Developmental systems of plasticity and trans-generational epigenetic inheritance in nematodes

Serobyan, Vahan; Sommer, Ralf J.

doi:10.1016/j.gde.2017.03.001

Cited by 31 publications

(24 citation statements)

References 39 publications

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“…Understanding the molecular mechanisms of plasticity and how these mechanisms evolve––and how their evolution, in turn, impacts plasticity's evolution––is an important frontier in ecology and evolution (Gilbert & Epel, 2015; Levis & Pfennig, 2020). While a growing number of studies have begun to illuminate how plasticity is regulated (Beldade et al, 2011; Lafuente & Beldade, 2019; Parsons et al., 2016; Projecto‐Garcia, Biddle, & Ragsdale, 2017; Richard, Le Trionnaire, Danchin, & Sentis, 2019; Serobyan & Sommer, 2017), much work remains. For instance, as noted in the Introduction, the prevailing view is that plasticity and its resulting phenotypes are regulated by different loci (Lafuente et al., 2018; Ørsted et al., 2018; Scheiner & Lyman, 1991; Schlichting & Pigliucci, 1993; Windig et al., 2004).…”

Section: Discussionmentioning

confidence: 99%

Identification of candidate loci for adaptive phenotypic plasticity in natural populations of spadefoot toads

Levis

Reed

Pfennig

et al. 2020

Ecology and Evolution

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Phenotypic plasticity allows organisms to alter their phenotype in direct response to changes in the environment. Despite growing recognition of plasticity's role in ecology and evolution, few studies have probed plasticity's molecular bases—especially using natural populations. We investigated the genetic basis of phenotypic plasticity in natural populations of spadefoot toads (Spea multiplicata). Spea tadpoles normally develop into an “omnivore” morph that is favored in long‐lasting, low‐density ponds. However, if tadpoles consume freshwater shrimp or other tadpoles, they can alternatively develop (via plasticity) into a “carnivore” morph that is favored in ephemeral, high‐density ponds. By combining natural variation in pond ecology and morph production with population genetic approaches, we identified candidate loci associated with each morph (carnivores vs. omnivores) and loci associated with adaptive phenotypic plasticity (adaptive vs. maladaptive morph choice). Our candidate morph loci mapped to two genes, whereas our candidate plasticity loci mapped to 14 genes. In both cases, the identified genes tended to have functions related to their putative role in spadefoot tadpole biology. Our results thereby form the basis for future studies into the molecular mechanisms that mediate plasticity in spadefoots. More generally, these results illustrate how diverse loci might mediate adaptive plasticity.

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Section: Discussionmentioning

confidence: 99%

Identification of candidate loci for adaptive phenotypic plasticity in natural populations of spadefoot toads

Levis

Reed

Pfennig

et al. 2020

Ecology and Evolution

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“…yeast, plants and in the nematode Caenorhabditis elegans have been published previously [22][23][24][25][26][27][28][29] . Here, we discuss examples of MEI and epigenome reprogramming in vertebrates and elaborate on the mechanisms of MEI, namely through DNA methylation, histone modifica tions, tRNA fragments (tRFs) and other small RNAs.…”

Section: Intergenerational Epigenetic Inheritancementioning

confidence: 99%

“…Although many studies of meiotic epigenetic inheritance (meI) in animals have been published to date, the field is still facing substantial challenges. Whereas meI in plants and nematodes encompasses a series of well-studied phenomena [24][25][26][27][28] , meI studies in mammals have proved especially challenging to set up and to interpret owing to many external confounding factors, which can easily result in the misinterpretation of acquired data 88 . First, studies dealing with meI should, where possible, incorporate robust dNA sequencing controls to exclude potential genetic contributions to the studied phenomena 84 .…”

Section: Box 1 | Interpreting Meiotic Epigenetic Inheritance Studies mentioning

confidence: 99%

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Functions and mechanisms of epigenetic inheritance in animals

Skvortsova

Iovino

Bogdanović

2018

Nat Rev Mol Cell Biol

355

256

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| The idea that epigenetic determinants such as DNA methylation, histone modifications or RNA can be passed to the next generation through meiotic products (gametes) is long standing. Such meiotic epigenetic inheritance (MEI) is fairly common in yeast, plants and nematodes, but its extent in mammals has been much debated. Advances in genomics techniques are now driving the profiling of germline and zygotic epigenomes, thereby improving our understanding of MEI in diverse species. Whereas the role of DNA methylation in MEI remains unclear, insights from genome-wide studies suggest that a previously underappreciated fraction of mammalian genomes bypass epigenetic reprogramming during development. Notably , intergenerational inheritance of histone modifications, tRNA fragments and microRNAs can affect gene regulation in the offspring. It is important to note that MEI in mammals rarely constitutes transgenerational epigenetic inheritance (TEI), which spans multiple generations. In this Review , we discuss the examples of MEI in mammals, including mammalian epigenome reprogramming, and the molecular mechanisms of MEI in vertebrates in general. We also discuss the implications of the inheritance of histone modifications and small RNA for embryogenesis in metazoans, with a particular focus on insights gained from genome-wide studies.

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“…In Caenorhabditis elegans nematodes, much knowledge has been gained in recent years regarding the mechanisms that enable transgenerational gene regulation via inheritance of small RNAs Serobyan and Sommer, 2017). Dedicated small RNA inheritance proteins, which are required specifically for heritable responses, have been identified (de Albuquerque et al, 2015;Ashe et al, 2012;Buckley et al, 2012;Houri-Ze'evi et al, 2016;Lev et al, 2017Lev et al, , 2019Shirayama et al, 2012;Wan et al, 2018;Xu et al, 2018)).…”

Section: Introductionmentioning

confidence: 99%

Stress Resets Transgenerational Small RNA Inheritance

Houri-Zeevi

Teichman

Gingold

et al. 2019

Preprint

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Transgenerational inheritance of small RNAs is challenging basic concepts of heredity and achieving control over such responses is of great interest. In C. elegans nematodes, small RNAs are transmitted across generations to establish a transgenerational memory trace of ancestral environments and distinguish self from non-self genes. Inheritance of small RNAs is regulated by dedicated machinery and carryover of aberrant heritable small RNA responses was shown to be maladaptive and to induce sterility. Here we show that various types of stress (starvation, high temperatures, and high osmolarity) but not non-stressful changes in cultivation conditions, lead to resetting of small RNA inheritance. We found that stress leads to a genome-wide reduction in heritable small RNA levels and that mutants defective in different stress pathways exhibit irregular RNAi inheritance dynamics. Moreover, we discovered that resetting of heritable RNAi is orchestrated by MAPK pathway factors, the transcription factor SKN-1, and the MET-2 methyltransferase. Termination of small RNA inheritance, and the fact that this process depends on stress, could protect from run-on of environment-

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Developmental systems of plasticity and trans-generational epigenetic inheritance in nematodes

Cited by 31 publications

References 39 publications

Identification of candidate loci for adaptive phenotypic plasticity in natural populations of spadefoot toads

Identification of candidate loci for adaptive phenotypic plasticity in natural populations of spadefoot toads

Functions and mechanisms of epigenetic inheritance in animals

Stress Resets Transgenerational Small RNA Inheritance

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