Physiological Responses of Higher Plants to UVB Radiation

Ivanka S. Fedina and Maya Y. Velitchkova

13.1 Introduction

Seven percent of the electromagnetic radiation emitted from the sun is in the range of 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. Short-wave UV-C radiation (200-280 nm) is completely absorbed by atmospheric gases. UV-B radiation is often defined as 280-320 nm. However, the legal definition provided by the International Commission on Illumination sets the UV-B radiation range as 280-315 nm. UV-B radiation is maximally absorbed by stratospheric ozone and thus, only a very small proportion is transmitted to the Earth's surface, whereas UV-A radiation (315-400 nm) is hardly absorbed by ozone. In the past 50 years, the concentration of ozone has decreased by about 5%, mainly due to anthropogenic pollutants, such as chlorofluorocarbons, releasing Cl atoms that catalytically remove ozone molecules from the atmosphere. The surface concentration of ozone has risen from less than 10 ppb prior to the industrial revolution to a day-time mean concentration of approximately 40 ppb over much of the northern temperate zone. If current global emission trends continue, surface ozone might rise over 50% by this century. Ozone depletion is particularly severe over the Antarctic continent, where a dynamically isolated air mass cools down to extremely low temperatures during the austral winter, facilitating ozone photo-destruction and formation of the so called springtime "ozone hole". Depletion of stratospheric ozone has increased solar ultraviolet-B radiation at high- and mid-latitudes in both Southern and Northern hemispheres (Frederick et al. 1994). However, ozone destruction is more intense over the Southern hemisphere with measured solar UV-B fluxes up to 50% more than those at comparable latitudes in the Northern hemisphere (Seckmeyer et al. 1995). Consequently, enhanced solar UV-B may have a greater impact on plants in agricultural production and in natural ecosystems in the Southern than in the Northern hemisphere (Madronich et al. 1995). The global trend of increasing solar UV-B

Academic Metodi Popov Institute of Plant Physiology, Bulgarian Academy of Sciences, Academic Georgi Bonchev Street, Building 21, Sofia 1113, Bulgaria e-mail: [email protected]

S.N. Singh (ed.), Climate Change and Crops, Environmental Science and Engineering, DOI 10.1007/978-3-540-88246-6.13, © Springer-Verlag Berlin Heidelberg 2009

radiation has been confirmed in mid-latitude in Japan (Sasaki et al. 2002) and in New Zealand in the 1990s (McKenzie et al. 1999). Furthermore, according to the report of UNEP (2002) (United Nations Environmental Programme: Environmental effects of ozone depletion and its interactions with climate change), it will take several years before a beginning of an ozone recovery can be confirmed at individual locations, nevertheless the concentrations of most anthropogenic precursors of ozone depletion are now decreasing (McKenzie et al. 2003). Although UV-B is only a minor component of solar radiation, its potential for causing biological damage is exceptionally very high due to its high energy and even small increase could lead to significant biological damage. The UV-B region of the spectrum is absorbed by a wide range of biologically active molecules, such as nucleic acids, aromtic amino acids, lipids and phenolic compounds. However, no specific photoreceptor molecule has been identified that can perceive the UV-B signal.

The crop growth, total biomass, final seed yield, thousand-grain weight and the amount of photosynthetic pigments decreased under near-ambient and enhanced UV-B radiation, while crop development was promoted by enhanced UV-B radiation (Yao et al. 2006). UV-B radiation-exclusion studies have indicated that many plants exhibit greater productivity in the absence of solar UV-B radiation (Krizet et al. 1997, 1998; Mazza et al. 1999; Kumagai et al. 2001).

The differences in the sensitivity to UV-B radiation were not related to the geographical locations. Physiological effects of UV-B on plants depend on plant species, the nature of UV-B treatment and interaction with other environmental factors. There were differences in the UV-B sensitivity among the cultivars of the same crop (Hidema et al. 2001). Deleterious UV-B effects on plants include reduced photosynthesis, biomass reduction, decreased protein synthesis, impaired chloroplast function, damage to DNA. UV-B radiation also produces oxidative stress increasing active oxygen species (AOS). These AOS have been proposed as the common second messenger for signal cascade leading to activation of a number of transcription factors (Schreck and Baeuerle 1991). The four compounds - AOS, salicylic acid (SA), jasmonic acid (JA) and ethylene, have been shown to be key regulators of gene expression in response to UV-B. The rise of AOS levels appears to regulate the synthesis of SA, JA and ethylene.

UV-B stress and resultant damage in plants can be classified as (i) DNA damage: formation of single-strand breaks (cyclobutane dimers) and indirect physical damage to the DNA by free radical formation, (ii) membrane damage: peroxidation of unsaturated fatty acids and alteration in the membrane lipid composition, (iii) photosynthetic apparatus damage: changes in the routes of electron paths in PSII, thylakoid ultrastructural damage, chlorophyll reduction and damage to Rubisco, (iv) hormonal damage: photodestruction of indole acetic acid and resultant inhibition of cell expansion. Each of these types of damage is directly or indirectly related to the formation of AOS under UV-B stress. Physically avoiding UV-B from penetrating into the plant system offers the first line of strategy to counter UV-B stress; this can be done by manipulating epidermal and cuticular layers of the leaf (wax, hairs). The second line involves increasing UV-B absorbing pigments, such as flavonoids and anthocyanins. The third line is to ameliorate or alleviate UV-B stress. Recent research has identified several beneficial effects of Se in plants which include antioxidative properties that can stimulate plant growth (Hartikainen et al. 2000).

