Chloroplast division protein ARC3 regulates chloroplast FtsZ-ring assembly and positioning in Arabidopsis through interaction with FtsZ2

Plant Cell

Volumn 25, Issue 5, 2013, Pages 1787-1802

  Zhang, Min ^a   Schmitz, Aaron J ^a,b   Kadirjan Kalbach, Deena K ^a   TerBush, Allan D ^a   Osteryoung, Katherine W ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84879468064     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.111047     Document Type: Article

References (79)

1. 2+-ATPase stimulated by AtMinE1. J. Biol. Chem. 280: 31673-31678.
2. Bi, E.F., and Lutkenhaus, J. (1991). FtsZ ring structure associated with division in Escherichia coli. Nature 354: 161-164.
3. Bi, E., and Lutkenhaus, J. (1993). Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J. Bacteriol. 175: 1118-1125.
4. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
5. 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.
6. Dajkovic, A., Lan, G., Sun, S.X., Wirtz, D., and Lutkenhaus, J. (2008). MinC spatially controls bacterial cytokinesis by antagonizing the scaffolding function of FtsZ. Curr. Biol. 18: 235-244.
7. de Boer, P.A.J. (2010). Advances in understanding E. coli cell fission. Curr. Opin. Microbiol. 13: 730-737.
8. 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.
9. El-Kafafi, 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 localization. Biochem. J. 387: 669-676.
10. Erickson, H.P., Taylor, D.W., Taylor, K.A., and Bramhill, D. (1996). Bacterial cell division protein FtsZ assembles into protofilament sheets andminirings, structural homologs of tubulin polymers. Proc. Natl. Acad. Sci. USA 93: 519-523.
11. Forsburg, S.L. (1993). Comparison of Schizosaccharomyces pombe expression systems. Nucleic Acids Res. 21: 2955-2956.
12. 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.
13. Fujiwara, M.T., Hashimoto, H., Kazama, Y., Abe, T., Yoshida, S., Sato, N., and Itoh, R.D. (2008). The assembly of the FtsZ ring at the mid-chloroplast division site depends on a balance between the activities of AtMinE1 and ARC11/AtMinD1. Plant Cell Physiol. 49: 345-361.
14. Fujiwara, M.T., Nakamura, A., Itoh, R., Shimada, Y., Yoshida, S., and Møller, S.G. (2004). Chloroplast division site placement requires dimerization of the ARC11/AtMinD1 protein in Arabidopsis. J. Cell Sci. 117: 2399-2410.
15. Fujiwara, M.T., Sekine, K., Yamamoto, Y.Y., Abe, T., Sato, N., and Itoh, R.D. (2009). Live imaging of chloroplast FtsZ1 filaments, rings, spirals, and motile dot structures in the AtMinE1 mutant and overexpressor of Arabidopsis thaliana. Plant Cell Physiol. 50: 1116-1126.
16. Gao, H.B., 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.
17. Glynn, J.M., Froehlich, J.E., and Osteryoung, K.W. (2008). Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20: 2460-2470.
18. Glynn, J.M., Miyagishima, S.Y., Yoder, D.W., Osteryoung, K.W., and Vitha, S. (2007). Chloroplast division. Traffic 8: 451-461.
19. Glynn, J.M., Yang, Y., Vitha, S., Schmitz, A.J., Hemmes, M., Miyagishima, S.Y., and Osteryoung, K.W. (2009). PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis. Plant J. 59: 700-711.
20. Gray, M.W. (1992). The endosymbiont hypothesis revisited. Int. Rev. Cytol. 141: 233-357.
21. Hu, Z., Gogol, E.P., and Lutkenhaus, J. (2002). Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc. Natl. Acad. Sci. USA 99: 6761-6766.
22. Hu, Z., and Lutkenhaus, J. (1999). Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE. Mol. Microbiol. 34: 82-90.
23. Hu, Z., and Lutkenhaus, J. (2001). Topological regulation of cell division in E. coli. Spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. Mol. Cell 7: 1337-1343.
24. Hu, Z., and Lutkenhaus, J. (2003). A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol. Microbiol. 47: 345-355.
25. 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.
26. 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.
27. Leech, R.M., Thomson, W.W., and Plattaloia, K.A. (1981). Observations on the mechanism of chloroplast division in higher plants. New Phytol. 87: 1-9.
