Intergenerational Transmission of Gene Regulatory Information in Caenorhabditis elegans

Minkina, Olga; Hunter, Craig P.

doi:10.1016/j.tig.2017.09.012

Cited by 53 publications

(47 citation statements)

References 62 publications

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“…At the across‐generations timescale, they affect the mutability of the very same DNA sequences, hence affecting evolutionary changes in the relevant functional DNA sequence over generations (Rey et al ., ). These two timescales are illustrated in C. elegans where neuron‐produced double‐stranded RNAs generate both intragenerational epigenetic silencing in somatic cells, and intergenerational epigenetic silencing in germ cells (Ashe et al ., ; Devanapally et al ., ; Klosin et al ., ; review in Vastenhouw et al ., ; Remy, ; Minkina & Hunter, ). Such unsuspected soma‐to‐germen communication (Sharma, ) in animals provides a potential mechanistic basis for the arrows converging towards epigenetics in Fig.…”

Section: Where To Next? Evolutionary Implications and Applications Ofmentioning

confidence: 99%

“…Studies in Caenorhabditis elegans underlined the role of non-coding RNAs in the non-genetic inheritance of environmentally induced phenotypes resulting from specific gene silencing. Such effects have been documented to persist for 3 (Greer et al, 2011), 14 (Klosin et al, 2017), 20 (Ashe et al, 2012), 25 (Devanapally, Ravikumar & Jose, 2015) and even 80 generations (for a review of epigenetic inheritance in C. elegans see Minkina & Hunter, 2018; see also Vastenhouw et al, 2006;Remy, 2010;review in Wang et al, 2017) -TrgE -probably NGGT Inheritance of traumatic exposure over several generations F1 and F2 offspring of F0 mice subjected to odour fear-conditioning before reproduction show an increased sensitivity to the usually ignored F0-conditioned odour but not to other odours (Dias & Ressler, 2014;Szyf, 2014). The fear conditioning in F0 parents leads to hypomethylation in the gametes of the conditioned F0 parents of the specific gene involved in the reception of that odour.…”

Section: Inheritance Of the Fitness-affecting Effects Of Pollutantsmentioning

confidence: 99%

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Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis

et al. 2018

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After decades of debate about the existence of non‐genetic inheritance, the focus is now slowly shifting towards dissecting its underlying mechanisms. Here, we propose a new mechanism that, by integrating non‐genetic and genetic inheritance, may help build the long‐sought inclusive vision of evolution. After briefly reviewing the wealth of evidence documenting the existence and ubiquity of non‐genetic inheritance in a table, we review the categories of mechanisms of parent–offspring resemblance that underlie inheritance. We then review several lines of argument for the existence of interactions between non‐genetic and genetic components of inheritance, leading to a discussion of the contrasting timescales of action of non‐genetic and genetic inheritance. This raises the question of how the fidelity of the inheritance system can match the rate of environmental variation. This question is central to understanding the role of different inheritance systems in evolution. We then review and interpret evidence indicating the existence of shifts from inheritance systems with low to higher transmission fidelity. Based on results from different research fields we propose a conceptual hypothesis linking genetic and non‐genetic inheritance systems. According to this hypothesis, over the course of generations, shifts among information systems allow gradual matching between the rate of environmental change and the inheritance fidelity of the corresponding response. A striking conclusion from our review is that documented shifts between types of inherited non‐genetic information converge towards epigenetics (i.e. inclusively heritable molecular variation in gene expression without change in DNA sequence). We then interpret the well‐documented mutagenicity of epigenetic marks as potentially generating a final shift from epigenetic to genetic encoding. This sequence of shifts suggests the existence of a relay in inheritance systems from relatively labile ones to gradually more persistent modes of inheritance, a relay that could constitute a new mechanistic basis for the long‐proposed, but still poorly documented, hypothesis of genetic assimilation. A profound difference between the genocentric and the inclusive vision of heredity revealed by the genetic assimilation relay proposed here lies in the fact that a given form of inheritance can affect the rate of change of other inheritance systems. To explore the consequences of such inter‐connection among inheritance systems, we briefly review published theoretical models to build a model of genetic assimilation focusing on the shift in the engraving of environmentally induced phenotypic variation into the DNA sequence. According to this hypothesis, when environmental change remains stable over a sufficient number of generations, the relay among inheritance systems has the potential to generate a form of genetic assimilation. In this hypothesis, epigenetics appears as a hub by which non‐genetically inherited environmentally induced variation in traits can be...