13.2 UV-B Sensitivity and Productivity

A reduction in biomass accumulation is often a reliable indication of plant's sensitivity to UV-B radiation, since it represents the cumulative effects of damaged or inhibited physiological functions (Smith et al. 2000). However, measurements of other physiological parameters, such as chlorophyll content and levels of UV-B absorbing compounds, have also proved to be useful indicators of UV-B tolerance or sensitivity (Greenberg et al. 1997). Morphological characteristics can also affect species' sensitivity to UV-B radiation by influencing the amount of UV-B radiation intercepted (Bornman and Teramura 1993). For example, canopy leaves receive more sunlight, and hence more UV-B than under storey plants. Monocots, which have a vertical pattern of leaf growth, tend to intercept less direct sunlight than herbaceous dicots, whose leaves tend to grow horizontally (He et al. 1993). In addition, leaf hairs can also attenuate ultraviolet light (Karabourniotis et al. 1992, 1994) and leaf reflectance.

Since photosynthesis is dependent on the light-harvesting properties of the chlorophylls a, UV-B induced reduction in chlorophyll may result in lower levels of biomass accumulation, and hence it might be an useful indicator of UV-B sensitivity. Many plants display reduced photosynthetic function and chlorosis as symptoms of UV-B stress (Renger et al. 1989; Barnes et al. 1990; Strid et al. 1994). Conversely, plants adapted to high UV-B conditions retain higher photosynthetic integrity during UV-B exposure than those originating from low UV-B environments (Caldwell et al. 1994; Barnes et al. 1987). Therefore, the plants, which are able to maintain chlorophyll levels during UV-B exposure, are often less sensitive (Bornman and Vogelmann 1990; Greenberg et al. 1997). Increased levels of UV-B absorbing compounds lessen the symptoms of UV-B damage, such as growth inhibition and photosynthetic damage (Mirecki and Teramura 1984; Murali and Tera-mura 1986). Flavonoids and related compounds absorb strongly the light in the UV-region, but not in the photosynthetically active regions of the spectrum (Bornman and Vogelmann 1990; Cen and Bornman 1993), thus allowing photosynthesis to continue while UV wavelengths are attenuated at the epidermis. It has been reported that cultivars with higher levels of flavonoids prior to the onset of UV-B treatment (Gonzales et al. 1996) as well as those that can rapidly accumulate these compounds (Murali and Teramura 1986) are better protected during UV-B exposure. Since their protective properties are well established, it was expected that plants with high levels of UV-absorbing compounds would be more tolerant than those with lower levels. However, such a trend was not observed by Smith et al. (2000). Mean levels of UV-absorbing compounds did not differ significantly between the tolerant and sensitive groups, nor did an ability to increase the level of UV-screening pigments in response to UV-B necessarily reduce sensitivity. As tolerance to UV-B radiation probably involves many mechanisms, it is not unexpected that a species' sensitivity to UV-B cannot be determined by a single factor, such as UV-absorbing compounds. Leaf surface properties can affect the amount of UV-B that reaches underlying tissue through altered reflectance (Cen and Bornman 1993). Leaf hairs (trichomes) modify the micro-environment of the leaf, primarily through their extension of the boundary layer and reduction in the water loss (Ehleringer 1984). They can also reduce the amount of UV-B radiation penetrating to the epidermis (Karabourniotis et al. 1992), by their UV-absorbing pigment content (Karabourniotis et al. 1992, 1994). Waxes, which are sometimes UV-B targets themselves (Gonzales et al. 1996), are among the factors that can contribute to reflectance, at least in the visible light region. Hence, plants with a thick waxy cuticle were UV-B tolerant. The plants, which wax cover is lesser, were more susceptible to UV-B radiation, considering primary photosynthesis reactions, recorded by chlorophyll a fluorescence (Skorska and Szwarc 2007). Waxiness may contribute to tolerance, but when a few plants with waxy cuticles were tested, the connection was found tenuous. Recently, Gonzales et al. (1996) showed that the difference in sensitivity among six Pisum sativum cultivars was not associated with surface wax amounts or properties. Similarly, the removal of waxes from the epidermis of plants does not increase UV-B damage (Day et al. 1992). Thus, it seems unlikely that the presence of epicuticular wax is itself a protective feature. High reflectance of visible radiation by desert or alpine plants is attributed to epicuticular wax on the leaf surface (Reicosky and Hanover 1978), but this property does not cover the UV-B range of the spectrum (Day et al. 1992; Gonzales et al. 1996). The heavy shading, that occurs in plants with large leaf area and small internodes, could make these plants less susceptible to UV-B damage. Differences in UV-B sensitivity between species represent the relative contributions of morphological, physiological and biochemical differences, but variations in sensitivity within species are usually subtle. Sato and Kumagai (1993) examined 198 rice cultivars, belonging to five Asian rice ecotypes and Japanese lowland and upland rice groups. They found that sensitivity to UV-B radiation varies widely among different culti-vars belonging to the same ecotype and the same group. In addition, rice cultivars originating from regions with higher ambient UV-B radiation do not necessarily exhibit higher tolerance. The differences in sensitivity to UV-B radiation were not related to the geographical locations at which these cultivars are grown.

