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. 2006 Jun;97(6):933–942. doi: 10.1093/aob/mcl044

Sensitivity of Rice to Ultraviolet-B Radiation

JUN HIDEMA 1,*, TADASHI KUMAGAI 1
PMCID: PMC2803405  PMID: 16520342

Abstract

• Background Depletion of the stratospheric ozone layer leads to an increase in ultraviolet-B (UVB: 280–320 nm) radiation reaching the earth's surface, and the enhanced solar UVB radiation predicted by atmospheric models will result in reduction of growth and yield of crops in the future. Over the last two decades, extensive studies of the physiological, biochemical and morphological effects of UVB in plants, as well as the mechanisms of UVB resistance, have been carried out.

• Scope In this review, we describe recent research into the mechanisms of UVB resistance in higher plants, with an emphasis on rice (Oryza sativa), one of the world's most important staple food crops. Recent studies have brought to light the following remarkable findings. UV-absorbing compounds accumulating in the epidermal cell layers have traditionally been considered to function as UV filters, and to play an important role in countering the damaging effects of UVB radiation. Although these compounds are effective in reducing cyclobutane pyrimidine dimer (CPD) induction in plants exposed to a challenge exposure to UVB, certain levels of CPD are maintained constitutively in light conditions containing UVB, regardless of the quantity or presence of visible light. These findings imply that the systems for repairing DNA damage and scavenging reactive oxygen species (ROS) are essential for plants to grow in light conditions containing UVB.

• Conclusion CPD photolyase activity is a crucial factor determining the differences in UVB sensitivity between rice cultivars. The substitution of one or two bases in the CPD photolyase gene can alter the activity of the enzyme, and the associated resistance of the plant to UVB radiation. These findings open up the possibility, in the near future, of increasing the resistance of rice to UVB radiation, by selective breeding or bioengineering of the genes encoding CPD photolyase.

Keywords: Ultraviolet-B radiation (UVB: 280–320 nm), rice (Oryza sativa), cyclobutane pyrimidine dimer (CPD), CPD photolyase, reactive oxygen species (ROS), UV-absorbing compounds, UVB resistance, UVB sensitivity, photorepair, dark repair, bioengineering, selective breeding

INTRODUCTION

The depletion of stratospheric ozone, caused by the emission of chlorofluorocarbons (CFCs) and other gases, has resulted in increased amounts of ultraviolet-B radiation (UVB: 280–320 nm) reaching the Earth's surface (Blumthaler and Ambach, 1990). The global trend of increasing UVB radiation has been confirmed in response to stratospheric ozone loss in mid-latitude Japan (Sasaki et al., 2002), in New Zealand in the 1990s (McKenzie et al., 1999), and measurements of global ozone levels between the 1970s and 1990s, at high and mid-latitudes in both hemispheres indicated significant increases in UVB radiation (Madronich et al., 1995; Munakata et al., 2005). Furthermore, according to the report of the 2002 UNEP (United Nations Environmental Programme: Environmental effects of ozone depletion and its interactions with climate change), it will be several years before stratospheric ozone recovery can be confirmed unambiguously, although the concentrations of most of the anthropogenic gases causing the depletion are now decreasing (McKenzie et al., 2003).

The UV spectrum is divided into three regions: UVC (<280 nm), UVB and UVA (>320 nm). UVC, which comprises highly energetic wavelengths, is eliminated by the stratospheric ozone layer and is not encountered by plants. UVB radiation reaches the earth's surface. Incident UVB radiation (in particular, the waveband 297–310 nm) is increasing due to the reduction in the stratospheric ozone concentration (Caldwell et al., 1989). The UVA region of the spectrum is not attenuated by ozone, so the fluence will be unaffected by the reduction of the ozone layer. Even a small increase in incident UVB radiation can have significant biological effects, since UVB is readily absorbed by a number of important biological macromolecules, such as DNA and proteins. For example, in mammalian cells, UVB radiation has been shown to interfere with processes such as transcription and replication, resulting in reduction of RNA synthesis, arrest of cell cycle progression, and apoptosis (Sancar et al., 2004). Indeed, UVB radiation is a well-documented universal carcinogen (Brash et al., 1991; Ziegler et al., 1993, 1994).

