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475
Plastid division: evidence for a prokaryotically derived
mechanism
Katherine W Osteryoung* and Kevin A Pyke†
Plastid division is a critical process in plant cell biology but it is
poorly understood. Recent studies combining mutant analysis,
gene cloning, and exploitation of genomic resources have
revealed that the molecular machinery associated with plastid
division is derived evolutionarily from the bacterial cell division
apparatus. Comparison of the two processes provides a basis
for identifying new components of the plastid division
mechanism, but also serves to highlight the differences, not least
of which is the nuclear control of the plastid division process.
Addresses
*Department of Biology/314, University of Nevada, Reno, Nevada
89557, USA; e-mail: [email protected]
†School of Biological Sciences, Royal Holloway, University of London,
Egham, Surrey TW20 0EX, UK; e-mail: [email protected]
Current Opinion in Plant Biology 1998, 1:475–479
http://biomednet.com/elecref/1369526600100475
© Current Biology Ltd ISSN 1369-5266
Abbreviations
ARC
accumulation and replication of chloroplasts
EST
expressed sequence tag
FTS
filamentation temperature sensitive
ZipA
Z-interacting protein A
Introduction
A major factor in the successful evolution of higher plants
has been the development of an intimate cellular relationship with plastids originally derived by endosymbiosis from
a single free-living photosynthetic prokaryote [1]. The
maintenance of plastid populations in plant cells undergoing division, as well as the developmentally regulated
establishment of large plastid populations in some cell
types, requires that plastids replicate. A sizable body of literature has built up over the past 40 years [2•] which has
established that both chloroplasts, in which plastid division
has been studied most extensively, and their progenitors in
meristematic cells, the proplastids, divide by a process
termed binary fission. This process starts as a centrally
located constriction of the plastid envelope that narrows
progressively [3]. In later stages, a thin isthmus joining the
two daughter plastids can occasionally be observed,
although the stages of chloroplast division in which morphological structures are present are short-lived and not
readily apparent in all dividing chloroplasts. A key morphological feature of this process is the formation of an
electron-dense plastid dividing ring [4••] which encircles
the isthmus and has been shown to be a double-ring structure, with one ring on the stromal side of the inner
envelope and the other ring on the cytosolic side of the
outer envelope. It is generally assumed that components of
this ring function in the division process by constricting the
membranes, leading to a final pinching off and separation of
the daughter plastids. The molecular composition of these
rings, however, and how they function have yet to be established. In this article we will consider the recent advances
in understanding the molecular machinery that accomplishes plastid division, which have come about largely through
the application of Arabidopsis molecular genetics.
Mutations in ARC genes radically affect
plastid division
The complex genetic basis of the plastid division process
in higher plants has been partially established by characterization of the Arabidopsis arc mutants (accumulation and
replication of chloroplasts), which exhibit altered chloroplast numbers in mesophyll cells and define at least seven
distinct loci important in the control of chloroplast number
[2•]. The most extreme arc mutant is arc6 [5] in which
chloroplast number is reduced from >100 in wild type to 23 greatly enlarged chloroplasts per cell. The arc6
phenotype results primarily from interference with proplastid division in the shoot and root meristems [6]. Plastid
segregation into new cells still occurs, however, as evidenced by the lack of aplastidic cells in most tissues,
possibly resulting from physical breakage of the proplastids during cytokinesis. Thylakoid ultrastructure and
plastid function are unaffected in arc6 [5], and developmentally controlled redifferentiation of arc6 chloroplasts
into colorless leucoplasts in petals occurs normally in spite
of their dramatic increase in size [7•]. Two other ARC
genes, ARC3 [8] and ARC5 [3,9], may function directly in
the division mechanism. These mutants have normal proplastid division, but either fail to initiate chloroplast
divisions (arc3) or stop in the latter stages of chloroplast
constriction (arc5), producing mesophyll cells containing
about 15 chloroplasts per cell. Analysis of the arc mutants
has been instrumental in establishing the strict cellular
control that exists over total chloroplast compartment volume, because changes in chloroplast number in the
mutants are always compensated for by an inversely related change in chloroplast size [2•].
A prokaryotic cell division gene discovered
in plants
A significant breakthrough in understanding the mechanistic basis for plastid division was the discovery of a
nuclear gene from Arabidopsis encoding a homologue of a
bacterial cell division protein called FtsZ, an essential
component of the prokaryotic cell division machinery
[10]. The Arabidopsis FtsZ protein, now called AtFtsZ1-1
[11••], shares 40-50% amino acid identity with most of its
prokaryotic counterparts, and is most similar to the FtsZ
sequences from cyanobacteria. AtFtsZ1-1 was shown to be
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Cell biology
targeted to the chloroplast, strongly implicating the protein in chloroplast division and inspiring the hypothesis
that the plastid division machinery in plants has its evolutionary origin in the endosymbiotic progenitor of the
organelles [10]. Two studies have now established that
FtsZ proteins are essential for chloroplast division in
plants [11••,12••], confirming that a prokaryotically based
apparatus functions in plastid division and setting the
stage for advancing our understanding of this critical
process in plant cell biology. Here we briefly summarize
previous work on FtsZ function in bacterial cell division
and then describe the recent findings on the role of these
proteins in plants.
