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Skeletons in the closet. How do chloroplasts stay in shape?

McFadden GI - J. Cell Biol. (2000)

View Article: PubMed Central - PubMed

Affiliation: Plant Cell Biology Research Centre, School of Botany, University of Melbourne, Parkville 3010, Australia.

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FtsZ tubules, which may be higher order versions of the sheets and rings (Lu et al. 2000), bear superficial resemblance to cytosolic microtubules of eukaryotes... Tubules are not routinely visualized in bacteria (Bermudes et al. 1994), which made it difficult to assess the physiological importance of the in vitro assembled FtsZ tubules (Lu et al. 2000)... This model for chloroplast tubules bears an extraordinary resemblance to the models for in vitro polymerized bacterial FtsZ tubules (Trusca et al. 1998; Lu et al. 2000)... FtsZ tubules have an outer diameter of 23 nm, a wall thickness of 5.4 nm, and comprise a twin helix with a pitch of either 18° or 24°, depending on whether the tubes are four or five start helices (Lu et al. 2000)... At this time, eukaryotic cytosolic microtubules were only beginning to be characterized, and Hoffman 1967 and Pickett-Heaps 1968 related the chloroplast tubules to cytoplasmic microtubules, although at the same time they recognized key differences in the substructure of the two types of tubules... Kiessling et al. 2000 also observed possible plastid division rings at the constriction between two nascent daughter chloroplasts, and these could be plastid division rings or chloroplast Z rings... Interestingly, plants have multiple chloroplast FtsZ genes, so the protein may have multiple functions in chloroplasts and plastids, perhaps being responsible not only for division, but also for maintenance of plastid shape, just as tubulin has roles in mitosis and cell shape in the eukaryotic cytoplasm... Kiessling et al. 2000 propose that the plastoskeleton evolved to compensate for the loss of the peptidoglycan wall during integration of the cyanobacterial endosymbiont... This hypothesis predicts that plastids of the alga Cyanophora, which retain a peptidoglycan wall, will lack a plastoskeleton... It will also be interesting to learn whether FtsZ tubules have skeletal roles in wall-less bacteria, or even mitochondria... FtsZ was recently implicated as having a role in mitochondrial division of certain algae (Beech and Gilson 2000; Beech et al. 2000), but dynamins appear to have taken over the division function in animal and yeast mitochondria (Erickson 2000)... There is no evidence of cytoskeletal structures within mitochondria as yet, so how is their shape maintained?

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(a) Transmission electron micrograph of tubules from chloroplast of Volvox sp. showing longitudinal section through three tubules with spiral substructure. Micrograph courtesy of J. Pickett-Heaps. (b) Model for tubules redrawn from Hoffman 1967. The architecture and dimensions of the model are remarkably similar (see text) to models for in vitro polymerized tubules of bacterial FtsZ (Trusca et al. 1998; Lu et al. 2000).
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Figure 2: (a) Transmission electron micrograph of tubules from chloroplast of Volvox sp. showing longitudinal section through three tubules with spiral substructure. Micrograph courtesy of J. Pickett-Heaps. (b) Model for tubules redrawn from Hoffman 1967. The architecture and dimensions of the model are remarkably similar (see text) to models for in vitro polymerized tubules of bacterial FtsZ (Trusca et al. 1998; Lu et al. 2000).

Mentions: The cytoskeleton-like structures observed in Physcomitrella chloroplasts with FtsZ/GFP fusions (Fig. 1) correlate well with the tubules observed in other chloroplasts, which are described as forming anastomosing or reticulated networks ramifying throughout the entire chloroplast (Hoffman 1967; Pickett-Heaps 1968; Rivera and Arnott 1982; Lawrence and Possingham 1984). These tubules are relatively long (up to 2.5 μm) and often associate into orderly bundles incorporating between 2 and 30 tubules (Hoffman 1967). The different sized bundles of tubules could explain the bramble-like fluorescence images observed in Physcomitrella (Fig. 1). But it is the structure of the chloroplast tubules (Fig. 2) that provides the most compelling evidence for them being composed of FtsZ. Hoffman (1976) examined chloroplast tubules of the green alga Oedogonium and proposed a detailed model for their substructure. Hoffman's model describes a two helix, hollow tubule with an outer diameter of 25–27 nm and a wall thickness of 5.5 nm (Hoffman 1967). The two helical gyres ascend at a pitch of between 17° and 27° (Hoffman 1967). This model for chloroplast tubules bears an extraordinary resemblance to the models for in vitro polymerized bacterial FtsZ tubules (Trusca et al. 1998; Lu et al. 2000). FtsZ tubules have an outer diameter of 23 nm, a wall thickness of 5.4 nm, and comprise a twin helix with a pitch of either 18° or 24°, depending on whether the tubes are four or five start helices (Lu et al. 2000). The prominent helical element of the plastid tubules (Fig. 2) would be more closely matched by the open, two-protofilament FtsZ helix than the four-protofilament solid tube.


Skeletons in the closet. How do chloroplasts stay in shape?

