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Power law relationship between cell cycle duration and cell volume in the early embryonic development of Caenorhabditis elegans.

Arata Y, Takagi H, Sako Y, Sawa H - Front Physiol (2015)

Bottom Line: Here, we found that the relationship between cell cycle duration and cell size in Caenorhabditis elegans embryos exhibited a power law distribution.Furthermore, we found that the volume ratio between the nucleus and cell exhibited a power law relationship in the size-correlated classes.Thus, our quantitative measurements shed a light on the possibility that early embryonic C. elegans cell cycle duration is coordinated with cell size as a result of geometric constraints between intracellular structures.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Cell Fate Decision, Center for Developmental Biology, RIKEN Hyogo, Japan ; Cellular Informatics Laboratory, RIKEN Saitama, Japan.

ABSTRACT
Cell size is a critical factor for cell cycle regulation. In Xenopus embryos after midblastula transition (MBT), the cell cycle duration elongates in a power law relationship with the cell radius squared. This correlation has been explained by the model that cell surface area is a candidate to determine cell cycle duration. However, it remains unknown whether this second power law is conserved in other animal embryos. Here, we found that the relationship between cell cycle duration and cell size in Caenorhabditis elegans embryos exhibited a power law distribution. Interestingly, the powers of the time-size relationship could be grouped into at least three classes: highly size-correlated, moderately size-correlated, and potentially a size-non-correlated class according to C. elegans founder cell lineages (1.2, 0.81, and <0.39 in radius, respectively). Thus, the power law relationship is conserved in Xenopus and C. elegans, while the absolute powers in C. elegans were different from that in Xenopus. Furthermore, we found that the volume ratio between the nucleus and cell exhibited a power law relationship in the size-correlated classes. The power of the volume relationship was closest to that of the time-size relationship in the highly size-correlated class. This correlation raised the possibility that the time-size relationship, at least in the highly size-correlated class, is explained by the volume ratio of nuclear size and cell size. Thus, our quantitative measurements shed a light on the possibility that early embryonic C. elegans cell cycle duration is coordinated with cell size as a result of geometric constraints between intracellular structures.

No MeSH data available.


Related in: MedlinePlus

Relationship between cell cycle duration and cell volume. This relationship of cells in embryos is shown in a double logarithmic plot (A) and a linear plot (B). The relationship of cells in AB [green dot, (C)], MS [blue square, (D)], C [light green triangle, (E)], P [magenta triangle, (F)], E [orange x-mark, (G)], and D [gray cross, (H)] lineages are shown in the double logarithmic plot. Cell volume and cell cycle duration data were obtained from four wild-type embryos. Data in the logarithmic scale were fitted to the formula, y = a + bx, by the linear least-squares method. (G) E cells are indicated by squares, and their descendants are indicated by orange x-marks. Downward bracket indicates the daughter cells of E cells. Regression analysis of cells in E lineage was performed without the E cells. Degrees of freedom in fitting in (C–H) were 68, 19, 10, 11, 8, and 4, respectively.
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Figure 2: Relationship between cell cycle duration and cell volume. This relationship of cells in embryos is shown in a double logarithmic plot (A) and a linear plot (B). The relationship of cells in AB [green dot, (C)], MS [blue square, (D)], C [light green triangle, (E)], P [magenta triangle, (F)], E [orange x-mark, (G)], and D [gray cross, (H)] lineages are shown in the double logarithmic plot. Cell volume and cell cycle duration data were obtained from four wild-type embryos. Data in the logarithmic scale were fitted to the formula, y = a + bx, by the linear least-squares method. (G) E cells are indicated by squares, and their descendants are indicated by orange x-marks. Downward bracket indicates the daughter cells of E cells. Regression analysis of cells in E lineage was performed without the E cells. Degrees of freedom in fitting in (C–H) were 68, 19, 10, 11, 8, and 4, respectively.

Mentions: Next, we examined the T–V relationship. Cell cycle duration was defined as the time from nuclear formation in a cell to nuclear formation in one of the daughter cells, in which the nucleus was formed earlier. Cell cycle duration correlated negatively with cell volume (Figures 2A,B). When we classified the T–V relationship data by cell lineage, cell cycle duration vs. cell volume appeared linear in double logarithmic plots (Figures 2C–H), suggesting a power law relationship. We fitted three different models (Gaussian, exponential, and power law) to the plots of cell cycle duration vs. cell volume in linear scale. The χ2-value in the model fitting was smallest (except for the E lineage) when the data were fitted by the power law model (Figure S2). Therefore, we concluded that the C. elegans T–V relationship in the AB, MS, C, and P lineages follows a power law relationship.


