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: oster_k@med.unr.edu
†School of Biological Sciences, Royal Holloway, University of London,
Egham, Surrey TW20 0EX, UK; e-mail: k.pyke@rhbnc.ac.uk
Current Opinion in Plant Biology1998, 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 relation-ship with plastids originally derived by endosymbiosis from a single free-living photosynthetic prokaryote [1]. The maintenance of plastid populations in plant cells undergo-ing division, as well as the developmentally regulated establishment of large plastid populations in some cell types, requires that plastids replicate. A sizable body of lit-erature 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 mor-phological structures are present are short-lived and not readily apparent in all dividing chloroplasts. A key morpho-logical 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 struc-ture, 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 estab-lished. In this article we will consider the recent advances in understanding the molecular machinery that accomplish-es plastid division, which have come about largely through the application of Arabidopsismolecular 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 charac-terization of the Arabidopsis arcmutants (accumulation and replication of chloroplasts), which exhibit altered chloro-plast 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 2-3 greatly enlarged chloroplasts per cell. The arc6 phenotype results primarily from interference with pro-plastid division in the shoot and root meristems [6]. Plastid segregation into new cells still occurs, however, as evi-denced by the lack of aplastidic cells in most tissues, possibly resulting from physical breakage of the proplas-tids during cytokinesis. Thylakoid ultrastructure and plastid function are unaffected in arc6 [5], and develop-mentally 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 pro-plastid 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 arcmutants has been instrumental in establishing the strict cellular control that exists over total chloroplast compartment vol-ume, because changes in chloroplast number in the mutants are always compensated for by an inversely relat-ed change in chloroplast size [2•].
A prokaryotic cell division gene discovered
in plants
A significant breakthrough in understanding the mecha-nistic basis for plastid division was the discovery of a nuclear gene from Arabidopsisencoding a homologue of a bacterial cell division protein called FtsZ, an essential component of the prokaryotic cell division machinery [10]. The ArabidopsisFtsZ 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. AtFtsZ1-1was shown to be
Plastid division: evidence for a prokaryotically derived
mechanism
targeted to the chloroplast, strongly implicating the pro-tein in chloroplast division and inspiring the hypothesis that the plastid division machinery in plants has its evolu-tionary 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 cytoskele-tal protein found both in archaebacteria and eubacteria [13–15]. It was first identified in a genetic screen for tem-perature-sensitive mutants of E. colithat 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-sensi-tive) [16]. Although numerous ftsgenes have been isolated from bacteria, to date only FtsZhas been extensively char-acterized with regard to its role in cell division [17,18,19•,20•]. Immunogold labeling [21] and immunoflu-orescence 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 struc-ture 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 prop-erties became evident from experiments demonstrating that purified FtsZ undergoes GTP-dependent assembly into polymers that resemble tubulin protofilaments assem-bled 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 evolu-tionary 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 meso-phyll 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 FtsZgenes are essential for chloro-plast 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 FtsZgenes fall into two distinct families, des-ignated FtsZ1and FtsZ2, encoding proteins that differ both in their overall amino acid sequence similarities and in their apparent subcellular localizations [11••]. FtsZ1 pro-teins contain amino-terminal extensions with features common to chloroplast transit peptides, and at least one member of this family, AtFtsZ1-1, can be post-translation-ally imported into isolated chloroplasts where the transit peptide is processed [10]. FtsZ2 proteins, which include PpFtsZfrom Physcomitrellaand a second nuclear-encoded FtsZ protein from Arabidopsis, called AtFtsZ2-1, lack obvi-ous 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 AtFtsZ2-1is also essential for chloroplast and proplas-tid division in Arabidopsis [11••]. These findings revealed that at least two functionally distinct, and probably differ-entially localized, FtsZ gene products mediate plastid division in higher plants [11••]. The role of FtsZs in plas-tid division may be more complex, however, as Arabidopsis contains at least one other FtsZ2family member [11••].
