Summary

Plants are continuously exposed to fluctuating environmental conditions. As sessile organisms, they have a restricted capacity to select the features of their environment; hence, it is crucial for them to respond to environmental changes successfully. A way how plants can cope with environmental changes is phenotypic plasticity (i.e. the ability of one genotype to produce more phenotypes when exposed to different environments). Despite the importance of phenotypic plasticity in plant adaptation to environmental changes, the molecular mechanisms underlying phenotypic variation remain still largely obscure.

Phenotypic plasticity seems to be regulated by epigenetic modifications (i.e. histone modifications, DNA methylation and RNA molecules), which affect phenotypes by regulating gene activity. Interestingly, epigenetic modifications are partly heritable across mitotic and (to some extent) meiotic cell divisions, suggesting that they may mediate phenotypic responses even across clonal or sexual generations (i.e. transgenerational plasticity). In particular, epigenetic modifications seem to be better maintained across clonal than sexual generations. Thus, transgenerational plasticity may be more relevant for clonal species, as it may allow them to bypass their potentially low-standing genetic diversity. However, if and when plastic responses are inherited across generations is further complicated by several factors, such as the predictability of the offspring environment and specific plant characteristics (e.g. sex, genotype and species). Furthermore, plastic responses can also occur independently of epigenetic modifications when they are mediated, for example, by physiological and developmental events or maternal seed provisioning. Thus, the combined effects of all these variables make the study and understanding of phenotypic plasticity difficult.

This chapter aims to overview the variables affecting phenotypic plasticity and the potential role of phenotypic plasticity in rapid plant adaptation to environmental changes.

Despite the abundance of studies investigating the phenotypes produced in response to changing environments, the molecular mechanisms underlying phenotypic variation remain still largely unknown in both plants and animals. Organisms need to process environmental signals and respond appropriately accordingly to their significance. They achieve this through a system common to all organisms based on signal reception, transduction and translation, and the resulting product(s). In particular, environmental stimuli are perceived and transmitted by different signal transduction pathways. These pathways switch on specific transcription factors, which activate genes, ultimately affecting the phenotype.

Notably, in some cases, this process driving phenotypic plasticity was affected by epigenetic mechanisms (Schlichting, 1986; Mirouze and Paszkowski, 2011). Epigenetic mechanisms (e.g. changes in chromatin structure and small RNAs) can regulate gene expression at both the transcriptional and post-transcriptional level. Thus, epigenetic modifications could be a key mechanism in the modulation of gene expression after the environmental signal perception. This hypothesis received support by accumulating evidence that epigenetic modifications may contribute to the regulation of phenotypically plastic traits (e.g. Tatra et al., 2000; Bossdorf et al., 2010; Kooke et al., 2015). One of the best-studied examples is the timing of flowering, in which epigenetic factors evidently play an essential role (He, 2009; Jeong et al., 2015). Proper flowering time is crucial to ensure reproductive success, especially in annual species. Therefore, it is finely regulated by integrating various endogenous and environmental signals to ensure that flowering initiates under the most favorable conditions. In A. thaliana, among other environmental signals, flowering time is regulated by cold exposure through the vernalization pathway. In this pathway, prolonged exposure to low temperatures triggers flowering by silencing the flowering repressor FLOWERING LOCUS C (FLC) through epigenetic modifications (Bastow et al., 2004; Sung and Amasino, 2004; Sung et al., 2006; Finnegan and Dennis, 2007; Greb et al., 2007; Schmitz et al., 2008). This repression is mitotically stable and allows rapid flowering in spring. It functions as a memory of prior cold exposure. However, FLC expression is re-activated during embryogenesis so that the next generation requires vernalization again to accelerate flowering (Sheldon et al., 2008). Therefore, vernalization-mediated FLC repression is mitotically stable but meiotically unstable, and this way reliably times one of the most critical transitions for an annual plant. Clearly, the vernalization response (accelerated flowering) is not immediately triggered by the stimulus (low temperatures); on the contrary, the plant starts flowering when the original stimulus (low temperatures) is removed. This is possible thanks to the epigenetic basis of vernalization, which allows preserving the low-temperature stimulus occurring in winter until the following spring, promoting in this way the floral transition (Lang, 1965).

