Plant Epigenetics Research Articles

Epigenetic responses of trees to environmental stress in the context of climate change.

In long-lived tree populations, when environmental change outpaces rates of evolutionary adaptation, plasticity in traits related to stress tolerance, dormancy, and dispersal may be vital for preventing extinction. While a population's genetic background partly determines its ability to adapt to a changing environment, so too do the many types of epigenetic modifications that occur within and among populations, which vary on timescales orders of magnitude faster than the emergence of new beneficial alleles. Consequently, phenotypic plasticity driven by epigenetic modification may be especially critical for sessile, long-lived organisms such as trees that must rely on this plasticity to keep pace with rapid anthropogenic environmental change. While studies have reported large effects of DNA methylation, histone modification, and non-coding RNAs on the expression of stress-tolerance genes and resulting phenotypic responses, little is known about the role of these effects in non-model plants and particularly in trees. Here, we review new findings in plant epigenetics with particular relevance to the ability of trees to adapt to or escape stressors associated with rapid climate change. Such findings include specific epigenetic influences over drought, heat, and salinity tolerance, as well as dormancy and dispersal traits. We also highlight promising findings concerning transgenerational inheritance of an epigenetic 'stress memory' in plants. As epigenetic information is becoming increasingly easy to obtain, we close by outlining ways in which ecologists can use epigenetic information better to inform population management and forecasting efforts. Understanding the molecular mechanisms behind phenotypic plasticity and stress memory in tree species offers a promising path towards a mechanistic understanding of trees' responses to climate change.

Unveiling the epigenetic landscape of plants using flow cytometry approach.

Plants are sessile creatures that have to adapt constantly changing environmental circumstances. Plants are subjected to a range of abiotic stressors as a result of unpredictable climate change. Understanding how stress-responsive genes are regulated can help us better understand how plants can adapt to changing environmental conditions. Epigenetic markers that dynamically change in response to stimuli, such as DNA methylation and histone modifications are known to regulate gene expression. Individual cells or particles' physical and/or chemical properties can be measured using the method known as flow cytometry. It may therefore be used to evaluate changes in DNA methylation, histone modifications, and other epigenetic markers, making it a potent tool for researching epigenetics in plants. We explore the use of flow cytometry as a technique for examining epigenetic traits in this thorough discussion. The separation of cell nuclei and their subsequent labeling with fluorescent antibodies, offering information on the epigenetic mechanisms in plants when utilizing flow cytometry. We also go through the use of high-throughput data analysis methods to unravel the complex epigenetic processes occurring inside plant systems.

Epigenomics: a new tool for the generation of climate resilient grapevines

Climate change is expected to increase the occurrence of extreme environmental conditions. Viticulture, as agriculture in general, is highly dependent on climatic conditions, not only for yield but also for fruit quality, which is the most important factor affecting produce value at the farm-gate. This demands the development of novel plant breeding techniques that will lead to the accelerated production of more resilient grape varieties, as conventional breeding programs for perennials are often prolonged. Recent research has suggested that environmental conditions can activate a memory of stress that could result in a primed response to subsequent stress events. This is a process capable of increasing plant’s resilience to abiotic stimuli, allowing plants to better adapt to extreme environmental conditions. While the effect of priming has been observed in many plants, the underlying mechanisms are puzzling and seldom studied in perennial crops. A large body of research has been developed in the last decade linking response to stress, stress priming, and memory of stress with epigenetic mechanisms. This understanding of plant epigenetics has opened the door to the application of epigenetics to crop improvement, such as the use of epigenetic breeding for the generation of more resilient crops. Perennial crop agriculture in general, and viticulture in particular, would benefit from more in-depth knowledge on epigenetic memory of stress.

A review of plant epigenetics through the lens of almond.

While genomes were originally seen as static entities that stably held and organized genetic information, recent advances in sequencing have uncovered the dynamic nature of the genome. New conceptualizations of the genome include complex relationships between the environment and gene expression that must be maintained, regulated, and sometimes even transmitted over generations. The discovery of epigenetic mechanisms has allowed researchers to understand how traits like phenology, plasticity, and fitness can be altered without changing the underlying deoxyribonucleic acid sequence. While many discoveries were first made in animal systems, plants provide a particularly complex set of epigenetic mechanisms due to unique aspects of their biology and interactions with human selective breeding and cultivation. In the plant kingdom, annual plants have received the most attention; however, perennial plants endure and respond to their environment and human management in distinct ways. Perennials include crops such as almond, for which epigenetic effects have long been linked to phenomena and even considered relevant for breeding. Recent discoveries have elucidated epigenetic phenomena that influence traits such as dormancy and self-compatibility, as well as disorders like noninfectious bud failure, which are known to be triggered by the environment and influenced by inherent aspects of the plant. Thus, epigenetics represents fertile ground to further understand almond biology and production and optimize its breeding. Here, we provide our current understanding of epigenetic regulation in plants and use almond as an example of how advances in epigenetics research can be used to understand biological fitness and agricultural performance in crop plants.