Second, it is apparent that in Arabidopsis the same FtsZ genes function in the division of both undifferentiated pro-plastids and differentiated chloroplasts. As the number of plastids and the relative cell volume occupied by them dif-fers 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. ARC6also functions in the division both of proplastids and of chloroplasts [5,6], but does not cosegregate with either AtFtsZgene, 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 estab-lished 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 eukaryot-ic 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 plas-tid 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 bacteri-al 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 for-mation is under control of the minB locus, which comprises three genes: minC, minDand minE[34]. Mutant strains lacking MinC and MinD are characterized by the formation of ‘minicells’, tiny, nonviable cells lacking chro-mosomes. 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 divi-sion site, resulting in septation near the cell pole rather than at midcell. This phenotype indicates that the previ-ous 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
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 sug-gest 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, unpub-lished data). The protein encoded by the Arabidopsisgene includes an amino-terminal extension with characteristics suggesting a chloroplast targeting function. Although these Mingenes must still be tested for roles in plastid division, their existence provides evidence that the mechanism con-trolling 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 struc-ture 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 pro-tein 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 mole-cule proposed to play an important role, however, is the recently identified ZipA [38••]. ZipA (Z-interacting pro-tein 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 bidi-rectionally from a single nucleation point on the cytoplasmic membrane [39]. Whether ZipA or some other factor is involved in the nucleation event is unknown.
post-translational modification could provide a lipid-solu-ble membrane anchor allowing plant FtsZ proteins to reversibly associate with the envelope membranes. Post-translational 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 ftsgenes whose functions are less well under-stood 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, howev-er, 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 enve-lope surfaces, consistent with the involvement of two plastid dividing rings and two FtsZ genes in plastid divi-sion. Perhaps the requirement for cell wall ingrowth in bacteria has been supplanted by the evolution of an exter-nal plastid dividing ring composed of FtsZ in plants.
At present, we can only speculate on other types of mole-cules that might play a part in the constriction and separation phases of plastid division, but one strong con-tender is ARC5 [3,9]. Chloroplasts in arc5mutants 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 con-striction. Because the formation of a long, narrow isthmus is sometimes observed late in plastid division, it is conceiv-able 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 foun-dation 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 pro-duce 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
1. Gray MW: The endosymbiont hypothesis revisited. Int Rev Cytol
1992, 141:233-357.
2. Pyke KA: The genetic control of plastid division in higher plants.
• Am J Bot 1997, 84:1017-1027.
A general overview of the understanding of chloroplast division derived main-ly from microscopical and developmental studies over the past 40 years and
a description of the characterisation of arcmutants.
3. Robertson EJ, Rutherford SM, Leech RM: Characterisation of
chloroplast division using the Arabidopsis mutant arc5.Plant Physiol 1996, 112:149-159.
4. Kuroiwa T, Kuroiwa H, Sakai A, Takahashi H, Toda K, Itoh R: The
•• division apparatus of plastids and mitochondria. Int Rev Cytol
1988, 181:1-41.
An up to date and indispensable review and analysis of evidence pertaining to the structure and function of the plastid dividing rings in both lower and higher plants.
5. Pyke KA, Rutherford SM, Robertson EJ, Leech RM: arc6, a fertile
Arabidopsis mutant with only 2 mesophyll cell chloroplasts.Plant Physiol1994, 106:1169-1177.
6. Robertson EJ, Pyke KA, Leech RM: arc6, an extreme chloroplast
division mutant of Arabidopsisalso alters proplastid proliferation and morphology in shoot and root apices.J Cell Sci1995,
108:2937-2944.
7. Pyke KA, Page AM: Plastid ontogeny during petal development in
• Arabidopsis.Plant Physiol1998, 116:797-803.
This paper shows that chloroplasts in petals of arc6 differentiate into
leu-coplasts in a normal manner despite the dramatically increased size of the plastids in the mutant. In wild-type, the chloroplasts in the rapidly expanding cells of the petal stalk all appear to initiate divisions as shown by virtually all chloroplasts having central constrictions.
