Year: 2003
Type: review
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 time courses under constant conditions precludes conclusions on whether CPD photolyase oscillations are under endogenous control or not. CPDs and 6-4 PPs can also be removed in the dark through nucleotide excision repair through endonucleolytic cleavage, release of the damaged nucleotides, and strand resynthesis (Liu et al., 2000). This multistep process involving multiple enzymes has been found to operate with only a low capacity in plants (Gallego et al., 2000). In addition, plants respond to DNA-damaging treatments such as high doses of UV with repair by homologous recombination (Ries et al., 2000a). During UV-B irradiation, the increased homologous recombination frequency correlates with the amount of CPDs formed, and this frequency is significantly enhanced in the photolyase-deficient uvr2-1 mutant devoid of CPD-mediated photoreactivation (Ries et al., 2000b). These findings implicate homologous recombination in the removal of CPDs. Although homologous recombination in plants is generally classified as a dark repair process, it is stimulated by red but not by far-red exposure after UV-B treatment. These observations indicate that photosynthetic activity or other as yet undefined processes dependent on photosynthetic active radiation (400–700 nm; compare with Fig. 1) may promote UV-B induced homologous recombination in plants (Ries et al., 2000b). Low UV-B fluence rates (<1 μmol m-2 s-1) cause no or very low amounts of CPDs that are below the limit of detection but stimulate protective and photomorphogenetic responses (Batschauer et al., 1996; Kim et al., 1998; Frohnmeyer et al., 1999) that affect the plant's resistance to UV-B stress and to other biotic stress types (Kim et al., 1998; Ballaré, 2003). The most effective protection mechanism stimulated under such a light regime is the biosynthesis of flavonoids and other UV-B-absorbing phenolic components. Their physiological relevance as UV-B sunscreens was confirmed by the UV-B hypersensitive phenotype of mutants devoid of these compounds on the one hand and the increased resistance to UV radiation of mutants with enhanced flavonoid and sinapate levels on the other hand (Li et al., 1993; Landry et al., 1995; Bieza and Lois, 2001). A similar strategy is employed by cyanobacteria to withstand deleterious UV-B radiation impinging on them. They are thought to use a special class of compounds with absorption maxima between 310 and 360 nm as UV protectants. In the filamentous and heterocystous N2-fixing Anabaene sp., Nostoc commune, and Scytonema sp. shinorine, a representative of these mycosporin-like amino acids that are defined by the presence of a cyclohexenone or cyclohexenimine chromophore conjugated with an amino acid or its imino alcohol accumulates in response to solar UV-B radiation, mostly during the daily light period (Sinha et al., 2001). Plants grown in UV-exposed locations, i.e. at higher altitudes or geographical latitudes, are commonly more UV-B tolerant than plants grown at places with low UV-B exposure (Jordan, 1996). Such a variety of UV-B tolerance has been even shown between different Arabidopsis ecotypes (Torabinejad and Caldwell, 2000). Many morphological and anatomical changes have been reported from plants grown under long-term UV-B regimes of which the best characterized are summarized in Table I. Photomorphogenesis in seedlings is largely controlled by red/far-red-absorbing phytochromes (phyA–E) and by blue/UV-A-absorbing cryptochromes (Batschauer, 1999; Quail, 2002). Interestingly, low doses of UV-B also stimulate photomorphogenesis in etiolated seedlings, because the inhibition of hypocotyl elongation and opening of the apical hook are mediated independently of phytochromes and cryptochromes and exhibit a UV-B fluence response relationship (Ballaré et al., 1991, 1995; Kim et al., 1998; Suesslin and Frohnmeyer, 2003). In parsley (Petroselinum crispum) plants as well as in isogenic cell cultures, another UV-B-mediated response—the biosynthesis of flavonoids—has been elaborated in detail. In this case, phytochromes and cryptochromes are modulating the UV-B response but are not sufficient to stimulate increased flavonoid levels without UV-B (Beggs et al., 1986). This response pattern is not confined to parsley but was also described for defined developmental stages of other plant species (Batschauer et al., 1996; Wade et al., 2001) as well as in cell cultures (Beggs et al., 1986). With respect