Emerging facets of plastid division regulation

Planta

Volumn 237, Issue 2, 2013, Pages 389-398

  Basak, Indranil ^a   Møller, Simon Geir ^a,b,c  

^a ST JOHN'S UNIVERSITY   (United States)

^b STAVANGER UNIVERSITY HOSPITAL   (Norway)

^c UNIVERSITY OF STAVANGER   (Norway)

Author keywords

Plastid division; Protein complexes; Regulation

Indexed keywords

EUKARYOTA; PROKARYOTA;

EID: 84873088646     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-012-1743-6     Document Type: Review

References (88)

1. Adams S, Maple J, Møller SG (2008) Functional conservation of the MIN division homologues of Chlamydomonas reinhardtii. Planta 227: 1199-1211.
2. Addinall SG, Holland B (2002) The tubulin ancestor, FtsZ, draughtsman, designer and driving force for bacterial cytokinesis. J Mol Biol 318: 219-236.
3. Ajjawi I, Coku A, Froehlich JE, Yang Y, Osteryoung KW, Benning C, Last RL (2011) A J-like protein influences fatty acid composition of chloroplast lipids in Arabidopsis. PLoS ONE 6: e25368.
4. 2+-ATPase stimulated by AtMinE1. J Biol Chem 280: 31673-31678.
5. Asano T, Yoshioka Y, Kurei S, Sakamoto W, Machida Y, Sodmergen (2004) A mutation of the CRUMPLED LEAF gene that encodes a protein localized in the outer envelope membrane of plastids affects the pattern of cell division, cell differentiation, and plastid division in Arabidopsis. Plant J 38: 448-459.
6. Bédard J, Jarvis P (2005) Recognition and envelope translocation of chloroplast preproteins. J Exp Bot 56: 2287-2320.
7. Bramhill D (1997) Bacterial cell division. Annu Rev Cell Dev Biol 13: 395-424.
8. Cavalier-Smith T (2000) Membrane heredity and early chloroplast evolution. Trends Plant Sci 5: 174-182.
9. Chan CX, Gross J, Yoon HS, Bhattacharya D (2011) Plastid origin and evolution: new models provide insights into old problems. Plant Physiol 155: 1552-1560.
10. Colletti KS, Tattersall EA, Pyke KA, Froelich JE, Stokes KD, Osteryoung KW (2000) A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol 10: 507-516.
11. de Boer PAJ, Crossley RE, Rothfield LI (1988) Isolation and properties of minB, a complex genetic locus involved in correct placement of the division site in Escherichia coli. J Bacteriol 170: 2106-2112.
12. de Boer PAJ, Crossley RE, Rothfield L (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.
13. Dinkins R, Reddy MS, Leng M, Collins GB (2001) Overexpression of the Arabidopsis thaliana MinD1 gene alters chloroplast size and number in transgenic tobacco plants. Planta 214: 180-188.
14. El-Kafafi El-S, Karamoko M, Pignot-Paintrand I, Grunwald D, Mandaron P, Lerbs-Mache S, Falconet D (2008) Developmentally regulated association of plastid division protein FtsZ1with thylakoid membranes in Arabidopsis thaliana. Biochem J 409: 87-94.
15. Erickson HP, Taylor DW, Taylor KA, Bramhill D (1996) Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc Natl Acad Sci USA 93: 519-523.
16. Fan J, Xu C (2011) Genetic analysis of Arabidopsis mutants impaired in plastid lipid import reveals a role of membrane lipids in chloroplast division. Plant Signal Behav 6: 458-460.
17. Fujiwara MT, Nakamura A, Itoh R, Shimada Y, Yoshida S, Møller SG (2004) Chloroplast division site placement requires dimerization of the ARC11/AtMinD1 protein in Arabidopsis. J Cell Sci 117: 2399-2410.
18. Fujiwara T, Misumi O, Tashiro K, Yoshida Y, Nishida K, Yagisawa F, Imamura S, Yoshida M, Mori T, Tanaka K, Kuroiwa H, Kuroiwa T (2009) Periodic gene expression patterns during the highly synchronized cell nucleus and organelle division cycles in the unicellular red alga Cyanidioschyzon merolae. DNA Res 16: 59-72.