8. Pyke KA, Leech, RM: Nuclear mutations radically alter chloroplast
division and expansion in Arabidopsis thaliana.Plant Physiol
1992, 99:1005-1008.
9. Pyke KA, Leech, RM: A genetic analysis of chloroplast division in
Arabidopsis thaliana.Plant Physiol1994, 104:201-207.
10. Osteryoung KW, Vierling E: Conserved cell and organelle division.
Nature1995, 376:473-474.
11. Osteryoung KW, Stokes KD, Rutherford SM, Percival AL , Lee WY:
•• Chloroplast division in higher plants requires members of two functionally divergent FtsZ gene families. Plant Cell1998, in press. A key paper, not only because it confirmed that the chloroplast-targeted FtsZ described in [10] was essential for division of higher plant chloroplasts, but also because it demonstrated that a second FtsZ gene product, probably localized in the cytosol, was also essential. The data revealed that important differences exist between bacteria and chloroplasts with regard to the dis-position of the division apparatus.
12. Strepp R, Scholz S, Kruse S, Speth V, Reski R: Plant nuclear gene
•• knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin.Proc Natl Acad Sci USA 1998, 95:4368-4373.
this case in the moss Physcomitrella patens. Its greater contribution,
how-ever, was the use of homologous recombination as a means of testing FtsZ
function. Efficient generation of targeted nuclear gene deletions in plants has been a kind of ‘holy grail’ among plant biologists. The ability to achieve this in the moss holds promise for analyzing the functions of many other plant genes, including additional plastid division genes.
13. Baumann P, Jackson SP: An archaebacterial homolog of the
essential eubacterial cell division protein FtsZ. Proc Natl Acad Sci
USA 1996, 93:6726-6730.
14. Margolin W, Wang R, Kumar M: Isolation of an ftsZhomolog from
the archaebacterium Halobium salinarium: implications for the evolution of FtsZ and tubulin. J Bacteriol1996, 178:1320-1327.
15. Wang, W, Lutkenhaus, J: FtsZ ring: the eubacterial division
apparatus conserved in archaebacteria. Mol Microbiol 1996,
21:313-319.
16. Lutkenhaus, JF, Wolf-Watz H, Donachie WD: Organization of genes in
the ftsA-envAregion of the Escherichia coligenetic map and identification of a new ftslocus (ftsZ).J Bacteriol1980, 142:615-620.
17. Erickson HP: FtsZ, a tubulin homologue in prokaryote cell division.
Trends Cell Biol1997, 7:362-367.
18. Rothfield LI, Justice SS:Bacterial cell division: the cycle of the ring.
Cell1997, 88:581-584.
19. Lutkenhaus J, Addinall SG: Bacterial cell division and the Z ring.
• Annu Rev Biochem 1997, 66:93-116.
An interesting aspect of this review is its discussion of FtsZ function in dif-ferent groups of bacteria and the implications for mechanistic differences in the septation process. These comparisons are relevant to comparisons between bacterial cell and plant plastid division.
20. Bramhill D: Bacterial cell division.Annu Rev Cell Dev Biol,1997,
• 13:395-424.
A helpful review because it succinctly summarizes the available information on all the bacterial cell division genes identified to date.
21. Bi E, Lutkenhaus J: FtsZ ring structure associated with division in
Escherichia coli.Nature1991, 354:161-164.
22. Ma X, Ehrhardt DW, Margolin W: Co-localization of cell division
proteins FtsZ and FtsA to cytoskeletal structures in living
Escherichia coli.Proc Natl Acad Sci USA1996, 93:12998-13003.
23. Bramhill D, Thompson CM: GTP-dependent polymerization of
Escherichia coli FtsZ protein to form tubules. Proc Natl Acad Sci
USA 1994, 91:5813-5817.
24. Erickson HP, Taylor DW, Taylor KA, Bramhill D:Bacterial cell division
protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers.Proc Natl Acad Sci USA
1996, 93:519-523.