FtsZ function in bacteria
FtsZ is an ancient, highly conserved prokaryotic cytoskeletal protein found both in archaebacteria and eubacteria
[13–15]. It was first identified in a genetic screen for temperature-sensitive mutants of E. coli that were defective in
cell division. These cells formed long filaments at the
restrictive temperature due to incomplete formation of the
division septum (the structure formed by invagination of
the bacterial membranes and cell wall), and were, therefore,
designated fts mutants (filamentation temperature-sensitive) [16]. Although numerous fts genes have been isolated
from bacteria, to date only FtsZ has been extensively characterized with regard to its role in cell division
[17,18,19•,20•]. Immunogold labeling [21] and immunofluorescence localization studies with fusions to green
fluorescent protein [22] have shown that, at an early stage
in the bacterial cell division cycle, FtsZ is recruited to the
presumptive division site where it forms a ring-like structure on the interior surface of the cytoplasmic membrane.
The FtsZ ring constricts during septation, remaining at the
leading edge of the invaginating septum, and disassembles
once septation is complete. The dynamic nature of the
FtsZ ring suggests it has a contractile function that pulls on
the cytoplasmic membrane to initiate cytokinesis, though it
could also act as a scaffold upon which other components of
the division apparatus can assemble. The structure of the
FtsZ ring in vivo is not yet known, but its cytoskeletal properties became evident from experiments demonstrating
that purified FtsZ undergoes GTP-dependent assembly
into polymers that resemble tubulin protofilaments assembled under similar conditions [23–25]. These studies, along
with alignments showing limited but convincing amino acid
sequence similarities between FtsZ and tubulins [25–28],
triggered speculation that prokaryotic FtsZ is the evolutionary progenitor of the eukaryotic tubulins, a hypothesis
strengthened considerably by recent crystallographic data
confirming that FtsZ and tubulins are indeed structural
homologues of one another [29••,30••].
FtsZ function in plants
Two recent studies provide evidence that FtsZ proteins
are essential for chloroplast division in all land plants. In
the first, targeted disruption of PpFtsZ, a nuclear FtsZ
gene from the moss Physcomitrella patens, severely
inhibited chloroplast division in that organism, yielding
cells containing only a single large chloroplast [12••]. In the
second, antisense suppression of the Arabidopsis AtFtsZ1-1
gene described above perturbed division both of mesophyll cell chloroplasts and of proplastids in the shoot apical
meristem, resulting in leaf mesophyll cells containing as
few as one greatly enlarged chloroplast [11••]. These
results confirmed that FtsZ genes are essential for chloroplast division in both lower and higher plants. The latter
investigation went further, however, demonstrating that
the situation is considerably more complex than these
findings initially suggest, at least in higher plants.
Comparisons among the available plant FtsZ sequences
revealed that FtsZ genes fall into two distinct families, designated FtsZ1 and FtsZ2, encoding proteins that differ both
in their overall amino acid sequence similarities and in
their apparent subcellular localizations [11••]. FtsZ1 proteins contain amino-terminal extensions with features
common to chloroplast transit peptides, and at least one
member of this family, AtFtsZ1-1, can be post-translationally imported into isolated chloroplasts where the transit
peptide is processed [10]. FtsZ2 proteins, which include
PpFtsZ from Physcomitrella and a second nuclear-encoded
FtsZ protein from Arabidopsis, called AtFtsZ2-1, lack obvious subcellular sorting signals. Further, AtFtsZ2-1 could
not be imported into isolated chloroplasts or mitochondria
in vitro, strongly suggesting it is a cytosolic protein.
Nevertheless, antisense experiments clearly demonstrated
that AtFtsZ2-1 is also essential for chloroplast and proplastid division in Arabidopsis [11••]. These findings revealed
that at least two functionally distinct, and probably differentially localized, FtsZ gene products mediate plastid
division in higher plants [11••]. The role of FtsZs in plastid division may be more complex, however, as Arabidopsis
contains at least one other FtsZ2 family member [11••].
