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Reviews and Opinions 1 Role of L-Ascorbic Acid in Rice Plants Ching Huei Kao * Department of Agronomy, National Taiwan University, Taipei 10617, Taiwan ROC ABSTRACT INTRODUCTION The role of ascorbic acid (AsA) in rice plants is reviewed. It is now well established that AsA in rice plants is biosynthesized through D-mannose/ L-galactose pathway. Monodehydroascorbate (MDHA) and dehydroascorbate (DHA) can be recycled to AsA by MDHA reductase and DHA reductase, respectively. AsA content in rice plants can be altered through manipulation of AsA biosynthetic or recycling pathways. Evidence is provided to show that AsA plays a critical role in regulating tiller formation, as well as in resistance to environmental stress. Key words: Ascorbic acid, Rice, Stress, Tiller. L-Ascorbic acid (AsA; vitamin C) or simply ascorbate, a naturally occurring compound, plays a multifunctional role in both plants and animals. AsA has a key role in keeping human health. In contrast to the most animals, humans are unable to synthesize AsA due to a mutation to the gene encoding L-gulono-1,4-lactone oxidase, the last enzyme in the AsA biosynthesis in animals (Gallie 2013a). Thus, plants provide the major source of AsA in human diet. AsA has many functions in plants, including preventing plants from reactive oxygen species (ROS) damage, cofactor of many enzymes, regulating cell division, cell expansion, cell wall metabolism, shoot apical meristem formation, root development, photosynthesis, leaf senescence, hormones (ethylene and gibberellins) biosynthesis, abiotic and biotic stress, and flowering time (Anjum et al. 2015, Gallie 2013a, Zhang 2013). Additionally, AsA can function as a precursor for the biosynthesis of oxalic and L-tartaric acid in certain plants (DeBolt et al. 2007). Compared with Arabidoposis, the role of AsA in rice plants is less well known. For the purpose of increasing our understanding the role of AsA in rice plants, several strategies have been used to alter endogenous AsA levels. In this review, an attempt has been made to show the role of AsA in growth, development, and stress tolerance in rice plants. 抗壞血酸與水稻生理 高景輝* 國立臺灣大學農藝系 摘要 本 文 旨 在 綜 合 討 論 抗 壞 血 酸 (ascorbic acid; AsA)在水稻所扮演之角色。目前已知水 稻抗壞血酸係經由 D-mannose/L-galactose 途徑合成。單脫氫抗壞血酸與脫氫抗壞血酸, 可經由單脫氫抗壞血酸還原及脫氫抗壞血酸 還原酵素作用轉變為抗壞血酸。水稻抗壞血 酸之含量可透過合成與回復(recycling)之途 徑而改變。證據顯示,抗壞血酸可調控水稻 分糱之形成及增加水稻對逆境之抗性。 關鍵詞︰抗壞血酸、水稻、逆境、分蘗。 * 通信作者, [email protected] 投 稿 日 期: 2014 年 10 月 23 日 接 受 日 期: 2014 年 12 月 16 日 作 物 、 環境 與生 物 資 訊 12:1-7 (2015) Crop, Environment & Bioinformatics 12:1-7 (2015) 189 Chung-Cheng Rd., Wufeng District, Taichung City 41362, Taiwan ROC BIOSYNTHESIS, TRANSPORT, OXIDATION, AND REYCLING OF ASCORBIC ACID AsA biosynthesis occurs in almost all plant tissues. A complex network for producing AsA through L-galactose (Gal), D-galacturonate, and myoinositol has been proposed (Smirnoff 2011,Venkatesh and Park 2014). It is now widely accepted that Gal pathway is the major plant pathway for AsA biosynthesis (Anjum et al. 2015, 2 Crop, Environment & Bioinformatics, Vol. 12, March 2015 Ishikwa et al. 2006, Smirnoff 2011, Venkatesh and Park 2014). Gal pathway is also named as Smirnoff-Wheeler pathway or D-mannose (Man)/Gal pathway. Man/Gal pathway of AsA biosynthesis consists of the formation of AsA from guanosine diphosphate mannose (GDP-Man), GDP-L-galactose (GDP-Gal), Gal, and L-galactono-1,4-lactone (GalL) (Fig. 1). All the genes involved in this pathway are well characterized. These genes encode GDP-D-mannose pyrophosphorylase (GMP), GDP-D-mannose-3’5’-epimerase (GME), GDP-L-galactose posphorylase (GGP), L-galactose-1-P phosphatase (GalPPase), L-galactose dehydrogenase (GalDH), and L-galactono 1,4-lactone dehydrogenase (GalLDH). Studies by Fukunaga et al. (2010) confirmed that Man/Gal pathway is responsible for the synthesis of AsA in rice shoots. They also found that the AsA synthesis in rice shoots is regulated by light and the promoter regions in genes encoding AsA biosynthetic enzymes (GalPPase and GallDH) contain light responsible cis-element. All enzymes except GalLDH in the pathway of AsA biosynthesis