Transgenic rice plants bearing the CPD photolyase gene of the UV-resistant rice cultivar had 5.1 and 45.7 fold higher CPD photolyase activities than the wild-type and were significantly more resistant to UVB-induced growth damage, and maintained significantly lower CPD levels in their leaves during growth under elevated UV-B radiation. Conversely, plants with little photolyase activity, was severely damaged by elevated UV-B radiation, and maintained higher CPD levels in its leaves (Hidema et al. 2007).

It is suggested that generalizations on plant sensitivity to UV-B, based on growth form and functional type, could be misleading (Musil et al. 2002). Seventeen herb, shrub and tree species of commercial and ecological importance in southern Africa were exposed to ultraviolet-B (UV-B, 280-315 nm) radiation. Leaves of trees had altered chlorophyll a and b, carotenoid and flavonoid concentrations, but those of shrubs or herbs did not. Correlation analyses did not support the view that growth is less negatively affected in species with thick leaves or in those where leaf thickness increases, or in species with naturally high leaf flavonoid contents or that are able to synthesize additional flavonoids in response to UV-B enhancement.

Crop response to UV-B radiation is associated with UV-B intensity, environmental factors and growing season (Yao et al. 2006). Plant photosynthetic productivity is determined by leaf area and the photosynthetic rate per unit area. Light attenuation can be modified by leaf ultrastructural changes under enhanced UV-B, and this could contribute to resultant changes in photosynthesis. A common response is addition of spongy mesophyll cells which increases leaf thickness. Several layers of shorter and wider palisade cells are formed under high UV irradiance. The logical interpretation of these changes is that a padding of cells is developed in the surface to prevent UV from reaching the site of electron transport, both in the chloroplast and mitochondria. The reduction of mesophyll cells under UV radiation would affect the CO2-concentrating mechanism in C4 plants and subsequent transport of CO2 to bundle sheath cells. The increase in mitochondria and decrease in peroxisomes would imply that there would have been an imbalance in the transport of malate and glycine between mitochondria and peroxisome and a concomitant decrease in photorespiration (Shanker 2006). Bornman and Teramura (1993) suggested that the seedlings in the early stages of development may be particularly sensitive to UV-B, while Teramura and Caldwell (1981) reported greater inhibition of photosynthesis in developing leaves of soybean than those irradiated at full expansion. Leaves growing under elevated UV-B will receive greater cumulative exposure throughout the lifetime of leaves than mature leaves irradiated after developing without UV-B. Nogues et al. ( 1998) have suggested that the primary cause of reduced area of leaves was UV-B-induced inhibition of cell division. According to Logemann et al. (1995), this is an adaptive rather than injurious response.

Pumpkin (Cucurbita pepo L.) plants, grown in the field, have been shown to be sensitive to ambient UV-B radiation, resulting in significantly reduced yields of fruit (Germ et al. 2005). Total grain nitrogen content and grain storage protein content increased under elevated UV-B radiation, while tiller number, dry mass, panicle number, grain yield and grain size significantly decreased (Hidema et al. 2005). Such reductions were enhanced by lower temperature and less sunshine (Kumagai et al. 2001). UV-B radiation significantly increased the concentrations of both ros-marinic and carnosic acids, as well as other rosemary compounds, such as naringin and carnosol (Luis et al. 2007). Leaf rutin concentration and the amount of UV-B absorbing compounds were increased by UV-B exposure (Yao et al. 2006).

13.3 UV-B-Induced Photomorphogenesis

Many morphological and anatomical changes have been reported from plants grown under long-term UV-B regimes. Photomorphogenesis in seedlings is largely controlled by red/far-red-absorbing phytochromes and by blue/UV-A- absorbing cryptochromes (Batschauer 1999; Quail 2002). 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. 1996). The nature of UV-B receptors, however, has been not elucidated so far. There is a large agreement that a UV-B receptor consists of a protein with a bound pterin or flavin as chromophores (Galland and Senger 1988). Low doses of UV-B stimulate photomorphogenesis in etiolated seedlings, because the inhibition of hypocotyls elongation and opening of the apical hook are mediated independently of phytochromes and cryptochromes and exhibit a UV-B influence response relationship (Ballare et al. 1991; Suesslin and Frohnmeyer 2003). Enhanced UV-B significantly inhibited pollen germination and tube growth in most of investigated species (Feng et al. 2000). Plants grown at high UV-B produced smaller flowers with shorter standard petal and staminal column lengths. Flowers so produced had less pollen with poor pollen germination and shorter tube lengths (Koti et al. 2005).

Decreases in whole plant growth were associated with reductions in attributes linked to cell division and cell expansion (Hofmann et al. 2001). The reduced proportion of palisade parenchyma and increased proportion of spongy parenchyma and intercellular space may have been specific reactions to enhanced UV-B radiation (Bornman and Teramura 1993; Heijari et al. 2006). Nogues et al. (1998) observed that in response to UV-B, there was a large reduction in the number of palisade mesophyll cells rather than formation of smaller cells. The reduced number of leaves was a further UV-B-induced change in morphology. In the cells exposed to enhanced UV-B radiation, the number of mitochondria increases, while the number of peroxisomes significantly decreases (Heijari et al. 2006). It was suggested that this might be an adaptive mechanism to compensate for the photodamage in perox-isomes. Even below-ambient levels of UV-B were capable to induce an increase in thylakoid surface area relative to the chloroplast volume typical of a low-PAR shade response in sunflowers and alter starch metabolism (Fagerberg 2007).

