The term priming is mostly used for biotic interactions (e.g., with herbivores or parasites), while the term acclimation is commonly used for abiotic stress events (e.g., heat or frost). They both denote the sensitivity and responsiveness to stress that results from a prior experience and often causes enhanced defense readiness. For simplicity, we will use the term 'priming' in this section for both biotic and abiotic stressors (Mauch-Mani et al. 2017). Priming is a robust defense because it has no or minimal fitness costs in terms of growth or reproduction, and often it is transient and only activated by a stimulus (Mauch-Mani et al. 2017).

‌Defense priming has been observed in a wide range of plant taxa, including wild species and model organisms. Notably, experimental evidence suggests that epigenetic changes were observed following priming. Several studies have hypothesized that epigenetic changes could influence the way how plants respond to biotic and abiotic stresses (Bruce et al. 2007; Mauch-Mani et al. 2017). The general idea is that an induced defense can associate molecular, biochemical, and physiological cues with stronger and/or activated phenotypic defense mechanisms in primed versus unprimed plants (Fig 2)(Bruce et al. 2007; Mauch-Mani et al. 2017). A possible response could be in the form of DNA hypo-hyper methylation (Boyko et al. 2007; Verhoeven et al. 2010), inducing methylation of small, non-coding RNAs as the stress response.

Transgenerational defense induction denotes a change in offspring phenotype guided by the environmental signal in the parental generation. This is a form of priming spanning across two generations. To assess the transmission of a priming signal, it is important to study parental environmental effects for different offspring traits (e.g., time of germination, resource allocation, plant architecture, and chemistry, etc.) (Verhoeven and van Gurp 2012; Liza M. Holeski et al. 2012). Plants in each generation can face combinations of different environmental challenges or stress and can often increase the resistance, growth, and reproduction success of their offspring under similar conditions (Karban et al. 1999; Herman and Sultan 2011).

A recent meta-analysis suggested that transgenerational transmission is also influenced by the developmental stage of parental and offspring during stress exposure, such that the transgenerational effect is stronger if the stress was experienced during the early development of the parental plants (Yin et al. 2019). Stress-relevant features like stress occurrence and its predictability in the parental environment can enhance the defense in offspring for the same stress and thus transmit as transgenerational defense (Yin et al. 2019). For example, Arabidopsis thaliana plants showed enhanced performance when exposed to single parental stress treatment (temperature shock or clipping), but not when two different treatments were combined, suggesting that environmental complexity is an important driver of efficient transgenerational defense (Lampei 2019).

Current studies reported that the transgenerational transmission of stress defense includes specific growth variations that are functionally adaptive to the parental conditions, but there are strong differences between the typical laboratory conditions to the complex environment of natural plant populations (Herman and Sultan 2011). However, first evidence exists that the required predictable environmental conditions for the selection of transgenerational effects indeed exist in nature. Lampei et al. (2017) showed in a recent study with a Mediterranean annual plant that winter precipitation predicted the following winter's seedling densities. In order to reduce competition in the offspring generation (avoidance strategy), plants from high water treatments reduced offspring germination (stronger seed dormancy) proportional to the long-term correlation between precipitation and the following winter's seedling density (Lampei et al. 2017). This example demonstrates the high complexity of the natural environments in which the plants live, but at the same time, it also demonstrates how seemingly random and very noisy variables, such as weather, can produce strong environmental correlations between generations that select for transgenerational plasticity.

But how does the transgenerational defense transmission work on the molecular scale? There are several possible mechanisms, including components of seed provisioning. But epigenetic mechanisms are often indicated as one of the most significant underlying mechanisms of transgenerational stress response (Boyko and Kovalchuk 2010; Luna et al. 2012). There are three major reasons supporting this suggestion.

1. The state of epigenetic modifications can be heritably transmitted, it is principally reversible, and the transition can take place rapidly (see Chapters 6, 7, and 8).

2. Epigenetic modifications are known to shape ecologically meaningful traits that also could be stably inherited. For example, histone modifications have been reported to be responsible for priming and transgenerational plant defense (Bej & Basak 2017; Jablonka and Raz 2009).

3. Epigenetic modifications can keep the memory potentially for a longer time than other types of transgenerational phenotype transmitters, such as components of seed provisioning.

Therefore, it is not unlikely that epigenetic modifications play a role also in the phenotype transition to the next generation. For a more detailed discussion of the molecular transmission of transgenerational plant defenses, refer to Chapter 1.

