Molecular epigenetic mechanisms for memory of temperature stresses in plants (2022)

Table of Contents
Journal of Genetics and Genomics ABSTRACT Section snippets INTRODUCTION Epigenetic regulation of ‘memory of winter cold’ Thermomemory to overcome recurring heat stress Perspectives Declaration of Competing Interest Acknowledgements References (106) Plant Sci Mol. Plant Cell Biochim. Biophys. Acta. Mol. Cell Mol. Plant Mol. Cell Plant Sci Gene Plant Commun Curr. Opin. Plant Biol. Mol. Cell Heat stress effects on source–sink relationships and metabolome dynamics in wheat J. Exp. Bot. Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment Proc. Natl. Acad. Sci. U S A The genetic basis of flowering responses to seasonal cues Nat. Rev. Genet. A Polycomb-based switch underlying quantitative epigenetic memory Nature Preparing plants for improved cold tolerance by priming Plant Cell Environ The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis Plant Physiol The molecular principles of gene regulation by Polycomb repressive complexes Nat. Rev. Mol. Cell Biol. Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin Nat. Cell Biol. Winter memory throughout the plant kingdom: different paths to flowering Plant Physiol BRUSHY1/TONSOKU/MGOUN3 is required for heat stress memory Plant Cell Environ Arabidopsis FORGETTER1 mediates stress-induced chromatin memory through nucleosome remodeling Elife Transcription-dependence of histone H3 lysine 27 trimethylation at the Arabidopsis Polycomb target gene FLC Plant J A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis Plant Physiol Arabidopsis HSA32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation Plant Physiol Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering PLoS Genet HSI2/VAL1 silences AGL15 to regulate the developmental transition from seed maturation to vegetative growth in Arabidopsis Plant Cell The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors Plant Cell Abscisic acid: Emergence of a core signaling network Annu. Rev. Plant Biol. A PHD-Polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization Proc. Natl. Acad. Sci. U S A Expression of vernalization responsive genes in wheat is associated with histone H3 trimethylation Mol. Genet. Genomics Genome-wide mapping of alternative splicing in Arabidopsis thaliana Genome Res The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor Plant Cell Chromatin-based mechanisms of temperature memory in plants Plant Cell Environ Heteromeric HSFA2/HSFA3 complexes drive transcriptional memory after heat stress in Arabidopsis Nat. Commun. The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals Ann. Bot. The chloroplast small heat shock protein undergoes oxidation-dependent conformational changes and may protect plants from oxidative stress Cell Stress Chaperones PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis Genes Dev Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA Science Cytosol-localized heat shock factor-binding protein, AtHSBP, functions as a negative regulator of heat shock response by translocation to the nucleus and is required for seed development in Arabidopsis Plant Physiol DNA replication-coupled histone modification maintains Polycomb gene silencing in plants Science Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development PLoS Genet Central role of the LEAFY COTYLEDON1 transcription factor in seed development J. Integr. Plant Biol. Comprehensive hormone profiling in developing Arabidopsis seeds: Examination of the site of ABA biosynthesis, ABA transport and hormone interactions Plant Cell Physiol The two clock proteins CCA1 and LHY activate VIN3 transcription during vernalization through the vernalization-responsive cis-element Plant Cell A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory Embo J Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance Plant Physiol Concerted genomic targeting of H3K27 demethylase REF6 and chromatin-remodeling ATPase BRM in Arabidopsis Nat. Genet. Cited by (0) Recommended articles (6) FAQs Videos
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Journal of Genetics and Genomics

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ABSTRACT

The sessile plants encounter various stresses; some are prolonged, whereas some others are recurrent. Temperature is crucial for plant growth and development, and plants often encounter adverse high temperature fluctuations (heat stresses) as well as prolonged cold exposure such as seasonal temperature drops in winter when grown in temperate regions. Many plants can remember past temperature stresses to get adapted to adverse local temperature changes to ensure survival and/or reproductive success. Here, we summarize chromatin-based mechanisms underlying acquired thermotolerance or thermomemory in plants and review recent progresses on molecular epigenetic understanding of ‘remembering of prolonged cold in winter’ or vernalization, a process critical for various over-wintering plants to acquire competence to flower in the coming spring. In addition, perspectives on future study in temperature stress memories of economically-important crops are discussed.

