scholarly journals Intercellular transport of RNA can limit heritable epigenetic changes

2021 ◽  
Author(s):  
Nathan Shugarts ◽  
Andrew L. Yi ◽  
Winnie M. Chan ◽  
Julia A. Marré ◽  
Aishwarya Sathya ◽  
...  

AbstractRNAs in circulation carry sequence-specific regulatory information between cells in animal, plant, and host-pathogen systems. Double-stranded RNA (dsRNA) delivered into the extracellular space of the nematode C. elegans accumulates within the germline and reaches progeny. Here we provide evidence for spatial, temporal, and substrate specificity in the transport of dsRNA from parental circulation to progeny. Temporary loss of dsRNA transport resulted in the persistent accumulation of mRNA from a germline gene. The expression of this gene varied among siblings and even between gonad arms within one animal. Perturbing RNA regulation of the gene created new epigenetic states that lasted for many generations. Thus, one role for the transport of dsRNA into the germline in every generation is to limit heritable changes in gene expression.One Sentence SummaryRNA from parental circulation reduces heritable changes in gene expression.

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.


Cell ◽  
2013 ◽  
Vol 155 (7) ◽  
pp. 1532-1544 ◽  
Author(s):  
Colin C. Conine ◽  
James J. Moresco ◽  
Weifeng Gu ◽  
Masaki Shirayama ◽  
Darryl Conte ◽  
...  

2000 ◽  
Vol 6 (3) ◽  
pp. 605-616 ◽  
Author(s):  
Valerie Reinke ◽  
Harold E. Smith ◽  
Jeremy Nance ◽  
John Wang ◽  
Carrie Van Doren ◽  
...  

2013 ◽  
Vol 27 (6) ◽  
pp. 664-671 ◽  
Author(s):  
Christopher J. Wedeles ◽  
Monica Z. Wu ◽  
Julie M. Claycomb

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Sindhuja Devanapally ◽  
Pravrutha Raman ◽  
Mary Chey ◽  
Samual Allgood ◽  
Farida Ettefa ◽  
...  

AbstractStable epigenetic changes appear uncommon, suggesting that changes typically dissipate or are repaired. Changes that stably alter gene expression across generations presumably require particular conditions that are currently unknown. Here we report that a minimal combination of cis-regulatory sequences can support permanent RNA silencing of a single-copy transgene and its derivatives in C. elegans simply upon mating. Mating disrupts competing RNA-based mechanisms to initiate silencing that can last for >300 generations. This stable silencing requires components of the small RNA pathway and can silence homologous sequences in trans. While animals do not recover from mating-induced silencing, they often recover from and become resistant to trans silencing. Recovery is also observed in most cases when double-stranded RNA is used to silence the same coding sequence in different regulatory contexts that drive germline expression. Therefore, we propose that regulatory features can evolve to oppose permanent and potentially maladaptive responses to transient change.


2021 ◽  
Vol 220 (9) ◽  
Author(s):  
Mezmur D. Belew ◽  
Emilie Chien ◽  
Matthew Wong ◽  
W. Matthew Michael

While much is known about how transcription is controlled at individual genes, comparatively little is known about how cells regulate gene expression on a genome-wide level. Here, we identify a molecular pathway in the C. elegans germline that controls transcription globally in response to nutritional stress. We report that when embryos hatch into L1 larvae, they sense the nutritional status of their environment, and if food is unavailable, they repress gene expression via a global chromatin compaction (GCC) pathway. GCC is triggered by the energy-sensing kinase AMPK and is mediated by a novel mechanism that involves the topoisomerase II/condensin II axis acting upstream of heterochromatin assembly. When the GCC pathway is inactivated, then transcription persists during starvation. These results define a new mode of whole-genome control of transcription.


2013 ◽  
Vol 27 (6) ◽  
pp. 656-663 ◽  
Author(s):  
Meetu Seth ◽  
Masaki Shirayama ◽  
Weifeng Gu ◽  
Takao Ishidate ◽  
Darryl Conte ◽  
...  

2018 ◽  
Author(s):  
En-Zhi Shen ◽  
Hao Chen ◽  
Ahmet R. Ozturk ◽  
Shikui Tu ◽  
Masaki Shirayama ◽  
...  

SUMMARYpiRNAs (Piwi-interacting small RNAs) engage Piwi Argonautes to silence transposons and promote fertility in animal germlines. Genetic and computational studies have suggested that C. elegans piRNAs tolerate mismatched pairing and in principle could target every transcript. Here we employ in vivo cross-linking to identify transcriptome-wide interactions between piRNAs and target RNAs. We show that piRNAs engage all germline mRNAs and that piRNA binding follows microRNA-like pairing rules. Targeting correlates better with binding energy than with piRNA abundance, suggesting that piRNA concentration does not limit targeting. In mRNAs silenced by piRNAs, secondary small RNAs accumulate at the center and ends of piRNA binding sites. In germline-expressed mRNAs, however, targeting by the CSR-1 Argonaute correlates with reduced piRNA binding density and suppression of piRNA-associated secondary small RNAs. Our findings reveal physiologically important and nuanced regulation of individual piRNA targets and provide evidence for a comprehensive post transcriptional regulatory step in germline gene expression.


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