Two important conclusions can be drawn from the
Arabidopsis study. First, chloroplast division in higher
plants appears to require both plastid-localized and cytosolic forms of FtsZ. These data correspond well with
ultrastructural studies showing that two electron-dense
plastid dividing rings, each localized on opposite sides of
the chloroplast envelope membranes, participate in constriction of the organelle [4••]. Taken together, the
evidence supports a model whereby FtsZ1 and FtsZ2 are
components of the inner and outer plastid dividing rings
respectively, a prediction that can be tested in high-resolution localization studies of AtFtsZ1-1 and AtFtsZ2-1 or their
homologues in other plants. The finding that plastid division is disrupted by reduced expression of either AtFtsZ1-1
or AtFtsZ2-1 further implies that FtsZ1 and FtsZ2 functions are co-ordinated in some way to bring about the
constriction of the chloroplast. Because double plastid
dividing rings have been observed in lower as well as in
higher plants, we expect that an FtsZ1 homologue may
also be identified and shown to be required for chloroplast
division in Physcomitrella.
Plastid division Osteryoung and Pyke
Second, it is apparent that in Arabidopsis the same FtsZ
genes function in the division of both undifferentiated proplastids and differentiated chloroplasts. As the number of
plastids and the relative cell volume occupied by them differs greatly between meristematic and developing
mesophyll cells, these results indicate that AtFtsZ1-1 and
AtFtsZ2-1 accumulation or activity may be differentially
controlled in different types of cells. ARC6 also functions
in the division both of proplastids and of chloroplasts [5,6],
but does not cosegregate with either AtFtsZ gene, raising
the possibility that all three genes are subject to similar
regulatory controls in different cell types.
Bacterial cell division as a model for
identifying new plastid division genes: lessons
and limitations
Although the experiments described above firmly established the prokaryotic origin of the plastid division
apparatus, significant differences exist between plastid
and bacterial cell division. Perhaps the most obvious is that
the former occurs within the environment of the eukaryotic cytosol. A consequence of this is that plastids are not
subject to the osmotic forces experienced by free-living
bacteria, and except for the glaucophyte cyanelles, most no
longer possess the peptidoglycan cell wall present in their
prokaryotic ancestors [31,32]. The studies of FtsZ function
in Arabidopsis [11••] further suggest that specific cytosolic
as well as plastid-localized components participate in plastid division. Nevertheless, the process of bacterial cell
division is clearly a useful, if incomplete, model upon
which to base further analysis of plastid division in plants.
Here we consider how each phase in plastid division
resembles and differs from the analogous phase in bacterial cell division, with an eye towards defining other
potential components of the plastid division apparatus.
Phase one: selection of the division site
Plastid division always occurs at the center of the plastid,
perpendicular to the longitudinal axis [33••]. This implies
that a mechanism exists for ensuring proper placement of
the division machinery. In E. coli, the site of septum formation is under control of the minB locus, which
comprises three genes: minC, minD and minE [34]. Mutant
strains lacking MinC and MinD are characterized by the
formation of ‘minicells’, tiny, nonviable cells lacking chromosomes. Minicells are formed by the frequent
misplacement of the FtsZ ring at a position near the cell
pole that corresponds to the location of the previous division site, resulting in septation near the cell pole rather
than at midcell. This phenotype indicates that the previous sites of septation retain their potential for division
even after separation of the daughter cells, and that MinC
and MinD act together in wild-type cells to inhibit FtsZ
ring assembly at these former division sites [34,35].
Normally the activity of MinC and MinD is restricted to
the former division site near the cell pole. In minE
mutants, however, MinC and MinD can also act at the cell
center, preventing FtsZ ring formation at its normal site
477
and thereby inhibiting cell division. Thus, the function of
MinE is to impart topological specificity to the activity of
MinC and MinD so that division occurs only at the cell
center [34]. This activity involves formation of a MinE
ring at the midcell [36], which is important for FtsZ ring
placement, but not for FtsZ ring assembly per se.
Recent data from two genome sequencing programs suggest that a similar system operates in positioning of the
plastid division apparatus in plants. Homologues of minD
and minE have been identified in the plastid genome of
the unicellular green alga Chlorella vulgaris [37••] and a
MinD homologue has been uncovered in the Arabidopsis
nuclear genome (KA Pyke and KW Osteryoung, unpublished data). The protein encoded by the Arabidopsis gene
includes an amino-terminal extension with characteristics
suggesting a chloroplast targeting function. Although these
Min genes must still be tested for roles in plastid division,
their existence provides evidence that the mechanism controlling placement of the plastid division apparatus has also
been conserved during the evolution of chloroplasts. MinE
has not yet been identified in land plants, but on the basis
of its role in bacteria, it seems probable that a functional
homologue of MinE will be involved in proper positioning
of the plastid division machinery. If a cytosolic FtsZ ring
participates in plastid division as hypothesized [11••] then
additional cytosolic Min proteins or other factors would
presumably be required for correct placement of that structure as well.