28. Lutkenhaus, J. (2007). Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu. Rev. Biochem. 76: 539-562.
29. Lutkenhaus, J. (2008). Min oscillation in bacteria. Adv. Exp. Med. Biol. 641: 49-61.
30. Maple, J., Aldridge, C., and Møller, S.G. (2005). Plastid division is mediated by combinatorial assembly of plastid division proteins. Plant J. 43: 811-823.
31. Maple, J., Chua, N.H., and Møller, S.G. (2002). The topological specificity factor AtMinE1 is essential for correct plastid division site placement in Arabidopsis. Plant J. 31: 269-277.
32. Maple, J., and Møller, S.G. (2007). Interdependency of formation and localisation of the Min complex controls symmetric plastid division. J. Cell Sci. 120: 3446-3456.
33. Maple, J., Vojta, L., Soll, J., and Møller, S.G. (2007). ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Rep. 8: 293-299.
34. Margolin, W. (2005). FtsZ and the division of prokaryotic cells and organelles. Nat. Rev. Mol. Cell Biol. 6: 862-871.
35. 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.
36. Mazouni, K., Domain, F., Cassier-Chauvat, C., and Chauvat, F. (2004). Molecular analysis of the key cytokinetic components of cyanobacteria: FtsZ, ZipN and MinCDE. Mol. Microbiol. 52: 1145-1158.
37. 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.
38. McAndrew, R.S., Olson, B.J., Kadirjan-Kalbach, D.K., Chi-Ham, C.L., Vitha, S., Froehlich, J.E., and Osteryoung, K.W. (2008). In vivo quantitative relationship between plastid division proteins FtsZ1 and FtsZ2 and identification of ARC6 and ARC3 in a native FtsZ complex. Biochem. J. 412: 367-378.
39. Meinhardt, H., and de Boer, P.A.J. (2001). Pattern formation in Escherichia coli: A model for the pole-to-pole oscillations of Min proteins and the localization of the division site. Proc. Natl. Acad. Sci. USA 98: 14202-14207.
40. Mingorance, J., Tadros, M., Vicente, M., González, J.M., Rivas, G., and Vélez, M. (2005). Visualization of single Escherichia coli FtsZ filament dynamics with atomic force microscopy. J. Biol. Chem. 280: 20909-20914.
41. Miyagishima, S.Y. (2011). Mechanism of plastid division: From a bacterium to an organelle. Plant Physiol. 155: 1533-1544.
42. Miyagishima, S.Y., Froehlich, J.E., and Osteryoung, K.W. (2006). PDV1 and PDV2 mediate recruitment of the dynamin-related protein ARC5 to the plastid division site. Plant Cell 18: 2517-2530.
43. Nakanishi, H., Suzuki, K., Kabeya, Y., and Miyagishima, S.Y. (2009). Plant-specific protein MCD1 determines the site of chloroplast division in concert with bacteria-derived MinD. Curr. Biol. 19: 151-156.
44. Neff, M.M., Neff, J.D., Chory, J., and Pepper, A.E. (1998). dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: Experimental applications in Arabidopsis thaliana genetics. Plant J. 14: 387-392.
45. Okazaki, K., Kabeya, Y., and Miyagishima, S.Y. (2010). The evolution of the regulatory mechanism of chloroplast division. Plant Signal. Behav. 5: 164-167.
46. Olson, B.J.S.C., Wang, Q.A., and Osteryoung, K.W. (2010). GTPdependent heteropolymer formation and bundling of chloroplast FtsZ1 and FtsZ2. J. Biol. Chem. 285: 20634-20643.
47. Osawa, M., Anderson, D.E., and Erickson, H.P. (2009). Curved FtsZ protofilaments generate bending forces on liposome membranes. EMBO J. 28: 3476-3484.
48. Osteryoung, K.W., and McAndrew, R.S. (2001). The plastid division machine. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52: 315-333.
49. 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.
50. Osteryoung, K.W., and Vierling, E. (1995). Conserved cell and organelle division. Nature 376: 473-474.
51. Park, K.T., Wu, W., Lovell, S., and Lutkenhaus, J. (2012). Mechanism of the asymmetric activation of the MinD ATPase by MinE. Mol. Microbiol. 85: 271-281.
52. Pichoff, S., and Lutkenhaus, J. (2001). Escherichia coli division inhibitor MinCD blocks septation by preventing Z-ring formation. J. Bacteriol. 183: 6630-6635.
