Red Algae in the Genomic Age (Cellular Origin, Life in Extreme Habitats and Astrobiology)

442 Pages·2010·10.1 MB·English

by  Joseph Seckbach

Biodata of Shin-Ya Miyagishima and Hiromitsu Nakanishi, authors of “The
Chloroplast Division Machinery: Origin and Evolution”
Dr. Shin-Ya Miyagishima is currently the Unit leader of Miyagishima Initiative
Research Unit in RIKEN, Japan. He obtained his Ph.D. from the University
of Tokyo in 2002 and continued his studies and research at Michigan State
University. His scientific interests are in the areas of mechanism of chloro-
plast and mitochondrial division, evolution of chloroplasts, and mechanism of
endosymbiosis.
E-mail: [email protected]
Dr. Hiromitsu Nakanishi is currently the Research Scientist of Miyagishima
Initiative Research Unit in RIKEN, Japan. He obtained his Ph.D. from the
Shinshu University in 2006. His scientific interests are in the areas of mechanism
of chloroplast division and morphogenesis of chloroplast.
E-mail: [email protected]
Shin-Ya Miyagishima Hiromitsu Nakanishi
3
J. Seckbach and D.J. Chapman (eds.), Red Algae in the Genomic Age,
Cellular Origin, Life in Extreme Habitats and Astrobiology 13, 3–23
DOI 10.1007/978-90-481-3795-4_1, © Springer Science+Business Media B.V. 2010
THE CHLOROPLAST DIVISION MACHINERY: ORIGIN AND EVOLUTION
SHIN-YA MIYAGISHIMA AND HIROMITSU NAKANISHI
Miyagishima Initiative Research Unit, Frontier Research System,
RIKEN, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan
1. Introduction
It is widely believed that chloroplasts and mitochondria arose from bacterial
endosymbionts related to cyanobacteria and a-proteobacteria, respectively
(reviewed in Reyes-Prieto et al., 2007; Fig. 1). Although most of their genes
have either been lost or transferred to the host nuclear genome, they retain sev-
eral features similar to bacteria. Both organelles contain nucleoids and ribo-
somes, and neither are synthesized de novo. Chloroplasts multiply by binary
division, as do cyanobacteria (Leech et al., 1981; Possingham and Lawrence,
1983; Boffey and Lloyd, 1988; Kuroiwa, 1991; Kuroiwa et al., 1998). However,
the chloroplast genome does not contain sufficient information for division, indi-
cating that the host eukaryotic cell genome regulates the division of chloro-
plasts. Understanding the mechanism of chloroplast division should provide
important insights into the question of how the eukaryotic host cell coordinates
its own division with that of the endosymbiont to establish the permanent endo-
symbiotic relationship.
The first important insight into chloroplast division was obtained from studies
of the red algae Cyanidium caldarium in 1986. A ring structure was identified on the
cytosolic side of the outer envelope membrane at the chloroplast division site by
electron microscopy (Mita et al., 1986). After the identification in C. caldarium, this
structure, called a plastid-dividing (PD) ring, was found in a number of plant and
algae species (summarized in Kuroiwa et al., 1998; Fig. 2). These findings suggested
that chloroplast division is performed by a division apparatus, which forms at the
division site in a manner similar to actomyosin contractile rings in cytokinesis. The
history up to the discovery of the PD ring, including details on the structure, has
been summarized elsewhere (Leech et al., 1981; Possingham and Lawrence, 1983;
Boffey and Lloyd, 1988; Kuroiwa, 1991; Kuroiwa et al., 1998).
