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Effects of Ultraviolet-B Radiation in Plant Physiology

Effects of Ultraviolet-B Radiation in Plant Physiology Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 − 15 Review DOI: 10.2478/agri-2021-0001 RANA NASSOUR , ABDULKARIM AYASH Al-Andalus University for Medical Sciences, Tartous, Syria Nassour, R. and Ayash, A. (2021). Effects of ultraviolet-B radiation in plant physiology. Agriculture (Poľnohospodárstvo), 67(1), 1 – 15. Over the past few decades, anthropogenic activities contributed to the depletion of the ozone layer, which increased the levels of solar ultraviolet-B (UV-B) radiation reaching the Earth`s surface. Generally, UV-B is harmful to all living organisms. It damages the cell`s Deoxyribonucleic acid (DNA), proteins, and lipids, and as a consequence, it affects the bio-membranes negatively. In this review, we summarize the major effects of UV-B in the plant`s main molecules and physiological reactions, in addition to the possible defence mechanisms against UV-B including accumulating UV-B absorbing pigments to alleviate the harmful impact of UV-B. Key words: ultraviolet-B radiation, reactive oxygen species, respiration, photosynthesis, phenolic compounds Solar radiation is a part of the electromagnetic field Ultraviolet (UV) radiation comprises three types and is considered an essential condition for life on of waves varying by their wavelengths and energy: Earth. The electromagnetic spectrum includes differ- UV-C (100 ‒ 280 nm), UV-B (280 ‒ 320 nm), and ent types of waves; gamma radiation (<0.1 nm), X-rays UV-A (320 ‒ 390 nm). UV-C has the highest energy (0.1 ‒ 100 nm), ultraviolet radiation (100 ‒ 390 nm), level and it is the most hazardous part of the ultravi- visible waves (390 ‒ 780 nm), infrared radiation olet radiation. Luckily, it is completely absorbed by (780 nm ‒ 1 mm), microwaves (1 mm ‒ 1 cm) and ra- the atmospheric oxygen (O ) and stratospheric ozone dio waves (1 cm – 100 km) (Sliney & Chaney 2006; (O ), while most of the UV-B radiation is absorbed Mandi 2016; Zwinkels 2016). efficiently by O , and UV-A is fully transmitted to Although visible light forms only a very small the Earth’s surface to a large extend (Madronich et part of the entire sun`s electromagnetic spectrum, it al. 1998; Mandi 2016). In this context, the ozone provides the energy needed for plants to perform pho- acts as a natural barrier to the Earth from sunlight tosynthesis, the most important process for the pro- and its effects. It blocks and isolates harmful UV duction of reduced carbon (e.g. carbohydrates, amino radiation before it reaches the surface of our planet, acids, fatty acids, etc.) and oxygen. That makes pho- damaging the cells of humans and other organisms. tosynthesis the main source of building blocks and The stratospheric ozone is continuously pro- energy-supplying molecules in living organisms. duced and broken down according to a natural pro- Rana Nassour (*Corresponding author), Department of Basic Science, Faculty of Pharmacy, Al-Andalus University for Medical Sciences, Tartous, Syria. E-mail: ranahn1985@gmail.com Abdulkarim Ayash, Department of Basic Science, Faculty of Pharmacy, Al-Andalus University for Medical Sciences, Tartous, Syria. E-mail: abdulkarimayash@gmail.com © 2021 Authors. This is an open access article licensed under the Creative Commons Attribution-NonComercial-NoDerivs License (http://creativecommons.org/licenses/by-nc-nd/4.0/). 1 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 − 15 cess with dynamic equilibrium, via oxygen pho- in various subcellular sites, including mitochondrial tolysis by short ultraviolet radiation (UV-C shorter respiration, photosynthesis, and photo-respiratory than 250 nm). The released atomic oxygen (O) reactions (Mhamdi & Breusegem 2018). then bonds with molecular oxygen (O ), resulting Plants possess an antioxidant system to protect in ozone (O ). The O is then broken down by long their cells from ROS. The major antioxidants are en- 3 3 ultraviolet radiation (UV-B) to produce O and O, zymes, including superoxide dismutase (SOD), cat- according to the following equations (Häder 1991; alase (CAT), various peroxidases like ascorbate per- Mandi 2016): oxidase (APX), and glutathione peroxidase (GPX). Besides, there are some low molecular weight anti- short UV radiation (>250 mm) O 2O oxidants (LMWAs) in plant cells, such as ascorbate (vitamin C), tocopherols (vitamin E), β-carotene, 2O 2O + 2O 2 3 and