Volume segregation programming in a nematode's early embryogenesis

Guan, Guoye; Wong, Ming-Kin; Zhao, Zhongying; Tang, Lei-Han; Tang, Chao

doi:10.1103/physreve.104.054409

Cited by 8 publications

(15 citation statements)

References 37 publications

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“…The discrepancy may be related to the definition of symmetry (see Discussion). A recent study that performed quantitative analysis of cell volume showed that divisions of EMS and Ca were symmetric (Guan et al, 2021), which is consistent with our results. Altogether, our results showed agreement with the previous study in 93% (25/27) of divisions.…”

Section: Reproduction and Extension Of A Previous Studysupporting

confidence: 93%

Systematic analysis of cell morphodynamics in C. elegans early embryogenesis

2023

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The invariant cell lineage of Caenorhabditis elegans allows unambiguous assignment of the identity for each cell, which offers a unique opportunity to study developmental dynamics such as the timing of cell division, dynamics of gene expression, and cell fate decisions at single-cell resolution. However, little is known about cell morphodynamics, including the extent to which they are variable between individuals, mainly due to the lack of sufficient amount and quality of quantified data. In this study, we systematically quantified the cell morphodynamics in 52 C. elegans embryos from the two-cell stage to mid-gastrulation at the high spatiotemporal resolution, 0.5 μm thickness of optical sections, and 30-second intervals of recordings. Our data allowed systematic analyses of the morphological features. We analyzed sphericity dynamics and found a significant increase at the end of metaphase in every cell, indicating the universality of the mitotic cell rounding. Concomitant with the rounding, the volume also increased in most but not all cells, suggesting less universality of the mitotic swelling. Combining all features showed that cell morphodynamics was unique for each cell type. The cells before the onset of gastrulation could be distinguished from all the other cell types. Quantification of reproducibility in cell-cell contact revealed that variability in division timings and cell arrangements produced variability in contacts between the embryos. However, the area of such contacts occupied less than 5% of the total area, suggesting the high reproducibility of spatial occupancies and adjacency relationships of the cells. By comparing the morphodynamics of identical cells between the embryos, we observed diversity in the variability between cells and found it was determined by multiple factors, including cell lineage, cell generation, and cell-cell contact. We compared the variabilities of cell morphodynamics and cell-cell contacts with those in ascidian Phallusia mammillata embryos. The variabilities were larger in C. elegans, despite smaller differences in embryo size and number of cells at each developmental stage.

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Section: Reproduction and Extension Of A Previous Studysupporting

confidence: 93%

Systematic analysis of cell morphodynamics in C. elegans early embryogenesis

2023

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“…For instance, in modeling cell positioning, physical simulations show why the timing and orientation of cell division and cell–cell adhesion are programmed as they are in vivo [57] , [90] , [195] , [196] . In mechanical terms, this programming ensures the precise and robust realization of the developmental path of embryonic morphology [19] , [20] , [75] , [89] , [91] , [92] , [93] , [94] , [95] , [197] , [209] , [212] . Physical modeling also provides answers to the perennial question of why and how the C. elegans developmental procedure is so reproducible.…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, the severely deformed cell shape that comprises filopodia and lamellipodia structures can mediate the movement of cells, such as ABpl during the left–right asymmetric chiral morphogenesis from the 7- to 8-cell stages [75] , [76] , [87] , [88] . Second, cell volume, which is determined by the symmetric or asymmetric division of a mother cell, influences the nucleus-to-cytoplasm ratio and the molecular contents allocated to the daughter cell, which regulates this cell’s fate, cycle length and the robustness of its arrangement [89] , [90] , [91] , [92] . Third, cell–cell contact serves as a physical basis for signal transduction between specific cell pairs that regulates the signal-receiving cell’s orientation during division (e.g., Wnt signaling from C to ABar at the 8-cell stage) and fate specification (e.g., Notch signaling from MS to ABalp and ABara instead of to ABala and ABarp at the 12-cell stage) [22] , [23] , [24] , [93] .…”

Section: Cellular-resolution Studies Of Embryogenesismentioning

confidence: 99%

“…Overall, these above-described theoretical explorations have delineated crucial aspects of the diverse and precise control of cell polarization in C. elegans . These programs give rise to the stereotypical development of C. elegans embryos and are vital for optimal cell proliferation, morphogenesis, and differentiation [92] , [160] , [191] . Other experimental observations, such as that the LGL-1 is localized in the posterior of C. elegans , can be included to form a complete interaction network for future studies [191] .…”

Section: Physical Modelsmentioning

confidence: 99%

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Delineating the mechanisms and design principles of Caenorhabditis elegans embryogenesis using in toto high-resolution imaging data and computational modeling

Guan

Zhao²,

Tang³

2022

Computational and Structural Biotechnology Journal

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“…J. , 2023]? About the downstream, as the cell size asymmetry is accurately programmed with a limited tolerance for successful embryogenesis and is critical for cell cycle length asymmetry as well as consequential cell arrangement progression [Jankele et al, eLife , 2021; Guan et al, Phys. Rev.…”

Section: Introductionmentioning

confidence: 99%

Quantitative cell morphology inC. elegansembryos reveals regulations of cell volume asymmetry

Guan,

Li,

et al. 2023

Preprint

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The dynamics of cellular morphology throughout development are crucial for morphogenesis and organogenesis, yet their systematic characterization remains a significant challenge. By integrating both nuclear position and advanced cell membrane labeling, we develop a novel method that enables the segmentation of surfaces for over 95% of cells produced duringCaenorhabditis elegansembryogenesis. With this method, we segment eight wild-type and four perturbed embryos. The output, including cell identity, shape, volume, surface and contact area, can be visualized using our custom software. We demonstrate that signaling interactions, such as Notch and Wnt, regulate not only the asymmetry of cell fate but also the asymmetry of cell volume in conjunction with mechanical compression. Furthermore, we find that the asymmetries of fate and volume are generally interconnected.ONE SENTENCE SUMMARYSystematic quantification of cell morphology with resolved cell lineage and cell fate in developingC. elegansembryo uncovers multimodal regulations of cell size.Potential Cover/Featured Image: Smiling “ghost” face ofC. elegansembryo.Center: shown are skins (colored in red, dorsal view with anterior to the bottom) of a 400-celledC. elegansembryo. Cells not covered by the skins are colored in gray, green, blue, and transparent yellow, respectively. Internal and external circles: confocal fluorescence images (GFP for cell nucleus and mCherry for cell membrane) and reconstructed cell morphologies of theC. elegansembryo from the 2- to 550-cell stages respectively, connected with images of aC. elegansadult expressing the same markers.

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Volume segregation programming in a nematode's early embryogenesis

Cited by 8 publications

References 37 publications

Systematic analysis of cell morphodynamics in C. elegans early embryogenesis

Systematic analysis of cell morphodynamics in C. elegans early embryogenesis

Delineating the mechanisms and design principles of Caenorhabditis elegans embryogenesis using in toto high-resolution imaging data and computational modeling

Quantitative cell morphology inC. elegansembryos reveals regulations of cell volume asymmetry

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