In the decade following the PD ring discovery, the molecular mechanisms
underlying the division process began to be understood, in particular because of
the identification of two self-assembling GTPase proteins. A homolog of bacte-
rial division protein FtsZ was identified in the nuclear genome of Arabidopsis
thaliana in 1995 (Osteryoung and Vierling, 1995). A member of the dynamin family
of eukaryotic GTPases was identified in the red alga Cyanidioschyzon merolae
5
6 SHIN-YA MIYAGISHIMA AND HIROMITSU NAKANISHI
Figure 1. The phylogenetic relationship of eukaryotes and the origin of chloroplasts. The lineages
indicated by squares have chloroplasts or nongreeen plastids. After the establishment of mitochondria,
chloroplasts were established in the ancestor of Plantae by primary endosymbiosis and enslavement of
an ancestral cyanobacterium. The ancestor of Plantae evolved to form glaucophytes, red algae, green
algae, and land plants. A red algal cell that was engulfed and enslaved (secondary endosymbiosis)
by the ancestral chromalveolate gave rise to chloroplasts in Chromista and Alveolata. Ciliates, such
as Paramecium and Tetrahymena, and parasitic stramenopiles, such as oomycetes, lost the secondary
chloroplasts. A green algal cell was enslaved by the ancestors of excavates (including Euglenozoa) and
Rhizaria (including chlorarachniophytes). The dinoflagellates replaced their existing red algal second-
ary chloroplasts (shared with other alveolates) with another chloroplast by engulfing stramenopiles,
haptophytes, or green algae. Details are summarized in Reyes-Prieto et al. (2007). G and R on the
arrows indicate chloroplasts of green algal and red algal origin, respectively.
(Miyagishima et al., 2003a) and A. thaliana (Gao et al., 2003). Both FtsZ and
dynamin were shown to localize at the chloroplast division site and to be involved
in the division process (reviewed in Osteryoung and Nunnari, 2003; Miyagishima
et al., 2003b; Fig. 2). These results revealed that a part of the division machinery,
including FtsZ, is descended from the cyanobacterial endosymbiont, whereas the
other part, which includes dynamin, is evolved from the eukaryotic host cell.
The mechanism of chloroplast division has been extensively examined in the
red algae C. merolae and the land plant A. thaliana. Studies using C. merolae have
yielded important information, in part owing to the highly synchronous system of
organellar division (Suzuki et al., 1994). In addition, the organellar and nuclear
genomes were completely sequenced (Matsuzaki et al., 2004; Misumi et al., 2005;
Nozaki et al., 2007) and the results showed that the genomes have very simple
contents. Studies in C. merolae and A. thaliana have shown commonalities in the
division mechanisms of red algae and land plants. However, certain factors identi-
fied in A. thaliana do not exist in other lineages of photosynthetic eukaryotes,
THE CHLOROPLAST DIVISION MACHINERY: ORIGIN AND EVOLUTION 7
Figure 2. The PD (plastid-dividing), FtsZ, and dynamin rings. (a) Electron micrographs of a C. merolae
cell containing a dividing chloroplast and mitochondrion. cp, chloroplast; mt, mitochondrion; n, nucleus.
(b) Magnified cross-section of the PD ring, corresponding to the boxed-region in a. The PD ring is
composed of an outer ring (on the cytosolic side of the outer envelope; arrowheads), a middle ring (in
the intermembrane space; triple arrowheads), and an inner ring (on the stromal side of the inner envelope;
double arrowheads). The MD (mitochondrion-dividing) ring, a structure similar to the PD ring, is
also observed at mitochondrial division site (arrows). (c, d) Immunofluorescence images of the FtsZ
(CmFtsZ2; c) and dynamin (CmDnm2; d) rings during C. merolae chloroplast division. The bright
fluorescence indicates the localization of each protein and the transparent fluorescence is chloroplast
autofluorescence. (e) Dividing chloroplasts in petiole cells of A. thaliana. The dividing chloroplasts are
indicated by arrowheads. (f, g) FtsZ2-1-GFP (f) and GFP-ARC5 dynamin (g) localize at the chloro-
plast division sites in A. thaliana. Note that dynamin localizes at the division site as a discontinuous
ring (the right arrow) and then forms a continuous ring during a late stage of the division site constriction
(the left arrow).
suggesting that the division machinery has been modified differently in different
lineages since the system was established in the ancestral algae. To summarize the
results from several lineages of eukaryotes, we first describe a brief summary of
the current understanding of the origin and evolution of chloroplasts.
