Plant responses to UV‐B: time to look beyond stratospheric ozone depletion?

The response of terrestrial plants to UV-B radiation has been an active subject of research by plant scientists for little more than 30 years. Research during these past three decades has been driven largely by concern over stratospheric ozone depletion and the resultant increase in irradiances of UV-B at the earth's surface. Research assessing the possible consequences of ozone depletion has greatly increased our understanding of how UV-B affects plants. However, the focus of UV-B research on ozone depletion may also have distracted attention from UV-B as a component of the ‘ambient’ light environment. Plant responses to UV-B above ambient, such as would result from ozone depletion, have rarely been assessed in the broader context of the possible effects of variation in UV-B within the ambient range. In their study of the UV-B responses of silver birch (Betula pendula), de la Rosa et al. (see pp. 121–131 in this issue) used a range of integrated daily UV-Bplant doses between 1.6 and 13.0 kJ m−2 d−1 (in biological research, UV-B is always ‘weighted’ to take account of the increase in biological activity with decreasing wavelength: UV-Bplant is weighted according to the wavelength sensitivity of plant responses). The highest dose used is equivalent to a 55% ozone depletion coinciding with the summer maximum in solar radiation. Given the reduced emissions of ozone-depleting substances following the implementation of the Montreal protocol, such extreme events are now beyond the worst ozone loss predicted for the Northern hemisphere. However, even this extreme dose is environmentally relevant as it is comparable to UV-B doses at high altitude sites in the tropics. At mid latitudes, daily UV-Bplant dose may vary from zero to around 6 kJ m−2 d−1. Such variation is predictable with time of year, latitude and, to some extent, altitude, and highly unpredictable in response to changing cloud cover (Blumthaler, 1996, see Fig. 1). On a smaller scale, UV-B is also strongly attenuated within plant canopies (Brown et al., 1994; Flint & Caldwell, 1998). At mid-latitudes, ozone depletion within the range now expected may increase UV-Bplant by 10–20%, depending on season and latitude (Fig. 1). Thus, the effects of ozone depletion represent a relatively small increase in the magnitude of variation of an already highly dynamic component of the environment (Fig. 1). This is not to detract from the potential effects of ozone depletion. Without the successful limits on ozone-depleting substances, increases in UV-B would be large and cause wide-ranging biological damage. At high latitudes, where significant depletions continue, long-term ecosystem effects remain a real possibility (Rousseaux et al., 1998; Bjorn et al., 1999). However, the extensive evidence of a wide range of significant biological responses to relatively small increases in UV-B above the current ambient rather begs the question of what effects variation within the ambient range might have. Plant weighted UV-B doses (kJ m −2 d −1 ) measured under ambient conditions at Lancaster (54N, 2 W) during 1996 (closed symbols) and estimated under a 10% ozone depletion (open symbols). Ambient UV-B was measured using a BW100-UVB sensor (Vital technologies, Bolton, Canada) and integrated daily doses are derived from mean irradiances averaged every 10 min from measurements recorded every 0.5 s. UV-B under a 10% ozone depletion was estimated from the ambient data using the model of Bjorn & Murphy (1985 ). This model was used to calculate theoretical clear sky UV-B doses at Lancaster at each day of the year for zero and 10% ozone depletion. A percentage increase in UV-B due to 10% ozone loss was then calculated for each day, and this applied to measured data. A consistent result of UV-B research, from molecular biology through to field experiments, is that changing UV-B can significantly alter the phenolic chemistry of plants (Miejkamp et al., 1999). The data of de la Rosa et al. (see pp. 121–131 in this issue) relating to phenolic chemistry, are particularly noteworthy. Many previous studies have quantified the UV-B absorption of leaf extracts, which are usually considered to the function, largely, of flavonoid concentration, while other studies have directly quantified phenolics, but only in bulk terms, for example total soluble phenolics (Miejkamp et al., 1999). Such broad-brush measurements are valuable in many respects, but clearly disguise much complexity. In B. pendula, the concentrations of six out of nine phenolic compounds were significantly