AOBPreview originally published online on November 30, 2006
Annals of Botany 2007 99(4):565-579; doi:10.1093/aob/mcl249
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INVITED REVIEW |
Plastid Division: Evolution, Mechanism and Complexity
Department of Mathematics and Natural Sciences, University of Stavanger, 4036 Stavanger, Norway
* For correspondence. E-mail simon.g.moller{at}uis.no
Received: 8 August 2006 Returned for revision: 18 September 2006 Accepted: 29 September 2006 Published electronically: 30 November 2006
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ABSTRACT |
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TOP
ABSTRACT
INTRODUCTIONBackground: The continuity of chloroplasts is maintained by division of pre-existing chloroplasts. Chloroplasts originated as bacterial endosymbionts; however, the majority of bacterial division factors are absent from chloroplasts and the eukaryotic host has added several new components. For example, the ftsZ gene has been duplicated and modified, and the Min system has retained MinE and MinD but lost MinC, acquiring at least one new component ARC3. Further, the mechanism has evolved to include two members of the dynamin protein family, ARC5 and FZL, and plastid-dividing (PD) rings were most probably added by the eukaryotic host.
Scope: Deciphering how the division of plastids is coordinated and controlled by nuclear-encoded factors is key to our understanding of this important biological process. Through a number of molecular-genetic and biochemical approaches, it is evident that FtsZ initiates plastid division where the coordinated action of MinD and MinE ensures correct FtsZ (Z)-ring placement. Although the classical FtsZ antagonist MinC does not exist in plants, ARC3 may fulfil this role. Together with other prokaryotic-derived proteins such as ARC6 and GC1 and key eukaryotic-derived proteins such as ARC5 and FZL, these proteins make up a sophisticated division machinery. The regulation of plastid division in a cellular context is largely unknown; however, recent microarray data shed light on this. Here the current understanding of the mechanism of chloroplast division in higher plants is reviewed with an emphasis on how recent findings are beginning to shape our understanding of the function and evolution of the components.
Conclusions: Extrapolation from the mechanism of bacterial cell division provides valuable clues as to how the chloroplast division process is achieved in plant cells. However, it is becoming increasingly clear that the highly regulated mechanism of plastid division within the host cell has led to the evolution of features unique to the plastid division process.
Key words: Arabidopsis, ARC, E. coli cell division, Min system, plastid division, FtsZ
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INTRODUCTION |
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Plastids are essential plant organelles in which photosynthesis and many other fundamental intermediary metabolic reactions are housed (reviewed in Tetlow et al., 2004). In plants, an integral part of chloroplast development is division, as they are not created de novo but arise by division from pre-existing plastids in the cytosol. Chloroplasts are derived from cyanobacteria that were engulfed by a heterotrophic eukaryotic host cell (Gray, 1999; McFadden, 1999) and, reminiscent of their prokaryotic ancestors chloroplasts, divide by binary fission. This led to a number of groups investigating the possibility that essential bacterial cell division genes have been conserved through the evolution of the chloroplast division machinery. Using the Escherichia coli and cyanobacterial cell division proteins as input sequences, Arabidopsis has been found to encode functional homologues of the bacterial cell division proteins FtsZ (Osteryoung and Vierling, 1995; Osteryoung et al., 1998), MinD (Colletti et al., 2000; Dinkins et al., 2001), MinE (Itoh et al., 2001; Maple et al., 2002; Reddy et al., 2002) and GC1/SulA (Maple et al., 2004; Raynaud et al., 2004). Further components of the chloroplast division machinery were identified through cloning of the disrupted loci in several of the accumulation and replication of chloroplasts (arc) mutants, a collection of ethylmethane sulfonate- and T-DNA-mutagenized seedlings with altered numbers of chloroplasts in mesophyll cells (Pyke and Leech, 1991; Rutherford, 1996). The identification of ARC5 (Gao et al., 2003), ARC6 (Vitha et al., 2003) and ARC3 (Shimada et al., 2004) provided insights into the complex evolution of the chloroplast division machinery. More recently, the identification of components that affect chloroplast division but are not directly involved in the division machinery, such as the MSL proteins (Haswell and Meyerowitz, 2006), has added another level of complexity to our understanding of the division process.
The continued identification of new plastid division proteins means that it is now possible to begin to address the evolution, mechanism and complexity of the plastid division machinery. It is well established that the chloroplast division machinery requires components of both prokaryotic and eukaryotic origin, but how these are coordinated is still unclear. Although the components of prokaryotic origin have been shown to share many functional features with their prokaryotic counterparts, the recent identification and functional characterization of new components is beginning to shed light on how the division machinery has evolved to adapt to the environment of the chloroplast. Furthermore, although in its infancy, studies addressing the regulation of the chloroplast division mechanism are starting to reveal how the division process may be controlled and coordinated by the host cell.
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COMPONENTS OF PROKARYOTIC ORIGIN |
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Bacteria have sophisticated molecular machineries dedicated to regulate their growth and division with remarkable accuracy. Because of the endosymbiotic origin of chloroplasts, it was speculated relatively early that plastid division might share common features with bacterial cell division. In the last few years, substantial progress has been made in several aspects of cell division, particularly the molecular basis for Z-ring placement by the Min system, the assembly of the division protein machinery and the solution of the crystal structures of several division proteins (reviewed in Rothfield et al., 2005). The superiorly defined status of the bacterial cell division system has made it an invaluable tool to accelerate the investigation of the molecular mechanism of plastid division, and recent evidence has begun to shed light on the similarities and differences between cell and chloroplast division.
The plastid FtsZ ring(s)
The identification of a homologue of the bacterial cell division protein FtsZ in the nuclear genome of Arabidopsis (Osteryoung and Vierling, 1995) led to the concept that chloroplast division utilizes at least part of the ancestral bacterial division machinery. Since then, FtsZ genes have been identified in many plant and algae species (reviewed in Gilson and Beech, 2001), indicating that the FtsZ protein is a universal component of the plastid division machinery.
The FtsZ protein of E. coli was initially identified as part of a screen for temperature-sensitive E. coli mutants, designated fts (filamentous temperature sensitive), which show a filamentous phenotype because they are unable to divide under non-permissive temperatures (Bi and Lutkenhaus, 1991; Dai and Lutkenhaus, 1991). FtsZ is by far the most conserved bacterial cell division protein, with FtsZ proteins from widely divergent bacteria showing approx. 50 % amino acid identity. FtsZ is essential throughout the process of cell division (Ma et al., 1996; Bramhill, 1997; Lutkenhaus and Addinall, 1997; Rothfield and Justice, 1997; Margolin, 2000; Addinall and Holland, 2002; Romberg and Levin, 2003). FtsZ self-assembles into a contractile ring (Z-ring) beneath the cytoplasmic membrane at the division site (Addinall et al., 1996; Ma et al., 1996), and the formation of the Z-ring after daughter chromosome segregation is believed to be the earliest event in the cell division process. The Z-ring is essential for the hierarchical recruitment of at least ten other proteins (ZipA, FtsA, FtsE, FtsX, FtsK, FtsQ, FtsL, FtsW, FtsI and FtsN) that are recruited to the septum to form the divisome. All of the components of the divisome are required for the progression and completion of cell division (Ma et al., 1996; Addinall and Lutkenhaus, 1996; Lutkenhaus and Addinall, 1997; Wang et al., 1997; Din et al., 1998; Chen et al., 1999; Ma and Margolin, 1999; Weiss et al., 1999; Goehring at al., 2006; Vicente et al., 2006).