Section snippets

INTRODUCTION

Plant growth and development is greatly affected by temperature, and adverse temperature stresses including cold and heat are major challenges for crop production under global climate change (Pandey et al., 2021; Perrella et al., 2022). The sessile plants have evolved a set of delicate physiological and molecular mechanisms to effectively deal with the prolonged and recurring temperatre stresses (Zhu, 2016; Oberkofler et al., 2021). In response to fluctuating local temperatures, prior exposure

Epigenetic regulation of ‘memory of winter cold’

Many over-wintering plants can ‘remember’ past winter cold experience to acquire competence to flower in the coming spring (Bouche et al., 2017; Luo and He, 2020). Generally, chromatin-based mechanisms underly the epigenetic ‘memory of winter cold’ in the warmth in diverse plants, but different epigenetic players and chromatin modifications are involved in discrete plant groups (Bouche et al., 2017; Luo and He, 2020). ‘Memory of winter cold’ has been extensively studied in the model crucifer

Thermomemory to overcome recurring heat stress

In addtion to adaption to prolonged cold through vernalization, many plants are able to acclimate to adverse high temeperatures, and an exposure to a short-term heat stress (HS) primes plants to acquire thermotolerance or improved response to recurring severe HS events. Generally, acquired theromotolerance (AT) or HS memory is a form of somatic stress memory and often lasts for a few days in Arabidopsis and other plants (Oberkofler et al., 2021; Perrella et al., 2022). HS memory is regulated

Perspectives

Plant environmental memories depend on the maintenance of the expression states of regulatory genes induced by environmental signals (stresses). Both acquisition and subsequent maintenance of ‘memory of winter cold’ and HS memory require chromatin modifications at regulatory loci, and maintenance of active or repressed chromatin state in the absence of cold or heat underlies memory of past temperature experience (Luo and He, 2020; Perrella et al., 2022). It becomes evident that chromatin-based

Declaration of Competing Interest

The authors declare no competing interests.

Acknowledgements

Research in the He laboratory is supported partly by the National Natural Science Foundation of China (grant nos. 31830049, 31721001 and 31970327) and State Key Laboratory of Protein and Plant Gene Research.

(Video) What is epigenetics? - Carlos Guerrero-Bosagna

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    FAQs

    Which mechanism of epigenetics is involved under stress condition of crop? ›

    Two classes of non-coding RNA; miRNA and siRNA are reported to be often actively involved in the epigenetic modifications when plants are exposed to stress conditions (Chinnusamy and Zhu 2009).

    How do epigenetics work? ›

    Epigenetics allows the muscle cell to turn “on” genes to make proteins important for its job and turn “off” genes important for a nerve cell's job. Your epigenetics change throughout your life. Your epigenetics at birth is not the same as your epigenetics during childhood or adulthood.

    Why is epigenetics important? ›

    The epigenetic apparatus is essential for controlling normal development and homeostasis, and also provides a means for the organism to integrate and react upon environmental cues.

    What is epigenetic regulation? ›

    Epigenetic regulation of a gene is the process by which the activity of a particular gene is controlled by the structure of nearby chromatin.

    What are epigenetic changes in plants? ›

    Plant epigenetic changes include DNA methylation and histone modification. Non-coding RNA activity has also been shown to play an important role in regulating translation and transcription.

    Is DNA methylated? ›

    In mammals, DNA methylation occurs at cytosines in any context of the genome. However, more than 98% of DNA methylation occurs in a CpG dinucleotide context in somatic cells, while as much as a quarter of all methylation appears in a non-CpG context in embryonic stem cells (ESCs).

    What are the three major epigenetic mechanisms? ›

    Cellular
    • Epigenetic mechanisms form a layer of control within a cell that regulates gene expression and silencing. ...
    • Three different epigenetic mechanisms have been identified: DNA methylation, histone modification, and non-coding RNA (ncRNA)-associated gene silencing.
    8 Aug 2022

    What is an example of epigenetic? ›

    Examples of epigenetics

    Epigenetic changes alter the physical structure of DNA. One example of an epigenetic change is DNA methylation — the addition of a methyl group, or a "chemical cap," to part of the DNA molecule, which prevents certain genes from being expressed. Another example is histone modification.

