Large-scale analysis and computer modeling reveal hidden regularities behind variability of cell division patterns in Arabidopsis thaliana embryogenesis

  1. Elise Laruelle
  2. Katia Belcram
  3. Alain Trubuil  Is a corresponding author
  4. Jean-Christophe Palauqui  Is a corresponding author
  5. Philippe Andrey  Is a corresponding author
  1. Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin, France
  2. Université Paris-Saclay, INRAE, MaIAGE, France
12 figures, 3 tables and 1 additional file

Figures

Variability within and between embryos in cell shapes and cell arrangements.

(A) The four embryo domains defined by longitudinal and radial axes at stage 16C (longitudinal view): apical/basal × outer/inner. (BC) Invariant patterns in embryos up to generation 4 (16C). (DE) …

Cell shape diversity in Arabidopsis thaliana early embryogenesis.

(A) Summary of 3D image analysis pipeline: 3D cell segmentation of confocal image stacks and cell lineage reconstruction by recursive merging of daughter cells. At 32C and 16C stages, some cells are …

Figure 3 with 4 supplements
Reconstructed division patterns and cell lineages in the four embryo domains.

(A) Classification of cell division patterns (illustration in the apical outer domain) based on mother and daughter cell shapes and on the absolute orientation of division planes within the embryo. …

Figure 3—figure supplement 1
Complete reconstructed cell lineages in the apical outer domain.

Frequencies were computed based on observed patterns and patterns reconstructed at intermediate generations when rewinding lineages back to 16C stage from observed configurations. Numbers in …

Figure 3—figure supplement 2
Complete reconstructed cell lineages in the apical inner domain.

Frequencies were computed based on observed patterns and patterns reconstructed at intermediate generations when rewinding lineages back to 16C stage from observed configurations. Numbers in …

Figure 3—figure supplement 3
Distance between cell division plane and cell center at different generations in Arabidopsis thaliana embryos.

Distance was measured in mother cells reconstructed from identified sister cells at the immediately following generation.

Figure 3—figure supplement 4
Volume-ratio of cell divisions at the G4-G5 transition in the four embryo domains (shown at G4 above the graph).

Volume-ratio of each division was computed as the ratio of cellular volumes between the smallest daughter cell and the mother cell.

Analyzing cell divisions as graph cuts on polyhedral graphs.

(A) The three main cell shapes and their corresponding polyhedral graphs shown as Schlegel diagrams. Dots in the graphs correspond to cell vertices and lines correspond to cell edges. (B) Cell …

Figure 4—source data 1

Theoretical and observed frequencies of daughter cell shapes.

https://cdn.elifesciences.org/articles/79224/elife-79224-fig4-data1-v1.txt
Figure 5 with 1 supplement
Computational strategy to analyze cell divisions: illustration with a synthetic example (symmetrical vertical division of a cuboid).

Starting from a sample division, the mother cell is reconstructed and a large number of divisions at various volume-ratios is simulated. The distance from the cell center and the surface area of the …

Figure 5—figure supplement 1
Quantifying the similarity between observed and simulated cell divisions.

The matching score is computed based on the maximum overlap between observed and daughter cells.

Figure 6 with 8 supplements
Modeling division patterns at G5 in outer cells based on geometrical features.

(A) Left: distribution plot of simulation results in a basal outer cell (N=1000). Simulated planes are positioned based on their surface area and distance to the mother cell center. The dot color …

Figure 6—figure supplement 1
Convergence of the 3D computational model of cell division: cumulative variation of division plane area as a function of Monte Carlo cycle.

Five independent runs are illustrated. The model was run on the mother cell shown Figure 6A.

Figure 6—figure supplement 2
Reproducibility of simulation results: distribution plots of two independent batches of 1000 simulation runs each.

The simulations were run in a basal outer mother cell reconstructed at G4. Each simulated division is represented as a point. The color code indicates the match score between simulated and observed …

Figure 6—figure supplement 3
Robustness of simulation results to mother cell segmentation.

A basal outer mother cell was reconstructed at G4. Simulations were run in its raw 3D binary mask (No opening) or in its mask filtered with a mathematical morphological opening with radius R=1, 2, …

Figure 6—figure supplement 4
Results of cell division simulations at the 16C-32C transition in basal outer cells: distance to cell center as a function of plane surface area.

Each plot corresponds to a mother cell at generation 4 that was reconstructed by merging two observed sister cells at generation 5. Each dot corresponds to a simulated division in the mother cell. …

Figure 6—figure supplement 5
Mother cell shapes for simulations in basal outer cells.

These shapes were used for the simulations reported in Figure 6—figure supplement 4. Cells are shown from the outside of the embryo and displayed as transparent surfaces.