How does UVB radiation affect biological processes in plants? Over the last two decades, extensive studies of the physiological, biochemical and morphological effects of UVB in plants, as well as the mechanisms of UVB resistance, have been carried out. Recently, researchers have begun to apply some of the lessons learned, in attempts to develop plant strains that will show increased resistance to damage in future UVB-enriched environments. In this review, we describe recent research into the genes which are potentially important to UVB radiation and the mechanisms of UVB resistance in higher plants, with an emphasis on rice (Oryza sativa), one of the world's most important staple food crops.

YIELD AND GRAIN DEVELOPMENT UNDER SUPPLEMENTARY UVB RADIATION

UVB radiation augmentation studies have identified many UVB radiation-sensitive cultivars of commercially valuable higher plants (Teramura et al., 1990, 1991; Sato and Kumagai, 1993; Correia et al., 1998). Teramura et al. (1990) examined the potential for changes in the yield and seed quality of two soybean cultivars, Essex and Williams, grown for six seasons in the field. The cultivar Essex was found to be sensitive to UVB radiation (yield reduction 20 %), while the cultivar Williams was tolerant. However, the effect of UVB radiation on yield was strongly influenced by seasonal variations in microclimate, such as temperature and the frequency of precipitation. Kumagai et al. (2001) investigated the effects of supplementary UVB radiation on the growth and yield of Japanese rice cultivars in a paddy field, at a middle latitude in Japan, over a 5-year period. They found that supplementary UVB radiation inhibited either growth and yield, or grain development. These inhibitory effects were enhanced significantly by unusual climatic conditions, such as lower temperature and reduced sunshine. Supplementary UVB radiation was also found to influence storage protein status in the rice grains; whereas grain size decreased significantly, total nitrogen and storage proteins (specifically glutelin) increased significantly (Hidema et al., 2005b). These results suggest that supplementary UVB may result in a change in the taste of the grain. Gao et al. (2004) investigated the effects of supplementary UVB radiation on the growth, yield and seed qualities of maize under field conditions. Increased UVB radiation caused a significant reduction in dry matter and yield, and affected seed quality as follows: protein, sugar and starch levels decreased, whereas lysine levels increased. Furthermore, solar UVB radiation exclusion studies have indicated that ambient levels of solar UVB radiation reduce biomass accumulation and grain yield in cucumber (Krizet et al., 1997), lettuce (Krizet et al., 1998), barley (Mazza et al., 1999) and soybean (Mazza et al., 2000). Taken together, the results of these studies suggest that the enhanced solar UVB radiation predicted by atmospheric models will result in reduction of growth and yield of crops in the future.

SENSITIVITY TO UVB RADIATION VARIES WIDELY AMONG RICE CULTIVARS

There is considerable intra- and interspecific variability in sensitivity of crop plants to UVB radiation, and the sensitivity of plants to UVB radiation varies widely among species and cultivars (Teramura et al., 1983; Bornman and Teramura, 1993; Correia et al., 1998; Mazza et al., 2000). Teramura et al. (1991) have shown that Asian rice cultivars differ in their responses to elevated UVB in terms of growth and physiological processes, and suggested that the geographical location where the cultivars had been cultivated might influence sensitivity to UVB radiation. Conversely, Barnes et al. (1993) and Dai et al. (1998) demonstrated that the geographical location where the cultivars had been cultivated had no discernible effect on sensitivity. Sato and Kumagai (1993) examined the sensitivity to UVB radiation of 198 rice cultivars, belonging to five Asian rice ecotypes (aus, aman and boro from the Bengal region, and tjereh and bulu from Indonesia) and Japanese lowland and upland rice groups. They found that sensitivity to UVB radiation varies widely among different cultivars belonging to the same ecotype and the same group. For example, among Japanese lowland rice cultivars, Sasanishiki (a leading variety) is more resistant to UVB radiation, while Norin 1, a progenitor of Sasanishiki, is less resistant (Kumagai and Sato, 1992). In addition, they found that rice cultivars originating from regions with higher ambient UVB radiation do not necessarily exhibit higher levels of tolerance. Many rice cultivars belonging to the Japanese lowland rice group, and the Indonesian boro ecotype, are resistant to UVB, while the more sensitive cultivars were found to belong to the aus and aman ecotypes from the Bengal region. It is speculated that spontaneous mutation of UVB sensitivity in rice has occurred throughout the various regions in which the crop has been cultivated.