    What are three factors that affect epigenetics? ›

    Several lifestyle factors have been identified that might modify epigenetic patterns, such as diet, obesity, physical activity, tobacco smoking, alcohol consumption, environmental pollutants, psychological stress, and working on night shifts.

    How many epigenetic mechanisms are there? ›

    Three classes of epigenetic regulation exist: DNA methylation, histone modification, and noncoding RNA action.

    Who defined epigenetics? ›

    Conrad Waddington introduced the term epigenetics in the early 1940s. He defined epigenetics as ''the branch of biology which studies the causal interactions between genes and their products which bring the phenotype into being.

    What factors influence your epigenome? ›

    Epigenetic marks can be affected by exposure to metals, air pollution, benzene, organic pollutants, and electromagnetic radiation [98]. Chemical and xenobiotic compounds in water or the atmosphere are other potential environmental stressors capable of changing epigenetic status.

    How do you measure epigenetics? ›

    Key Epigenetic Analysis Techniques
    1. DNA Methylation Analysis. Investigate methylation patterns quantitatively across the genome using sequencing- and array-based techniques. ...
    2. DNA–Protein Interaction Analysis. Gain insight into protein–DNA interactions. ...
    3. Chromatin Accessibility Analysis.

    How are epigenetic factors measured? ›

    The DNA is assayed with sequencing (ChIP-Seq) or microarray (ChIP-Chip) technologies to determine the nucleotide sequence where the protein was bound. Any modification to histone proteins can be examined with ChIP as long as an antibody is available.

    Which is not an example of an epigenetic process? ›

    Answer and Explanation: Epigenetics is the study of heritable changes in DNA that do not include changes in the sequence. Therefore, (b) the inheritance of a single nucleotide mutation in the DNA would not be an example of epigenetic inheritance, as it is a change in a base pair in the DNA sequence.

    What is the evidence for epigenetic inheritance in plants? ›

    Methylation of DNA is one of the most extensively studied mechanisms of epigenetic inheritance. Studies in plants were one of the first to identify the heritable nature of DNA methylation. Plants lack a clear separation between soma and germ cells early in development, unlike most animal phyla.

    What is the relationship between methylation and genomic imprinting? ›

    In genomic imprinting, several epigenetic processes are involved to result in a unique epigenetic signature observed at a subset of loci in the genome [1, 2]. DNA methylation is the mainstay of establishing imprinting marks on either paternal or maternal alleles.

    What is the relationship between linked genes and syntenic genes? ›

    Syntenic genes are genes that are physically located on the same chromosome, whether or not the genes themselves exhibit linkage (Passarge et al., 1999). Therefore, all linked genes are syntenic, but not all syntenic genes show genetic linkage.

    Where is epigenome located? ›

    Within the complete set of DNA in a cell (genome), all of the modifications that regulate the activity (expression) of the genes is known as the epigenome.

    How do master regulatory genes function in cell differentiation? ›

    Answer and Explanation: Master regulatory genes function by affecting the expression of many target genes using their protein products.

    How are epigenetic changes inherited? ›

    Transgenerational epigenetic inheritance. According to the classical definition of transgenerational epigenetic inheritance, environmental triggers that hit pregnant female individuals (F0) can affect “directly” not only the first new generation (F1), but also its germ cells that represent the second generation (F2).

    What are the 2 common mechanisms of epigenetics? ›

    Thus, a precise understanding of epigenetic mechanisms, including DNA methylation and histone modification, is important for elucidating the pathogenic pathways involved in neurodevelopmental disorders.

    What are the main epigenetic mechanisms that interfere with the expression of genes? ›

    Regardless of the exact definition, the epigenetic processes that stably alter gene expression patterns (and/or transmit the alterations at cell division) are thought to include: (1) cytosine methylation; (2) post-translational modification of histone proteins and remodelling of chromatin; and (3) RNA-based mechanisms.