Figure 6—figure supplement 6
Results of cell division simulations at the 16C-32C transition in apical external cells dividing with a cuboid to the left: distance to cell center as a function of plane surface area.

Each plot corresponds to a mother cell at generation 4 that was reconstructed by merging two observed sister cells at generation 5. Each dot corresponds to a simulated division in the mother cell. …

Figure 6—figure supplement 7
Results of cell division simulations at the 16C-32C transition in apical external cells dividing with a cuboid to the right: distance to cell center as a function of plane surface area.

Each plot corresponds to a mother cell at generation 4 that was reconstructed by merging two observed sister cells at generation 5. Each dot corresponds to a simulated division in the mother cell. …

Figure 6—figure supplement 8
Results of cell division simulations at the 16C-32C transition in apical external cells dividing transversely: distance to cell center as a function of plane surface area.

Each plot corresponds to a mother cell at generation 4 that was reconstructed by merging two observed sister cells at generation 5. Each dot corresponds to a simulated division in the mother cell. …

Figure 7 with 4 supplements
Modeling division patterns at G5 in internal cells based on geometrical features.

(A) Left: distribution plot of simulation results in a basal inner cell (N=1000). Simulated planes are positioned based on their surface area and distance to the mother cell center. The dot color …

Figure 7—figure supplement 1
Results of cell division simulations at the 16C-32C transition in basal inner cells: distance to cell center as a function of plane surface area.

Each plot corresponds to a mother cell at generation 4 that was reconstructed by merging two observed sister cells at generation 5. Each dot corresponds to a simulated division in the mother cell. …

Figure 7—figure supplement 2
Results of cell division simulations at the 16C-32C transition in apical inner cells dividing with a triangular prism to the left: distance to cell center as a function of plane surface area.

Each plot corresponds to a mother cell at generation 4 that was reconstructed by merging two observed sister cells at generation 5. Each dot corresponds to a simulated division in the mother cell. …

Figure 7—figure supplement 3
Results of cell division simulations at the 16C-32C transition in apical inner cells dividing with a triangular prism to the right: distance to cell center as a function of plane surface area.

Each plot corresponds to a mother cell at generation 4 that was reconstructed by merging two observed sister cells at generation 5. Each dot corresponds to a simulated division in the mother cell. …

Figure 7—figure supplement 4
Results of cell division simulations at the 16C-32C transition in apical inner cells dividing longitudinally and radially: distance to cell center as a function of plane surface area.

Each plot corresponds to a mother cell at generation 4 that was reconstructed by merging two observed sister cells at generation 5. Each dot corresponds to a simulated division in the mother cell. …

Asymmetries in mother cell geometry in the apical domain at stage 16C and their relations with division plane orientation.

(A) Measured lengths of outer (Left) and inner (Right) mother cells. H: length along the longitudinal direction; L and R: lengths along the left and right radial directions. (B) Radial asymmetry. …

Attractor patterns buffer variability in division plane positioning.

(A) Similar cell patterns observed at G6 in the apical outer domain that have been reached through distinct cell division paths from G4. (B) Main (Left) and rare (Right) division patterns in the …

Schematic interpretation for the origin of variability in division patterns in Arabidopsis thaliana embryo.

A deterministic selection of division plane orientation, combined with noise in the precise positioning of the division plane, can generate variable orientation patterns. (A) In rotationnally …

Appendix 1—figure 1
Polyhedral graphs (Bottom row) for the three main cell shapes (Top row) found in Arabidopsis thaliana early embryogenesis.

Note that in these representations (Schlegel diagrams), the outside counts as one face of the corresponding polyhedron.

Appendix 1—figure 2
Cell division as cuts on polyhedral graphs: illustration with the division of a cuboid.

The division on the left corresponds to the edge cut shown in the middle. Completing the two subgraphs of this cut with nodes and edges (Blue) yields the two subgraphs of the daughter cells. The …

Tables

Appendix 1—table 1
Divisions of the tetrahedral cell shape (4.6.4).
p/V-p1/32/2
N(p)43
p-shape4.6.46.9.5
q-shape6.9.56.9.5
Appendix 1—table 2
Divisions of the triangular prismatic cell shape (6.9.5).

α refers to the case where the p-subgraph is acyclic, β to the case where it is cyclic.

p/V-p1/52/43/3α3/3β
N(p)69121
p-shape4.6.46.9.58.12.66.9.5
q-shape8.12.68.12.68.12.66.9.5
Appendix 1—table 3
Divisions of the cuboidal cell shape (8.12.6).

α refers to the case where the p-subgraph is acyclic, β to the case where it is cyclic.

p/V-p1/72/63/54/4α4/4β
N(p)8121843
p-shape4.6.46.9.58.12.610.15.78.12.6
q-shape10.15.710.15.710.15.710.15.78.12.6

Additional files

Download links