REMARKABLE REDUCTION IN RUBISCO CONTENT CAUSED BY SUPPLEMENTARY UVB RADIATION

UVB radiation causes a multitude of physiological and biochemical changes in plants, including inhibition of photosynthesis (Teramura, 1983; Strid et al., 1990; Bornman and Teramura, 1993). This inhibititon is due to reduced levels of chlorophyll (Chl), chloroplast proteins such as Rubisco (ribulose-1, 5-bisphosphate carboxylase/oxygenase) and LHCII (light-harvesting chlorophyll a/b-binding protein of photosystem II) (Vu et al., 1982, 1984; Strid et al., 1990), and photosynthesis-related gene expression (Strid et al., 1996a, b; A-H-Mackerness et al. 1997a, b; 1999a, b). Allen et al. (1997) reported that loss of Rubisco is a primary factor in UVB inhibition of photosynthesis in oilseed rape. We showed that supplementary UVB radiation results in a reduction in the amounts of total leaf nitrogen, Chl, soluble protein and Rubisco in fully expanded leaves in rice (Hidema et al., 1996). Further, it was apparent that the UVB-induced reduction in Rubisco was greater in UV-sensitive, than in UV-resistant strains. These finding pose two questions: why did supplementary UVB radiation cause a marked reduction in Rubisco; and why was this effect greater in UV-sensitive, than in UV-resistant strains?

There are two potential primary mechanisms involved in UVB-induced physiological and biochemical damage. DNA lesions, such as cyclobutane pyrimidine dimer (CPD) and pyrimidine (6–4) pyrimidone photoproducts [(6–4) photoproduts], interfere with DNA replication and transcription (Britt, 1996). The second mechanism is through modification of proteins by photooxidation, or by reactive oxygen species (ROS) and free radicals produced during photosensitization (Caldwell, 1993; Foyer et al., 1994). These modifications include cross-linking, aggregation, denaturation and degradation (Andley and Clark, 1989; Kochevar, 1990; Wilson and Greenberg, 1993; Borkman and Mclaughlin, 1995; Wilson et al., 1995; Ferreira et al., 1996; Greenberg et al., 1996). Studies involving the effects of supplementary UVB radiation must take into account the natural changes in levels of Rubisco and other photosynthesis-associated proteins such as LHCII, caused by leaf ageing (Mae et al., 1983; Hidema et al., 1992). As an example, Takeuchi et al. (2002) examined the effects of supplementary UVB radiation on synthesis and degradation of Rubisco and LHCII in UV-sensitive (Norin 1) and UV-resistant (Sasanishiki) strains. They used 15N tracer, and mRNA levels, for both the small and large subunits of Rubisco (rbcS and rbcL, respectively) and LHCII (cab). The results demonstrated that Rubisco synthesis was significantly suppressed by UVB during early leaf developmental stages in the UV-sensitive cultivar, whereas LHCII synthesis was not. In addition, gene expression of rbcS, rbcL and cab was suppressed by UVB at the early stages just after the leaf had emerged from the stem in both cultivars; however, the degree of reduction in mRNA levels for these genes differed between the two, with the greater reduction occurring in the UV-sensitive cultivar. The results suggest that the difference in UVB sensitivity of Rubisco synthesis between the two cultivars is due to both transcriptional and post-transcriptional suppression, during the early stages of leaf development. In the same study, the authors found that degradation of Rubisco was enhanced by UVB at leaf maturation in both cultivars.

