In vivo quantitative relationship between plastid division proteins FtsZ1 and FtsZ2 and identification of ARC6 and ARC3 in a native FtsZ complex

Biochemical Journal

Volumn 412, Issue 2, 2008, Pages 367-378

  McAndrew, Rosemary S ^a   Olson, Bradley J S C ^a,b   Kadirjan Kalbach, Deena K ^a   Chi Ham, Cecilia L ^a,c   Vitha, Stanislav ^a,d   Froehlich, John E ^a   Osteryoung, Katherine W ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Texas AandM University   (United States)

Author keywords

Arabidopsis thaliana; Bacterial cell division; Cytoskeleton; FtsZ; Organelle division; Pea

Indexed keywords

BACTERIA; BIOCHEMISTRY; BIOLOGICAL MEMBRANES; CHLOROPHYLL; PLANT CELL CULTURE;

ARABIDOPSIS THALIANA; BACTERIAL CELL DIVISION; CYTOSKELETON; MOLAR RATIO; ORGANELLE DIVISION;

PROTEINS;

FTSZ PROTEIN;

ARABIDOPSIS; ARTICLE; CELL DIVISION; CHLOROPLAST; DENSITY GRADIENT CENTRIFUGATION; ESCHERICHIA COLI; GEL ELECTROPHORESIS; GEL FILTRATION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VIVO STUDY; MORPHOMETRICS; PLASTID; PRIORITY JOURNAL; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; STOICHIOMETRY; WILD TYPE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DIVISION; CHLOROPLASTS; MULTIPROTEIN COMPLEXES; PEAS; PLANT PROTEINS; PLASTIDS; RECOMBINANT FUSION PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PISUM SATIVUM;

EID: 44449129474     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20071354     Document Type: Article

References (64)

