Somatic epigenetic drift during shoot branching: a cell lineage-based model.

Plant architecture is shaped by the production of new organs, most of which emerge postembryonically. This process includes the formation of new lateral branches along existing shoots. Current evidence supports a detached-meristem model as the cellular basis of lateral shoot initiation. In this model, a small number of undifferentiated cells are sampled from the periphery of the shoot apical meristem (SAM) to act as precursors for axillary buds, which eventually develop into new shoots. Repeated branching thus creates cellular bottlenecks (i.e. somatic drift) that affect how de novo (epi)genetic mutations propagate through the plant body during development. Somatic drift could be particularly relevant for stochastic DNA methylation gains and losses (i.e. spontaneous epimutations), as they have been shown to arise rapidly with each cell division. Here, we formalize a special case of the detached-meristem model, where precursor cells are randomly sampled from the SAM periphery in a way that maximizes cell lineage independence. We show that somatic drift during repeated branching gives rise to a mixture of cellular phylogenies within the SAM over time. This process is dependent on the number of branch points, the strength of drift as well as the epimutation rate. Our model predicts that cell-to-cell DNA methylation heterogeneity in the SAM converges to nonzero states during development, suggesting that epigenetic variation is an inherent property of the SAM cell population. Our insights have direct implications for empirical studies of somatic (epi)genomic diversity in long-lived perennial and clonal species using bulk or single-cell sequencing approaches.

Plant histone variants at the nexus of chromatin readouts, stress and development.

Histones are crucial proteins that are involved in packaging the DNA as condensed chromatin inside the eukaryotic cell nucleus. Rather than being static packaging units, these molecules undergo drastic variations spatially and temporally to facilitate accessibility of DNA to replication, transcription as well as wide range of gene regulatory machineries. In addition, incorporation of paralogous variants of canonical histones in the chromatin is ascribed to specific functions. Given the peculiar requirement of plants to rapidly modulate gene expression levels on account of their sessile nature, histones and their variants serve as additional layers of gene regulation. This review summarizes the mechanisms and implications of distribution, modifications and differential incorporation of histones and their variants across plant genomes, and outlines emerging themes.

Epigenetic Control of Plant Response to Heavy Metals.

Plants are sessile organisms that must adapt to environmental conditions, such as soil characteristics, by adjusting their development during their entire life cycle. In case of low-distance seed dispersal, the new generations are challenged with the same abiotic stress encountered by the parents. Epigenetic modification is an effective option that allows plants to face an environmental constraint and to share the same adaptative strategy with their progeny through transgenerational inheritance. This is the topic of the presented review that reports the scientific progress, up to date, gained in unravelling the epigenetic response of plants to soil contamination by heavy metals and metalloids, collectively known as potentially toxic elements. The effect of the microbial community inhabiting the rhizosphere is also considered, as the evidence of a transgenerational transfer of the epigenetic status that contributes to the activation in plants of response mechanisms to soil pollution.

Covalent RNA modifications and their budding crosstalk with plant epigenetic processes.

Our recent cognizance of diverse RNA classes undergoing dynamic covalent chemical modifications (or epitranscriptomic marks) in plants has provided fresh insight into the underlying molecular mechanisms of gene expression regulation. Comparatively, epigenetic marks comprising heritable modifications of DNA and histones have been extensively studied in plants and their impact on plant gene expression is quite established. Based on our growing knowledge of the plant epitranscriptome and epigenome, it is logical to explore how the two regulatory layers intermingle to intricately determine gene expression levels underlying key biological processes such as development and response to stress. Herein, we focus on the emerging evidence of crosstalk between the plant epitranscriptome with epigenetic regulation involving DNA modification, histone modification, and non-coding RNAs.

Plant DNA Methylation: An Epigenetic Mark in Development, Environmental Interactions, and Evolution.

DNA methylation is an epigenetic modification of the genome involved in the regulation of gene expression and modulation of chromatin structure. Plant genomes are widely methylated, and the methylation generally occurs on the cytosine bases through the activity of specific enzymes called DNA methyltransferases. On the other hand, methylated DNA can also undergo demethylation through the action of demethylases. The methylation landscape is finely tuned and assumes a pivotal role in plant development and evolution. This review illustrates different molecular aspects of DNA methylation and some plant physiological processes influenced by this epigenetic modification in model species, crops, and ornamental plants such as orchids. In addition, this review aims to describe the relationship between the changes in plant DNA methylation levels and the response to biotic and abiotic stress. Finally, we discuss the possible evolutionary implications and biotechnological applications of DNA methylation.

DNA Methylation in Plant Responses and Adaption to Abiotic Stresses.