Power law relationship between cell cycle duration and cell volume in the early embryonic development of Caenorhabditis elegans.

Arata Y, Takagi H, Sako Y, Sawa H - Front Physiol (2015)

Relationship between cell cycle duration and cell volume. This relationship of cells in embryos is shown in a double logarithmic plot (A) and a linear plot (B). The relationship of cells in AB [green dot, (C)], MS [blue square, (D)], C [light green triangle, (E)], P [magenta triangle, (F)], E [orange x-mark, (G)], and D [gray cross, (H)] lineages are shown in the double logarithmic plot. Cell volume and cell cycle duration data were obtained from four wild-type embryos. Data in the logarithmic scale were fitted to the formula, y = a + bx, by the linear least-squares method. (G) E cells are indicated by squares, and their descendants are indicated by orange x-marks. Downward bracket indicates the daughter cells of E cells. Regression analysis of cells in E lineage was performed without the E cells. Degrees of freedom in fitting in (C–H) were 68, 19, 10, 11, 8, and 4, respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4309120&req=5

Figure 2: Relationship between cell cycle duration and cell volume. This relationship of cells in embryos is shown in a double logarithmic plot (A) and a linear plot (B). The relationship of cells in AB [green dot, (C)], MS [blue square, (D)], C [light green triangle, (E)], P [magenta triangle, (F)], E [orange x-mark, (G)], and D [gray cross, (H)] lineages are shown in the double logarithmic plot. Cell volume and cell cycle duration data were obtained from four wild-type embryos. Data in the logarithmic scale were fitted to the formula, y = a + bx, by the linear least-squares method. (G) E cells are indicated by squares, and their descendants are indicated by orange x-marks. Downward bracket indicates the daughter cells of E cells. Regression analysis of cells in E lineage was performed without the E cells. Degrees of freedom in fitting in (C–H) were 68, 19, 10, 11, 8, and 4, respectively.
Mentions: Next, we examined the T–V relationship. Cell cycle duration was defined as the time from nuclear formation in a cell to nuclear formation in one of the daughter cells, in which the nucleus was formed earlier. Cell cycle duration correlated negatively with cell volume (Figures 2A,B). When we classified the T–V relationship data by cell lineage, cell cycle duration vs. cell volume appeared linear in double logarithmic plots (Figures 2C–H), suggesting a power law relationship. We fitted three different models (Gaussian, exponential, and power law) to the plots of cell cycle duration vs. cell volume in linear scale. The χ2-value in the model fitting was smallest (except for the E lineage) when the data were fitted by the power law model (Figure S2). Therefore, we concluded that the C. elegans T–V relationship in the AB, MS, C, and P lineages follows a power law relationship.

Bottom Line: Here, we found that the relationship between cell cycle duration and cell size in Caenorhabditis elegans embryos exhibited a power law distribution.Furthermore, we found that the volume ratio between the nucleus and cell exhibited a power law relationship in the size-correlated classes.Thus, our quantitative measurements shed a light on the possibility that early embryonic C. elegans cell cycle duration is coordinated with cell size as a result of geometric constraints between intracellular structures.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Cell Fate Decision, Center for Developmental Biology, RIKEN Hyogo, Japan ; Cellular Informatics Laboratory, RIKEN Saitama, Japan.

ABSTRACT
Cell size is a critical factor for cell cycle regulation. In Xenopus embryos after midblastula transition (MBT), the cell cycle duration elongates in a power law relationship with the cell radius squared. This correlation has been explained by the model that cell surface area is a candidate to determine cell cycle duration. However, it remains unknown whether this second power law is conserved in other animal embryos. Here, we found that the relationship between cell cycle duration and cell size in Caenorhabditis elegans embryos exhibited a power law distribution. Interestingly, the powers of the time-size relationship could be grouped into at least three classes: highly size-correlated, moderately size-correlated, and potentially a size-non-correlated class according to C. elegans founder cell lineages (1.2, 0.81, and <0.39 in radius, respectively). Thus, the power law relationship is conserved in Xenopus and C. elegans, while the absolute powers in C. elegans were different from that in Xenopus. Furthermore, we found that the volume ratio between the nucleus and cell exhibited a power law relationship in the size-correlated classes. The power of the volume relationship was closest to that of the time-size relationship in the highly size-correlated class. This correlation raised the possibility that the time-size relationship, at least in the highly size-correlated class, is explained by the volume ratio of nuclear size and cell size. Thus, our quantitative measurements shed a light on the possibility that early embryonic C. elegans cell cycle duration is coordinated with cell size as a result of geometric constraints between intracellular structures.

No MeSH data available.


Related in: MedlinePlus