDIOSCHYZON MEROLAE; DNA DETERMINATION; DNA PURIFICATION; DNA SYNTHESIS; ENZYME ACTIVITY; ESCHERICHIA COLI; IMMUNOBLOTTING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSYNTHESIS; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RED ALGA;

ALGAE, RED; ALGAL PROTEINS; AMINO ACID SEQUENCE; DNA POLYMERASE II; GENE EXPRESSION REGULATION, PLANT; GREEN FLUORESCENT PROTEINS; MITOCHONDRIA; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASTIDS; RECOMBINANT FUSION PROTEINS; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TEMPERATURE;

ANIMALIA; ARABIDOPSIS; BACTERIA (MICROORGANISMS); CYANIDIOSCHYZON MEROLAE; ESCHERICHIA COLI; EUKARYOTA; NICOTIANA TABACUM; RHODOPHYTA;

EID: 43549098066     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06426.x     Document Type: Article

References (60)

1. Margulis L Bermudes D (1985) Symbiosis as a mechanism of evolution: status of cell symbiosis theory. Symbiosis 1, 101 124.
2. Wang Y, Farr CL Kagni LS (1997) Accessory subunit of mitochondrial DNA polymerase from Drosophila embryos. Cloning, molecular analysis, and association in the native enzyme. J Biol Chem 272, 13640 13646.
3. Lecrenier N Foury F (2000) New features of mitochondrial DNA replication system in yeast and man. Gene 246, 37 48.
4. Kaguni LS (2004) DNA polymerase gamma, the mitochondrial replicase. Annu Rev Biochem 73, 293 320.
5. Bailey JC, Heinhorst S Cannon GC (1995) Accuracy of deoxynucleotide incorporation by soybean chloroplast DNA polymerases is independent of the presence of a 3′ to 5′ exonuclease. Plant Physiol 107, 1277 1284.
6. Heinhorst S, Cannon GC Weissbach A (1990) Chloroplast and mitochondrial DNA polymerases from cultured soybean cells. Plant Physiol 92, 939 945.
7. Keim CA Mosbaugh DW (1991) Identification and characterization of a 3′ to 5′ exonuclease associated with spinach chloroplast DNA polymerase. Biochemistry 30, 11109 11118.
8. Keller SJ, Biedenbach SA Meyer RR (1973) Partial purification of a chloroplast DNA polymerase from Euglena gracilis. Biochem Biophys Res Commun 50, 620 628.
9. McKown RL Tewari KK (1984) Purification and properties of a pea chloroplast DNA polymerase. Proc Natl Acad Sci USA 81, 2354 2358.
10. Sala F, Amileni AR, Parisi B Spadari S (1980) A gamma-like DNA polymerase in spinach chloroplasts. Eur J Biochem 112, 211 217.
11. Wang ZF, Yang J, Nie ZQ Wu M (1991) Purification and characterization of a gamma-like DNA polymerase from Chlamydomonas reinhardtii. Biochemistry 30, 1127 1131.
12. Castroviejo M, Tharaud D, Tarrago-Litrak L Litvak S (1979) Multiple deoxyribonucleic acid polymerases from quiescent wheat embryos. Purification and characterization of three enzymes from the soluble cytoplasm and one from purified mitochondria. Biochem J 181, 183 191.
13. Christophe L, Tarrago-Litvak L, Castroviejo M Litvak S (1981) Mitochondrial DNA polymerase from wheat embryos. Plant Sci Lett 21, 181 192.
14. Fukasawa H Chou MY (1980) Mitochondrial DNA polymerase from cauliflower inflorescence. Jpn J Genet 55, 441 445.
15. Meißner K, Heinhorst S, Cannon GC Börner T (1993) Purification and characterization of a gamma-like DNA polymerase from Chenopodium album L. Nucleic Acids Res 21, 4893 4899.
16. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796 815.
17. Cavalier-Smith T (2006) Cell evolution and earth history: stasis and revolution. Phil Trans R Soc Lond Biol 361, 969 1006.
18. Sakai A (2001) In vitro transcription/DNA synthesis using isolated organelle-nuclei: application to the analysis of the mechanisms that regulate organelle genome function. J Plant Res 114, 199 211.
19. Sakai A, Suzuki T, Nagata N, Sasaki N, Miyazawa Y, Saito C, Inada N, Nishimura Y Kuroiwa T (1999) Comparative analysis of DNA synthesis activity in plastid-nuclei and mitochondrial-nuclei simultaneously isolated from cultured tobacco cells. Plant Sci 140, 9 19.