The precise role of FtsZ during cell division is not known. It is possible that FtsZ function is limited to its role as a scaffold protein during divisome assembly, but the FtsZ ring remains associated with the septum throughout division and could therefore play an active role in the ingrowth of the new septum. In support of this model, in the prokaryote mycoplasma, which lacks a cell wall and contains a small genome, FtsZ is the only conserved cell division protein and is thought to be sufficient to complete the division process (Margolin, 2001).
In contrast to bacteria that contain a single ftsZ gene, paralogues of ftsZ have arisen in higher plants and algae which contain several FtsZ genes that are clustered into two families termed FtsZ1 and FtsZ2 (Osteryoung et al., 1998; Osteryoung and McAndrew, 2001; Stokes and Osteryoung, 2003). The mature Arabidopsis AtFtsZ1-1 and AtFtsZ2-1 proteins show approx. 40 % similarity and 30 % identity to the E. coli FtsZ protein, respectively. The duplication of the FtsZ gene is believed to have occurred in the cyanobacterial progenitor of chloroplasts between the divergence of red and green algae (Stokes and Osteryoung, 2003).
In Arabidopsis, both AtFtsZ1-1 and AtFtsZ2-1 are imported into chloroplasts and co-localize to a ring-like structure at the chloroplast division site on the stromal side of the chloroplast envelope (Fig. 1B; Fujiwara and Yoshida, 2001; McAndrew et al., 2001; Vitha et al., 2001). Similar to the bacterial homologues, AtFtsZ1-1 and AtFtsZ2-1 can both form dimers and heterodimers in planta (Fig. 1A; Maple et al., 2005), and AtFtsZ1-1 has been shown to polymerize in vitro (El-Kafafi et al., 2005). The exact composition of the Z-ring is still uncertain, and determination of this will help shed light on the precise function of the two FtsZ proteins. The interaction between the FtsZ proteins in both bacteria and plants requires the central region [E. coli: amino acids 100–326 (Wang et al., 1997) and Arabidopsis: amino acids 145–302 (Maple et al., 2005)] and like the bacterial FtsZ proteins AtFtsZ1-1 and AtFtsZ2-1 can polymerize into additional structures including filaments and mini-circles in planta (Erickson et al., 1996; Maple et al., 2005). This suggests that the Arabidopsis Z-ring(s) may resemble the bacterial Z-ring. In prokaryotes, the estimated number of FtsZ molecules per cell (estimates between 4000 and 15 000; Lutkenhaus, 1993; Lu et al., 1998; Rueda et al., 2003) indicates that the Z-ring is probably composed of protofilaments organized into a spiral structure rather than closed rings. However, in plants, this model will be further complicated by the presence of two forms of functional FtsZ protein.
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Disruption of FtsZ protein levels in chloroplasts of Arabidopsis, Physcomitrella patens and tobacco has confirmed that they are essential division proteins (Osteryoung et al., 1998; Strepp et al., 1998; Stokes et al., 2000). In Physcomitrella, a knockout of FtsZ2-1 causes inhibition of chloroplast division and cells contain only one large chloroplast (Strepp et al., 1998). The same phenotype is observed in Arabidopsis where depletion of either AtFtsZ1-1 or AtFtsZ2-1 causes inhibition of chloroplast division, resulting in one large chloroplast per mesophyll cell (Osteryoung et al., 1998), demonstrating that rather than being redundant each FtsZ protein has a distinct function. The correct stoichiometric amount of each Arabidopsis FtsZ protein is essential for correct plastid division to occur, since slight overexpression of either protein leads to chloroplast division arrest (Stokes et al., 2000).
Since the discovery of two families of FtsZ proteins in plants and algae, there has been much speculation as to how they are functionally distinct. Sequence comparisons reveal that AtFtsZ1-1 and AtFtsZ2-1 are highly similar and at the secondary and tertiary level both are almost identical to the bacterial FtsZ proteins (Stokes and Osteryoung, 2003). The mature AtFtsZ1-1 and AtFtsZ2-1 proteins are composed of a variable N-terminal segment, a highly conserved central region and a more variable C-terminal region. The central region contains the Rossmann fold, a motif frequently found in nucleotide-binding proteins (Löwe and Amos, 1998). The Rossmann fold harbours the GTP-binding tubulin signature motif GGGTG(T/S)G (de Boer et al., 1992a; RayChadhuri and Park, 1992) and contains additional residues that contact the guanine nucleotide (Wang et al., 1997; Löwe and Amos, 1999; Osteryoung and McAndrew, 2001). In AtFtsZ1-1, but not AtFtsZ2-1, one of these residues is substituted, possibly representing an important divergence between these two protein families (Stokes and Osteryoung, 2003). However, although there are no experimental data, the high level of conservation of the Rossmann fold suggests that both AtFtsZ1-1 and AtFtsZ2-1 are functional GTPases. The GTPase activity of seven FtsZ proteins has been confirmed (de Boer et al., 1992a; Wang and Lutkenhaus, 1993; Lu et al., 1998; Sossong et al., 1999; Nagahisa et al., 2000; Rajagopalan et al., 2005), although the in vivo significance is yet to be established. It is, however, speculated that the contraction of FtsZ probably involves GTP hydrolysis and that polymerized-induced GTP hydrolysis is sufficient to provide the force for division. The establishment of the precise role of GTP hydrolysis by FtsZ in any species will have wide-reaching implications in both the chloroplast and bacterial cell division fields.
Interestingly, FtsZ is structurally and evolutionarily related to the eukaryotic tubulins, the main component of microtubules in eukaryotic cells, and the 3D structures of FtsZ and the 
ß tubulin dimer revealed that the overall structures of the two proteins are nearly identical (Lowe and Amos, 1998; Nogales et al., 1998). The greatest divergence between structures is found between the C-terminal domain of FtsZ and tubulin. The C-terminal tail of tubulin lies on the outside of the microtubule where it interacts with motor proteins (Desai and Mitchison, 1997). Based on the structural similarity of FtsZ to tubulin, the C-terminal tail of FtsZ is predicted to lie on the outside of the FtsZ filaments, locating the region to interact with accessory proteins of the division machinery. Indeed, in E. coli, the extreme C-terminal CORE domain of FtsZ is essential for the interaction of FtsZ with both FtsA and ZipA (Wang et al., 1997; Din et al., 1998; Liu et al., 1999; Hale et al., 2000; Mosyak et al., 2000; Yan et al., 2000). The core domain is a surface-exposed hydrophilic domain at the extreme C-terminal end with the highly conserved sequence (D/E-I/V-P-X-F/Y-L) (Ma and Margolin, 1999). The core domain is conserved in all FtsZ2 proteins but absent in all FtsZ1 proteins. Although there are no homologues of FtsA or ZipA in the genomes of plants, it was recently found that the Arabidopsis plastid division protein ARC6 (see below) interacts specifically with AtFtsZ2-1 but not with AtFtsZ1-1, in vitro and in planta, and that this interaction is mediated by the CORE domain (Fig. 1A; Maple et al., 2005).