2. The Evolution and Spread of Chloroplasts in Eukaryotes
Chloroplasts are found in several eukaryotic lineages in addition to red algae, green
algae, and plants. For example, remnants of the chloroplast (called “apicoplasts”)
are found in apicomplexan parasites that cause serious human diseases, including
malaria and toxoplasmosis (reviewed in Reyes-Prieto et al., 2007; Fig. 1). Given
the diversity of these lineages, the mechanisms of chloroplast division might be
expected to vary. However, since current understanding in evolutionary biology
8 SHIN-YA MIYAGISHIMA AND HIROMITSU NAKANISHI
holds that all chloroplasts have the same endosymbiotic origin (a cyanobacterium),
it is reasonable to postulate that the mechanism of chloroplast division was, in
principle, first established in algal chloroplasts. As described in this chapter, the
overall mechanism of chloroplast division is conserved across diverse species,
although several modifications have been introduced. The results obtained from
different species must be understood in the context of the evolutionary history of
chloroplasts.
Evolutionary studies have suggested that three types of endosymbiosis
(primary, secondary, and tertiary) have resulted in the establishment of chloro-
plasts in eukaryotes (Reyes-Prieto et al., 2007; Fig. 1). In primary endosymbiosis,
which occurred in the ancestor of Plantae including glaucophytes, red algae, and
Chlorophyta (land plants and green algae), engulfment of a prokaryotic cyano-
bacterium gave rise to a chloroplast bound by two membranes. In secondary
endosymbiosis, previously nonphotosynthetic eukaryotes engulfed eukaryotic
algae (either red or green algae), which were then reduced to secondary chloro-
plasts. Secondary chloroplasts have three or four envelope membranes; the third
and fourth membranes (going from the innermost to outermost) are thought to
correspond to the plasma membrane of the engulfed alga and the phagosomal
membrane of the host cell, respectively (Reyes-Prieto et al., 2007).
The most favored hypothesis is that secondary endosymbiosis of a red alga
may have resulted in the origin of the chromalveolates, including cryptophytes, hap-
tophytes, stramenopiles, and apicomplexa (Cavalier-Smith, 1999; Fast et al., 2001).
Plastids (apicoplasts) of apicomplexan parasites are not capable of photosynthesis.
According to the above endosymbiotic theory, the division of the first and
second envelope membranes of secondary chloroplasts and their contents is the
same phenomenon as seen in primary chloroplast division. In this chapter, we first
describe chloroplast division in Plantae, especially focusing on the red algae C.
merolae and the land plant A. thaliana, and then expand the description to the
secondary chloroplasts.
3. The Mechanism of Chloroplast Division in Model Organisms
3.1. MECHANISMS DERIVED FROM THE CYANOBACTERIAL
ENDOSYMBIONT
3.1.1. Involvement of FtsZ Proteins in Chloroplast Division
The mechanism of chloroplast division began to be revealed at the molecular
level with the identification of FtsZ proteins encoded in plant and algal nuclear
genomes. FtsZ is a bacterial division protein that was identified by the analyses of
filamentous, temperature-sensitive (fts) Escherichia coli mutants (reviewed in Weiss,
2004; Harry et al., 2006). Owing to defects in cytokinesis, fts mutants elongate to
form filaments. FtsZ, one of the several Fts proteins, is a GTPase structurally
similar to tubulin (Lowe and Amos, 1998) and is conserved in most bacteria and
THE CHLOROPLAST DIVISION MACHINERY: ORIGIN AND EVOLUTION 9
archaea. It self-assembles into a ring structure beneath the cytoplasmic membrane
at the division site. The formation of the FtsZ ring is the first known event at the
division site, and it initiates the recruitment of the other proteins that comprise
the bacterial division complex (Weiss, 2004; Harry et al., 2006). Therefore, FtsZ is
thought to play a central role in prokaryotic cell division.