Phase two: assembly of the FtsZ ring
The earliest step in the formation of the division septum
in bacteria is assembly of the FtsZ ring at midcell [19•].
Immediately following separation of the daughter cells,
the FtsZ ring disassembles, and for a short period the protein can be detected throughout the cytoplasm before it
reassembles at the new division site. What triggers FtsZ
ring assembly and how the protein becomes localized and
anchored to the membrane are still unknown. One molecule proposed to play an important role, however, is the
recently identified ZipA [38••]. ZipA (Z-interacting protein A), identified biochemically on the basis of its ability
to bind purified FtsZ, is an integral membrane protein
containing a cytoplasmic domain predicted to form a rigid,
rod-like structure. Like FtsZ, the protein localizes in a ring
at midcell early in the division process. These properties
suggest that ZipA acts as a membrane anchor and possibly
stimulatory factor for FtsZ polymerization [18,38 ••].
Exactly how FtsZ ring assembly ensues is not understood,
but evidence suggests that polymerization proceeds bidirectionally from a single nucleation point on the
cytoplasmic membrane [39]. Whether ZipA or some other
factor is involved in the nucleation event is unknown.
Because plant FtsZ proteins, like their bacterial counterparts, lack transmembrane domains, a ZipA-like molecule
may also be necessary for assembly of the plastid dividing
rings in plants. Another possibility, however, is that
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Cell biology
post-translational modification could provide a lipid-soluble membrane anchor allowing plant FtsZ proteins to
reversibly associate with the envelope membranes. Posttranslational modification of bacterial FtsZ has not been
reported, but reversible palmitoylation of tubulin in
human platelets has been demonstrated [40,41]. The
high degree of amino acid conservation between plant
and bacterial FtsZs argues that the polymerization
process itself and structural properties of the FtsZ ring or
rings in plants will closely resemble those in bacteria.
Phases three and four: constriction and
separation
Constriction of dividing bacterial cells is still a poorly
understood process. FtsZ presumably participates, but
several other fts genes whose functions are less well understood are also required. Most of these appear to be
involved either in cell wall peptidoglycan synthesis, which
is essential for septation in E. coli, or in coupling cell wall
synthesis to the FtsZ ring [19•,20•]. These genes, however, are absent in the mycoplasmas, which lack cell walls,
and presumably would not be involved in plastid division
if their functions are specifically related to septal cell wall
ingrowth. It may be that constriction of the plastid still
requires the participation of rigid structures on both envelope surfaces, consistent with the involvement of two
plastid dividing rings and two FtsZ genes in plastid division. Perhaps the requirement for cell wall ingrowth in
bacteria has been supplanted by the evolution of an external plastid dividing ring composed of FtsZ in plants.
At present, we can only speculate on other types of molecules that might play a part in the constriction and
separation phases of plastid division, but one strong contender is ARC5 [3,9]. Chloroplasts in arc5 mutants initiate
but become arrested during constriction, indicating the
gene product acts late in division and may be a component
of the division apparatus. Other potential participants
include molecules that co-ordinate constriction of the two
plastid dividing rings, and those in addition to FtsZ that
contribute to the mechanics of plastid dividing ring constriction. Because the formation of a long, narrow isthmus is
sometimes observed late in plastid division, it is conceivable that other cytoskeletal elements in the cytosol and
their associated motor proteins could facilitate daughter
plastid movement and separation by a pulling mechanism.
Conclusions
The recent studies on plant FtsZ function establish a foundation for further dissecting the components of the plastid
division apparatus. The molecular infrastructure provided
by the Arabidopsis and other genome sequencing efforts
will continue as important resources for identification of
new plastid division genes, though other approaches will
clearly be important as well. Challenges for the future
include determining how the plastid division mechanism is
integrated with the developmental programming to produce different plastid numbers in different cell types, and
discovering how the cell senses and controls chloroplast
compartment volume. Progress in the last two years has
been dramatic and we anticipate that our understanding
will progress significantly in the near future by the
exploitation of both new and existing mutants and genes.
Acknowledgements
We thank members of our two laboratories and M Odell for helpful
discussions. We gratefully acknowledge support to KW Osteryoung from
the National Science Foundation and Nevada Agricultural Experiment
Station, and to KA Pyke from the Biotechnology and Biological Sciences
Research Council.
References and recommended reading
Papers of particular interest, published within the annual period of review,
have been highlighted as:
• of special interest
•• of outstanding interest
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•
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Plastid division Osteryoung and Pyke
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An interesting aspect of this review is its discussion of FtsZ function in different groups of bacteria and the implications for mechanistic differences in
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•
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A helpful review because it succinctly summarizes the available information
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479
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of the plastid division apparatus in plants.
