Plants and related carbon cycling under elevated ground-level ozone: A mini review
Introduction
As the nexus of carbon biogeochemical cycling in terrestrial ecosystems, plants play a vital role in the global carbon cycle. Green plants can absorb atmospheric carbon dioxide (CO2) through photosynthesis and therefore forests act as a large and persistent natural carbon sinks (Pan et al., 2011). Plants are also the primary way CO2 is transferred to soil through roots and litter (Felzer et al., 2005; Sitch et al., 2007; Ainsworth et al., 2012). Meanwhile, carbon backflows from vegetated lands to the atmosphere through the release of volatile organics from leaves (Guenther et al., 1993, 2012) and the release of CO2 from the decomposition of soil organic matter and litter (Krishna and Mohan, 2017; Chen and Chen, 2018). Since climate and environmental conditions impact heavily on the physiology of plants, there is a growing concern about the disturbance of carbon cycling, crop yields, and biodiversity by global warming and changing atmospheric compositions (Ainsworth et al., 2008; Bonan, 2008; Wilkinson et al., 2012; Agathokleous and Saitanis, 2020a; Feng et al., 2015, 2019, 2021, 2022; Chaudhry and Sidhu, 2022). Apart from elevated levels of CO2, atmospheric oxidation capacity is also an emerging factor that significantly influences plants and related issues, such as forest net primary productivity (NPP) and carbon storage (King et al., 2005; Ren et al., 2011; Ainsworth et al., 2012; Chapin and Eviner, 2014; Fuhrer et al., 2016; Yue et al., 2017; Lefohn et al., 2018; Xia et al., 2021).
Ozone (O3) and its two photodissociation products, hydroxyl radical (OH) and hydrogen peroxide (H2O2), are the principal oxidants in the lower atmosphere (Finlayson-Pitts and Pitts, 2000). In recent centuries, especially since the 1950s, vast amounts of ozone-precursor trace gases (e.g., nitrogen oxides, nonmethane hydrocarbons, methane and carbon monoxide) have been released into the atmosphere from human activities (McDuffie et al., 2020), resulting in elevated levels of ambient ozone on global or regional scales (Mills et al., 2018). Ground-level ozone is produced mainly from the complex photochemical reactions of volatile organic compounds (VOCs) and nitrogen oxides (NOx) in the presence of solar irradiation (NRC, 1991; Finlayson-Pitts et al., 1993). As a major component of photochemical smog, ozone has become an air pollution problem in succession from developed to developing worlds (Monks et al., 2015; Schultz et al., 2017; Archibald et al., 2020; Gao et al., 2020). Ozone is also an important greenhouse gas contributing to radiative forcing (IPCC, 2013). There is accumulating evidence that ozone increases significantly not only in populated areas (Lu et al., 2018; Mills et al., 2018; Li et al., 2019; Gao et al., 2020; Sicard, 2021; Wang et al., 2021) but also in background regions with relatively high vegetation coverage (Akimoto, 2003; Cooper et al., 2014; Wang et al., 2017, 2019; Xu et al., 2020; Sicard, 2021). Tropospheric ozone concentrations increased at a rate of 1–5 ppb per decade by the end of the 20th century and are predicted to exceed 80 ppb by the end of this century (Thompson, 1992; Vingarzan, 2004; Sitch et al., 2007; Verstraeten et al., 2015), doubling its current concentrations of 30–40 ppb (Fleming et al., 2018).
As ozone is a strong atmospheric oxidant, elevated ground-level ozone would harm plant growth and human health (Ainsworth, 2017; Wang et al., 2007; Lefohn et al., 2018; Liu et al., 2018; Pleijel et al., 2018; Feng et al., 2022). Extensive studies are available about the impacts of ozone on plant physiology and crop yields (Ashmore, 2005; Häikiö et al., 2007; Velikova et al., 2005b; Agathokleous et al., 2015; Yuan et al., 2017b; Ainsworth et al., 2019), but few focus on plants and carbon cycling with increasing ozone levels. In this review, we put our focus on the influence of increasing atmospheric ozone on plant-related carbon geochemical cycling processes, including assimilation of atmospheric CO2 by plant leaves, emissions of volatiles from plant leaves, carbon transfer to root and soil, soil microbial activity and decomposition of organics, as well as the decay of litter (Fig. 1).
