Environmental hormesis of non-specific and specific adaptive mechanisms in plants
Graphical abstract
Introduction
Adaptation to environmental stressors (i.e., to environmental factors that cause stress) is an essential property of plants which allows them, like other organisms, to survive in changeable environment (Pereira, 2016), including new environmental challenges, such as human and veterinary pharmaceuticals, pesticides, nanoparticles, micro/nanoplastics (Geissen et al., 2015; Rillig et al., 2019; Agathokleous et al., 2021a, Agathokleous et al., 2021b), ground-level ozone (Agathokleous et al., 2019a; Leung et al., 2020;), hydrocarbons (Agathokleous et al., 2020a). Understanding the patterns of plant adaptation to environmental challenges is directly related to managing the productivity of agricultural crops and, consequently, food security (Pitesky et al., 2014; Agathokleous and Calabrese, 2020). In addition, adaptive plant responses are widely used in biomonitoring and bioindication to assess environmental quality (Mukhopadhyay et al., 2020), as well as to reduce soil, water, and air pollution through phytoremediation (Mukhopadhyay et al., 2020; Diarra et al., 2021).
Furthermore, plants play a crucial role in many aspects of the biogeochemical cycles in the biosphere, thereby ensuring stability of the biosphere, especially through the fixation of carbon (C) by photosynthesis, which provides the basis for the energy flow of ecosystems. Plants are most prominent as controlling players of net primary production in all terrestrial and aquatic environments (Austin and Zanne, 2015). Thus, adaptive plant responses affect global processes in the biosphere via the primary production of ecosystems. Therefore, they can be used not only to assess the environmental quality of local areas but also for the estimation and prediction of global changes at the biosphere level (Sakalli et al., 2017). For example, those caused by climate change due to the accumulation of carbon dioxide in the atmosphere (DeLucia et al., 1999; Sakalli et al., 2017).
In recent years, the concept of environmental hormesis has been increasingly used to explain the adaptive responses of living organisms, including plants, to low doses of natural factors, both abiotic (temperature, soil moisture, and light, among others) (Agathokleous et al., 2019e; Duarte-Sierra et al., 2020; Erofeeva, 2021) and biotic (allelochemicals, biotic elicitors) (Vargas-Hernandez et al., 2017; Park et al., 2020) as well as various pollutants, for instance, ground-level ozone (Agathokleous et al., 2021d), heavy (Shahid et al., 2020) and rare earth (Agathokleous et al., 2019d) metals, and different organic compounds (herbicides, antibiotics, nanopesticides, hydrocarbons, among others) (Belz et al., 2018; Belz and Sinkkonen, 2019; Agathokleous et al., 2018a, Agathokleous et al., 2020a, Agathokleous et al., 2020c, Agathokleous et al., 2021c). Hormesis is considered an adaptive biphasic response to stress factors that are characterised by an improvement in the indicators of living systems (from cells to communities and ecosystems) at low factor doses and their deterioration in the high-dose zone relative to the control level (Calabrese, 2008; Agathokleous and Calabrese, 2020) (Fig. 1).
In turn, the term ‘environmental hormesis’ is proposed to be used for hormesis caused by environmental factors inducing stress in biological organisms at low and high levels of exposure (Agathokleous, 2018) and having stimulating and inhibitory effects, respectively. In a recent review (Erofeeva, 2021), the author of this article demonstrated that environmental hormesis can also be observed in plants under exposure to various abiotic factors (light, temperature, humidity, etc.). Unlike many pollutants, which are xenobiotics, abiotic factors do not have a zero control level, but rather an optimal one; therefore, their dose effects are described by Shelford's tolerance law curve (Erofeeva, 2021). Nevertheless, even in this case, a moderate deviation of the abiotic factor from its optimum causes hormetic stimulation (trait improvement relative to the optimum), and a significant deviation has an inhibitory effect (trait deterioration relative to the optimum). Unlike hormetic stimulation, which requires adaptation costs, in the optimum zone, the plants use energy only for the main life processes; therefore, in the long term, this state is more optimal (Erofeeva, 2021). Thus, environmental hormesis can be caused by any environmental factor (abiotic, biotic, anthropogenic), regardless of the control level (zero or optimal) and the type of factor (natural or anthropogenic).
The molecular mechanisms (e.g., receptors and cell signaling pathways) and patterns of adaptive processes underlying hormesis are still poorly understood (Agathokleous et al., 2020e). Hormetic stimulation is considered an overcompensation or a direct stimulation, which can increase the resilience to a subsequent strong impact/impacts (Calabrese, 2008). Hormesis is associated with stress; therefore, the focus of research is on studying the general patterns and mechanisms underpinning hormetic stimulation induced by various mild stressors (Agathokleous et al., 2020e).
