Amongst air pollutants, tropospheric ozone (O3) is potentially the most detrimental to forest trees (Matyssek & Sandermann, 2003). Its negative effects depend on the amount of O3 entering the leaves (Guderian et al., 1985; Runeckles, 1991; Heath, 1994; Polle, 1998) and on the presence and efficiency of defense mechanisms available inside the tissue (Runeckles & Vaartnou, 1997; Polle, 1998). Trees respond to O3 stress through mechanisms of avoidance and defense (i.e. stress tolerance; Hogsett & Andersen, 1998) such as restriction of O3 uptake by stomatal closure and metabolic detoxification in the leaf, respectively. Similar considerations have been discussed in relation to the effects of sulfur dioxide on vegetation (for a review, see Winner et al., 1985). Recently, based on chamber and field experiments with seedlings and mature trees, respectively, Wieser et al. (2002) reported that the extent of O3-induced injury can be related to the amount of available antioxidants vs stomatal flux or uptake. Similarly, a conceptual model presented by Massman et al. (2000) and Musselman et al. (2006) suggests that it is the balance between stomatal O3 uptake and apoplastic detoxification that initiates, upon metabolic signaling of oxidative stress, further metabolic processes in leaves which control injury expression vs stimulation of defense.
Detoxification can be constitutive or inducible. Constitutive detoxification is already operative in the apoplast and symplast when O3 enters the leaf (Heath, 1994). Upon influx through the stomata, O3 (and its derivatives) reacts with the antioxidants in the apoplast and induces the production of reactive oxygen species (ROS). As a first line of defense, the ‘density’ of reduced ascorbate in the apoplast determines the amount of ROS which can reach the plasmalemma, where ROS will initiate stress signalling and will set the metabolism ‘on alert’. Thereafter, self-amplification of the oxidative stress (‘oxidative burst’), which can repeatedly occur even after the primary O3 impact, represents a component of the intrinsic redox system of the plant and may induce a wide range of metabolic changes (Sandermann, 1996; Kangasjärvi et al., 2005; Nunn et al., 2005) and responses to various oxidative stressors (Sandermann, 1996, 2004; Matyssek et al., 2006). Hence, the plant ‘manages’ its performance under oxidative stress, in particular O3 stress, through the internal regulatory redox mechanisms.
Under chronic O3 exposure, the carbon gain may progressively decline with cumulative O3 uptake (Fig. 1). Such a decline may be attributed to enhanced dark respiration, indicating stimulated metabolic activity, as a consequence of increased demands for maintenance and repair processes (Dizengremel, 2001), as well as for the maintenance of the pool of reduced ascorbate in both the apoplast and the symplast (Matyssek & Sandermann, 2003).
In addition, O3-induced reduction of net photosynthesis causes depletion of starch, glucose and fructose (also draining reserve storage; Einig et al., 1997; Landolt et al., 1997; Blumenröther et al., in press), suggesting that energy supply to counteract the impact of O3 gradually becomes limiting under chronic O3 stress. In parallel with the exhaustion of constitutive defense, inducible defense mechanisms became stimulated (Fig. 1).
O3-induced detoxification processes require energy for the regeneration and de novo synthesis of antioxidants and other related chemical compounds (cf. Smirnoff & Pallanca, 1996). Although there is evidence that under exposure to low O3 concentrations CO2 assimilation and stomatal conductance initially may increase (Havranek et al., 1990; Le Thiec et al., 1994; Dixon et al., 1998), on a long-term scale carbon gain and carbohydrate accumulation typically decrease in parallel with the increase in antioxidants (Kronfußet al., 1998; Wieser et al., 1998). As a consequence, we postulate O3-induced injury to occur when the costs of building up defense compounds exceed the supply of assimilate (i.e. energy) resources. Thus, at a critical level of cumulative O3 uptake, the antioxidative defense system becomes overwhelmed. This is similar to what is known about defense against metabolic poisoning in the liver in animals, where, as in plants, ascorbate as well as glutathione is involved in detoxification (and oxidative toxins such as alcohol may induce liver cancer; McKillop & Schrum, 2005). If toxins are not detoxified they may cause, both in animals and in plants, injury and – in the worst case – irreversible destruction.
We conclude that there is a need to consider both uptake and defense processes in O3 risk assessment, when focusing on the effects of an oxidative air pollutant such as ozone. Given this need, a ‘phytomedical’ perspective is mandatory for risk assessment in plants – analogous to the rationale used in the medical sciences in animals and humans. A mechanistic understanding of the ‘effective O3 dose’, i.e. the O3 dose at the primary site of impact (http://medical-dictionary.thefreedictionary.com), and the subsequently evoked responsiveness, integrating O3 uptake and defense processes, needs to be promoted in evaluating plant performance under chronic O3 stress. It should prove rewarding to include estimates of detoxification and plant susceptibility in definitions of air quality standards in the light of plant protection against ozone.
From this perspective it is clear that O3 risk assessment on the physiologically effective O3 dose (or the dose of the oxidative derivatives of ozone).