    Which of the following causes epigenetic modifications to DNA that affect gene expression without changing the DNA sequence? ›

    Epigenetic modifications refer to changes in the gene expression that are not caused by changes in the DNA sequences but are due to events like DNA methylations, histone modifications, miRNA expression modulation, etc.

    What is epigenetic cell memory? ›

    Epigenetic memory is an essential process of life that governs the inheritance of predestined functional characteristics of normal cells and the newly acquired properties of cells affected by cancer and other diseases from parental to progeny cells.

    What is the definition of epigenesis? ›

    1 : development of a plant or animal from an egg or spore through a series of processes in which unorganized cell masses differentiate into organs and organ systems also : the theory that plant and animal development proceeds in this way — compare preformation sense 2.

    What is epigenesis theory? ›

    preformation”. Epigenesis is, roughly, the thesis that every developing entity starts from material that is unformed, with form emerging gradually, over time, in the process of development.

    What is an example of epigenetics in psychology? ›

    Figure 4.11: Identical twins are the perfect example of epigenetics. Although they share exactly the same DNA, their unique experiences in life will cause some genes (and not others) to express themselves. This is why, over time, identical twins come to look and behave differently.

    What is epigenetics and how does it relate to psychology? ›

    Moreover, epigenetics in psychology provides a framework for understanding how the expression of genes is influenced by experiences and the environment to produce individual differences in behavior, cognition, personality, and mental health.

    What are three physiological systems processes that are responsible for epigenetic change? ›

    At least three systems including DNA methylation, histone modification and non-coding RNA (ncRNA)-associated gene silencing are currently considered to initiate and sustain epigenetic change.

    What are the molecular mechanisms of epigenetics? ›

    The definition of epigenetics and its specific mechanisms including DNA methylation and gene imprinting, modifications of nucleosomal histones associated with silencing or activation of gene transcription, RNA interference, chromosomal silencing, and the role of mobile elements are discussed.

    Which of the following is an example of an epigenetic mechanism? ›

    Epigenetic mechanisms are important regulators of gene expression that establish potentially heritable changes in gene expression without altering the underlying nucleotide sequence. These mechanisms include CpG methylation, chromatin remodeling, and regulatory ncRNAs.

    Which of the following is an example of epigenetic inheritance quizlet? ›

    Dosage compensation is not required for all X linked genes in mammals. Genomic imprinting is an example of epigenetic inheritance.

    Does epigenetics change DNA? ›

    The word “epigenetic” literally means “in addition to changes in genetic sequence.” The term has evolved to include any process that alters gene activity without changing the DNA sequence, and leads to modifications that can be transmitted to daughter cells (although experiments show that some epigenetic changes can be ...

    Is epigenetics a branch of science? ›

    The answer is epigenetics, a rapidly growing area of science that focuses on the processes that help direct when individual genes are turned on or off. While the cell's DNA provides the instruction manual, genes also need specific instructions.

    How long do epigenetic changes last? ›

    These epigenetic changes are thus the basis for changes in the endometrial morphology like regeneration (1–7 days), proliferation (7–14 days), ovulation (13–17 days), differentiation (15–22 days), degradation (22–28 days) during the proliferative phase and secretory phase.

    When was epigenetics discovered? ›

    Abstract. The term "epigenetics" was introduced in 1942 by embryologist Conrad Waddington, who, relating it to the 17th century concept of "epigenesis", defined it as the complex of developmental processes between the genotype and phenotype.

    What is the difference between gene environment interaction and epigenetics? ›

    Unlike genetic changes, epigenetic changes are more dynamic and are often reversible, depending on the existence or removal of the inducing factors. Gene-environment interactions can alter gene activities and lead to cascades of cellular events to facilitate the adaptation of an individual cell to its environment.

    How do you study epigenetic modifications? ›

    1. DNA Methylation Analysis.
    2. Bisulfite Conversion. DNA methylation can be detected using several different approaches. ...
    3. High Resolution Melt Analysis. ...
    4. Methylated DNA Immunoprecipitation. ...
    5. Analysis of DNA/Protein Interactions.
    6. Chromatin Accessibility and Conformation Assays.
    7. Chromatin accessibility. ...
    8. EpiQ™ Chromatin Analysis Kit.