Gaps in current method and empirical knowledge: the transition from model to non-model plants

Deciphering the role of epigenetics for plant stress response has started with model species and only recently included species with different life-history. This is a challenging step that requires continuous improvement of molecular tools and collaboration among molecular geneticists, ecologists, and bioinformaticians. Experimental studies in plants with distinctive genomic and ecological features could contribute to understanding epigenetic responses to stress in terms of molecular and phenotypic changes. We need to extend the study by associating the role of stress-relevant features towards the stability of epigenetic marks for both priming and transgenerational defense using suitable tools. In order to get an approximate overview, I screened the literature studies for epigenetic contribution for explaining biotic and abiotic stress response of plants without attempting to cover all literature available. In ISI Web of Science (www.webofknowledge.com), I conducted a search for the articles published in English between 1990 and 2020 (last accessed 17th January 2020) using the following keywords combination [(plant stress) AND (epigenet*)] that gave us 1281 results on abiotic and biotic stress studies. Adding the keyword [AND (abiotic)/ AND (biotic)], the search retained 377 abiotic studies and 164 biotic studies, respectively, that also contained the keyword epigenetics, which does not mean that these studies identified correlating or causative epigenetic mechanisms for plant defense. Although the numbers of studies are increasing for the two types of stress events, there is also huge inadequacy of these studies with non-model plants due to several experimental shortcomings. In the following, I outline the most important gaps which are still understudied and where we still need to establish the proper relation of epigenetic contribution to plant defense strategies.

Representation of plant species:

First and foremost, the representation of diverse plant species in epigenetic studies of plant stress responses is important as most of the existing knowledge is based on studies conducted using model systems or cultivated plants that tend to be plants with a fast life-cycle. To gain generality in ecological settings, we need to study more non-model species with different life histories that can explain the phenotypic consequences and the epigenetic contribution to different stress responses.

Porper toolkit & statistical relevance:

The most studied epigenetic mechanism in plants is DNA methylation, though others like SmallRNA and histones are increasing in frequency. However, while for DNA methylation, reduced representation methods like provide the means to conduct large-scale ecological studies, such methods are mostly non-existent in other epigenetic contexts. This makes it often difficult to study more than DNA methylation in such projects or in plants with large and polyploid genomes.

Distinguish genetic and epigenetic contribution

A prevailing gap includes the lack of measures to untangle genetic and epigenetic contribution as ecological studies are often focused on collections from natural populations in situ. Ecological relationships should be evaluated across environmental gradients to gain an overview of the stress response, paired with an analysis of spatial genetic and epigenetic structure in the wild populations to understand the respective contribution (Herrera, Medrano, et al. 2012).

Understanding the cross-talk of epigentic regulators:

The link between epigenetic regulators (e.g., DNA methylation, histone modifications, and small RNAs) is often missing in current projects. However, it is often indispensable to understand the mechanisms of both the biotic and the abiotic stress response. This is because the cross-talks between epigenetic regulators themselves may have a role in gene expression (Grativol et al. 2012). More synthesis studies are needed to connect the dots in plant stress response by understanding the cross-talk of significant epigenetic regulators.

Preceding frequent abiotic stress can acclimatize plants by inducing a change in the epigenetic state, and the persistence of the induced state can be plastic. The epigenetic regulation of the abiotic stress response is complex in nature and could be interlinked with genetic networks or can be an independent event. From literature, we could observe a gap in in-depth studies conducted in natural populations. Most studies are done in artificial environments with model plants or cultivars. Reviews by Bej and Basak (2017) and Li et. al (2017) combined the information on abiotic factors and the contribution of different epigenetic mechanisms for different species (Bej & Basak 2017; Li et al. 2017). ‌In the natural environment, plants are exposed to many abiotic stresses such as salinity, drought, temperature, heavy metals. Epigenetic control of stress-responsive mechanisms was observed in several plant species under various abiotic stress conditions, such as extreme temperatures (Ding et al. 2019), drought (Huang et al. 2019), salinity (Yang and Guo 2018), herbivory, and pathogen (Holeski 2007). For example, increased salinity was associated with DNA methylation changes, histone acetylation, methylation, and phosphorylation in species like rice, Arabidopsis thaliana, tobacco, and mangrove plants (Kim et al. 2015).

