FtsZ in chloroplast division: Structure, function and evolution

Current Opinion in Cell Biology

Volumn 25, Issue 4, 2013, Pages 461-470

  TerBush, Allan D ^a   Yoshida, Yamato ^a   Osteryoung, Katherine W ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FTSZ PROTEIN; GUANOSINE TRIPHOSPHATASE;

CELL DIVISION; CHLOROPLAST; CHLOROPLAST DIVISION; EMBRYOPHYTA; ENDOPLASMIC RETICULUM; ENDOSYMBIOSIS; ENZYME ACTIVITY; GENE DUPLICATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PHAGOCYTOSIS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW;

BACTERIAL PROTEINS; CHLOROPLAST PROTEINS; CHLOROPLASTS; CYANOBACTERIA; EVOLUTION, MOLECULAR; GENE DUPLICATION; PHOTOSYNTHESIS; PLANT CELLS; PLANTS;

BACTERIA (MICROORGANISMS); CYANOBACTERIA; EMBRYOPHYTA; EUKARYOTA;

EID: 84883466241     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2013.04.006     Document Type: Review

References (66)

1. Leech R.M., Baker N.R. The development of photosynthetic capacity in leaves. The Growth and Functioning of Leaves 1983, Cambridge University Press. J.E. Dale, F.L. Milthorpe (Eds.).
2. Gould S.B., Waller R.F., McFadden G.I. Plastid evolution. Annu Rev Plant Biol 2008, 59:491-517.
3. Miyagishima S., Nakanishi H., Kabeya Y. Structure, regulation, and evolution of the plastid division machinery. Int Rev Cell Mol Biol 2011, 291:115-153.
4. Falconet D. Origin, evolution and division of plastids. Photosynthesis: Plastid Biology, Energy Conversion and Carbon Assimilation 2012, Vol 34. Springer, Dordrecht/New York, 35-61.
5. Osteryoung K.W., Nunnari J. The division of endosymbiotic organelles. Science 2003, 302:1698-1704.
6. Yoshida Y., Kuroiwa H., Misumi O., Yoshida M., Ohnuma M., Fujiwara T., Yagisawa F., Hirooka S., Imoto Y., Matsushita K., et al. Chloroplasts divide by contraction of a bundle of nanofilaments consisting of polyglucan. Science 2010, 329:949-953.
7. Nakanishi H., Suzuki K., Kabeya Y., Miyagishima S. Plant-specific protein MCD1 determines the site of chloroplast division in concert with bacteria-derived MinD. Curr Biol 2009, 19:151-156.
8. de Pater S., Caspers M., Kottenhagen M., Meima H., ter Stege R., de Vetten N. Manipulation of starch granule size distribution in potato tubers by modulation of plastid division. Plant Biotechnol J 2006, 4:123-134.
9. Yun M.S., Kawagoe Y. Amyloplast division progresses simultaneously at multiple sites in the endosperm of rice. Plant Cell Physiol 2009, 50:1617-1626.
10. Osawa M., Anderson D.E., Erickson H.P. Reconstitution of contractile FtsZ rings in liposomes. Science 2008, 320:792-794.
11. Osawa M., Anderson D.E., Erickson H.P. Curved FtsZ protofilaments generate bending forces on liposome membranes. EMBO J 2009, 28:3476-3484.
12. Adams D.W., Errington J. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 2009, 7:642-653.
13. Erickson H.P., Anderson D.E., Osawa M. FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 2010, 74:504-528.
14. Miyagishima S., Nozaki H., Nishida K., Nishida K., Matsuzaki M., Kuroiwa T. Two types of FtsZ proteins in mitochondria and red-lineage chloroplasts: the duplication of FtsZ is implicated in endosymbiosis. J Mol Evol 2004, 58:291-303.
15. Osteryoung K.W., McAndrew R.S. The plastid division machine. Annu Rev Plant Physiol Plant Mol Biol 2001, 52:315-333.