The absence of the CORE domain in all FtsZ1 family proteins suggests that the acquisition of an additional FtsZ protein, lacking the CORE domain, is an essential requirement of the plastid division process. The first evidence for the specific role of the FtsZ1 proteins was discovered earlier this year when it was found that AtFtsZ1-1 but not AtFtsZ2-1 interacts with the stromal plastid division component ARC3 (see below). Furthermore, this interaction is mediated by the C-terminus of AtFtsZ1-1, again providing evidence that the C-terminal tails of the two families of FtsZ have been modified significantly during evolution to fulfil separate roles in the dividing chloroplasts, allowing additional protein components to interact with the Z-ring during plastid division. Although the functions of the accessory proteins remain to be identified, further analysis of the role of the FtsZ–accessory protein interactions will shed light on the requirement for the evolution of two forms of FtsZ.
The role of AtMinD1 and AtMinE1 in division site selection in chloroplasts
In E. coli, the localization of the division plane is remarkably precise (reviewed in Rothfield et al., 2005). The correct position of the Z-ring at the cell centre is mediated, in part, by the proteins encoded by the minB operon, MinC, MinD and MinE (de Boer et al., 1990). After the discovery of the FtsZ genes in the nuclear genome of Arabidopsis, database searches led to the discovery of homologues of the bacterial minD and minE genes in many higher plants and algae; however, to date, no homologue of minC has been identified.
The min mutants of E. coli are so called because septal placement is perturbed in these mutants, resulting in the frequent occurrence of division at the cell poles instead of at midcell, and formation of small anucleate cells (minicells) (de Boer et al., 1989). MinC, MinD and MinE work in concert to prevent septation at potential division sites located near the cell poles. MinC is a non-specific inhibitor of FtsZ polymerization, binding to and disrupting FtsZ polymers to prevent the formation of a stable Z-ring (Hu and Lutkenhaus, 2000). Topological specificity is conferred on MinC activity by the combined action of MinE and MinD. The primary function of MinD is to enhance MinC activity, but MinD is also responsible for the association of MinC and MinE with the cell membrane. MinD is a member of a large family of ATPases and, when bound to ATP, recruits MinC to the membrane, forming a stable inhibition complex at the pole of the cell (de Boer et al., 1991, 1992b; Huang and Lutkenhaus, 1996; Huang et al., 2003; Zhou and Lutkenhaus, 2004). MinE is a topological specificity factor and acts by stimulating the ATPase activity of MinD, resulting in MinD dissociating from the membrane and relocating to the opposite pole (Fu et al., 2001; Huang et al., 2003). This results in a remarkable oscillatory behaviour of the MinCD proteins that are capable of marking a midcell site by ensuring the lowest concentration of the MinC–MinD inhibition complex at the mid-point of the cell.
Homologues of minD and minE were first identified in the plastid genome of the unicellular chlorophyte Chlorella vulgaris (Wakasugi et al., 1997). This was followed by the identification of homologues of minD and minE in the nuclear genome of Arabidopsis (Colletti et al., 2000; Itho et al., 2001; Maple et al., 2002), tobacco (Dinkins et al., 2001; Reddy et al., 2002), rice and marigold (Moehs et al., 2001), indicating that a Min-like system is a highly conserved component of the plastid division machinery. The Arabidopsis homologues, referred to as AtMinD1 and AtMinE1, share approx. 60 and 20 % amino acid similarity to MinD and MinE from E. coli, respectively.
AtMinD1 and AtMinE1 are both stromal chloroplast division components (Colletti et al., 2000; Itho et al., 2001; Maple et al., 2002). The role of the Arabidopsis Min proteins in plastid division site selection was clearly demonstrated by the observation that decreased levels of functional AtMinD1 (Colletti et al., 2000; Fujiwara et al., 2004) or elevated levels of AtMinE1 (Maple et al., 2002) result in asymmetric chloroplast division events. In these plants, the division site is frequently observed towards the poles of the chloroplasts, resulting in a heterogeneous population of enlarged and ‘mini’ chloroplasts within individual cells. The heterogeneity in chloroplast size is reminiscent of the asymmetric division and subsequent minicell formation in E. coli when MinD is inactivated or MinE is overexpressed (de Boer et al., 1989). Analogous to their bacterial counterparts (de Boer et al., 1989), overexpression of AtMinD1 (Colletti et al., 2000) or decreased levels of AtMinE1 (J. Maple and S. G. Møller, unpubl. res.) results in inhibition of the chloroplast division process. Furthermore, expression of AtMinE1 or AtMinD1 in wild-type E. coli cells phenocopies the effects of overexpressing the endogenous Min proteins (Maple et al., 2002; J. Maple and S. G. Møller, unpubl. res.). This suggests that the Arabidopsis Min proteins are functionally conserved to their bacterial counterparts. In compelling support of this, AtMinE1 can complement an E. coli strain null for minE (J. Maple and S. G. Møller, unpubl. res.). Whilst these data clearly indicate that at the phenotypic level the Min proteins of Arabidopsis are highly conserved with their bacterial counterparts, mounting molecular and biochemical data are only now revealing the levels of mechanistic conservation between the two systems.
AtMinD1 contains a deviant Walker A motif responsible for ATP binding and hydrolysis (Aldridge and Møller, 2005). Biochemical data have also revealed that like MinD from E. coli and Neisseria gonorrhoea, AtMinD1 is a functional but weak ATPase and, like the bacterial proteins, is stimulated by AtMinE1 (de Boer et al., 1991; Aldridge and Møller, 2005; Eng et al., 2006). However, detailed biochemical studies have revealed differences between the way the bacterial and plant proteins function: the stimulation of AtMinD1 by AtMinE1 can occur independently of membrane binding, in contrast to the phospholipid-dependent MinE stimulation of E. coli MinD, and the E. coli MinE is unable to stimulate AtMinD1 activity (Aldridge and Møller, 2005). Additionally, in contrast to its bacterial counterpart, the ATPase activity is activated by Ca2+ rather than Mg2+ (de Boer et al., 1991: Aldridge and Møller, 2005). These differences probably signify an evolutionary adaptation as many plant processes are regulated by calcium (Sai and Johnson, 2002).
At the molecular level, both AtMinD1 and AtMinE1 can homodimerize and interact with each other, suggesting that, like their bacterial counterparts, AtMinD1 and AtMinE1 operate as a complex during plastid division (Fig. 1: Huang et al., 1996; Maple et al., 2005). These interactions are conserved between Arabidopsis and E. coli proteins, suggesting that the precise determinants that mediate these interactions are conserved (J. Maple and S. G. Møller, unpubl. res.). The importance of the dimerization of AtMinD1 has been determined through analysis of ARC11 in which a point mutation in the C-terminal helix of AtMinD1(A296G) abolishes the ability of AtMinD1 to dimerize, resulting in frequent asymmetric chloroplast division events (Fujiwara et al., 2004).