25. Mukherjee A, Lutkenhaus J: Guanine nucleotide-dependent
assembly of FtsZ into filaments.J Bacteriol 1994, 176:2754-2758.
26. de Pereda JM, Leynadier D, JA, Chacon P, Andreu JM: Tubulin
secondary structure analysis, limited proteolysis sites and homology to ftsZ.Biochemistry1996, 35:14203-14215.
27 Lutkenhaus J: Escherichia colicell division.Curr Opin Genet Devel
1993, 3:783-788.
28. Lutkenhaus J: FtsZ ring in bacterial cytokinesis. Mol Microbiol
1993, 9:403-409.
29. Lowe J, Amos LA: Crystal structure of the bacterial cell-division
•• protein FtsZ.Nature 1998, 391:203-206.
This paper and [30••], published back-to-back, confirmed the structural
sim-ilarity between FtsZ and tubulin.
30. Nogales E, Wolf SG, Downing KH: Structure of the abtubulin
•• dimer by electron crystallography. Nature1998, 391:199-203.
This paper and [29••], published back-to-back, confirmed the structural
sim-ilarity between FtsZ ans tubulin.
31. Loffelhardt W, Bohnert HJ: Structure and function of the cyanelle
genome. Int Rev Cytol 1994, 151:29-65.
32. Whatley JM: The endosymbiotic origin of chloroplasts.Int Rev
Cytol 1994, 144:259-299.
33. Pyke KA: Plastid division and development.Plant Cell1999, in
•• press.
This article discusses the role of plastid division in cell development and con-siders broadly the possible molecular bases for division and its control. In addition, attention is given to cellular factors that might control the popula-tion size of chloroplasts within a leaf cell, both in initiapopula-tion of divisions and in a stop control to prevent over-dividing.
34. de Boer P, Crossley RE, Rothfield LI: A division inhibitor and a
topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell
1989, 56:641-649.
35. Bi E, Lutkenhaus J: Cell division inhibitors SulA and MinCD prevent
formation of the FtsZ ring.J Bacteriol1993, 175:1118-1125.
36. Raskin DM, de Boer PA: The MinE ring: an FtsZ-independent cell
structure required for selection of the correct division site in E.
coli.Cell1997, 91:685-694.
37. Wakasugi T, Nagai T, Kapoor M, Sugita M, Ito M, Ito S, Tsudzuki J,
•• Nakashima K, Tsudzuki T, Suzuki Y et al.: Complete nucleotide
sequence of the chloroplast genome from the green alga
Chlorella vulgaris: the existence of genes possibly involved in chloroplast division.Proc Natl Acad Sci USA1997, 94:5967-5972.
Sequencing of the Chlorellachloroplast genome revealed a minDand minE
gene next to each other, similar to their arrangement in the minlocus in E.
coli. These genes are missing from higher plant chloroplast genomes, but a
minDhomologue has been identified in the Arabidopsisnuclear genome (KA
Pyke and KW Osteryoung, unpublished data). The presence of these genes in plants suggests they may have a function in plastid division analogous to their function in bacterial cell division.
38. Hale CA, de Boer PA: Direct binding of FtsZ to ZipA, an essential
•• component of the septal ring structure that mediates cell division in E. coli.Cell1997, 88:175-185.
An important paper because it described a new bacterial cell division pro-tein not previously identified from genetic studies that could be important in initiating FtsZ ring assembly. A ZipA-like molecule may well be a component of the plastid division apparatus in plants.
39. Addinall SG, Lutkenhaus J: FtsZ-spirals and -arcs determine the
shape of the invaginating septa in some mutants of Escherichia coli.Mol Microbiol1996, 22:231-237.
40. Caron JM: Post-translational modification of tubulin by
palmitoylation: I. In vivo and cell-free studies.Mol Biol Cell1997,
8:621-636.
41. Ozols J, Caron JM: Post-translational modification of tubulin by
palmitoylation: II. Identification of sites of palmitoylation.Mol Biol
