ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2

Plant Cell

Volumn 15, Issue 8, 2003, Pages 1918-1933

  Vitha, Stanislav ^a   Froehlich, John E ^a   Koksharova, Olga ^a,c   Pyke, Kevin A ^b   Van Erp, Harrie ^a   Osteryoung, Katherine W ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c VAVILOV INSTITUTE OF GENERAL GENETICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; FLUORESCENCE; MORPHOLOGY;

PLASTID DIVISION;

PROTEINS;

ARABIDOPSIS; CYANOBACTERIA; PROKARYOTA;

EID: 0041920563     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.013292     Document Type: Article

References (93)

1. Addinall, S.G., and Holland, B. (2002). The tubulin ancestor, FtsZ, draughtsman, designer and driving force for bacterial cytokinesis. J. Mol. Biol. 318, 219-236.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
3. Bi, E., and Lutkenhaus, J. (1991). FtsZ ring structure associated with division in Escherichia coli. Nature 354, 161-164.
4. Bi, E., and Lutkenhaus, J. (1993). Cell division inhibitors SuIA and MinCD prevent formation of the FtsZ ring. J. Bacteriol. 175, 1118-1125.
5. Bramhill, D. (1997). Bacterial cell division. Annu. Rev. Cell Dev. Biol. 13, 395-424.
6. Bukau, B., and Norwich, A.L. (1998). The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366.
7. Bukau, B., and Walker, G.C. (1989). Cellular defects caused by deletion of the Escherichia coli dnaK gene indicate roles for heat shock protein in normal metabolism. J. Bacteriol. 171, 2337-2346.
8. Burge, C., and Karlin, S. (1997). Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268, 78-94.
9. Cheetham, M.E., and Caplan, A.J. (1998). Structure, function and evolution of DnaJ: Conservation and adaptation of chaperone function. Cell Stress Chaperon. 3, 28-36.
10. Claros, M.G., and von Heijne, G. (1994). TopPred II: An improved software for membrane protein structure predictions. Comput. Appl. Biosci. 10, 685-686.
11. Cline, K., Werner-Washburne, M., Andrews, J., and Keegstra, K. (1984). Thermolysin is a suitable protease for probing the surface of intact pea chloroplasts. Plant Physiol. 75, 675-678.
12. Colletti, K.S., Tattersall, E.A., Pyke, K.A., Froelich, J.E., Stokes, K.D., and Osteryoung, K.W. (2000). A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr. Biol. 10, 507-516.
13. Cserzo, M., Wallin, E., Simon, I., von Heijne, G., and Elofsson, A. (1997). Prediction of transmembrane α-helices in prokaryotic membrane proteins: The dense alignment surface method. Protein Eng. 10, 673-676.
14. 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.
15. de Boer, P.A.J., Crossley, R.E., and Rothfield, L.I. (1992). Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli. J. Bacteriol. 174, 63-70.
16. Dinkins, R., Reddy, M.S.S., Leng, M., and Collins, G.B. (2001). Overexpression of the Arabidopsis thaliana MinD1 gene alters chloroplast size and number in transgenic tobacco plants. Planta 214, 180-188.
17. Douglas, S.E. (1998). Plastid evolution: Origins, diversity, trends. Curr. Opin. Genet. Dev. 8, 655-661.
18. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005-1016.
19. Errington, J., Daniel, R.A., and Scheffers, D.-J. (2003). Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67, 52-65.
20. Ewing, B., Millier, L., Wendl, M.C., and Green, P. (1998). Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8, 175-185.
21. Fourney, R., Miyakoshi, J., Day, R., and Paterson, M. (1988). Northern blotting: Efficient RNA staining and transfer. Focus 10, 5-7.
22. Fu, X., Shih, Y.L., Zhang, Y., and Rothfield, L.I. (2001). The MinE ring required for proper placement of the division site is a mobile structure that changes its cellular location during the Escherichia coli division cycle. Proc. Natl. Acad. Sci. USA 98, 980-985.