    How do epigenetic changes occur? ›

    Environmental influences, such as a person's diet and exposure to pollutants, can impact the epigenome. Epigenetic modifications can be maintained from cell to cell as cells divide and, in some cases, can be inherited through the generations. A common type of epigenetic modification is called DNA methylation.

    How does epigenetics affect human behavior? ›

    Epigenetic mechanisms are molecular events that govern the way the environment regulates the genomes of organisms. Epigenetic processes lead to individual differences in appearance, physiology, cognition, and behavior—the group of traits known as the phenotype.

    How does epigenetics control gene expression? ›

    Epigenetic mechanisms constrain expression by adapting regions of the genome to maintain either gene silencing or gene activity. This is achieved through direct chemical modification of the DNA region itself and by modification of proteins that are closely associated with the locus.

    How are epigenetics inherited? ›

    Epigenetic inheritance is an unconventional finding. It goes against the idea that inheritance happens only through the DNA code that passes from parent to offspring. It means that a parent's experiences, in the form of epigenetic tags, can be passed down to future generations.

    How many epigenetic mechanisms are there? ›

    Three classes of epigenetic regulation exist: DNA methylation, histone modification, and noncoding RNA action.

    What is an example of epigenetics in psychology? ›

    Figure 4.11: Identical twins are the perfect example of epigenetics. Although they share exactly the same DNA, their unique experiences in life will cause some genes (and not others) to express themselves. This is why, over time, identical twins come to look and behave differently.

    Which is not an example of an epigenetic process? ›

    Answer and Explanation: Epigenetics is the study of heritable changes in DNA that do not include changes in the sequence. Therefore, (b) the inheritance of a single nucleotide mutation in the DNA would not be an example of epigenetic inheritance, as it is a change in a base pair in the DNA sequence.

    What is the role of epigenetics in evolution? ›

    Finally, epigenetic processes, particularly DNA methylation, contribute directly to DNA sequence evolution, because they act as mutagens on the one hand and modulate genome stability on the other by keeping transposable elements in check.

    What are examples of epigenetic inheritance? ›

    However, a few examples of epigenetic inheritance in humans have also been reported, in particular, examples of the impact of stress as a possible transgenerational risk factor for depression, or the effect of diet on the risk for cardiovascular diseases and diabetes across generations, and multigenerational effects of ...

    Which of the following is an example of epigenetic inheritance? ›

    Histone methylation patterns, however, are not contained within the DNA. This heritable information has various effects on gene expression that is not due to the sequence of DNA, thus making it an example of epigenetic inheritance.

    Where does epigenetic regulation occur? ›

    Epigenetic modifications, such as histone acetylation, occur at the amino terminal tails of the histones that protrude from the nucleosomes. Acetylation of histones is generally acknowledged to play a key role in the regulation of gene expression.

    Which of the following is an epigenetic modification? ›

    Rather, epigenetic modifications, or “tags,” such as DNA methylation and histone modification, alter DNA accessibility and chromatin structure, thereby regulating patterns of gene expression. These processes are crucial to normal development and differentiation of distinct cell lineages in the adult organism.

    What is the mechanism of gene regulation? ›

    Gene regulation is the process used to control the timing, location and amount in which genes are expressed. The process can be complicated and is carried out by a variety of mechanisms, including through regulatory proteins and chemical modification of DNA.

    What are the two types of epigenetic inheritance patterns? ›

    Epigenetic variation within multicellular organisms is either endogenous or exogenous. Endogenous is generated by cell–cell signaling (e.g. during cell differentiation early in development), while exogenous is a cellular response to environmental cues.

    What is epigenetic cell memory? ›

    Epigenetic memory is an essential process of life that governs the inheritance of predestined functional characteristics of normal cells and the newly acquired properties of cells affected by cancer and other diseases from parental to progeny cells.

    How long do epigenetic changes last? ›

    These epigenetic changes are thus the basis for changes in the endometrial morphology like regeneration (1–7 days), proliferation (7–14 days), ovulation (13–17 days), differentiation (15–22 days), degradation (22–28 days) during the proliferative phase and secretory phase.

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