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Plastid division: evidence for a prokaryotically derived
mechanism
Katherine W Osteryoung* and Kevin A Pyke†
Plastid division is a critical process in plant cell biology but it is
poorly understood. Recent studies combining mutant analysis,
gene cloning, and exploitation of genomic resources have
revealed that the molecular machinery associated with plastid
division is derived evolutionarily from the bacterial cell division
apparatus. Comparison of the two processes provides a basis
for identifying new components of the plastid division
mechanism, but also serves to highlight the differences, not least
of which is the nuclear control of the plastid division process.
Addresses
*Department of Biology/314, University of Nevada, Reno, Nevada
89557, USA; e-mail: [email protected]
†School of Biological Sciences, Royal Holloway, University of London,
Egham, Surrey TW20 0EX, UK; e-mail: [email protected]
Current Opinion in Plant Biology 1998, 1:475–479
http://biomednet.com/elecref/1369526600100475
© Current Biology Ltd ISSN 1369-5266
Abbreviations
ARC
accumulation and replication of chloroplasts
EST
expressed sequence tag
FTS
filamentation temperature sensitive
ZipA
Z-interacting protein A
Introduction
A major factor in the successful evolution of higher plants
has been the development of an intimate cellular relationship with plastids originally derived by endosymbiosis from
a single free-living photosynthetic prokaryote [1]. The
maintenance of plastid populations in plant cells undergoing division, as well as the developmentally regulated
establishment of large plastid populations in some cell
types, requires that plastids replicate. A sizable body of literature has built up over the past 40 years [2•] which has
established that both chloroplasts, in which plastid division
has been studied most extensively, and their progenitors in
meristematic cells, the proplastids, divide by a process
termed binary fission. This process starts as a centrally
located constriction of the plastid envelope that narrows
progressively [3]. In later stages, a thin isthmus joining the
two daughter plastids can occasionally be observed,
although the stages of chloroplast division in which morphological structures are present are short-lived and not
readily apparent in all dividing chloroplasts. A key morphological feature of this process is the formation of an
electron-dense plastid dividing ring [4••] which encircles
the isthmus and has been shown to be a double-ring structure, with one ring on the stromal side of the inner
envelope and the other ring on the cytosolic side of the
outer envelope. It is generally assumed that components of
this ring function in the division process by constricting the
membranes, leading to a final pinching off and separation of
the daughter plastids. The molecular composition of these
rings, however, and how they function have yet to be established. In this article we will consider the recent advances
in understanding the molecular machinery that accomplishes plastid division, which have come about largely through
the application of Arabidopsis molecular genetics.
Mutations in ARC genes radically affect
plastid division
The complex genetic basis of the plastid division process
in higher plants has been partially established by characterization of the Arabidopsis arc mutants (accumulation and
replication of chloroplasts), which exhibit altered chloroplast numbers in mesophyll cells and define at least seven
distinct loci important in the control of chloroplast number
[2•]. The most extreme arc mutant is arc6 [5] in which
chloroplast number is reduced from >100 in wild type to 23 greatly enlarged chloroplasts per cell. The arc6
phenotype results primarily from interference with proplastid division in the shoot and root meristems [6]. Plastid
segregation into new cells still occurs, however, as evidenced by the lack of aplastidic cells in most tissues,
possibly resulting from physical breakage of the proplastids during cytokinesis. Thylakoid ultrastructure and
plastid function are unaffected in arc6 [5], and developmentally controlled redifferentiation of arc6 chloroplasts
into colorless leucoplasts in petals occurs normally in spite
of their dramatic increase in size [7•]. Two other ARC
genes, ARC3 [8] and ARC5 [3,9], may function directly in
the division mechanism. These mutants have normal proplastid division, but either fail to initiate chloroplast
divisions (arc3) or stop in the latter stages of chloroplast
constriction (arc5), producing mesophyll cells containing
about 15 chloroplasts per cell. Analysis of the arc mutants
has been instrumental in establishing the strict cellular
control that exists over total chloroplast compartment volume, because changes in chloroplast number in the
mutants are always compensated for by an inversely related change in chloroplast size [2•].