23. Fujiwara, M., and Yoshida, S. (2001). Chloroplast targeting of chloroplast division FtsZ2 proteins in Arabidopsis. Biochem. Biophys. Res. Commun. 287, 462-467.
24. Fulgosi, H., Gerdes, L., Westphal, S., Glockmann, C., and Soll, J. (2002). Cell and chloroplast division requires ARTEMIS. Proc. Natl. Acad. Sci. USA 99, 11501-11506.
25. Gao, H., Kadirjan-Kalbach, D., Froehlich, J.E., and Osteryoung, K.W. (2003). ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc. Natl. Acad. Sci. USA 100, 4328-4333.
26. Cleave, P. (1992). A versatile binary vector system with T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 20, 1203-1207.
27. Gueiros-Filho, F.J., and Losick, R. (2002). A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev. 16, 2544-2556.
28. 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.
29. Hale, C.A., and de Boer, P.A.J. (2002). ZipA is required for recruitment of FtsK, FtsQ, FtsL, and FtsN to the septal ring in Escherichia coli. J. Bacteriol. 184, 2552-2556.
30. Hashimoto, H. (2003). Plastid division: Its origins and evolution. Int. Rev. Cytol. 222, 63-98.
31. Hennessy, F., Cheetham, M.E., Dirr, H.W., and Blatch, G.L. (2000). Analysis of the levels of conservation of the J domain among the various types of DnaJ-like proteins. Cell Stress Chaperon. 5, 347-358
32. Hirokawa, T., Boon-Chieng, S., and Mitaku, S. (1998). SOSUI: Classification and secondary structure prediction system for membrane proteins. Bioinformatics 14, 378-379.
33. 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. USA 96, 14819-14824.
34. Itoh, R., Fujiwara, M., Nagata, N., and Yoshida, S. (2001). A chloroplast protein homologous to the eubacterial topological specificity factor MinE plays a role in chloroplast division. Plant Physiol. 127, 1644-1655.
35. Jackson, D.T., Froehlich, J.E., and Keegstra, K. (1998). The hydrophilic domain of Tic110, an inner envelope membrane component of the chloroplastic protein translocation apparatus, faces the stromal compartment. J. Biol. Chem. 273, 16583-16588.
36. Joyard, J., Billecocq, A., Bartlett, S.G., Block, M.A., Chua, N.H., and Douce, R. (1983). Localization of polypeptides to the cytosolic side of the outer envelope membrane of spinach chloroplasts. J. Biol. Chem. 258, 10000-10006.
37. Juretic, D., Zoranic, L., and Zucic, D. (2002). Basic charge clusters and predictions of membrane protein topology. J. Chem. Inf. Comp. Sci. 42, 620-632.
38. Kanamaru, K., Fujiwara, M., Kim, M., Nagashima, A., Nakazato, E., Tanaka, K., and Takahashi, H. (2000). Chloroplast targeting, distribution and transcriptional fluctuation of AtMinD1, a eubacteria-type factor critical for chloroplast division. Plant Cell Physiol. 41, 1119-1128.
39. Kelley, L.A., MacCallum, R.M., and Sternberg, M.J. (2000). Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol. 299, 499-520.
40. 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.
41. Koksharova, O.A., and Wolk, P.C. (2002). A novel gene that bears a DnaJ motif influences cyanobacterial cell division. J. Bacteriol. 184, 5524-5528.
42. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L.L. (2001). Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 305, 567-580.
43. Kulp, D., Haussler, D., Reese, M.G., and Eeckman, F.H. (1996). A generalized hidden Markov model for the recognition of human genes in DNA. Proc. Int. Conf. Intell. Syst. Mol. Biol. 4, 134-142.
44. Kuroiwa, T., Kuroiwa, H., Sakai, A., Takahashi, H., Toda, K., and Itoh, R. (1998). The division apparatus of plastids and mitochondria. Int. Rev. Cytol. 181, 1-41.
