Explore the vast range of titles available.

Epigenetic modifications control gene expression and are essential for turning genes on and off to regulate and maintain differentiated cell types. Epigenetics are also modified by a multitude of environmental exposures, including diet and pollutants, allowing an individual’s environment to influence gene expression and resultant phenotypes and clinical outcomes. These epigenetic modifications due to gene–environment interactions can also be transmitted across generations, raising the possibility that environmental influences that occurred in one generation may be transmitted beyond the second generation, exerting a long-lasting effect. In this review, we cover the known mechanisms of epigenetic modification acquisition, reprogramming and persistence, animal models and human studies used to understand multigenerational epigenetic transmission, and examples of environmentally induced epigenetic change and its transmission across generations. We highlight the importance of environmental health not only on the current population but also on future generations that will experience health outcomes transmitted through epigenetic inheritance.

DNA methylation is a conserved epigenetic mark that plays important roles in maintaining genome stability and regulating gene expression. As sessile organisms, plants have evolved sophisticated regulatory systems to endure or respond to diverse adverse abiotic environmental challenges, i.e., abiotic stresses, such as extreme temperatures (cold and heat), drought and salinity. Plant stress responses are often accompanied by changes in chromatin modifications at diverse responsive loci, such as 5-methylcytosine (5mC) and N 6 -methyladenine (6mA) DNA methylation. Some abiotic stress responses are memorized for several hours or days through mitotic cell divisions and quickly reset to baseline levels after normal conditions are restored, which is referred to as somatic memory. In some cases, stress-induced chromatin marks are meiotically heritable and can impart the memory of stress exposure from parent plants to at least the next stress-free offspring generation through the mechanisms of transgenerational epigenetic inheritance, which may offer the descendants the potential to be adaptive for better fitness. In this review, we briefly summarize recent achievements regarding the establishment, maintenance and reset of DNA methylation, and highlight the diverse roles of DNA methylation in plant responses to abiotic stresses. Further, we discuss the potential role of DNA methylation in abiotic stress-induced somatic memory and transgenerational inheritance. Future research directions are proposed to develop stress-tolerant engineered crops to reduce the negative effects of abiotic stresses.

Similar to environmental factors, EDCs (endocrine-disrupting chemicals) can influence gene expression without modifying the DNA sequence. It is commonly accepted that the transgenerational inheritance of parentally acquired traits is conveyed by epigenetic alterations also known as “epimutations”. DNA methylation, acetylation, histone modification, RNA-mediated effects and extracellular vesicle effects are the mechanisms that have been described so far to be responsible for these epimutations. They may lead to the transgenerational inheritance of diverse phenotypes in the progeny when they occur in the germ cells of an affected individual. While EDC-induced health effects have dramatically increased over the past decade, limited effects on sperm epigenetics have been described. However, there has been a gain of interest in this issue in recent years. The gametes (sperm and oocyte) represent targets for EDCs and thus a route for environmentally induced changes over several generations. This review aims at providing an overview of the epigenetic mechanisms that might be implicated in this transgenerational inheritance.

Plants respond to drought stress by producing abscisic acid, a chemical messenger that regulates gene expression and thereby expedites various physiological and cellular processes including the stomatal operation to mitigate stress and promote tolerance. To trigger or suppress gene transcription under drought stress conditions, the surrounding chromatin architecture must be converted between a repressive and active state by epigenetic remodeling, which is achieved by the dynamic interplay among DNA methylation, histone modifications, loop formation, and non-coding RNA generation. Plants can memorize chromatin status under drought conditions to enable them to deal with recurrent stress. Furthermore, drought tolerance acquired during plant growth can be transmitted to the next generation. The epigenetically modified chromatin architectures of memory genes under stressful conditions can be transmitted to newly developed cells by mitotic cell division, and to germline cells of offspring by overcoming the restraints on meiosis. In mammalian cells, the acquired memory state is completely erased and reset during meiosis. The mechanism by which plant cells overcome this resetting during meiosis to transmit memory is unclear. In this article, we review recent findings on the mechanism underlying transcriptional stress memory and the transgenerational inheritance of drought tolerance in plants.

Experiences during the lifetime of an animal have been proposed to have consequences for subsequent generations. Although it is unclear how such intergenerational transfer of information occurs, RNAs found extracellularly in animals are candidate molecules that can transfer gene-specific regulatory information from one generation to the next because they can enter cells and regulate gene expression. In support of this idea, when double-stranded RNA (dsRNA) is introduced into some animals, the dsRNA can silence genes of matching sequence and the silencing can persist in progeny. Such persistent gene silencing is thought to result from sequence-specific interaction of the RNA within parents to generate chromatin modifications, DNA methylation, and/or secondary RNAs, which are then inherited by progeny. Here, we show that dsRNA can be directly transferred between generations in the worm Caenorhabditis elegans. Intergenerational transfer of dsRNA occurs even in animals that lack any DNA of matching sequence, and dsRNA that reaches progeny can spread between cells to cause gene silencing. Surprisingly, extracellular dsRNA can also reach progeny without entry into the cytosol, presumably within intracellular vesicles. Fluorescently labeled dsRNA is imported from extracellular space into oocytes along with yolk and accumulates in punctate structures within embryos. Subsequent entry into the cytosol of early embryos causes gene silencing in progeny. These results demonstrate the transport of extracellular RNA from one generation to the next to regulate gene expression in an animal and thus suggest a mechanism for the transmission of experience-dependent effects between generations.

