Elsevier

Environmental Research

Volume 176, September 2019, 108527
Environmental Research

Review article
A quantitative assessment of hormetic responses of plants to ozone

https://doi.org/10.1016/j.envres.2019.108527Get rights and content

Abstract

Evaluations of ozone effects on vegetation across the globe over the last seven decades have mostly incorporated exposure levels that were multi-fold the preindustrial concentrations. As such, global risk assessments and derivation of critical levels for protecting plants and food supplies were based on extrapolation from high to low exposure levels. These were developed in an era when it was thought that stress biology is framed around a linear dose-response. However, it has recently emerged that stress biology commonly displays non-linear, hormetic processes. The current biological understanding highlights that the strategy of extrapolating from high to low exposure levels may lead to biased estimates. Here, we analyzed a diverse sample of published empirical data of approximately 500 stimulatory, hormetic-like dose-responses induced by ozone in plants. The median value of the maximum stimulatory responses induced by elevated ozone was 124%, and commonly <150%, of the background response (control), independently of species and response variable. The maximum stimulatory response to ozone was similar among types of response variables and major plant species. It was also similar among clades, between herbaceous and woody plants, between deciduous and evergreen trees, and between annual and perennial herbaceous plants. There were modest differences in the stimulatory response between genera and between families which may reflect different experimental designs and conditions among studies. The responses varied significantly upon type of exposure system, with open-top chambers (OTCs) underestimating the maximum stimulatory response compared to free-air ozone-concentration enrichment (FACE) systems. These findings suggest that plants show a generalized hormetic stimulation by ozone which is constrained within certain limits of biological plasticity, being highly generalizable, evolutionarily based, and maintained over ecological scales. They further highlight that non-linear responses should be taken into account when assessing the ozone effects on plants.

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).

References (85)

  • E.J. Calabrese et al.

    The occurrence of hormetic dose responses in the toxicological literature, the hormesis database: An overview

    Toxicol. Appl. Pharmacol.

    (2005)
  • E.J. Calabrese et al.

    Hormesis and plant biology

    Environ. Pollut.

    (2009)
  • E.J. Calabrese et al.

    The hormesis database: The occurrence of hormetic dose responses in the toxicological literature

    Regul. Toxicol. Pharmacol.

    (2011)
  • E.J. Calabrese et al.

    Estimating the range of the maximum hormetic stimulatory response

    Environ. Res.

    (2019)
  • N. Cedergreen et al.

    Can glyphosate stimulate photosynthesis?

    Pestic. Biochem. Physiol.

    (2010)
  • N. Cedergreen et al.

    Chemical stress can increase crop yield

    Field Crop. Res.

    (2009)
  • A. Chappelka et al.

    Evaluation of ozone injury on foliage of black cherry (Prunus serotina) and tall milkweed (Asclepias exaltata) in Great Smoky Mountains National Park

    Environ. Pollut.

    (1997)
  • A. Christou et al.

    Can the pharmaceutically active compounds released in agroecosystems be considered as emerging plant stressors?

    Environ. Int.

    (2018)
  • J. Drzeżdżon et al.

    The impact of environmental contamination on the generation of reactive oxygen and nitrogen species – Consequences for plants and humans

    Environ. Int.

    (2018)
  • Z. Feng et al.

    Assessing the impacts of current and future concentrations of surface ozone on crop yield with meta-analysis

    Atmos. Environ.

    (2009)
  • Z. Feng et al.

    Assessing the impacts of current and future concentrations of surface ozone on crop yield with meta-analysis

    Atmos. Environ.

    (2009)
  • Z. Feng et al.

    Current ambient and elevated ozone effects on poplar: A global meta-analysis and response relationships

    Sci. Total Environ.

    (2019)
  • J. Fuhrer et al.

    Critical levels for ozone effects on vegetation in Europe

    Environ. Pollut.

    (1997)
  • J. Gressel et al.

    Commentary: Hormesis can be used in enhancing plant productivity and health; but not as previously envisaged

    Plant Sci.

    (2013)
  • S.-A. Kim et al.

    Evolutionarily adapted hormesis-inducing stressors can be a practical solution to mitigate harmful effects of chronic exposure to low dose chemical mixtures

    Environ. Pollut.

    (2018)
  • T. Koike et al.

    Chapter 17 – Effects of ozone on forest ecosystems in East and Southeast Asia

  • R. Matyssek et al.

    Advances in understanding ozone impact on forest trees: Messages from novel phytotron and free-air fumigation studies

    Environ. Pollut.

    (2010)
  • G. Mills et al.

    A synthesis of AOT40-based response functions and critical levels of ozone for agricultural and horticultural crops

    Atmos. Environ.

    (2007)
  • G. Mills et al.

    New stomatal flux-based critical levels for ozone effects on vegetation

    Atmos. Environ.

    (2011)
  • R. Mittler

    ROS are good

    Trends Plant Sci.

    (2017)
  • B.B. Moura et al.

    Ozone phytotoxic potential with regard to fragments of the Atlantic semi-deciduous forest downwind of Sao Paulo, Brazil

    Environ. Pollut.

    (2014)
  • S. Nussbaum et al.

    Difference in ozone uptake in grassland species between open-top chambers and ambient air

    Environ. Pollut.

    (2000)
  • E. Oksanen et al.

    Impacts of increasing ozone on Indian plants

    Environ. Pollut.

    (2013)
  • A.K. Pandey et al.

    Searching for common responsive parameters for ozone tolerance in 18 rice cultivars in India: Results from ethylenediurea studies

    Sci. Total Environ.

    (2015)
  • A.K. Pandey et al.

    High variation in resource allocation strategies among 11 Indian wheat (Triticum aestivum) cultivars growing in high ozone environment

    Climate

    (2019)
  • E. Paoletti et al.

    A new-generation 3D ozone FACE (free air controlled exposure)

    Sci. Total Environ.

    (2017)
  • K. Piikki et al.

    The open-top chamber impact on vapour pressure deficit and its consequences for stomatal ozone uptake

    Atmos. Environ.

    (2008)
  • C. Poschenrieder et al.

    Do toxic ions induce hormesis in plants?

    Plant Sci.

    (2013)
  • P. Sicard et al.

    An epidemiological assessment of stomatal ozone flux-based critical levels for visible ozone injury in Southern European forests

    Sci. Total Environ.

    (2016)
  • A.R.D. Stebbing

    Hormesis — The stimulation of growth by low levels of inhibitors

    Sci. Total Environ.

    (1982)
  • X. Wang et al.

    Characterizing distributions of surface ozone and its impact on grain production in China, Japan and South Korea: 1990 and 2020

    Atmos. Environ.

    (2004)
  • G. Adaros et al.

    Impact of ozone on growth and yield parameters of two spring wheat cultivars (Triticum aestivum L.)

    J. Plant Dis. Prot.

    (1991)
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