Present and future challenges for the investigation of transgenerational epigenetic inheritance

Fallet, Manon; Blanc, Mélanie; Criscio, Michela Di; Antczak, Philipp; Engwall, Magnus; Guerrero-Bosagna, Carlos; Rüegg, Joëlle; Keiter, Steffen H.

doi:10.1016/j.envint.2023.107776

Cited by 30 publications

(19 citation statements)

References 184 publications

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“…Similar results were found in the clonal species Alternanthera philoxeroides, where parental herbivory could affect the growth and defense of offspring plants [61]. Emerging research has shown that such transgenerational effects are mediated by epigenetic modifications such as DNA methylation, histone modification, and chromatin remodeling, without alteration of the nucleotide sequence that can persist across multiple generations [62][63][64][65]. Our previous research further demonstrated that clonal transgenerational dwarfism effects induced by grazing history in L. chinensis were mediated by DNA methylation [46].…”

Section: Discussionsupporting

confidence: 75%

Clonal Transgenerational Effects of Parental Grazing Environment on Offspring Shade Avoidance

Yin,

Ren,

Fry

et al. 2024

Agronomy

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Grassland plants that endure livestock grazing exhibit a dwarf phenotype, which can be transmitted to clonal offspring. Yet to date, it remains poorly understood whether such transgenerational dwarf effects alter the plants’ response to shade. Here, we conducted a common garden experiment under sunlight and shade conditions with clonal Leymus chinensis offspring, the parents of which had endured livestock overgrazing (OG) and non-grazing (NG) in the field, respectively. Plant morphological, physiological, and transcriptomic analyses were carried out. The results indicated that NG offspring showed greater shade avoidance than OG offspring. That is, NG offspring exhibited greater plasticity of vegetative height and leaf width, which may be contributed to their greater photosynthetic capacity and gibberellin (GA3) content compared with OG offspring when treated with shade. In addition, RNA-Seq profiling showed that differentially expressed genes in NG offspring were mainly enriched in RNA modification and metabolic processes, which facilitated rapid response to shade. Phytochrome interacting factors (PIFs) promoted downstream shade marker genes in NG offspring by significantly downregulating the expression of PHYC, SPY, and DELLA. Our findings suggest that light conditions should be taken into account to better understand transgenerational dwarf effects induced by livestock grazing on grassland ecosystems. These results provide new insights into the inducible factors of phenotypic variations in grassland plants that experience grazing.

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Section: Discussionsupporting

confidence: 75%

Clonal Transgenerational Effects of Parental Grazing Environment on Offspring Shade Avoidance

Yin,

Ren,

Fry

et al. 2024

Agronomy

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“…However, the assessment of parental effects being the result of nongenetic inheritance of chemical-induced effects requires to detangle nongenetic from genetic effects, which is recognized as a highly tricky task. 61 Indeed, epigenetic mechanisms could mediate nongenetic effects, 62 and epigenetic divergence could be faster and predominant over genetic divergence in rapid adaptation of oysters. 63 Besides, the data herein do not allow to quantify the relative prevalence of genetic and epigenetic effects.…”

Section: Discussionmentioning

confidence: 99%

Ancestors’ Gift: Parental Early Exposure to the Environmentally Realistic Pesticide Mixture Drives Offspring Phenotype in a Larger Extent Than Direct Exposure in the Pacific Oyster, Crassostrea gigas

Sol Dourdin,

Guyomard,

Rabiller

et al. 2024

Environ. Sci. Technol.