At the same time, adaptive plant responses have certain specificity to environmental factors, since these responses are aimed at eliminating specific disruptions (i.e., specific ‘strains’) caused by stressors (Blum, 2016). For example, excessive soil moisture causes hypoxia in plants (Loreti and Striker, 2020), salt stress and drought lead to osmotic stress (Acosta-Motos et al., 2017). In addition, salt stress, unlike drought, disrupts the ion balance of plant cells (Ma et al., 2020). The herbicide glyphosate inhibits the plant enzyme 5-enolpyruvylshikimate-3-phosphate synthase in the shikimate pathway (Zulet-González et al., 2020). However, the issues of whether plant hormesis is similar/different in terms of stimulated traits' sets when it is induced by mild stressors having different specific effects and what is the contribution of hormetic stimulation of non-specific and specific adaptive mechanisms in plant resilience to strong stressors (i.e., preconditioning) remain unclear.
To this end, this paper: 1) reviews the literature concerning hormetic stimulation of non-specific and specific adaptive mechanisms in plants; 2) evaluates the importance of hormetic stimulation of non-specific and specific adaptive mechanisms for preconditioning; 3) analyses the phenomenon of hormetic trade-off for these mechanisms; and 4) considers the position of hormesis in the system of plant adaptations to the environment.
Section snippets
Non-specific adaptive mechanisms and hormesis in plants
The casual relationship between hormesis and plant stress is currently considered proven because various low-dose stressors cause hormetic stimulation of plant traits (Calabrese, 2008; Agathokleous and Calabrese, 2020). Hans Selye, 1956, Selye, 1974, the author of the Stress concept, considered stress a set of non-specific (i.e., universal) adaptive mechanisms, which are adaptive responses involved in creating resistance to any stressor. These non-specific adaptive mechanisms are due to the
Specific adaptive mechanisms and hormesis in plants
Various stress factors induce different specific disruptions (‘strains’) of plant traits (Blum, 2016), which are determined by the nature of the factor and the ‘points’ of its impact on plant metabolism. Therefore, for successful adaptation to stress factors, non-specific adaptive responses are not enough. For example, heavy metals, by disrupting the function of cellular proteins, induce biosynthesis of phytochelatins, metallothioneins, and/or organic acids in plants binding heavy metals and
Hormetic trade-off of non-specific and specific adaptive mechanisms in plants
Evolutionary trade-off is considered a situation when evolutionary adaptation is accompanied by deterioration in some traits (Bennett and Lenski, 2007). Trade-off is observed not only in the process of evolution, but also during adaptation to the environment via phenotypic plasticity, including plant hormesis (Agathokleous et al., 2019c; Agathokleous and Calabrese, 2020). In the case of hormesis, some traits/functions that are needed to prepare for coming threats may be enhanced, whereas other
Preconditioning and hormetic stimulation of non-specific and specific adaptive mechanisms in plants
Preconditioning or priming is known to be a phenomenon when low-dose factors that have a stimulating hormetic effect increase organism resilience to subsequent more severe stressors (Calabrese, 2016; Agathokleous et al., 2020e). Preconditioning can increase plant resistance to high doses of this environmental factor or to other strong impacts. The latter phenomenon is called cross-adaptation or cross-tolerance and can be caused not only by hormetic doses but also by strong stressors (Foyer et
Importance of hormetic stimulation of non-specific and specific adaptive mechanisms for plant resilience to environmental challenges
The adaptive significance of hormesis in plants is generally recognised because the hormetic overcompensation of traits is considered a preparation for the impact of strong stressors (Calabrese, 2008; Agathokleous and Calabrese, 2020). As shown above, hormetic overcompensation can be observed for both non-specific and specific adaptive mechanisms in plants. However, the position of this phenomenon in the system of plant adaptive responses has not yet been analysed in detail. Here, based on the
Conclusion
Both non-specific and specific adaptive mechanisms of plants can be stimulated hormetically by mild stressors. Therefore, hormesis caused by different stressors may have different sets of stimulated traits and create varying resilience to subsequent strong impacts. Therefore, hormesis of both non-specific and specific adaptive mechanisms is important for plant preconditioning, especially in the case of cross-tolerance. At the same time, the contribution of these stimulations to plant resistance
CRediT authorship contribution statement
Elena Erofeeva: Literature analysis, Writing of This Review.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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