Plant Responses to Heat Stress: Physiology, Transcription, Noncoding RNAs, and Epigenetics.
Zhao Jianguo,Lu Zhaogeng,Wang Li,Jin Biao
International journal of molecular sciences
Global warming has increased the frequency of extreme high temperature events. High temperature is a major abiotic stress that limits the growth and production of plants. Therefore, the plant response to heat stress (HS) has been a focus of research. However, the plant response to HS involves complex physiological traits and molecular or gene networks that are not fully understood. Here, we review recent progress in the physiological (photosynthesis, cell membrane thermostability, oxidative damage, and others), transcriptional, and post-transcriptional (noncoding RNAs) regulation of the plant response to HS. We also summarize advances in understanding of the epigenetic regulation (DNA methylation, histone modification, and chromatin remodeling) and epigenetic memory underlying plant-heat interactions. Finally, we discuss the challenges and opportunities of future research in the plant response to HS.
10.3390/ijms22010117
Plant Epigenetic Stress Memory Induced by Drought: A Physiological and Molecular Perspective.
Godwin James,Farrona Sara
Methods in molecular biology (Clifton, N.J.)
Drought stress is one of the most common stresses encountered by crops and other plants and leads to significant productivity losses. It commonly happens that drought stress occurs more than once during the plant's life cycle. Plants suffering from drought stress can adapt their life strategies to acclimate and survive in many different ways. Interestingly, some plants have evolved a stress response strategy referred to as stress memory which leads to an enhanced response the next time the stress is encountered. The acquisition of stress memory leads to a reprogrammed transcriptional response during subsequent stress and subsequent changes both at the physiological and molecular level. Recent advances in understanding chromatin dynamics have demonstrated the involvement of chromatin modifications, especially histone marks, associated with drought stress-responsive memory genes and subsequent enhanced transcriptional responses to repeated drought stress. In this chapter, we describe recent progress in this area and summarize techniques for the study of plant epigenetic responses to stress, including the roles of ABA and transcription factors in superinduced transcriptional activation during recurrent drought stress. We also review the possible use of seed priming to induce stress memory later in the plant life cycle. Finally, we discuss the potential implications of understanding the epigenetic mechanisms involved in plant stress memory for future applications in crop improvement and drought resistance.
10.1007/978-1-0716-0179-2_17
Exposome and Immunity Training: How Pathogen Exposure Order Influences Innate Immune Cell Lineage Commitment and Function.
Adams Kevin,Weber K Scott,Johnson Steven M
International journal of molecular sciences
Immune memory is a defining characteristic of adaptive immunity, but recent work has shown that the activation of innate immunity can also improve responsiveness in subsequent exposures. This has been coined "trained immunity" and diverges with the perception that the innate immune system is primitive, non-specific, and reacts to novel and recurrent antigen exposures similarly. The "exposome" is the cumulative exposures (diet, exercise, environmental exposure, vaccination, genetics, etc.) an individual has experienced and provides a mechanism for the establishment of immune training or immunotolerance. It is becoming increasingly clear that trained immunity constitutes a delicate balance between the dose, duration, and order of exposures. Upon innate stimuli, trained immunity or tolerance is shaped by epigenetic and metabolic changes that alter hematopoietic stem cell lineage commitment and responses to infection. Due to the immunomodulatory role of the exposome, understanding innate immune training is critical for understanding why some individuals exhibit protective phenotypes while closely related individuals may experience immunotolerant effects (e.g., the order of exposure can result in completely divergent immune responses). Research on the exposome and trained immunity may be leveraged to identify key factors for improving vaccination development, altering inflammatory disease development, and introducing potential new prophylactic treatments, especially for diseases such as COVID-19, which is currently a major health issue for the world. Furthermore, continued exposome research may prevent many deleterious effects caused by immunotolerance that frequently result in host morbidity or mortality.
10.3390/ijms21228462
Mitochondrial Stress Induces Plant Resistance Through Chromatin Changes.