A prokaryotic cell division gene discovered
in plants
A significant breakthrough in understanding the mechanistic basis for plastid division was the discovery of a
nuclear gene from Arabidopsis encoding a homologue of a
bacterial cell division protein called FtsZ, an essential
component of the prokaryotic cell division machinery
[10]. The Arabidopsis FtsZ protein, now called AtFtsZ1-1
[11••], shares 40-50% amino acid identity with most of its
prokaryotic counterparts, and is most similar to the FtsZ
sequences from cyanobacteria. AtFtsZ1-1 was shown to be
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Cell biology
targeted to the chloroplast, strongly implicating the protein in chloroplast division and inspiring the hypothesis
that the plastid division machinery in plants has its evolutionary origin in the endosymbiotic progenitor of the
organelles [10]. Two studies have now established that
FtsZ proteins are essential for chloroplast division in
plants [11••,12••], confirming that a prokaryotically based
apparatus functions in plastid division and setting the
stage for advancing our understanding of this critical
process in plant cell biology. Here we briefly summarize
previous work on FtsZ function in bacterial cell division
and then describe the recent findings on the role of these
proteins in plants.
FtsZ function in bacteria
FtsZ is an ancient, highly conserved prokaryotic cytoskeletal protein found both in archaebacteria and eubacteria
[13–15]. It was first identified in a genetic screen for temperature-sensitive mutants of E. coli that were defective in
cell division. These cells formed long filaments at the
restrictive temperature due to incomplete formation of the
division septum (the structure formed by invagination of
the bacterial membranes and cell wall), and were, therefore,
designated fts mutants (filamentation temperature-sensitive) [16]. Although numerous fts genes have been isolated
from bacteria, to date only FtsZ has been extensively characterized with regard to its role in cell division
[17,18,19•,20•]. Immunogold labeling [21] and immunofluorescence localization studies with fusions to green
fluorescent protein [22] have shown that, at an early stage
in the bacterial cell division cycle, FtsZ is recruited to the
presumptive division site where it forms a ring-like structure on the interior surface of the cytoplasmic membrane.
The FtsZ ring constricts during septation, remaining at the
leading edge of the invaginating septum, and disassembles
once septation is complete. The dynamic nature of the
FtsZ ring suggests it has a contractile function that pulls on
the cytoplasmic membrane to initiate cytokinesis, though it
could also act as a scaffold upon which other components of
the division apparatus can assemble. The structure of the
FtsZ ring in vivo is not yet known, but its cytoskeletal properties became evident from experiments demonstrating
that purified FtsZ undergoes GTP-dependent assembly
into polymers that resemble tubulin protofilaments assembled under similar conditions [23–25]. These studies, along
with alignments showing limited but convincing amino acid
sequence similarities between FtsZ and tubulins [25–28],
triggered speculation that prokaryotic FtsZ is the evolutionary progenitor of the eukaryotic tubulins, a hypothesis
strengthened considerably by recent crystallographic data
confirming that FtsZ and tubulins are indeed structural
homologues of one another [29••,30••].
FtsZ function in plants
Two recent studies provide evidence that FtsZ proteins
are essential for chloroplast division in all land plants. In
the first, targeted disruption of PpFtsZ, a nuclear FtsZ
gene from the moss Physcomitrella patens, severely
inhibited chloroplast division in that organism, yielding
cells containing only a single large chloroplast [12••]. In the
second, antisense suppression of the Arabidopsis AtFtsZ1-1
gene described above perturbed division both of mesophyll cell chloroplasts and of proplastids in the shoot apical
meristem, resulting in leaf mesophyll cells containing as
few as one greatly enlarged chloroplast [11••]. These
results confirmed that FtsZ genes are essential for chloroplast division in both lower and higher plants. The latter
investigation went further, however, demonstrating that
the situation is considerably more complex than these
findings initially suggest, at least in higher plants.
Comparisons among the available plant FtsZ sequences
revealed that FtsZ genes fall into two distinct families, designated FtsZ1 and FtsZ2, encoding proteins that differ both
in their overall amino acid sequence similarities and in
their apparent subcellular localizations [11••]. FtsZ1 proteins contain amino-terminal extensions with features
common to chloroplast transit peptides, and at least one
member of this family, AtFtsZ1-1, can be post-translationally imported into isolated chloroplasts where the transit
peptide is processed [10]. FtsZ2 proteins, which include
PpFtsZ from Physcomitrella and a second nuclear-encoded
FtsZ protein from Arabidopsis, called AtFtsZ2-1, lack obvious subcellular sorting signals. Further, AtFtsZ2-1 could
not be imported into isolated chloroplasts or mitochondria
in vitro, strongly suggesting it is a cytosolic protein.
Nevertheless, antisense experiments clearly demonstrated
that AtFtsZ2-1 is also essential for chloroplast and proplastid division in Arabidopsis [11••]. These findings revealed
that at least two functionally distinct, and probably differentially localized, FtsZ gene products mediate plastid
division in higher plants [11••]. The role of FtsZs in plastid division may be more complex, however, as Arabidopsis
contains at least one other FtsZ2 family member [11••].