In Arabidopsis thaliana, histone modifications are involved in the drought stress response (Kim et al. 2015). For heat stress, DNA methylation differed between heat-sensitive and heat-tolerant genotypes in rapeseed (Gao et al.). And in forest trees (Cork oak), an interplay between DNA methylation and H3 acetylation was observed at elevated temperatures (Correia et al. 2013). Also, cold stress response in A. thaliana and maize affect DNA methylation and histone acetylation (Steward et al. 2002). An interesting example was recently reported by Song et al. (2015), who found that the alpine subnival plant Chorispora bungeana revealed DNA methylation changes that correlated with the exposure to chilling and freezing. Notably, several of the candidate genes were related to physiological chilling and freezing resistance pathways (Song et al. 2015). In summary, induced plant response following abiotic stress seems to be closely related to epigenetic mechanisms that even take an active role in the acclimatization to changing environmental conditions.

Table 1: List of epigenetic modifications reported for abiotic stress:

Prior exposure to biotic stresses has been reported to have improved the defense response of plants. Studies on this topic have a similar bias towards Arabidopsis and cultivated plants as studies on abiotic stress. Reviews by Alonso et al. (2018) and Mauch-Mani et al. (2017) combined the information on biotic interactions and the epigenetic contribution in the response for several plant species (Alonso, Ramos‐Cruz et al. 2019; Mauch-Mani et al. 2017).‌

In the natural environment, plants encounter biotic stress like the occurrence of herbivores, parasites, and pathogens, or the absence of symbiotic partners, and competition with other plants, and hence plant defense response has coevolved with the evolution of interacting species and consequently developed diverse strategies of plant defense mechanisms (Karban et al. 1999; Holeski et al. 2012). These strategies have provided plant fitness benefits against stressors, e.g., herbivore damage (Baldwin et al. 1998). Priming and somatic memory to stress, like the exposure to a pathogen, has been repeatedly reported in correlation with epigenetic changes (Lämke and Bäurle 2017). The task for the future, as the authors note, is to overcome "correlation" and test causation. In other words, it is yet unresolved if these epigenetic changes are actively involved in the priming response. However, a notable study by Yu et al. (2013) demonstrated that treating Arabidopsis thaliana with a peptide of bacterial origin induced the active demethylation of transposable elements (TE), which mobilized short-interfering RNAs/siRNAs and led to the transcriptional activation of genes involved in the defense against bacteria (Yu et al. 2013). The study further found that DNA demethylation negatively affected the growth of a bacterial pathogen, suggesting a close link between the two.

Table 2: List of epigenetic modification reported for biotic stress:

Understanding the within- and inter-generation plant defense response through epigenetics requires the combined analyses of diverse species, their functional phenotypes, and the associated epigenetic variation. This chapter simultaneously shows the significance of epigenetics and the dire necessity of new studies that also should be conducted long-term with diverse species under conditions better matching the plant's natural environment to observe an ecologically more meaningful plant defense response. I also show that low genomic resolution has hindered the investigation of the correlation between ecological factors and epigenetic mechanisms in non-model organisms.

Furthermore, to have complete knowledge of underlying mechanisms, it is compulsory to have a collaboration between ecologists and molecular biologists to develop a proper toolkit. Following these recommendations, it should be possible to unravel the combined contribution of genetic and epigenetic variation to the expression of phenotypes and contribute to filling current knowledge gaps.

In a natural setting, plants are exposed to a complex environment, often with multiple stress conditions, and thus, to simulate ecological realism, we should have more than one stress factor in experimental design (see Lampei 2019). To study plant stress response, it is important to establish the causal links between epigenetic variation and phenotypes, as well the interference of genetic and epigenetic variation. Thus, one challenge lies in identifying the relevance of epigenetic factors for modulating the phenotypic response to specific stress factors. To this aim, it may be beneficial to include plant species with different life histories and genomic features. A few approaches have been reported by which epigenetic variation can be potentially measured for larger populations in an ecological setting.

Study system

Where possible, experiments should include several genetically divergent lines or diverse natural populations from one species. Single line, or genotype, experiments may provide very detailed information but lack generality of conclusion. Often, repeating the experiment with another genotype of the same species yields different results. This is not only true for epigenetic experiments but even more important in these because of frequent interactions with the genomic background. However, the enhanced generality comes with an increased complexity of the study. Therefore, epigenetic studies should preferably be conducted in ecological settings that control genotypic variability. For example, non-model species or natural populations that contain a low level of genetic diversity and reproduce asexually like, for instance, clonal plants, provide these properties (Richards, Bossdorf, et al. 2010).