Frontiers in plant science
Plants respond more efficiently when confronted with previous similar stress. In the case of pathogens, this memory of a previous infection confers resistance to future ones, which possesses a high potential for agricultural purposes. Some of the defense elements involved in this resistance phenotype, as well as epigenetic mechanisms participating in the maintenance of the memory, are currently known. However, the intracellular cascade from pathogen perception until the establishment of the epigenetic memory is still unexplored. Here, through the induction of mitochondrial stress by exogenous applications of Antimycin A in plants, we discovered and characterized a role of mitochondrial stress in plant-induced resistance. Mitochondrial stress-induced resistance (MS-IR) is effective locally, systemically, within generation and transgenerationally. Mechanistically, MS-IR seems to be mediated by priming of defense gene transcription caused by epigenetic changes. On one hand, we observed an increment in the deposition of H3K4me3 (a positive epigenetic mark) at the promoter region of the primed genes, and, on the other hand, the DNA (de)methylation machinery seems to be required for the transmission of MS-IR to the following generations. Finally, we observed that MS-IR is broad spectrum, restricting the colonization by pathogens from different kingdoms and lifestyles. Altogether, this evidence positions mitochondria as a prominent organelle in environment sensing, acting as an integrating platform to process external and internal signals, triggering the appropriate response, and inducing the epigenetic memory of the stress to better react against future stressful conditions.
10.3389/fpls.2021.704964
ROS and redox balance as multifaceted players of cross-tolerance: epigenetic and retrograde control of gene expression.
Locato Vittoria,Cimini Sara,De Gara Laura
Journal of experimental botany
Retrograde pathways occurring between chloroplasts, mitochondria, and the nucleus involve oxidative and antioxidative signals that, working in a synergistic or antagonistic mode, control the expression of specific patterns of genes following stress perception. Increasing evidence also underlines the relevance of mitochondrion-chloroplast-nucleus crosstalk in modulating the whole cellular redox metabolism by a controlled and integrated flux of information. Plants can maintain the acquired tolerance by a stress memory, also operating at the transgenerational level, via epigenetic and miRNA-based mechanisms controlling gene expression. Data discussed in this review strengthen the idea that ROS, redox signals, and shifts in cellular redox balance permeate the signalling network leading to cross-tolerance. The identification of specific ROS/antioxidative signatures leading a plant to different fates under stress is pivotal for identifying strategies to monitor and increase plant fitness in a changing environment. This review provides an update of the plant redox signalling network implicated in stress responses, in particular in cross-tolerance acquisition. The interplay between reactive oxygen species (ROS), ROS-derived signals, and antioxidative pathways is also discussed in terms of plant acclimation to stress in the short and long term.
10.1093/jxb/ery168
[Epigenetics and memory].
Gräff Johannes,Franklin Tamara B,Mansuy Isabelle M
Biologie aujourd'hui
The epigenetic marking of chromatin in the brain has recently been recognized as an essential mechanism for brain functions such as learning and memory formation. It allows nerve cells not only to respond to environmental stimuli and modulate their profile of gene expression, but also to establish and maintain their own identity. The epigenetic code is conferred by a set of covalent modifications on the basic elements of chromatin, DNA and histone proteins. These changes are catalyzed by specific enzymes and mechanisms, which include DNA methylation, and post-translational modifications of histone proteins such as acetylation, phosphorylation, methylation and ubiquitination. They are both stable and highly dynamic, and are triggered during stimulation of neuronal circuits but can also persist thereafter. Their study in animal models has demonstrated their importance, and revealed some of their modes of function.
10.1051/jbio/2010007
Mechanical stress acclimation in plants: Linking hormones and somatic memory to thigmomorphogenesis.
Plant, cell & environment
A single event of mechanical stimulation is perceived by mechanoreceptors that transduce rapid transient signalling to regulate gene expression. Prolonged mechanical stress for days to weeks culminates in cellular changes that strengthen the plant architecture leading to thigmomorphogenesis. The convergence of multiple signalling pathways regulates mechanically induced tolerance to numerous biotic and abiotic stresses. Emerging evidence showed prolonged mechanical stimulation can modify the baseline level of gene expression in naive tissues, heighten gene expression, and prime disease resistance upon a subsequent pathogen encounter. The phenotypes of thigmomorphogenesis can persist throughout growth without continued stimulation, revealing somatic-stress memory. Epigenetic processes regulate TOUCH gene expression and could program transcriptional memory in differentiating cells to program thigmomorphogenesis. We discuss the early perception, gene regulatory and phytohormone pathways that facilitate thigmomorphogenesis and mechanical stress acclimation in Arabidopsis and other plant species. We provide insights regarding: (1) the regulatory mechanisms induced by single or prolonged events of mechanical stress, (2) how mechanical stress confers transcriptional memory to induce cross-acclimation to future stress, and (3) why thigmomorphogenesis might resemble an epigenetic phenomenon. Deeper knowledge of how prolonged mechanical stimulation programs somatic memory and primes defence acclimation could transform solutions to improve agricultural sustainability in stressful environments.