McFadden GI - J. Cell Biol. (2000)

(a) Transmission electron micrograph of tubules from chloroplast of Volvox sp. showing longitudinal section through three tubules with spiral substructure. Micrograph courtesy of J. Pickett-Heaps. (b) Model for tubules redrawn from Hoffman 1967. The architecture and dimensions of the model are remarkably similar (see text) to models for in vitro polymerized tubules of bacterial FtsZ (Trusca et al. 1998; Lu et al. 2000).
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Related In: Results  -  Collection

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Figure 2: (a) Transmission electron micrograph of tubules from chloroplast of Volvox sp. showing longitudinal section through three tubules with spiral substructure. Micrograph courtesy of J. Pickett-Heaps. (b) Model for tubules redrawn from Hoffman 1967. The architecture and dimensions of the model are remarkably similar (see text) to models for in vitro polymerized tubules of bacterial FtsZ (Trusca et al. 1998; Lu et al. 2000).
Mentions: The cytoskeleton-like structures observed in Physcomitrella chloroplasts with FtsZ/GFP fusions (Fig. 1) correlate well with the tubules observed in other chloroplasts, which are described as forming anastomosing or reticulated networks ramifying throughout the entire chloroplast (Hoffman 1967; Pickett-Heaps 1968; Rivera and Arnott 1982; Lawrence and Possingham 1984). These tubules are relatively long (up to 2.5 μm) and often associate into orderly bundles incorporating between 2 and 30 tubules (Hoffman 1967). The different sized bundles of tubules could explain the bramble-like fluorescence images observed in Physcomitrella (Fig. 1). But it is the structure of the chloroplast tubules (Fig. 2) that provides the most compelling evidence for them being composed of FtsZ. Hoffman (1976) examined chloroplast tubules of the green alga Oedogonium and proposed a detailed model for their substructure. Hoffman's model describes a two helix, hollow tubule with an outer diameter of 25–27 nm and a wall thickness of 5.5 nm (Hoffman 1967). The two helical gyres ascend at a pitch of between 17° and 27° (Hoffman 1967). This model for chloroplast tubules bears an extraordinary resemblance to the models for in vitro polymerized bacterial FtsZ tubules (Trusca et al. 1998; Lu et al. 2000). FtsZ tubules have an outer diameter of 23 nm, a wall thickness of 5.4 nm, and comprise a twin helix with a pitch of either 18° or 24°, depending on whether the tubes are four or five start helices (Lu et al. 2000). The prominent helical element of the plastid tubules (Fig. 2) would be more closely matched by the open, two-protofilament FtsZ helix than the four-protofilament solid tube.

View Article: PubMed Central - PubMed

Affiliation: Plant Cell Biology Research Centre, School of Botany, University of Melbourne, Parkville 3010, Australia.

AUTOMATICALLY GENERATED EXCERPT
Please rate it.

FtsZ tubules, which may be higher order versions of the sheets and rings (Lu et al. 2000), bear superficial resemblance to cytosolic microtubules of eukaryotes... Tubules are not routinely visualized in bacteria (Bermudes et al. 1994), which made it difficult to assess the physiological importance of the in vitro assembled FtsZ tubules (Lu et al. 2000)... This model for chloroplast tubules bears an extraordinary resemblance to the models for in vitro polymerized bacterial FtsZ tubules (Trusca et al. 1998; Lu et al. 2000)... FtsZ tubules have an outer diameter of 23 nm, a wall thickness of 5.4 nm, and comprise a twin helix with a pitch of either 18° or 24°, depending on whether the tubes are four or five start helices (Lu et al. 2000)... At this time, eukaryotic cytosolic microtubules were only beginning to be characterized, and Hoffman 1967 and Pickett-Heaps 1968 related the chloroplast tubules to cytoplasmic microtubules, although at the same time they recognized key differences in the substructure of the two types of tubules... Kiessling et al. 2000 also observed possible plastid division rings at the constriction between two nascent daughter chloroplasts, and these could be plastid division rings or chloroplast Z rings... Interestingly, plants have multiple chloroplast FtsZ genes, so the protein may have multiple functions in chloroplasts and plastids, perhaps being responsible not only for division, but also for maintenance of plastid shape, just as tubulin has roles in mitosis and cell shape in the eukaryotic cytoplasm... Kiessling et al. 2000 propose that the plastoskeleton evolved to compensate for the loss of the peptidoglycan wall during integration of the cyanobacterial endosymbiont... This hypothesis predicts that plastids of the alga Cyanophora, which retain a peptidoglycan wall, will lack a plastoskeleton... It will also be interesting to learn whether FtsZ tubules have skeletal roles in wall-less bacteria, or even mitochondria... FtsZ was recently implicated as having a role in mitochondrial division of certain algae (Beech and Gilson 2000; Beech et al. 2000), but dynamins appear to have taken over the division function in animal and yeast mitochondria (Erickson 2000)... There is no evidence of cytoskeletal structures within mitochondria as yet, so how is their shape maintained?

Show MeSH
Related in: MedlinePlus