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Asymmetric inheritance of cytoophidia in Schizosaccharomyces pombe.

Zhang J, Hulme L, Liu JL - Biol Open (2014)

Bottom Line: Our time-lapse studies suggest that cytoophidia are dynamic.Once the mother cell divides, the cytoplasmic and nuclear cytoophidia independently partition into one of the two daughter cells.Our findings on asymmetric inheritance of cytoophidia in S. pombe offer an exciting opportunity to study the inheritance of metabolic enzymes in a well-studied model system.

View Article: PubMed Central - PubMed

Affiliation: MRC Functional Genomics Unit, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK.

No MeSH data available.


Related in: MedlinePlus

S. pombe cells are morphologically asymmetric and polarized.(A–F) A group of S. pombe cells at different phases of cell cycle. The difference between the two poles can be appreciated when the cell wall (B) and the cytoplasm (C) are outlined by Calcofluor white staining. (G–L) A pair of S. pombe cells. These two cells are morphologically distinct from one another. In these panels, the cell on the left inheriting the old end (‘Smooth cell’) also inherits the C- and the N-cytoophidium, while the other cell (‘Isis Rough cell’) inherits neither cytoophidia. Scale bars: 2 µm.
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f04: S. pombe cells are morphologically asymmetric and polarized.(A–F) A group of S. pombe cells at different phases of cell cycle. The difference between the two poles can be appreciated when the cell wall (B) and the cytoplasm (C) are outlined by Calcofluor white staining. (G–L) A pair of S. pombe cells. These two cells are morphologically distinct from one another. In these panels, the cell on the left inheriting the old end (‘Smooth cell’) also inherits the C- and the N-cytoophidium, while the other cell (‘Isis Rough cell’) inherits neither cytoophidia. Scale bars: 2 µm.

Mentions: Next we analysed in the frequencies and numbers of C- and N-cytoophidia in S. pombe cells. We found that the most majority of S. pombe cells have one C-cytoophidium and one N-cytoophidium. This raises a fundamental issue: how C- and N-cytoophidia are passed into the next generation after cell division. S. pombe has been a popular system for studies of cell growth and division due to its regular shape and size. As in most systems, the central events of S. pombe cell reproduction are chromosome replication in S phase, followed by chromosome segregation and nuclear division (mitosis) and cell division (cytokinesis) in M phase. While S. cerevisiae has an extended period at the gap between M and S phases (G1), S. pombe remains in G2 phase of the cell cycle for an extended period (Hartwell et al., 1974; Mitchison, 1972; Nurse et al., 1976). In S. pombe, two daughter cells remain associated with each other physically after mitosis and cytokinesis at G1/S phases. The abscission of the paired cells occurs afterwards. We analyzed cells at G1/S phase when two daughter cells are still clearly associating with each other (after cytokinesis but before scission) and observed that the distributions of C- and N-cytoophidia in one cell differ from those in another cell. After S. pombe cells undergo cell division, we can see only one out of the two daughter cells has C-cytoophidia (Fig. 4). In 99.5% cells (n = 358), we observed that C-cytoophidia can be detected in only one of the two daughter cells or the C-cytoophidia in one daughter cell are dramatically larger than those in the other cell (supplementary material Fig. S3). Similarly, N-cytoophidia are only detectable in one of these two daughter cells. These data suggest that both C- and N-cytoophidia are differentially inherited during S. pombe cell division. Interestingly, N-cytoophidium is not always inherited by the same cell that inherits the C-cytoophidium (Fig. 3).


Asymmetric inheritance of cytoophidia in Schizosaccharomyces pombe.

Zhang J, Hulme L, Liu JL - Biol Open (2014)

S. pombe cells are morphologically asymmetric and polarized.(A–F) A group of S. pombe cells at different phases of cell cycle. The difference between the two poles can be appreciated when the cell wall (B) and the cytoplasm (C) are outlined by Calcofluor white staining. (G–L) A pair of S. pombe cells. These two cells are morphologically distinct from one another. In these panels, the cell on the left inheriting the old end (‘Smooth cell’) also inherits the C- and the N-cytoophidium, while the other cell (‘Isis Rough cell’) inherits neither cytoophidia. Scale bars: 2 µm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4232767&req=5

f04: S. pombe cells are morphologically asymmetric and polarized.(A–F) A group of S. pombe cells at different phases of cell cycle. The difference between the two poles can be appreciated when the cell wall (B) and the cytoplasm (C) are outlined by Calcofluor white staining. (G–L) A pair of S. pombe cells. These two cells are morphologically distinct from one another. In these panels, the cell on the left inheriting the old end (‘Smooth cell’) also inherits the C- and the N-cytoophidium, while the other cell (‘Isis Rough cell’) inherits neither cytoophidia. Scale bars: 2 µm.
Mentions: Next we analysed in the frequencies and numbers of C- and N-cytoophidia in S. pombe cells. We found that the most majority of S. pombe cells have one C-cytoophidium and one N-cytoophidium. This raises a fundamental issue: how C- and N-cytoophidia are passed into the next generation after cell division. S. pombe has been a popular system for studies of cell growth and division due to its regular shape and size. As in most systems, the central events of S. pombe cell reproduction are chromosome replication in S phase, followed by chromosome segregation and nuclear division (mitosis) and cell division (cytokinesis) in M phase. While S. cerevisiae has an extended period at the gap between M and S phases (G1), S. pombe remains in G2 phase of the cell cycle for an extended period (Hartwell et al., 1974; Mitchison, 1972; Nurse et al., 1976). In S. pombe, two daughter cells remain associated with each other physically after mitosis and cytokinesis at G1/S phases. The abscission of the paired cells occurs afterwards. We analyzed cells at G1/S phase when two daughter cells are still clearly associating with each other (after cytokinesis but before scission) and observed that the distributions of C- and N-cytoophidia in one cell differ from those in another cell. After S. pombe cells undergo cell division, we can see only one out of the two daughter cells has C-cytoophidia (Fig. 4). In 99.5% cells (n = 358), we observed that C-cytoophidia can be detected in only one of the two daughter cells or the C-cytoophidia in one daughter cell are dramatically larger than those in the other cell (supplementary material Fig. S3). Similarly, N-cytoophidia are only detectable in one of these two daughter cells. These data suggest that both C- and N-cytoophidia are differentially inherited during S. pombe cell division. Interestingly, N-cytoophidium is not always inherited by the same cell that inherits the C-cytoophidium (Fig. 3).

Bottom Line: Our time-lapse studies suggest that cytoophidia are dynamic.Once the mother cell divides, the cytoplasmic and nuclear cytoophidia independently partition into one of the two daughter cells.Our findings on asymmetric inheritance of cytoophidia in S. pombe offer an exciting opportunity to study the inheritance of metabolic enzymes in a well-studied model system.

View Article: PubMed Central - PubMed

Affiliation: MRC Functional Genomics Unit, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK.

No MeSH data available.


Related in: MedlinePlus