Analysis of the localization of AtMinD1 and AtMinE1 in Arabidopsis and tobacco revealed subtle difference in their intraplastidic distribution (Maple et al., 2002, 2005). AtMinD1–YFP (yellow fluorescent protein) localizes to one or two discrete spots at polar zones of chloroplasts, whilst AtMinE1–YFP localizes most commonly to a single spot or as two spots in close proximity towards one end of the chloroplast. Both AtMinE1 and AtMinD1 localize in close proximity to the chloroplast membrane (Maple et al., 2002). Analysis of the AtMinD1(A296G) (Fujiwara et al., 2004) and a truncated form of AtMinD1 lacking the C-terminal helix (J. Maple and S. G. Møller, unpubl. res.) reveals that, like the bacterial counterparts, this membrane localization of AtMinD1 is probably mediated by the C-terminal amphipathic helix (Szeto et al., 2002). The determinants that mediate the localization of AtMinE1 are as yet unknown.
Taken together with the fact that the observed interactions between the Arabidopsis Min proteins are relatively weak (Maple et al., 2005), the subtle differences in the localization patterns of the two proteins probably reflect that AtMinD1 and AtMinE1 exhibit dynamic localization during the division process. Further support for this is provided by the finding that AtMinE1 has been observed to exhibit dynamic behaviour in E. coli reminiscent of the endogenous E. coli MinE end-to-end oscillatory patterns (Fu et al., 2001; Maple et al., 2002).
How the bacterial model might be extrapolated to explain Min protein movement in plastids is still unclear. Analogous to the E. coli system, the stimulation of AtMinD1 ATPase activity by AtMinE1 (de Boer et al., 1991; Aldridge and Møller, 2005) may lead to the release of MinD-ADP from the chloroplast membrane and redistribution to the opposite pole of the chloroplast, thus establishing a ‘pole-to-pole’ oscillation pattern (Fig. 2A). In E. coli, the Min proteins are redistributed along coiled polymers that extend along the inner surface of the cytoplasmic membrane (Shih et al., 2003). There is currently no evidence that the Arabidopsis Min proteins can form filamentous structures; however, if they form similar structures during the chloroplast division process, then it is possible that AtMinE1 and AtMinD1 travel around the chloroplast along a spiral pathway in association with the membrane to circumvent the thylakoid membranes. Alternatively, the Min proteins may move in an analogous manner to the Min proteins in spherical cells (Fig. 2B) such as the E. coli round-cell rodA mutant or naturally spherical species such as N. gonorrhoeae (Westling-Haggstrom et al., 1977; Donachie et al., 1995; Begg and Donachie, 1998; Zaritsky et al., 1999; Pas et al., 2001). In spherical rodA cells, the Min proteins move to and from multiple sites on the cell surface, tending to move a certain maximum distance from their previous site and as a result favour movement along the cell's long axis. When the cell enters division, the Min proteins oscillate parallel to the long axis and symmetric division occurs (Corbin et al., 2002). A third alternative is that, as in Bacillus subtilis, which has homologues of MinC and MinD (Levin et al., 1992) but in which topological control of MinCD activity is provided by DivIVA, there is no oscillation of the proteins (Fig. 2C): DivIVA is stably associated with the cell poles and recruits MinCD to the cell poles, thus preventing FtsZ polymerization at polar division sites (Marston et al., 1998; Marston and Errington, 1999; Karoui and Errington, 2001). Finally, AtMinE1 and AtMinD1 may have established a novel oscillatory mechanism to avoid the thylakoid membrane network, and detailed analysis of the dynamics of the Min complex during plastid division will be required to establish this (Fig. 2D).
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The missing MinC component?
The components of the Min system are distributed unequally among bacteria, suggesting that many ways have evolved for a Min-like system to regulate the position of the Z-ring (reviewed in Margolin, 2002). However, the strict conservation of homologues of FtsZ, MinE and MinD in higher plants has made the absence of a homologue of MinC puzzling.
ARC3 was initially identified through cloning of the disrupted loci in arc3 (Shimada et al., 2004). ARC3 (At1g75010) encodes a protein of 742 amino acids and was initially described as a cytoplasmic chloroplast division protein localizing to the outer membrane of the chloroplast (Shimada et al., 2004); however, recent data show that ARC3 is in fact a bona fide stromal plastid division component (J. Maple and S. G. Møller, unpubl. res.). ARC3 is a chimeric protein consisting of an N-terminal region with homology to prokaryotic FtsZ proteins and a C-terminal domain containing MORN (membrane occupation and recognition nexus) repeats linked by a unique middle region. It was suggested that ARC3 was a novel chimera of a prokaryotic ftsZ gene and a eukaryotic phosphatidylinositol-4-phosphate 5-kinase (PIP5K) gene (Shimada et al., 2004). However, the homology of ARC3 to PIP5K is limited to the MORN repeat region and, since ARC3 lacks all catalytic residues important for PIP5K function, it is possible that ARC3 is of prokaryotic origin, arising by fusion of a prokaryotic FtsZ and MORN repeat-containing protein.
The number of chloroplasts in mesophyll cells of arc3 plants was documented as being the same as the final proplastid number (Pyke and Leech, 1992: Marrison et al., 1999); however, arc3 chloroplasts have a wider size distribution than wild-type or arc5 chloroplasts (Pyke 2 and Leech, 1994). Recently, detailed analysis has documented size heterogeneity and asymmetric division site placement. This reveals that decreased levels of ARC3 disrupt division site placement and suggests that ARC3 may function as part of the Min system (J. Maple and S. G. Møller, unpubl. res.). In support of this hypothesis, it was found that overexpression of ARC3 results in the arrest of division. This is compelling since in E. coli MinC lacks site specificity and, when overexpressed, causes a global block in cell division and the formation of long filaments (de Boer et al., 1989).
MinC acts as a dimer and is the primary FtsZ-destabilizing agent, binding to and disrupting FtsZ polymers (Hu and Lutkenhaus, 2000). ARC3 was found to dimerize and interact through the N-terminal FtsZ-like domain with AtFtsZ1-1 but not with AtFtsZ2-1 (Fig. 1). As expected of a protein partner of AtFtsZ1-1, ARC3 localizes to a ring-like structure and co-localizes with AtFtsZ1-1 (Shimada et al., 2004; J. Maple and S. G. Møller, unpubl. res.). ARC3 has also been observed to localize to discrete loci in chloroplasts in close association with the chloroplast membrane. These patterns are reminiscent of the localization of AtMinE1 and AtMinD1, and quantitative yeast two-hybrid and bimolecular fluorescence complementation assays have revealed that ARC3 can also interact with both AtMinE1 and AtMinD1 through the unique middle domain (Fig. 1).
Although there is currently no evidence that ARC3 can perturb the Z-ring structure in Arabidopsis, the results of such assays will greatly help to increase our understanding of division site placement in Arabidopsis and point to whether ARC3 represents the sole replacement of MinC or whether additional components have evolved to function in the higher plant Min system.
