Challenges to our current view on chloroplasts

Biological Chemistry

Volumn 390, Issue 8, 2009, Pages 731-738

  Reski, Ralf ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Acetabularia; Arabidopsis; Chlamydomonas; Chloroplast division; Endosymbiosis; FtsZ; Mesostigma; Physcomitrella; Plastoskeleton; Stromule

Indexed keywords

AMPICILLIN; BETA LACTAM ANTIBIOTIC; CEFOTAXIME; FTSZ PROTEIN; INTERMEDIATE FILAMENT PROTEIN; MREB PROTEIN; PENICILLIN G;

CELL DIFFERENTIATION; CELL STRUCTURE; CHLOROPLAST; CYANOBACTERIUM; CYTOLOGY; CYTOSKELETON; EUKARYOTE; EVOLUTION; NONHUMAN; PLASTID; PRIORITY JOURNAL; REVIEW; STROMULE;

ARABIDOPSIS; BACTERIA; BACTERIAL PROTEINS; BETA-LACTAMS; BRYOPSIDA; CELL DIVISION; CHLOROPLASTS; CYANOBACTERIA; CYTOSKELETAL PROTEINS; EVOLUTION, MOLECULAR; PHOTOSYNTHESIS; PHYLOGENY;

ACETABULARIA; ARABIDOPSIS; ARCHAEPLASTIDA; BACTERIA (MICROORGANISMS); CHLAMYDOMONAS; EUKARYOTA; MESOSTIGMA; PHYSCOMITRELLA;

EID: 70349439088     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2009.089     Document Type: Review

References (68)

