Functional traits of poplar leaves and fine roots responses to ozone pollution under soil nitrogen addition

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Abstract

Concurrent ground-level ozone (O3) pollution and anthropogenic nitrogen (N) deposition can markedly influence dynamics and productivity in forests. Most studies evaluating the functional traits responses of rapid-turnover organs to O3 have specifically examined leaves, despite fine roots are another major source of soil carbon and nutrient input in forest ecosystems. How elevated O3 levels impact fine root biomass and biochemistry remains to be resolved. This study was to assess poplar leaf and fine root biomass and biochemistry responses to five different levels of O3 pollution, while additionally examining whether four levels of soil N supplementation were sufficient to alter the impact of O3 on these two organs. Elevated O3 resulted in a more substantial reduction in fine root biomass than leaf biomass; relative to leaves, more biochemically-resistant components were present within fine root litter, which contained high concentrations of lignin, condensed tannins, and elevated C:N and lignin: N ratios that were associated with slower rates of litter decomposition. In contrast, leaves contained more labile components, including nonstructural carbohydrates and N, as well as a higher N:P ratio. Elevated O3 significantly reduced labile components and increased biochemically-resistant components in leaves, whereas they had minimal impact on fine root biochemistry. This suggests that O3 pollution has the potential to delay leaf litter decomposition and associated nutrient cycling. N addition largely failed to affect the impact of elevated O3 levels on leaves or fine root chemistry, suggesting that soil N supplementation is not a suitable approach to combating the impact of O3 pollution on key functional traits of poplars. These results indicate that the significant differences in the responses of leaves and fine roots to O3 pollution will result in marked changes in the relative belowground roles of these two litter sources within forest ecosystems, and such changes will independently of nitrogen load.

Introduction

Ground-level ozone (O3) is a major air pollutant that has well-documented adverse effects on global vegetation and ecosystem productivity (Mills al., 2018; Sicard et al., 2017). While there have been concerted legislative effects to minimize O3 precursor emissions, O3 pollution remains a persistent environmental hazard in China and many other regions of the globe (Feng et al., 2015; Lefohn et al., 2017; Verstraeten et al., 2015; Zeng et al., 2019). Recent research indicates that vegetation in China is exposed to significantly higher levels of O3 as compared to vegetation in other industrialized regions including Japan, Europe, and the United States (Lu et al., 2018b), with total O3-induced annual forest tree biomass losses in China reaching up to 11%−13% (Feng et al., 2019a). Six key ecological restoration projects have been launched in China since the 1970s including efforts to enhance C sinks via promoting reforestation and afforestation (Lu et al., 2018a), making the protection of these Chinese forest ecosystems from O3 pollution an increasingly important concern.

Nutrient and soil carbon (C) cycling in terrestrial ecosystems is significantly influenced by plant rapid-turnover organs (i.e., leaves and fine roots), with the quantity and quality of these organs being a main determinant of forest growth and productivity (Aneja et al., 2007; Berg and McClaugherty, 2014). Ozone pollution can result in significant reductions in above- and belowground plant production while also alter litter chemical quality in forest soils (Kainulainen et al., 2003; Li et al., 2019; Liu et al., 2005, 2007; Shang et al., 2017), thus potentially change the substrates that are available to support the microbial metabolism within the soils. These changes can in turn result in substantial changes in nutrient dynamics and soil organic C formation such that the strength of forest ecosystem C sinks may be compromised by O3 pollution (Andersen, 2003). In order to fully understand how O3 pollution impacts C and nutrient cycling within terrestrial ecosystems, it is therefore essential that the functional traits of these rapid-turnover organs be studied in the context of such pollution (Liu et al., 2005, 2009).

Most mechanistic studies of forest dynamic responses to O3 exposure have focused specifically on leaves (Fu et al., 2018; Kainulainen et al., 2003; Liu et al., 2005, 2007, 2009; Parsons et al., 2004), despite the fact that fine root litter accounts for ~48% of the annual plant litter produced in many forest ecosystems (Freschet et al., 2013; Xia et al., 2015). Indeed, roughly 33% of net primary productivity is transferred to the soil via the turnover of fine roots in terrestrial ecosystems, and in certain forest ecosystems this percentage can rise as high as 75% (Gill and Jackson, 2000). Even though it is essential to the integrity of forest ecosystems, little is known regarding how O3 pollution impacts fine roots quantity and chemical quality. Given that O3 is difficult to penetrate the soil, it is just able to modulate root biology through changes in photosynthesis sink allocation and root activity. However, fine roots can rapidly respond to elevated O3 levels, doing so more quickly than aboveground responses are detectable in some instances (Li et al., 2019; Shang et al., 2017). Studying the belowground effects of O3 may therefore be informative as well as assessing aboveground changes as a means of understanding the long-term impact of such pollution on forest ecosystems (Andersen, 2003; Li et al., 2020a). Litterbag and isotopic tracer studies have also revealed that fine roots, which contain condensed tannins and lignin, have a more biochemically-resistant composition than leaves, which contain high levels of nonstructural carbohydrates, simple phenolics, and other readily degraded substrates (See et al., 2019; Sun et al., 2018; Xia et al., 2015, 2017). As such, we hypothesized that the biomass and chemical traits of leaves and fine roots would respond differently to an O3 concentration gradient because of the distinct physiological functions of these fast-turnover organs.