Due to their sessile state, plants are inevitably affected by and respond to the external environment. So far, plants have developed multiple adaptation and regulation strategies to abiotic stresses. One such system is epigenetic regulation, among which DNA methylation is one of the earliest and most studied regulatory mechanisms, which can regulate genome functioning and induce plant resistance and adaption to abiotic stresses. In this review, we outline the most recent findings on plant DNA methylation responses to drought, high temperature, cold, salt, and heavy metal stresses. In addition, we discuss stress memory regulated by DNA methylation, both in a transient way and the long-term memory that could pass to next generations. To sum up, the present review furnishes an updated account of DNA methylation in plant responses and adaptations to abiotic stresses.

Concerto on Chromatin: Interplays of Different Epigenetic Mechanisms in Plant Development and Environmental Adaptation.

Epigenetic mechanisms such as DNA methylation, histone post-translational modifications, chromatin remodeling, and noncoding RNAs, play important roles in regulating plant gene expression, which is involved in various biological processes including plant development and stress responses. Increasing evidence reveals that these different epigenetic mechanisms are highly interconnected, thereby contributing to the complexity of transcriptional reprogramming in plant development processes and responses to environmental stresses. Here, we provide an overview of recent advances in understanding the epigenetic regulation of plant gene expression and highlight the crosstalk among different epigenetic mechanisms in making plant developmental and stress-responsive decisions. Structural, physical, transcriptional and metabolic bases for these epigenetic interplays are discussed.

The EpiDiverse Plant Epigenome-Wide Association Studies (EWAS) Pipeline.

Bisulfite sequencing is a widely used technique for determining DNA methylation and its relationship with epigenetics, genetics, and environmental parameters. Various techniques were implemented for epigenome-wide association studies (EWAS) to reveal meaningful associations; however, there are only very few plant studies available to date. Here, we developed the EpiDiverse EWAS pipeline and tested it using two plant datasets, from P. abies (Norway spruce) and Q. lobata (valley oak). Hence, we present an EWAS implementation tested for non-model plant species and describe its use.

Epigenetics for Crop Improvement in Times of Global Change.

Epigenetics has emerged as an important research field for crop improvement under the on-going climatic changes. Heritable epigenetic changes can arise independently of DNA sequence alterations and have been associated with altered gene expression and transmitted phenotypic variation. By modulating plant development and physiological responses to environmental conditions, epigenetic diversity-naturally, genetically, chemically, or environmentally induced-can help optimise crop traits in an era challenged by global climate change. Beyond DNA sequence variation, the epigenetic modifications may contribute to breeding by providing useful markers and allowing the use of epigenome diversity to predict plant performance and increase final crop production. Given the difficulties in transferring the knowledge of the epigenetic mechanisms from model plants to crops, various strategies have emerged. Among those strategies are modelling frameworks dedicated to predicting epigenetically controlled-adaptive traits, the use of epigenetics for in vitro regeneration to accelerate crop breeding, and changes of specific epigenetic marks that modulate gene expression of traits of interest. The key challenge that agriculture faces in the 21st century is to increase crop production by speeding up the breeding of resilient crop species. Therefore, epigenetics provides fundamental molecular information with potential direct applications in crop enhancement, tolerance, and adaptation within the context of climate change.

Plants' Epigenetic Mechanisms and Abiotic Stress.

Plants are sessile organisms that need to adapt to constantly changing environmental conditions. Unpredictable climate change places plants under a variety of abiotic stresses. Studying the regulation of stress-responsive genes can help to understand plants' ability to adapt to fluctuating environmental conditions. Changes in epigenetic marks such as histone modifications and DNA methylation are known to regulate gene expression by their dynamic variation in response to stimuli. This can then affect their phenotypic plasticity, which helps with the adaptation of plants to adverse conditions. Epigenetic marks may also provide a mechanistic basis for stress memory, which enables plants to respond more effectively and efficiently to recurring stress and prepare offspring for potential future stresses. Studying epigenetic changes in addition to genetic factors is important to better understand the molecular mechanisms underlying plant stress responses. This review summarizes the epigenetic mechanisms behind plant responses to some main abiotic stresses.

Analysis of Plant DNA Methylation Profiles Using R.

DNA methylation is a transgenerational stable epigenetic modification able to regulate gene expression and genome stability. The analysis of DNA methylation by genome-wide bisulfite sequencing become the main genomic approach to study epigenetics in many organisms; leading to standardization of the alignment and methylation call procedures. However, subsequent steps of the computational analysis should be tailored to the biological questions and the organisms used. Since most bioinformatics tools designed for epigenetic studies are built using mammalian models, they are potentially unsuitable for organisms with substantially different epigenetic regulation, such as plants. Therefore, in this chapter we propose a computational workflow for the analysis, visualization, and interpretation of data obtained from alignment of whole genome bisulfite sequencing of plant samples. Using almost exclusively the R working environment we will examine in depth how to tackle some plant-related issues during epigenetic analysis.