Supplementary UV-B radiation suppresses the growth not only of shoots, but also of plant roots (Naito et al. 1997). Kalbina and Strid (2006) established UV-B-dependent decrease in biomass, rosette size and leaf area and significant ecotype-specific genetic variability in general UV-B responses in Arabidopsis.

13.4 UV-B and Other Factors

In the nature, plants usually experience several stresses simultaneously. The effect of enhanced UV-B radiation on plants can be modified by other co-occurring or simply by changing environmental factors, like atmospheric CO2, water availability, mineral nutrient availability, heavy metals, temperature, air pollutants. Plant response can be also modified by plant growth rate, developmental stage, growth form (herbs cf. trees) and functional type. Visible radiation is an important ameliorating factor. There are some suggestions that plant responsiveness to UV-B may be influenced by the ratio of UV-B light to visible sunlight as much as by the absolute level of UV-B radiation (Deckmyn and Impens 1997). White light ameliorates UV-B induced responses, including gene expression. These effects were the consequences of photosynthetic electron transport and photophosphorylation (A-H-Mackerness et al. 1996; Jordan 2002). The sensitivity of plants to UV-B irradiation is much greater at low PPFD and UV-A levels (Cen and Bornman 1990). UV-A was particularly effective at ameliorating UV-B damage when PPFD was low, but has no effect at higher PPFDs (Caldwell et al. 1994). High PPFDs may confer protection from UV-B damage by increasing photosynthesis and the available biochemical energy for defence and/or repair processes. This hypothesis was supported by the observations that UV-B-induced reduction in plant growth were less severe when elevated CO2 concentrations were used to increase photosynthesis in the absence of any change in flavonoid content (Adamse and Britz 1992). UV-B-induced damage was alleviated either by elevated CO2 or exposure to high irradiance-visible radiation (Kumagai and Sato 1992). It was shown that either elevated CO2 or somewhat higher temperature had similar effects in reducing the growth-inhibiting effects of elevated UV-B radiation on sunflower and maize seedlings (Mark and Tevini 1997). Elevated CO2 levels compensated the damaging effects caused by UV-B radiation on the physiological parameters, such as plant height, leaf the area, total biomass, net photosynthesis, total chlorophyll content, phenolic content, relative injury and wax content (Koti et al. 2007). UV-A, which is closer to PAR, has generally been assumed to be less detrimental to plant growth, but recent findings have demonstrated that UV-A has the ability to decompose the UV-B absorbing pigments, thereby reducing the capacity of the plants to fight off UV-B stress (Fukuchi et al. 2004). The effects observed under UV-A stress can be attributed to the presence of a cryptochrome, operating in the blue-UV-A spectral range. It must be noted that the ratio of UV-A to biologically effective UV-B radiation in the field is up to 7.5 times greater than in the greenhouse (Dai et al. 1995). Heijari et al. (2006) suggest that biological effects of the UV-A component of sunlight may be of much greater importance than was believed formerly. UV-A helps to develop a protective pathway against UV-B-induced damage of photosynthetic apparatus (Joshi et al. 2007).

Sullivan and Teramura (1990) have established that as a result of water stress, the concentration of leaf flavonoids in plants increased, which provided greater UV-B protection. On the other hand, elevated UV-B radiation in the field tended to alleviate drought symptoms (Manetas et al. 1997). In the moss species, UV-B radiation inhibited growth when the moss was under water stress, but stimulated growth when the moss was well hydrated (Gehrke 1998). Enhanced UV-B radiation and drought stress have an additive negative effect on growth of willows (Turtola et al. 2006). Higher tolerance to drought stress for Arabidopsis plants grown under UV-B radiation may be attributed to both increased proline content and decreased stomatal conductance (Poulson et al. 2006).

In pine seedlings grown in a growth chamber, enhanced ozone concentration led to an increased sensitivity of the seedlings to UV-B radiation, since ozone reduced the contents of UV-B-absorbing pigments in the plant tissues. In tobacco, UV-B radiation increased the level of ozone-induced foliage lesions (Thalmair et al. 1996). Soybean plants grown in the field were found sensitive to ozone in the air, but not sensitive to supplementary UV-B (Miller et al. 1994).

The uptake of certain nutrients may be modified by UV-B radiation. In oilseed rape (Brassica napus) plants grown under enhanced UV-B and simultaneously exposed to different cadmium concentrations, the manganese content in the shoots decreased while the contents of magnesium, calcium, cooper and potassium significantly increased. The UV-B had no additional influence on the nutrient content of the roots (Larsson et al. 1998). Prasad and Zeeshan (2005) reported that the effect of combination UV-B and Cd was more detrimental to growth, photosynthesis and antioxidant enzymes. According to Yao and Liu (2007), supplemental nitrogen made the plants more sensitive to enhanced UV-B, although some antioxidant indexes increased. The ability of Se to ameliorate UV stress has been shown by Hartikainen and Xue (1999) and Germ et al. (2005).