1. Abel, W.O., Knebel, W., Koop, H.-U., Marienfeld, J.R., Quader, H., Reski, R., Schnepf, E., and Spörlein, B. (1989). A cytokinin- sensitive mutant of the moss, Physcomitrella patens, defective in chloroplast division. Protoplasma 152, 1-13.
2. Adl, S.M., Simpson, A.G.B., Farmer, M.A., Andersen, R.A., Anderson, O.R., Barta, J.R., Bowser, S.S., Brugerolle, G., Fensome, R.A., Fredericq, S., et al., (2005). The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52, 339-451.
3. Ausmees, N., Kuhn, J.A., and Jacobs-Wagner, C. (2003). The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115, 705-713.
4. Berenguer, J., Rojo, F., de Pedro, M.A., Pfanzagl, B., and Löffelhardt, W. (1987). Penicillin-binding proteins in the cyanelles of Cyanophora paradoxa, a eukaryotic photoautotroph sensitive to β-lactam antibiotics. FEBS Lett. 224, 401-405.
5. Block, M.A., Douce, R., Joyard, J., and Rolland, N. (2007). Chloroplast envelope membranes: a dynamic interface between plastids and the cytosol. Photosynth. Res. 92, 225-244.
6. Errington, J. (2003). Dynamic proteins and a cytoskeleton in bacteria. Nat. Cell Biol. 5, 175-178.
7. Garcia, M., Myouga, F., Takechi, K., Sato, H., Nabeshima, K., Nagata, N., Takio, S., Shinozaki, K., and Takano, H. (2008). An Arabidopsis homolog of the bacterial peptidoglycan synthesis enzyme MurE has an essential role in chloroplast development. Plant J. 53, 924-934.
8. Glynn, J.M., Miyagishima, S., Yoder, D.W., Osteryoung, K.W., and Vitha, S. (2007). Chloroplast division. Traffic 8, 451-461.
9. Graumann, P.L. (2007). Cytoskeletal elements in bacteria. Annu. Rev. Microbiol. 61, 589-618.
10. Gray, J.C., Sullivan, J.A., Hibberd, J.M., and Hansen, M.R. (2001). Stromules: mobile protrusions and interconnections between plastids. Plant Biol. 3, 223-233.
11. Gremillon, L., Kiessling, J., Hause, B., Decker, E.L., Reski, R., and Sarnighausen, E. (2007). Filamentous temperature-sensitive Z (FtsZ) isoforms specifically interact in the chloroplasts and in the cytosol of Physcomitrella patens. New Phytologist 176, 299-310.
12. Hanson, M.R. and Sattarzadeh, A. (2008). Dynamic morphology of plastids and stromules in angiosperm plants. Plant Cell Environ. 31, 646-657.
13. Hohe, A., Egener, T., Lucht, J.M., Holtorf, H., Reinhard, C., and Reski, R. (2004). An improved and highly standardised transformation procedure allows efficient production of single and multiple targeted gene knockouts in a moss, Physcomitrella patens. Curr. Genet. 44, 339-347.
14. Hoffman, L. (1967). Observations on the fine structure of Oedogonium. III. Microtubular elements in the chloroplasts of Oe. cardicacum. J. Phycol. 3, 212-221.
15. Iino, M. and Hashimoto, H. (2003). Intermediate features of cyanelle division of Cyanophora paradoxa (Glaucocystophyta) between cyanobacterial and plastid division. J. Phycol. 39, 561-569.
16. Kasten, B. and Reski, R. (1997). β-Lactam antibiotics inhibit chloroplast division in a moss (Physcomitrella patens) but not in tomato (Lycopersicon esculentum). J. Plant Physiol. 150, 137-140.
17. Kasten, B., Buck, F., Nuske, J., and Reski, R. (1997). Cytokinin affects nuclear- and plastome-encoded energy-converting plastid enzymes. Planta 201, 261-272.
18. Katayama, N., Takano, H., Sugiyama, M., Takio, S., Sakai, A., Tanaka, K., Kuroiwa, H., and Ono, K. (2003). Effects of antibiotics that inhibit the bacterial peptidoglycan synthesis pathway on moss chloroplast division. Plant Cell Physiol. 44, 776-781.
19. Kies, L. (1988). The effect of penicillin on the morphology and ultrastructure of Cyanophora, Gloechaete and Glaucocystis (Glaucophyceae) and their cyanelles. Endocytobiosis Cell Res. 5, 361-372.
20. Kiessling, J., Kruse, S., Rensing, S.A., Harter, K., Decker, E.L., and Reski, R. (2000). Visualization of a cytoskeleton-like FtsZ network in chloroplasts. J. Cell Biol. 151, 945-950.
21. Kiessling, J., Martin, A., Gremillon, L., Rensing, S.A., Nick, P., Sarnighausen, E., Decker, E.L., and Reski, R. (2004). Dual targeting of plastid division protein FtsZ to chloroplasts and the cytoplasm. EMBO Rep. 5, 889-894.