How might ARC3 function as part of the Min system in Arabidopsis? The interaction of MinC with MinD is required to activate MinC-mediated division inhibition (de Boer et al., 1991; Zhou and Lutkenhaus, 2004), and determining whether MinD has a similar effect on ARC3 will be very important. Interestingly, MinC and MinE interact with the surface of MinD at two overlapping sites so that the binding of one protein to MinD displaces the other. The middle domain of ARC3 mediates the interaction of both AtMinD1 and AtMinE1, and it will be important to determine how this is of functional significance during chloroplast division.
Other components of prokaryotic origin
ARC6 is a homologue of the bacterial Ftn2 cell division protein and was originally identified through cloning of the arc6 mutant (Pyke et al., 1994; Vitha et al., 2003). ARC6 encodes an 810 amino acid protein containing regions of homology to Ftn2 and an N-terminal J-domain motif characteristic of DNAJ chaperones (Vitha et al., 2003). ARC6 spans the inner chloroplast envelope membrane, with the N-terminus, including the J-domain, extending into the chloroplast stroma (Vitha et al., 2003), and localizes to a discontinuous ring-like structure at the chloroplast division site (Vitha et al., 2003; Maple et al., 2005). Depletion of the cyanobacterial homologue of ARC6, Ftn2, results in a global cell division block and a subsequent filamentous cell phenotype (Koksharova and Wolk, 2002). Similarly arc6 mesophyll cells contain one giant chloroplast per cell (Vitha et al., 2003). However, the function of Ftn2 remains to be elucidated.
ARC6 has been shown to interact with the CORE domain of AtFtsZ2-1 (Fig. 1; Maple et al., 2005). In E. coli, the CORE domain of FtsZ mediates the interaction with both FtsA and ZipA proteins. FtsA and ZipA are believed to be involved in regulating or controlling the FtsZ polymerization reaction. Although no homologues of these bacterial proteins have been identified in the genomes of higher plants or cyanobacteria, ARC6 may prove to play a role analogous to that of FtsA and ZipA, stabilizing or anchoring the Z-ring. Indeed Z-ring formation by either FtsZ protein is dependent on functional ARC6 since in the arc6 background both AtFtsZ1-1 and AtFtsZ2-1 form short filaments (Vitha et al., 2003). Furthermore, in plants overexpressing ARC6, FtsZ filaments are more numerous and form spiral patterns around the enlarged chloroplast. This is particularly interesting in light of the discovery that ARC6 interacts specifically with AtFtsZ2-1, and it is possible that inner membrane-bound AtFtsZ2-1 is stabilized though its interactions with ARC6 and that, subsequently, AtFtsZ1-1 polymerizes and interacts with AtFtsZ2-1, allowing further protein recruitment to the site of division.
Quantitative yeast two-hybrid assays using truncated forms of the ARC6 stromal domain revealed that the conserved domain was sufficient for the interaction between ARC6 and AtFtsZ2-1 and that this interaction was not dependent on the presence of the J-domain (Maple et al., 2005). Proteins containing J-domains are found in most organisms where the J-domain interacts with Hsp70 proteins stimulating the Hsp70 ATPase activity necessary for stable binding to its protein substrate (Bukau and Horwich, 1998). Additionally, J-domain proteins can associate with substrates of the chaperone system and prevent their aggregation (Han and Christen, 2004). In E. coli, HscA (an Hsp70 family protein) is involved in FtsZ-ring formation through a chaperon-like interaction with FtsZ (Uehara et al., 2001), and it is attractive to speculate that ARC6 may play a similar role in Arabidopsis, associating with AtFtsZ2-1 and then transferring AtFtsZ2-1 to an Hsp70-like protein.
GIANT CHLOROPLAST 1 (GC1) (also called AtSulA) is a descendant of a cyanobacterial cell division inhibitor (Maple et al., 2004; Raynaud et al., 2004). GC1 is plastid localized and is anchored to the stromal surface of the chloroplast inner envelope by a C-terminal amphipathic helix. GC1–YFP localizes uniformly to the entire chloroplast envelope in transgenic Arabidopsis plants, as well as in a number of arc mutants, indicating that the entire Arabidopsis chloroplast envelope is competent for GC1 recruitment and, furthermore, that GC1's mode of action is probably envelope associated (Fig. 1B; Maple et al., 2004).
A role for GC1 in chloroplast division was initially demonstrated through analysis of transgenic Arabidopsis plants with greatly reduced (approx. 95 %) levels of GC1 transcript showing a complete arrest of plastid division, suggesting that GC1 acts early during the division (Maple et al., 2004). Reports on the effect of the overexpression of GC1 are conflicting; initial studies demonstrated that plants in which there is a > 250 % rise in transcript levels maintain a wild-type chloroplast division profile (Maple et al., 2004) but, subsequently, transgenic Arabidopsis plants overexpressing a GC1–YFP fusion protein were shown to harbour a range of chloroplast numbers per cell [60 % with 80 (wild type-like); 11 % with 40–60, 24 % with 10–40 and 2 % with one chloroplast per cell] although overexpression did not alter plastid division in the same way in all plants from the same line or in all cells (Raynaud et al., 2004). Clearly further functional analysis of GC1 is required to resolve these discrepancies and will aid in the elucidation of the role of GC1 in the plastid division process.
Sequence analysis has suggested two possible functions for GC1: that of a SulA-like protein or a nucleotide–sugar epimerase. SulA in E. coli is part of the SOS response, mediating a stress-dependent division checkpoint when DNA damage occurs. SulA specifically inhibits the GTPase activity of FtsZ and the ability of FtsZ to form polymers though a direct interaction (Bi and Lutkenhaus, 1990, 1993). Since SulA functions by binding to FtsZ in a 1 : 1 ratio, one would expect that a SulA protein in Arabidopsis would interact with either AtFtsZ1-1 or AtFtsZ2-1. However, no interaction between GC1 and AtFtsZ1-1 or AtFtsZ2-1 is detected in the yeast two-hybrid system (Maple et al., 2004; Raynaud et al., 2004). In addition, E. coli sulA mutants show no cell division phenotype (Huisman et al., 1984) and this is in contrast to results obtained in Synechocystis where reduced levels of slr1223 revealed that slr1223 is required for correct cell division (Raynaud et al., 2004). Additionally, the phylogenetic evidence to maintain that GC1 is a SulA-like protein is weak: the similarity between the E. coli SulA protein and GC1 or slr1223 is low (11 and 19 %, respectively), whereas GC1's closest homologue in E. coli, YfcH, is approx. 51 % similar to both GC1 and slr1223 proteins, indicating that GC1 and slr1223 are more closely related to YfcH than the SulA protein of E. coli. YfcH is of unknown function, and it will be interesting to discover whether this protein is involved in cell division.