In conclusion, despite the genetic and epigenetic basis of some phenotypic responses are relatively well characterized (e.g. flowering time), the molecular mechanisms regulating the majority of phenotypic responses remain poorly understood. More studies are thus needed to unravel the role of epigenetic mechanisms in phenotypic plasticity, improving our understanding of the role of epigenetic mechanisms in evolution and adaptation.

Phenotypic plasticity can occur both within and across generations. It is defined as within-generation plasticity if it occurs within a single generation: an individual encounters distinct environments and reacts accordingly. Conversely, transgenerational plasticity includes heritable phenotypic responses that persist for multiple generations, in which the conditions experienced in one generation can interact with conditions experienced by subsequent generations (Agrawal et al., 1999; Salinas et al., 2013). It is essential to point out that some authors distinguish even further between "intergenerational" and "transgenerational" plastic responses. Intergenerational responses (or parental effects) refer to phenomena spanning short timescales (i.e. one generation after the initial trigger) (reviewed in: Badyaev & Uller, 2009). Transgenerational effects refer to phenomena persisting for multiple generations in the absence of the initial trigger and thus cannot be ascribed to direct effects of the trigger. For simplicity reasons, in this chapter, we will use the broad definition of "transgenerational" to encompass both of these sub-categories. Furthermore, when not specified either “within-generation” or “transgenerational, we will refer to the broad definition of “transgenerational” plasticity.

Intuitively, one could think that similar conditions cause the expression of analogous within-generation and transgenerational phenotypic responses. However, simulation models suggest a different scenario. Natural selection may act on them independently. In particular, within-generation plasticity seems to be favored in an environment characterized by high temporal variability. In contrast, transgenerational responses are favored when the offspring environment is predictable across generations, showing low temporal variability and a slow rate of environmental change (Leimar and McNamara, 2015). That such environmental conditions exist in nature was recently demonstrated using 120 years of climate records for the United States of America (Colicchio and Herman, 2020). However, selection can also favor transgenerational plasticity in highly variable environments (Lampei et al., 2017). It all depends on the environmental correlations between the parental and the offspring generation. This correlation can have the form of a temporal autocorrelation in, e.g. temperatures (Leimar and McNamara, 2015; Colicchio and Herman, 2020) or a correlation between different environmental variables so that, e.g. the amount of rain in the parental season affects the density of seedlings in the offspring season (Lampei et al., 2017).

In particular, transgenerational plasticity can be adaptive, maladaptive or neutral. Transgenerational plasticity is neutral when the parental environment has no effects on the fitness of the offspring, and it is maladaptive when the parental environment limits the fitness of the offspring (Sultan, 1996; Roach and Wulff, 1987; Galloway, 1995; Donohue and Schmitt, 1998). Transgenerational plasticity is adaptive when the parental environment increases the fitness of the offspring, or in other words, when the parental environment allows the plants to pre-adapt their offspring to the conditions they will experience.

For example, Whittle et al. (2009) reported evidence for adaptive transgenerational responses to heat stress in A. thaliana that persisted over at least two generations. Using a set of homozygous inbred lines, they exposed the F0 and F1 generations to heat stress (30°C), and they found that the F3 progeny increased the reproductive output fivefold under heat stress. This effect persisted into the F3 generation, even when F2 plants were grown at a moderate temperature (23°C) (Whittle et al., 2009). The specific mechanisms leading to this fitness increase in the offspring were, however, not documented. The effects of temperature stress also appear to be heritable and potentially adaptive in the cosmopolitan weed Plantago lanceolata. Case et al. (1996) showed that the effects of cold temperature treatment persisted across two generations, significantly enhancing seed weight and fitness-related leaf and life-history traits in adult grandchild plants. Contrary to what was often assumed, this result clearly showed that transgenerational effects might not be confined to the seedling stage. Furthermore, in this species, the paternal temperature also significantly affected offspring traits via interactions with the maternal temperature environment (Lacey, 1996). Furthermore, the paternal environment may also be relevant in outcrossing species, though less than the maternal environment (Roach and Wulff, 1987; Mazer and Gorchov, 1996; Diggle et al., 2010).