20. Sakai A, Takano H Kuroiwa T (2004) Organelle nuclei in higher plants: structure, composition, function, and evolution. Int Rev Cytol 238, 59 118.
21. Christensen AC, Lyznik A, Mohammed S, Elowsky CG, Elo A, Yule R Mackenzie SA (2005) Dual-domain, dual-targeting organellar protein presequences in Arabidopsis can use non-AUG start codons. Plant Cell 17, 2805 2816.
22. Kimura S, Uchiyama Y, Kasai N, Namekawa S, Saotome A, Ueda T, Ando T, Ishibashi T, Oshige M, Furukawa T et al. (2002) A novel DNA polymerase homologous to Escherichia coli DNA polymerase I from a higher plant, rice (Oryza sativa L.). Nucleic Acids Res 30, 1585 1592.
23. Mori Y, Kimura S, Saotome A, Kasai N, Sakaguchi N, Uchiyama Y, Ishibashi T, Yamamoto T, Chiku H Sakaguchi K (2005) Plastid DNA polymerases from higher plants, Arabidopsis thaliana. Biochem Biophys Res Commun 334, 43 50.
24. Ono Y, Sakai A, Takechi K, Takio S, Takusagawa M Takano H (2007) NtPolI-like1 and NtPolI-like2, bacterial DNA polymerase I homologues isolated from BY-2 cultured tobacco cells, encode DNA polymerases engaged in DNA replication in both plastids and mitochondria. Plant Cell Physiol 48, 1679 1692.
25. Sato N, Terasawa K, Miyajima K Kabeya Y (2003) Organization, developmental dynamics, and evolution of plastid nucleoids. Int Rev Cytol 232, 217 262.
26. Matsuzaki M, Misumi O, Shin-i T, Maruyama S, Takahara M, Miyagishima S, Mori T, Nishida K, Yagisawa F, Nishida K et al. (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428, 653 657.
27. Nozaki H, Takano H, Misumi O, Terasawa K, Matsuzaki M, Maruyama S, Nishida K, Yagisawa F, Yoshida Y, Fujiwara T et al. (2007) A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol 5, 28.
28. Grossman AR, Harris EE, Hauser C, Lefebvre PA, Martinez D, Rokhsar D, Sharager J, Silflow CW, Stern D Zang Z (2003) Chlamydomonas reinhardtii at the crossroads of genomics. Eukaryot Cell 2, 1137 1150.
29. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M et al. (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306, 79 86.
30. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436, 793 800.
31. Takeuchi R, Kimura S, Saotome A Sakaguchi K (2007) Biochemical properties of a plastidial DNA polymerase of rice. Plant Mol Biol 64, 601 611.
32. Filée J, Forterre P, Sen-Lin T Laurent J (2002) Evolution of DNA polymerase families: evidence for multiple gene exchange between cellular and viral proteins. J Mol Evol 54, 763 773.
33. Inagaki S, Suzuki T, Ohto M, Urawa H, Horiuchi T, Nakamura K Morikami A (2006) Arabidopsis TEBICHI, with helicase and DNA polymerase domains, is required for regulated cell division and differentiation in meristems. Plant Cell 18, 879 892.
34. Chiu W, Niwa Y, Zeng W, Hirano T, Kobayashi H Sheen J (1996) Engineered GFP as a vital reporter in plants. Curr Biol 6, 325 330.
35. Nakazono M, Imamura T, Tsutsumi N, Sasaki T Hirai A (2000) Characterization of two cDNA clones encoding isozymes of the F(1)F(0)-ATPase inhibitor protein of rice mitochondria. Planta 210, 188 194.
36. Schnurr JA, Shockey JM, de Boer GJ Browse JA (2002) Fatty acid export from the chloroplast. Molecular characterization of a major plastidial acyl-coenzyme A synthetase from Arabidopsis. Plant Physiol 129, 1700 1709.
37. Sato N Moriyama T (2007) Genomic and biochemical analysis of lipid biosynthesis in the unicellular rhodophyte Cyanidioschyzon merolae: lack of a plastidic desaturation pathway results in the coupled pathway of galactolipid synthesis. Eukaryot Cell 6, 1006 1017.
38. Holmes AM (1981) Studies on the inhibition of highly purified calf thymus 8S and 7.3S DNA polymerase alpha by aphidicolin. Nucleic Acids Res 9, 161 168.
