Dokument

Zusammenfassung:
Die vorliegende Arbeit beschäftigt sich mit der Evolution der plastidären RNA-Edierung und dem evolutionären Hintergrund der komplexen Plastide in Peridinin-haltigen Dinoflagellaten. Das Plastidengenom des Lebermooses P. endiviifolia wurde vollständig sequenziert (120554 bp) und C zu U Edierung konnte an 54 Stellen nachgewiesen werden. Aufgrund der relativ geringen Anzahl an Edierungen stützt dies einen sekundären Verlust der RNA-Edierung in dem Lebermoos M. polymorpha. Weiterhin sind die Edierungsstellen in P. endiviifolia auf einen Sequenzkontext mit geringerer Mutationsrate konzentriert. Dadurch erfüllen sie die Kriterien für das Modell der Entstehung der RNA-Edierung nach Tillich (Tillich et al., 2006). Ein RNA-Edierungssystem entwickelte sich um Mutationen der DNA auf RNA Ebene zu kurieren. Rückmutationen, teilweise begünstigt durch Zeiten dynamischer Sequenzevolution, führten zu den heute beobachtbaren Editotypen bzw. zum Verlust der Edierung in M. polymorpha. Außerdem wurde die plastidäre Genomreduktion der Peridinin-haltigen Dinoflagellaten untersucht. Mittels Transposonmutagenese konnten minicircles aus A. carterae isoliert werden, die unter anderem eine Stammspezifität der core-Region verdeutlichen. Die minicircles zeigen eine ausgesprochene Varianz und ihre möglichen Funktionen, unter anderem als mögliches Gen-shuttle, werden diskutiert. Im Zuge der Betrachtung des plastidären Proteinimports zeigte sich, dass die Transitpeptide Nukleus-codierter Plastidenproteine der Peridinin-haltigen Dinoflagellaten und Chromisten, entgegen bisherigen in vitro Daten, keinen Import in die primäre Plastide von Landpflanzen vermitteln können und die sogenannten Klasse I Transitpeptide weitere potentielle Zielsteuerungsinformationen enthalten (TPL2), welche die nötigen Informationen für eine Assoziation mit einer primären Plastide tragen. Proteine dieser Klasse weisen häufig eine größere Homologie zu ‚grünen Genen‘ auf, was auf einen Ursprung aus einem potentiellen horizontalen Gentransfer schließen lässt. Zusätzlich konnte durch elektronenmikroskopische Studien bestätigt werden, dass Proteine mit Klasse I Transitpeptid nicht sensitiv für eine Inhibition mit Brefeldin A sind und somit einen vom Golgi-Apparat unabhängigen Transportweg in die komplexe Plastide zu nutzen scheinen. Diese Klasse zeigt also Besonderheiten im plastidären Proteinimport, womöglich resultierend aus einem abweichenden evolutionären Ursprung.

Bibliographie / References

1. Bendtsen, J.D., Nielsen, H., von Heijne, G., & Brunak, S. (2004). Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340, 783-795.
2. Allen, C.A., Allen, J.F., & Puthiyaveetil, S. (2005). Energy transduction anchors genes in organelles. BioEssays 27, 426-435.
3. Allen, J.F. (2003). Why chloroplasts and mitochondria contain genomes. Comp Funct Genomics 4, 31- 36.
4. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., & Lipman, D.J. (1990). Basic local alignment search tool. J Mol Biol 215, 403-410.
5. Bhaya, D., & Grossman, A. (1991). Targeting proteins to diatom plastids involves transport through an endoplasmic reticulum. Mol Gen Genet 229, 400-404.
6. Schnepf, E., & Deichgräber, G. (1984). "Myzocytosis", a kind of endocytosis with implications to compartmentation in endosymbiosis. Naturwissenschaften 71, 218-219.
7. Morton, B.R., Oberholzer, V.M., & Clegg, M.T. (1997). The influence of specific neighboring bases on substitution bias in noncoding regions of the plant chloroplast genome. J Mol Evol 45, 227- 231.
8. Rüdinger, M., Volkmar, U., Lenz, H., Groth-Malonek, M., & Knoop, V. (2012). Nuclear DYW-Type PPR gene families diversify with increasing RNA editing frequencies in liverwort and moss mitochondria. J Mol Evol 74, 37-51.