A gene encoding chloroplast-targeted FtsZ was found in the A. thaliana
nuclear genome in 1995 (Osteryoung and Vierling, 1995). The amino acid sequence
of the protein is most similar to cyanobacterial FtsZ, supporting an endosymbi-
otic origin for FtsZ (Osteryoung and Vierling, 1995). After the identification in A.
thaliana, ftsZ genes were found in several additional species of plants and algae.
Gene disruption experiments in the moss Physcomitrella patens (Strepp et al.,
1998) and the expression of antisense RNA in A. thaliana (Osteryoung et al., 1998)
inhibited chloroplast division generating giant chloroplasts. These results indicated
that FtsZ proteins are required for chloroplast division in plants. Subsequently,
immunocytochemical studies showed that plant FtsZ proteins form ring structures
at chloroplast division sites in land plants (Mori et al., 2001; Vitha et al., 2001;
Fig. 2) and the red algae C. merolae (Miyagishima et al., 2001c; Fig. 2). The FtsZ
proteins have an N-terminal transit peptide and localize on the stromal side of the
inner envelope membrane (Mori et al., 2001; Miyagishima et al., 2001c; McAndrew
et al., 2001; Kuroiwa et al., 2002). These results revealed that at least a part of the
chloroplast division machinery is descended from cyanobacteria, although the
genes have been transferred to the host nuclear genome.
3.1.2. Other Chloroplast Division Proteins of Cyanobacterial Origin
The suggestion that the FtsZ descended from the cyanobacterial endosymbiont
is involved in chloroplast division led to the identification and characterization
of additional homologs of bacterial division proteins in plants and algae. The
molecular mechanism of bacterial cell division has been extensively studied in
Escherichia coli, a Gram-negative g-proteobacterium, and Bacillus subtilis, a
Gram-positive bacterium (Weiss, 2004; Harry et al., 2006). In E. coli, once an
FtsZ ring is formed at the division site, the remaining division proteins, ZipA,
FtsA, FtsE, FtsX, FtsK, FtsQ, FtsL, FtsW, FtsI, and FtsN, are recruited to the
site in this order to activate septation (Weiss, 2004; Harry et al., 2006). Proteins
regulating FtsZ ring formation in bacteria have also been identified. These pro-
teins include MinC, MinD, MinE, and DivIVA, which regulate the placement of
the FtsZ ring (Weiss, 2004; Harry et al., 2006). In E. coli, MinC, MinD, and MinE
are involved in the positioning of FtsZ ring, whereas B. subtilis does not have
MinE, and DivIVA, MinC, and MinD are involved in the process.
Of the several division genes identified in E. coli and B. subtilis, ftsE, ftsI,
ftsQ, ftsW, ftsZ, minC, minD, minE, sepF (ylmF), and divIVA are well conserved
in cyanobacterial genomes (Miyagishima et al., 2005), and some of these proteins
have been confirmed to be involved in cyanobacterial cell division as well
(Mazouni et al., 2004; Miyagishima et al., 2005). Studies in cyanobacteria also
have identified additional genes specific to cyanobacteria that are involved in cell
10 SHIN-YA MIYAGISHIMA AND HIROMITSU NAKANISHI
division, including ftn2 (Koksharova and Wolk, 2002) and certain other genes
(Koksharova and Wolk, 2002; Miyagishima et al., 2005).
Searches of the A. thaliana nuclear genome identified genes homologous to
cyanobacterial minD (Colletti et al., 2000) and minE (Itoh et al., 2001). The
results of antisense RNA, overexpression, or gene disruption experiments con-
firmed that these genes are involved in chloroplast division (Colletti et al., 2000;
Itoh et al., 2001; Reddy et al., 2002; Maple et al., 2002).