Beyond temperature, also other environmental variables can trigger adaptive transgenerational plasticity. In P. lanceolata, offspring showed improved relative fitness when exposed to maternal nutrient availability (Latzel et al., 2014). In Mimulus guttatus, parental wounding induced resistance against natural herbivory (Colicchio, 2017). Also known for strong adaptive parental effects is the maternal shading status that prepares offspring of several herbs for growing in the open (sun) or under canopy (shade) (Galloway and Etterson, 2007; McIntyre and Strauss, 2014). So, despite the rather specific nature of environments that favor transgenerational plasticity, it appears to be frequently found among plants. However, this seems to depend on life history. In a recent meta-study, transgenerational plasticity was frequent and adaptive among annual plants but less frequent and neutral or negative among perennial plants (Yin et al., 2019).

Transgenerational effects are also genotype‐specific as seed families differed in transgenerational plasticity (Alexander and Wulff, 1985; Schmitt et al., 1992; Schmid and Dolt, 1994; Andalo et al., 1998; Agrawal, 2001, 2002; Riginos et al., 2007; Bossdorf et al., 2009). More recently, these differences were used to demonstrate that the reaction norm of parental effects can correlate with climate variables (Groot et al., 2016). In other words, the differences between genotypes in transgenerational plasticity seem to occur not at random but were likely favored by past selection.

To conclude, we do have evidence from different sources that transgenerational plasticity contributes to plant adaptation. However, for a more comprehensive overview, we need more examples, especially studies that include many genotypes or many species, to increase the generality of conclusions.

Plastic responses to environmental stress can be transmitted across plant generations via multiple mechanisms, independently or even in the absence of DNA sequence variation (Cortijo et al., 2014; Zhang et al., 2013). In particular, adaptive transgenerational plasticity can be mediated by starch reserves, mRNAs, proteins, hormones, and other primary and secondary metabolites packaged in the seed (Roach and Wulff, 1987; Leishman et al., 2000; Fenner and Thompson, 2005; Moles and Leishman, 2008), and by epigenetic mechanisms (Rossiter, 1996; Boyko et al., 2010; Richards et al., 2017), via the alteration of gene expression through heritable changes in cytosine methylation or histone modification (Richards, 2006; Bird, 2007; Richards et al., 2017). Since provisioning effects are mediated directly by maternal individuals, environmental effects that persist for multiple generations must be mediated by mechanisms capable of longer-term stability (e.g. epigenetic mechanisms). However, these mechanisms are neither completely separate nor mutually exclusive. On the contrary, multiple mechanisms can cooperatively influence heritable phenotypes (see paragraph: "Combined effects of transgenerational plasticity mechanisms").

a. Seed provisioning and maternally derived proteins and mRNAs

Seed provisioning refers to the carbohydrate, lipid, protein, and mineral nutrient reserves stored by the mother plant in the developing seed (Koller, 1972; Srivastava, 2002). It is often reduced in the deprivation of resources in maternal plants, resulting in an offspring with diminished early growth rates, seedling size, and competitive ability (Haig and Westoby, 1988; Fenner and Thompson, 2005), causing maladaptive transgenerational effects. Alternatively, resource-deprived maternal plants can maintain or even increase seed provisioning (Roach and Wulff, 1987; Schmitt et al., 1992; Sultan, 1996, 2001; Donohue and Schmitt, 1998), maximizing in this way seedling survival. For example, well-provisioned offspring can produce more extensive root systems in dry soil or larger shoot systems under canopy shade (Silvertown, 1984; Wulff, 1986; Leishman et al., 2000). In natural populations, however, the adaptive benefit of such enhanced provisioning may be limited. Resource-deprived maternal plants, in such cases, tend to produce fewer seeds with more chances of surviving. Furthermore, an increased seed provisioning can correlate with decreased persistence in the soil seed bank (Sultan, 1996; Donohue and Schmitt, 1998; Fenner and Thompson, 2005). Hence, in stressful maternal conditions, transgenerational effects mediated via seed provisioning can promote offspring success in specific ecological settings.