UV-B exposure caused increases in jasmonic acid (JA) levels and ethylene production in Arabidopsis thaliana (A-H-Mackerness et al. 1999a, b). Both jasmonic acid and ethylene are components of signal pathways leading to regulation of gene expression in response to UV-B radiation and subsequent resistance/tolerance to UV-B (A-H-Mackerness et al. 2001). The production of ethylene in plant tissue under normal conditions is low, but the level of this hormone increases in response to external stresses (Wang et al. 1990). JA and its methyl ester (JA-Me) are endogenous growth substances identified in many plant species (Sembdner and Parthier 1993). Jasmonates are one of the simplest non-traditional plant hormones with diverse roles and functions, including a potential role in plant defence (Creelman and Mullet 1997a, b). Jasmonic acid is derived from linolenic acid via octadecanoid pathway (Reinbothe et al. 1994). UV-B irradiation results in the perturbation of plant membranes and/or the activation of lipases which induces the signal-transduction pathway which activates stress inducible genes; DNA damage might be initial signal that activated the octadecanoid pathway. Thus, the response to UV-B radiation may be regulated by jasmonic acid derived from linolenic acid through the octadecanoid pathway.

Salt (NaCl, KCl, NaNO3) pre-treatment resulted in considerable loss of UV-induced and UV-B absorbing compounds. In the meantime, chlorophyll fluorescence parameters and oxygen evolution in salt pre-treated seedlings were less affected by UV-B (Fedina et al. 2006). Application of mineral nutrients (N, P and K) showed a significant positive response in wheat and mung bean by ameliorating the negative impact of UV-B (Agarwal and Rathore 2007). An increase of polyamines (Lutz et al. 2005), and especially of putrescine level in thylakoid membranes upon elevated UV-B exposure, comprises one of the primary protective mechanisms in the photosynthetic apparatus of the tobacco variety against UV-B radiation.

13.5 UV-B and Photosynthesis

Photosynthetic damage is associated with stomatal behaviour, photosynthetic enzymes and pigments (Teramura and Sullivan 1994; Tevini 1994), electron transport chain (Tevini et al. 1991), as well as disruption of the chloroplast membrane

(Bornman 1989). Examination of a single process or component does not allow identification of the primary UV-B-induced limitation. UV-B can cause decreases in the light-saturated CO2 assimilation rate in the absence of any major inhibition of the quantum efficiency of PSII photochemistry, thus demonstrating that UV-B inhibition of PSII photochemistry is not a ubiquitous primary limitation to photosynthesis (Middleton and Teramura 1993). UV-B radiation can induce stomatal closure directly by inhibiting K+ accumulation (Wright and Murphy 1982) as well as opening of stomata. However, the mechanism of this complex effect of UV-B is not clear (He et al. 2005). Allen et al. (1997) demonstrated that UV-B-induced decrease of CO2 assimilation rate was associated with reduction in the maximum carboxylation activity of Rubisco and this was confirmed by in vitro biochemical assays of Rubisco activity. UV-B induced reduction in both Rubisco activity and content (He et al. 1993; Fedina et al. 2007). The rate of RuBP regeneration can decline as a result of UV-B irradiation in the absence of any significant effects on quantum efficiencies of PSII photochemistry (Ziska and Teramura 1992). The inhibition of photosynthesis or electron transport under excess light or UV irradiation (Niyogi 1999) may elevate the photosensitization process as well as the formation of AOS in this way. The formation of singlet oxygen via photosensitization was suggested to play an important role in damaging the D1 protein (Hideg et al. 1994). The probable electron transfer from electron transport chain, especially in photosystem I (PSI), to molecular oxygen, the way to quench extensive energy is an alternative source of AOS. Photoreduction of molecular oxygen by primary electron acceptor in PSI complex is thought to be the main source of superoxide in illuminated chloroplasts. The rate of H2O2 production in the Mehler reaction is sufficiently high to cause an inhibition of CO2 fixation of up to 50% (Asada 1994). Although more attention has been focused on the production of AOS during photosynthesis, UV-B-induced damage in the respiration pathway may increase the electron transfer from the respiratory transport chain to molecular oxygen and thus results in the oxidative stress indirectly (Norbury and Hickson 2001). A research on etiolated tissue is indicative of a strong link between the photosynthetic apparatus and UV-B-induced gene expression (Jordan et al. 1994). This may, in part, account for the lack of UV-B effect on gene expression in etiolated tissue when photosystems are not functional. In etiolated seedlings, the degree of increase in UV-induced cyclobutyl pyrimidine dimers (CPD) levels was the highest, while the contents of UV-absorbing compounds were the lowest and no photorepair of CPD could be detected (Kang et al. 1998). In addition, the levels of AOS and antioxidants have been related to UV-B response at different developmental stages of photosynthetic apparatus (A-H-Mackerness et al. 1998). Photosystem II and to some extent, PSI may also be impaired (Okada et al. 1976). In PSII, ultraviolet-B radiation has been shown to inactivate primarily the water-oxidizing complex with additional damage to quinone electron acceptors and tyrosine donors (Renger et al. 1989; Vass et al. 1996). UV-B-induced impairment of photosynthesis resembled visible light-induced photoinhibition, being associated with enhanced degradation of the D1, and to a lesser extent, the D2 protein (Greenberg et al. 1997). It appeared that no significant replacement of the D2 occurred under UV-B stress (Babu et al. 1999).

Although most studies suggest that UV primarily affects D2 and D1 proteins of PSII, Baker et al. (1997) suggested that the primary damaging effect of UV-B on photosynthesis is not on PSII reaction centers, but on a range of important soluble enzymes in the chloroplast. On the other hand, it has been reported that solar UV-B filtering does not cause any change in the photochemical efficiency of PSII (Huiskes etal. 2001).