In addition to the reverse genetic studies on ftsZ, minD, and minE, forward
genetic studies in A. thaliana yielded the identification of other chloroplast divi-
sion genes of cyanobacterial origin. A. thaliana mutants with altered numbers of
chloroplasts per mesophyll cell were collectively named arc (accumulation and
replication of chloroplasts) mutants (Pyke and Leech, 1992, 1994; Pyke, 1999;
Marrison et al., 1999). Cells in most of the arc mutants contain very large chlo-
roplasts and the numbers of chloroplasts per cell are reduced, suggesting that the
chloroplasts can grow but their division is blocked in these mutants. The arc6
mutation was mapped to an A. thaliana nuclear gene that is orthologous to cyano-
bacterial ftn2 (Vitha et al., 2003). The ARC6 protein was shown to localize at the
chloroplast division site, spanning the inner envelope membrane (Vitha et al.,
2003), and later Ftn2 was shown to localize at the cell division site in cyanobac-
teria (Mazouni et al., 2004).
These results indicate that certain cyanobacterial cell division genes in addi-
tion to ftsZ were transferred to the nuclear genome of the eukaryotic host, where
they play roles in chloroplast division. However, database searches revealed that
ftsE, ftsI, ftsQ, ftsW, and divIVA, which are present in cyanobacterial genomes,
are missing from the A. thaliana genome (Miyagishima et al., 2005). The genome
of C. merolae has only the ftsZ gene from among the above-mentioned cyanobac-
terial division genes (Miyagishima et al., 2005). Examination of both the A. thal-
iana and C. merolae genomes indicate that the majority of bacterial cell division
genes were lost after endosymbiosis.
3.1.3. Possible Division Factors of Cyanobacterial Origin
Three genes in addition to the ones described earlier have also been implicated
in chloroplast division in A. thaliana. When either the ARTEMIS (Fulgosi et al.,
2002) or CRUMPLED LEAF (Asano et al., 2004) gene is disrupted, chloroplast
division is impaired, with giant chloroplasts generated in the cells. Similarly,
knock-down or overexpression of the AtSulA/GC1 gene reportedly impairs chlo-
roplast division (Maple et al., 2004; Raynaud et al., 2004). These three genes
are most likely descended from the cyanobacterial endosymbiont (Fulgosi et al.,
2002; Asano et al., 2004; Maple et al., 2004; Raynaud et al., 2004). ARTEMIS
contains a YidC/Oxa1/Alb3 translocase-like domain and localizes at the inner
envelope membrane of chloroplasts (Fulgosi et al., 2002), and the CRUMPLED
LEAF protein localizes on the outer envelope membrane (Asano et al., 2004).
Neither the ARTEMIS nor the CRUMPLED LEAF protein localizes spe-
cifically to the division sites, and their roles in chloroplast division are unknown.
THE CHLOROPLAST DIVISION MACHINERY: ORIGIN AND EVOLUTION 11
AtSulA/GC1 is annotated as a protein similar to E. coli SulA, which is induced by
the SOS response, and inhibits FtsZ polymerization, delaying cell division until
DNA damage is repaired in E. coli (Weiss, 2004; Harry et al., 2006). However,
the similarity of primary structures between AtSulA/GC1 and SulA is not sig-
nificant. At present, it is not known whether AtSulA/GC1 is directly involved in
chloroplast division.
Factors derived from the bacterial peptidoglycan synthesis pathway have
also been suggested to play a role in chloroplast division. Some antibiotics
that inhibit bacterial peptidoglycan synthesis also inhibit chloroplast division in
the moss P. patens (Kasten and Reski, 1997; Katayama et al., 2003), and some
genes in A. thaliana and P. patens encode the homologs of enzymes that act in
peptidoglycan synthesis in bacteria (Katayama et al., 2003). Disruption of the
genes in P. patens impaired chloroplast division (Machida et al., 2006). However,
peptidoglycans have never been detected in chloroplasts (except for glaucophyte
chloroplasts), and plant genomes do not have the full complement of genes that
are required for peptidoglycan synthesis in bacteria. In chloroplasts, homologs of
the bacterial peptidoglycan synthesis pathway may have other functions.