At the secondary structure level, GC1 has high (80–90 %) structural similarity to nucleotide–sugar epimerases and contains the epimerase active site residues serine and tyrosine in the correct protein environment, and the GxxGxxG motif which is involved in binding the cofactor NAD(P)+ (Allard et al., 2001). Epimerases can be found in animals, plants and microorganisms where they control and change the stereochemistry of carbohydrate–hydroxyl substitutions, often modifying protein activity or surface recognition (Baker et al., 1998). Interestingly, mutations in htrM, which encodes an epimerase in E. coli, result in a minicelling phenotype (Raina and Georgopoulos, 1991). HtrM is required for lipopolysaccharide biosynthesis and is upregulated in response to heat shock (Pegues et al., 1990). However, the function of GC1 during chloroplast division remains unclear and it is possible that GC1 has epimerase activity. GC1 can form homodimers, which is a common trait among prokaryotic epimerases (Thoden et al., 2002), and close homologues of GC1 in Arabidopsis have been shown to be active epimerases. The prospect of a link between the regulation of chloroplast division and the modification of lipids in the chloroplast membrane or of glycoproteins is intriguing and certainly worthy of further investigation.
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COMPONENTS OF EUKARYOTIC ORIGIN |
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Cytosolic chloroplast division rings
Ultrastructural studies revealed that plastid division entails the coordinated action of components on the stromal and cytoplasmic faces of the chloroplast envelope. These components were originally visualized in 1981 as fuzzy plaques of electron-dense material covering or displacing the constricting isthmus of dividing chloroplasts (Leech et al., 1981). However, detailed studies utilizing Cyanidium caldarium and Avena sativa later revealed these plaques to be composed of electron-dense ring-like structures on both the stromal and outer face of the envelope, termed the inner and outer plastid division (PD) rings, respectively (Hashimoto, 1986; Mita et al., 1986). The two PD rings have now been detected in many plant and algal species, and are thought to represent a universal feature of dividing chloroplasts in all plant cells. Additionally, a middle PD ring has been identified in the intermembrane space of single chloroplasts found in the unicellular red alga Cyanidioschyzon merolae (Miyagishima et al., 2001a).
It was originally hypothesized that at least the inner PD ring may be composed of FtsZ filaments; however, detailed studies revealed that in C. merolae the Z-ring forms 3–4 h before the formation of the PD rings and it is now believed that the PD ring system has probably been recruited from the eukaryotic host. Additionally, it was found that all three rings form before any visual constriction of the division site, leading to the suggestion that Z-ring placement pre-determines the site of PD ring formation (Kuroiwa et al., 2002). The composition of all PD rings remains unknown; however, the timing of assembly and the behaviour of each ring is different, suggesting that the composition of each is different: the inner PD ring forms first, followed by the middle and outer PD rings (Miyagishima et al., 2001b). Late in constriction, the middle and inner PD rings disassemble before the daughter plastids are severed, whilst the outer PD ring remains attached until after completion of division and then disassembles, suggesting that the outer PD ring is required to complete division (Miyagishima et al., 2001b).
The first component of eukaryotic origin to be identified, ARC5 (DRP5B), was identified through cloning of the arc5 mutant (Robertson et al., 1996; Gao et al., 2003). ARC5 is a dynamin-like protein and harbours an N-terminal GTPase domain, a pleckstrin homology (PH) domain and a C-terminal GTPase effector domain. Interestingly, the ARC5 transcript is alternatively spliced, resulting in two cDNA populations that encode proteins of 777 and 741 amino acids. These protein products are identical, with the exception of a 36 amino acid deletion in the smaller protein that results in a shorter PH domain. PH domains have been implicated in membrane localization, and it has been suggested that the two transcripts may encode proteins with different functions or localization patterns (Miyagishima et al., 2001c; Klockow et al., 2002; Gao et al., 2003). Because some dynamin strands have an approximate diameter of 6 nm (Klockow et al., 2002), the idea has been raised that ARC5 might represent the observed 5 nm filaments of the outer PD ring; however, the major component of the outer PD ring is thought to be 56 kDa, and at 87 kDa ARC5 is larger than expected (Gao et al., 2003).
Dynamins are mechanochemical proteins with a range of roles including membrane pinching events in eukaryotes (Praefcke and McMahon, 2004). ARC5 attaches to the outer membrane of the chloroplasts and can be faintly detected in unconstricted chloroplasts, and clearly forms a speckled ring-like structure in constricted chloroplasts (Gao et al., 2003). The homologue of ARC5 in C. merolae, CmDnm2, also localizes to a ring-like structure at the chloroplast division site; however, during early division stages, CmDnm2 locates to cytosolic patches and is recruited to the cytosolic side of the division site only after outer PD ring formation (Miyagishima et al., 2003).
The localization pattern of ARC5 is analogous to that of mitochondrial dynamin-like division proteins, such as ADL2b, CmDnm1 and Dnm1p (Bleazard et al., 1999; Arimura and Tsutsumi, 2002; Nishida et al., 2003) and, although phylogenetic analysis shows that the dynamins recruited for chloroplast and mitochondria division are distinct, it is reasonable that ARC5 may play a role in generating mechanical force to pinch off the outer chloroplast membrane at late stages of the division process. The requirement for this function may have arisen when the cell wall, which plays a role in bacteria in septum formation, was lost. Analysis of chloroplast division in glaucophyte algae, which retained a peptidoglycan wall between the membranes of their primitive chloroplast, may lend support to this hypothesis (Keeling, 2004).
A second dynamin-like protein has been discovered that is imported into chloroplasts, although it may not be directly involved in the division machinery. Fzo is a dynamin-related membrane-remodelling protein that mediates fusion between mitochondrial outer membranes in animals and fungi (reviewed in Mozdy and Shaw, 2003). Arabidopsis harbours one homologue of Fzo, Fzo-like (FZL), that was unexpectedly found to localize exclusively to chloroplasts (Gao et al., 2006). Like Fzo, FZL is a transmembrane protein and has a conserved GTPase domain. Insertional mutants in fzl show abnormalities in both chloroplast and thylakoid morphology. FZL–GFP (green fluorescent protein) is associated with both the chloroplast inner membrane and the thylakoid membranes. This distinct localization pattern and/or predicted GTPase activity is important for the function of FZL since mutation of a conserved amino acid in the predicted GTPase domain (L362M) results in loss of localization, and FZL(L362M) is unable to complement an fzl knockout line. The primary function of FZL is predicted to be in thylakoid organization and, since overexpression of FZL does not affect the chloroplast division process, the heterogeneous chloroplast size and shape observed when FLZ levels are depleted may arise from a change in membrane morphology or dynamics (Gao et al., 2006).
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THE REGULATION OF PLASTID DIVISION |
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The observation that plants with severe plastid division defects can appear macroscopically normal illustrates that plastid division can be uncoupled from the cell cycle. However, the strict maintenance of plastid populations in dividing plant cells and the regulation of plastid number in different cell types is indicative of cellular regulation of plastid division.