It has been reported that, in chloroplasts under illumination, the large subunit (LSU) of Rubisco is directly fragmented into two polypeptides by ROS (Ishida et al., 1998, 1999). Other authors have demonstrated that UVB-generated ROS induce photodamage to Rubisco (Caldwell, 1993), and that ROS cause proteolytic degradation of the LSU (Desimone et al., 1996, 1998). Thus, the generation of ROS is thought to be involved in UVB-induced degradation of Rubisco in rice. However, it should be noted that active growth draws to a close, and senescence begins, as the leaf reaches maturity. John et al. (2001) reported that, in Arabidopsis, exposure to UVB radiation induces expression of senescence-associated genes (SAGs), including SAG12, which encodes a cysteine protease (Lohman et al., 1994; Noh and Amasino, 1999). This result suggests that the formation of some kind of protease may also be involved in the enhancement of Rubisco degradation in rice (Callis, 1995).

SEVERAL GENES CONTROL THE DEGREE OF UVB SENSITIVITY

What genes are involved in controlling the UVB sensitivity of rice cultivars? A genetic analysis on the UVB sensitivity of rice, using progeny from a cross between UV-resistant (Sasanishiki) and UV-sensitive (Norin 1) strains, showed that UVB sensitivity is controlled by more than two major recessive genes (Sato et al., 1994).

Quantitative trait locus (QTL) analysis is a powerful tool for analysing genes affecting traits under multiple gene control, and has been employed in many studies investigating complex trait inheritance. Recently, the development of a high-density linkage map, based on DNA markers, has made it possible to detect QTLs associated with the inheritance of traits such as heading date in rice (Yano et al., 2000), disease resistance in tomato (Martin et al., 1993) and photoperiod sensitivity in Arabidopsis (Putterill et al., 1995). Sato et al. (2003) detected three QTLs associated with UVB resistance in rice, on chromosomes 1, 3 and 10, using backcross inbred lines (BILs) derived from a cross of a UV-sensitive indica cultivar (Kasalath) and a UV-resistant japonica cultivar (Nipponbare). Among the QTLs, qUVR-10 (the QTL for UVB resistance on chromosome 10) showed the largest allelic difference (the percentage of variance explained was approx. 40 %). Plants homozygous for the Nipponbare allele at qUVR-10 were more resistant to UVB than those that were homozygous for the Kasalath allele. In the following sections, we describe several factors controlling UVB sensitivity in rice.

WHAT ARE THE CRUCIAL FACTORS DETERMINING UVB SENSITIVITY IN RICE?

UVB-induced DNA damage and repair

DNA is one of the major targets of UV damage, and UVB radiation is capable of directly altering its structure. The two main photoproducts formed between adjacent pyrimidines on the same strand are the CPDs and the (6–4) photoproducts (Britt, 1996). CPDs account for the majority of the DNA damage (approx. 75 %); the (6–4) products account for most of the remainder (Mitchell and Nairn, 1989). Such damage may be lethal to simple or complex organisms (Brash et al., 1987), and may induce cancer in humans (Brash et al., 1991). It can also impede replication and transcription, a mechanism postulated to be responsible for the adverse effects observed in higher plants. There are two main mechanisms for DNA repair of CPDs and (6–4) photoproducts; ‘photorepair’ and ‘dark repair’. In photorepair, the enzyme photolyase mediates the repair of damaged DNA by binding to CPDs or (6–4) photoproducts in a lesion-specific manner, and forming a complex that is stable in the absence of light. Photolyases show substrate specificity for either CPDs (CPD photolyase) or (6–4) photoproducts (6–4 photolyase). When a photon in the wavelength range of 300–600 nm is absorbed, the reversion of the dimer to its constituent monomer pyrimidines is mediated by the enzyme, which is then released (Sancar, 1994; Nakajima et al., 1998). In dark repair, the photoproducts are removed from DNA by nucleotide excision repair (NER). This is a complex, multistep process, which involves the concerted action of approx. 30 proteins, to execute damage recognition, chromatin remodelling, excision of the damaged oligonucleotide, gap-filling DNA synthesis and strand ligation, in the correct order (Sancar et al., 2004). Photorepair and/or dark repair of DNA damage have been reported for a number of plant species (see Hidema et al., 2000, and citations therein). In higher plants, photorepair is thought to be the major pathway for the repair of UV radiation induced-DNA damage, since the rate of dark repair is slower than that of photorepair (Britt, 1999).