9. Braukmann, T.W., Kuzmina, M., & Stefanovic, S. (2009). Loss of all plastid ndh genes in Gnetales and conifers: Extent and evolutionary significance for the seed plant phylogeny. Curr Genet 55, 323-337.
10. Wang, B., Xue, J., Li, L., Liu, Y., & Qiu, Y.L. (2009). The complete mitochondrial genome sequence of the liverwort Pleurozia purpurea reveals extremely conservative mitochondrial genome evolution in liverworts. Curr Genet 55, 601-609.
11. Rüdinger, M., Funk, H.T., Rensing, S.A., Maier, U.G., & Knoop, V. (2009). RNA editing: Only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal. Mol Genet Genomics 281, 473-481.
12. Smith, D.R. (2009). Unparalleled GC content in the plastid DNA of Selaginella. Plant Mol Biol 71, 627- 639.
13. Benne, R., Van den Burg, J., Brakenhoff, J.P., Sloof, P., Van Boom, J.H., & Tromp, M.C. (1986). Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46, 819-826.
14. Spector, D.L. (1984). Dinoflagellate nuclei. In Dinoflagellates, D.L. Spector, Hrsg (New York: Academic Press), pp. 107-147.
15. Archibald, J.M. (2009). The puzzle of plastid evolution. Curr Biol 19, R81-88.
16. Chan, C.X., Yang, E.C., Banerjee, T., Yoon, H.S., Martone, P.T., Estevez, J.M., & Bhattacharya, D. (2011). Red and green algal monophyly and extensive gene sharing found in a rich repertoire of red algal genes. Curr Biol 21, 328-333.
17. Broughton, M.J., Howe, C.J., & Hiller, R.G. (2006). Distinctive organization of genes for light- harvesting proteins in the cryptophyte alga Rhodomonas. Gene 369, 72-79.
18. Rudhe, C., Clifton, R., Chew, O., Zemam, K., Richter, S., Lamppa, G., Whelan, J., & Glaser, E. (2004). Processing of the dual targeted precursor protein of glutathione reductase in mitochondria and chloroplasts. J Mol Biol 343, 639-647.
19. Wiese, A., Groner, F., Sonnewald, U., Deppner, H., Lerchl, J., Hebbeker, U., Flugge, U., & Weber, A. (1999). Spinach hexokinase I is located in the outer envelope membrane of plastids. FEBS Lett 461, 13-18.
20. Miyata, Y., Sugiura, C., Kobayashi, Y., Hagiwara, M., & Sugita, M. (2002). Chloroplast ribosomal S14 protein transcript is edited to create a translation initiation codon in the moss Physcomitrella patens. Biochim Biophys Acta 1576, 346-349.
21. Bouligand, Y., & Norris, V. (2001). Chromosome separation and segregation in dinoflagellates and bacteria may depend on liquid crystalline states. Biochimie 83, 187-192.
22. Schnell, D.J., Blobel, G., Keegstra, K., Kessler, F., Ko, K., & Soll, J. (1997). A consensus nomenclature for the protein-import components of the chloroplast envelope. Trends Cell Biol 7, 303-304.
23. Sommer, M.S., Daum, B., Gross, L.E., Weis, B.L., Mirus, O., Abram, L., Maier, U.G., Kuhlbrandt, W., & Schleiff, E. (2011). Chloroplast Omp85 proteins change orientation during evolution. Proc Natl Acad Sci U S A 108, 13841-13846.
24. Wakasugi, T., Hirose, T., Horihata, M., Tsudzuki, T., Kossel, H., & Sugiura, M. (1996). Creation of a novel protein-coding region at the RNA level in black pine chloroplasts: the pattern of RNA editing in the gymnosperm chloroplast is different from that in angiosperms. Proc Natl Acad Sci U S A 93, 8766-8770.
25. Bölter, B., Soll, J., Schulz, A., Hinnah, S., & Wagner, R. (1998). Origin of a chloroplast protein importer. Proc Natl Acad Sci U S A 95, 15831-15836.
26. Reumann, S., Davila-Aponte, J., & Keegstra, K. (1999). The evolutionary origin of the protein- translocating channel of chloroplastic envelope membranes: Identification of a cyanobacterial homolog. Proc Natl Acad Sci U S A 96, 784-789.
27. Bullmann, L., Haarmann, R., Mirus, O., Bredemeier, R., Hempel, F., Maier, U.G., & Schleiff, E. (2010). Filling the gap, evolutionarily conserved Omp85 in plastids of chromalveolates. J Biol Chem 285, 6848-6856.