to circadian rhythmicity, at least in Arabidopsis, the phytochromes phyA, phyB, phyD, and phyE as well as cryptochrome 1 and 2 convey light input to the circadian clock to synchronize the endogenous timekeeper to local time each day (Devlin, 2002; Fankhauser and Staiger, 2002). In contrast, no systematic study has been reported yet to investigate a potential influence of UV-B on the clock. The existence of UV-B receptors has been questioned for decades, although the effect of UV-B on anthocyanin biosynthesis has long been known (Arthur, 1936). Rather, the perception of UV-B radiation has been either connected to the action of phytochromes and cryptochromes, as they partially absorb UV-B, or attributed to DNA, aromatic amino acids, and phospholipids (Beggs et al., 1986). High doses of UV-B or UV-C are damaging to cellular components, and the energy of the radiation is sufficient to cause photochemical changes to a certain set of molecules. This does not involve specific cellular receptors and the deleterious effects of such radiation stimulate general stress responses such as wound signaling (Conconi et al., 1996) or repair mechanisms, i.e. homologous recombination to remove genotoxic substrates (Ries et al., 2000a). Especially the DNA molecule itself has been considered an attractive candidate for a UV-B receptor, and a number of responses in plants and animals were related to UV-B absorption by DNA, because they were maximally stimulated by wavelengths between 250 and 280 nm (Herrlich et al., 1997). However, action spectra of UV-B responses in plants revealed their maximal stimulation between 290 and 310 nm, whereas wavelengths below 290 nm inhibited these responses (Herrlich et al., 1997). In addition, a lack of correlation between the increase of DNA damage (finally caused by UV-B impinging on DNA) and UV-B-elicited changes in transcript profiles contradicts the theory that damaged DNA serves as a UV-B receptor (Kim et al., 1998; Frohnmeyer et al., 1999; Kalbin et al., 2001). The hypothesis that phytochromes and cryptochromes serve as putative UV-B receptors has also been disproven for most light responses. For example, the hypocotyl elongation response has been exclusively attributed to phytochrome- or cryptochrome action in plants (Mohr and Schäfer, 1983). Studies with mutants devoid of these photoreceptors now demonstrate that UV-B radiation independently affects the hypocotyl elongation response (Kim et al., 1998; Suesslin and Frohnmeyer, 2003). Because some UV-B responses, e.g. chalcone synthase (CHS) expression, can be modulated by blue or red light, there is evidence that a complex web exists between phytochrome-, cryptochrome-, and UV-B-signaling chains in cell cultures (Ohl et al., 1989) and plants (Boccalandro et al., 2001; Wade et al., 2001). The nature of UV-B receptors, however, has been not elucidated so far. In animal cells, a putative receptor seems to be located in the cytosol and might also be attached to membranes (Devary et al., 1993), which is consistent with pharmacological studies in Arabidopsis (Long and Jenkins, 1998). There is large agreement that a UV-B receptor consists of a protein with a bound pterin or flavin as chromophores (Galland and Senger, 1988; Ensminger and Schäfer, 1992). Feeding of parsley cell cultures with radioactively labeled flavins enhanced the amount of UV-B-induced flavonoid end products and has been taken as a hint that flavins might represent the chromophore of a UV-B receptor in this system (Ensminger and Schäfer, 1992). Taken together, biochemical or genetic approaches will be useful tools for the isolation of UV-B photoreceptors. However, two premises are necessary to succeed: First, a given response should be specifically stimulated by UV-B to omit possible interaction with phytochrome- or cryptochrome-mediated signaling networks. Second, only low doses of UV-B that generate no or only negligible amounts of DNA damage should be considered to exclude responses unrelated to UV-B photoreceptor action. on transduction has by a of cell and genetic The transduction expression in seedlings and cell cultures has been by and pharmacological agents et al., 1993; et al., These studies that the light to a protein and that of this include and However, although molecular approaches to the isolation of components involved in signaling these are not related with the found by In to the phytochrome- and components described the about UV-B-mediated transduction is to such UV-B-signaling components the