UV-B radiation caused reductions in the amount of chlorophyll, oxygen evolution, activity of PSII and CO2 fixation in barley seedlings (Fedina et al. 2003), chloroplast proteins, especially ribulose-5-bisphosphate carboxylase/oxygenase (Rubisco), light-harvesting chlorophyll a/b binding protein of PSII (Takeuchi et al. 2002). Allen et al. (1997) reported that the loss of Rubisco was a primary factor in UV-B inhibition of CO2 assimilation. According to Hidema et al. (1996), a reduction in Rubisco was greater in UV-sensitive than in UV-resistant strains. Takeuchi et al. (2002) showed that synthesis of Rubisco, but not LHCII, was significantly suppressed by UV-B.

13.6 DNA Damage and Repair

DNA is one of the major targets of UV damage, and UV-B radiation is capable of directly altering its structure. UV radiation induces lethal photodamage in DNA, resulting in the production of CPDs and pyrimidine (6-4) pyrimidone phoproducts [(6-4) products]. The majority of DNA damage consists of CPDs (approximately 75%) that are formed between adjacent pyrimidines on the same strand. Such DNA damage may be lethal or mutagenic to organisms and may impede replication and transcription (Brash et al. 1987; Sancar et al. 2004). DNA damage can be repaired by three kinds of reaction: photoreactivation of CPDs and 6-4 photoproducts by specific photolyase, nucleotide excision repair (dark repair) and recombination repair (homologous recombination - the removal of CPDs (Ries et al. 2000). Photore-activation is a light-dependent enzymatic process using UV-A and blue light to monomerize pyrimidine dimers: the enzyme photolyase binds to the photoproducts and breaks the chemical bonds of the cyclobutane ring and restores integrity of the bases. Photolyase is activated by light ranging from 300 to 600 nm (Sancar 1994). Photolyases of 6-4 photoproducts are expressed constitutively in etiolated seedlings (Chen et al. 1994; Hada et al. 1999), whereas the expression of CPD photolyases is frequently regulated by the light. Photorepair of CPDs has been reported in several plant species, including gingko (Trosko and Mansour 1969), Arabidopsis (Britt et al. 1993), alfalfa (Quaite et al. 1994), soybean (Sutherland et al. 1996), cucumber (Takeuchi et al. 1996), rice (Hidema et al. 1997), maize (Stapleton et al. 1997), and wheat (Taylor et al. 1996). CPD photoreactivation is the major pathway in plants for repairing UV-radiation induced DNA damage (Britt 1996). Studies in various plant species have shown that this photoregulation may involve phytochromes (Langer and Wellmann 1990), blue/UV-A (Hada et al. 1999), visible light (Ahmad et al. 1997; Kang et al. 1998), and UV-B-receptors (Ries et al. 2000). There is no information about the photocontrol of photolyase activity under natural conditions, when all these photoreceptors are simultaneously excited. Hidema et al. (2000) found that CPD photorepair ability is one of the main factors determining UV-B sensitivity in rice. Examination of 17 rice cultivars showed that the more resistant cultivars to UV-B exhibited higher photolyase activities in comparison to less resistant cultivars (Teranishi et al. 2004). Visible radiation included in the natural sunlight was sufficient to photorepair CPDs formed by solar UV-B radiation alone or solar plus supplemental UV-B. An increase in visible radiation during culture could enhance the capacity for photorepair in rice. The degree of photorepair of CPDs in the seedlings grown at high irradiance (350 ^mol m-2 s-1) was higher than that in the seedlings grown at low irradiance (50 ^molm-2 s-1). No photorepair of CPDs could be detected in etiolated dark-grown seedlings (Kang et al. 1998). In this connection, Langer and Wellmann (1990) observed differences in photoreacti-vating enzyme activity of CPDs between hypocotyls from etiolated and light-grown bean seedlings and concluded that the induction of CPD photolyase was under phy-tochrome control. Ahmad et al. (1997) have reported that the expression of PHR1 gene for photolyase in etiolated seedlings of Arabidopsis is induced by high white light. Takeuchi et al. (1996) have shown that a high activity of CPD photolyase was present in etiolated cucumber cotyledons.

In excision repair, dimmers are replaced by de novo synthesis in which the undamaged complementary strand is employed as a template. This multistep process involving multiple enzymes has been found to operate with only a low capacity in plants.