45. Lutkenhaus, J. (1998). The regulation of bacterial cell division: A time and place for it. Curr. Opin. Microbiol. 1, 210-215.
46. Lutkenhaus, J. (2002). Dynamic proteins in bacteria. Curr. Opin. Microbiol. 5, 548-552.
47. Lutkenhaus, J., and Addinall, S.G. (1997). Bacterial cell division and the Z ring. Annu. Rev. Biochem. 66, 93-116.
48. Maniatis, T., Fritsch, E.F., and Sambrook, J. (1982). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
49. Maple, J., Chua, N.H., and Moller, S.G. (2002). The topological specificity factor AtMinE1 is essential for correct plastid division site placement in Arabidopsis. Plant J. 31, 269-277.
50. Margolin, W. (2001). Spatial regulation of cytokinesis in bacteria. Curr. Opin. Microbiol. 4, 647-652.
51. Marrison, J.L., Rutherford, S.M., Robertson, E.J., Lister, C., Dean, C., and Leech, R.M. (1999). The distinctive roles of five different ARC genes in the chloroplast division process in Arabidopsis. Plant J. 18, 651-662.
52. Martin, W., Stoebe, B., Goremykin, V., Hansmann, S., Hasegawa, M., and Kowallik, K.V. (1998). Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393, 162-165.
53. 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.
54. McCarty, J.S., and Walker, G.C. (1994). DnaK mutants defective in ATPase activity are defective in negative regulation of the heat shock response: Expression of mutant DnaK proteins results in filamentation. J. Bacteriol. 176, 764-780.
55. Miernyk, J.A. (2001). The J-domain proteins of Arabidopsis thaliana: An unexpectedly large and diverse family of chaperones. Cell Stress Chaperon. 6, 209-218.
56. Miyagishima, S., Nishida, K., Mori, T., Matsuzaki, M., Higashiyama, T., Kuroiwa, H., and Kuroiwa, T. (2003). A plant-specific dynaminrelated protein forms a ring at the chloroplast division site. Plant Cell 15, 655-665.
57. Mori, T., Kuroiwa, H., Takahara, M., Miyagishima, S., and Kuroiwa, T. (2001). Visualization of an FtsZ ring in chioroplasts of Lilium longiflorum leaves. Plant Cell Physiol. 42, 555-559.
58. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15, 473-497.
59. Nakazawa, M., and Matsui, M. (2003). Selection of hygromycin-resistant Arabidopsis seedlings. Biotechniques 34, 28-30.
60. Osteryoung, K.W., and McAndrew, R.S. (2001). The plastid division machine. Annu. Rev. Plant Physiol. Plant MoL. Biol. 52, 315-333.
61. 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.
62. Osteryoung, K.W., and Vierling, E. (1995). Conserved cell and organelle division. Nature 376, 473-474.
63. Pichoff, S., and Lutkenhaus, J. (2001). Escherichia coli division inhibitor MinCD blocks septation by preventing Z-ring formation. J. Bacteriol. 183, 6630-6635.
64. Pichoff, S., and Lutkenhaus, J. (2002). Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J. 21, 685-693.
65. Pyke, K.A. (1997). The genetic control of plastid division in higher plants. Am. J. Bot. 84, 1017-1027.
66. Pyke, K.A. (1999). Plastid division and development. Plant Cell 11, 549-556.
67. Pyke, K.A., and Leech, R.M. (1992). Chloroplast division and expansion is radically altered by nuclear mutations in Arabidopsis thaliana. Plant Physiol. 99, 1005-1008.
68. Pyke, K.A., and Page, A.M. (1998). Plastid ontogeny during petal development in Arabidopsis. Plant Physiol. 116, 797-803.
69. Pyke, K.A., Rutherford, S.M., Robertson, E.J., and Leech, R.M. (1994). arc6, a fertile Arabidopsis mutant with only two mesophyll cell chioroplasts. Plant Physiol. 106, 1169-1177.
70. Raskin, D.M., and de Boer, P.A.J. (1997). The MinE ring: An FtsZ-independent cell structure required for selection of the correct division site in Escherichia coli. Cell 91, 685-694.
71. RayChaudhuri, D. (1999). ZipA is a MAP-Tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division. EMBO J. 18, 2372-2383.