10.1111/pce.14252
Joint memory.
Thierry B,Theraulaz G,Gautier J Y,Stiegler B
Behavioural processes
Joint memory is defined as the property of a social group in actualizing its own past transformations. It may result from the coupling of individual memories or be inscribed in the external environment. The concept of joint memory becomes heuristic when it subsumes an ensemble of social processes that are sufficiently integrated to be treated as an entity belonging to the real world. In social insects, colonies can perform action-perception loops which give rise to collective outcomes based on past experience; selective pressures could favour individual behavioural algorithms the combination of which provides a historical record organizing activities both in space and time. In contrast, social groups do not appear sufficiently autonomous in most vertebrates for joint memory be more than a way of seeing collective performances. However, in human beings, the development of external representations has made possible the growth of a socially distributed cognition; the accumulation of epigenetic events through cultural processes produces a set of material and symbolic products that feed back upon the conditions of evolution of the species.
10.1016/0376-6357(95)00039-9
Pivotal roles of environmental sensing and signaling mechanisms in plant responses to climate change.
Bigot Servane,Buges Julie,Gilly Lauriane,Jacques Cécile,Le Boulch Pauline,Berger Marie,Delcros Pauline,Domergue Jean-Baptiste,Koehl Astrid,Ley-Ngardigal Béra,Tran Van Canh Loup,Couée Ivan
Global change biology
Climate change reshapes the physiology and development of organisms through phenotypic plasticity, epigenetic modifications, and genetic adaptation. Under evolutionary pressures of the sessile lifestyle, plants possess efficient systems of phenotypic plasticity and acclimation to environmental conditions. Molecular analysis, especially through omics approaches, of these primary lines of environmental adjustment in the context of climate change has revealed the underlying biochemical and physiological mechanisms, thus characterizing the links between phenotypic plasticity and climate change responses. The efficiency of adaptive plasticity under climate change indeed depends on the realization of such biochemical and physiological mechanisms, but the importance of sensing and signaling mechanisms that can integrate perception of environmental cues and transduction into physiological responses is often overlooked. Recent progress opens the possibility of considering plant phenotypic plasticity and responses to climate change through the perspective of environmental sensing and signaling. This review aims to analyze present knowledge on plant sensing and signaling mechanisms and discuss how their structural and functional characteristics lead to resilience or hypersensitivity under conditions of climate change. Plant cells are endowed with arrays of environmental and stress sensors and with internal signals that act as molecular integrators of the multiple constraints of climate change, thus giving rise to potential mechanisms of climate change sensing. Moreover, mechanisms of stress-related information propagation lead to stress memory and acquired stress tolerance that could withstand different scenarios of modifications of stress frequency and intensity. However, optimal functioning of existing sensors, optimal integration of additive constraints and signals, or memory processes can be hampered by conflicting interferences between novel combinations and novel changes in intensity and duration of climate change-related factors. Analysis of these contrasted situations emphasizes the need for future research on the diversity and robustness of plant signaling mechanisms under climate change conditions.
10.1111/gcb.14433
Priming seeds for the future: Plant immune memory and application in crop protection.
Frontiers in plant science
Plants have evolved adaptive strategies to cope with pathogen infections that seriously threaten plant viability and crop productivity. Upon the perception of invading pathogens, the plant immune system is primed, establishing an immune memory that allows primed plants to respond more efficiently to the upcoming pathogen attacks. Physiological, transcriptional, metabolic, and epigenetic changes are induced during defense priming, which is essential to the establishment and maintenance of plant immune memory. As an environmental-friendly technique in crop protection, seed priming could effectively induce plant immune memory. In this review, we highlighted the recent advances in the establishment and maintenance mechanisms of plant defense priming and the immune memory associated, and discussed strategies and challenges in exploiting seed priming on crops to enhance disease resistance.