Besides seed provisioning, stressed maternal plants can transmit to the offspring also proteins, mRNAs, small RNAs, secondary metabolites, and hormones. Maternally-derived proteins can act both as regulatory molecules and as nutritive elements (via seed provisioning). Together with maternally-derived mRNAs, they are key regulators of seed dormancy and germination (Donohue, 2009). Since stress can significantly alter maternal gene expression, maternally-derived mRNAs and proteins may facilitate adaptive growth responses in seeds germinating under stressful conditions (Rajjou et al., 2004).

b. Epigenetic inheritance: DNA methylation, histone modifications and small RNAs

Epigenetic mechanisms can also mediate transgenerational effects. DNA methylation seems to be both environmentally sensitive and heritable over multiple (i.e., ≥8) generations (Johannes et al., 2009; Reinders et al., 2009; Hauser et al., 2011; reviewed by Jablonka and Raz, 2009). Therefore, DNA methylation (and possibly other epigenetic mechanisms) may also play a role in regulating transgenerational effects of environmental stress (Kalisz and Purugganan, 2004; Grant-Downton and Dickinson, 2006; Boyko and Kovalchuk, 2011). After exposing A. thaliana plants to salt stress, Boyko et al. (2010) found an increased tolerance to the same stress in the progeny that correlated with the inheritance of stress-induced DNA methylation marks. In tobacco plants, infection with tobacco mosaic virus (TMV) also caused heritable changes in DNA methylation. It increased resistance to viral, bacterial, and fungal pathogens in the progeny (Kathiria et al., 2010).

To some degree, the transgenerational effects mediated by DNA methylation seem to be genotype-specific (Herman and Sultan, 2016; Rendina González et al., 2018). Herman and Sultan (2016) investigated the transmission mechanisms of adaptive transgenerational responses to drought stress in different genetic lines of the annual plant Polygonum persicaria. The offspring of the drought-stressed parental plants were treated with the demethylating agent zebularine and grown in dry soil. These plants did not present the adaptive phenotypes shown by the naturally methylated offspring (more extended root systems and greater biomass), suggesting that demethylation removed the adaptive effect of parental drought stress (without significantly altering phenotypic expression in offspring of well-watered parents). Since the seed provisioning between offspring of drought-stressed and well-watered parents was equivalent, differential seed provisioning did not contribute to the effect of parental drought on offspring phenotypes. Furthermore, the effect of demethylation on the expression of the parental drought effect was found to differ among the genetic lines. These results suggest that DNA methylation can mediate adaptive, genotype-specific effects of parental stress on offspring phenotypes. However, demethylation of the whole genome is not targeted and may result in random demethylation variation among replicate lines (see also “Chapter 3: Plant defense response”) or may activate previously inactive transposable elements (see also “Chapter 4: Epigenetics in evolution”).

Despite being to some extent genotype-specific, plastic transgenerational responses to environmental stress can occur even in the absence of genetic variation. To investigate this aspect, a potent approach is the use of A. thaliana epigenetic recombinant inbred lines (epiRILs), characterized by high DNA methylation variation but no DNA sequence variation (Johannes et al., 2009; Reinders et al., 2009; Teixeira et al., 2009). In A. thaliana, studies of epiRILs showed that DNA methylation variants can cause substantial heritable variation in key traits such as primary root length and flowering time (Cortijo et al., 2014; Zhang et al., 2013). In particular, Zhang et al. (2013) tested the response of a large number of epiRILs of A. thaliana to drought and increased nutrient conditions, and they found significant variance components and heritabilities in several phenotypic traits, including flowering time, plant height and total biomass, fruit number, and root:shoot ratio. Thus, this study provides evidence that variation in DNA methylation can cause substantial heritable variation of ecologically important plant traits even in the absence of genetic variation.

In sexually reproducing plants, another layer of complexity is represented by the parental sex, since the inheritance of epigenetic modifications mediating transgenerational effects seems to be sex-specific. In the yellow monkeyflower plants (Mimulus guttatus), Akkerman et al. (2016) tested for differences between maternal and paternal transmission of the transgenerational induction of increased glandular trichome density in response to simulated insect damage. Both maternal and paternal damage resulted in similar and additive increases in progeny trichome production. Notably, the treatment of germinating seeds with 5-azaC erased the effect of maternal but not paternal damage. These results indicate that transgenerational effects can occur through maternal and paternal germlines, but they differ in the proximate mechanism of epigenetic inheritance.

Not only DNA methylation, but even histone modifications can affect gene expression by altering chromatin structure. Histone modifications can also be transferred from one generation to the other, as shown in A. thaliana (Lang-Mladek et al., 2010). Lang-Mladek et al. (2010) found that both heat stress and UV-B exposure could induce heritable changes in gene expression in A. thaliana, correlating with histone H3 deacetylation and with no DNA methylation changes. This effect was found only in small groups of cells within the plant and persisted for two offspring generations.