Distinct levels of regulation can be deduced from several studies: first, chloroplast division can respond to a cellular parameter, such as cell size, since, when Arabidopsis plants are grown in high light, the palisade cells elongate and chloroplasts multiply to the extent of occupying the new space available (Pyke, 1999). Also, Hashimoto and Possigham (1989) demonstrated that the progression from dumb-bell formation to completion of plastid division is greatly extended in the dark relative to the progression of plastid division in the light. The first molecular evidence for regulation of chloroplast division came from the study of unicellular algae. The synchronization of C. merolae cell division and plastid division has revealed that the two cycles are tightly coupled (Suzuki et al., 1994) and that levels of CmFtsZ1 protein are drastically increased during cell division (Takahara et al., 2000). Similarly, using synchronized Chlamydomonas cell cultures, the transcript levels of the FtsZ1, FtsZ2 and Min chloroplast division homologues are shown to increase significantly during cell division, with levels falling as division reaches completion (S. Adams and S. G. Møller, unpubl. res.). It is likely that plastid division also keeps pace with cell division in higher plants: FtsZ has been demonstrated to show a degree of upregulation when synchronized tobacco BY-2 cell suspension cultures undergo mitotic phase (El-Shami et al., 2002), FtsZ is induced in developing lateral roots (Himanen et al., 2004) and the levels of FtsZ increase when dark-grown cotyledons of cucumber are exposed to light or cytokinin (Ullanat and Jayabaskaran, 2002).
The first molecular component linking the cell and plastid division cycles is AtCDT1, a cyclin-dependent kinase that forms part of the pre-replication complex (Raynaud et al., 2005). AtCDT1 is targeted to both plastids and the nucleus, and downregulation of AtCDT1 increases endoreduplication in rosette leaves and severe developmental defects. This is coupled with a severe reduction in chloroplast number and, interestingly, AtCDT1 interacts with the plastid division component ARC6 (Raynaud et al., 2005). However, the role of AtCDT1 in the control or regulation of plastid division remains unclear. Continued analysis of AtCDT1 will provide valuable insight into the coordination of chloroplast division and whole plant development.
Studies of leaf mesophyll cells in several plant species have shown that a mutually compensating mechanism between chloroplast number and chloroplast size exists, resulting in a consistent relationship between chloroplast compartment size and the size of a cell. This has been demonstrated in comparisons between different species (Pyke, 1999) and also remains true when chloroplast division is severely inhibited (Pyke and Leech, 1992) or when cell size is greatly increased (Jasinski et al., 2003). For example, overexpression of NtKIS2, a cyclin-dependent kinase inhibitor which acts primarily at the G1 phase of the cell cycle to inhibit cell division, results in greatly enlarged cells but the number of chloroplasts is still tightly correlated with mesophyll cell area, resulting in cells with higher numbers of chloroplasts (Jasinski et al., 2003). One documented exception to this rule is the high pigment-1 (hp-1) mutant in tomato where in fully expanded leaves there is increased chloroplast density and increased chloroplast size (Cookson et al., 2003). The HP-1 gene has been identified as the UV-damaged DNA-binding protein 1 (DDB1) (Lieberman et al., 2004; Liu et al., 2004). The homologue of DDB1 in Arabidopsis (DDB1A; Schroeder et al., 2002) has been shown to interact with DET1 both biochemically and genetically. Based on studies in Arabidopsis, tomato, Drosophila and humans (Berloco et al., 2001; Martinez et al., 2001; Benvenuto et al., 2002; Schroeder et al., 2002), the DET1/DDB1 complex is proposed to play at least two roles: DET1/DDB1 may interact with chromatin via an association with the non-acetylated tail of histone H2 to regulate negatively the transcription of hundreds of genes (Schroeder et al., 2002) and also DET1/DDB1 forms a complex with COP10 and enhances the activity of ubiquitin-conjugating enzymes (Yanagawa et al., 2004). The challenge will now be to determine the downstream targets for these modes of regulation. One potential target is ARC5 (Gao et al., 2003), the cytosolic dynamin-like protein that may be regulated by the ubiquitin/26S proteasome system.
Mechnosensitive channels of small conductance-like proteins (MSLs) have been identified in the nuclear genome of Arabidopsis and provide the first evidence for control of chloroplast division at the level of the individual chloroplast (Haswell and Meyerowitz, 2006). MSL2 and MSL3 are stromal chloroplast proteins and localize to discrete foci, in close proximity to the chloroplast envelope, in an analogous manner to AtMinE1 and AtMinD1 (Maple et al., 2002; Haswell and Meyerowitz, 2006). Indeed, MSL2 and MSL3 have been found to co-localize with AtMinE1, although it is suggested that this is via an as yet unknown mechanism rather than through a direct interaction (Haswell and Meyerowitz, 2006). In E. coli mechnosensitive (MS) ion channels are opened by force and help to protect the cells against osmotic shock (Levina et al., 1999). Interestingly, in Arabidopsis double insertional mutants in MSL2 and MSL3, the chloroplasts appear large and spherical, suggesting increased internal osmotic pressure (Haswell and Meyerowitz, 2006). MSL2 and MSL3 may be required to release ions from the plastid during division as the constriction forms. msl2-1 msl3-1 double mutants also show defects in leaf morphogenesis, and it has been suggested that in the double mutants aberrant levels of metabolic intermediates either in the stroma or in the cytosol might disrupt a retrograde signalling pathway and lead to aberrant leaf development (Haswell and Meyerowitz, 2006).
CRUMPLED LEAF (CRL) is unique to plants and cyanobacteria, and it is hypothesized that CRL might also be involved in the production or export of a developmental signal (Asano et al., 2004). CRL is localized to the plastid envelope and, strikingly, the crl mutants have few but enlarged chloroplasts and display abnormalities in cell division orientation, cell differentiation and overall plant development, and thus offer a possible link between plastid division, cell division and plastid differentiation (Asano et al., 2004). It will clearly be very interesting to determine the function of this protein.
Our understanding of the regulation of plastid division is still in its infancy and, to date, most components that have been implicated in playing a role in controlling plastid division have been identified fortuitously. However, as the complexity of the chloroplast division machinery is revealed, it is clear that there may be several levels of regulation: the eukaryotic host has taken control of the chloroplast division genes for the machinery and also added new components to the system which must be coordinated. Additionally, novel approaches will be required to address more specific questions to allow an understanding of how the mechanism is regulated at the level of the individual plastid and how the division of a population of plastids within a cell is controlled. As a step towards identifying genes of potential importance to the mechanism and regulation of chloroplast division, global expression profiling has been performed on Arabidopsis plants that constitutively overexpress AtMinD1 (C. A. Aldridge and S. G. Møller, unpubl. res.). Comparison of transcripts that showed a > 3-fold change revealed that a substantial number of chloroplast genes were affected (Fig. 3); however, it was found that the transcript levels of the known chloroplast division components were not substantially affected by a > 20-fold increase in AtMinD1 levels (Fig. 3). Since slight perturbations in the levels of chloroplast division components dramatically affect the division process (Stokes et al., 2000), it is maybe surprising that overexpression of AtMinD1 does not result in a compensatory feedback mechanism. However, it is possible that the components are regulated at the protein level or that extreme overexpression of a division component is not a physiologically occurring event and so no feedback mechanisms are provoked. Interestingly, analysis of transcripts that changed > 3-fold revealed that kinases (5 and 9 % up- and downregulated, respectively) and transcription factor activity (5 and 9 % up- and downregulated, respectively) were substantially represented, and it will be interesting to investigate the possibility that the protein products of some of these genes are involved in signalling pathways specifically related to the chloroplast division process.