Section snippets
Elevated ozone and CO2 assimilation
The capacity of the terrestrial biosphere to sequester carbon is governed by the ability of vegetation to capture CO2 (Oliver et al., 2018). Plants respond to elevated ozone by various physiological mechanisms, ultimately reducing carbon assimilation and changing carbon allocation (Felzer et al., 2007). The injuries to plants caused by elevated ozone can be visible and physiological. Visible injury generally refers to changes in pigmentation or bronzing, fleck, stippling chlorosis, and
Elevated ozone and volatile emissions
Trees emit a large quantity and variety of terpenoids, including isoprene, monoterpenes, and sesquiterpenes (Peñuelas and Llusià, 2001; Laothawornkitkul et al., 2009; Pellegrini et al., 2018). Typically, broad-leaved forests mainly emit isoprene, while coniferous forests mainly emit monoterpenes (Guenther et al., 1993). These compounds play important roles in atmospheric chemistry and in plant biology and ecology (Laothawornkitkul et al., 2009). However, increased ozone affects the global
Elevated ozone and soil carbon
The plant carbon pool is an important part that connects the atmospheric carbon pool and soil carbon pool. Approximately 35–80% of the carbon fixed by plant photosynthesis is allocated to the underground ecosystem to maintain the continuous growth, death and renewal of the roots (Ryan and Law, 2005; Haverd et al., 2016). The carbon fixed through the plant by photosynthesis will be transferred into the soil carbon pool through the decomposition of roots and foliar litter. The soil-derived
Elevated ozone and litter decomposition
Plant litter decomposition is another critical biogeochemical process that controls soil carbon dynamics in terrestrial ecosystems (Aragão et al., 2009; Beer et al., 2010). It sustains ecosystem productivity, and decomposition products enter the atmosphere in the form of CO2 and enter the soil in the form of organic carbon (Chen et al., 2019). Elevated ozone alters plant carbon and nutrient distribution patterns, accelerates leaf senescence, and thereby changes the quantity and quality of
Perspectives
Plants play a crucial role in the land-atmosphere interactions. The influence of human activities on the vegetation carbon pool comes not only from land-use changes, but also from climate and environmental changes. It is essential to assess plants’ carbon sinks in a dynamic way under changing atmospheric compositions (e.g. CO2 and oxidants) to achieve carbon neutrality goals. Although great efforts have been made to investigate the potential effects of elevated ozone on NPP and carbon storage
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.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Nos. 42022023 and 41961144029), the Chinese Academy of Sciences (Nos. XDA23010303, XDPB1901, XDA23020301 and QYZDJ-SSW-DQC032), the Youth Innovation Promotion Association of the Chinese Academy of Sciences (Y2021096), the Hong Kong Research Grants Council (No. T24-504/17-N), and the Department of Science and Technology of Guangdong (Nos. 2020B1111360001 and 2020B1212060053).
Dr. Yanli Zhang is a professor in the State Key Laboratory of Organic Geochemistry at Guangzhou Institute of Geochemistry (GIG), Chinese Academy of Sciences (CAS). She got her Ph.D. degree at GIG in 2013 and then joined GIG as a research staff. She worked at the Hong Kong University of Science and Technology from 2017 to 2019 as a ‘Hong Kong Scholar’. Her research interests are trace-level reactive organic gases (ROG) that directly and indirectly impact global and regional climate change, air
References (197)
- et al.
Plant susceptibility to ozone: a tower of Babel?
Sci. Total Environ.
(2020) - et al.
Tropospheric ozone effects on chemical composition and decomposition rate of Quercus ilex L. leaves
Sci. Total Environ.
(2011) Role of Biogenic Volatile Organic Compounds (BVOC) emitted by urban trees on ozone concentration in cities: a review
Environ. Pollut.
(2013)- et al.
BVOC responses to realistic nitrogen fertilization and ozone exposure in silver birch
Environ. Pollut.
(2016) - et al.
10.6 - biogeochemical interactions governing terrestrial net primary production
- et al.
Ozone visible symptoms and reduced root biomass in the subalpine species Pinus uncinata after two years of free-air ozone fumigation
Environ. Pollut.
(2012) - et al.
Impacts of ozone on trees and crops
Compt. Rendus Geosci.
(2007) A stomatal ozone flux-response relationship to assess ozone-induced yield loss of winter wheat in subtropical China
Environ. Pollut.
(2012)- et al.
Ground-level O3 pollution and its impacts on food crops in China: a review
Environ. Pollut.
(2015) - et al.
Chapter 4 - photochemistry of important atmospheric species
A flux-based assessment of above and below ground biomass of Holm oak (Quercus ilex L.) seedlings after one season of exposure to high ozone concentrations
Atmos. Environ.
Herbivore-induced BVOC emissions of Scots pine under warming, elevated ozone and increased nitrogen availability in an open-field exposure
Agric. For. Meteorol.
Terpenoids as plant antioxidants
Microbiota and host nutrition across plant and animal kingdoms
Cell Host Microbe
The role of polyphenols in terrestrial ecosystem nutrient cycling
Trends Ecol. Evol.
The FACE program
Agric. For. Meteorol.
Ozone-induced stomatal sluggishness develops progressively in Siebold's beech (Fagus crenata)
Environ. Pollut.
