scholarly journals Deterministic Nature of Cellular Position Noise During C. elegans Embryogenesis

2018 ◽  
Author(s):  
Xiaoyu Li ◽  
Zhiguang Zhao ◽  
Weina Xu ◽  
Rong Fan ◽  
Long Xiao ◽  
...  

ABSTRACTIndividuals with identical genotypes exhibit great phenotypic variability known as biological noise, which has broad implications. While molecular-level noise has been extensively studied, in-depth analysis of cellular-level noise is challenging. Here, we present a systems-level quantitative and functional analysis of noise in cellular position during embryogenesis, an important phenotype indicating differentiation and morphogenesis. We show that cellular position noise is deterministic, stringently regulated by intrinsic and extrinsic mechanisms. The noise level is determined by cell lineage identity and is coupled to developmental properties including embryonic localization, cell contact, and left-right symmetry. Cells follow a concordant low-high-low pattern of noise dynamics, and fate specification triggers a global down-regulation of noise that provide a noise-buffering strategy. Noise is stringently regulated throughout embryogenesis, especially during cell division and cell adhesion and gap junctions function to restrict noise. Collectively, our study reveals system properties and regulatory mechanisms of cellular noise control during development.

2018 ◽  
Author(s):  
Long Chen ◽  
Vincy Wing Sze Ho ◽  
Ming-Kin Wong ◽  
Xiaotai Huang ◽  
Lu-yan Chan ◽  
...  

AbstractIntercellular signaling interaction plays a key role in breaking fate symmetry during animal development. Identification of the signaling interaction at cellular resolution is technically challenging, especially in a developing embryo. Here we develop a platform that allows automated inference and validation of signaling interaction for every cell cycle of C. elegans embryogenesis. This is achieved by generation of a systems-level cell contact map that consists of 1,114 highly confident intercellular contacts by modeling analysis and is validated through cell membrane labeling coupled with cell lineage analysis. We apply the map to identify cell pairs between which a Notch signaling interaction takes place. By generating expression patterns for two ligands and two receptors of Notch signaling pathway with cellular resolution using automated expression profiling technique, we are able to refine existing and identify novel Notch interactions during C. elegans embryogenesis. Targeted cell ablation followed by cell lineage analysis demonstrates the roles of signaling interactions over cell division in breaking fate symmetry. We finally develop a website that allows online access to the cell-cell contact map for mapping of other signaling interaction in the community. The platform can be adapted to establish cellular interaction from any other signaling pathways.


2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Jianfeng Cao ◽  
Guoye Guan ◽  
Vincy Wing Sze Ho ◽  
Ming-Kin Wong ◽  
Lu-Yan Chan ◽  
...  

AbstractThe invariant development and transparent body of the nematode Caenorhabditis elegans enables complete delineation of cell lineages throughout development. Despite extensive studies of cell division, cell migration and cell fate differentiation, cell morphology during development has not yet been systematically characterized in any metazoan, including C. elegans. This knowledge gap substantially hampers many studies in both developmental and cell biology. Here we report an automatic pipeline, CShaper, which combines automated segmentation of fluorescently labeled membranes with automated cell lineage tracing. We apply this pipeline to quantify morphological parameters of densely packed cells in 17 developing C. elegans embryos. Consequently, we generate a time-lapse 3D atlas of cell morphology for the C. elegans embryo from the 4- to 350-cell stages, including cell shape, volume, surface area, migration, nucleus position and cell-cell contact with resolved cell identities. We anticipate that CShaper and the morphological atlas will stimulate and enhance further studies in the fields of developmental biology, cell biology and biomechanics.


1999 ◽  
Vol 15 (8) ◽  
pp. 307-313 ◽  
Author(s):  
Michel Labouesse ◽  
Susan E Mango
Keyword(s):  

Development ◽  
1994 ◽  
Vol 120 (3) ◽  
pp. 505-514 ◽  
Author(s):  
I.A. Hope

Promoter trapping has identified a gene, pes-1, which is expressed during C. elegans embryogenesis. The beta-galactosidase expression pattern, directed by the pes-1/lacZ fusion through which this gene was cloned, has been determined precisely in terms of the embryonic cell lineage and has three components. One component is in a subset of cells of the AB founder cell lineage during early embryogenesis, suggesting pes-1 may be regulated both by cell autonomous determinants and by intercellular signals. Analysis of cDNA suggests pes-1 has two sites for initiation of transcription and the two transcripts would encode related but distinct proteins. The predicted PES-1 proteins have homology to the fork head family of transcription factors and therefore may have important regulatory roles in early embryogenesis.


Development ◽  
1987 ◽  
Vol 100 (1) ◽  
pp. 1-12 ◽  
Author(s):  
G.M. Technau

The mechanisms leading to the commitment of a cell to a particular fate or to restrictions in its developmental potencies represent a problem of central importance in developmental biology. Both at the genetic and at the molecular level, studies addressing this topic using the fruitfly Drosophila melanogaster have advanced substantially, whereas, at the cellular level, experimental techniques have been most successfully applied to organisms composed of relatively large and accessible cells. The combined application of the different approaches to one system should improve our understanding of the process of commitment as a whole. Recently, a method has been devised to study cell lineage in Drosophila embryos at the single cell level. This method has been used to analyse the lineages, as well as the state of commitment of single cell progenitors from various ectodermal, mesodermal and endodermal anlagen and of the pole cells. The results obtained from a clonal analysis of wild-type larval structures are discussed in this review.