The plant hormone abscisic acid (ABA) triggers cellular tolerance responses to osmotic stress caused by drought and salinity. ABA controls the turgor pressure of guard cells in the plant epidermis, leading to stomatal closure to minimize water loss. However, stomatal apertures open to uptake CO2 for photosynthesis even under stress conditions. ABA modulates its signaling pathway via negative feedback regulation to maintain plant homeostasis. In the nuclei of guard cells, the clade A type 2C protein phosphatases (PP2Cs) counteract SnRK2 kinases by physical interaction, and thereby inhibit activation of the transcription factors that mediate ABA-responsive gene expression. Under osmotic stress conditions, PP2Cs bind to soluble ABA receptors to capture ABA and release active SnRK2s. Thus, PP2Cs function as a switch at the center of the ABA signaling network. ABA induces the expression of genes encoding repressors or activators of PP2C gene transcription. These regulators mediate the conversion of PP2C chromatins from a repressive to an active state for gene transcription. The stress-induced chromatin remodeling states of ABA-responsive genes could be memorized and transmitted to plant progeny; i.e., transgenerational epigenetic inheritance. This review focuses on the mechanism by which PP2C gene transcription modulates ABA signaling.

Background Hybridization and backcrossing are commonly used in animal and plant breeding to induce heritable variation including epigenetic changes such as paramutation. However, the molecular basis for hybrid-induced epigenetic memory remains elusive. Results Here, we report that hybridization between the inbred parents B73 and Mo17 induces trans -acting hypermethylation and hypomethylation at thousands of loci; several hundreds (~ 3%) are transmitted through six backcrossing and three selfing generations. Notably, many transgenerational methylation patterns resemble epialleles of the nonrecurrent parent, despite > 99% of overall genomic loci are converted to the recurrent parent. These epialleles depend on 24-nt siRNAs, which are eliminated in the isogenic hybrid Mo17xB73: mop1-1 that is defective in siRNA biogenesis. This phenomenon resembles paramutation-like events and occurs in both intraspecific (Mo17xB73) and interspecific (W22xTeosinte) hybrid maize populations. Moreover, siRNA abundance and methylation levels of these epialleles can affect expression of their associated epigenes, many of which are related to stress responses. Conclusion Divergent siRNAs between the hybridizing parents can induce trans -acting epialleles in the hybrids, while the induced epigenetic status is maintained for transgenerational inheritance during backcross and hybrid breeding, which alters epigene expression to enhance growth and adaptation. These genetic and epigenetic principles may apply broadly from plants to animals.

[This corrects the article DOI: 10.3389/fpls.2022.958350.].

If food and feed production are to keep up with world demand in the face of climate change, continued progress in understanding and utilizing both genetic and epigenetic sources of crop variation is necessary. Progress in plant breeding has traditionally been thought to be due to selection for spontaneous DNA sequence mutations that impart desirable phenotypes. These spontaneous mutations can expand phenotypic diversity, from which breeders can select agronomically useful traits. However, it has become clear that phenotypic diversity can be generated even when the genome sequence is unaltered. Epigenetic gene regulation is a mechanism by which genome expression is regulated without altering the DNA sequence. With the development of high throughput DNA sequencers, it has become possible to analyze the epigenetic state of the whole genome, which is termed the epigenome. These techniques enable us to identify spontaneous epigenetic mutations (epimutations) with high throughput and identify the epimutations that lead to increased phenotypic diversity. These epimutations can create new phenotypes and the causative epimutations can be inherited over generations. There is evidence of selected agronomic traits being conditioned by heritable epimutations, and breeders may have historically selected for epiallele-conditioned agronomic traits. These results imply that not only DNA sequence diversity, but the diversity of epigenetic states can contribute to increased phenotypic diversity. However, since the modes of induction and transmission of epialleles and their stability differ from that of genetic alleles, the importance of inheritance as classically defined also differs. For example, there may be a difference between the types of epigenetic inheritance important to crop breeding and crop production. The former may depend more on longer-term inheritance whereas the latter may simply take advantage of shorter-term phenomena. With the advances in our understanding of epigenetics, epigenetics may bring new perspectives for crop improvement, such as the use of epigenetic variation or epigenome editing in breeding. In this review, we will introduce the role of epigenetic variation in plant breeding, largely focusing on DNA methylation, and conclude by asking to what extent new knowledge of epigenetics in crop breeding has led to documented cases of its successful use.

Plants differ from animals in their capability to easily regenerate fertile adult individuals from terminally differentiated cells. This unique developmental plasticity is commonly observed in nature, where many species can reproduce asexually through the ectopic initiation of organogenic or embryogenic developmental programs. While organ-specific epigenetic marks are not passed on during sexual reproduction, the fate of epigenetic marks during asexual reproduction and the implications for clonal progeny remain unclear. Here we report that organ-specific epigenetic imprints in Arabidopsis thaliana can be partially maintained during asexual propagation from somatic cells in which a zygotic program is artificially induced. The altered marks are inherited even over multiple rounds of sexual reproduction, becoming fixed in hybrids and resulting in heritable molecular and physiological phenotypes that depend on the identity of the founder tissue. Consequently, clonal plants display distinct interactions with beneficial and pathogenic microorganisms. Our results demonstrate how novel phenotypic variation in plants can be unlocked through altered inheritance of epigenetic marks upon asexual propagation.