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Physical determinants of asymmetric cell divisions in the early development of Caenorhabditis elegans.

ABSTRACT: Asymmetric cell divisions are of fundamental importance for the development of multicellular organisms, e.g. for the generation of founder cells. Prime examples are asymmetric cell divisions in germline precursors during the early embryogenesis of the transparent roundworm Caenorhabditis elegans, one of the major developmental model organisms. However, due to a lack of quantitative data it has remained unclear how frequent unequal daughter cell sizes emerge in the worm's early embryogenesis, and whether these originate from sterical or biochemical cues. Using quantitative light-sheet microscopy, we have found that about 40% of all cell divisions in C. elegans until gastrulation generate daughter cells with significantly different volumes. Removing the embryo's rigid eggshell revealed asymmetric divisions in somatic cells to be primarily induced by steric effects. Division asymmetries in the germline remained unaltered and were correctly reproduced by a model based on a cell-size independent, eccentric displacement of the metaphase plate. Our data suggest that asymmetric cell divisions, imposed by physical determinants, are essential for establishing important cell-cell interactions that eventually fuel a successful embryogenesis.

SUBMITTER: Fickentscher R

PROVIDER: S-EPMC5571195 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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Physical determinants of asymmetric cell divisions in the early development of Caenorhabditis elegans.

Fickentscher Rolf R Weiss Matthias M

Scientific reports 20170824 1

Asymmetric cell divisions are of fundamental importance for the development of multicellular organisms, e.g. for the generation of founder cells. Prime examples are asymmetric cell divisions in germline precursors during the early embryogenesis of the transparent roundworm Caenorhabditis elegans, one of the major developmental model organisms. However, due to a lack of quantitative data it has remained unclear how frequent unequal daughter cell sizes emerge in the worm's early embryogenesis, and ...[more]

PMID: 28839200

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Project description:BackgroundGene duplicates often exhibit asymmetric rates of molecular evolution in their early evolutionary existence. This asymmetry in rates is thought to signify the maintenance of the ancestral function by one copy and the removal of functional constraint on the other copy, enabling it to embark on a novel evolutionary trajectory. Here I focused on a large population of evolutionarily young gene duplicates (KS ? 0.14) in the Caenorhabditis elegans genome in order to conduct the first combined analysis of four predictors (evolutionary age, chromosomal location, structural resemblance between duplicates, and duplication span) which may be implicated in the asymmetric sequence divergence of paralogs at the nucleotide and amino acid level. In addition, I investigate if either paralog is equally likely to embark on a trajectory of accelerated sequence evolution or whether the derived paralog is more likely to exhibit faster sequence evolution.ResultsThree predictors (evolutionary age of duplicates, chromosomal location and duplication span) serve as major determinants of sequence asymmetry between C. elegans paralogs. Paralogs diverge asymmetrically in sequence with increasing evolutionary age, the relocation of one copy to a different chromosome and attenuated duplication spans that likely fail to capture the entire ancestral repertoire of coding sequence and regulatory elements. Furthermore, for paralogs residing on the same chromosome, opposite transcriptional orientation and increased genomic distance do not increase sequence asymmetry between paralogs. For a subset of duplicate pairs wherein the ancestral versus derived paralog could be distinguished, the derived paralogs are more likely to evolve at accelerated rates.ConclusionsThis genome-wide study of evolutionarily young duplicates stemming primarily from DNA-mediated small-scale duplication events demonstrates that genomic relocation to a new chromosome has important consequences for asymmetric divergence of paralogs, akin to paralogs arising from RNA-mediated duplication events. Additionally, the duplication span is negatively correlated with sequence rate asymmetry among paralogs, suggesting that attenuated duplication spans stemming from incomplete duplication of the ORF and/or ancestral regulatory elements further accelerate sequence divergence between paralogs. Cumulatively, derived copies exhibit accelerated rates of sequence evolution suggesting that they are primed for a divergent evolutionary trajectory by changes in structure and genomic context at inception.

Dataset Information

Physical determinants of asymmetric cell divisions in the early development of Caenorhabditis elegans.

Publications

Physical determinants of asymmetric cell divisions in the early development of Caenorhabditis elegans.

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