Review articleA quantitative assessment of hormetic responses of plants to ozone
Graphical abstract
Introduction
Ground-level ozone (O3) is a secondary air pollutant formed by photochemical reactions among precursors emitted by anthropogenic and natural sources such as nitrogen oxides, methane and volatile organic compounds. Annual mean background O3 concentrations were commonly 10–25 ppb in vast areas of the Northern Hemisphere prior to the mid. 20th century (Akimoto, 2003; Lelieveld and Dentener, 2000; Volz and Kley, 1988). However, these concentrations doubled by the end of the 20th century (Akimoto, 2003; Cooper et al., 2014), and the exposure of plants to O3 is projected to remain elevated for decades, even if some regions are predicted to display a decrease in the O3 levels (Sicard et al., 2017).
Seven decades of research show that elevated O3 concentrations cause adverse effects on vegetation, such as growth and productivity inhibition and yield reduction (Grantz et al., 2006; McGrath et al., 2015; Morgan et al., 2003; Osborne et al., 2016; Wang and Mauzerall, 2004; Wittig et al., 2007). Such adverse effects of O3 pollution can cause severe economic losses and threaten food supplies and biosphere sustainability (Ainsworth et al., 2012; Avnery et al., 2011; Feng and Kobayashi, 2009a; Koike et al., 2013; Matyssek et al., 2010; Oksanen et al., 2013; Osborne et al., 2016), hence, underlying a substantial need to define environmental “safe” levels of O3. Dose-response1 studies should be conducted to study O3 effects on plants and derive critical levels (CLs) for protecting vegetation (Fuhrer et al., 1997; Mills et al., 2007; Sicard et al., 2016).
Two dose-response models have dominated the biomedical and toxicological literature throughout the 20th century, the Threshold and Linear No Threshold (LNT) models (Calabrese, 2017a, 2017b; 2017c, 2009). Both models assume a linear increase of the biological response with increasing dose levels. The Threshold model assumes that damage starts increasing only after a threshold dose level below which there is no response. The LNT model assumes that damage starts increasing after a null dose (no threshold), and it has been typically applied in O3-plants dose-response studies (Fuhrer et al., 1997; Mills et al., 2011, 2007).2 The O3 CLs were developed in a period of time when it was assumed that stress biology following a linear function is the norm.
A third dose-response model, the hormetic model (Fig. 1), is built upon the assumption that low doses of stressors upregulate adaptive responses that may enhance both productivity and biological resilience, while high doses may induce inhibitory responses and/or toxicity (Luckey, 1980; Stebbing, 1982). A substantial literature published from 2000 onward confirms the occurrence of non-linear, hormetic responses with similar quantitative characteristics across biological models, response variables (i.e. endpoints), and stressor agents, supporting the assumption that hormesis is a general and fundamental phenomenon (Calabrese et al., 2015; Calabrese and Blain, 2011; Calabrese and Mattson, 2017; Costantini et al., 2010; Iavicoli et al., 2018; Kim et al., 2018; Linning and Eck, 2018; Marasco et al., 2018).
Efforts made in the last 10 years revealed the existence of non-linear, hormetic responses in plants as well. These were induced by a plethora of chemical and environmental factors in numerous plant species, with a maximum stimulatory response in the low-dose zone (MAX) commonly <200% of control response, i.e. the response to a zero/background dose (Agathokleous et al., 2018, 2019d; Belz et al., 2008; Belz and Cedergreen, 2010; Belz and Piepho, 2015, 2017; Calabrese and Blain, 2011; Cedergreen et al., 2007, 2009; Cedergreen and Olesen, 2010). Recently, a review study suggested that O3 is also among the factors that can induce non-linear, hormetic responses in plants (Agathokleous et al., 2019b). These recent findings suggest that the current estimates of O3 impacts on plants that are based on extrapolation from high to low doses may be inaccurate if plants display non-linear, hormetic responses to O3.