28. Ahting, U., Waizenegger, T., Neupert, W., & Rapaport, D. (2005). Signal-anchored proteins follow a unique insertion pathway into the outer membrane of mitochondria. J Biol Chem 280, 48-53.
29. Balsera, M., Goetze, T.A., Kovács-Bogdán, E., Schürmann, P., Wagner, R., Buchanan, B.B., Soll, J., & Bölter, B. (2009). Characterization of Tic110, a channel-forming protein at the inner envelope membrane of chloroplasts, unveils a response to Ca2+ and a stromal regulatory disulfide bridge. J Biol Chem 284, 2603-2616.
30. Akita, M., Nielsen, E., & Keegstra, K. (1997). Identification of protein transport complexes in the chloroplastic envelope membranes via chemical cross-linking. J Cell Biol 136, 983-994.
31. Rapaport, D., & Neupert, W. (1999). Biogenesis of Tom40, core component of the TOM complex of mitochondria. J Cell Biol 146, 321-331.
32. Chou, M.L., Chu, C.C., Chen, L.J., Akita, M., & Li, H.M. (2006). Stimulation of transit-peptide release and ATP hydrolysis by a cochaperone during protein import into chloroplasts. J Cell Biol 175, 893-900.
33. Schleiff, E., Tien, R., Salomon, M., & Soll, J. (2001). Lipid composition of outer leaflet of chloroplast outer envelope determines topology of OEP7. Mol Biol Cell 12, 4090-4102.
34. Vacula, R., Steiner, J.M., Krajcovic, J., Ebringer, L., & Loffelhardt, W. (1999). Nucleus-encoded precursors to thylakoid lumen proteins of Euglena gracilis possess tripartite presequences. DNA Res 6, 45-49.
35. Schmitz-Linneweber, C., Tillich, M., Herrmann, R.G., & Maier, R.M. (2001). Heterologous, splicing- dependent RNA editing in chloroplasts: Allotetraploidy provides trans-factors. EMBO J 20, 4874-4883.
36. Woehle, C., Dagan, T., Martin, W.F., & Gould, S.B. (2011). Red and problematic green phylogenetic signals among thousands of nuclear genes from the photosynthetic and apicomplexa-related Chromera velia. Genome Biol Evo 3, 1220-1230.
37. Albiniak, A.M., Baglieri, J., & Robinson, C. (2012). Targeting of lumenal proteins across the thylakoid membrane. J Exp Bot 63, 1689-1698.
38. Ueda, M., Fujimoto, M., Arimura, S., Tsutsumi, N., & Kadowaki, K. (2006). Evidence for transit peptide acquisition through duplication and subsequent frameshift mutation of a preexisting protein gene in rice. Mol Biol Evol 23, 2405-2412.
39. Nash, E.A., Barbrook, A.C., Edwards-stuart, R.K., Bernhardt, K., Howe, C.J., & Nisbet, R.E.R. (2007). Organization of the mitochondrial genome in the dinoflagellate Amphidinium carterae. Biosystems 24, 1528-1536.
40. Wickett, N.J., Zhang, Y., Hansen, S.K., Roper, J.M., Kuehl, J.V., Plock, S.A., Wolf, P.G., DePamphilis, C.W., Boore, J.L., & Goffinet, B. (2008). Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Mol Biol Evol 25, 393-401.
41. Rüdinger, M., Polsakiewicz, M., & Knoop, V. (2008). Organellar RNA editing and plant-specific extensions of pentatricopeptide repeat proteins in jungermanniid but not in marchantiid liverworts. Mol Biol Evol 25, 1405-1414.
42. Moszczynski, K., Mackiewicz, P., & Bodyl, A. (2012). Evidence for horizontal gene transfer from bacteroidetes bacteria to dinoflagellate minicircles. Mol Biol Evol 29, 887-892.
43. Bernsel, A., Viklund, H., Hennerdal, A., & Elofsson, A. (2009). TOPCONS: Consensus prediction of membrane protein topology. Nucleic Acids Res 37, W465-468.
44. Zhang, Z., Cavalier-Smith, T., & Green, B.R. (2001). A family of selfish minicircular chromosomes with jumbled chloroplast gene fragments from a dinoflagellate. Mol Biol Evol 18, 1558-1565.
