The Plant Cell, Vol. 15, 577, March 2003, www.plantcell.org © 2003 American Society of Plant Biologists

IN THIS ISSUE

Dynamic Trio: FtsZ, Plastid-Dividing, and Dynamin Rings Control
Chloroplast Division
Chloroplasts and mitochondria likely
evolved from endosymbiosis of bacterial
progenitors with a host cell. Thus, it is expected that the division of these organelles bears some resemblance toprokaryotic cell division. However, organelle division is controlled by proteinsencoded in the nucleus (host cell genome),
and mitochondrial and chloroplast genomes have lost most of the genes necessary for the control of their own division.
Some of the nuclear genes involved in organelle division are homologous with bacterial cell division genes, suggesting horizontal gene transfer from endosymbiont to
the host genome at some time during theirevolutionary history, whereas others are ofnuclear origin (Lang et al., 1999).
Organelle division is a complex processthat is regulated both in concert with andindependently of host cell division. During
cell division, division of the organelles
ensures their inheritance and the maintenance of copy number within progeny
cells. Independently of cell division, thecopy number of both chloroplasts and mitochondria within an organism varies considerably depending on the cell type,developmental stage, and even environmental conditions. The primitive singlecelled red alga Cyanidioschyzon merolae
is a useful model system for the study oforganelle division. Each Cyanidioschyzon
cell contains a single mitochondrion anda single chloroplast, thus reducing organelle division to a somewhat more simple system than in higher eukaryotes andfacilitating experimental control and observation (Figure 1). A complete picture of
the organellar dividing apparatuses in thislower eukaryote can be expected to yield
important insights into the origin and evolution of these organelles as well as theregulation of their division.
In this issue of The Plant Cell, Miyagishima
et al. (pages 655–665) characterize thefunction of a nucleus-encoded dynamin-related protein, CmDnm2, in Cyanidioschyzon chloroplast division. This represents an important step forward in our
understanding of the mechanism and evolution of chloroplast division. Dynamins,
which are not found in prokaryotes, previously were known to be involved in endocytosis and mitochondrial division in
eukaryotes and cell plate formation inplants, but little evidence suggested thatthese proteins were involved in chloroplast
division. Rather, it has been assumed thatchloroplasts have retained more of a bac-terial-type division apparatus, a notion
supported by the observation that chloroplasts contain numerous homologs ofbacterial division genes (Erickson, 2000;
Osteryoung, 2001).
For example, Arabidopsis contains afamily of dynamin-like proteins (ADLs) thatare known to function in various membrane scission events. ADL1A is associated with cell plate formation (Kang et al.,2001), ALD6 plays a role in vesicle formation in the trans-Golgi network (Jin et al.,2001), and ADL2b appears to be involved
in mitochondrial division (Arimura andFigure 1. CmDnm2 Forms a Ring at the Chloroplast Division Site.
Immunofluorescence image of the single-celled red alga Cyanidioschyzon showing the CmDnm2 dynamin protein (in green) forming a ring at the chloroplast division site during the late stages of division.
The main body of the cell with the nucleus is at top, the single mitochondrion appears in the center ofthe cell (in orange), and the dividing chloroplast is at bottom. Chlorophyll autofluorescence is shown inred. (Figure courtesy of S. Miyagishima.)

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IN THIS ISSUETsutsumi, 2002). ADL1 has been observed inthylakoid membranes and is hypothesized toplay a role in their biogenesis (Park et al.,1998), and ADL2 is localized to plastids andshows high expression in flower tissues(Kang et al., 1998), but dynamins have notbeen observed previously in association withthe chloroplast division apparatus.

DYNAMINS: EUKARYOTICMEMBRANE SCISSORS

Dynamins constitute a superfamily of GTPases. However, instead of (or possibly inaddition to) functioning as classic “molecular switch” GTPases, dynamins are capable of self-assembling into multimeric ring
structures that function in the regulation ofmembrane scission events, such as thosethat occur during endocytosis and organelle division. The prototype for dynamin and dynamin-related proteins ismammalian Dynamin1, which self-assembles into stacks of interconnected rings inbudding clathrin-coated vesicles that subsequently close and pinch off into newly
formed vesicles (Hinshaw, 2000). Most dynamin-related proteins that have been examined readily self-assemble, suggesting ageneral mechanism of action for this protein
family. The precise roles of the GTPase andself-assembly activities of dynamins are unclear, but it appears that self-assembly promotes ring formation and constriction at thedivision site and stimulates a high rate of
GTPase activity, which is required for ringdisassembly and subsequent membrane
fission (Sever et al., 2000).