are located in the cytoplasm. GalLDH is located within the mitochondrion (DelBolt et al. 2007). Once the AsA is synthesized on the inner mitochondrial membrane, it is transported to different cellular compartments. AsA transport is possibly mediated by facilitated diffusion or active transport systems (Ishikawa et al. 2006). The transport of AsA from the source to sink tissues occurs via the phloem (Franceschi and Tarlyn 2002). Manipulation of AsA transport in the phloem may provide the useful approach to increase the AsA content of fruits and tubers. Ascorbate oxidase (AAO) and ascorbate peroxidase (APX) are enzymes responsible for the oxidation of AsA (Fig. 2). AAO is located in the apoplast (Pignocchi et al. 2003). It catalyzes the oxidation of AsA to monodehydroascorbate (MDHA) using oxygen. The modulation of AAO activity would result in the alteration of AsA accumulation. APXs are members of the class I family of heme peroxidases that catalyze the reduction of hydrogen peroxide to water with concomitant oxidation of AsA to MDHA (Terxeira et al. 2004). MDHA is reduced (or recycled) back to AsA by monodehydroascorbate reductase (MDHAR) using NADH/NADPH as electron donors (Fig. 2). MDHA can also disproportionate to AsA and dehydroascorbate (DHA) (Fig. 2). The rate of AsA turnover is relatively fast (Conklin et al. 1997, Pallanca and Smirnoff 2000), thus MDHA and DHA should be efficiently recycled to maintain the AsA pool size. AsA recycling by dehydroascorbate reductase (DHAR) is another means for a plant to recycle DHA into AsA (Fig. 2). If DHA is not recycled to AsA, it undergoes irreversible hydrolysis to 2,3-diketogulonic acid (Fig. 2). The importance of MDHAR- and DHAR-mediated mechanisms of AsA recycling has been excellently reviewed by Gallie (2003b). Fig. 1. AsA biosynthetic pathway in plants. Enzymes: 1,GMP; 2, GME, 3, GGP 4, GalPPase; 5, GalDH, 6, GalLDH. Fig. 2. Oxidation and recycling AsA in plants. Enzymes: 1, AAO; 2, APX; 3, MDHAR; 4, DHAR. Role of L-Ascorbic Acid in Rice Plants All together, the AsA pool size is dependent on the rate of AsA biosynthesis, ability of AsA transport, and rate of AsA oxidation as well as efficiency of AsA recycling. ASCORBIC ACID IS INVOLVED IN GROWTH AND TILLER FORMATIION OF RICE PLANTS GalLDH catalyzes the last step of the AsA biosynthetic pathway in plants (Anjum et al. 2015, Ishikwa et al. 2006, Smrnoff 2011, Venkatesh and Park 2014), thus this enzyme is a good candidate for controlling the variations in AsA contents of plants. Using silencing and overexpressing GalLDH techniques, Yu et al. (2010) have generated transgenic rice plants with very different levels of AsA. GalLDH-silencing and -overexpression rice plants indeed have low and high leaf AsA content, respectively, when compared with wild type (Liu et al. 2011, Yu et al. 2010). GalLDH-silencing rice plants display a reduced growth rate (plant height, root length, and leaf weight) (Liu et al. 2011). It appears that a lower leaf AsA content in rice plants suppressed for GalLDH contribute to lower growth rate. Smirnoff and Wheeler (2000) have proposed that AsA could influence cell growth. Little is known about the exact mechanisms by which AsA regulates cell growth in plants. Further studies by Liu (2013) demonstrated that GalLDH-silencing rice plants have higher level of abscisic acid (ABA) and jasmonic acid. Higher ABA contents have also been reported in AsA defective Arabidopsis mutant vtc1 (Pastori et al. 2003). It is possible that AsA in rice leaves could regulate the growth through interaction with plant hormones. Tiller number is one of key factors that determines rice grain yields (Wang and Li 2011). It has been shown that seed priming by soaking wheat seeds in AsA solution increases the number of tillers, fertile tillers, biological and grain yield (Jafar et al. 2012). Similar results were observed in wheat leaves sprayed with AsA (Amin et al. 2008). Rice tillers are specialized branches bearing panicle. Recent work by Liu et al. (2013) demonstrated that AsA-deficient rice plants exhibit a significantly reduced tiller number. In another report, they also showed that GalLDH-suppressed