Uncovering plant epigenetics: new insights into cytosine methylation in rye genomes.

This article comments on: Kalinka A, Starczak M, Gackowski D, Stępień E, Achrem M. 2023. Global DNA 5-hydroxymethylcytosine level and its chromosomal distribution in four rye species. Journal of Experimental Botany 74, 3488–3502.

EpiCass and CassavaNet4Dev Advanced Bioinformatics Workshop

EpiCass and CassavaNet4Dev are collaborative projects funded by the Swedish Research Council between the Swedish University of Agriculture (SLU) and the International Institute of Tropical Agriculture (IITA). The projects aim to investigate the influence of epigenetic changes on agricultural traits such as yield and virus resistance while also providing African students and researchers with advanced bioinformatics training and opportunities to participate in big data analysis events. The first advanced bioinformatics training workshop took place from May 16th to May 18th, 2022, followed by an online mini-symposium titled "Epigenetics and crop improvement" on May 19th. The symposium featured international speakers covering a wide range of topics related to plant epigenetics, cassava viral diseases, and cassava breeding strategies. A new online and on-site teaching concept was developed for the three-day workshop to ensure maximum student participation across Western, Eastern, and Southern Africa. Initially planned in Nigeria, Kenya, Ethiopia, Tanzania, and Zambia, the workshop ultimately focused on Nigeria, Kenya, and Ethiopia due to a lack of qualified candidates in the other countries. Each classroom hosted 20 to 25 students, with at least one bioinformatician present for support. The classrooms were connected via video conferencing, whereas teachers located in different places in Africa and Europe joined the video stream to conduct teaching sessions. The workshop was divided into theoretical classes and hands-on sessions, where participants could run data analysis with support from online teachers and local bioinformaticians. To enable participants to run guided, CPU and RAM-intensive data analysis workflows and overcome local computing and internet access restrictions, a system of virtual machines (VMs) hosted in the cloud was developed. The teaching platform provided teaching and exercise materials to support the use of the VMs. Although some students could not run heavy data analysis workflows due to unforeseen restrictions in the cloud, these issues were solved. All participants had the opportunity to run the analysis steps independently in the cloud using the protocols hosted on the teaching platform.

Beyond the Primary Structure of Nucleic Acids: Potential Roles of Epigenetics and Noncanonical Structures in the Regulations of Plant Growth and Stress Responses.

Epigenetics deals with changes in gene expression that are not caused by modifications in the primary sequence of nucleic acids. These changes beyond primary structures of nucleic acids not only include DNA/RNA methylation, but also other reversible conversions, together with histone modifications or RNA interference. In addition, under particular conditions (such as specific ion concentrations or protein-induced stabilization), the right-handed double-stranded DNA helix (B-DNA) can form noncanonical structures commonly described as "non-B DNA" structures. These structures comprise, for example, cruciforms, i-motifs, triplexes, and G-quadruplexes. Their formation often leads to significant differences in replication and transcription rates. Noncanonical RNA structures have also been documented to play important roles in translation regulation and the biology of noncoding RNAs. In human and animal studies, the frequency and dynamics of noncanonical DNA and RNA structures are intensively investigated, especially in the field of cancer research and neurodegenerative diseases. In contrast, noncanonical DNA and RNA structures in plants have been on the fringes of interest for a long time and only a few studies deal with their formation, regulation, and physiological importance for plant stress responses. Herein, we present a review focused on the main fields of epigenetics in plants and their possible roles in stress responses and signaling, with special attention dedicated to noncanonical DNA and RNA structures.

Epigenetics for crop adaptation to climate change

Epigenetics for crop adaptation to climate change

Epigenetic variation: A major player in facilitating plant fitness under changing environmental conditions.