In addition to DNA methylation and histone modifications, small RNAs (sRNAs) can also have a role in plant transgenerational effects. Changes in sRNA composition have been associated with heat (Ito et al., 2011; Bilichak et al., 2015; Song et al., 2016), drought (Matsui et al., 2008; Tricker et al., 2012), salinity (Borsani et al., 2005; Matsui et al., 2008; Ding et al., 2009; Song et al., 2016), cold, and osmotic stress (Song et al., 2016), and in some cases they even persisted in the offspring of stressed plants (Bilichak et al., 2015; Morgado et al., 2017). In A. thaliana, mutants in the biogenesis of sRNA showed compromised transgenerational caterpillar herbivore resistance (Rasmann et al., 2012), suggesting that sRNAs were required to sustain induced defense responses across generations.

c. Combined effects of transgenerational plasticity mechanisms

As mentioned previously, several modes of transgenerational responses can act together to influence offspring phenotypes. In the wild radish Raphanus raphanistrum, both seed mass-dependent and seed mass-independent transgenerational responses to maternal caterpillar herbivory were found (Agrawal et al., 1999; Agrawal, 2001, 2002). Seed mass is often used as a proxy for seed provisioning (Moles and Leishman, 2008, Lacey et al., 1997). The molecular mechanism behind non-provisioning effects was not investigated in this study (Agrawal, 2001, 2002). However, these results show how even a relatively simple environmental change can induce multiple physiological changes that together enhance offspring performance.

d. Transgenerational plasticity in clonally reproducing plants

Transgenerational effects have been studied mostly across sexual generations, but they have high potential relevance, especially for asexual (or clonal) species (e.g. Latzel and Klimešová, 2010). When plants reproduce clonally, they produce genetically identical offspring not arising from seeds (except in the case of apomixis, in which seeds are asexually produced). Therefore, seed provisioning cannot play a role in transgenerational effects occurring in non-apomictic clonal plants. On the contrary, epigenetic inheritance can occur both across clonal and sexual reproduction (reviewed by Jablonka and Raz, 2009). Epigenetic inheritance even seems to be more prominent across clones, which bypass the epigenetic erasure associated with meiosis (Feng et al., 2010). Thus, it has been suggested that epigenetic inheritance could play a key role in transgenerational plasticity in clonally reproducing plants (Latzel and Klimešová, 2010; Verhoeven and Preite, 2014; González et al., 2016; Rendina González et al., 2018).

González et al. (2016) exposed plants of white clover (Trifolium repens) to different drought treatments and analyzed the transgenerational effects (i.e. offspring biomass) on the untreated clonal offspring. To assess whether DNA methylation was essential to mediate these effects, half of the plants were treated with the demethylating agent 5-azacitidine. In the naturally methylated clonal offspring, they found stress-driven transgenerational effects. However, these effects were not present in the demethylated plants, suggesting that DNA methylation was involved in the observed transgenerational effects.

In the same system, Rendina González et al., 2018 explored whether the effects of transgenerational plasticity were genotype-specific and under epigenetic control. They analyzed the effects of transgenerational plasticity induced by multiple parental stresses on the clonal offspring using five different genotypes. They found that transgenerational plasticity induced by different stresses was genotype-specific and that at least one stress (drought) induced DNA methylation variation that was maintained across several clonal offspring generations. These results suggest that transgenerational effects in Trifolium repens are genotype-specific, potentially under epigenetic control and inherited across several clonal generations.

Phenotypic plasticity seems to be adaptive and inherited across generations. Therefore, it can play a significant role in population dynamics and evolution. However, our understanding of the importance of adaptive transgenerational plasticity across different environmental factors and taxa is still limited. For example, plasticity might be even more important in perennial species with long life cycles, respect to annual plants (Walter et al., 2016; Herman and Sultan, 2011). In perennial species, genetic adaptation through natural selection could be indeed too slow to keep pace with rapid environmental changes (but see Yin et al., 2019 for more frequent adaptive transgenerational effects in annual plants).