phenolic compounds such as the flavonoids (Ren et al. 2006; Hatier & Gould 2009; Reboredo long UV radiation (UV-B) & Lidon 2012; Zlatev et al. 2012; Fu & Shen 2017; 2O 2O + 2O Zhang et al. 2017; Bhattacharjee 2019). Unfortunately, the ozone layer has been undergo- ROS formation increases in the plant cell under ing a gradual decline in its quantity for nearly four stress conditions, such as ultraviolet radiation due to decades due to gaseous pollutants, such as chlo- their high-energy photons that damage the cell struc- rinated fluorocarbons (CFCs), chloroform, hydro- ture (oxidize proteins, lipids, and other biomole- chlorofluorocarbons (HCFCs), carbon tetrachloride, cules), disrupt the functionality and integrity of en- methyl bromide, and reactive nitrogen species (ni- zymes and cell membranes, and cause an imbalance tric oxide, nitrous oxide, etc.) (Rastogi et al. 2014; in the redox reactions. So, a considerable part of the Sreelakshmi & Raza 2014; Mandi 2016). These sta- electrons leaks from electron transport systems to ble compounds can remain in the upper atmosphere ), reducing it to superoxide free radical oxygen (O •- for millions of years (20 ‒ 100 million years), where (O ) (Hideg et al. 2013; Bhattacharjee 2019; Dmi- chlorine and bromine atoms are released from them trieva et al. 2020). via UV. Each atom, which acts as a free radical, is In general, it is agreed that chloroplasts are the capable of initiating a series of reactions that can major sources of ROS in the plant cell, particular- destroy more than 100,000 ozone molecules. This ly under illumination, while the mitochondria are significant destruction of O reduces the UV absorp- the main source of ROS in the darkness and non- tion efficiency, so more of this radiation reaches green parts of the plant. The excitation of oxygen the surface of the Earth (1% reduction of O causes (O ) produces singlet oxygen ( O ), while reduction 3 2 2 •- 1.3 ‒ 1.8% increase of UV-B on the Earth’s surface) produces superoxide radicals (O ), hydrogen per- (Caldwell & Flint 1994; Sivasakthivel & Reddy oxide (H O ), and hydroxyl radicals (OH ), (Fig- 2 2 2011; Lidon et al. 2012). ure 1) (Mhamdi & Breusegem 2018). Chloroplasts 1 •- It`s worth noting that due to the ban of hydro- produce O , O and H O during photosynthetic 2 2 2 2 chlorofluorocarbons according to the 1987 Mon- electron transport, whereas mitochondria produce •- treal Protocol, the ozone layer is about to recover, O mainly at complex I and III of electron transport although there is still a long way to go (Chipperfield chain (Bhattacharjee 2019; Huang et al. 2019). The et al. 2017). Still, latitudes between 60° S and 60° N latter can be explained by the direct reduction of oxy- •- did not show recovery for unclear reasons (Ball et gen to O in complex I (the flavoprotein region of al. 2018). NADH (reduced nicotinamide adenine dinucleotide) dehydrogenase segment). Regarding complex III UV-B INDUCES REACTIVE OXYGEN SPECIES (the ubiquinone-cytochrome region), it is believed PRODUCTION that fully reduced ubiquinone donates an electron to Reactive oxygen species (ROS) are toxic cytochrome C1 and leaves an unstable highly reduc- by-products generated during metabolism, even un- ing ubisemiquinone radical that is favourable for the •- der natural conditions. They are produced in plants electron leakage to O and, hence, to O formation 2 2 2 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 − 15 (Bhattacharjee 2019). The increased production of posed to UV exhibit a decline in photosynthesis, ROS in living organisms under stress conditions is protein synthesis, and other biochemical processes. very toxic because it can react with vital biomol- These impairments lead to the reductions in plant ecules, altering and reducing their biochemical ac- height, dry weight, leaf area, relative growth rate, tivities, causing oxidative damage and eventually and total biomass (Caldwell et al. 2007; Kumari et resulting in cell death (Jithesh et al. 2006; Piri et al. al. 2009; Piri et al. 2011; Reddy et al. 2013; Bacelar 2011; Pessoa 2012; Zlatev et al. 2012; Kataria et al. et al. 2015; Reyes-Díaz et al. 2016; Fina et al. 2017; 2014; Yokawa et al. 2016) Fu & Shen 2017; Rai & Agrawal 2017; Neugart & Schreiner 2018; Parani & Vidhya 2018; Alves & De- UV-B EFFECTS IN PLANTS schamps 2019; Alemu & Gebre 2020), an increase Although UV-B is just a small fraction of the in the leaf thickness and downward leaf curling (Go- electromagnetic field, it