Two important conclusions can be drawn from the
Arabidopsis study. First, chloroplast division in higher
plants appears to require both plastid-localized and cytosolic forms of FtsZ. These data correspond well with
ultrastructural studies showing that two electron-dense
plastid dividing rings, each localized on opposite sides of
the chloroplast envelope membranes, participate in constriction of the organelle [4••]. Taken together, the
evidence supports a model whereby FtsZ1 and FtsZ2 are
components of the inner and outer plastid dividing rings
respectively, a prediction that can be tested in high-resolution localization studies of AtFtsZ1-1 and AtFtsZ2-1 or their
homologues in other plants. The finding that plastid division is disrupted by reduced expression of either AtFtsZ1-1
or AtFtsZ2-1 further implies that FtsZ1 and FtsZ2 functions are co-ordinated in some way to bring about the
constriction of the chloroplast. Because double plastid
dividing rings have been observed in lower as well as in
higher plants, we expect that an FtsZ1 homologue may
also be identified and shown to be required for chloroplast
division in Physcomitrella.
Plastid division Osteryoung and Pyke
Second, it is apparent that in Arabidopsis the same FtsZ
genes function in the division of both undifferentiated proplastids and differentiated chloroplasts. As the number of
plastids and the relative cell volume occupied by them differs greatly between meristematic and developing
mesophyll cells, these results indicate that AtFtsZ1-1 and
AtFtsZ2-1 accumulation or activity may be differentially
controlled in different types of cells. ARC6 also functions
in the division both of proplastids and of chloroplasts [5,6],
but does not cosegregate with either AtFtsZ gene, raising
the possibility that all three genes are subject to similar
regulatory controls in different cell types.
Bacterial cell division as a model for
identifying new plastid division genes: lessons
and limitations
Although the experiments described above firmly established the prokaryotic origin of the plastid division
apparatus, significant differences exist between plastid
and bacterial cell division. Perhaps the most obvious is that
the former occurs within the environment of the eukaryotic cytosol. A consequence of this is that plastids are not
subject to the osmotic forces experienced by free-living
bacteria, and except for the glaucophyte cyanelles, most no
longer possess the peptidoglycan cell wall present in their
prokaryotic ancestors [31,32]. The studies of FtsZ function
in Arabidopsis [11••] further suggest that specific cytosolic
as well as plastid-localized components participate in plastid division. Nevertheless, the process of bacterial cell
division is clearly a useful, if incomplete, model upon
which to base further analysis of plastid division in plants.
Here we consider how each phase in plastid division
resembles and differs from the analogous phase in bacterial cell division, with an eye towards defining other
potential components of the plastid division apparatus.
Phase one: selection of the division site
Plastid division always occurs at the center of the plastid,
perpendicular to the longitudinal axis [33••]. This implies
that a mechanism exists for ensuring proper placement of
the division machinery. In E. coli, the site of septum formation is under control of the minB locus, which
comprises three genes: minC, minD and minE [34]. Mutant
strains lacking MinC and MinD are characterized by the
formation of ‘minicells’, tiny, nonviable cells lacking chromosomes. Minicells are formed by the frequent
misplacement of the FtsZ ring at a position near the cell
pole that corresponds to the location of the previous division site, resulting in septation near the cell pole rather
than at midcell. This phenotype indicates that the previous sites of septation retain their potential for division
even after separation of the daughter cells, and that MinC
and MinD act together in wild-type cells to inhibit FtsZ
ring assembly at these former division sites [34,35].
Normally the activity of MinC and MinD is restricted to
the former division site near the cell pole. In minE
mutants, however, MinC and MinD can also act at the cell
center, preventing FtsZ ring formation at its normal site
477
and thereby inhibiting cell division. Thus, the function of
MinE is to impart topological specificity to the activity of
MinC and MinD so that division occurs only at the cell
center [34]. This activity involves formation of a MinE
ring at the midcell [36], which is important for FtsZ ring
placement, but not for FtsZ ring assembly per se.
Recent data from two genome sequencing programs suggest that a similar system operates in positioning of the
plastid division apparatus in plants. Homologues of minD
and minE have been identified in the plastid genome of
the unicellular green alga Chlorella vulgaris [37••] and a
MinD homologue has been uncovered in the Arabidopsis
nuclear genome (KA Pyke and KW Osteryoung, unpublished data). The protein encoded by the Arabidopsis gene
includes an amino-terminal extension with characteristics
suggesting a chloroplast targeting function. Although these
Min genes must still be tested for roles in plastid division,
their existence provides evidence that the mechanism controlling placement of the plastid division apparatus has also
been conserved during the evolution of chloroplasts. MinE
has not yet been identified in land plants, but on the basis
of its role in bacteria, it seems probable that a functional
homologue of MinE will be involved in proper positioning
of the plastid division machinery. If a cytosolic FtsZ ring
participates in plastid division as hypothesized [11••] then
additional cytosolic Min proteins or other factors would
presumably be required for correct placement of that structure as well.