16. Osteryoung K.W., Stokes K.D., Rutherford S.M., Percival A.L., Lee W.Y. Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell 1998, 10:1991-2004.
17. Osteryoung K.W., Vierling E. Conserved cell and organelle division. Nature 1995, 376:473-474.
18. Fujiwara M., Yoshida S. Chloroplast targeting of chloroplast division FtsZ2 proteins in Arabidopsis. Biochem Biophys Res Commun 2001, 287:462-467.
19. McAndrew R.S., Froehlich J.E., Vitha S., Stokes K.D., Osteryoung K.W. Colocalization of plastid division proteins in the chloroplast stromal compartment establishes a new functional relationship between FtsZ1 and FtsZ2 in higher plants. Plant Physiol 2001, 127:1656-1666.
20. Vitha S., McAndrew R.S., Osteryoung K.W. FtsZ ring formation at the chloroplast division site in plants. J Cell Biol 2001, 153:111-119.
21. Hopkins J.F., Spencer D.F., Laboissiere S., Neilson J.A.D., Eveleigh R.J.M., Durnford D.G., Gray M.W., Archibald J.M. Proteomics reveals plastid- and periplastid-targeted proteins in the chlorarachniophyte alga Bigelowiella natans. Genome Biol Evol 2012, 4:1391-1406.
22. Sato M., Nishikawa T., Kajitani H., Kawano S. Conserved relationship between FtsZ and peptidoglycan in the cyanelles of Cyanophora paradoxa similar to that in bacterial cell division. Planta 2007, 227:177-187.
23. Takano H., Takechi K. Plastid peptidoglycan. Biochim Biophys Acta 2010, 1800:144-151.
24. Webster W.A.J., McFadden G.I. Organelle division: dynamin-related proteins in apicomplexans. Curr Biol 2009, 19:R334-R336.
25. Lowe J., Amos L.A. Crystal structure of the bacterial cell-division protein FtsZ. Nature 1998, 391:203-206.
26. Oliva M.A., Cordell S.C., Lowe J. Structural insights into FtsZ protofilament formation. Nat Struct Mol Biol 2004, 11:1243-1250.
27. Ma X.L., Margolin W. Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol 1999, 181:7531-7544.
28. Nishikawa T., Kajitani H., Sato M., Mogi Y., Moriyanna Y., Kawano S. Isolation of chloroplast FtsZ and AtpC, and analysis of protein targeting into the complex chloroplast of the haptophyte Pavlova pinguis. Cytologia (Tokyo) 2010, 75:203-210.
29. Nishikawa T., Moriyama Y., Sato M., Sano T., Hasezawa S., Ota S., Kawano S. Isolation of mitochondrial and plastid ftsZ genes and analysis of the organelle targeting sequence in the diatom Chaetoceros neogracile (Diatoms, Bacillariophyceae). Phycol Res 2012, 60:123-136.
30. Vieler A., Wu G., Tsai C.H., Bullard B., Cornish A.J., Harvey C., Reca I.B., Thornburg C., Achawanantakun R., Buehl C.J., et al. Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779. PLoS Genet 2012, 8:e1003064.
31. Vitha S., Froehlich J.E., Koksharova O., Pyke K.A., van Erp H., Osteryoung K.W. ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 2003, 15:1918-1933.
32. Maple J., Aldridge C., Moller S.G. Plastid division is mediated by combinatorial assembly of plastid division proteins. Plant J 2005, 43:811-823.
33. Stokes K.D., McAndrew R.S., Figueroa R., Vitha S., Osteryoung K.W. Chloroplast division and morphology are differentially affected by overexpression of FtsZ1 and FtsZ2 genes in Arabidopsis. Plant Physiol 2000, 124:1668-1677.