rice plants display a reduced 3 seed sets and thousand-grain-weight (Liu et al. 2011). All these results strongly suggest that the importance of AsA in determining rice yield. Strigolactones are now considered as a new class of plant hormone inhibiting shoot branching (Gomez-Roldan et al. 2008, Umehara et al. 2008). Recently, Cardoso et al. (2014) demonstrated that Japonica rice Azucena contains high strigolactone levels and is a low tillering cultivar, whereas Indica rice Bala is a low-strigolactone producer and is highly tillered. Strigolactones are compounds derived from carotenoids. It is not known whether the decline of carotenoids in AsA-deficient rice plants plays a role in the synthesizing strigolactones (Liu et al. 2013). ASCORBIC ACID AND STRESS TOLERANCE OF RICE Oxygen is essential for the existence of aerobic life, but toxic reactive oxygen species (ROS) including the superoxide anion, hydroxyl radical and hydrogen peroxide are generated in all aerobic cells during metabolic processes (Noctor and Foyer 1998). Injury caused by ROS, known as oxidative stress, is one of the major damaging factors in plants exposed to environmental stresses. AsA is the most abundant antioxidant in plants and plays a role in coping with oxidative stress (Noctor and Foyer 1998). The decrease in AsA content is prior to the occurrence of toxicity in the leaves of rice seedlings treated with Cd (Chao et al. 2010). AsA and GalL, the precursor of AsA biosynthesis, pretreatments significantly reduce Cd toxicity in the leaves of rice seedlings (Chao and Kao 2010). Similarly, heat shock-induced AsA accumulation in leaves of rice seedlings results in an increase in Cd tolerance (Chao and Kao 2010). AsA-deficient Arabidopsis mutant vtc2-1 (60% less AsA than wild type, Col-0) (Zechmann et al. 2011) showed high sensitivity to Cd than wild type (Koffler et al. 2014). However, recent work demonstrated that development of Cd toxic symptom is related to low subcellular glutathione content rather than AsA content (Koffler et al. 2014). It seems that low glutathione content rather than low AsA content in subcellular compartments is responsible for high Cd sensitivity in this AsA-deficient Arabidopsis. 4 Crop, Environment & Bioinformatics, Vol. 12, March 2015 Surface ozone pollution may cause reduction in rice yield (Sawada and Kohno 2009). Ozone exposure results in ROS production. GME is an important enzyme in AsA biosynthetic pathway. Frei et al. (2012) screened rice mutants for OsGME1 and identified a homozogous ‘TOS 17’ insertion mutant line (ND6172). This mutant, 20-30% lower AsA contents than wild type, exhibits a higher visible leaf damage upon ozone exposure. In an another report, Frei et al. (2010) also exposed two chromosome segment substitution lines (SL15 and SL41) of rice and their parent ‘Nipponbare’ to ozone at 120 nl l-1. SL15 and ‘Nipponbare’ are more sensitive to ozone damage than SL41. Using gene expression profiling by microarray hybridization, they identified a potential ozone tolerance gene which encodes AAO, an apoplastic enzyme responsible for AsA degradation. The putative AAO gene showed consistently lower expression in SL41 under ozone expression, which is linked to a higher concentration of apoplastic AsA in LS41 exposed to ozone. For maintenance of the AsA pool, AsA recycling is required. MDHAR and DHAR are two enzymes responsible for AsA recycling. Chen et al. (2003) confirmed that overexpression of DHAR in plants would increase AsA content through improved recycling. A cDNA encoding the rice DHAR was first cloned by Urano et al. (2000). The mRNA level of DHAR1, the protein level of Dharlp, and the DHAR activity in rice seedlings were elevated by high temperature, indicating the protection role of DHAR at high temperature. This cDNA was used in the generation of transgenic Arabidopsis expressing DHAR in the cytosol (Ushimar et al. 2006). The overexpress of this enzyme enhances resistance to salt stress (Ushimaru et al.2006). Martret et al. (2011) also used this DHAR gene to generate transgenic tobacco. They demonstrated that DHAR enzyme can be successfully expressed in the chloroplasts, leading