‌Another approach is to study outcrossed species by evaluating both the DNA sequence and DNA methylation profiles of individuals using statistical approaches to understand the relation of genetic and epigenetic variation (Herrera and Bazaga 2011; Schulz et al. 2019). As the field is still developing for non-model species, we must be aware of the trade-off between the depth/resolution of functional information and cost-effectiveness. Following experimental methods to study epigenetic inheritance could help to fill the gaps in the field (Bossdorf et al. 2008).

Experimental method

An interesting option is the use of inhibitors for epigenetic factors such as the DNA methyltransferases (e.g., 5-azacytidine, zebularine) or histone deacetylases (e.g., Trichostatin). Together with knockout mutants, experimental demethylation can be used to establish the link between epigenetic factors and phenotypic response. However, this method has disadvantages in the first place because it is not targeted and reduces DNA methylation scattered across the genome so that connections between phenotype and methylation can be made, but it is often difficult to identify the specific methylation changes that were involved in the response. ‌

The study should choose the molecular mechanisms that are confirmatory and cost-effective to study epigenetics in natural populations. For example, for evaluating the methylation status, Reduced Representation Bisulfite Sequencing methods (RRBS) can also work without the availability of a high-quality genome (Niederhuth and Schmitz 2017), and it is cost-effective. This is a very nice option for studying methylation in non-model species. However, we need more methods with such criteria for studying other epigenetic factors. Quantitative genetics mapping approaches such as Epigenome-wide association studies (EWAS) can be another method to study the approximate genetic and epigenetic associations with the phenotype (Kreutz et al. 2020).

Overview

‌As sessile organisms of divergent life-history, plants are constantly exposed to a wide range of environmental fluctuations of abiotic conditions (e.g., temperature, drought, precipitation, nutrients) and biotic interactions (e.g., herbivory, pest, mycorrhiza) that can affect their growth, reproduction, and survival. When fluctuations of abiotic or biotic factors become extreme, plants experience stress, and their responses vary across life history, traits, and environmental context. Both for ecology and plant breeding/cultivation, it has become important to understand the means of plant stress responses because changes in plant productivity affect both biodiversity and agriculture. Natural populations can show differences in performance when they are exposed to changes in environmental conditions, partly because of their genetic variation but also because of their epigenetic variation. A general overview of the different types of plant stress factors, their physiological effects, and individual plant defense response mechanisms to overcome their impacts have been previously reported mainly for model and crop species (Mosa et al. 2017; Liza M. Holeski et al. 2012). In earlier chapters, we have discussed phenotypic plasticity and life-history traits in a more general way. In this chapter, we focus on the plant defense response to stresses from the viewpoint of epigenetics in order to understand the full depiction of the plant defense response.

‌

Understanding the role of epigenetic regulation in plant stress responses in the ecological context of natural populations has been a topic that received wide attention in ecological research (Thiebaut et al. 2019; Richards, Alonso, et al. 2017). For untangling the contribution of genotypes and epigenotypes to the stress response in natural populations, our current knowledge needs to be improved by conferring the epigenetic contribution to different types of stress that involves plant phenotypic variation in key traits of populations (Balao et al. 2018). For example, the diversity of life history (reported in Chapter 2) plays a role in the epigenetic regulation of plant stress responses for species with different longevities (annual, perennial, long-lived, etc.) and type of reproduction (sexual, asexual) (Alonso, Medrano et al. 2019). However, to date, the adaptive and evolutionary importance of epigenetic variation in terms of the plant stress response has only rarely been addressed. The incorporation of epigenetics for understanding the plant defense response is only starting (Balao et al. 2018). Different key traits, analysis of varied plant tissue types (root, leaf, bud, etc.), stress relevant features, and 'epiphenotypes' along with DNA sequence information should be analyzed to have more empirical information, which is needed to comprehend plant defense response in natural populations.