increased by UV-B radiation (de la Rosa et al., 2001). It is interesting that the authors found no significant change in phenolic acids or condensed tannins, although this is clearly not the case in many other species (Meijkamp et al., 1999). Although key enzymes at the core of phenylpropanoid metabolism are induced by UV-B, these data demonstrate that UV-B should not be seen as a general up-regulator of plant phenolics. Four of the six compounds increased by UV-B in B. pendula, all flavonoids, showed significant positive relationships with increasing UV-B dose. However, within the flavonoids, increases in concentration between UV-B doses of 1.6 and 13.0 kJ m−2 d−1 varied from nonsignificant (myricitin) to around fivefold for hyperin. Variation in the induction of different phenolics by UV-B has been observed before (Meijkamp et al., 1999) but de la Rosa et al. (2001) add dose responses to these earlier studies. In those phenolics where concentration was significantly affected by UV-B dose, variation was adequately explained by linear dose responses (de la Rosa et al., 2001). Response to increasing UV-B above ambient was a continuation of the response to variation within the ambient range. There is no evidence here for a threshold UV-B dose required to induce significant changes in flavonoids. Unfortunately, rather few UV-B dose responses have been published, and these few show a range of responses. However, in general, from dose responses encompassing plant growth, morphology and biochemistry, there is little evidence that ambient UV-B doses are below a threshold for significant effects (Paul & Gonzalez, 1998). Thus, plant responses to UV-B within the environmental range may be at least as great as those occurring in response to moderate ozone depletion. Clearly, quantitative assessment of the impacts of different ozone depletion scenarios must put responses to increases above ambient in the context of those to variation in UV-B within the ambient range. This will depend on dose response analyses of the type presented by de la Rosa et al. (2001). The conclusion that ‘ambient’ UV-B has significant effects on plants should not be unexpected. Martyn Caldwell's ground-breaking studies of plant responses to UV-B dealt with the effects of ambient UV-B at altitude in the Rocky Mountains (Caldwell, 1968). Focusing on flavonoids, there is evidence that concentrations of UV-B-absorbing compounds in different position within a canopy are correlated with incident UV-B: with significantly lower concentrations within the canopy and on the shaded side (Liakoura et al., 1997). The marked diurnal variation in leaf flavonoid concentrations that occurs in at least some species can be eliminated when solar UV-B is removed by filters that selectively attenuate the UV-B component of sunlight (Veit et al., 1996). A substantial number of field experiments using selective filters to attenuate solar UV-B have shown a range of significant responses, especially in terms of plant morphology and UV-B absorbing properties of leaves, flavonoid concentration or phenolic chemistry (Pal et al., 1997; Cybulski & Peterjohn, 1999; Hunt & McNeil, 1999; Lingakumar et al., 1999; Mazza et al., 1999; Turunen et al., 1999; Sullivan & Rozema, 1999). Filtering UV-B from ambient sunlight may also alter herbivory (Ballare et al., 1996; Rousseaux et al., 1998) and pathogen infection (Gunasekera et al., 1996). These observations link back to the study of de la Rosa et al. (2001; in this issue) who placed the responses of secondary metabolites to UV-B in the context of comparable responses to nutrient supply, which have been widely studied. Variation in UV-B, like nutrient supply, is clearly a potent factor influencing plant chemical composition. UV-B induced changes in secondary metabolites are complex, but taken with other responses, such as altered leaf morphology and nitrogen concentration, might be expected to have a wide range of effects, not least on plant interactions with herbivores and pathogens. Do such responses to ambient UV-B have ecological significance in the context, for example, variation between foliage in different areas of a canopy, between plants in more or less shaded sites, or between plants growing at different altitude? Similarly, what contribution do the photomorphogenic effects of UV-B make to their overall response to the light environment? Papers such as the one byde la Rosa et al. (2001) highlight a way forward in which the technologies, methodologies and scientific understanding developed for ozone depletion research can be applied to address these much wider biological questions.