34. McAndrew R.S., Olson B.J.S.C., Kadirjan-Kalbach D.K., Chi-Ham C.L., Vitha S., Froehlich J.E., Osteryoung K.W. In vivo quantitative relationship between plastid division proteins FtsZ1 and FtsZ2 and identification of ARC6 and ARC3 in a native FtsZ complex. Biochem J 2008, 412:367-378.
35. Schmitz A.J., Glynn J.M., Olson B.J.S.C., Stokes K.D., Osteryoung K.W. 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 2009, 2:1211-1222.
36. Maple J., Vojta L., Soll J., Moller S.G. ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Rep 2007, 8:293-299.
37. Osawa M., Erickson H.P. Inside-out Z rings - constriction with and without GTP hydrolysis. Mol Microbiol 2011, 81:571-579.
38. Smith A.G., Johnson C.B., Vitha S., Holzenburg A. Plant FtsZ1 and FtsZ2 expressed in a eukaryotic host: GTPase activity and self-assembly. FEBS Lett 2010, 584:166-172.
39. Olson B.J.S.C., Wang Q.A., Osteryoung K.W. GTP-dependent heteropolymer formation and bundling of chloroplast FtsZ1 and FtsZ2. J Biol Chem 2010, 285:20634-20643.
40. Lohse S., Hause B., Hause G., Fester T. FtsZ characterization and immunolocalization in the two phases of plastid reorganization in arbuscular mycorrhizal roots of Medicago truncatula. Plant Cell Physiol 2006, 47:1124-1134.
41. El-Kafafi E.S., Mukherjee S., El-Shami M., Putaux J.L., Block M.A., Pignot-Paintrand I., Lerbs-Mache S., Falconet D. The plastid division proteins, FtsZ1 and FtsZ2, differ in their biochemical properties and sub-plastidial localization. Biochem J 2005, 387:669-676.
42. Smith A.G., Johnson C.B., Vitha S., Holzenburg A. Oligomerization of plant FtsZ1 and FtsZ2 plastid division proteins. Arch Biochem Biophys 2011, 513:94-101.
43. TerBush A.D., Osteryoung K.W. Distinct functions of chloroplast FtsZ1 and FtsZ2 in Z-ring structure and remodeling. J Cell Biol 2012, 199:623-637.
44. Buske P.J., Levin P.A. Extreme C terminus of bacterial cytoskeletal protein FtsZ plays fundamental role in assembly independent of modulatory proteins. J Biol Chem 2012, 287:10945-10957.
45. Yoder D.W., Kadirjan-Kalbach D., Olson B.J.S.C., Miyagishima S., DeBlasio S.L., Hangarter R.P., Osteryoung K.W. Effects of mutations in Arabidopsis FtsZ1 on plastid division, FtsZ ring formation and positioning, and FtsZ filament morphology in vivo. Plant Cell Physiol 2007, 48:775-791.
46. El-Kafafi E.S., Karamoko M., Pignot-Paintrand I., Grunwald D., Mandaron P., Lerbs-Mache S., Falconet D. Developmentally regulated association of plastid division protein FtsZ1 with thylakoid membranes in Arabidopsis thaliana. Biochem J 2008, 409:87-94.
47. Karamoko M., El-Kafafi E.S., Mandaron P., Lerbs-Mache S., Falconet D. Multiple FtsZ2 isoforms involved in chloroplast division and biogenesis are developmentally associated with thylakoid membranes in Arabidopsis. FEBS Lett 2011, 585:1203-1208.
48. Yun M.S., Kawagoe Y. Septum formation in amyloplasts produces compound granules in the rice endosperm and is regulated by plastid division proteins. Plant Cell Physiol 2010, 51:1469-1479.
49. Kiessling J., Martin A., Gremillon L., Rensing S.A., Nick P., Sarnighausen E., Decker E.L., Reski R. Dual targeting of plastid division protein FtsZ to chloroplasts and the cytoplasm. EMBO Rep 2004, 5:889-894.