Spontaneously occurring mutations in the gene encoding CPD photolyase cause differential sensitivity to UVB in rice

The performance of photorepair may be a crucial factor in the ability of plants to withstand UVB-induced damage. Britt et al. (1993) showed that a UV-sensitive mutant of Arabidopsis, uvr1, exhibited normal CPD photorepair, but defective (6–4) photoproduct repair. Landry et al. (1997) demonstrated that another Arabidopsis UVB-hypersensitive mutant, uvr2-1, is deficient in photorepair of CPDs. An Arabidopsis UV-tolerant mutant, uvi-1, was found to have enhanced capacity for CPD photorepair and dark repair of (6–4) photoproducts (Tanaka et al., 2002). Our previous data showed that the capacity for CPD photorepair was significantly higher in a UV-resistant rice cultivar (Sasanishiki) than in a UV-sensitive cultivar (Norin 1) (Fig. 1) (Hidema et al., 1997; Hidema and Kumagai, 1998).

Fig. 1.

Fig. 1.

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UVB sensitivity, cyclobutane pyrimidine dimer (CPD) photorepair activity and the CPD photolyase gene of Sasanishiki, Norin 1 and Surjamkhi rice cultivars. (A) Effects of supplementary UVB radiation on growth of Sasanishiki ( japonica), Norin 1 ( japonica) and Surjamkhi (indica) cultivars, grown under visible radiation with (+UVB) or without (–UVB) supplementary UVB radiation, in a large growth cabinet (Hidema et al., 2005a). Supplementary UVB radiation had little effect on the growth of the Sasanishiki cultivar, but decreased growth and caused browning in leaves of both Norin 1 and Surjamkhi. (B) Organization of the Oryza sativa CPD photolyase gene, alignments of the nucleotide sequence, and corresponding amino acid sequences, of the rice cultivars Sasanishiki, Norin 1 and Surjamkhi. Alignment of the genomic sequence with corresponding cDNA sequences reveals 10 exons (open boxes) and nine introns (thin lines) in the coding region (Hirouchi et al., 2003). The nucleotide adenine at position 377 in exon 2, in Sasanishiki, is changed to a guanine in Norin 1 and Surjamkhi. Thus, the codon CAG, which encodes glutamine (Q), is mutated to the codon CGG, which encodes arginine (R). The nucleotide guanine at position 888 in exon 4 in Sasanishiki and Norin 1 is changed to a cytosine in Surjamkhi, i.e. the codon CAG encoding glutamine is mutated to CAC, which encodes histidine (H). Neutral mutations at positions 939 (C/T) and 1248 (T/A) do not alter the amino acid sequence from valine (V) and threonine (T), respectively (Teranishi et al., 2004; Hidema et al., 2005a).

Is the difference in the UVB sensitivity amongst rice cultivars due to differences in photorepair capacity? In order to determine the inheritance of characteristics exhibiting stronger resistance to UVB radiation in japonica rice cultivars, Teranishi et al. (2004) examined the correlation between UVB sensitivity and the capacity for CPD photorepair in 17 japonica rice cultivars (including four ancient strains) that were the progenitors and relatives of the UV-resistant (Sasanishiki) and UV-sensitive (Norin 1) strains. They found that the cultivars could be divided into two groups: a UV-resistant group, with higher CPD photorepair ability, similar to Sasanishiki; and a UV-sensitive group, with lower CPD photorepair ability, similar to Norin 1. Further, it was evident that the higher activity of CPD photolyase was due to a single amino acid change, which altered both the structure and activity of the enzyme (Fig. 1) (Teranishi et al., 2004). These results suggest the possibility that there are only two types of photolyase, ‘Sasanishiki type’ and ‘Norin 1 type’, in japonica rice cultivars.

