Home LiteratureArticle Details
PMID: 11595800 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Plastid division is driven by a complex mechanism that involves differential transition of the bacterial and eukaryotic division rings.

The Plant cell ·Vol. 13 ·No. 10 ·2001-10-00 ·Pages 2257-68

Miyagishima Sy, Takahara M, Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T

Abstract

During plastid division, two structures have been detected at the division site in separate analyses. The plastid-dividing ring can be detected by transmission electron microscopy as two (or three) electron-dense rings: an outer ring on the cytosolic face of the outer envelope, occasionally a middle ring in the intermembrane space, and an inner ring on the stromal face of the inner envelope. The FtsZ ring, which plays a central role in bacterial division, also is involved in plastid division and is believed to have descended to plastids from cyanobacterial endosymbiosis. The relationship between the two structures is not known, although there is discussion regarding whether they are identical. Biochemical and immunocytochemical investigations, using synchronized chloroplasts of the red alga Cyanidioschyzon merolae, showed that the plastid FtsZ ring is distinct and separable from the plastid-dividing ring. The FtsZ ring localizes in stroma and faces the inner plastid-dividing ring at the far side from the inner envelope. The FtsZ ring and the inner and outer plastid-dividing rings form in that order before plastid division. The FtsZ ring disappears at the late stage of constriction before dissociation of the plastid-dividing ring, when the constriction is still in progress. Our results suggest that the FtsZ ring;-based system, which originated from a plastid ancestor, cyanobacteria, and the plastid-dividing ring;-based system, which probably originated from host eukaryotic cells, form a complex and are involved in plastid division by distinct modes.