19. Gao H, Kadirjan-Kalbach D, Froehlich JE, Osteryoung KW (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci USA 100: 4328-4333.
20. Gargano D, Maple-Grodem J, Moller SG (2012) In vivo phosphorylation of FtsZ2 in Arabidopsis thaliana. Biochem J (in press).
21. Glynn JM, Yang Y, Vitha S, Schmitz AJ, Hemmes M, Miyagishima SY, Osteryoung KW (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.
22. Hale CA, Meinhardt H, de Boer PA (2001) Dynamic localization cycle of the cell division regulator MinE in Escherichia coli. EMBO J 20: 1563-1572.
23. Hashimoto H (1986) Double ring structure around the constricting neck of the dividing plastids of Avena sativa. Protoplasma 135: 166-172.
24. Hu Z, 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.
25. Hu Z, 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.
26. Hu Z, 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.
27. Hu Z, Gogol EP, Lutkenhaus J (2002) Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc Natl Acad Sci USA 99: 6761-6766.
28. Inoue K (2011) Emerging roles of the chloroplast outer envelope membrane. Trends Plant Sci 16: 550-557.
29. Itoh R, Fujiwara M, Nagata N, 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.
30. Jeong WJ, Park YI, Suh K, Raven JA, Yoo OJ, Liu JR (2002) A large population of small chloroplasts in tobacco leaf cells allows more effective chloroplast movement than a few enlarged chloroplasts. Plant Physiol 129: 112-121.
31. Li C, Wang Y, Liu L, Hu Y, Zhang F, Mergen S, Wang G, Schläppi MR, Chu C (2011) A rice plastidial nucleotide sugar epimerase is involved in galactolipid biosynthesis and improves photosynthetic efficiency. PLoS Genet 7: e1002196.
32. Lopez-Juez E, Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49: 557-577.
33. Lutkenhaus J, Addinall SG (1997) Bacterial cell division and the Z ring. Annu Rev Biochem 66: 93-116.
34. Ma X, Ehrhardt DW, Margolin W (1996) Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. Proc Natl Acad Sci U S A 93: 12998-13003.
35. Maple J, Møller SG (2007) Plastid division coordination across a double-membraned structure. FEBS Lett 581: 2162-2167.
36. Maple J, Møller SG (2010) The complexity and evolution of the plastid-division machinery. Biochem Soc Trans 38: 783-788.
37. Maple J, Chua NH, Møller SG (2002) The topological specificity factor AtMinE1 is essential for correct plastid division site placement in Arabidopsis. Plant J 31: 269-277.
38. Maple J, Fujiwara MT, Kitahata N, Lawson T, Baker NR, Yoshida S, Møller SG (2004) GIANT CHLOROPLAST 1 is essential for correct plastid division in Arabidopsis. Curr Biol 14: 776-781.
39. Maple J, Aldridge C, Møller SG (2005) Plastid division is mediated by combinatorial assembly of plastid division proteins. Plant J 43: 811-823.
40. Maple J, Vojta L, Soll J, Møller SG (2007) ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Rep 8: 293-299.
41. Maple J, Winge P, Tveitaskog AE, Gargano D, Bones AM, Møller SG (2011) Genome-wide gene expression profiles in response to plastid division perturbations. Planta 234: 1055-1063.
42. Margolin W (2000) Themes and variations in prokaryotic cell division. FEMS Microbiol Rev 24: 531-548.
43. Margolin W (2005) FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6: 862-871.
44. McAndrew RS, Olson BJ, Kadirjan-Kalbach DK, Chi-Ham CL, Vitha S, Froehlich JE, Osteryoung KW (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.
45. McFadden GI (1999) Endosymbiosis and evolution of the plant cell. Curr Opin Plant Biol 2: 513-519.
46. Meinhardt H, de Boer PA (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.