On the other hand, many UV-sensitive rice cultivars belong to the aus ecotype from the Bengal region (Sato and Kumagai, 1993). Surjamkhi, a local variety of the aus ecotype, is more sensitive to UVB radiation than Norin 1 (Fig. 1A). The relative rates of CPD photorepair among three varieties were Sasanishiki > Norin 1 > Surjamkhi (Fig. 1A) (Teranishi et al., 2004; Hidema et al., 2005a). Figure 1B shows the organization of the O. sativa CPD photolyase gene, as well as the alignments of the nucleotide sequences, and the corresponding amino acid sequences, of the three cultivars. The sequences of the Sasanishiki and Norin 1 CPD photolyases differ by one nucleotide. The adenine (A) at position 377 (exon 2) in the Sasanishiki CPD photolyase allele changes to guanine (G) in the Norin 1 allele. This alteration leads to an amino acid change at position 126 (Sasanishiki, glutamine; Norin 1, arginine) (Teranishi et al., 2004). A photoflash analysis demonstrated that this mutation in Norin 1 altered the function of photolyase, resulting in a decreased rate of binding to CPD (Hidema et al., 2000). Conversely, the sequences of the Sasanishiki and Surjamkhi CPD photolyases differ at positions 377, 888, 939 and 1248. Among them, the nucleotide alterations at positions 377 and 888 lead to corresponding changes in the amino acid residues: the CAG codons at positions 126 and 296 in the Sasanishiki protein encode glutamine, whereas the CGG codon at position 126 in the Surjamkhi protein encodes arginine, and the CAC codon at position 296 in the Surjamkhi protein encodes histidine. The amino acid change at position 126 in Norin 1 CPD photolyase was also observed in the Surjamkhi CPD photolyase, but the deduced amino acid at position 296 in the latter also changes from glutamine to histidine. Thus, the reduced CPD photorepair activity in Norin 1 and Surjamkhi is the result of one or two changes in the nucleotide sequence of the photolyase-encoding gene.

Hidema et al. (2005a) carried out QTL analysis to test the linkage between CPD photolyase and UVB sensitivity, using F2 and F3 plants derived from crosses between UV-resistant (Sasanishiki) and UV-hypersensitive (Surjamkhi) plants. The results demonstrated that UVB sensitivity is a quantitative inherited trait, and the tight linkage of the CPD photolyase locus in a QTL explains a major portion of the genetic variation for this trait. Ueda et al. (2005) reported that qUVR-10, which showed the largest allelic difference among the QTLs associated with UVB resistance, encoded CPD photolyase, and that a structural/functional alteration of photolyase, due to the alteration of a single amino acid in the encoding sequence, led to a difference in sensitivity to UVB in the Nipponbare and Kasalath cultivars. These findings suggest that CPD photolyase activity is a crucial factor in the determination of UVB sensitivity in rice.

OTHER FACTORS ASSOCIATED WITH UVB SENSITIVITY IN RICE

UV-absorbing compounds

The accumulation of certain phenylpropanoid compounds (such as flavonoids and anthocyanins), in the vacuoles of the epidermal and subepidermal cell layers, plays a role in mitigating UVB-induced damage (Bornman and Teramura, 1993; D'Surney et al., 1993; Lois and Buchanan, 1994; Reuber et al., 1996; Bharti and Khurana, 1997). Li et al. (1993) showed that flavonoid-deficient mutants of Arabidopsis, in which the expression of chalcone synthase (tt4) or chalcone-flavanone isomerase (tt5) is blocked, were hypersensitive to UVB radiation. Conversely, an Arabidopsis mutant tolerant to UVB radiation showed constitutively elevated accumulation of flavonoids and other phenolics (Bieza and Lois, 2001). However, in the case of rice cultivars, it is questionable whether or not differences in UVB sensitivity can be related to varying foliar content of UV-absorbing compounds. Indeed, Teranishi et al. (2004) demonstrated no significant correlation between the two in 17 Japanese rice cultivars. Similarly, Dai et al. (1992) reported no significant correlation between sensitivity to UVB radiation and the accumulation of flavonoids among four rice cultivars; and Adamse and co-workers reported a similar result for two cucumber cultivars (UV-sensitive Poinsett and UV-insensitive Ashley) (Adamse et al., 1994; Adamse and Britz, 1996).