45. Zeng, W.H., Liao, S.C., & Chang, C.C. (2007). Identification of RNA editing sites in chloroplast transcripts of Phalaenopsis aphrodite and comparative analysis with those of other seed plants. Plant Cell Physiol 48, 362-368.
46. Nanjo, Y., Oka, H., Ikarashi, N., Kaneko, K., Kitajima, A., Mitsui, T., Munoz, F.J., Rodriguez-Lopez, M., Baroja-Fernandez, E., & Pozueta-Romero, J. (2006). Rice plastidial N-glycosylated nucleotide pyrophosphatase/phosphodiesterase is transported from the ER-golgi to the chloroplast through the secretory pathway. Plant Cell 18, 2582-2592.
47. Schuster, W., Hiesel, R., Wissinger, B., & Brennicke, A. (1990). RNA editing in the cytochrome b locus of the higher plant Oenothera berteriana includes a U-to-C transition. Mol Cell Biol 10, 2428- 2431.
48. Nassoury, N., Cappadocia, M., & Morse, D. (2003). Plastid ultrastructure defines the protein import pathway in dinoflagellates. J Cell Sci 116, 2867-2874.
49. Sugita, M., Miyata, Y., Maruyama, K., Sugiura, C., Arikawa, T., & Higuchi, M. (2006). Extensive RNA editing in transcripts from the psbB operon and rpoA gene of plastids from the enigmatic moss Takakia lepidozioides. Biosci Biotechnol Biochem 70, 2268-2274.
50. Weber, A.P., Linka, M., & Bhattacharya, D. (2006). Single, ancient origin of a plastid metabolite translocator family in plantae from an endomembrane-derived ancestor. Eukaryot Cell 5, 609-612.
51. Chow, M., Yan, K., Bennett, M., & Wong, J. (2010). Birefringence and DNA condensation of liquid crystalline chromosomes. Eukaryot Cell 9, 1577-1587.
52. Becker, T., Jelic, M., Vojta, A., Radunz, A., Soll, J., & Schleiff, E. (2004). Preprotein recognition by the TOC complex. EMBO J 23, 520-530.
53. Adl, S.M., Simpson, A.G., Farmer, M.A., Andersen, R.A., Anderson, O.R., Barta, J.R., Bowser, S.S., Brugerolle, G., Fensome, R.A., Fredericq, S., James, T.Y., Karpov, S., Kugrens, P., Krug, J., Lane, C.E., Lewis, L.A., Lodge, J., Lynn, D.H., Mann, D.G., McCourt, R.M., Mendoza, L., Moestrup, O., Mozley-Standridge, S.E., Nerad, T.A., Shearer, C.A., Smirnov, A.V., Spiegel, F.W., & Taylor, M.F. (2005). The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52, 399-451.
54. Moore, R.B., Ferguson, K.M., Loh, W.K., Hoegh-Guldberg, O., & Carter, D.A. (2003). Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium. Int J Syst Evol Microbiol 53, 1725-1734.
55. Bachvaroff, T.R., & Place, A.R. (2008). From stop to start: Tandem gene arrangement, copy number and trans-splicing sites in the dinoflagellate Amphidinium carterae. PLoS One 3, e2929.
56. Morton, B.R. (2003). The role of context-dependent mutations in generating compositional and codon usage bias in grass chloroplast DNA. J Mol Evol 56, 616-629.
57. Wang, Y., Joly, S., & Morse, D. (2008). Phylogeny of dinoflagellate plastid genes recently transferred to the nucleus supports a common ancestry with red algal plastid genes. J Mol Evol 66, 175- 184.
58. Barbrook, A.C., & Howe, C.J. (2000). Minicircular plastid DNA in the dinoflagellate Amphidinium operculatum. Mol Gen Genet 263, 152-158.
59. Barbrook, A.C., Dorrell, R.G., Burrows, J., Plenderleith, L.J., Nisbet, R.E., & Howe, C.J. (2012). Polyuridylylation and processing of transcripts from multiple gene minicircles in chloroplasts of the dinoflagellate Amphidinium carterae. Plant Mol Biol 79, 347-357.
60. Richter, S., & Lamppa, G.K. (1998). A chloroplast processing enzyme functions as the general stromal processing peptidase. Proc Natl Acad Sci U S A 95, 7463-7468.