studies by using pharmacological agents in cell and Arabidopsis cell cultures a after UV-B The response is stimulated by blue light and is completely to red and far-red irradiation, a action of other photoreceptors during UV-B stimulation and Jenkins, 1996; Frohnmeyer et al., 1997). In to the proposed components of to and of not affect UV-B-induced expression. of and UV-B-mediated transcription and Jenkins, 1996; Frohnmeyer et al., whereas they not expression et al., These were confirmed in cell cultures that exhibit and UV-B with respect to expression and that independently a cell et al., 1998). The of in UV-B signaling was in parsley cell UV-B caused an of for more than levels correlated with the stimulation of expression et al., A for so but a possible candidate a protein has been found by for UV-B-induced et al., 2000). The of during light transduction in parsley cell cultures has been shown by different of cytosol and a of et al., Such a be involved in the of transcription because their transfer from the cytosol into the and their to the of the parsley on the et al., A recent of UV-B-induced protein activity in cell cultures et al., can be taken as a that a during UV-B-mediated The has also been in UV-B-induced expression in Arabidopsis et al., 2001). However, the of this is a of and may studies and Strid, 2003). of other UV-B-induced events that species serve as signaling components. UV-B irradiation of plant itself causes the of such as and and that the expression of is mediated by in In addition, more expression can be modulated by have been found in Arabidopsis et al., 2001). Interestingly, is not linked to expression and 1995; Frohnmeyer et al., that at least two different signaling UV-B-induced responses (Fig. The correlation between and gene expression is not to plants. studies in cell cultures revealed that UV-B radiation as a for related to (Devary et al., et al., 1997). for UV-B-mediated The is from Brosché and protein from a Arabidopsis the and a by high doses of UV-B has been proposed and Strid, 2003). This might be by deleterious effects of radiation and is linked to wound transduction in plants (Conconi et al., 1996). Because the response was connected to this was in the proposed of UV-B-mediated transduction (Fig. However, the between a stimulated by high doses of UV-B and a stimulated by low doses of UV-B is not defined so far. Taken together, at least two independently transduction are in plants that different of (Fig. As will be in the on genetic photoreceptor or transduction mutants should be therefore in of these responses. in gene expression by UV-B largely on the as observed for phytochrome- and cryptochrome-mediated responses. number of studies have UV-B-mediated transcriptome changes with the repair of DNA (Ries et al., cell control et al., of et al., of photosynthetic capacity et al., and the production of protective of (Beggs et al., and Scheel, 1989). transcriptome changes were from plants grown in a UV-B in the et al., or in the and using gene UV-B has also been shown to stimulate a of more than a transcriptome changes of flavonoid have been described in parsley cell components of this are in a a (Hahlbrock and Scheel, et al., et al., 2000). of this were and and a number of elements were described that light of these elements also as in that control the expression of homologous in other species et al., et al., et al., and 1996). A of the parsley consists of one that binds and of one the of et al., et al., 1997). This to light but is not specific to UV-B. studies in Arabidopsis seedlings under the control of such a increased gene activity also under phytochrome- or light conditions (Batschauer et al., 1996). Therefore, the specificity of responses stimulated by a certain might be by the presence of signaling compounds or the of transcription in the cell of in to the of light-dependent However, the large of and about and more than respectively, in the Arabidopsis it to the transcription for the of specific and flavonoid enzymes by biochemical A of these from genetic approaches described from and to Arabidopsis that were to mutants with A of these mutants are below to the complex of transcriptome changes. transcription to elements are generally thought to as at least one as a in and of in caused the of the and acid et al., 1998). The of an Arabidopsis mutant in the the The mutant contains levels of due to of et al., 2000). As a the plant is more tolerant to UV-B. In are in light but UV-B The of seems to be an