Phenotypic plasticity may be an adaptive strategy also for clonal plants, as it can allow them to colonize new environments even with low standing genetic diversity. It may be particularly relevant also across clonal generations since it can be mediated by epigenetic mechanisms, which seem to be better maintained across clonal than sexual generations. The transgenerational effects mediated by heritable environmentally-induced epigenetic changes can, therefore, enable a rapid adaptation to changing environments, which infers implications in the short-term microevolution of clonal plants (Latzel and Klimešová, 2010; Verhoeven and Preite, 2014; Dodd and Douhovnikoff, 2016).

Notably, transgenerational plasticity gives rise to adaptive heritable variation precisely when required, as opposed to randomly occurring genetic variation (Verhoeven et al., 2010). Furthermore, particular environmental stress can induce the same adaptive phenotype in various offspring individuals in a population at the same time, as opposed to a phenotype based on genetic variation, which is shared only by part of the population. Consequently, populations can undergo rapid and extensive phenotypic adaptation based on transgenerational plasticity even in the absence of changes in the DNA sequence (Jablonka and Raz, 2009).

Transgenerational plasticity might be relevant also for understanding the ecological impacts of climate change, including global temperature and moisture changes predicted to arise very rapidly due to human activities (IPCC, 2014). Since adaptive transgenerational plasticity can be established even within one generation, it can shortly buffer populations against the immediate effects of climate change and provide time for genetic adaptation or genetic assimilation to act in the long run (Chevin, Lande, & Mace, 2010; Kopp & Matuszewski, 2014). For more details, refer to "Chapter 4: Epigenetics in evolution". In conclusion, our understanding of plant phenotypic plasticity has drastically improved in the last decades. Many phenotypic responses seem to be affected by epigenetic mechanisms, and they seem to facilitate plant adaptation to environmental changes. However, a vast majority of these phenotypic responses seem to be genotype-, species- and taxa-specific, which makes it hard to draw general conclusions on the role of epigenetically-driven phenotypic plasticity in plant adaptation. But then again, it is the nature of local adaptation that the effects are specific to the specific local environment and the genetic properties of the local population. There is thus the need to explore epigenetically-driven phenotypic responses across several genotypes, non-model plant species and taxa.

The study and understanding of phenotypic plasticity require a multidisciplinary approach, including different areas of biology, such as molecular biology, ecology and evolutionary biology. From one side, the multifaceted nature of phenotypic plasticity justifies its attraction; from the other side, it explains the difficulty to unravel a plastic phenotype in toto. In fact, the ecological and evolutionary role of phenotypic plasticity, as well as the molecular mechanisms regulating its responses, are still relatively unknown.

This chapter provides insight into the current state of knowledge of phenotypic plasticity ranging from its historical definition, passing through the known molecular mechanisms and transgenerational responses, and concluding with the possible role of phenotypic plasticity in evolution and adaptation. These concepts are explained using real examples, emphasizing the importance of epigenetic mechanisms as a key regulator of these responses.

a. Historical insights

Phenotypic plasticity started to gain the interest of the scientific community at the beginning of the 20th century. In 1909, Richard Woltereck performed the first experiments on plastic characters and coined the term "reaction norm" to describe the relationship between the expressions of phenotypic traits across a range of different environments (Schlichting and Pigliucci, 1998). Johannsen (1911) was then the first to distinguish between genotype and phenotype, introducing the concept of genotype-environment interaction, which was developed further by the British developmental biologist Waddington. In particular, Waddington introduced the concept of genetic assimilation, which is how a phenotype initially produced in response to an environmental alteration becomes later genetically encoded (Waddington, 1961). Such a process was identified by studying the phenotypes displayed by Drosophila pupae exposed to environmental stresses (i.e. heat shock or ether vapor) (Waddington, 1953; Waddington, 1956). These phenotypes were indeed initially induced by environmental stress and became then genetically fixed, i.e. they were expressed even without environmental induction. Since these phenotypes were not innate but induced by an environmental event, Waddington argued that genetic assimilation was a change in the pathways of the developmental program due to an environmental change. He claimed that phenotypes result from the interaction between genes and often environment-sensitive developmental factors, which he called for the first time epigenetic factors (Waddington, 1957).