13.7 UV-B Defence-Flavonoids and Antioxidants

UV-B radiation causes an increased production of active oxygen species (AOS) (Smirnoff 1993; Rao et al. 1996; A-H-Mackerness et al. 1998; Costa et al. 2002) which include superoxide radicals (JO—), singlet oxygen (*O2), hydrogen peroxide (H2O2) and hydroxyl radical (OH+). The mechanism of singlet oxygen generation by UV radiation is not clear, but the process does not appear to be linked to the UV-induced damage of photosynthesis (Barta et al. 2004). Under UV-B irradiation, the generation of AOS is dependent on, but not proportional to, the dose of UV-B. The presence of photosynthetically active radiation (PAR, 400-700 nm) in the irradiation regime is important for photosynthetic organisms. It was found that AOS formation was higher when PAR was included. This suggests that photosynthetic electron transport chain and photosynthetic processes both contribute to the formation of AOS (Foyer et al. 1994a; Asada 1994). The overproduction of AOS is potentially toxic to cells and induces oxidative damage, while on the other hand, increased AOS may act as an alert signal to induce protective responses. It has been shown that H2O2 acts as a signal to induce defence gene expression (Desikan et al. 2000). As might be expected, some of these genes encode antioxidant enzymes, defence and stress-related proteins (Desikan et al. 2001). The antioxidant defence system includes enzymatic antioxidants, such as superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), ascorbat peroxidase (APX), dehydroascorbate reduc-tase (DHAR) and glutathione reductase (GR) and non-enzymatic low molecular weight antioxidants, such as ascorbat, glutathione, a-tocopherol and carotenoids (Ahmad 1995). The antioxidants, like ascorbat and glutathione participate in both enzymic and non-enzymic H2O2 degradation (Foyer et al. 1994b).

SOD (EC 1. 15. 1. 1) converts JO— radicals into H2O2 and O2. In plants, CAT (EC 1.11.1.6) is one of the main H2O2-scavenging enzymes that dismutates H2O2 into water and O2, and it is a constitutive component of peroxisomes (Corpas et al. 1999). CAT activity slightly increased at UV-B irradiation (Yannarelli et al. 2006), but the pattern of isoforms remained unchanged. APX (EC 1.11.1.11) is a specific peroxidase that catalyses the elimination of the toxic product H2O2 at the expense of oxidizing ascorbate to monodehydroascorbate. APX isoenzymes are distributed in at least four cells compartments: the stroma, the thylakoid membrane, the microbody and the cytosol (Asada 1992). Peroxidases (EC 1.11.1.7) are enzymes that catalyse the H2O2 -dependent oxidation of a wide variety of substrates, mainly phenolics (Dunford 1986), and they are often found in multiple molecular forms. The function of these isozymes and their regulation remain largely unknown. It was suggested that sunflower acclimatizes themselves to UV-B radiation by induction of different isoforms of POD (Yannarelli et al. 2006). After supplemental UV-B radiation, CAT and SOD activities enhanced; meanwhile APX did not change (Dai et al. 1997). In UV-B irradiated sunflower cotyledons, total APX activity was not modified, but their isozymes were clearly affected demonstrating a selective response of each isoform, presumable due to its location (Yannarelli et al. 2006). The induction of antioxidant enzymes with peroxidase activity (CAT and GPX) indicated that hydrogen peroxide participates actively on UV-B plant response (Rao etal. 1996).

13.7.1 Flavonoids

It has been reported that flavonoids and related phenolic compounds are specifically increased, when plants are exposed to enhanced UV-B radiation (Beggs and Wellmann 1994; Wagner et al. 2003) and were linearly dependent on UV-B influence (Cen and Bornman 1993). In plants, the protective role of flavonoid polypheno-lics in the expression of tolerance to UV-B radiation has been shown repeatedly (Li et al. 1993; Lavola et al. 2003). Flavonoid synthesis can be increased by elevating PPFD and UV-A levels (Cen and Bornman 1990). UV-A and blue light stimulates expression of the chalcone synthase gene of the flavonoid biosynthesis pathway (Jenkins et al. 1997; Wade et al. 2001). As very low irradiance is not inductive for chalcone synthase gene expression, the size of the irradiance may also be important (Bilger et al. 2007). In N. officinale, total flavonoid quantities were 10-fold lower in UV exposed young leaves compared to S. alba, in which flavonoid accumulation was induced by UV specifically in old leaves. In S. alba, relative contents of quercetin flavonols increased at the expense of kaempferols in UV exposed leaves. Hydroxycinnamic acid concentrations were not affected in both species (Reifenrath and Muller 2007).

Accumulation of phenolic compounds in epidermal cells is an useful tool for effective screening of UV-B radiation, thus protecting the mesophyll tissue (Bornman et al. 1997; Kolb et al. 2001). UV-absorbing compounds are mainly phenylpropanoids, such as cinnamoyl esters, flavones, flavonols, and anthocyanins esterrified with cinnamic acids. These compounds are likely to impart protection to the plants by absorbing radiation in the UV-B region of the spectrum (not absorbing photosynthetically active radiation) and thereby diminishing the penetration of UV radiation. In the pea (Pisum sativum) mutant Argenteum, whose epidermal cell layers can be removed easily and analyzed separately from the mesophyll, flavonol glycosides (putatively protective UV-B-absorbing compounds) were found to be located mainly (Weissenbock et al. 1986) or entirely (Hrazdina et al. 1982) in the epidermis. UV-B absorbing pigments are present all through the leaf, but accumulate significantly in adaxial epidermal cells (Cen and Bornman 1993). Olsson et al. (1999) showed that in Brassica napus, kaempferol glycosides were the most abundant flavonoid compounds of the adaxial epidermis, whereas the abaxial cell layer chiefly contained hydroxycinnamic acid derivatives. Quercetin glycosides were the compounds that were increased most in both epidermal cell layers in UV-B stressed plants relative to control plants (Olsson et al. 1999). The protecting action of flavonoid compounds is due to their strong absorbance in the range of 220-380 nm and their photostability. However, a little is known about the relative contribution of different phenolic compounds to the UV-B screening capacity of leaves. In this respect, the investigation of UV-B tolerance and resistance of flavonoid deficient mutants can throw more light on involvement of different classes of UV-B absorbing compounds. Two groups of higher plants can be distinguished in relation to flavonoid accumulation in different tissues. In the most of the dicotyledons (legumes, bean, soybean, pea etc.), flavonoids are usually situated in the epidermis. However, in monocotyledons (barley, oat, rye), the epidermis as well as mesophyll can accumulate flavonoids (McClure et al. 1986; Weissenbock et al. 1986). Protective responses are stimulated by UV-B radiation, including increased production of UV-B-absorbing compounds. Sensitivity to UV-B radiation is strongly parallel to the levels of constitutive and UV-induced flavonoids, thus demonstrating the protective role of flavonoids towards UV radiation. On the other hand, the response of plant to UV-B radiation depends also on development and physiological state of the plant and on other stress factors acting simultaneously with UV-B radiation. Temperature is a significant factor controlling biosynthesis of phenolic compounds and modulating UV-B screening and possibly also UV-B resistance (Bilger et al. 2007). As a results of exposure to UV-B, the content of total flavonoids increases in a time dependent manner. For barley plants, flavonoid accumulation starts 4 h after UV-B exposure and increases up to 120 h after radiation (Fedina et al. 2005). In the case of callus cultures of Lysimachia, continuous irradaiation with UV-B results in more vigorous increase at the first 24 h and reached its maximum at 72 h and slightly decreased thereafter