Recent research in plant epigenetics has increased our understanding of how epigenetic variability can contribute to adaptive phenotypic plasticity in natural populations. Studies show that environmental changes induce epigenetic switches either independently or in complementation with the genetic variation. Although most of the induced epigenetic variability gets reset between generations and is short-lived, some variation becomes transgenerational and results in heritable phenotypic traits. The short-term epigenetic responses provide the first tier of transient plasticity required for local adaptations while transgenerational epigenetic changes contribute to stress memory and help the plants respond better to recurring or long-term stresses. These transgenerational epigenetic variations translate into an additional tier of diversity which results in stable epialleles. In recent years, studies have been conducted on epigenetic variation in natural populations related to various biological processes, ecological factors, communities, and habitats. With the advent of advanced NGS-based technologies, epigenetic studies targeting plants in diverse environments have increased manifold to enhance our understanding of epigenetic responses to environmental stimuli in facilitating plant fitness. Taking all points together in a frame, the present review is a compilation of present-day knowledge and understanding of the role of epigenetics and its fitness benefits in diverse ecological systems in natural populations.

Unraveling the Epigenetic Landscape for Salt Tolerance in Plants

In every organism, the expression of genes is regulated in response to the changes in the surrounding environment. The study of epigenetics in plants is essential in view of the improvement of agricultural productivity. Epigenetic modifications can enhance crops’ yield and stress tolerance without making any alteration within their genomic sequences. The routes of epigenetic modifications include processes such as methylation of DNA, modifications of histone proteins, chromatin remodeling, and non-coding RNA-mediated regulation of genes. Genome-wide epigenetic profiles, coined as the epigenome, of several plants have been identified in recent years. In the scope of this review, we are going to discuss progress made in the field of plant epigenomics under the limelight of stress tolerance, especially saline conditions.

Systematic histone H4 replacement in Arabidopsis thaliana reveals a role for H4R17 in regulating flowering time.

Despite the broad array of roles for epigenetic mechanisms on regulating diverse processes in eukaryotes, no experimental system is currently available in plants for the direct assessment of histone function. In this work, we present the development of a genetic strategy in Arabidopsis (Arabidopsis thaliana) whereby modified histone H4 transgenes can completely replace the expression of endogenous histone H4 genes. Accordingly, we established a collection of plants expressing different H4 point mutants targeting residues that may be post-translationally modified in vivo. To demonstrate its utility, we screened this new H4 mutant collection to uncover substitutions in H4 that alter flowering time. We identified different mutations in the H4 tail (H4R17A) and the H4 globular domain (H4R36A, H4R39K, H4R39A, and H4K44A) that strongly accelerate the floral transition. Furthermore, we identified a conserved regulatory relationship between H4R17 and the ISWI chromatin remodeling complex in plants: As with other biological systems, H4R17 regulates nucleosome spacing via ISWI. Overall, this work provides a large set of H4 mutants to the plant epigenetics community that can be used to systematically assess histone H4 function in Arabidopsis and a roadmap to replicate this strategy for studying other histone proteins in plants.

Moving Beyond DNA Sequence to Improve Plant Stress Responses.

Plants offer a habitat for a range of interactions to occur among different stress factors. Epigenetics has become the most promising functional genomics tool, with huge potential for improving plant adaptation to biotic and abiotic stresses. Advances in plant molecular biology have dramatically changed our understanding of the molecular mechanisms that control these interactions, and plant epigenetics has attracted great interest in this context. Accumulating literature substantiates the crucial role of epigenetics in the diversity of plant responses that can be harnessed to accelerate the progress of crop improvement. However, harnessing epigenetics to its full potential will require a thorough understanding of the epigenetic modifications and assessing the functional relevance of these variants. The modern technologies of profiling and engineering plants at genome-wide scale provide new horizons to elucidate how epigenetic modifications occur in plants in response to stress conditions. This review summarizes recent progress on understanding the epigenetic regulation of plant stress responses, methods to detect genome-wide epigenetic modifications, and disentangling their contributions to plant phenotypes from other sources of variations. Key epigenetic mechanisms underlying stress memory are highlighted. Linking plant response with the patterns of epigenetic variations would help devise breeding strategies for improving crop performance under stressed scenarios.

Tracing Mobile DNAs: From Molecular to Population Scales.