Immunochemical Detection of Modified Species of Cytosine in Plant Tissues.

Methylated cytosine (5-methylcytosine) is the most studied epigenetic mark involved in the regulation of gene expression. Although it displays highly variable dynamics during plant ontogenesis, it is possible to gain a fine spatial perspective with immunohistochemistry techniques that use specific antibodies and fluorochromes. Besides, there are other cytosine modifications described in plants, although their biological significance is still unknown (i.e., 5-hydroxymethylcytosine, 5-formylcytosine and 5-carboxylcytosine). Here we present a standardized protocol to detect cytosine modifications in plant tissues.

Epigenetic Mechanisms of Plant Adaptation to Biotic and Abiotic Stresses.

Unlike animals, plants are immobile and could not actively escape the effects of aggressive environmental factors, such as pathogenic microorganisms, insect pests, parasitic plants, extreme temperatures, drought, and many others. To counteract these unfavorable encounters, plants have evolved very high phenotypic plasticity. In a rapidly changing environment, adaptive phenotypic changes often occur in time frames that are too short for the natural selection of adaptive mutations. Probably, some kind of epigenetic variability underlines environmental adaptation in these cases. Indeed, isogenic plants often have quite variable phenotypes in different habitats. There are examples of successful "invasions" of relatively small and genetically homogenous plant populations into entirely new habitats. The unique capability of quick environmental adaptation appears to be due to a high tendency to transmit epigenetic changes between plant generations. Multiple studies show that epigenetic memory serves as a mechanism of plant adaptation to a rapidly changing environment and, in particular, to aggressive biotic and abiotic stresses. In wild nature, this mechanism underlies, to a very significant extent, plant capability to live in different habitats and endure drastic environmental changes. In agriculture, a deep understanding of this mechanism could serve to elaborate more effective and safe approaches to plant protection.

Spontaneous epimutations in plants.

Contents Summary 1253 I. Introduction 1253 II. What is the rate and molecular spectrum of spontaneous epimutations? 1254 III. Do spontaneous epimutations have phenotypic consequences? 1257 IV. Conclusion and discussion 1258 Acknowledgements 1258 References 1258 SUMMARY: Heritable gains or losses of cytosine methylation can arise stochastically in plant genomes independently of DNA sequence changes. These so-called 'spontaneous epimutations' appear to be a byproduct of imperfect DNA methylation maintenance and epigenome reinforcement events that occur in specialized cell types. There is continued interest in the plant epigenetics community in trying to understand the broader implications of these stochastic events, as some have been shown to induce heritable gene expression changes, shape patterns of methylation diversity within and among plant populations, and appear to be responsive to multi-generational environmental stressors. In this paper we synthesized our current knowledge of the molecular basis and functional consequences of spontaneous epimutations in plants, discuss technical and conceptual challenges, and highlight emerging research directions.

Retrospective and perspective of plant epigenetics in China.

Epigenetics refers to the study of heritable changes in gene function that do not involve changes in the DNA sequence. Such effects on cellular and physiological phenotypic traits may result from external or environmental factors or be part of normal developmental program. In eukaryotes, DNA wraps on a histone octamer (two copies of H2A, H2B, H3 and H4) to form nucleosome, the fundamental unit of chromatin. The structure of chromatin is subjected to a dynamic regulation through multiple epigenetic mechanisms, including DNA methylation, histone posttranslational modifications (PTMs), chromatin remodeling and noncoding RNAs. As conserved regulatory mechanisms in gene expression, epigenetic mechanisms participate in almost all the important biological processes ranging from basal development to environmental response. Importantly, all of the major epigenetic mechanisms in mammalians also occur in plants. Plant studies have provided numerous important contributions to the epigenetic research. For example, gene imprinting, a mechanism of parental allele-specific gene expression, was firstly observed in maize; evidence of paramutation, an epigenetic phenomenon that one allele acts in a single locus to induce a heritable change in the other allele, was firstly reported in maize and tomato. Moreover, some unique epigenetic mechanisms have been evolved in plants. For example, the 24-nt siRNA-involved RNA-directed DNA methylation (RdDM) pathway is plant-specific because of the involvements of two plant-specific DNA-dependent RNA polymerases, Pol IV and Pol V. A thorough study of epigenetic mechanisms is of great significance to improve crop agronomic traits and environmental adaptability. In this review, we make a brief summary of important progress achieved in plant epigenetics field in China over the past several decades and give a brief outlook on future research prospects. We focus our review on DNA methylation and histone PTMs, the two most important aspects of epigenetic mechanisms.