61. Spork, S., Hiss, J.A., Mandel, K., Sommer, M., Kooij, T.W., Chu, T., Schneider, G., Maier, U.G., & Przyborski, J.M. (2009). An unusual ERAD-like complex is targeted to the apicoplast of Plasmodium falciparum. Eukaryot Cell 8, 1134-1145.
62. Moore, R.B., Oborník, M., Janouškovec, J., Chrudimský, T., Vancová, M., Green, D.H., Wright, S.W., Davies, N.W., Bolch, C.J.S., Heimann, K., Šlapeta, J., Hoegh-Guldberg, O., Logsdon, J.M., & Carter, D.A. (2008). A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451, 959-963.
63. Schaffner, W., & Weissmann, C. (1973). A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal Biochem 56, 502-514.
64. Schimper, A.F.W. (1883). Über die Entwicklung der Chlorophyllkörner und Farbkörper. Botanische Zeitung 41, 106-114.
65. Nebenfuhr, A., Ritzenthaler, C., & Robinson, D. (2002). Brefeldin A: Deciphering an enigmatic inhibitor of secretion. Plant Physiol 130, 1102-1108.
66. Nassoury, N., Wang, Y., & Morse, D. (2005). Brefeldin A inhibits circadian remodeling of chloroplast structure in the dinoflagellate Gonyaulax. Traffic 6, 548-561.
67. Schleiff, E., Motzkus, M., & Soll, J. (2002). Chloroplast protein import inhibition by a soluble factor from wheat germ lysate. Plant Mol Biol 50, 177-185.
68. Sugiura, C., Kobayashi, Y., Aoki, S., Sugita, C., & Sugita, M. (2003). Complete chloroplast DNA sequence of the moss Physcomitrella patens: Evidence for the loss and relocation of rpoA from the chloroplast to the nucleus. Nucleic Acids Res 31, 5324-5331.
69. Wilson, R.J., Denny, P.W., Preiser, P.R., Rangachari, K., Roberts, K., Roy, A., Whyte, A., Strath, M., Moore, D.J., Moore, P.W., & Williamson, D.H. (1996). Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol 261, 155-172.
70. Sato, S., Nakamura, Y., Kaneko, T., Asamizu, E., & Tabata, S. (1999). Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res 6, 283-290.
71. Schnepf, E., & Elbrächter, M. (1999). Dinophyte chloroplasts and phylogeny -A review. Grana 38, 81- 97.
72. Bozarth, A., Grosche, C., Gould, S.B., Lieske, S., Weber, C., & Zauner, S. (2012). Heterologous in vivo plastid import using dinoflagellate targeting signals. J Eukaryot Microbio. Eingereicht.
73. Wyatt, R., Odrzykoski, I., & Cronberg, N. (2005). High levels of genetic variation in the haploid leafy liverwort Porella platyphylla from the southeastern United States. J Bryol 27, 247-252.
74. Wolf, P.G., Rowe, C.A., & Hasebe, M. (2004). High levels of RNA editing in a vascular plant chloroplast genome: Analysis of transcripts from the fern Adiantum capillus-veneris. Gene 339, 89 -97.
75. Sláviková, S., Vacula, R., Fang, Z., Ehara, T., Osafune, T., & Schwartzbach, S.D. (2005). Homologous and heterologous reconstitution of Golgi to chloroplast transport and protein import into the complex chloroplasts of Euglena. J Cell Sci 118, 1651-1661.
76. Tu, S.L., Chen, L.J., Smith, M.D., Su, Y.S., Schnell, D.J., & Li, H.M. (2004). Import pathways of chloroplast interior proteins and the outer-membrane protein OEP14 converge at Toc75. Plant Cell 16, 2078-2088.
77. Bozarth, A. (2010). Investigation of dinoflagellate plastid protein transport using heterologous and homologous in vivo systems. Dissertation. Am Fachbereich Biologie. Philipps-Universität Marburg.
78. Schnell, D.J., Kessler, F., & Blobel, G. (1994). Isolation of components of the chloroplast protein import machinery. Science 266, 1007-1012.
79. Sambrook, J., Fritsch, E.F., & Maniatis, T. (1989). Molecular cloning. A laboratory manual. (New York: Cold Spring Habor Laboratory Press).
80. Stirewalt, V., Michalowski, C., Löffelhardt, W., Bohnert, H., & Bryant, D. (1995). Nucleotide sequence of the cyanelle genome from Cyanophora paradoxa. Plant Mol Biol Report 13, 327- 332.