10.3389/fpls.2022.961840
Pleiotropy in the wild: the dormancy gene DOG1 exerts cascading control on life cycles.
Chiang George C K,Barua Deepak,Dittmar Emily,Kramer Elena M,de Casas Rafael Rubio,Donohue Kathleen
Evolution; international journal of organic evolution
In the wild, organismal life cycles occur within seasonal cycles, so shifts in the timing of developmental transitions can alter the seasonal environment experienced subsequently. Effects of genes that control the timing of prior developmental events can therefore be magnified in the wild because they determine seasonal conditions experienced by subsequent life stages, which can influence subsequent phenotypic expression. We examined such environmentally induced pleiotropy of developmental-timing genes in a field experiment with Arabidopsis thaliana. When studied in the field under natural seasonal variation, an A. thaliana seed-dormancy gene, Delay Of Germination 1 (DOG1), was found to influence not only germination, but also flowering time, overall life history, and fitness. Flowering time of the previous generation, in turn, imposed maternal effects that altered germination, the effects of DOG1 alleles, and the direction of natural selection on these alleles. Thus under natural conditions, germination genes act as flowering genes and potentially vice versa. These results illustrate how seasonal environmental variation can alter pleiotropic effects of developmental-timing genes, such that effects of genes that regulate prior life stages ramify to influence subsequent life stages. In this case, one gene acting at the seed stage impacted the entire life cycle.
10.1111/j.1558-5646.2012.01828.x
Maternal effects strengthen interactions of temperature and precipitation, determining seed germination of dominant alpine grass species.
Veselá Andrea,Hadincová Věroslava,Vandvik Vigdis,Münzbergová Zuzana
American journal of botany
PREMISE:Despite the existence of many studies on the responses of plant species to climate change, there is a knowledge gap on how specific climatic factors and their interactions regulate seed germination in alpine species. This understanding is complicated by the interplay between responses of seeds to the environment experienced during germination, the environment experienced by the maternal plant during seed development and genetic adaptations of the maternal plant to its environment of origin. METHODS:The study species (Anthoxanthum alpinum, A. odoratum) originated from localities with factorial combinations of temperature and precipitation. Seed germination was tested in conditions simulating the extreme ends of the current field conditions and a climate change scenario. We compared the performance of field-collected seeds with that of garden-collected seeds. RESULTS:A change to warmer and wetter conditions resulted in the highest germination of A. alpinum, while A. odoratum germinated the most in colder temperature and with home moisture. The maternal environment did have an impact on plant performance of the study species. Field-collected seeds of A. alpinum tolerated warmer conditions better than those from the experimental garden. CONCLUSIONS:The results demonstrate how knowledge of responses to climate change can increase our ability to understand and predict the fate of alpine species. Studies that aim to understand the germination requirements of seeds under future climates should use experimental designs allowing the separation of genetic differentiation, plasticity and maternal effects and their interactions, since all these mechanisms play an important role in driving species' germination patterns.
10.1002/ajb2.1657
Plant Transgenerational Epigenetics.
Quadrana Leandro,Colot Vincent
Annual review of genetics
Transgenerational epigenetics is defined in opposition to developmental epigenetics and implies an absence of resetting of epigenetic states between generations. Unlike mammals, plants appear to be particularly prone to this type of inheritance. In this review, we summarize our knowledge about transgenerational epigenetics in plants, which entails heritable changes in DNA methylation. We emphasize the role of transposable elements and other repeat sequences in the creation of epimutable alleles. We also argue that because reprogramming of DNA methylation across generations seems limited in plants, the inheritance of DNA methylation defects results from the failure to reinforce rather than reset this modification during sexual reproduction. We compare genome-wide assessments of heritable DNA methylation variation and its phenotypic impact in natural populations to those made using near-isogenic populations derived from crosses between parents with experimentally induced DNA methylation differences. Finally, we question the role of the environment in inducing transgenerational epigenetic variation and briefly present theoretical models under which epimutability is expected to be selected for.
10.1146/annurev-genet-120215-035254
Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations.