53. Plattaloia, K.A., and Thomson, W.W. (1977). Chloroplast development in young sesame plants. New Phytol. 78: 599-605.
54. Popp, D., Iwasa, M., Narita, A., Erickson, H.P., and Maéda, Y. (2009). FtsZ condensates: An in vitro electron microscopy study. Biopolymers 91: 340-350.
55. Pyke, K.A. (1999). Plastid division and development. Plant Cell 11: 549-556.
56. Pyke, K.A., and Leech, R.M. (1991). Rapid image analysis screening procedure for identifying chloroplast number mutants in mesophyll cells of Arabidopsis thaliana (L.) Heynh. Plant Physiol. 96: 1193-1195.
57. 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.
58. Pyke, K.A., and Leech, R.M. (1994). A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol. 104: 201-207.
59. Raskin, D.M., and de Boer, P.A.J. (1999). Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc. Natl. Acad. Sci. USA 96: 4971-4976.
60. Rowland, S.L., Fu, X., Sayed, M.A., Zhang, Y., Cook, W.R., and Rothfield, L.I. (2000). Membrane redistribution of the Escherichia coli MinD protein induced by MinE. J. Bacteriol. 182: 613-619.
61. Schmitz, A.J., Glynn, J.M., Olson, B.J.S.C., Stokes, K.D., and Osteryoung, K.W. (2009). Arabidopsis FtsZ2-1 and FtsZ2-2 are functionally redundant, but FtsZ-based plastid division is not essential for chloroplast partitioning or plant growth and development. Mol. Plant 2: 1211-1222.
62. C)/MinD. Mol. Microbiol. 72: 410-424.
63. N in E. coli suggests how MinC disrupts Z rings. Mol. Microbiol. 75: 1285-1298.
64. Shimada, H., Koizumi, M., Kuroki, K., Mochizuki, M., Fujimoto, H., Ohta, H., Masuda, T., and Takamiya, K. (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.
65. Shiomi, D., and Margolin, W. (2007). The C-terminal domain of MinC inhibits assembly of the Z ring in Escherichia coli. J. Bacteriol. 189: 236-243.
66. Smith, A.G., Johnson, C.B., Vitha, S., and Holzenburg, A. (2010). Plant FtsZ1 and FtsZ2 expressed in a eukaryotic host: GTPase activity and self-assembly. FEBS Lett. 584: 166-172.
67. Srinivasan, R., Mishra, M., Wu, L.F., Yin, Z.C., and Balasubramanian, M.K. (2008). The bacterial cell division protein FtsZ assembles into cytoplasmic rings in fission yeast. Genes Dev. 22: 1741-1746.
68. 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.
69. Sussman, M.R., Amasino, R.M., Young, J.C., Krysan, P.J., and Austin-Phillips, S. (2000). The Arabidopsis knockout facility at the University of Wisconsin-Madison. Plant Physiol. 124: 1465-1467.
70. TerBush, A.D., and Osteryoung, K.W. (2012). Distinct functions of chloroplast FtsZ1 and FtsZ2 in Z-ring structure and remodeling. J. Cell Biol. 199: 623-637.
71. 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.
72. Vitha, S., McAndrew, R.S., and Osteryoung, K.W. (2001). FtsZ ring formation at the chloroplast division site in plants. J. Cell Biol. 153: 111-120.
73. Warrens, A.N., Jones, M.D., and Lechler, R.I. (1997). Splicing by overlap extension by PCR using asymmetric amplification: An improved technique for the generation of hybrid proteins of immunological interest. Gene 186: 29-35.
74. Wilson, M.E., Jensen, G.S., and Haswell, E.S. (2011). Two mechanosensitive channel homologs influence division ring placement in Arabidopsis chloroplasts. Plant Cell 23: 2939-2949.
75. 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.
76. Yang, Y., Sage, T.L., Liu, Y., Ahmad, T.R., Marshall, W.F., Shiu, S.H., Froehlich, J.E., Imre, K.M., and Osteryoung, K.W. (2011). CLUMPED CHLOROPLASTS 1 is required for plastid separation in Arabidopsis. Proc. Natl. Acad. Sci. USA 108: 18530-18535.
77. 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.
78. Yoshida, Y., Miyagishima, S.Y., Kuroiwa, H., and Kuroiwa, T. (2012). The plastid-dividing machinery: Formation, constriction and fission. Curr. Opin. Plant Biol. 15: 714-721.
79. Zhang, M., Hu, Y., Jia, J.J., Li, D.P., Zhang, R.J., Gao, H.B., and He, Y.K. (2009). CDP1, a novel component of chloroplast division site positioning system in Arabidopsis. Cell Res. 19: 877-886.