Kang et al. (1998) showed that UV-absorbing compounds in rice leaves were effective in reducing susceptibility to CPD induction by challenge UVB exposure, but had no effect on steady-state CPD levels during growth under chronic exposure to supplementary UVB radiation. Similarly, Stapleton and Walbot (1994) showed that flavonoids reduced the susceptibility to CPD induction by short-term UVB exposure, but that there was no difference in steady-state CPD levels between field-grown green and purple maize plants. Why does the accumulation of UV-absorbing compounds have no effect on reducing steady-state CPD levels during plant growth under chronic exposure to UVB radiation supplemented to visible radiation? Maekawa et al. (2001) produced near isogenic lines (NILs) for three rice purple leaf genes, Pl, Plw and Pli, with a genetic background of Taichung 65 (T-65), a normal rice variety from Taiwan. The Pl gene controls expression of chalcone synthase, the first enzyme of the flavonoid biosynthetic pathway (Dooner, 1983). Interestingly, the growth of the NILs (T-65 Pl) was reduced significantly by supplementary UVB radiation, despite an increase in accumulation of foliar anthocyanins and other UV-absorbing compounds. This result makes the isogenic line T-65 Pl well suited for use in investigating the role of anthocyanins and other UV-absorbing compounds in the response of rice to elevated UVB radiation levels. Using these two strains (T-65 and T-65 Pl), Hada et al. (2003) examined: (a) the relationship between changes in steady-state CPD levels and accumulation of flavonoids (anthocyanins and other UV-absorbing compounds) in leaves relative to leaf age; (b) the susceptibility to CPD induction by UVB radiation; and (c) the ability to photorepair CPDs. They showed that flavonoids functioned by effectively reducing susceptibility to CPD induction by a challenge UVB exposure, but not for the steady-state CPD levels during growth under chronic exposure to elevated levels of UVB radiation. The ability to repair CPDs using blue radiation was lower in the T-65 Pl than in T-65. However, there was no significant difference in the ability to photorepair CPD in the crude enzyme extracts of either strain, from which the flavonoids alone were removed. This might be due to the interception of the leaf-penetrating blue/UVA radiation by anthocyanins, with concomitant effects on CPD-photolyase activity. These results indicate that the balance of blue/UVA and UVB radiation levels reaching the tissues is important for sustaining steady-state levels of CPD photolyase activity during growth.

Reactive oxygen species-scavenging enzymes

UVB radiation also produces ROS such as superoxide, H2O2 and singlet oxygen (Andley and Clark, 1989; Takeuchi et al., 1996; Dai et al., 1997; Hideg et al., 1997; Kubo et al., 1999). The generation of ROS causes direct or indirect oxidative damage to DNA, proteins, membranes, lipids, etc. (Takeuchi et al., 1995; A-H-Mackerness, 2000; Booij-James et al., 2000). Karpinski et al. (1997) reported that an increased H2O2 level is detected simultaneously with the inhibition of photosynthesis by UVB radiation, suggesting that the UVB-induced oxidative burst of H2O2 is associated with the damage and degradation of the D1 and D2 proteins of the photosystem II reaction centre.

However, plants have several ROS-scavenging systems. ROS are rapidly dissipated by antioxidant enzymes, such as superoxide dismutase, catalase, ascorbate peroxidase and glutathione S-transferase, as well as by low molecular weight antioxidants such as ascorbate, glutathione and carotenoids (Asada et al., 1999; A-H-Mackerness, 2000). Furthermore, anthocyanins act not only as UV filters, but also as ROS scavengers (Gould et al., 2002). Enhancement of the ROS-scavenging system may produce UVB resistance in rice. Recently, Fujibe et al. (2004) reported that a methyl viologen-resistant Arabidopsis mutant (rcd1-2), which posessed enhanced activity of plastidic Cu/Zn superoxide dismutase and stromal ascorbate peroxidase [active oxygen species (AOS)-scavenging enzymes], exhibited an enhanced tolerance to short-term UVB supplementation treatment.