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Marine organisms are threatened by the presence of pesticides in coastal waters. Among them, the Pacific oyster is one of the most studied invertebrates in marine ecotoxicology where numerous studies highlighted the multiscale impacts of pesticides. In the past few years, a growing body of literature has reported the epigenetic outcomes of xenobiotics. Because DNA methylation is an epigenetic mark implicated in organism development and is meiotically heritable, it raises the question of the multigenerational implications of xenobioticinduced epigenetic alterations. Therefore, we performed a multigenerational exposure to an environmentally relevant mixture of 18 pesticides (nominal sum concentration: 2.85 μg•L −1 ) during embryo−larval stages (0−48 hpf) of a second generation (F1) for which parents where already exposed or not in F0. Gene expression, DNA methylation, and physiological end points were assessed throughout the life cycle of individuals. Overall, the multigenerational effect has a greater influence on the phenotype than the exposure itself. Thus, multigenerational phenotypic effects were observed: individuals descending from exposed parents exhibited lower epinephrine-induced metamorphosis and field survival rates. At the molecular level, RNA-seq and Methyl-seq data analyses performed in gastrula embryos and metamorphosis-competent pediveliger (MCP) larvae revealed a clear F0 treatment-dependent discrimination. Some genes implicated into shell secretion and immunity exhibited F1:F0 treatment interaction patterns (e.g., Calm and Myd88). Those results suggest that low chronic environmental pesticide contamination can alter organisms beyond the individual scale level and have long-term adaptive implications.

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“…Relatively little is known or empirically demonstrated about the conditions under which the evolution of adaptive TEI would be anticipated 26 , and—perhaps controversially to some—it is hypothesized that transgenerational epigenetic effects may not consistently confer benefits in adaptive plasticity under challenging environments 25,26,37 . Existing empirical work on the phenotypic effects of TEI primarily relies on correlational findings due to the complexity of epigenetic modifications and their varied impacts on organismal fitness 38–40 . Despite efforts to discover causal relationships, distinguishing between adaptive, nonadaptive, and maladaptive epigenetic changes remains challenging, as some modifications may lack discernable physiological consequences or remain silent 24,40,41 .…”

Section: Main Textmentioning

confidence: 99%

“…Existing empirical work on the phenotypic effects of TEI primarily relies on correlational findings due to the complexity of epigenetic modifications and their varied impacts on organismal fitness 38–40 . Despite efforts to discover causal relationships, distinguishing between adaptive, nonadaptive, and maladaptive epigenetic changes remains challenging, as some modifications may lack discernable physiological consequences or remain silent 24,40,41 . Another potential outcome of TEI is an overall increase in phenotypic variance, which could result either through selection and be categorized as ‘heritable bet hedging’ 26 , or as a result of cumulative stress 42 .…”

Section: Main Textmentioning

confidence: 99%

Transgenerational epigenetic inheritance increases trait variation but is not adaptive

Shahmohamadloo,

Fryxell,

Rudman

2024

Preprint

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Understanding processes that can produce adaptive phenotypic shifts in response to rapid environmental change is critical to reducing biodiversity loss. The ubiquity of environmentally induced epigenetic marks has led to speculation that epigenetic inheritance could potentially enhance population persistence in response to environmental change. Yet, the magnitude and fitness consequences of epigenetic marks carried beyond maternal inheritance are largely unknown. Here, we tested how transgenerational epigenetic inheritance (TEI) shapes the phenotypic response ofDaphniaclones to the environmental stressorMicrocystis. We split individuals from each of eight genotypes into exposure and control treatments (F0 generation) and tracked the fitness of their descendants to the F3 generation. We found transgenerational epigenetic exposure toMicrocystisled to reduced rates of survival and individual growth and no consistent effect on offspring production. Increase in trait variance in the F3 relative to F0 generations suggests potential for heritable bet hedging driven by TEI, which could impact population dynamics. Our findings are counter to the working hypothesis that TEI is a generally adaptive mechanism likely to prevent extinction for populations inhabiting rapidly changing environments.

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Present and future challenges for the investigation of transgenerational epigenetic inheritance

Cited by 30 publications

References 184 publications

Clonal Transgenerational Effects of Parental Grazing Environment on Offspring Shade Avoidance

Clonal Transgenerational Effects of Parental Grazing Environment on Offspring Shade Avoidance

Ancestors’ Gift: Parental Early Exposure to the Environmentally Realistic Pesticide Mixture Drives Offspring Phenotype in a Larger Extent Than Direct Exposure in the Pacific Oyster, Crassostrea gigas

Transgenerational epigenetic inheritance increases trait variation but is not adaptive

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