Transposable elements (TEs, transposons) are mobile DNAs that are prevalent in most eukaryotic genomes. In plants, their mobility has vastly contributed to genetic diversity which is essential for adaptive changes and evolution of a species. Such mobile nature of transposon has been also actively exploited in plant science research by generating genetic mutants in non-model plant systems. On the other hand, transposon mobilization can bring about detrimental effects to host genomes and they are therefore mostly silenced by the epigenetic mechanisms. TEs have been studied as major silencing targets and acted a main feature in the remarkable growth of the plant epigenetics field. Despite the importance of transposon in plant biology and biotechnology, their mobilization and the underlying mechanisms are largely left unanswered. This is mainly because of the sequence repetitiveness of transposons, which makes their detection and analyses difficult and complicated. Recently, some attempts have been made to develop new experimental methods detecting active transposons and their mobilization behavior. These techniques reveal TE mobility in various levels, including the molecular, cellular, organismal and population scales. In this review, we will highlight the novel technical approaches in the study of mobile genetic elements and discuss how these techniques impacted on the advancement of transposon research and broadened our understanding of plant genome plasticity.

Effects of ploidy variation on DNA methylation and gene expression in Pear (Pyrus communis L.)

Polyploid plants of fruit trees are generally characterized by dwarf growth, larger organs, and strong resistance to disease. They are therefore of great value in fruit breeding. Plant epigenetics generally has the forms of DNA methylation, RNA interference, and histone modification. The mechanisms of phenotypic variation and the physiological characteristics of plant polyploids are closely related to epigenetics. However, there have been few studies examining the relationship between DNA methylation and polyploidization in perennial woody plants. In this study, we compared the DNA methylation of unconverted diploids (q2x-1), tetraploids (4x-1, 4x-2) and diploid reference (2x-1) by methylation-sensitive amplification polymorphism (MSAP). The total methylation level of q2x-1, 4x-1, and 4x-2 was higher than that of 2x-1. The total methylation level of q2x-1 was higher than that of 4x-1 and 4x-2. Compared with 2x-1, the methylation pattern was mainly maintenance of methylation in q2x-1, 4x-1, and 4x-2, but the trend of demethylation of q2x-1, 4x-1, and 4x-2 was greater than that of methylation. Compared with q2x-1, the methylation pattern in 4x-1 and 4x-2 is also mainly maintaining methylation, but the trend of demethylation in 4x-1 and 4x-2 is less than that of methylation. The results of BLAST homology comparison and expression verification showed that the ploidy change of plants may affect the expression of genes related to adenosine triphosphate binding, RNA binding, arginine biosynthesis, and cell shape regulation, as well as promoting the polarization growth of leaf epidermis, auxin mediation, and RNA modification by causing a change of DNA methylation. This study provides a theoretical basis for studying the molecular mechanisms of plant ploidy change from the perspective of epigenetics.

Paradoxes of Plant Epigenetics

Plants have a unique ability to adapt ontogenesis to changing environmental conditions and the influence of stress factors. This ability is based on the existence of two specific features of epigenetic regulation in plants, which seem to be mutually exclusive at first glance. On the one hand, plants are capable of partial epigenetic reprogramming of the genome, which can lead to adaptation of physiology and metabolism to changed environmental conditions as well as to changes in ontogenesis programs. On the other hand, plants can show amazing stability of epigenetic modifications and the ability to transmit them to vegetative and sexual generations. The combination of these inextricably linked epigenetic features not only ensures survival in the conditions of a sessile lifestyle but also underlies a surprisingly wide morphological diversity of plants, which can lead to the appearance of morphs within one population and the existence of interpopulation morphological differences. The review discusses the molecular genetic mechanisms that cause a paradoxical combination of the stability and lability properties of epigenetic modifications and underlie the polyvariance of ontogenesis. We also consider the existing approaches for studying the role of epigenetic regulation in the manifestation of polyvariance of ontogenesis and discuss their limitations and prospects.