72. Reddy, S.M.S., Dinkins, R., and Collins, G.B. (2002). Overexpression of the Arabidopsis thaliana MinE1 bacterial division inhibitor homologue gene alters chloroplast size and morphology in transgenic Arabidopsis and tobacco plants. Planta 215, 167-176.
73. Robertson, E.J., Pyke, K.A., and Leech, R.M. (1995). arc6, an extreme chloroplast division mutant of Arabidopsis also alters proplastid proliferation and morphology in shoot and root apices. J. Cell Sci. 108, 2937-2944.
74. Rothfield, L., Justice, S., and Garca-Lara, J. (1999). Bacterial cell division. Annu. Rev. Genet. 33, 423-428.
75. Rutherford, S.M. (1996). The Genetic and Physical Analysis of Mutants of Chloroplast Number and Size in Arabidopsis thaliana. PhD dissertation (York, UK: University of York).
76. Shih, Y.-L., Fu, X., King, G.F., Le, T., and Rothfield, L. (2002). Division site placement in E coli: Mutations that prevent formation of the MinE ring lead to loss of the normal midcell arrest of growth of polar MinD membrane domains. EMBO J. 21, 3347-3357.
77. 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.
78. 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.
79. Sun, Q., and Margolin, W. (1998). FtsZ dynamics during the division cycle of live Escherichia coli cells. J. Bacteriol. 180, 2050-2056.
80. Tusnady, G.E., and Simon, I. (2001). The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849-850.
81. Uehara, T., Matsuzawa, H., and Nishimura, A. (2001). HscA is involved in the dynamics of FtsZ-ring formation in Escherichia coli K12. Genes Cells 6, 803-814.
82. 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.
83. Wakasugi, T., et al. (1997). Complete nucleotide sequence of the chloroplast genome from the ga Chlorella vulgaris: The existence of genes possibly involved in chloroplast division. Proc. Natl. Acad. Sci. USA 94, 5967-5972.
84. Walter, S., and Buchner, J. (2002). Molecular chaperones: Cellular machines for protein folding. Angew. Chem. Int. Ed. Engl. 41, 1098-1113.
85. Wang, D., Kong, D., Wang, Y., Hu, Y., He, Y., and Sun, J. (2003). Isolation of two plastid division ftsZ genes from Chlamydomonas reinhardtii and its evolutionary implication for the role of FtsZ in plastid division. J. Exp. Bot. 54, 1115-1116.
86. Wang, D., Kong, D.D., Ju, C.L., Hu, Y., He, Y.K., and Sun, J.S. (2002). Effects of tobacco plastid division genes NtFtsZ1 and NtFtsZ2 on the division and morphology of chloroplasts. Acta Bot. Sin. 44, 838-844.
87. Whatley, J.M. (1993). The endosymbiotic origin of chloroplasts. Int. Rev. Cytol. 144, 259-299.
88. Xu, Y., and Uberbacher, B.C. (1997). Automated gene identification in iarge-scale genomic sequences. J. Comput. Biol. 4, 325-338.
89. Yamamoto, K., Pyke, K.A., and Kiss, J.Z. (2002). Reduced gravitropism in inflorescence stems and hypocotyls, but not roots, of Arabidopsis mutants with large plastids. Physiol. Plant. 114, 627-636.
90. Yoshimune, K., Yoshimura, T., Nakayama, T., Nishino, T., and Esaki, N. (2002). Hsc62, Hsc56, and GrpE, the third Hsp70 chaperone system of Escherichia coli. Biochem. Biophys. Res. Commun. 293, 1389-1395.
91. Yu, X.C., and Margolin, W. (1999). FtsZ ring clusters in min and partition mutants: Role of both the Min system and the nucieoid in regulating FtsZ ring localization. Mol. Microbiol. 32, 315-326.
92. Zhang, H., and Forde, B.G. (1998). An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407-409.
93. Zhao, C.R., de Boer, P.A.J., and Rothfield, L.I. (1995). Proper placement of the Escherichia coli division site requires two functions that are associated with different domains of the MinE protein. Proc. Natl. Acad. Sci. USA 92, 4313-4317.