It has been reported that UVB radiation enhances the activities of ROS-scavenging enzymes and the accumulation of UV-absorbing compounds (Murali and Teramura, 1985), and that these enhancements are mediated at the level of gene expression, through a signal transduction pathway activated by UVB exposure (Strid, 1993; Christie et al., 1996; Rao et al., 1996; Takeuchi et al., 1996; Orozco-Cardenas et al., 2001). However, the signal transduction pathway is at present poorly understood. Recently, ROS and some plant hormones such as salicylic acid, jasmonic acid and ethylene have been shown to be key regulators of gene expression in response to UVB exposure (A-H-Mackerness et al., 1997b, 1999b; Surplus et al., 1998; Holley et al., 2003). A-H-Mackerness et al. (1999b) reported that an increase in ROS levels leads to the synthesis of salicylic acid, jasmonic acid and ethylene. The study indicated that ROS play a pivotal role as secondary messengers in a number of UVB signal transduction pathways among key regulators. Therefore, identification of ROS associated with the signal transduction pathway, and early events in the signal transduction pathway following UVB detection, might provide a useful bioengineering target for enhancement of the activity of ROS-scavenging enzymes and accumulation of UV-absorbing compounds.

DNA damage repair enzymes other than CPD photolyase

As described previously, CPD photolyase activity is a crucial factor determining UVB sensitivity in rice. In addition, it has been reported that several repair systems for UVB-induced DNA damage, other than CPD photolyase, are involved in Arabidopsis. Britt et al. (1993) showed that a UV-sensitive mutant of Arabidopsis, uvr1, had normal CPD photorepair, but defective repair of (6–4) photoproducts. A mutation in AtXPF (Gallego et al., 2000; Liu et al. 2000), AtXPG (Liu et al. 2001) or AtXPD (Liu et al. 2003), which are related to NER enzymes, results in UV sensitivity. The UV-sensitive mutant rev3-1 is deficient in a translesion synthesis DNA polymerase, DNA polymerase ζ (AtREV3) (Sakamoto et al. 2003). Conversely, a UV-tolerant Arabidopsis mutant has an enhanced capacity for dark repair of (6–4) photoproducts and CPD photorepair (Tanaka et al., 2002). Taken together, the results indicate that these repair enzymes are important for plants to grow under UVB radiation. However, it is still open to debate whether or not the repair systems described above are associated with UVB resistance in rice.

CONCLUDING REMARKS

This review has covered the various responses of rice plant to UVB radiation, as well as several of the factors involved in potential resistance to UVB radiation. Recent studies have brought to light the following remarkable findings. First, UV-absorbing compounds accumulating in the epidermal and subepidermal cell layers have traditionally been considered to function as UV filters, and to play an important role in countering the damaging effects of UVB radiation. Although these compounds are effective in reducing CPD induction in plants exposed to a challenge exposure to UVB, certain levels of CPD (i.e. steady-state levels) are maintained constitutively in light conditions containing UVB, regardless of the quantity or presence of visible light. In fact, excess accumulation of flavonoids (such as anthocyanins) reduces the amount of blue/UVA radiation reaching cells, and may sometimes lower the ability to photorepair damaged DNA. For example, purple rice is highly UVB sensitive, despite posessing elevated levels of anthocyanins in leaves. These results imply that the systems for repairing DNA damage and scavenging ROS are essential for plants to grow in light conditions containing UVB. There are two interesting reports in connection with this idea. First, a methyl viologen-resistant Arabidopsis mutant, with higher activities of ROS-scavenging enzymes, exhibits higher tolerance to UVB, and some kinds of anthocyanins function as ROS scavengers. Secondly, a variety of UV-sensitive and UV-resistant Arabidopsis mutants have been isolated recently that have mutations in their UVB-induced DNA damage repair enzymes. These mutants will facilitate study of the mechanisms of UVB tolerance at the molecular and cellular levels. Finally, CPD photolyase activity is a crucial factor determining the differences in UVB sensitivity between rice cultivars. The substitution of one or two bases in the CPD photolyase gene can alter the activity of the enzyme, and the associated resistance of the plant to UVB radiation. These findings open up the possibility, in the near future, of increasing the resistance of rice to UVB radiation, by selective breeding or bioengineering of the genes encoding CPD photolyase.

Acknowledgments

A part of our research described in this review was supported by Grants-In-Aid (nos 14704060 and 17510037 to J.H, and 15201010 and 16651019 to T.K.) for Scientific Research from the Ministry of Education, Science and Culture of Japan.

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