1. Romberg, L. and Levin, P. A. (2003) Assembly dynamics of the bacterial cell division protein FtsZ: poised at the edge of stability. Annu. Rev. Microbiol. 57, 125-154
2. Michie, K. and Lowe, J. (2006) Dynamic filaments of the bacterial cytoskeleton. Annu. Rev. Biochem. 75, 467-492
3. Margolin, W. (2005) Bacterial mitosis: actin in a new role at the origin. Curr. Biol. 15, R259-R261
4. Anderson, D. E., Gueiros-Filho, F. J. and Erickson, H. P. (2004) Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J. Bacteriol. 186, 5775-5781
5. Chen, Y. and Erickson, H. P. (2005) Rapid in vitro assembly dynamics and subunit turnover of FtsZ demonstrated by fluorescence resonance energy transfer. J. Biol. Chem. 280, 22549-22554
6. Chen, Y., Bjornson, K., Redick, S. D. and Erickson, H. P. (2005) A rapid fluorescence assay for FtsZ assembly indicates cooperative assembly with a dimer nucleus. Biophys. J. 88, 505-514
7. Redick, S. D., Stricker, J., Briscoe, G. and Erickson, H. P. (2005) Mutants of FtsZ targeting the protofilament interface: effects on cell division and GTPase activity. J. Bacteriol. 187, 2727-2736
8. Stricker, J., Maddox, P., Salmon, E. D. and Erickson, H. P. (2002) Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc. Natl. Acad. Sci. U.S.A. 99, 3171-3175
9. Sossong, Jr, T. M., Brigham-Burke, M. R., Hensley, P. and Pearce, Jr, K. H. (1999) Self-activation of guanosine triphosphatase activity by oligomerization of the bacterial cell division protein FtsZ. Biochemistry 38, 14843-14850
10. Wang, X. and Lutkenhaus, J. (1993) The FtsZ protein of Bacillus subtilis is localized to the division site and has a GTPase activity that is dependent upon the FtsZ concentration. Mol. Microbiol. 9, 435-442
11. Dai, K. and Lutkenhaus, J. (1992) The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J. Bacteriol. 174, 6145-6151
12. Dewar, S. J., Begg, K. J. and Donachie, W. D. (1992) Inhibition of cell division initiation by an imbalance in the ratio of FtsA to FtsZ. J. Bacteriol. 174, 6314-6316
13. Hale, C. A. and de Boer, P. A. J. (1997) Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell 88, 175-185
14. Takada, A., Nagai, K. and Wachi, M. (2005) A decreased level of FtsZ is responsible for inviability of RNase E-deficient cells. Genes Cells 10, 733-741
15. Margolin, W. (2005) FtsZ and the division of prokaryotic cells and organelles. Nat. Rev. Mol. Cell Biol. 6, 862-871
16. Pradel, N., Santini, C.-L., Bernadac, A., Fukumori, Y. and Wu, L.-F. (2006) Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles. Proc. Natl. Acad. Sci. U.S.A. 103, 17485-17489
17. Osteryoung, K. W. and Vierling, E. (1995) Conserved cell and organelle division. Nature 376, 473-474
18. 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
19. Stokes, K. D., McAndrew, R. S., Figueroa, R., Vitha, S. and Osteryoung, K. W. (2000) Chloroplast division and morphology are differentially affected by overexpression of FtsZ1 and FtsZ2 genes in Arabidopsis. Plant Physiol. 124, 1668-1677
20. McAndrew, R. S., Froehlich, J. E., Vitha, S., Stokes, K. D. and Osteryoung, K. W. (2001) Colocalization of plastid division proteins in the chloroplast stromal compartment establishes a new functional relationship between FtsZ1 and FtsZ2 in higher plants. Plant Physiol. 127, 1656-1666
21. 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
22. Miyagishima, S., Takahara, M., Mori, T., Kuroiwa, H., Higashiyama, T. and Kuroiwa, T. (2001) Plastid division is driven by a complex mechanism that involves differential transition of the bacterial and eukaryotic division rings. Plant Cell 13, 2257-2268
23. Maple, J., Vojta, L., Soll, J. and Moller, S. G. (2007) ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Rep. 8, 293-299
24. Maple, J., Aldridge, C. and Moller, S. G. (2005) Plastid division is mediated by combinatorial assembly of plastid division proteins. Plant J. 43, 811-823
25. Glynn, J. M., Miyagishima, S., Yoder, D. W., Osteryoung, K. W. and Vitha, S. (2007) Chloroplast division. Traffic 8, 451-461
26. Fujiwara, M. and Yoshida, S. (2001) Chloroplast targeting of chloroplast division FtsZ2 proteins in Arabidopsis. Biochem. Biophys. Res. Commun. 287, 462-467
27. Vitha, S., Froehlich, J. E., Koksharova, O., Pyke, K. A., van Erp, H. and Osteryoung, K. W. (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15, 1918-1933
28. Yoder, D. W., Kadirjan-Kalbach, D., Olson, B. J. S. C., Miyagishima, S. Y., Deblasio, S. L., Hangarter, R. P. and Osteryoung, K. W. (2007) Effects of mutations in Arabidopsis FtsZ1 on plastid division, FtsZ ring formation and positioning, and FtsZ filament morphology in vivo. Plant Cell Physiol. 48, 775-791
29. El-Kafafi, S., Karamoko, M., Pignot-Paintrand, I., Grunwald, D., Mandaron, P., Lerbs-Mache, S. and Falconet, D. (2008) Developmentally regulated association of plastid division protein FtsZ1 with thylakoid membranes in Arabidopsis thaliana. Biochem. J. 409, 87-94
30. 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. U.S.A. 95, 4368-4373
31. Raynaud, C., Cassier-Chauvat, C., Perennes, C. and Bergounioux, C. (2004) An Arabidopsis homolog of the bacterial cell division inhibitor SulA is involved in plastid division. Plant Cell 16, 1801-1811
32. Bruce, B. D., Perry, S., Froehlich, J. and Keegstra, K. (1994) In vitro import of proteins into chloroplasts. In Plant Molecular Biology Manual J1 (Gelvin, S. B. and Schilperoort, R. B., eds), pp. 1-15, Kluwer Academic Publishers, Boston