to a significant enhancement in the ability of the plant to withstand cold and salt stress. Recently, Kim et al. (2013) investigated whether DHAR affects rice yield under normal environmental conditions. Their results indicate that OsDHAR1 overexpression in rice plants increases AsA content and enhances grain yield and biomass. Compared with the work of DHAR expression, few studies were conducted on the expression of MDHAR in rice. Sultana et al. (2012) demonstrated that overexpression of mangrove MDHAR in rice exhibits an increase in AsA content and enhanced tolerance to salt stress. APX plays an important role in scavenging ROS in plants. It is located in different cellular compartments. In rice, APX genes have been described: two cytosolic (OsAPX1 and OsAPX2), two putative peroxisomal (OsAPX3 and OsAPX4), and five chloroplastic isoforms (OsAPX5, OsAPX6, OsAPX7, and OsAPX8) (Hong et al. 2007, Teixeira et al. 2004, 2006). Recently, Lazzarotto et al. (2011) identified a new class of rice heme perxoidases, APX-R (APX-related), which is localized in both chloroplasts and mitochondria and functionally associated with APX. It has long been recognized that prior exposure to heat shock temperatures protect plants from the subsequent chilling stress (Saltveit 1991). Rice seedlings pretreated with heat shock temperature (42℃) for 24 h did not show the subsequent chilling injury (4℃) (Sato et al. 2001). Heat shock induction of the APX1 gene has been proved to be the cause of reduced chilling in rice seedlings (Sato et al. 2001). Overexpression of OsAPX1 in rice was later proved to be effective in enhancing tolerance to chilling at booting stage (Sato et al. 2011). Additionally, overexpression of OsAPX2 in transgenic Medicago sativa or Arabidopais improves salt tolerance compared with wild plants (Guan et al. 2012, Lu et al. 2007, Zhang et al. 2013). In contrast, down regulation of OsAPX2 gene results in rice seedlings sensitive to drought, salt, or cold stress, suggesting that rice cytosolic APX2 plays a critical role in stress tolerance (Zhang et al. 2013). CONCLUSIONS AND PERSPECTIVES AsA is now known to be biosynthesized through Man/Gal pathway in rice plants. AsA plays a critical role in scavenging stress-induced ROS. Several key genes in the AsA biosynthetic pathway have been introduced into rice plants through genetic engineering to increase the AsA content and consequently enhance tolerance to stresses such as chilling, salinity and drought. Of particular interest are the recent findings by Liu et al. (2013) who emphasized the importance of AsA in tiller formation of rice plants. Whether the Role of L-Ascorbic Acid in Rice Plants synthesis of strigolactones is related to the synthesis of AsA in rice plants will be the subject of further research. To maintain the AsA pool size, MDHA and/or DHA should be recycled to AsA. The studies of the role of MDHAR and/or DHAR are essential to generation of AsA for maintenance of ROS activity. To study whether coover-expression of OsMDHAR and OsDHAR to rice plants confers stress tolerance will be rewarding. Biochemical methods are generally used to analyze AsA content in stress-induced rice plants. AsA content is rarely available in individual cellular compartments. It would of great interest to understand the importance of subcellular AsA in enhancing stress tolerance. Apoplastic AsA is associated with many physiological functions such as cell division and elongation, and its homeostasis in the apoplast is easily disturbed. Studies of the changes in apoplastic AsA to DHA ratio and AsA transport across the plasmalemma in rice plants under stress conditions are thus required. ACKNOWLEDGEMENTS Research in the author’s laboratory has been supported by grants from the Ministry of Science and Technology (formerly National Science Council) of the Republic of China. REFERENCES Amin AA, ESM Rashad, FAE Gharib (2008) Changes in morphological, physiological and reproductive characters of wheat plants as affected by foliar application with salicylic acid and ascorbic acid. Aust. J. Basic. Appl. Sci. 2:252-261. 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