Regulation of genome-wide DNA methylation by mobile small RNAs.

Contents Summary 540 I. Introduction 540 II. There are different types of sRNA mobility 541 III. Mechanisms of sRNA movement 541 IV. Long-distance, shoot-root, mobile siRNAs influence DNA methylation in recipient tissues 541 V. Classes of interactions between shoot-root mobile siRNAs and DNA methylation 542 VI. Loci targeted directly and indirectly by shoot-root mobile siRNAs are associated with different histone modifications 543 VII. Is mobile siRNA-regulated DNA methylation important in specific tissues or under specific conditions? 543 VIII. Mobile sRNAs can be used to modify plant traits 544 IX. Conclusions 544 Acknowledgements 544 References 544 SUMMARY: RNA-directed DNA methylation (RdDM) at cytosine residues regulates gene expression, silences transposable elements and influences genome stability. The mechanisms responsible for RdDM are guided to target loci by small RNAs (sRNAs) that can move within plants cell to cell and long distance. Here we discuss recent advances in the understanding of interactions between mobile sRNAs and DNA methylation. We describe the mechanisms of sRNA movement, the differences between known classes of mobile sRNA-DNA methylation interactions and the limits of current knowledge. Finally, we discuss potential applications of mobile sRNAs in modifying plant traits.

The ISWI remodeler in plants: protein complexes, biochemical functions, and developmental roles.

Imitation Switch (ISWI) is a member of the ATP-dependent chromatin remodeling factor family, whose members move or restructure nucleosomes using energy derived from ATP hydrolysis. ISWI proteins are conserved in eukaryotes and usually form complexes with DDT (DNA-binding homeobox and different transcription factors)-domain proteins. Here, we review recent research on ISWI in the model plant Arabidopsis thaliana (AtISWI). AtISWI forms complexes with AtDDT-domain proteins, many of which have domain structures that differ from those of DDT-domain proteins in yeast and animals. This might suggest that plant ISWI complexes have unique roles. In vivo studies have shown that AtISWI is involved in the formation of the evenly spaced pattern of nucleosome arrangement in gene bodies-this pattern is associated with high transcriptional levels of genes. In addition, AtISWI and the AtDDT-domain protein RINGLET (RLT) are involved in many developmental processes in A. thaliana, including meristem fate transition and organ formation. Studies on the functions of AtISWI may shed light on how chromatin remodeling functions in plants and also provide new information about the evolution of ISWI remodeling complexes in eukaryotes.

Functions of plants long non-coding RNAs.

Long non-coding RNAs (lncRNAs) have been emerged as important players for various biological pathways, including dosage compensation, genomic imprinting, chromatin regulation, alternative splicing and nuclear organization. A large number of lncRNAs had already been identified by different approaches in plants, while the functions of only a few of them have been investigated. This review will summarize our current understanding of a wide range of plant lncRNAs functions, and highlight their roles in the regulation of diverse pathways in plants. This article is part of a Special Issue entitled: Clues to long noncoding RNA taxonomy1, edited by Dr. Tetsuro Hirose and Dr. Shinichi Nakagawa.

A dynamic architecture of life.

In recent decades, a profound conceptual transformation has occurred comprising different areas of biological research, leading to a novel understanding of life processes as much more dynamic and changeable. Discoveries in plants and animals, as well as novel experimental approaches, have prompted the research community to reconsider established concepts and paradigms. This development was taken as an incentive to organise a workshop in May 2014 at the Academia Nazionale dei Lincei in Rome. There, experts on epigenetics, regeneration, neuroplasticity, and computational biology, using different animal and plant models, presented their insights on important aspects of a dynamic architecture of life, which comprises all organisational levels of the organism. Their work demonstrates that a dynamic nature of life persists during the entire existence of the organism and permits animals and plants not only to fine-tune their response to particular environmental demands during development, but underlies their continuous capacity to do so. Here, a synthesis of the different findings and their relevance for biological thinking is presented.

Chemical probes in plant epigenetics studies.

Transcription potential is determined by the accessibility of DNA sequences within the context of chromatin, which is coordinately controlled by various epigenetic modifications. Chemical inhibition of epigenetic regulators provides a quick and effective approach to investigate the roles of epigenetic modifications in controlling many biological processes, especially for species in which genetic information is limited. This mini-review provides a brief overview of epigenetic regulators in the model organism Arabidopsis thaliana and summarizes compounds that have been applied in plant epigenetics studies, with highlights in the applications of these chemical probes in mechanistic and functional investigations.