81. Cavalier-Smith, T. (2004). Only six kingdoms of life. Proc Biol Sci 271, 1251-1262.
82. Chateigner-Boutin, A.-L., & Small, I. (2011). Organellar RNA editing. WIREs RNA 2, 493-506.
83. Barbrook, A.C., Symington, H., Nisbet, R.E., Larkum, A., & Howe, C.J. (2001). Organisation and expression of the plastid genome of the dinoflagellate Amphidinium operculatum. Molecular genetics and genomics : MGG 266, 632-638.
84. von Heijne, G. (1983). Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem 133, 17-21.
85. Steinhauser, S., Beckert, S., Capesius, I., Malek, O., & Knoop, V. (1999). Plant mitochondrial RNA editing. J Mol Evol, 303-312.
86. Steiner, J.M., & Loffelhardt, W. (2002). Protein import into cyanelles. Trends Plant Sci 7, 72-77.
87. Chaal, B.K., & Green, B.R. (2005). Protein import pathways in 'complex' chloroplasts derived from secondary endosymbiosis involving a red algal ancestor. Plant Mol Biol 57, 333-342.
88. Bolte, K., Bullmann, L., Hempel, F., Bozarth, A., Zauner, S., & Maier, U.G. (2009). Protein targeting into secondary plastids. J Eukaryot Microbiol 56, 9-15.
89. Brennicke, A., Marchfelder, A., & Binder, S. (1999). RNA editing. FEMS Microbiol Rev 23, 297-316.
90. Voulhoux, R., Bos, M.P., Geurtsen, J., Mols, M., & Tommassen, J. (2003). Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299, 262-265.
91. Morton, B.R. (1998). Selection on the codon bias of chloroplast and cyanelle genes in different plant and algal lineages. J Mol Evol 46, 449-459.
92. Zhang, H., Hou, Y., Miranda, L., Campbell, D.A., Sturm, N.R., Lin, S., & Gaasterland, T. (2007). Spliced leader RNA trans-splicing in dinoflagellates. Proc Natl Acad Sci U S A 104, 4618-4623.
93. Apt, K.E., Kroth-Pancic, P.G., & Grossman, A.R. (1996). Stable nuclear transformation of the diatom Phaeodactylum tricornutum. Mol Gen Genet 252, 572-579.
94. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245-250.
95. Rogers, M.B., Gilson, P.R., Su, V., McFadden, G.I., & Keeling, P.J. (2007). The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of chlorarachniophyte and euglenid secondary endosymbionts. Mol Biol Evol 24, 54-62.
96. Small, I.D., & Peeters, N. (2000). The PPR motif -a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25, 46-47.
97. Müller, M., & Klösgen, R.B. (2005). The Tat pathway in bacteria and chloroplasts (Review). Mol Membr Biol 22, 113-121.
98. Reynolds, E.S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17, 208-212.
99. Miyata, Y., & Sugita, M. (2004). Tissue-and stage-specific RNA editing of rps14 transcripts in moss (Physcomitrella patens) chloroplasts. J Plant Physiol 161, 113-115.
100. Ris, H., & Plaut, W. (1962). Ultrastructure of DNA-containing areas in the chloroplast of Chlamydomonas. J Cell Biol 13, 383-391.
101. Schmitz-Linneweber, C., Regel, R., Du, T.G., Hupfer, H., Herrmann, R.G., & Maier, R.M. (2002). The plastid chromosome of Atropa belladonna and its comparison with that of Nicotiana tabacum: The role of RNA editing in generating divergence in the process of plant speciation. Mol Biol Evol 19, 1602-1612.
102. Sommer, M.S., Gould, S.B., Lehmann, P., Gruber, A., Przyborski, J.M., & Maier, U.G. (2007). Der1- mediated preprotein import into the periplastid compartment of chromalveolates? Mol Biol Evol 24, 918-928.
103. Schattner, P., Brooks, A.N., & Lowe, T.M. (2005). The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33, W686-689.
104. Wang, Y., & Morse, D. (2006). Rampant polyuridylylation of plastid gene transcripts in the dinoflagellate Lingulodinium. Nucleic Acid Res. 34, 613-619.