Epigenetic modification for horticultural plant improvement comes of age

Our era has witnessed tremendous technique advances and mechanically epigenetic improvement in plant epigenetics, mainly including histone post-translational modifications (PTMs) and DNA methylation, which have been characterized as playing vital roles in development processes and plant response to environmental factors. Recently, chemical modifications on RNAs like 5-methylcytosine (m5C) and N6-methyladenosine (m6A) have been revealed as a new layer of epigenetic marks to regulate gene translation efficiency in model plant Arabidopsis thaliana and with later discovery of horticultural species like tomato (Solanum lycopersicum) and poplar (Populus trichocarpa). In model plants, these epigenetic modifications on DNA, RNA, and histone tails largely trigger innumerable studies on how epigenetic mechanisms are involved in gene regulation and biological functions. As an emerging research field in horticultural plants, epigenetic modifications have bloomed in fruit development and ripening, grafting, and bud dormancy. In this Review, we have demonstrated recent advances of high-throughput sequencing methods, summarized epigenetic enzymatic systems to install, remove and recognize epigenetic marks, discussed essential roles of epigenetic regulation, and proposed how innovative computation techniques like machine learning and deep learning are set to understanding epigenetic regulation mechanisms in horticultural plants. We also raise future perspectives on how epigenetic modifications act as new additions for understanding their roles in gene expression that is required for development and environmental adaptation in horticultural plants.

EpiDiverse Toolkit: a pipeline suite for the analysis of bisulfite sequencing data in ecological plant epigenetics.

The expanding scope and scale of next generation sequencing experiments in ecological plant epigenetics brings new challenges for computational analysis. Existing tools built for model data may not address the needs of users looking to apply these techniques to non-model species, particularly on a population or community level. Here we present a toolkit suitable for plant ecologists working with whole genome bisulfite sequencing; it includes pipelines for mapping, the calling of methylation values and differential methylation between groups, epigenome-wide association studies, and a novel implementation for both variant calling and discriminating between genetic and epigenetic variation.

A deep learning approach to automate whole-genome prediction of diverse epigenomic modifications in plants.

Epigenetic modifications function in gene transcription, RNA metabolism, and other biological processes. However, multiple factors currently limit the scientific utility of epigenomic datasets generated for plants. Here, using deep-learning approaches, we developed a Smart Model for Epigenetics in Plants (SMEP) to predict six types of epigenomic modifications: DNA 5-methylcytosine (5mC) and N6-methyladenosine (6mA) methylation, RNA N6-methyladenosine (m6 A) methylation, and three types of histone modification. Using the datasets from the japonica rice Nipponbare, SMEP achieved 95% prediction accuracy for 6mA, and also achieved around 80% for 5mC, m6 A, and the three types of histone modification based on the 10-fold cross-validation. Additionally, >95% of the 6mA peaks detected after a heat-shock treatment were predicted. We also successfully applied the SMEP for examining epigenomic modifications in indica rice 93-11 and even the B73 maize line. Taken together, we show that the deep-learning-enabled SMEP can reliably mine epigenomic datasets from diverse plants to yield actionable insights about epigenomic sites. Thus, our work opens new avenues for the application of predictive tools to facilitate functional research, and will almost certainly increase the efficiency of genome engineering efforts.

Epigenetics for Crop Improvement in Times of Global Change.

Simple SummaryResearch on plant epigenetics aims to understand how endogenous, biotic, and abiotic factors regulate plant development and growth independent of changes in the genome sequence. Often, the epigenetic changes are heritable across generations and modulate plant growth and crop tolerance, particularly in response to environmental stimuli. To take advantage of epigenetic adaptation, recent research has focused on implementing targeted epigenetic diversity to engineer plants that harbour advantageous traits for optimal crop production. Epigenetics has the potential to provide a powerful toolbox for crop breeders; however, most mechanistic studies are based on information from model plant species due to the challenges that arise when working with crops. Here, we summarise the contribution of epigenetics to optimising crop adaptation in response to climate change and overview potential future applications as well as challenges.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.

Deciphering the Epigenetic Alphabet Involved in Transgenerational Stress Memory in Crops.

Although epigenetic modifications have been intensely investigated over the last decade due to their role in crop adaptation to rapid climate change, it is unclear which epigenetic changes are heritable and therefore transmitted to their progeny. The identification of epigenetic marks that are transmitted to the next generations is of primary importance for their use in breeding and for the development of new cultivars with a broad-spectrum of tolerance/resistance to abiotic and biotic stresses. In this review, we discuss general aspects of plant responses to environmental stresses and provide an overview of recent findings on the role of transgenerational epigenetic modifications in crops. In addition, we take the opportunity to describe the aims of EPI-CATCH, an international COST action consortium composed by researchers from 28 countries. The aim of this COST action launched in 2020 is: (1) to define standardized pipelines and methods used in the study of epigenetic mechanisms in plants, (2) update, share, and exchange findings in epigenetic responses to environmental stresses in plants, (3) develop new concepts and frontiers in plant epigenetics and epigenomics, (4) enhance dissemination, communication, and transfer of knowledge in plant epigenetics and epigenomics.