Development ◽  
2001 ◽  
Vol 128 (18) ◽  
pp. 3395-3404
Author(s):  
Benno Jungblut ◽  
André Pires-daSilva ◽  
Ralf J. Sommer

The invariant cell lineage of nematodes allows the formation of organ systems, like the egg-laying system, to be studied at a single cell level. The Caenorhabditis elegans egg-laying system is made up of the vulva, the mesodermal gonad and muscles and several neurons. The gonad plays a central role in patterning the underlying ectoderm to form the vulva and guiding the migration of the sex myoblasts to their final position. In Pristionchus pacificus, the egg-laying system is homologous to C. elegans, but comparative studies revealed several differences at the cellular and molecular levels during vulval formation. For example, the mesoblast M participates in lateral inhibition, a process that influences the fate of two vulval precursor cells. Here, we describe the M lineage in Pristionchus and show that both the dorsal and ventral M sublineages are involved in lateral inhibition. Mutations in the homeotic gene Ppa-mab-5 cause severe misspecification of the M lineage, resembling more the C. elegans Twist than the mab-5 phenotype. Ectopic differentiation of P8.p in Ppa-mab-5 results from at least two separate interactions between M and P8.p. Thus, interactions among the Pristionchus egg-laying system are complex, involving multiple cells of different tissues occurring over a distance.


Development ◽  
1995 ◽  
Vol 121 (4) ◽  
pp. 1227-1236 ◽  
Author(s):  
B. Goldstein

Establishment of the gut founder cell (E) in C. elegans involves an interaction between the P2 and the EMS cell at the four cell stage. Here I show that the fate of only one daughter of EMS, the E cell, is affected by this induction. In the absence of the P2-EMS interaction, both E and its sister cell, MS, produce pharyngeal muscle cells and body wall muscle cells, much as MS normally does. By cell manipulations and inhibitor studies, I show first that EMS loses the competence to respond before it divides even once, but P2 presents an inducing signal for at least three cell cycles. Second, induction on one side of the EMS cell usually blocks the other side from responding to a second P2-derived signal. Third, microfilaments and microtubules may be required near the time of the interaction for subsequent gut differentiation. Lastly, cell manipulations in pie-1 mutant embryos, in which the P2 cell is transformed to an EMS-like fate and produces a gut cell lineage, revealed that gut fate is segregated to one of P2's daughters cell-autonomously. The results contrast with previous results from similar experiments on the response to other inductions, and suggest that this induction may generate cell diversity by a different mechanism.


Development ◽  
1994 ◽  
Vol 1994 (Supplement) ◽  
pp. 85-95
Author(s):  
Ralf J. Sommer ◽  
Lynn K. Carta ◽  
Paul W. Sternberg

The invariant development of free-living nematodes combined with the extensive knowledge of Caenorhabditis elegans developmental biology provides an experimental system for an analysis of the evolution of developmental mechanisms. We have collected a number of new nematode species from soil samples. Most are easily cultured and their development can be analyzed at the level of individual cells using techniques standard to Caenorhabditis. So far, we have focused on differences in the development of the vulva among species of the families Rhabditidae and Panagrolaimidae. Preceding vulval development, twelve Pn cells migrate into the ventral cord and divide to produce posterior daughters [Pn.p cells] whose fates vary in a position specific manner [from P1.p anterior to P12.p posterior]. In C. elegans hermaphrodites, P(3-8).p are tripotent and form an equivalence group. These cells can express either of two vulval fates (1° or 2°) in response to a signal from the anchor cell of the somatic gonad, or a non-vulval fate (3°), resulting in a 3°-3°-2°-1°-2°-3° pattern of cell fates. Evolutionary differences in vulval development include the number of cells in the vulval equivalence group, the number of 1° cells, the number of progeny generated by each vulval precursor cell, and the position of VPCs before morphogenesis. Examples of three Rhabditidae genera have a posterior vulva in the position of P9-P11 ectoblasts. In Cruznema tripartitum, P(5-7).p form the vulva as in Caenorhabditis, but they migrate posteriorly before dividing. Induction occurs after the gonad grows posteriorly to the position of P(5-7).p cells. In two other species, Mesorhabditis sp. PS 1179 and Teratorhabditis palmarum, we have found changes in induction and competence with respect to their presumably more C. elegans-like ancestor. In Mesorhabditis, P(5-7).p form the vulva after migrating to a posterior position. However, the gonad is not required to specify the pattern of cell fates 3°-2°-1°-2°-3°. Moreover, the Pn.p cells are not equivalent in their potentials to form the vulva. A regulatory constraint in this family thus forces the same set of precursors to generate the vulva, rather than more appropriately positioned Pn.p cells.


Development ◽  
1993 ◽  
Vol 118 (4) ◽  
pp. 1267-1277 ◽  
Author(s):  
B. Goldstein

The gut of C. elegans derives from all the progeny of the E blastomere, a cell of the eight cell stage. Previous work has shown that gut specification requires an induction during the four cell stage (Goldstein, B. (1992) Nature 357, 255–257). Blastomere isolation and recombination experiments were done to determine which parts of the embryo can respond to gut induction. Normally only the posterior side of the EMS blastomere contacts the inducing cell, P2. When P2 was instead placed in a random position on an isolated EMS, gut consistently differentiated from the daughter of EMS contacting P2, indicating that any side of EMS can respond to gut induction. Additionally, moving P2 around to the opposite side of EMS in an otherwise intact embryo caused EMS's two daughter cells to switch lineage timings, and gut to differentiate from the descendents of what normally would be the MS blastomere. The other cells of the four cell stage, ABa, ABp, and P2, did not form gut when placed in contact with the inducer. To determine whether any other inductions are involved in gut specification, timed blastomere isolations were done at the two and eight cell stages. In the absence of cell contact at the two cell stage, segregation of gut fate proceeded normally at both the two and four cell stages. Gut fate also segregated properly in the absence of cell contact at the eight cell stage. A model is presented for the roles of lineage-dependent mechanisms and cell interactions in establishing gut fate in the E lineage.


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