adversely affects the lives laszewska et al. 2003; Bacelar et al. 2015; Rai & of all living organisms, including plants. Plants ex- Agrawal 2017), and a decline in transpiration rate, Figure 1. Oxygen-derived reactive oxygen species (Mhamdi & Breusegem 2018) ‒ + 2+ Note: e ‒ electron; 2H ‒ 2 protons; Fe ‒ iron divalent ion; t ‒ the half-life time; µs ‒ microsecond; ns ‒ nanosecond; 1/2 ms ‒ millisecond 3 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 −15 beside a delay in flowering and fruiting (Bassman et sensitive to ROS; since hydroxyl radical and singlet al. 2003; Reddy et al. 2013; Rai & Agrawal 2017). oxygen can react with methylene groups of PUFA In addition, many studies referred to the negative and form lipid peroxy radicals and hydroperoxide. impact of UV-B on stomatal conductance, which re- In their turn, the peroxy radicals can abstract hydro- duces the amount of CO available for photosynthe- gen from other unsaturated fatty acids, leading to sis (Cechin et al. 2007; Lidon et al. 2012; Bacelar a chain reaction of peroxidation (Nasibi & M-Kalan- et al. 2015; Cechin et al. 2018; Reyes et al. 2018; tari 2005; Vass et al. 2005; Rastogi et al. 2014; Shar- Reyes et al. 2019). ma et al. 2014; Kumar et al. 2018). Based on the above, the negative impact of UV-B effects in cellular compounds UV-B causes destruction of biomembranes (cellu- UV-B forms a small part of the electromagnetic lar membranes, mitochondrial membranes (cris- field, yet it is very energetic affecting and modifying tae), thylakoids, tonoplast, etc.), because each one a wide range of important biochemicals and break- of these membranes consists of a bilayer of phos- ing them into smaller molecules. That makes it de- pholipids with proteins interspersed throughout. structive for the organism’s life in general. Therefore, any damage to the components of these Proteins: UV-B has negative effects on structur- membranes will lead to rupture them and disrupt the al and functional proteins. It destroys the peptide biochemical reactions in them (Bidlack & Jansky bonds in the protein and breaks them into polypep- 2018). tides. Proteins highly absorbance to UV-B (around Carbohydrates: they are the main product of pho- 280 nm) is due to the absorbance of their aromatic tosynthesis. Carbon is fixed in C3-plants within Cal- amino acids (such as tyrosine, phenylalanine, tryp- vin cycle in the form of phosphorylated triose and tophan, histidine, and cysteine), so they are consid- then convert to glucose, which binds to each other ered as one of the main targets for UV-B (Nawkar et to be stored as polysaccharides. UV-B causes a steep al. 2013; Parihar et al. 2017). drop in total carbohydrate content either directly by Proteins may undergo photomodification direct - inhibition of enzymes involved in the Calvin cycle, ly through photooxidation reactions or indirectly by or indirectly by inhibition of the photochemical re- the photosensitized production of reactive oxygen actions required to produce NADPH + H and ATP species (ROS) and free radicals. Ultraviolet radia- needed for the Calvin cycle (Prasad et al. 1998; tion modifies the structure of amino acids, which Bhandari & Sharma 2006; Ganapathy et al. 2017; leads to protein denaturation and enzyme deactiva- Kurinjimalar et al. 2019; Reyes et al. 2019). tion. This can be due to UV-B destruction of aromat- ic amino acids (free and within proteins), or to its Deoxyribonucleic acid (DNA): UV-B damages effect on the disulphide bonds (S-S) in amino acids, nuclear, mitochondrial, and chloroplast DNA by in- which contain a sulfhydryl group in their reaction direct oxidative stress or direct absorption of purines centre (Hollosy 2002; Vass et al. 2005; Xue et al. and pyrimidines to these wavelengths (between 2005; Castenholz and Garcia-Pichel 2012; Nawkar 220 ‒ 300 nm), although pyrimidines are more af- et al. 2013; Wang et al. 2017). fected. DNA lesions induced by UV-B include di- mers between two adjacent pyrimidine bases, cis- Lipids: When exposed to UV-B, lipids under- syn cyclobutane pyrimidine dimers (CPDs), espe- go lipid peroxidation whether they are glycolipids, cially thymine dimers (TTs) and pyrimidine (6 – 4) phospholipids, or unsaturated fatty acids. UV-B pyrimidone photoproducts [(6 – 4)PPs] (Draper & exposed phospholipids are sensitive to ROS in two Hays 2000; Sinha et al. 2001; Frohnmeyer & Staiger sites: the unsaturated double bond between the car- 2003; Roleda et al. 2006; Babele et al. 2012; Pfeifer