(Hollosy 2002). UV-B radiation stimulates the expression of the genes encoding phenylalanine ammonia-lyase, as the first stage of the phenylpropanoid pathway, and chalcone synthase, the key stage which commits the pathway to flavonoid synthesis (Bornman and Teramura 1993; Beggs and Wellmann 1994). In addition, they may offer an additional protection by having antioxidant activity (Brown et al. 1998). Kolb et al. (2001) observed that PSII was protected against UV-B damage by epidermal screening, related to increased leaf phenolics (A314 and A360), however, UV-B inhibition of CO2 assimilation rate was not diminished. According to Middleton and Teramura (1993), although both UV-B-absorbing compounds and carotenoids increased in response to UV-B irradiation, only carotenoids and not the UV-B absorbing compound (A300) could be related to protection of photosynthesis. Although some laboratory experiments have demonstrated that the concentration of phenolic compounds increases with increasing irradiance (Cen and Bornman 1990; Day 1993), the experimental data regarding the protective role of these compounds against UV-B radiation are still a few and speculative. An accumulation of certain phenolpropanoid compounds (such as flavonoids and anthocyanins) in the vacuoles of the epidermal and sub-epidermal cell layer, which is thought to act as UV-B filters, plays an important role in coping with UV-B-induced damage. Hada et al. (2003) have found that the higher accumulation of anthocyanins and UV-B absorbing compounds in rice plants did not effectively function as a shield to protect plants from supplementary UV-B radiation. Dai et al. (1995) also reported that the differences in the sensitivity to UV-B radiation among rice cultivars could not explain quantitative differences in flavonoid-shielding compounds. Markham et al. (1998) reported that flavonoids might play a more subtle role in plant UV-B protection than simple UV-B screening in a UV-B tolerant rice cultivars. Flavonoids act also as antioxidants (Gould et al. 2002). Thus, their importance in protecting mechanisms against UV-B induced biological damage in plants has been questioned.

13.8 Conclusion

UV-B radiation presents a potential risk for the plant growth, physiology, and quality of plant productivity. The threat to productivity in global agriculture due to stratospheric ozone depletion cannot be overstated, nor should it be overlooked. Attempts at quantitative and qualitative predictions of expected effects and the search for a suitable ameliorant or a stress alleviant are being met with mixed outcomes. One of the reasons for this is the limitation in controlled-environment studies. Results from greenhouse or growth-chamber studies and field studies on UV-B effects are often conflicting or difficult to interpret, because of unrealistically high UV irradiation levels, inadequate levels of UV-A, low PAR or other technical difficulties. Evidences do exist for quantitative and qualitative changes in crop yield. Plant breeding and genetic engineering for UV-B tolerance is an important aspect to be considered in order to avoid significant crop production loss. UV-B sensitive cultivars of many important plant species have been found in field and laboratory tests. In most cases, the origin of the sensitivity is unknown, making the design of bioengineering or breading programs for improving UV light resistance difficult. Identification of the receptors involved in perception of UV-B would be of great value and provides a means of manipulating UV-B responses. It is very important to perform studies under field conditions, at the different climates and latitudes, in which different cultivars are grown and where the UV-B quality is quite different. The effects of UV-B radiation on plants are strongly influenced by seasonal microclimate conditions. Unusual climatic conditions, such as lower temperature and less sunshine, enhanced harmful effects of UV-B. To such studies, should be added elevated levels of CO2. While such information is needed for direct effects on crop species, the studies must also include information about the possible long-term effects on growth, joint effects with other pollutants, incidence of pathogens and insect pests, intra-species competition, and crop-weed relationships. It appears that the effects of UV-B radiation on photosynthesis, growth, and development of plants are caused by altered gene action as consequences of UV-B damage of nucleic acids during the longer-term impact. This is currently a topic of intensive research. The ecological effects of UV-B at the community level are difficult to predict, as large variations occur between species. Perhaps the most pressing need at the moment is to obtain field information about the effects of UV-B.

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