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Section: Where To Next? Evolutionary Implications and Applications Ofmentioning

confidence: 99%

Section: Inheritance Of the Fitness-affecting Effects Of Pollutantsmentioning

confidence: 99%

Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis

et al. 2018

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“…Epigenetic changes due to environmental influence can also affect multiple generations. This phenomenon has been extensively studied in C. elegans (reviewed in Minkina & Hunter, 2018). For example, a change in transgene expression induced by high rearing temperature in one generation was carried through multiple subsequent generations, and specifically traced to Histone3K9 methylation (Klosin, Casas, Hidalgo‐Carcedo, Vavouri, & Lehner, 2017).…”

Section: Mechanisms For Developmental Robustnessmentioning

confidence: 99%

Embryonic canalization and its limits—A view from temperature

Irvine

2020

J Exp Zool Pt B

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Many animals are able to produce similar offspring over a range of environmental conditions. This property of the developmental process has been termed canalization—the channeling of developmental pathways to generate a stable outcome despite varying conditions. Temperature is one environmental parameter that has fundamental effects on cell physiology and biochemistry, yet developmental programs generally result in a stable phenotype under a range of temperatures. On the other hand, there are typically upper and lower temperature limits beyond which the developmental program is unable to produce normal offspring. This review summarizes data on how development is affected by temperature, particularly high temperature, in various animal species. It also brings together information on potential cell biological and developmental genetic factors that may be responsible for developmental stability in varying temperatures, and likely critical mechanisms that break down at high temperature. Also reviewed are possible means for studying temperature effects on embryogenesis and how to determine which factors are most critical at the high‐temperature limits for normal development. Increased knowledge of these critical factors will point to the targets of selection under climate change, and more generally, how developmental robustness in varying environments is maintained.

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“…Although orthologous RNA decay pathways controlling nascent and mature RNA transcript stability are largely undefined, operons contain more than 75% of C. elegans genes involved in mRNA degradation pathways (Blumenthal and Gleason 2003), suggesting that pervasive RNA transcription may be self-regulated by precise control of post-transcriptional RNA stability (Blumenthal 2012). We suspect that an RNA surveillance capacity encoded by endogenous RNAi pathways (Minkina and Hunter 2018;Seth et al 2018) or microRNAs (Jan et al 2011) might target the selective degradation of germline-expressed growth transcripts in embryonic tissues which do not resume proliferation after hatching (Almeida et al 2019). Informed by stable transmission of an identical set of accessible chromatin sites, we are further interested in examining how pervasive RNA transcription in C. elegans might have evolved with other genome regulatory pathways, such as DNA replication, meiosis, and small RNA pathways Gu et al 2009;Gu et al 2012;Pourkarimi et al 2016).…”

Section: Operons Pervasive Transcription and Post-transcriptional Mmentioning

confidence: 99%

Persistent chromatin states, pervasive transcription, and sharedcis-regulatory sequences have shaped theC. elegansgenome

Whitehouse

2019

Preprint

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Despite highly conserved chromatin states and cis-regulatory elements, studies of metazoan genomes reveal that gene organization and the strategies to control mRNA expression can vary widely among animal species. C. elegans gene regulation is often assumed to be similar to that of other model organisms, yet evidence suggests the existence of distinct molecular mechanisms to pattern the developmental transcriptome, including extensive post-transcriptional RNA control pathways, widespread splice leader (SL) trans-splicing of pre-mRNAs, and the organization of genes into operons. Here, we performed ChIP-seq for histone modifications in highly synchronized embryos cohorts representing three major developmental stages, with the goal of better characterizing whether the dynamic changes in embryonic mRNA expression are accompanied by changes to the chromatin state. We were surprised to find that thousands of promoters are persistently marked by active histone modifications, despite a fundamental restructuring of the transcriptome. We employed global run-on sequencing using a long-read nanopore format to map nascent RNA transcription across embryogenesis, finding that the invariant open chromatin regions are persistently transcribed by Pol II at all stages of embryo development, even though the mature mRNA is not produced. By annotating our nascent RNA sequencing reads into directional transcription units, we find extensive evidence of polycistronic RNA transcription genome-wide, suggesting that nearby genes in C. elegans are linked by shared transcriptional regulatory mechanisms. We present data indicating that the sharing of cisregulatory sequences has constrained C. elegans gene positioning and likely explains the remarkable retention of syntenic gene pairs over long evolutionary timescales.

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Intergenerational Transmission of Gene Regulatory Information in Caenorhabditis elegans

Cited by 53 publications

References 62 publications

Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis

Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis

Embryonic canalization and its limits—A view from temperature

Persistent chromatin states, pervasive transcription, and sharedcis-regulatory sequences have shaped theC. elegansgenome

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