Impact of elevated tropospheric ozone on soil C, N and microbial dynamics of winter wheat
Agric. Ecosyst. Environ.
Differential regulation of volatile emission from Eucalyptus globulus leaves upon single and combined ozone and wounding treatments through recovery and relationships with ozone uptake
Environ. Exp. Bot.
Impact of ozone on the growth of birch (Betula pendula) saplings
Environ. Pollut.
The effects of ozone on the root dynamics of seedlings and mature red oak (Quercus rubra L)
For. Ecol. Manag.
Sensitivity of Norway spruce physiology and terpenoid emission dynamics to elevated ozone and elevated temperature under open-field exposure
Environ. Exp. Bot.
The effect of ozone fumigation on the biogenic volatile organic compounds (BVOCs) emitted from Brassica napus above- and below-ground
PLoS One
Natural abundance carbon isotope composition of isoprene reflects incomplete coupling between isoprene synthesis and photosynthetic carbon flow
Plant Physiol.
Tropospheric O3, the nightmare of wild plants: a review study
J. Agric. Meteorol.
A review study on past 40 Years of research on effects of tropospheric O3 on belowground structure, functioning, and processes of trees: a linkage with potential ecological implications
Water, Air, Soil Pollut.
Ozone affects plant, insect, and soil microbial communities: a threat to terrestrial ecosystems and biodiversity
Sci. Adv.
Targets for crop biotechnology in a future high-CO2 and high-O3 world
Plant Physiol.
The effects of tropospheric ozone on net primary productivity and implications for climate change
Understanding and improving global crop response to ozone pollution
Plant J.
The influence of rising tropospheric carbon dioxide and ozone on plant productivity
Plant Biol.
Global air quality and pollution
Science
Source-sink balance and carbon allocation below ground in plants exposed to ozone
New Phytol.
Above- and below-ground net primary productivity across ten Amazonian forests on contrasting soils
Biogeosciences
Tropospheric Ozone Assessment Report: a critical review of changes in the tropospheric ozone burden and budget from 1850 to 2100
Elementa: Sci. Anthrop.
Assessing the future global impacts of ozone on vegetation
Plant Cell Environ.
Ozone fumigation of Quercus ilex L. slows down leaf litter decomposition with no detectable change in leaf composition
Ann. For. Sci.
Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate
Science
RNAi-mediated suppression of isoprene biosynthesis in hybrid poplar impacts ozone tolerance
Tree Physiol.
Impact of tropospheric ozone on terrestrial biodiversity: a literature analysis to identify ozone sensitive taxa
J. Appl. Bot. Food Qual.
Isotope ratio-based quantification of carbon assimilation highlights the role of plastidial isoprenoid precursor availability in photosynthesis
Plant Methods
Effects of chronic elevated ozone concentration on antioxidant capacity, photosynthesis and seed yield of 10 soybean cultivars
Plant Cell Environ.
Emission of herbivore-induced volatile terpenoids from two hybrid aspen (Populus tremula × tremuloides) clones under ambient and elevated ozone concentrations in the field
Global Change Biol.
Forests and climate change: forcings, feedbacks, and the climate benefits of forests
Science
Decomposition of soybean grown under elevated concentrations of CO2 and O3
Global Change Biol.
Natural variation in ozone sensitivity among Arabidopsis thaliana accessions and its relation to stomatal conductance
Plant Cell Environ.
Does ozone exposure affect herbivore-induced plant volatile emissions differently in wild and cultivated plants?
Environ. Sci. Pollut. Control Ser.
Carbon allocation and carbon isotope fluxes in the plant-soil-atmosphere continuum: a review
Biogeosciences
Isoprene emission rates under elevated CO2 and O3 in two field-grown aspen clones differing in their sensitivity to O3
New Phytol.
A mechanism for biogenic production and emission of MEK from MVK decoupled from isoprene biosynthesis
Atmos. Chem. Phys.
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Dr. Yanli Zhang is a professor in the State Key Laboratory of Organic Geochemistry at Guangzhou Institute of Geochemistry (GIG), Chinese Academy of Sciences (CAS). She got her Ph.D. degree at GIG in 2013 and then joined GIG as a research staff. She worked at the Hong Kong University of Science and Technology from 2017 to 2019 as a ‘Hong Kong Scholar’. Her research interests are trace-level reactive organic gases (ROG) that directly and indirectly impact global and regional climate change, air quality, and ecosystem/human health. She is an Emerging Investigator of Applied Geochemistry/International Association of Geochemistry, recipient of NSFC Excellent Young Scientists Fund, a member of the Expert Group on China's Implementation of the Montreal Protocol on Ozone Depleting Substances, and an outstanding member of CAS Youth Innovation Promotion Association (YIPA).