MeSH Terms
Arabidopsis Proteins Chloroplasts/physiology,ultrastructure Microscopy, Fluorescence Plant Proteins/analysis,metabolism Rhodophyta/physiology
Chemicals
Arabidopsis Proteins FTSZ protein, Arabidopsis Plant Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Miyagishima Sy
Department of Biological Sciences, Graduate School of Science, University of Tokyo, Hongo, Tokyo 113-0033, Japan. [email protected]
Takahara M
Mori T
Kuroiwa H
Higashiyama T
Kuroiwa T
References (39)
39 references, click to expand
  1. Visualization of an FtsZ ring in chloroplasts of Lilium longiflorum leaves.
    Plant Cell Physiol. 2001 Jun;42(6):555-9 PMID: 11427673
  2. Organelle division: Self-assembling GTPase caught in the middle.
    Curr Biol. 2000 May 4;10(9):R328-30 PMID: 10801435
  3. Mitochondrial FtsZ in a chromophyte alga.
    Science. 2000 Feb 18;287(5456):1276-9 PMID: 10678836
  4. Cell division protein FtsZ: running rings around bacteria, chloroplasts and mitochondria.
    Res Microbiol. 2001 Jan-Feb;152(1):3-10 PMID: 11281323
  5. Pea chloroplast FtsZ can form multimers and correct the thermosensitive defect of an Escherichia coli ftsZ mutant.
    Mol Gen Genet. 2000 Mar;263(2):213-21 PMID: 10778739
  6. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli.
    Cell. 1997 Jan 24;88(2):175-85 PMID: 9008158
  7. Isolation of dividing chloroplasts with intact plastid-dividing rings from a synchronous culture of the unicellular red alga cyanidioschyzon merolae
    Planta. 1999 Sep;209(3):371-5 PMID: 10502105
  8. Bacterial cell division.
    Annu Rev Cell Dev Biol. 1997;13:395-424 PMID: 9442879
  9. THE PLASTID DIVISION MACHINE.
    Annu Rev Plant Physiol Plant Mol Biol. 2001 Jun;52:315-333 PMID: 11337401
  10. The endosymbiont hypothesis revisited.
    Int Rev Cytol. 1992;141:233-357 PMID: 1452433
  11. The division apparatus of plastids and mitochondria.
    Int Rev Cytol. 1998;181:1-41 PMID: 9522454
  12. Behavior of mitochondria, chloroplasts and their nuclei during the mitotic cycle in the ultramicroalga Cyanidioschyzon merolae.
    Eur J Cell Biol. 1994 Apr;63(2):280-8 PMID: 8082652
  13. Bacterial cell division.
    Annu Rev Genet. 1999;33:423-48 PMID: 10690414
  14. Organelle fission. Crossing the evolutionary divide.
    Plant Physiol. 2000 Aug;123(4):1213-6 PMID: 10938340
  15. FtsZ and organelle division in Protists.
    Protist. 2000 May;151(1):11-6 PMID: 10896129
  16. Plastid division and development
    Plant Cell. 1999 Apr;11(4):549-56 PMID: 10213777
  17. A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus.
    Curr Biol. 2000 May 4;10(9):507-16 PMID: 10801439
  18. Novel filaments 5 nm in diameter constitute the cytosolic ring of the plastid division apparatus.
    Plant Cell. 2001 Mar;13(3):707-21 PMID: 11251107
  19. Plastid division: evidence for a prokaryotically derived mechanism.
    Curr Opin Plant Biol. 1998 Dec;1(6):475-9 PMID: 10066635
  20. Straight and curved conformations of FtsZ are regulated by GTP hydrolysis.
    J Bacteriol. 2000 Jan;182(1):164-70 PMID: 10613876
  21. Visualization of a cytoskeleton-like FtsZ network in chloroplasts.
    J Cell Biol. 2000 Nov 13;151(4):945-50 PMID: 11076976
  22. Analysis of FtsZ assembly by light scattering and determination of the role of divalent metal cations.
    J Bacteriol. 1999 Feb;181(3):823-32 PMID: 9922245
  23. 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. 1998 Apr 14;95(8):4368-73 PMID: 9539743
  24. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast.
    Nat Cell Biol. 1999 Sep;1(5):298-304 PMID: 10559943
  25. The timing and manner of disassembly of the apparatuses for chloroplast and mitochondrial division in the red alga Cyanidioschyzon merolae.
    Planta. 2001 Mar;212(4):517-28 PMID: 11525508
  26. Characterization of a chloroplast isoform of serine acetyltransferase from the thermo-acidiphilic red alga Cyanidioschyzon merolae.
    Biochim Biophys Acta. 1998 May 27;1403(1):72-84 PMID: 9622597
  27. Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ.
    Plant Cell. 1998 Dec;10(12):1991-2004 PMID: 9836740
  28. Dynamic assembly of FtsZ regulated by GTP hydrolysis.
    EMBO J. 1998 Jan 15;17(2):462-9 PMID: 9430638
  29. A putative mitochondrial ftsZ gene is present in the unicellular primitive red alga Cyanidioschyzon merolae.
    Mol Gen Genet. 2000 Nov;264(4):452-60 PMID: 11129049
  30. C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane.
    Mol Cell. 1999 Nov;4(5):815-26 PMID: 10619028
  31. The FtsZ protofilament and attachment of ZipA--structural constraints on the FtsZ power stroke.
    Curr Opin Cell Biol. 2001 Feb;13(1):55-60 PMID: 11163134
  32. GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules.
    Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5813-7 PMID: 8016071
  33. Dynamin and FtsZ. Missing links in mitochondrial and bacterial division.
    J Cell Biol. 2000 Mar 20;148(6):1103-5 PMID: 10725322
  34. In vitro assembly of cytoplasmic microtubules.
    Annu Rev Biochem. 1980;49:565-91 PMID: 6105842
  35. Observations on dividing plastids in the protonema of the moss Funaria hygrometrica Sibth. : Arrangement of microtubules and filaments.
    Planta. 1987 Nov;172(3):309-20 PMID: 24225915
  36. FtsZ ring formation at the chloroplast division site in plants.
    J Cell Biol. 2001 Apr 2;153(1):111-20 PMID: 11285278
  37. Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers.
    Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):519-23 PMID: 8552673
  38. Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space.
    Biochim Biophys Acta. 1973 Aug 31;314(2):224-41 PMID: 4747067
  39. Conserved cell and organelle division.
    Nature. 1995 Aug 10;376(6540):473-4 PMID: 7637778
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2001-10-00
Pages
2257-68
Language
English
Region
England
NLM ID
9208688
PMCID
PMC139157
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]