In natural plant populations, the most relevant features of environmental stress are the stress intensity, the occurrence frequency, and its predictability, as they will determine the most successful defense strategy to overcome its negative impact on plant performance. These features are properties of the natural environment of a population and are usually not taken into consideration in studies with model species. The defense strategies that plants can develop in nature after multidimensional biotic and abiotic stress exposure are highly related to the environments in which they live. In general, the intensity and frequency of stress factors tend to be inversely correlated, and the defense strategy is most likely selected by the dominant stress features the plants experience (derived from Grativol et al. 2012 and Walter et al. 2013). Further, the predictability of stress or the reliability of the environmental cue is important that plants can prepare a suitable plastic response, either within- or across generations (Reed et al. 2010). And, at which stage of lifespan a cue is received may also dictate the response strategy for different stresses. Studies suggested that when the environmental cue is persistent, plants also show stress-induced or environmentally induced defense mediated by epigenetic variation that could be transmitted over generations (Mauch-Mani et al. 2017). Both within and across generations, the stability of phenotypic responses depends on the degree and the predictability of environmental variation and on the (epi)genetic architecture (Herman et al. 2014). Therefore, the defense strategies of plants are selected according to the particular stress features in their natural environment, and they are specific for individuals or populations within a species and can also differ from species to species.

‌Plants use stress features as cues to fine-tune their defense responses so that they can minimize detrimental effects on plant fitness (Brown and Rant 2013). We can describe three general ways a plant can respond in accordance to the frequency and intensity of the stress: tolerance, avoidance, and induced defense (Walter et al. 2013; Grativol et al. 2012) (Fig 1).

‌

i) Induced defense: Plants show enhanced activation of induced defense when the intensity of stress is low but is encountered more frequently. Under such circumstances, plant performance will be higher if they have a plastic and reversible defense mechanism and, through prior frequent stress cues, an improved responsiveness or priming/acclimation (Fig 1). This means plants acquire this kind of defense by receiving frequent stimuli from pathogens, arthropods, chemicals, and abiotic cues that can trigger the establishment of priming (Mauch-Mani et al. 2017).

‌ii) Tolerance: Plants can show a neutral response of tolerance or a constitutive strategy where plants perform uniformly (same fitness and reproduction) regardless of the intensity and the frequency of stress occurrence. e.g., exposure to heavy metals or a high concentration of salts select plants with higher tolerance against that specific factor (Yaish 2013).

‌iii) Avoidance: Plants show avoidance or an escape strategy only during less frequent stress events of strong intensity because this strategy is usually associated with high costs. For example, fires, flooding, or complete defoliation events often favor avoidance by re-sprouting from below-ground shoots (Boyko & Kovalchuk 2008, "Epigenetic Control of Plant Stress Response"; Gong and Zhang, 2014).

Otherwise, plants also can have negative responses or damage after stress and eventually can suffer greater damage or even complete collapse when stress is recurrent.

Fig 1. Schematic representation of the relationship between plant performance and stress frequency and intensity according to the three plant defense strategies explained within the text. The two axes are continuous and relative. The X-axis denotes the usually inverse relationship between frequency and intensity for any given stress factor, and the Y-axis denotes plant performance, with zero being the average performance for the standard conditions at a certain environment. The dashed-dotted, straight, and dashed lines indicate the induced, the tolerance, and the avoidance plant defense strategy, respectively.

This ability of the immobile plants to survive under fluctuating conditions is sometimes aided by epigenetic mechanisms that can store information at a potentially low cost (Boyko & Kovalchuk 2008, "Epigenetic Control of Plant Stress Response"; Kranner et al. 2010; Grativol et al. 2012). Epigenetic regulation involves histone variants, histone post-translational modifications, small RNA, and DNA methylation that together alter the chromatin structure and determine changes in individual phenotypes without changing the DNA sequence. In plants, methylation of the 5th carbon of the DNA nuclein base cytosine (DNA methylation hereafter) is found within three sequence contexts along the genome: CG, CHG (H = A, T, C), and CHH. DNA methylation regulates the activation and movement of transposable elements and the expression of genes (see Chapter 6 for details). Furthermore, different histones (H2A, H2B, H3, and H4) can be covalently modified at different positions (mostly lysine and arginine residues) by different chemical marks (see Chapter 7 for details). Finally, small regulatory RNAs (sRNAs; approximately 21–24 nt in size, see Chapter 8 for details) also have emerged as important regulators of gene expression. The main aim of this chapter is to review how these epigenetic factors can contribute to the plants' stress responses and discuss how to fill the gaps in our current understanding, as well as how to untangle the genetic and epigenetic contributions.

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