22. Klebs, G. (1888). Beiträge zur Physiologie der Pflanzenzelle. In: Untersuchungen aus dem botanischen Institut zu Tübingen, Vol.II, W. Pfeffer, ed. (Leipzig, Germany: Verlag Wilhelm Engelmann), pp. 489-568.
23. Köhler, R.H., Cao, J., Zipfel, W.R., Webb, W.W., and Hanson, M.R. (1997). Exchange of protein molecules through connections between higher plant plastids. Science 276, 2039-2042.
24. Kugita, M., Kaneko, A., Yamamoto, T., Takeya, Y., Matsumoto, T., and Yoshinaga, K. (2003). The complete nucleotide sequence of the hornwort (Anthoceros formosae) chloroplast genome: insight into earliest land plants. Nucleic Acids Res. 31, 716-721.
25. Kuroiwa, T., Misumi, O., Nishida, K., Yagisawa, F., Yoshida, Y., Fujiwara, T., and Kuroiwa, H. (2008). Vesicle, mitochondrial, and plastid division machineries with emphysis on dynamin and electron-dense rings. Int. Rev. Cell Mol. Biol. 271, 97-152.
26. Kwok, E.Y. and Hanson, M.R. (2004a). Stromules and the dynamic nature of plastid morphology. J. Microsc. 214, 124-137.
27. Kwok, E.Y. and Hanson, M.R. (2004b). Plastids and stromules interact with the nucleus and cell membrane in vascular plants. Plant Cell Rep. 23, 188-195.
28. Lang, D., Zimmer, A.D., Rensing, S.A., and Reski, R. (2008). Exploring plant biodiversity: the Physcomitrella genome and beyond. Trends Plant Sci. 13, 542-549.
29. Lawrence, M. and Possingham, J. (1984). Observations of microtubule-like structures within spinach plastids. Biol. Cell 52, 77-82.
30. Lowe, J. and Amos, L.A. (1998). Crystal structure of the bacterial cell-division protein FtsZ. Nature 391, 203-206.
31. Lowe, J. and Amos, L.A. (2009). Evolution of cytomotive filaments: the cytoskeleton from prokaryotes to eukaryotes. Int. Rev. Biochem. Cell Biol. 41, 323-329.
32. Lowe, J. van den Ent, F., and Amos, L.A. (2004). Molecules of the bacterial cytoskeleton. Annu. Rev. Biophys. Biomol. Struct. 33, 177-198.
33. Lu, C.L., Reedy, M., and Erickson, H.P. (2000). Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J. Bacteriol. 182, 164-170.
34. Lutkenhaus, J. (1990). Regulation of cell division in E. coli. Trends Genet. 6, 22-25.
35. Lutkenhaus, J. (2003). Another cytoskeleton in the closet. Cell 115, 648-650.
36. Machida, M., Takechi, K., Sato, H., Chung, S.J., Kuroiwa, H., Takio, S., Seki, M., Shinozaki, K., Fujita, T., Hasebe, M., et al., (2006). Genes for the peptidoglycan synthesis pathway are essential for chloroplast division in moss. Proc. Natl. Acad. Sci. USA 103, 6753-6758.
37. Maple, J. and Moller, S.G. (2007). Plastid division coordination across a double-membraned structure. FEBS Lett. 581, 2162-2167.
38. Margolin, W. (1998). A green light for the bacterial cytoskeleton. Trends Microbiol. 6, 233-238.
39. Martin, W., Stoebe, B., Goremykin, V., Hapsmann, S., Hasegawa, M., and Kowallik, K.V. (1998). Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393, 162-165.
40. Martin, A., Lang, D., Heckmann, J., Zimmer, A.D., Vervliet- Scheebaum, M., and Reski, R. (2009). A uniquely high number of ftsZ genes in the moss Physcomitrella patens. Plant Biol., published online, DOI: 10.1111/j.1438-8677. 2008. 00174.x.
41. McFadden, G.I. (2000). Skeletons in the closet: how do chloroplasts stay in shape? J. Cell Biol. 151, F19-F21.
42. Menzel, D. (1994). An interconnected plastidom in Acetabularia- implications for the mechanism of chloroplast motility. Protoplasma 179, 166-171.
43. Nogales, E., Downing, K.H., Amos, L.A., and Lowe, J. (1998). Tubulin and FtsZ form a distinct family of GTPases. Nat. Struct. Biol. 5, 451-458.
44. Nott, A., Jung, H.S., Koussevitzky, S., and Chory, J. (2006). Plastid- to-nucleus retrograde signalling. Annu. Rev. Plant Biol. 57, 739-759.
45. Osteryoung, K.W., Stokes, K.D., Rutherford, S.M., Percival, A.L., and Lee, W.Y. (1998). Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell 10, 1991-2004.
46. Pickett-Heaps, J. (1968). Microtubule-like structures in the growing plastids or chloroplasts of two algae. Planta 81, 193-200.
