Elsevier

Applied Geochemistry

Volume 144, September 2022, 105400
Applied Geochemistry

Plants and related carbon cycling under elevated ground-level ozone: A mini review

https://doi.org/10.1016/j.apgeochem.2022.105400Get rights and content

Highlights

  • The effects of elevated ozone on plant-related carbon cycling processes are summarized.

  • In situ long-term observations under natural growing conditions are needed.

  • Feedbacks of plants to atmospheric oxidants should be considered in ozone-plant interactions.

Abstract

Plants play a crucial role in global carbon biogeochemical cycling and natural terrestrial carbon sinks. Dynamic changes in plant-related carbon cycling processes under changing climate and atmospheric compositions are hot scientific issues concerning carbon neutrality. Ozone, as a damaging oxidant, shows a rising trend near the ground where plants grow, directly and indirectly impacting forests and other types of vegetation. This review focuses on the effects of elevated atmospheric ozone levels on plant-related carbon cycling processes, including carbon dioxide (CO2) assimilation, carbon allocation to roots, volatile emissions, soil carbon sequestration and litter decomposition. Based on previous studies, we propose that field observations, especially in situ long-term observations under natural growing conditions in well-designed networks with a better representation, are needed to deeply understand the effects of elevated ozone on plants. Apart from an overwhelming concern about the influence of ozone on crop yields, studies on the effects of elevated ozone on forests, especially tropical and subtropical forests, should be strengthened in the future. Meanwhile, the interactions between ozone and plants should be considered in understanding plants’ feedback to oxidants through emissions of volatiles and other trace gases. Moreover, geochemical techniques such as carbon isotopes and molecular markers, along with big data and artificial intelligence approaches, can be extensively used to decode and constrain the ozone-plant relationships, such as those between net primary productivity and ozone.

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

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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).

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