In Chinese forests, trees are often simultaneously exposed to O3 pollution and nitrogen (N)-enriched conditions (Li et al., 2018, 2019; Yu et al., 2019; Zeng et al., 2019). There is some experimental evidence indicating that N fertilization can buffer plants against O3-dependent biomass and growth suppression (Yendrek et al., 2013). These buffering effects, however, are dependent upon a number of factors including the magnitude of N fertilization, the O3 exposure, species-specific sensitivities to these treatments, and the plant tissues affected by these treatments (Feng et al., 2019c; Li et al., 2019; Yamaguchi et al., 2007). In one study, Jones et al. (2010) found that N addition altered O3-mediated senescence thresholds in aboveground plant tissues without impacting such thresholds in belowground tissues. Similarly, Mills et al. (2016) determined that N addition achieved sustained benefits to aboveground biomass with increasing O3 exposure, whereas N-mediated beneficial effects on root biomass were lost at high O3 concentrations and the impacts of rising O3 levels root biomass became more pronounced as N increased. Given that N addition evidently has a differential impact of leaf and fine root responses to O3, the secondary aim of the present study was to evaluate whether N input would alter the chemical responses of these two different organs to O3 exposure.

The differences in how leaves and fine roots respond to N addition may be a consequence of differences in N doses that are below or above the maximal levels necessary for optimal plant growth or may be due to differing degrees of O3-induced injury that may exceed the detoxification and repair abilities of belowground but not aboveground tissues (Agathokleous et al., 2019). Leaves are the primary site of O3 action whereas fine roots are the primary site of N action, but leaf traits are more sensitive to N than fine roots (Li et al., 2015) while fine roots exhibit greater O3 sensitivity than leaves (Li et al., 2019). Recent research evidence has demonstrated that many biotic and abiotic stressors including drought, heat, O3, phytophagous insects, and N input induce biphasic adaptive responses to low- and high-dose stimulation in a range of plants (Agathokleous et al., 2019). There may thus be a tipping point at which the protective effects of N cease to be dominant and O3-induced damage is instead aggravated in plants exposed to both of these environmental inputs. This study thus also sought to determine whether leaves and fine root traits exhibit non-linear, biphasic responses to a range of O3 concentrations and N input levels. Poplar grow rapidly, are highly sensitive to O3 (Feng et al., 2019b), exhibit high N demands, and are widely used in ecological restoration projects in Northern China (Lu et al., 2018a). The results of the present study have the potential to guide better poplar plantations management in O3-polluted and N-enriched environments.

Section snippets

Experimental site and plant material

This study was conducted at Yanqing field and experimental base (40°47′N, 116°34′E, elevation 485 m a.s.l.), northwest of Beijing. This site is characterized by a temperate and semi-humid continental monsoon climate, with an annual mean temperature of 9°C and an annual mean precipitation of 400–500 mm. Root cuttings of the hybrid poplar clone ‘107' (Populus euramericana cv. ‘74/76') were grown in round 20 L plastic pots containing a mixture of local light loamy farmland soils and planting

Biomass

Both the relative biomass of leaves and fine roots declined linearly with AOT40 at all tested N levels, with no significant differences in slope values among these four N levels (P > 0.05, ANCOVA, Fig. 1). Linear decreases in leaf biomass (−0.2%) and fine root biomass (−0.6%) per μmol/(mol•hr) of AOT40 were observed for all tested N treatments (Fig. 1).

Biochemical traits

Tissue type (leaves vs. fine roots) was associated with greater biochemical variability than either elevated O3 levels or N addition. Non-metric

Responses of leaves and fine roots to ozone

As O3 pollution levels in China pose a serious risk to forest ecosystems, many studies to date have sought to gauge the environmental impact of such pollution (Feng et al., 2019a; Li et al., 2018). While most prior studies have examined the impact of elevated O3 on leaves, this study is the first to our knowledge to have assessed how high O3 concentrations impact fine root biochemistry. Relative to leaves, we found that fine roots exhibited higher C:N, lignin:N ratios, and lignin and CT

Conclusions

By exposing poplars to five O3 concentrations and four levels of N supplementation, we found that leaves and fine roots exhibit distinct biochemical responses to elevated O3. In general, fine root biochemistry was not as sensitive to O3 levels as compared to leaves. Higher O3 concentrations were associated with poorer leaf quality, with reductions in N concentrations and TNC therein that coincided with increases in lignin concentrations, lignin:N ratios, and C:N ratios. Soil N addition did not

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Nos. 31870458, 41675153) and the National Key Research and Development Program of China (No. 2017YFE0127700). The authors would like to thank Dr. Zhengzhen Li for kindly providing us with chemical analysis guidance and thank all the reviewers who participated in the review and MJEditor (www.mjeditor.com) for its linguistic assistance during the preparation of this manuscript.

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