Although several meta-analyses assessed the adverse effects of elevated O3 on plants (Feng et al., 2019, 2018b; Feng and Kobayashi, 2009b; Grantz et al., 2006; McGrath et al., 2015; Morgan et al., 2003; Osborne et al., 2016; Wittig et al., 2007), no study evaluated quantitatively hormetic dose responses (HDRs) induced by O3 in plants. Furthermore, even though it was demonstrated that O3 can induce HDRs in plants (Agathokleous et al., 2019b), it remains unknown whether O3-induced HDRs are a general phenomenon, and, thus, important in global change biology and in deriving CLs. To fill these research gaps, we aimed at evaluating quantitatively the O3-induced HDRs in plants in the available scientific literature and at providing a perspective for improving research protocols and advancing current knowledge on O3 effects on vegetation and plant biology under O3-induced stress. To assess the generality of O3-induced hormesis, we sought to first test whether the HDRs differ among types of response variables. Previous analyses suggested that HDRs of plants are similar among response variables, however, this hypothesis has not been statistically confirmed (Agathokleous et al., 2018, 2019d; Calabrese and Blain, 2011). Moreover, adverse responses of plants to O3 differ among taxonomic groups and life forms (Wittig et al., 2007). Therefore, we also tested whether hormetic responses of plants to O3 differ among taxonomic groups and life forms. This is the first analysis of its kind for HDRs in the Biology literature. Moreover, given that semi-open exposure systems underestimate the adverse effects of elevated O3 compared to open systems (Feng et al., 2018b), we hypothesized that this may apply to the hormetic stimulation as well. We also hypothesized that O3-induced hormesis may not show a high temporal variation as it was observed with chemical compounds (Agathokleous et al., 2019d) because of stomatal closure under longer low-dose O3 exposure that will restrict the accumulated influx (McAdam et al., 2017).
Section snippets
Methodology
To assess O3-induced HDRs, a previous literature review (Agathokleous et al., 2019b) was re-evaluated for the criteria explained below and significantly extended by surveying 26 additional reports fulfilling these criteria after searching scientific databases with the keywords “ozone” and “plant” or “tree” or “seedling” or “sapling” or “cutting” and “stimulation” or “stimulatory” or “biphasic” or “bi-phasic” or “non-monotonic” or “multiphasic” or “multi-phasic” or “hormesis” or “hormetic” or
Overall assessment (across plant species and response variables)
The median MAX was 123.5% of control, similar to previous analyses of dose responses induced by lanthanum3 and human and veterinary antibiotics in plants (
A viewpoint arising from these findings
This analysis suggests that hormetic responses of plants to O3 are demonstrated when the experimental design permits its detection (e.g. narrow spacing of exposure levels). In fact, the most up-to-date Biology literature suggests that plant stress biology is biphasic, rather than monotonic/linear, and framed within a hormetic framework (Agathokleous et al., 2019e; Drzeżdżon et al., 2018; Mittler, 2017). In this context, major stress components (e.g. reactive species, hormones, leaf volatile
Conclusions
Quantitative and qualitative characteristics of O3-induced hormesis in plants are herein documented and analyzed for the first time. This first extensive analysis of HDRs induced by a gas of the Earth’s atmosphere shows that while O3-induced hormesis depends upon experimental conditions (e.g. type of exposure system and number of doses below the ZEP), it commonly does not differ extensively among taxonomic groups and life forms.
Current findings challenge the prevailing view that O3 induces
Funding
EA and ZZF acknowledge multi-year support from The Startup Foundation for Introducing Talent of Nanjing University of Information Science & Technology (NUIST), Nanjing, China. EA was an International Research Fellow (ID No: P17102) of the Japan Society for the Promotion of Science (JSPS). EA and MK acknowledge JSPS KAKENHI Grant Number JP17F17102 for support. JSPS is a non-profit, independent administrative institution. RGB acknowledges longtime support from the German Research Foundation (
Acknowledgements
This study was prepared within the unit 7.01.09 Ground-Level Ozone, 7.01 Impacts of Air Pollution and Climate Change on Forest Ecosystems, Division 7 Forest Health, International Union of Forest Research Organizations (IUFRO).
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