39. Weiser T, Gassmann M, Thömmes P, Ferrari E, Hafkemeyer P Hübscher U (1991) Biochemical and functional comparison of DNA polymerases alpha, delta, and epsilon from calf thymus. J Biol Chem 266, 10420 10428.
40. Chavalitshewinkoon-Petmitr P, Chawprom S, Naesens L, Balzarini J Wilairat P (2000) Partial purification and characterization of mitochondrial DNA polymerase from Plasmodium falciparum. Parasitol Int 49, 279 288.
41. Shiraki K, Okuno T, Yamanishi K Takahashi M (1989) Phosphonoacetic acid inhibits replication of human herpesvirus-6. Antiviral Res 12, 311 318.
42. Leinbach SS, Reno JM, Lee LF, Isbell AF Boezi JA (1976) Mechanism of phosphonoacetate inhibition of herpesvirus-induced DNA polymerase. Biochemistry 15, 426 430.
43. Kornberg A Baker TA (1992) DNA Replication, 2nd edn. W.H. Freeman and Company, New York, NY.
44. Astatke M, Grindley NDF Joyce CM (1998) How E. coli DNA polymerase I (Klenow fragment) distinguishes between deoxy- and dideoxynucleotides. J Mol Biol 278, 147 165.
45. Korhonen JA, Gaspari M Falkenberg M (2003) TWINKLE has 5′→3′ DNA helicase activity and is specifically stimulated by mitochondrial single-stranded DNA-binding protein. J Biol Chem 278, 48627 48632.
46. Seow F, Sato S, Janssen CS, Riehle MO, Mukhopadhyay A, Phillips RS, Wilson RJ Barrett MP (2005) The plastidic DNA replication enzyme complex of Plasmodium falciparum. Mol Biochem Parasitol 141, 145 153.
47. Toda K, Takano H, Miyagishima S, Kuroiwa H Kuroiwa T (1998) Characterization of a chloroplast isoform of serine acetyltransferase from the thermo-acidiphilic red alga Cyanidioschyzon merolae. Biochim Biophys Acta 1403, 72 84.
48. Allen MB (1959) Studies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch Microbiol 32, 270 277.
49. Minoda A, Sakagami R, Yagisawa F, Kuroiwa T Tanaka K (2004) Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol 45, 667 671.
50. Sato N, Ishikawa M, Fujiwara M Sonoike K (2005) Mass identification of chloroplast proteins of endosymbiont origin by phylogenetic profiling based on organism-optimized homologous protein groups. Genome Inform 16, 56 68.
51. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792 1797.
52. Sato N (2000) SISEQ: manipulation of multiple sequence and large database files for common platforms. Bioinformatics 16, 180 181.
53. Jobb G, von Haeseler A Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4, 18.
54. Tamura K, Dudley J, Nei M Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24, 1596 1599.
55. Finn RD, Mistry J, Schuster-Böckler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R et al. (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34, D247 D251.
56. Kobayashi T, Takahara M, Miyagishima SY, Kuroiwa H, Sasaki N, Ohta N, Matsuzaki M Kuroiwa T (2002) Detection and localization of a chloroplast-encoded HU-like protein that organizes chloroplast nucleoids. Plant Cell 14, 1579 1589.
57. Sekine K, Hase T Sato N (2002) Reversible DNA compaction by sulfite reductase regulates transcriptional activity of chloroplast nucleoids. J Biol Chem 277, 24399 24404.
58. Sato N, Albrieux C, Joyard J, Douce R Kuroiwa T (1993) Detection and characterization of a plastid envelope DNA-binding protein which may anchor plastid nucleoids. EMBO J 12, 555 561.
59. Kabeya Y Sato N (2005) Unique translation initiation at the second AUG codon determines mitochondrial localization of the phage-type RNA polymerases in the moss Physcomitrella patens. Plant Physiol 138, 369 382.
60. Pavlov YI, Shcherbakova PV Kunkel TA (2001) In vivo consequences of putative active site mutations in yeast DNA polymerases alpha, epsilon, delta, and zeta. Genetics 159, 47 64.