3.2. MECHANISMS DERIVED FROM THE EUKARYOTIC HOST
3.2.1. Paralogous Evolution of FtsZ Proteins
Most bacteria (including cyanobacteria) have only one ftsZ gene, whereas
chloroplast-containing eukaryotes have two types of phylogenetically distinct
ftsZ genes of cyanobacterial origin, suggesting that ftsZ gene duplication occurred
subsequent to the endosymbiotic event. Because these genes (named FtsZ1 and
FtsZ2, Osteryoung et al., 1998) are present both in land plants and in green algae
(Wang et al., 2003; Stokes and Osteryoung, 2003), ftsZ gene duplication appears to
have occurred before plants branched from green algae. In A. thaliana, FtsZ1 and
FtsZ2 colocalize at the stromal side of the inner envelope membrane (McAndrew
et al., 2001; Kuroiwa et al., 2002), even when the expression level and assembly
pattern of each was altered experimentally (McAndrew et al., 2001). Like chloro-
phytes, red algae (Miyagishima et al., 2004) and stramenopiles (Kiefel et al., 2004;
Miyagishima et al., 2004) also have two types of ftsZ genes, but phylogenetic analyses
indicate that gene duplication arose independently in chlorophytes, red algae, and
stramenopiles (Miyagishima et al., 2004).
In both chlorophytes and nonchlorophytes, one of the two FtsZ proteins
contains a short, conserved domain at the C-terminus (C-terminal core domain)
that is also conserved in bacterial FtsZ (Osteryoung and McAndrew, 2001; Kiefel
et al., 2004; Miyagishima et al., 2004), whereas the other FtsZ protein does not
have the C-terminal core domain. In bacteria, the C-terminal core domain of
FtsZ binds to FtsA and ZipA (Weiss, 2004; Harry et al., 2006). Although neither
FtsA nor ZipA has been found in eukaryotic genomes, it was shown that ARC6
specifically interacts with the core domain of FtsZ2, but not with FtsZ1, which
12 SHIN-YA MIYAGISHIMA AND HIROMITSU NAKANISHI
lacks the core domain (Maple et al., 2005). Although it is still not known how
FtsZ proteins lacking the C-terminal domain contribute to chloroplast division,
depletion of either ftsZ gene in A. thaliana inhibits chloroplast division, suggesting
that both FtsZ1 and FtsZ2 are required (Osteryoung et al., 1998).
Recently, a third FtsZ-like protein was found in A. thaliana by cloning of the
ARC3 gene. The arc3 mutant cells have giant chloroplasts like other arc mutants,
suggesting that chloroplast division is inhibited in the mutant (Pyke and Leech,
1992, 1994). ARC3 encodes a protein that has an FtsZ-like N-terminal region and
a C-terminal region homologous to a region of phosphatidylinositol-4-phosphate
5-kinase (Shimada et al., 2004). The ARC3 protein localizes on the stromal side
of the chloroplast division site (Maple et al., 2007), like other FtsZ proteins.
Functional studies in A. thaliana suggest that ARC3 is involved in the placement
of the FtsZ ring in chloroplasts (Maple et al., 2007).
3.2.2. The PD Ring
The plastid-dividing (PD) ring was first identified as an electron-dense structure
encircling the chloroplast division site in the red algae C. caldarium (Mita et al.,
1986). After that, similar structures have been identified in green algae, land plants,
and stramenopiles (summarized in Kuroiwa et al., 1998). In most cases, the PD
rings were detected as a double ring structure, with one ring (the outer PD ring)
(Mita et al., 1986) on the cytosolic face of the outer envelope and one ring (the
inner PD ring) (Hashimoto, 1986) on the stromal face of the inner envelope. In the
red algae C. merolae, a middle PD ring was also identified in the intermembrane
space (Miyagishima et al., 1998a; Fig. 2).