Another conceptual advancement for plasticity research came in 1965 when Anthony Bradshaw suggested that plastic traits may be influenced by natural selection (Bradshaw, 1965). According to his model, plastic traits are environmentally induced and genetically controlled, so that selection can directly act on them. The link between plasticity and evolution was then further developed by Mary-Jane West-Eberhard. She proposed that the genetic accommodation of environmentally induced phenotypes can lead to morphological or behavioral diversification in animals and plants, arguing that phenotypic plasticity plays a crucial role in evolution and speciation (West-Eberhard, 2005).

b. Current understanding in plants

Phenotypic plasticity is today described as the ability of one genotype to produce more phenotypes when exposed to different environments (Pigliucci, 1997). Phenotypic plasticity includes all types of environmentally induced changes, such as physiological, morphological and life-historical traits. Even though it is common in all organisms, plasticity is more broadly expressed in plants, which cannot move away from unfavorable environments because of their sessile nature.

The relationship between phenotype and environment is often represented by a reaction norm (Stearns, 1992; Roff, 1997). In other words, the reaction norm shows the range of phenotypes that a single genotype can express across a range of environments. The reaction norm for any specific trait of a genotype can be visualized as a line or a curve on a two-dimensional plot of the environmental factor (x-axis) versus the phenotype/trait (y-axis) (Fig. 1). The reaction norm is linear when representing two distinct environmental states (e.g. two different temperatures) (Fig. 1A, 2B), while it is linear or non-linear when representing more than two environmental states (e.g. a whole range of temperatures) (Fig. 1D).

The slope of the reaction norm gives hints on the estimation of phenotypic plasticity: a positive (Fig. 1A) or a negative slope (Fig. 1B) implies that the genotype is phenotypically plastic, whereas a flat reaction norm with slope zero represents a non-phenotypically plastic genotype (Fig. 1C).

Figure 1: reaction norms of a single genotype. (A, B, C) Linear reaction norms with positive (A), negative (B) or flat (C) slopes. The positive or negative slopes indicate a phenotypically plastic genotype, while the flat slope a non-phenotypically plastic genotype. (D) Non-linear reaction norm representing more than two environmental states.

Reaction norms representing different genotypes can also be plotted on the same graph, which allows comparing the responses of different genotypes to the same environmental states (Fig. 2). If the two reaction norms are congruent, the two genotypes respond phenotypically in the same way when exposed to the same range of environments (Fig. 2A). When the two reaction norms have identical slope and shape and are shifted along the y-axis, the genotypes show phenotypes that differ on average, but the phenotypic response to the environment is the same (Fig. 2B). When the reaction norms are non-parallel, the two genotypes differ in their phenotypic response to the environment (Fig. 2C-E). Different genotypes of the same species showing non-parallel reaction norms indicate the presence of genotype-by-environment interactions.

Figure 2: reaction norms of two genotypes. (A) Congruent reaction norms indicate that two genotypes display the same phenotypic responses when exposed to the same environments. (B) Reaction norms with identical slope and shape but shifted along the y-axis show genotypes with different phenotypes on average. (C-E) Non-parallel reaction norms indicate that the two genotypes respond phenotypically differently to the same environments.

The sources of phenotypic variation within a population grown in different environments can be summarised by the following equation:

VP = VG + VE + VGxE + Vε.

Here VP is the total phenotypic variance in a trait, VG is the phenotypic variance attributed to differences between the genotypes, VE is the phenotypic variance attributed to differences between the environments, VGxE is the phenotypic variance attributed to the genotype-by-environment interaction, and Vε is the residual or error variance not explained by any of the other sources of variation (Scheiner and Goodnight, 1984).

Notably, each component of this equation can be influenced by epigenetic processes (Banta and Richards, 2018). Epigenetic processes can alter gene expression, ultimately shaping phenotypic variation in response to the environment (Duncan et al., 2014). However, phenotypic responses can also be mediated by indirect physiological and developmental events, such as biochemical mechanisms (reviewed in Kelly et al., 2012), not all of which involve epigenetic processes. For example, extreme temperatures or poor nutrition can directly alter cellular and developmental processes that may also influence complex phenotypic traits.

In summary, phenotypic plasticity arises from diverse mechanisms that can act together, resulting in a wide range of different phenotypes. Although phenotypic plasticity can potentially result also from epigenetic-independent biochemical and nutrient constraints, epigenetic mechanisms can still have a crucial role in mediating many phenotypic responses.

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