47. Miyagishima SY (2011) Mechanism of plastid division: from a bacterium to an organelle. Plant Physiol 155: 1533-1544.
48. Miyagishima SY, Froehlich JE, Osteryoung KW (2006) PDV1 and PDV2 mediate recruitment of the dynamin-related protein ARC5 to the plastid division site. Plant Cell 18: 2517-2530.
49. Miyagishima SY, Nakanishi H, Kabeya Y (2011) Structure, regulation, and evolution of the plastid division machinery. Int Rev Cell Mol Biol 291: 115-153.
50. Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (2003) A plant-specific dynamin-related protein forms a ring at the chloroplast division site. Plant Cell 15: 655-665.
51. Miyagishima SY, Nozaki H, Nishida K, Nishida K, Matsuzaki M, Kuroiwa T (2004) Two types of FtsZ proteins in mitochondria and red-lineage chloroplasts: the duplication of FtsZ is implicated in endosymbiosis. J Mol Evol 58: 291-303.
52. Nakanishi H, Suzuki K, Kabeya Y, Miyagishima SY (2009) Plant-specific protein MCD1 determines the site of chloroplast division in concert with bacteria-derived MinD. Curr Biol 19: 151-156.
53. Okazaki K, Kabeya Y, Suzuki K, Mori T, Ichikawa T, Matsui M, Nakanishi H, Miyagishima SY (2009) The PLASTID DIVISION 1 and 2 components of the chloroplast division machinery determine the rate of chloroplast division in land plant cell differentiation. Plant Cell 21: 1769-1780.
54. Olson BJ, Wang Q, Osteryoung KW (2010) GTP-dependent heteropolymer formation and bundling of chloroplast AtFtsZ1 and AtFtsZ2. J Biol Chem 285: 20634-20643.
55. Osawa M, Anderson DE, Erickson HP (2008) Reconstitution of contractile FtsZ rings in liposomes. Science 320: 792-794.
56. Osteryoung KW, McAndrew RS (2001) The plastid division machine. Annu Rev Plant Physiol Plant Mol Biol 52: 315-333.
57. Osteryoung KW, Vierling E (1995) Conserved cell and organelle division. Nature 376: 473-474.
58. Osteryoung KW, Stokes KD, Rutherford SM, Percival AL, Lee WY (1998) Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial FtsZ. Plant Cell 10: 1991-2004.
59. Pucadyil TJ, Schmid SL (2008) Real-time visualization of dynamin-catalyzed membrane fission and vesicle release. Cell 135: 1263-1275.
60. Pyke KA (1997) The genetic control of plastid division in higher plants. Am J Bot 84: 1017-1027.
61. Pyke KA (1999) Plastid division and development. Plant Cell 11: 549-556.
62. Pyke KA, Leech RM (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol 104: 201-207.
63. Pyke KA, Rutherford SM, Robertson EJ, Leech RM (1994) arc6, a fertile Arabidopsis mutant with only two mesophyll cell chloroplasts. Plant Physiol 106: 1169-1177.
64. Raynaud C, Cassier-Chauvat C, Perennes C, Bergounioux C (2004) An Arabidopsis homolog of the bacterial cell division inhibitor SulA is involved in plastid division. Plant Cell 16: 1801-1811.
65. Raynaud C, Perennes C, Reuzeau C, Catrice O, Brown S, Bergounioux C (2005) Cell and plastid division are coordinated through the prereplication factor AtCDT1. Proc Natl Acad Sci USA 102: 8216-8221.
66. Romberg L, Levin PA (2003) Assembly dynamics of the bacterial cell division protein FtsZ: poised at the edge of stability. Annu Rev Microbiol 57: 125-154.
67. Rothfield LI, Justice SS (1997) Bacterial cell division: the cycle of the ring. Cell 88: 581-584.
68. S El-Kafafi, Mukherjee S, El-shami M, Putaux JL, Block MA, Pignot-Paintrand I, Lerbs-Mache S, Falconet D (2005) The plastid division proteins, AtFtsZ1 and AtFtsZ2, differ in their biochemical properties and sub-plastidial localization. Biochem J 387: 669-676.
