Determinants of stomatal sluggishness in ozone-exposed deciduous tree species
Introduction
Tropospheric ozone (O3) is recognized as a significant phytotoxic air pollutant and greenhouse gas (Bytnerowicz et al., 2007, Serengil et al., 2011). Ozone concentrations have been increasing in the northern hemisphere since the pre-industrial age (Akimoto, 2003, Vingarzan, 2004). Especially in East Asian countries, further increases in O3 concentrations are predicted throughout this century because of rapid economic growth (Ohara et al., 2007, Yamaji et al., 2008).
The phytotoxic nature of O3 may cause adverse effects on physiological and biochemical processes in tree species (Karnosky et al., 2003, Matyssek and Sandermann, 2003, Ashmore, 2005, Paoletti, 2007). There is still little information on effects of O3 on native plant species of Asia (Royal Society, 2008). Many studies on European and North American species reported that O3 may reduce carbon assimilation, and limit the growth of trees (e.g., Wittig et al., 2007, Wittig et al., 2009). On the other hand, the effect of O3 on stomatal conductance is not straightforward (Mansfield, 1998, Paoletti and Grulke, 2005). Ozone has been reported to induce stomatal closure (Wittig et al., 2007). However, slower or less efficient stomatal control may occur, especially a weaker ability to close stomata, referred to as “O3-induced stomatal sluggishness” (Paoletti, 2005, Mills et al., 2009, Paoletti et al., 2009, Paoletti and Grulke, 2010, Hoshika et al., 2012a, Hoshika et al., 2013a, Hoshika et al., 2013b, Dumont et al., 2013). Sluggishness may occur because O3 reduces stomatal sensitivity to abscisic acid (ABA) (Mills et al., 2009). This loss of stomatal response to ABA is related to O3-induced ethylene emission (Wilkinson and Davies, 2010). Although our knowledge of the mechanism is still limited, such a reduced stomatal control may impair an efficient water use for plants (Sun et al., 2012).
Stomatal O3 flux is a crucial factor for the assessment of O3 effects, because stomata are the principal interface for entry of O3 into a leaf (Omasa et al., 2002, Karlsson et al., 2007, Mills et al., 2010). Stomatal response to environmental stimuli may be related to leaf anatomical traits such as stomatal density (e.g., Drake et al., 2013). Small stomata and their general association with high density of stomata provide the capacity for rapid response in the stomatal conductance of a leaf (Aasamaa et al., 2002, Heatherington and Woodward, 2003, Drake et al., 2013). This implies that fast response of stomata in leaves with high stomatal density and/or lower stomatal conductance during O3 exposure may result in less diffusion of O3 into a leaf, and may lead to a decrease in O3-induced injury (Pääkkönen et al., 1995).
Foliar O3 injury may also depend on the available resource for repair or biochemical O3 detoxification of a leaf (e.g., Tausz et al., 2007, Paoletti et al., 2008). Wieser et al. (2002) suggested that antioxidative capacity increased with increasing leaf mass per area (LMA). Inherent LMA may thus be roughly related to sensitivity to O3 stress (Bussotti, 2008, Zhang et al., 2012). Also Musselman and Minnick (2000) suggested that plant tolerance to O3 stress may depend on its photosynthetic capacity because detoxification and repair require energy (Noctor and Foyer, 1998). The sensitivity to foliar O3 injury may thus be explained by the ratio of stomatal O3 flux to net photosynthesis (Fredericksen et al., 1996, Kolb and Matyssek, 2001), indicating a balance between O3 exposure of mesophyll cells and availability of photosynthates for repair or detoxification.
In this study, we examined O3 effects on steady-state leaf gas exchange and dynamic stomatal response under severe water stress imposed by cutting a leaf in three tree species that are common in China. The objective of the study was to test whether the degree of O3-induced injury to stomatal control was related to stomatal density, LMA, stomatal O3 flux or the ratio of O3 flux to net photosynthesis.
Section snippets
Plant materials
We used one-year-old seedlings of Ailanthus altissima (Mill.) Swingle, Fraxinus chinensis Roxb. and Platanus orientalis L. Before bud burst, bare rooted seedlings were planted in 20 L circular plastic pots on 31 March, 2013 and grown at ambient field condition (outdoors). Pots were filled with native light loamy soil. Seedlings with similar height and basal diameter were selected for this study and pre-adapted to open-top chamber conditions for 10 days before O3 fumigation. All plants were
Leaf traits
Enhanced ozone concentrations did not affect stomatal density for any of the three species (data not shown). Average stomatal density was 211 mm− 2 in A. altissima, 116 mm− 2 in F. chinensis, and 118 mm− 2 in P. orientalis. There was no difference in LMA between O3 treatments for any species (data not shown). Average LMA was 44.9 g m− 2 in A. altissima, 53.6 g m− 2 in F. chinensis, and 40.7 g m− 2 in P. orientalis.
Steady-state leaf gas exchange and dynamic stomatal response after leaf excision
Ozone exposure induced a decline of steady-state net photosynthetic rate (Fig. 2). Lower net
Discussion
Ozone exposure caused a decrease in the steady-state values of net photosynthesis in all three species, while no difference in stomatal conductance was found (Fig. 2). This response of stomatal conductance is in contrast with a meta-analysis of physiological responses to O3 by trees (Wittig et al., 2007). Stomatal conductance is generally regulated so as to maintain the ratio of internal CO2 concentration to ambient CO2 concentration (Lambers et al., 2008). At a moderate level of chronic O3
Acknowledgments
We are grateful for financial support by a grant-in-aid from the Japanese Society for Promotion of Science (Young Scientists for research abroad) and the Hundred Talents Program, Chinese Academy of Science. We also thank Dr. Enzhu Hu from Chinese Academy of Science for the kind help in the calculation of ozone concentrations.
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