47. Qiu, Y.L. (2008). Phylogeny and evolution of charophytic algae and land plants. J. Systemat. Evol. 46, 287-306.
48. Reski, R. (1994). Plastid genes and chloroplast biogenesis. In: Cytokinins. Chemistry, Activity, and Function, D.W.S. Mok and M.C. Mok, eds. (Boca Raton/Ann Arbor/London/Tokyo: CRC Press), pp. 179-195.
49. Reski, R. (1998). Development, genetics and molecular biology of mosses. Botan. Acta 111, 1-15.
50. Reski, R. (2002). Rings and networks: the amazing complexity of FtsZ in chloroplasts. Trends Plant Sci. 7, 103-105.
51. Reski, R., Wehe, M., Hadeler, B., Marienfeld, J.R., and Abel, W.O. (1991). Cytokinin and light quality interact at the molecular level in the chloroplast-mutant PC22 of the moss Physcomitrella. J. Plant Physiol. 138, 236-243.
52. Reutter, K., Atzorn, R., Hadeler, B., Schmülling, T., and Reski, R. (1998). Expression of the bacterial ipt gene in Physcomitrella rescues mutations in budding and in plastid division. Planta 206, 196-203.
53. Rivera, E. and Arnott, H. (1982). Tubular structures in the plastids of Echimastus inertextus Brit. & Rose (Cactaceae). New Phytologist 90, 551-561.
54. Sato, M., Nishikawa, T., Kajitani, H., and Kawano, S. (2007). Conserved relationship between FtsZ and peptidoglycan in the cyanelles of Cyanophora paradoxa similar to that in bacterial cell division. Planta 227, 177-187.
55. Schneider, D., Fuhrmann, E., Scholz, I., Hess, W.R., and Graumann, P.L. (2007). Fluorescence staining of live cyanobacterial cells suggest non-stringent chromosome segregation and absence of a connection between cytoplasmic and thylakoid membranes. BMC Cell Biol. 8, 39.
56. Senn, G. (1908). Die Gestalts- und Lageveränderung der Pflanzen- Chromatophoren (Leipzig, Germany: Verlag Wilhelm Engelmann).
57. Simon, A., Glöckner, G., Felder, M., Melkonian, M., and Becker, B. (2006). EST analysis of the scaly green flagellate Mesostigma viride (Streptophyta): implications for the evolution of green plants (Viridiplantae). BMC Plant Biol. 6, 2.
58. Stegemann, S., Hartmann, S., Ruf, S., and Bock, R. (2003). High-frequency gene transfer from the chloroplast genome to the nucleus. Proc. Natl. Acad. Sci. USA 100, 8828-8833.
59. Strepp, R., Scholz, S., Kruse, S., Speth, V., and Reski, R. (1998). Plant nuclear gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin. Proc. Natl. Acad. Sci. USA 95, 4368-4373.
60. Sumiya, N., Hirata, A., and Kawano, S. (2008). Multiple FtsZ ring formation and reduplicated chloroplast DNA in Nannochloris bacillaris (Chlorophyta, Trebouxiophyceae) under phosphateenriched culture. J. Phycol. 44, 1476-1489.
61. Suppanz, I., Sarnighausen, E., and Reski, R. (2007). An integrated physiological and genetic approach to the dynamics of FtsZ targeting and organisation in a moss, Physcomitrella patens. Protoplasma 232, 1-9.
62. Uniacke, J. and Zerges, W. (2007). Photosystem II assembly and repair are differentially localized in Chlamydomonas. Plant Cell 19, 3640-3654.
63. Villarejo, A., Buren, S., Larsson, S., Dejardin, A., Monne, M., Rudhe, C., Karlsson, J., Jansson, S., Lerouge, P., Rolland, N., et al. (2005). Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat. Cell Biol. 7, 1224-1231.
64. Vitha, S., McAndrew, R.S., and Osteryoung, K.W. (2001). FtsZ ring formation at the chloroplast division site in plants. J. Cell Biol. 153, 111-119.
65. Wasmann, C.C., Löffelhardt, W., and Bohnert, H.J. (1987). Cyanelles: organization and molecular biology. In: The Cyanobacteria, P. Fay and C. van Baalen, eds. (Amsterdam, The Netherlands: Elsevier), pp. 303-324.
66. Wildman, S.G., Hongladarum, T., and Honda, S.I. (1962). Chloroplast and mitochondria in living plant cells: cinephotomicrographic studies. Science 138, 434-436.
67. Yang, Y., Glynn, J.M., Olson, B.J.S.C., Schmitz, A.J., and Osteryoung, K.W. (2008). Plastid division: across time and space. Curr. Opin. Plant Biol. 11, 577-584.
68. Zimmer, A., Lang, D., Richardt, S., Frank, W., Reski, R., and Rensing, S.A. (2007). Dating the early evolution of plants: detection and molecular clock analyses of orthologs. Mol. Genet. Genomics 278, 393-402.