DYNAMIN IN CYANIDIOSCHYZONCHLOROPLAST DIVISION

Chloroplast division is associated with theformation of a so-called FtsZ ring and aseries of distinct plastid-dividing (PD) rings(Miyagishima et al., 2001b; Kuroiwa et al.,2002). Two early events in chloroplast division are the accumulation of the GTPase
FtsZ and the formation of an FtsZ ring atthe future division site. FtsZ was identified
as a cell division protein in Escherichia
coli, and it plays a central role in regulating
the division of most prokaryotic cells(Bramhill, 1997). FtsZ self-assembles intoring structures, like dynamin, but it does
not show significant sequence similarity todynamin. Rather, it has similarity to andhas been proposed as a progenitor of tubulin. In plants, FtsZ is a nucleus-encoded
chloroplast protein (Osteryoung and Vierling,1995). The chloroplast FtsZ ring forms inthe stroma and faces a second series ofelectron-dense rings, the PD rings. The PD
rings consist of a main outer ring on thecytosolic face of the outer envelope, which
is made up of a bundle of unidentified 5-nm
filaments (Miyagishima et al., 2001a), an
inner ring that faces the FtsZ ring on thestromal side, and sometimes a middle ring
between the inner and outer envelope
membranes.
Miyagishima et al. show that chloroplast
division in Cyanidioschyzon is associatedwith the formation of a dynamin ring,which forms a third type of ring separate
from and in addition to the FtsZ and PDrings. Time-course experiments of theseven phases of chloroplast division, using
electron microscopy and immunofluorescence localization of FtsZ and CmDnm2,
showed that the FtsZ ring forms before theonset and disassembles during the final
stage of chloroplast constriction (phases 2to 5) and that the PD ring forms and disappears at a somewhat later stage (phases 3to 6). By contrast, CmDnm2 begins to accumulate in phase 3, after the FtsZ and PD
rings have formed, initiates the formationof a ring structure in phase 4, and appears
as a constricted ring during phase 5, the final phase of division. The protein often
persists in the daughter chloroplasts afterdivision (phase 6) and then disappears before cytokinesis (phase 7).

. . . IN GREEN PLANTS

Miyagishima et al. conducted sequencecomparisons of numerous dynamins fromdifferent organisms, which showed thatCmDnm2 is related most closely to two
previously uncharacterized Arabidopsis
proteins, NP_188606 and BAB02559.1.
Intriguingly, Gao et al. (2003) now haveshown that NP_188606 and NP_188607(corresponding to loci At3g19730 andAt3g19720, respectively) constitute asingle dynamin-like protein that is encoded by the gene ARC5 and that thisdynamin plays an important role in chloroplast division in Arabidopsis. Mutants ofARC5 are defective in chloroplast divisionand exhibit large dumbbell-shaped chloroplasts. Localization experiments suggested that ARC5 localizes to a ring at thechloroplast division site positioned on theouter surface of dividing chloroplasts (Gaoet al., 2003), which is consistent with theposition of the dynamin ring in Cyanidioschyzon chloroplasts. Thus, it appears
that this dynamic trio of rings—FtsZ, PD,and dynamin—functions in chloroplast division in higher plants as well as in Cyanidioschyzon.

. . . AND IN MITOCHONDRIAL DIVISION

This discovery has important implicationsfor organelle evolution. It has been hypothesized that dynamin replaced the functionof FtsZ in mitochondrial division in higher
eukaryotes and that chloroplasts retained
a prokaryotic FtsZ-type division, because
most higher eukaryotes lack mitochondrial
FtsZ and dynamin did not appear to be involved in chloroplast division in higher
plants (Erickson, 2000). However, the timing of certain events (e.g., the loss of FtsZ
and the acquisition of dynamin) is unclear.
Arimura and Tsutsumi (2002) proposed thepossibility that the acquisition of dynaminin eukaryotes occurred before the divergence of animals, fungi, green plants, andred algae, whereas the loss of mitochondrial FtsZ occurred separately in green
plants and the common ancestor of fungi
and animals after the divergence of thesegroups. In this scenario, therefore, thecommon ancestor of green plants and redMarch 2003

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algae would have used both FtsZ and dynamin in mitochondrial division. Recentwork has shown that Cyanidioschyzon(Nishida et al., 2003) and another primitive
eukaryote alga, the chromophyte Mallomonas splendens (Beech et al., 2000),
retain the use of FtsZ in mitochondrial division.
The work of Miyagishima et al. together
with that of Nishida et al. (2003) showsthat Cyanidioschyzon uses FtsZ and dynamin in both mitochondrial and chloroplast division. Therefore, Miyagishima etal. propose that mitochondria and chloroplasts in early eukaryotes likewise exhibited similar division apparatuses thatincluded an FtsZ ring, PD/mitochondriadividing (MD) rings, and a dynamin ring.
Importantly, in both the mitochondria
and chloroplasts of Cyanidioschyzon, theFtsZ ring forms early at the site of futuredivision, before the formation of the PD/MD rings (as it does in higher plant chloroplast division), whereas the dynamin ringappears to form later and to function onlyin the final separation, after the FtsZ andPD/MD rings have constricted (Miyagishimaet al., 2003; Nishida et al., 2003). Thus, theFtsZ, PD/MD, and dynamin rings areshown to have distinct functions in eukaryotic organelle division. This interestingobservation is sure to inspire additional
experiments aimed at gaining a more complete understanding of the mechanisms ofdivision and the course of organelle evolution in higher eukaryotes.
Nancy A. Eckardt
News and Reviews Editor
neckardt@aspb.or

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Dynamic Trio: FtsZ, Plastid-Dividing, and Dynamin Rings Control Chloroplast DivisionNancy A. Eckardt
Plant Cell 2003;15;577-579
DOI 10.1105/tpc.150310
This information is current as of May 2, 2014
References

This article cites 18 articles, 11 of which can be accessed free at:
http://www.plantcell.org/content/15/3/577.full.html#ref-list-1

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