bon atoms and the ester bond between glycerol and & Besaratinia 2012; Nawkar et al. 2013; Rastogi et fatty acids (Kramer et al. 1991; Moorthy & Kathire- al. 2014; Gill et al. 2015; Li et al. 2015; Robson et san 1998; Hollosy 2002; Bhandari & Sharma 2006; al. 2019). These DNA lesions together can act as the Noaman 2007; Pérez et al. 2012; Ganapathy et al. principal cause of UV-B induced growth inhibition 2017; Wang et al. 2017). Polyunsaturated fatty acids in plants. Additionally, these photoproducts block (PUFAs) in the membrane`s phospholipids are also 4 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 − 15 the activity of DNA and RNA polymerases along the reaction centres (Bornman 1989; Takeuchi et al. the DNA strand, which inhibit replication and tran- 2002; Kataria et al. 2014). scription, respectively, and can lead to genetic code UV-B reduces the content of photosynthetic pig- misreading and causing mutations and death (Sinha ments in the chloroplast, especially chlorophyll a, et al. 2001; Takahashi et al. 2015; Jansen 2017). which is considered the principal pigment in pho- UV radiation causes a decline in the cell divi- tosynthesis (Qi et al. 2003; Gupta et al. 2008; Juo- sion rates as well as in cell number. This can be due zaityte et al. 2008; Lidon & Ramalho 2011; Singh to the genetic material destruction and disrupting & Singh 2014; Sztatelman et al. 2015; Ayash et transcription processes (as mentioned above) be- al. 2017; Fu & Shen 2017; Sebastian et al. 2018). side inhibition of protein synthesis in G1 ‒ S phases This loss in chlorophyll can be attributed to proto- of the cell cycle (Buma et al. 1996; Nogués et al. chlorophyllide photoreduction to chlorophyllide by protochlorophyllide oxidoreductase during the early 1998; Hopkins et al. 2002; Juan et al. 2005; Gill et stages of chlorophyll biosynthesis, as well as chlo- al. 2015). Jiang et al. (2011) implied that UV-B-in- rophyllase induction, which is responsible for chlo- duced G1 to S arrest may be a protective mechanism rophyll breakdown (Agrawal 1996; Marwood & that prevents cells with damaged DNA from divid- Greenberg 1996; Pradhan et al. 2006; Sakalauskaite ing and may explain the plant growth inhibition un- et al. 2013; Ganapathy et al. 2017; Rai & Agrawal der increased solar UV-B. Besides, UV-B-treated 2017). cells age more quickly than those of the controls Concerning carotenoids, they are photosynthetic (Hopkins et al. 2002). accessory pigment. They invariably increase in re- Effect of UV-B in respiration sponse to UV-B (Kurinjimalar et al. 2019). A very few studies investigated the impact of Effects of UV-B in the thylakoid membranes UV-B on respiration. Under UV-B stress, respi- The thylakoid membranes consist of a bilayer of ration increase significantly in the plant cell. This phospholipids with proteins interspersed through- increment can be explained by the rise of energy de- out. UV-B destroys the basic components of these mands, which is used in protection and repair mech- membranes (proteins and phospholipids), leading to anisms, including the increase of the leaf thickness rupture them partially or completely, thus prevent- and phenolic compounds biosynthesis (Gwynn- ing the binding of electron acceptors, and disrupting Jones 2001; Bassman & Robberecht 2006; Suchar photoelectron transport (Sinha et al. 2001; Lidon & & Robberecht 2016). Ramalho 2011; Kataria et al. 2014; Allorent et al. Effect of UV-B in photosynthesis 2016; Bidlack & Jansky 2018). Based on the mentioned above, many studies Photosynthesis is the most important process in revealed that UV-B increases the permeability of the plant, because it is the main source of organic thylakoids membranes, which causes protons leak- matter on our planet, besides being responsible for age to stroma and lowers ATP synthesis rates (Sala- producing and releasing oxygen to the Earth’s at- ma et al. 2011; Zlatev et al. 2012; Rai & Agrawal mosphere, which is essential for the respiration of 2017). Also, swelled, disintegrated, and scattered aerial organisms. UV-B affects photosynthetic ap- thylakoids and the absence of grana can be noticed paratus in many sites as the following: under UV-B stress (Yu et al. 2013). Effects of UV-B in pigmentation Effects of UV-B in light reactions Photosynthetic pigments are bound to structural PSII: PSII is a multifunctional pigment-protein proteins in the thylakoid membranes in higher complex embedded in the thylakoid membranes, plants and algae to form