69. Schmitz AJ, Glynn JM, Olson BJSC, Stokes KD, Osteryoung KW (2009) Arabidopsis AtFtsZ2-1 and AtFtsZ2-2 are functionally redundant, but FtsZ-based plastid division is not essential for chloroplast partitioning or plant growth and development. Mol Plant 2: 1211-1222.
70. Seguí-Simarro JM, Staehelin LA (2009) Mitochondrial reticulation in shoot apical meristem cells of Arabidopsis provides a mechanism for homogenization of mtDNA prior to gamete formation. Plant Signal Behav 4: 168-171.
71. Shimada H, Koiyumi M, Kuroki K, Mochiyuki M, Fujimoto H, Ohta H, Masuda T, 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.
72. Šimková K, Kim C, Gacek K, Baruah A, Laloi C, Apel K (2012) The chloroplast division mutant caa33 of Arabidopsis thaliana reveals the crucial impact of chloroplast homeostasis on stress acclimation and retrograde plastid-to-nucleus signalling. Plant J 69: 701-712.
73. Smith AG, Johnson CB, Vitha S, Holzenburg A (2010) Plant AtFtsZ1 and AtFtsZ2 expressed in a eukaryotic host: GTPase activity and self-assembly. FEBS Lett 584: 166-172.
74. Smith AG, Johnson CB, Vitha S, Holzenburg A (2011) Oligomerization of plant FtsZ1 and FtsZ2 plastid division proteins. Arch Biochem Biophys 513: 94-101.
75. Stokes KD, Osteryoung KW (2003) Early divergence of the AtFtsZ1 and AtFtsZ2 plastid division gene families in photosynthetic eukaryotes. Gene 27: 97-108.
76. Sureka K, Hossain T, Mukherjee P, Chatterjee P, Datta P, Kundu M, Basu J (2010) Novel role of phosphorylation-dependent interaction between FtsZ and FipA in mycobacterial cell division. PLoS ONE 5: e8590.
77. Szeto TH, Rowland SL, Rothfield LI, King GF (2002) Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts. Proc Natl Acad Sci USA 99: 15693-15698.
78. Takahara M, Takahashi H, Matsunaga S, Miyagishima S, Sakai A, Kawano S, Kuroiwa T (2000) A putative mitochondrial ftsZ gene is encoded in the unicellular primitive red alga Cyanidioschyzon merola. Mol Gen Genet 264: 452-460.
79. Tetlow IJ, Morell MK, Emes MJ (2004) Recent developments in understanding the regulation of starch metabolism in higher plants. J Exp Bot 55: 2131-45.
80. Thakur M, Chakraborti PK (2006) GTPase activity of mycobacterial FtsZ is impaired due to its transphosphorylation by the eukaryotic-type Ser/Thr kinase, PknA. J Biol Chem 281: 40107-40113.
81. Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW (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.
82. Warnock DE, Hinshaw JE, Schmid SL (1996) Dynamin self-assembly stimulates its GTPase activity. J Biol Chem 271: 22310-22314.
83. Waters M, Pyke K (2005) Plastid development and differentiation. In: Møller SG (ed) Plastids. Annual Plant Review 13. Blackwell Scientific Publications, Oxford, pp 30-59.
84. Wu GZ, Xue HW (2010) Arabidopsis β-ketoacyl-[acyl carrier protein] synthase i is crucial for fatty acid synthesis and plays a role in chloroplast division and embryo development. Plant Cell 22: 3726-3744.
85. Yang Y, Sage TL, Liu Y, Ahmad TR, Marshall WF, Shiu SH, Froehlich JE, Imre KM, Osteryoung KW (2011) CLUMPED CHLOROPLASTS 1 is required for plastid separation in Arabidopsis. Proc Natl Acad Sci USA 108: 18530-18535.
86. Yun MS, Kawagoe Y (2010) Septum formation in amyloplasts produces compound granules in the rice endosperm and is regulated by plastid division proteins. Plant Cell Physiol 51: 1469-1479.
87. Zhang M, Hu Y, Jia J, Li D, Zhang R, Gao H, He Y (2009) CDP1, a novel component of chloroplast division site positioning system in Arabidopsis. Cell Res 19: 877-886.
88. Zhou H, Lutkenhaus J (2004) The switch I and II regions of MinD are required for binding and activating MinC. J Bacteriol 186: 1546-1555.