105. Birnboim, H.C., & Doly, J. (1979). A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7, 1513-1523.
106. Salone, V., Rudinger, M., Polsakiewicz, M., Hoffmann, B., Groth-Malonek, M., Szurek, B., Small, I., Knoop, V., & Lurin, C. (2007). A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett 581, 4132-4138.
107. Cavalier-Smith, T. (1999). Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46, 347-366.
108. Cavalier-Smith, T. (2003). Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Philos Trans R Soc Lond B Biol Sci 358, 109-134.
109. Morse, D., Salois, P., Markovic, P., & Hastings, J.W. (1995). A nuclear-encoded form II RuBisCO in dinoflagellates. Science 268, 1622-1624.
110. Mereschkowsky, C. (1905). Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Botansiches Centralblatt 25, 593-604.
111. Barbrook, A.C., Santucci, N., Plenderleith, L.J., Hiller, R.G., & Howe, C.J. (2006). Comparative analysis of dinoflagellate chloroplast genomes reveals rRNA and tRNA genes. BMC Genomics 15, 1-15.
112. Wallas, T.R., Smith, M.D., Sanchez-Nieto, S., & Schnell, D.J. (2003). The roles of Toc34 and Toc75 in targeting the Toc159 preprotein receptor to chloroplasts. J Biol Chem 278, 44289-44297.
113. Becker, T., Pfannschmidt, S., Guiard, B., Stojanovski, D., Milenkovic, D., Kutik, S., Pfanner, N., Meisinger, C., & Wiedemann, N. (2008). Biogenesis of the mitochondrial TOM complex: Mim1 promotes insertion and assembly of signal-anchored receptors. J Biol Chem 283, 120- 127.
114. Zhang, Z., Green, B.R., & Cavalier-Smith, T. (1999). Single gene circles in dinoflagellate chloroplast genomes. Nature 400, 155-159.
115. van Dooren, G.G., Tomova, C., Agrawal, S., Humbel, B.M., & Striepen, B. (2008). Toxoplasma gondii Tic20 is essential for apicoplast protein import. Proc Natl Acad Sci U S A 105, 13574-13579.
116. Ritzenthaler, C., Nebenführ, A., Movafeghi, A., Stussi-garaud, C., Behnia, L., Pimpl, P., Staehelin, L.A., & Robinson, D.G. (2002). Reevaluation of the effects of Brefeldin A on plant cells using tobacco bright yellow 2 cells expressing Golgi-targeted Green Fluorescent Protein and COPI Antisera. Plant Cell 14, 237-261.
117. Rivals, E., Bruyere, C., Toffano-Nioche, C., & Lecharny, A. (2006). Formation of the Arabidopsis pentatricopeptide repeat family. Plant Physiol 141, 825-839.
118. Bodansky, S., Mintz, L.B., & Holmes, D.S. (1979). The mesokaryote Gyrodinium cohnii lacks nucleosomes. Biochem Biophys Res Commun 88, 1329-1336.
119. Zauner, S., Greilinger, D., Laatsch, T., Kowallik, K.V., & Maier, U.G. (2004). Substitutional editing of transcripts from genes of cyanobacterial origin in the dinoflagellate Ceratium horridum. Grana 577, 535-538.
120. Sharpe, H.J., Stevens, T.J., & Munro, S. (2010). A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142, 158-169.
121. Rodriguez-Ezpeleta, N., Brinkmann, H., Burey, S.C., Roure, B., Burger, G., Loffelhardt, W., Bohnert, H.J., Philippe, H., & Lang, B.F. (2005). Monophyly of primary photosynthetic eukaryotes: Green plants, red algae, and glaucophytes. Curr Biol 15, 1325-1330.
122. Cavalier-Smith, T. (2000). Membrane heredity and early chloroplast evolution. Trends Plant Sci 5, 174-182.
123. Schmitz-Linneweber, C., & Small, I. (2008). Pentatricopeptide repeat proteins: A socket set for organelle gene expression. Trends Plant Sci 13, 663-670.
124. Moustafa, A., Beszteri, B., Maier, U.G., Bowler, C., Valentin, K., & Bhattacharya, D. (2009). Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324, 1724-1726.
125. Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 7, 1224-1231.
126. Wastl, J., & Maier, U.G. (2000). Transport of proteins into cryptomonads complex plastids. J Biol Chem 275, 23194-23198.

Das Dokument ist im Internet frei zugänglich - Hinweise zu den Nutzungsrechten