Ultraviolet-B Radiation-Mediated Responses in Plants. Balancing Damage and Protection

Abstract

Seven percent of the electromagnetic radiation emitted from the sun is in the UV range (200–400 nm). As it passes through the atmosphere, the total flux transmitted is greatly reduced, and the composition of the UV radiation is modified. Shortwave UV-C radiation (200–280 nm) is completely absorbed by atmospheric gases. UV-B radiation (280–320 nm) is additionally absorbed by stratospheric ozone and thus only a very small proportion is transmitted to the Earth's surface, whereas UV-A radiation (320–400 nm) is hardly absorbed by ozone (Fig. 1). In the past 50 years, the concentration of ozone has decreased by about 5%, mainly due to the release of anthropogenic pollutants such as chlorofluorocarbons (Pyle, 1996). Consequently, a larger proportion of the UV-B spectrum reaches the Earth's surface with serious implications for all living organisms (Xiong and Day, 2001; Caldwell et al., 2003). The solar spectrum perceived by higher plants. PAR, Photosynthetically active radiation. Elevated UV-B radiation (UV-B) has pleiotropic effects on plant development, morphology, and physiology, summarized in Table I. The morphological consequences of UV-B-supplemented white-light treatment include reduced growth, thickening of leaves and of cuticular wax layers. In addition, a lower photosynthetic capacity due to degradation of the D1 protein of photosystem II and reduced pollen fertility have been described for various plant species (Jansen et al., 1998; Caldwell et al., 2003). UV-B-induced alterations in plants Data from Jansen et al. (1998) and refs. therein. UV-B-induced alterations in plants Data from Jansen et al. (1998) and refs. therein. Their sessile life style forces plants to adapt to changing environmental conditions. In general, plants respond differently to irradiation with low or high doses of UV-B, either by stimulating protection mechanisms or by activating repair mechanisms to cope with the different types of stress. The most common protective mechanism against potentially damaging irradiation is the biosynthesis of UV-absorbing compounds (Hahlbrock and Scheel, 1989). These secondary metabolites, mainly phenolic compounds, flavonoids, and hydroxycinnamate esters, accumulate in the vacuoles of epidermal cells in response to UV-B irradiation and attenuate the penetration of the UV-B range of the solar spectrum into deeper cell layers with little effect on the visible region. Therefore, humans using sunscreen with UV-absorbing agents mimic ancient plant protection responses. It is well documented that the responses to low UV-B fluence rates are in part due to transcriptome changes. The molecular underpinnings of UV-B perception and the proposed signaling events set in motion by the proposed UV-B photoreceptor(s) have been reviewed in detail (Jordan, 1996; Jansen et al., 1998; Mackerness, 2000; Brosché and Strid, 2003). In this Update, we summarize recent progress on dose-dependent gene expression and on the characterization on putative signaling elements linked to gene expression. In addition, recent genetic approaches have shed some light on novel components that might be involved in the perception of UV-B and in the transduction of signals generated by UV-B. DNA is particularly sensitive to UV-B radiation because absorption of UV-B causes phototransformations, resulting in the production of cyclobutane pyrimidine dimers (CPDs) and pyrimidine (6-4) pyrimidinone dimers (6-4 PPs). Because DNA and RNA polymerases are not able to read through these photoproducts, their elimination is essential for DNA replication and transcription and thus for survival (Britt and May, 2003). To avoid the cytotoxic effects of UV-induced DNA damage, most organisms have developed a complex set of repair mechanisms including photoreactivation, excision, and recombination repair. Photoreactivation is a light-dependent enzymatic process using UV-A and blue light to monomerize pyrimidine dimers: Photolyase binds to the photoproducts and then uses light energy to initiate electron transfer to break the chemical bonds of the cyclobutane ring and restore integrity of the bases. Arabidopsis contains photolyases with substrate specificity for either CPDs or 6-4 PPs, respectively (Hoffman et al., 1996; Ahmad et al., 1997). Whereas 6-4 PP photolyase protein is constitutively expressed, CPD photolyase is induced by UV-B (Waterworth et al., 2002). In cucumber (Cucumis sativus), CPD photolyase shows diurnal changes: Transcript levels and enzymatic activity peak 3 to 6 h into the light period, respectively, and thus are inversely correlated with the growth inhibition elicited by supplementary UV-B irradiation (Takahashi et al., 2002). It has therefore been suggested that fluctuations in CPD repair activity may contribute to alleviating the UV-B induced detrimental effects on leaf growth. Oscillations with a reduced amplitude were also observed when plants were kept in darkness during the day (Takahashi et al., 2002). However, the lack of extended