mechanism for to UV-B. for Arabidopsis mutants with to a given of the solar spectrum have been approaches to of Such mutants to be either in the phytochromes and photoreceptors or in the transduction compounds (Batschauer, 1999; Quail, 2002). In the UV-B genetic were mainly to hypersensitive mutants with reduced tolerance to UV-B by on the of plants in the biosynthesis of phenolic sunscreens or DNA repair. The uvr2-1 mutant is in the CPD photolyase gene and the mutant has a in the 6-4 photolyase gene and is in photoreactivation of 6-4 of these mutants are hypersensitive to high doses of UV-B et al., et al., 1998). involved in nucleotide excision repair were and the action of these components a of the mechanisms DNA repair (Gallego et al., 2000; et al., 2000; and May, 2003). In contrast, mutants to UV-B or have been described so far. the UV-B 1 mutant was by of its growth under UV-B et al., 2002). The increased resistance correlated with photoreactivation of CPDs and dark repair of 6-4 The transcript CPD photolyase was at higher levels than in under white-light conditions and after exposure to UV-B. Although the has not yet been linked to the it is to represent a of the two DNA repair et al., 2002). The high UV-B tolerance of another mutant with a phenotype under UV-B, UV tolerant was on increased levels of UV-absorbing flavonoids and sinapate The of phenolic sunscreens may at least be caused by a constitutively transcript and Lois, 2001). Although the has not been located the correlation between increased levels of UV-absorbing and UV-B resistance has been In to the mutants that the of phenolic compounds or of an DNA repair system for protection against damaging UV-B, no mutant in a UV-B receptor has been so far. The to such mutants may be due to the of light conditions. under UV-B-supplemented light, which is absorbed by all may to of a UV-B response by other light responses, and high fluence rates of UV-B cause DNA damage that may affect the response of In contrast, low UV-B doses are not other photoreceptors and cause negligible amounts of DNA studies with plant species that these low UV-B doses are sufficient to i.e. the inhibition of hypocotyl elongation or apical hook opening in etiolated seedlings (Ballaré et al., Kim et al., 1998; Suesslin and Frohnmeyer, 2003). Such low doses of UV-B were to mutants with in UV-B perception or and the are summarized below and Frohnmeyer, 2003). seedlings were with UV-B for at a fluence that was sufficient to hypocotyl elongation but was to stimulate flavonoid biosynthesis or increased DNA To that levels of pyrimidine dimers are by this the hypocotyl elongation was also in photolyase-deficient mutants that respond to DNA-damaging irradiation (Kim et al., 1998). no phenotype in the uvr2-1 UV-B mutants were from that a hypocotyl with The was specific to UV-B and was not to or cryptochrome because all mutants were from the after or UV-A treatment. was not only in its hypocotyl elongation but was also in and gene expression after irradiation with UV-B. The gene is to an protein with to However, although a acid is in no were is at low levels in darkness and stimulated by UV in The protein is located in the cell layers of and but not in the cells, it was in the amounts were attached to the of mutants in with the and expression pattern the hypothesis that is a of a signaling Although and expression are mediated by different transduction are in therefore that be an of a signaling and might be linked to a UV-B receptor (Fig. UV-B radiation causes a of responses that are summarized as and responses similar to responses (Kim et al., 1998). Because different phytochromes and receptors are in Arabidopsis that light responses, the whether one UV-B photoreceptor is sufficient to all responses. In to phytochromes and cryptochromes, and responses be also by different UV-B A hint from the to UV-B in mutants with specific in UV-B perception and transduction are to this the relationship of photomorphogenetic responses, DNA damage, and UV-B radiation should be kept in about responses in Arabidopsis (Boccalandro et al., 2001) will to to mutants with a UV-B to not be due to are to two for on the of for of the and for the
Source: PLANT PHYSIOLOGY
Authors: Hanns Frohnmeyer, Dorothee Staiger
Institutions: University of Freiburg, Bielefeld University
Language: English
Topic: Light effects on plants
Subfield: Plant Science
Domain: Life Sciences
Open Access status: bronze
Funder: University of California, Davis
OpenAlex ID: W2167082201