Phase two: assembly of the FtsZ ring
The earliest step in the formation of the division septum
in bacteria is assembly of the FtsZ ring at midcell [19•].
Immediately following separation of the daughter cells,
the FtsZ ring disassembles, and for a short period the protein can be detected throughout the cytoplasm before it
reassembles at the new division site. What triggers FtsZ
ring assembly and how the protein becomes localized and
anchored to the membrane are still unknown. One molecule proposed to play an important role, however, is the
recently identified ZipA [38••]. ZipA (Z-interacting protein A), identified biochemically on the basis of its ability
to bind purified FtsZ, is an integral membrane protein
containing a cytoplasmic domain predicted to form a rigid,
rod-like structure. Like FtsZ, the protein localizes in a ring
at midcell early in the division process. These properties
suggest that ZipA acts as a membrane anchor and possibly
stimulatory factor for FtsZ polymerization [18,38 ••].
Exactly how FtsZ ring assembly ensues is not understood,
but evidence suggests that polymerization proceeds bidirectionally from a single nucleation point on the
cytoplasmic membrane [39]. Whether ZipA or some other
factor is involved in the nucleation event is unknown.
Because plant FtsZ proteins, like their bacterial counterparts, lack transmembrane domains, a ZipA-like molecule
may also be necessary for assembly of the plastid dividing
rings in plants. Another possibility, however, is that
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Cell biology
post-translational modification could provide a lipid-soluble membrane anchor allowing plant FtsZ proteins to
reversibly associate with the envelope membranes. Posttranslational modification of bacterial FtsZ has not been
reported, but reversible palmitoylation of tubulin in
human platelets has been demonstrated [40,41]. The
high degree of amino acid conservation between plant
and bacterial FtsZs argues that the polymerization
process itself and structural properties of the FtsZ ring or
rings in plants will closely resemble those in bacteria.
Phases three and four: constriction and
separation
Constriction of dividing bacterial cells is still a poorly
understood process. FtsZ presumably participates, but
several other fts genes whose functions are less well understood are also required. Most of these appear to be
involved either in cell wall peptidoglycan synthesis, which
is essential for septation in E. coli, or in coupling cell wall
synthesis to the FtsZ ring [19•,20•]. These genes, however, are absent in the mycoplasmas, which lack cell walls,
and presumably would not be involved in plastid division
if their functions are specifically related to septal cell wall
ingrowth. It may be that constriction of the plastid still
requires the participation of rigid structures on both envelope surfaces, consistent with the involvement of two
plastid dividing rings and two FtsZ genes in plastid division. Perhaps the requirement for cell wall ingrowth in
bacteria has been supplanted by the evolution of an external plastid dividing ring composed of FtsZ in plants.
At present, we can only speculate on other types of molecules that might play a part in the constriction and
separation phases of plastid division, but one strong contender is ARC5 [3,9]. Chloroplasts in arc5 mutants initiate
but become arrested during constriction, indicating the
gene product acts late in division and may be a component
of the division apparatus. Other potential participants
include molecules that co-ordinate constriction of the two
plastid dividing rings, and those in addition to FtsZ that
contribute to the mechanics of plastid dividing ring constriction. Because the formation of a long, narrow isthmus is
sometimes observed late in plastid division, it is conceivable that other cytoskeletal elements in the cytosol and
their associated motor proteins could facilitate daughter
plastid movement and separation by a pulling mechanism.
Conclusions
The recent studies on plant FtsZ function establish a foundation for further dissecting the components of the plastid
division apparatus. The molecular infrastructure provided
by the Arabidopsis and other genome sequencing efforts
will continue as important resources for identification of
new plastid division genes, though other approaches will
clearly be important as well. Challenges for the future
include determining how the plastid division mechanism is
integrated with the developmental programming to produce different plastid numbers in different cell types, and
discovering how the cell senses and controls chloroplast
compartment volume. Progress in the last two years has
been dramatic and we anticipate that our understanding
will progress significantly in the near future by the
exploitation of both new and existing mutants and genes.
Acknowledgements
We thank members of our two laboratories and M Odell for helpful
discussions. We gratefully acknowledge support to KW Osteryoung from
the National Science Foundation and Nevada Agricultural Experiment
Station, and to KA Pyke from the Biotechnology and Biological Sciences
Research Council.
References and recommended reading
Papers of particular interest, published within the annual period of review,
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• of special interest
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