33. Alonso, J. M., Stepanova, A. N., Leisse, T. J., Kim, C. J., Chen, H., Shinn, P., Stevenson, D. K., Zimmerman, J., Barajas, P., Cheuk, R. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657
34. Pyke, K. A., Marrison, J. L. and Leech, R. M. (1991) Temporal and spatial development of the cells of the expanding first leaf of Arabidopsis thaliana (L.) Heynh. J. Exp. Bot. 42, 1407-1416
35. Clos, J. and Brandau, S. (1994) pJC20 and pJC40: two high-copy-number vectors for T7 RNA polymerase-dependent expression of recombinant genes in Escherichia coli. Protein Expression Purif. 5, 133-137
36. Shimada, H., Koizumi, M., Kuroki, K., Mochizuki, M., Fujimoto, H., Ohta, H., Masuda, T. and Takamiya, K.-I. (2004) ARC3, a chloroplast division factor, is a chimera of prokaryotic FtsZ and part of eukaryotic phosphatidylinositol-4- phosphate 5-kinase. Plant Cell Physiol. 45, 960-967
37. Miroux, B. and Walker, J. E. (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298
38. de Boer, P. A. J., Crossley, R. E. and Rothfield, L. I. (1989) A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56, 641-649
39. Olson, B. J. S. C. and Markwell, J. P. (2007) Assays for determination of protein concentration. In Current Protocols in Protein Science (Coligan, J. E., Dunn, B. M., Speicher, D. W. and Wingfield, P. T., eds), pp. 3.4.1-3.4.29, John Wiley and Sons, Inc., Chichester
40. Lu, C., Stricker, J. and Erickson, H. P. (1998) FtsZ from Escherichia coli, Azotobacter vinelandii and Thermotoga maritima: quantitation, GTP hydrolysis, and assembly. Cell Motil. Cytoskeleton 40, 71-86
41. Fitzpatrick, L. M. and Keegstra, K. (2001) A method for isolating a high yield of Arabidopsis chloroplasts capable of efficient import of precursor proteins. Plant J. 27, 59-65
42. Arnon, D. I. (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24, 1-15
43. Laemmli, U. K. (1970) Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227, 680-685
44. Cline, K., Werner-Washburne, M., Andrews, J. and Keegstra, K. (1984) Thermolysin is a suitable protease for probing the surface on intact pea chloroplasts. Plant Physiol. 75, 675-678
45. Anderson, D. J. and Blobel, G. (1983) Immunoprecipitation of proteins from cell-free translations. Methods Enzymol. 96, 111-120
46. Nielsen, E., Akita, M., Davila-Aponte, J. and Keegstra, K. (1997) Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J. 16, 935-946
47. Weigel, D. and Glazebrook, J. (2002) Arabidopsis: a Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor
48. Pyke, K. A. and Leech, R. M. (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol. 104, 201-207
49. Löwe, J. (1998) Crystal structure determination of FtsZ from Methanococcus jannaschii. J. Struct. Biol. 124, 235-243
50. Lu, C., Reedy, M. and Erickson, H. P. (2000) Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J. Bacteriol. 182, 164-170
51. Romberg, L., Simon, M. and Erickson, H. P. (2001) Polymerization of ftsz, a bacterial homolog of tubulin is assembly cooperative? J. Biol. Chem. 276, 11743-11753
52. Gonzalez, J. M., Jimenez, M., Velez, M., Mingorance, J., Andreu, J. M., Vicente, M. and Rivas, G. (2003) Essential cell division protein FtsZ assembles into one monomer-thick ribbons under conditions resembling the crowded intracellular environment. J. Biol. Chem. 278, 37664-37671
53. Musser, S. M. and Theg, S. M. (2000) Proton transfer limits protein translocation rate by the thylakoid ΔpH/Tat machinery. Biochemistry 39, 8228-8233
54. Caplan, M. and Erickson, H. P. (2003) Apparent cooperative assembly of the bacterial cell-division protein FtsZ demonstrated by isothermal titration calorimetry. J. Biol. Chem. 278, 13784-13784
55. Rueda, S., Vicente, M. and Mingorance, J. (2003) Concentration and assembly of the division ring proteins FtsZ, FtsA, and ZipA during the Escherichia coli cell cycle. J. Bacteriol. 185, 3344-3351
56. Stokes, K. D. and Osteryoung, K. W. (2003) Early divergence of the FtsZ1 and FtsZ2 plastid division gene families in photosynthetic eukaryotes. Gene 320, 97-108
57. Rensing, S. A., Kiessling, J., Reski, R. and Decker, E. L. (2004) Diversification of ftsZ during early land plant evolution. J. Mol. Evol. 58, 154-162
58. Vaughan, S., Wickstead, B., Gull, K. and Addinall, S. G. (2004) Molecular evolution of FtsZ protein sequences encoded within the genomes of archaea, bacteria, and eukaryota. J. Mol. Evol. 58, 19-29
59. El-Kafafi, E. S., Mukherjee, S., El-Shami, M., Putaux, J. L., Block, M. A., Pignot-Paintrand, I., Lerbs-Mache, S. and Falconet, D. (2005) The plastid division proteins, FtsZ1 and FtsZ2, differ in their biochemical properties and sub-plastidial localisation. Biochem. J. 387, 669-676
60. Lohse, S., Hause, B., Hause, G. and Fester, T. (2006) FtsZ characterization and immunolocalization in the two phases of plastid reorganization in arbuscular mycorrhizal roots of Medicago truncatula. Plant Cell Physiol. 47, 1124-1134
61. Olson, B. J. S. C. and Osteryoung, K. W. (2007) Biochemical analysis of plant FtsZ1 and FtsZ2. Plant Biology and Botany 2007 Joint Congress, Chicago, IL, U.S.A., 7-11 July 2007, Abstract 234 or 707
62. Vitha, S., Holzenburg, A. and Osteryoung, K. W. (2005) Assembly dynamics of FtsZ and ARC6 plastid-dividing proteins. Microsc. Microanal. 11, 1154
63. Hu, Z., Mukherjee, A., Pichoff, S. and Lutkenhaus, J. (1999) The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc. Natl. Acad. Sci. U.S.A. 96, 14819-14824
64. Raynaud-Messina, B. and Merdes, A. (2007) γ-tubulin complexes and microtubule organization. Curr. Opin. Cell Biol. 19, 24-30