Frontiers in plant science
Plants respond to environmental conditions not only by plastic changes to their own development and physiology, but also by altering the phenotypes expressed by their offspring. This transgenerational plasticity was initially considered to entail only negative effects of stressful parental environments, such as production of smaller seeds by resource- or temperature-stressed parent plants, and was therefore viewed as environmental noise. Recent evolutionary ecology studies have shown that in some cases, these inherited environmental effects can include specific growth adjustments that are functionally adaptive to the parental conditions that induced them, which can range from contrasting states of controlled laboratory environments to the complex habitat variation encountered by natural plant populations. Preliminary findings suggest that adaptive transgenerational effects can be transmitted by means of diverse mechanisms including changes to seed provisioning and biochemistry, and epigenetic modifications such as DNA methylation that can persist across multiple generations. These non-genetically inherited adaptations can influence the ecological breadth and evolutionary dynamics of plant taxa and promote the spread of invasive plants. Interdisciplinary studies that join mechanistic and evolutionary ecology approaches will be an important source of future insights.
10.3389/fpls.2011.00102
DNA methylation mediates genetic variation for adaptive transgenerational plasticity.
Proceedings. Biological sciences
Environmental stresses experienced by individual parents can influence offspring phenotypes in ways that enhance survival under similar conditions. Although such adaptive transgenerational plasticity is well documented, its transmission mechanisms are generally unknown. One possible mechanism is environmentally induced DNA methylation changes. We tested this hypothesis in the annual plant Polygonum persicaria, a species known to express adaptive transgenerational plasticity in response to parental drought stress. Replicate plants of 12 genetic lines (sampled from natural populations) were grown in dry versus moist soil. Their offspring were exposed to the demethylating agent zebularine or to control conditions during germination and then grown in dry soil. Under control germination conditions, the offspring of drought-stressed parents grew longer root systems and attained greater biomass compared with offspring of well-watered parents of the same genetic lines. Demethylation removed these adaptive developmental effects of parental drought, but did not significantly alter phenotypic expression in offspring of well-watered parents. The effect of demethylation on the expression of the parental drought effect varied among genetic lines. Differential seed provisioning did not contribute to the effect of parental drought on offspring phenotypes. These results demonstrate that DNA methylation can mediate adaptive, genotype-specific effects of parental stress on offspring phenotypes.
10.1098/rspb.2016.0988
Adaptive transgenerational plasticity in an annual plant: grandparental and parental drought stress enhance performance of seedlings in dry soil.
Herman Jacob J,Sultan Sonia E,Horgan-Kobelski Tim,Riggs Charlotte
Integrative and comparative biology
Stressful parental (usually maternal) environments can dramatically influence expression of traits in offspring, in some cases resulting in phenotypes that are adaptive to the inducing stress. The ecological and evolutionary impact of such transgenerational plasticity depends on both its persistence across generations and its adaptive value. Few studies have examined both aspects of transgenerational plasticity within a given system. Here we report the results of a growth-chamber study of adaptive transgenerational plasticity across two generations, using the widespread annual plant Polygonum persicaria as a naturally evolved model system. We grew five inbred Polygonum genetic lines in controlled dry vs. moist soil environments for two generations in a fully factorial design, producing replicate individuals of each genetic line with all permutations of grandparental and parental environment. We then measured the effects of these two-generational stress histories on traits critical for functioning in dry soil, in a third (grandchild) generation of seedling offspring raised in the dry treatment. Both grandparental and parental moisture environment significantly influenced seedling development: seedlings of drought-stressed grandparents or parents produced longer root systems that extended deeper and faster into dry soil compared with seedlings of the same genetic lines whose grandparents and/or parents had been amply watered. Offspring of stressed individuals also grew to a greater biomass than offspring of nonstressed parents and grandparents. Importantly, the effects of drought were cumulative over the course of two generations: when both grandparents and parents were drought-stressed, offspring had the greatest provisioning, germinated earliest, and developed into the largest seedlings with the most extensive root systems. Along with these functionally appropriate developmental effects, seedlings produced after two previous drought-stressed generations had significantly greater survivorship in very dry soil than did seedlings with no history of drought. These findings show that plastic responses to naturalistic resource stresses experienced by grandparents and parents can "preadapt" offspring for functioning under the same stresses in ways that measurably influence realized fitness. Possible implications of these environmentally-induced, inherited adaptations are discussed with respect to ecological distribution, persistence under novel stresses, and evolution in natural populations.
10.1093/icb/ics041