scholarly journals Molecular evolution across developmental time reveals rapid divergence in early embryogenesis

2019 ◽  
Author(s):  
Asher D. Cutter ◽  
Rose H. Garrett ◽  
Stephanie Mark ◽  
Wei Wang ◽  
Lei Sun

AbstractOntogenetic development hinges on the changes in gene expression in time and space within an organism, suggesting that the demands of ontogenetic growth can impose or reveal predictable pattern in the molecular evolution of genes expressed dynamically across development. Here we characterize co-expression modules of the C. elegans transcriptome, using a time series of 30 points from early-embryo to adult. By capturing the functional form of expression profiles with quantitative metrics, we find fastest evolution in the distinctive set of genes with transcript abundance that declines through development from a peak in young embryos. These genes are highly enriched for oogenic function (maternal provisioning), are non-randomly distributed in the genome, and correspond to a life stage especially prone to inviability in inter-species hybrids. These observations conflict with the “early conservation model” for the evolution of development, though expression-weighted sequence divergence analysis provides some support for the “hourglass model.” Genes in co-expression modules that peak toward adulthood also evolve fast, being hyper-enriched for roles in spermatogenesis, implicating a history of sexual selection and relaxation of selection on sperm as key factors driving rapid change to ontogenetically distinguishable co-expression modules of genes. We propose that these predictable trends of molecular evolution for dynamically-expressed genes across ontogeny predispose particular life stages, early embryogenesis in particular, to hybrid dysfunction in the speciation process.Impact SummaryThe development of an organism from a single-celled embryo to a reproductive adult depends on dynamic gene expression over developmental time, with natural selection capable of shaping the molecular evolution of those differentially-expressed genes in distinct ways. We quantitatively analyzed the dynamic transcriptome profiles across 30 timepoints in development for the nematode C. elegans. In addition to rapid evolution of adult-expressed genes with functional roles in sperm, we uncovered the unexpected result that the distinctive set of genes that evolve fastest are those with peak expression in young embryos, conflicting with some models of the evolution of development. The rapid molecular evolution of genes in early embryogenesis contrasts with the exceptional conservation of embryonic cell lineages between species, and corresponds to a developmental period that is especially sensitive to inviability in inter-species hybrid embryos. We propose that these predictable trends of molecular evolution for dynamically-expressed genes across development predispose particular life stages, early embryogenesis in particular, to hybrid dysfunction in the speciation process.

2019 ◽  
Author(s):  
Meghan E. Costello ◽  
Lisa N. Petrella

AbstractTissue-specific establishment of repressive chromatin through creation of compact chromatin domains during development is necessary to ensure proper gene expression and cell fate. C. elegans synMuv B proteins are important for the soma/germline fate decision and mutants demonstrate ectopic germline gene expression in somatic tissue, especially at high temperature. We show that C. elegans synMuv B proteins regulate developmental chromatin compaction and that timing of chromatin compaction is temperature sensitive in both wild-type and synMuv B mutants. Chromatin compaction in mutants is delayed into developmental time-periods when zygotic gene expression is upregulated and demonstrates an anterior-to-posterior pattern. Loss of this patterned compaction coincides with the developmental time-period of ectopic germline gene expression that leads to a developmental arrest in synMuv B mutants. Thus, chromatin organization throughout development is regulated both spatially and temporally by synMuv B proteins to establish repressive chromatin in a tissue-specific manner to ensure proper gene expression.


2019 ◽  
Vol 3 (4) ◽  
pp. 359-373 ◽  
Author(s):  
Asher D. Cutter ◽  
Rose H. Garrett ◽  
Stephanie Mark ◽  
Wei Wang ◽  
Lei Sun

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Wenjing Qi ◽  
Erika D. V. Gromoff ◽  
Fan Xu ◽  
Qian Zhao ◽  
Wei Yang ◽  
...  

AbstractMulticellular organisms coordinate tissue specific responses to environmental information via both cell-autonomous and non-autonomous mechanisms. In addition to secreted ligands, recent reports implicated release of small RNAs in regulating gene expression across tissue boundaries. Here, we show that the conserved poly-U specific endoribonuclease ENDU-2 in C. elegans is secreted from the soma and taken-up by the germline to ensure germline immortality at elevated temperature. ENDU-2 binds to mature mRNAs and negatively regulates mRNA abundance both in the soma and the germline. While ENDU-2 promotes RNA decay in the soma directly via its endoribonuclease activity, ENDU-2 prevents misexpression of soma-specific genes in the germline and preserves germline immortality independent of its RNA-cleavage activity. In summary, our results suggest that the secreted RNase ENDU-2 regulates gene expression across tissue boundaries in response to temperature alterations and contributes to maintenance of stem cell immortality, probably via retaining a stem cell specific program of gene expression.


2014 ◽  
Vol 4 (1) ◽  
Author(s):  
L. Basten Snoek ◽  
Mark G. Sterken ◽  
Rita J. M. Volkers ◽  
Mirre Klatter ◽  
Kobus J. Bosman ◽  
...  

2011 ◽  
Vol 355 (2) ◽  
pp. 302-312 ◽  
Author(s):  
Eisuke Sumiyoshi ◽  
Sachiko Takahashi ◽  
Hatsue Obata ◽  
Asako Sugimoto ◽  
Yuji Kohara

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Mark G. Sterken ◽  
Marijke H. van Wijk ◽  
Elizabeth C. Quamme ◽  
Joost A. G. Riksen ◽  
Lucinda Carnell ◽  
...  

AbstractEthanol-induced transcriptional changes underlie important physiological responses to ethanol that are likely to contribute to the addictive properties of the drug. We examined the transcriptional responses of Caenorhabditis elegans across a timecourse of ethanol exposure, between 30 min and 8 h, to determine what genes and genetic pathways are regulated in response to ethanol in this model. We found that short exposures to ethanol (up to 2 h) induced expression of metabolic enzymes involved in metabolizing ethanol and retinol, while longer exposure (8 h) had much more profound effects on the transcriptome. Several genes that are known to be involved in the physiological response to ethanol, including direct ethanol targets, were regulated at 8 h of exposure. This longer exposure to ethanol also resulted in the regulation of genes involved in cilia function, which is consistent with an important role for the effects of ethanol on cilia in the deleterious effects of chronic ethanol consumption in humans. Finally, we found that food deprivation for an 8-h period induced gene expression changes that were somewhat ameliorated by the presence of ethanol, supporting previous observations that worms can use ethanol as a calorie source.


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