50. Martin A., Lang D., Heckmann J., Zimmer A.D., Vervliet-Scheebaum M., Reski R. A uniquely high number of ftsZ genes in the moss Physcomitrella patens. Plant Biol 2009, 11:744-750.
51. Miyagishima S., Suzuki K., Okazaki K., Kabeya Y. Expression of the nucleus-encoded chloroplast division genes and proteins regulated by the algal cell cycle. Mol Biol Evol 2012, 29:2957-2970.
52. Gargano D., Maple-Grodem J., Moller S.G. In vivo phosphorylation of FtsZ2 in Arabidopsis thaliana. Biochem J 2012, 446:517-521.
53. Balmer Y., Koller A., del Val G., Manieri W., Schurmann P., Buchanan B.B. Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci U S A 2003, 100:370-375.
54. Beech P.L., Nheu T., Schultz T., Herbert S., Lithgow T., Gilson P.R., McFadden G.I. Mitochondrial FtsZ in a chromophyte alga. Science 2000, 287:1276-1279.
55. Gilson P.R., Yu X.C., Hereld D., Barth C., Savage A., Kiefel B.R., Lay S., Fisher P.R., Margolin W., Beech P.L. Two Dictyostelium orthologs of the prokaryotic cell division protein FtsZ localize to mitochondria and are required for the maintenance of normal mitochondrial morphology. Eukaryot Cell 2003, 2:1315-1326.
56. Kiefel B.R., Gilson P.R., Beech P.L. Diverse eukaryotes have retained mitochondrial homologues of the bacterial division protein FtsZ. Protist 2004, 155:105-115.
57. Nishida K., Takahara M., Miyagishima S., Kuroiwa H., Matsuzaki M., Kuroiwa T. Dynamic recruitment of dynamin for final mitochondrial severance in a primitive red alga. Proc Natl Acad Sci U S A 2003, 100:2146-2151.
58. Yoshida Y., Kuroiwa H., Hirooka S., Fujiwara T., Ohnuma M., Yoshida M., Misumi O., Kawano S., Kuroiwa T. The bacterial ZapA-like protein ZED is required for mitochondrial division. Curr Biol 2009, 19:1491-1497.
59. Huecas S., Schaffner-Barbero C., Garcia W., Yebenes H., Palacios J.M., Diaz J.F., Menendez M., Andreu J.M. The interactions of cell division protein FtsZ with guanine nucleotides. J Biol Chem 2007, 282:37515-37528.
60. Fu G., Huang T., Buss J., Coltharp C., Hensel Z., Xiao J. In vivo structure of the E. coli FtsZ-ring revealed by photoactivated localization microscopy (PALM). PLoS ONE 2010, 5:e12680.
61. Li Z., Trimble M.J., Brun Y.V., Jensen G.J. The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J 2007, 26:4694-4708.
62. Strauss M.P., Liew A.T.F., Turnbull L., Whitchurch C.B., Monahan L.G., Harry E.J. 3D-SIM super resolution microscopy reveals a bead-like arrangement for FtsZ and the division machinery: implications for triggering cytokinesis. PLoS Biol 2012, 10:e1001389.
63. Yang Y., Sage T.L., Liu Y., Ahmad T.R., Marshall W.F., Shiu S.H., Froehlich J.E., Imre K.M., Osteryoung K.W. CLUMPED CHLOROPLASTS 1 is required for plastid separation in Arabidopsis. Proc Natl Acad Sci U S A 2011, 108:18530-18535.
64. Kelley L.A., Sternberg M.J.E. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 2009, 4:363-371.
65. Wass M.N., Kelley L.A., Sternberg M.J.E. 3DLigandSite: predicting ligand-binding sites using similar structures. Nucleic Acids Res 2010, 38:W469-W473.
66. Zhang M., Schmitz A.J., Kadirjan-Kalbach D., TerBush A.D., Osteryoung K.W. Chloroplast division protein ARC3 regulates chloroplast FtsZ-ring assembly and positioning in Arabidopsis through interaction with FtsZ2. Plant Cell 2013, in press.