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3-fold in plants where plastid division has been inhibited by constitutive overexpression of AtMinD1, based on their annotations to terms used in the GO cellular component ( |
EVOLUTION OF THE PLASTID DIVISION MECHANISM |
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The degree to which plastid division resembles the process of division in prokaryotic cells was first considered in 1995 with the discovery of a homologue of ftsZ in the nuclear genome of Arabidopsis (Osteryoung and Vierling, 1995). However, the list of known plastid division components has increased dramatically during the last 10 years and, with the recent increase in functional data, the question of how conserved the division mechanism actually is can now be addressed.
Although most bacterial cell division genes have been identified from E. coli, the current understanding of evolutionary biology indicates that the endosymbiotic origin of all plastids is a cyanobacterium (reviewed in McFadden, 1999). Indeed, of the bacterial homologues involved in plastid division in higher plants, ARC6 is unique to cyanobacteria and plants (Koksharova and Wolk, 2002; Vitah et al., 2003), and the FtsZ proteins, MinE and MinD are more closely related to their cyanobacterial homologues than the corresponding proteins in E. coli (Colletti et al., 2000; Itoh et al., 2001; Stokes and Osteryoung, 2003). Consequently, to address this obvious starting point is to consider how the complement of chloroplast division proteins differs from those identified in cyanobacteria. The availability of whole bacterial genome sequences has revealed that cyanobacteria encode homologues of cell division genes originally identified in E. coli: ftsE, ftsI, ftlK, ftsQ, ftsW, ftsZ, minC, minD and minE (Doherty and Adams, 1995; Mazouni et al., 2004; Miyagishima et al., 2005). Further to this, studies in Synechocystis have confirmed a role for six further cell division genes, sulA, ftn2, ftn6, cdv1, cdv2 and cdv3 (Koksharova et al., 2002; Raynaud et al., 2004; Miyagishima et al., 2005). Five cyanobacteria cell division genes have been retained in the nuclear genome of Arabidopsis [ftsZ, minD, minE, ftn2 (ARC6) and sulA (GC1)], and all of these have been shown to be key chloroplast division components (Osteryoung et al., 1998; Colletti et al., 2000; Itho et al., 2001; Maple et al., 2004).
Many of the cell division proteins that have not been retained by the Arabidopsis chloroplast division machinery are believed to form part of the prokaryotic peptidoglycan synthesizing machinery, or to be involved in directing this machinery to the division site (ftsE, ftsI, ftlK, ftsQ and ftsW; Lutkenhaus and Addinall, 1997). Unlike bacteria, chloroplasts do not have cell walls and so the loss of these genes during chloroplast evolution may not be all that surprising. No homologues of ftn6, cdv1, cdv2 or cdv3 have been identified in Arabidopsis, but, until the functions of the encoded proteins are understood, the reasons for this will remain unclear. As discussed, the loss of MinC as part of the Min system in chloroplasts is puzzling given the conservation of the FtsZ and MinE and MinD proteins; however, further analysis of the evolution and function of ARC3 will help to clarify this requirement.
Of the components that are conserved in the plastid division mechanism, recent data have revealed that they have retained many functional characteristics of their bacterial homologues. However, although superficially these components appear very similar, exhibiting analogous localization patterns, interacting partners and biochemistry, is it possible that the mechanisms of cell and chloroplast division are fundamentally different? If the mechanism of division is universal, the assembly of the Z-rings(s) may be the first event in plastid division. Analogous to the mechanism of E. coli cell division, the Arabidopsis Min proteins clearly influence the positioning of the Z-ring in chloroplasts: however, the mode of action of AtMinE1 and AtMinD1 is still speculative and may differ greatly from the bacterial system in the light of the evolution of ARC3. Currently, clear homologues of ARC3 have only been identified in Arabidopsis and rice (Shimada et al., 2004), and, since the two families of FtsZ proteins are found in all higher plants and algae, it is possible that FtsZ1 proteins may have evolved further unique functions compared with FtsZ2. Several models have been proposed for the Z-ring to provide the contractile force in E. coli cell division (reviewed in Bramhill, 1997) but, with the evolution of ARC5 and the PD rings of the chloroplast division machinery, is it now possible that the role of AtFtsZ1-1 and AtFtsZ2-1 in plants is solely to pre-determine the site of PD and ARC5 ring placement or to provide a site of assembly for membrane synthesis components. After Z-ring formation, the PD rings assemble and then constriction is seen to commence (Miyagishima et al., 2001a). Identification of which protein component(s) provide the force for chloroplast constriction will represent a key breakthrough in our understanding of the division process. However, until the components of the PD rings are identified, it will be difficult to understand the mechanism of these rings or how each one is coordinated with both the Z-ring and ARC5.
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CONCLUSIONS AND FUTURE PERSPECTIVES |
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The discovery that the chloroplast division machinery is composed of components of both prokaryotic and eukaryotic origin alluded to the complex mechanism and evolution of the chloroplast division machinery. However, only recently have molecular and biochemical data begun to reveal the extent of functional conservation and divergence of the mechanism of chloroplast division.
Whilst the continued identification of components involved directly or indirectly with the chloroplast division process will continue to increase our understanding of the process, the current status allows many of the questions that have compelled the plastid division field to begin to be addressed constructively. The FtsZ proteins share many properties with their bacterial homologues, and analysis of the composition of the Z-ring and the role of their novel interacting partners will advance our understanding of the role of these proteins during division. It is now also possible to begin to understand how the Z-ring(s) are positioned by the modified Min system. Additionally, the identification of the protein components of the three PD rings will enable the function of these rings and how they are coordinated with the Z-ring and ARC5 ring systems to begin to be addressed. The discovery of Fzo and the MSL proteins provides the first insight into different facets of the chloroplast division process and has undoubtedly opened new avenues of research.
The availability of new experimental methods in higher plants to study plastid division in real time, or to synchronize cell division, limits the progress with which our understanding of the molecular details of division can advance. For example, mounting evidence indicates that several of the stromal plastid division components exhibit dynamic localization patterns. To understand the functional relevance of this, it will be necessary to observe the different components during the process of plastid division, and future challenges will include the development of a system in which these experiments can be performed. Additionally, as has been discussed, research into the regulation of plastid division is in its infancy. Clearly novel approaches will need to be developed to address specific questions relating to the regulation of the division process both within a single chloroplast and within the environment of the host cell. It is unclear whether Arabidopsis can be used as a model system to study the regulation of this process or whether the development of new model systems will increase the speed with which our understanding of the process can advance.
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ACKNOWLEDGEMENTS |
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Plastid division work in our laboratory is supported by The Leverhulme Trust (F/00 212/M), The Functional Genomics (FUGE) Program/The Research Council of Norway and The EMBO Young Investigator Programme to S.G.M.
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