The ultrastructures and behaviors of the two (or three) PD rings were exten-
sively characterized in the red algae C. caldarium (Mita et al., 1986) and C. mero-
lae (Miyagishima et al., 1998b, 1999, 2001a). The studies showed that the structure
and behavior of the three rings are different, suggesting that each ring has distinct
function and is composed of distinct sets of proteins.
Characterization of the PD rings in green algae (Chida and Ueda, 1991;
Ogawa et al., 1995) and the land plant Pelargonium zonale (Kuroiwa et al., 2002)
provided results similar to those in the red algae, implying that the rings are
composed of orthologous proteins in several lineages. Electron-dense structures
were also reported in dividing chloroplasts of the glaucophyte Cyanophora para-
doxa (Iino and Hashimoto, 2003). In C. paradoxa, the ring structure was
observed at the stromal side of the inner envelope membrane and no structure
was observed on the cytosolic side of the outer envelope membrane at the divi-
sion site. At present, whether or not this ring structure corresponds to the inner
PD ring is unknown.
Although FtsZ was once believed to be a component of the inner PD ring
(Kuroiwa et al., 1998), or both the inner and outer PD rings (Osteryoung et al.,
1998), the FtsZ ring was ultimately shown to be a structure that is distinct and
separable from the PD rings (Miyagishima et al., 2001c). The FtsZ ring is
THE CHLOROPLAST DIVISION MACHINERY: ORIGIN AND EVOLUTION 13
Figure 3. Sequence of events in chloroplast division. (1) Chloroplasts elongate. (2) An FtsZ ring forms
at the division site. (3) The inner PD ring forms, followed by the formation of middle and the outer PD
rings (the inner and the middle PD rings are not shown.). Constriction of the division site commences
once the PD ring is assembled. (4) During constriction, cytosolic dynamin patches are recruited to the
cytosolic side of the division site to form a discontinuous ring. (5) A continuous dynamin ring forms in
the late stage of division. The FtsZ ring disassembles, followed by disassembly of the inner and middle
PD rings. (6) When division is complete, the remnant of the outer PD ring, which is now located
between the two daughter chloroplasts, disassembles. In contrast, the remnant of the dynamin ring is
retained by one of the two daughter organelles and subsequently disappears. Details are described in
Miyagishima et al. (2001a, c, 2003a).
positioned on the interior side of the inner PD ring, and it assembles prior to the
PD rings (Miyagishima et al., 2001c; Kuroiwa et al., 2002; Fig. 3).
Although none of the PD ring components have yet been identified, the
outer PD ring forms as a bundle of filaments (Kuroiwa et al., 1998). Biochemical
dissection in C. merolae has shown that the outer PD ring is a bundle of 5-nm
filaments (Miyagishima et al., 2001b; Yoshida et al., 2006). These filaments are
believed to be novel structures, based on their dimensions and their biochemical
stability (Miyagishima et al., 2001b). No electron-dense structures such as the PD
ring have been observed at the division sites of bacteria, including cyanobacteria.
Thus, the inner and outer PD rings (and the middle PD ring of C. merolae) do
not appear to correspond to any parts of the bacterial division machinery, sug-
gesting that they arose in the eukaryotic host after endosymbiosis.
3.2.3. Dynamin-Related Proteins
The above results from the study of the PD rings raise the possibility that some of
the components of chloroplast division machinery are derived from the eukaryotic
host. A mixed origin for the chloroplast division machinery was demonstrated by
the identification of a dynamin-related protein in chloroplast division.
The dynamin and dynamin-related proteins are a family of large GTPase
proteins involved in fission and fusion in several eukaryotic membrane systems