Light-harvesting complex- especially in the grana regions of the chloroplasts. es (LHCs) within photosystem II (PSII) and photo- This complex contains more than 20 protein sub- system I (PSI). Researches indicate that high inten- units and redox components that mediate light-in- sity of UV-B leads to a functional disconnection be- duced electron transport (Vass et al. 2005). Many tween LHC and photosystems (particularly within negative effects of UV-B have been reported in dif- PSII), which impairs the absorbed energy transfer to 5 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 −15 ferent sites of PSII, including the following: to S3 due to increased susceptibility to absorp- • Oxygen evolving complex (OEC): It is located in tion of these rays, which may result in the sepa- the lumenal side of the thylakoids, and includes ration of the Mn-OH bond and the formation of four manganese atoms and one calcium atom the hydroxyl radical and thus obstruct the release forming a Mn Ca cluster (Najafpour & Govindjee of oxygen (Sicora et al. 2006; Szilárd et al. 2007; 2011). According to Kok scheme, Mn shifts be- Vass 1996; Vass 2012; Kataria et al. 2014; Allor- tween five states during water oxidation (S0, S1, ent et al. 2016; Ayash et al. 2018; Mosadegh et S2, S3, S4), releasing one proton and one elec- al. 2019). tron in each state. The outcome of this process is • D1 protein: It is one of the most important struc- the evolving of four electrons, four protons, and tural protein (38.021 kDa) of PSII, binding essen- an oxygen molecule (Figure 2). Various stud- tial electron transporters such as tyrosine (Tyr-Z) ies indicated that UV-B might inhibit the OEC (Barber 2014). Under UV-B, D1 is degraded complex directly by absorbing this radiation via to a 20 kDa fragment which is subsequently the Mn cluster, which breaks the bonds between completely degraded by proteases enzymes in the manganese atoms, or by damaging the inter- a light-dependent manner (Bergo et al. 2003). mediates of the water evolving process. There is Besides the stability decrement of D1 and imbal- a gradual increase of UV-B sensitivity from S0 ance between its synthesis and breaking down Figure 2. S-state Kok scheme (Yano & Yachandra 2014) ‒ + Note: hv ‒ light; µs ‒ microsecond; ms ‒ millisecond; e ‒ electron; H ‒ proton; F ‒ flash 6 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 −15 rates, as the amount of ROS increases (in par- PSII and reduces plastocyanin (PC ‒ the electron ticular the active atomic oxygen) (Booij-James donor for PSI) (Vass et al. 2005). The previous stud- et al. 2000; Beardall & Raven 2004; Holzinger & ies suggest that the Cyt b /f complex is the least af- Lütz 2006; Cai et al. 2016; Tilbrook et al. 2016; fected thylakoid component by UV-B, which can be Parihar et al. 2017). explained by the fact that Cyt b /f complex contains • Tyrosine: Released electrons from OEC are trans- two quinine binding sites (one of them for quinol ferred to the reaction centre (RC) of PSII (P680) oxidation and the other for quinone reduction). Be- via a redox-active tyrosine residue (Tyr-Z) of the sides the UV-B minor sensitivity for genes encoded D1 protein. PSII contains another redox-active in the chloroplast, such as subunit IV of this com- tyrosine, called Tyr-D (on the D2 subunit) which plex (Kataria et al. 2014; Parihar et al. 2017). can donate electrons to P680, but is not involved PSI: PSI of higher plants contains approximately in electron transfer from OEC (Sicora et al. 15 protein subunits. PsaA and PsaB (each ≈80 kDa) 2003). Under UV-B, tyrosine may be inactivated form the central heterodimer of the reaction centre and/or photo-oxidized to 3,4-dihydroxyphenyla- and most of the electron carriers and pigments of lanine (DOPA) and form di-tyrosine as a result LHCI are bound to them (Niyogi et al. 2015). Un- (Vass 1996; Vass et al. 2005; Parihar et al. 2017). even distribution of the effect of UV-B has been • D2 protein: It is considered an essential struc- demonstrated by various studies to display minor or tural protein (39.418 kDa) of PSII, binding cru- no effects on PSI compared to PSII (Hollosy 2002; cial electron transporters, such as plastoquinone Kataria et al. 2014; Parihar et al. 2017). This can (PQ) (Barber 2014). A significant decrease in be attributed to the significant down-regulation of D2 content is reported in the exposed to UV-B many genes encoding PS I protein subunits in UV- thylakoids (Booij-James et al. 2000; Tilbrook et B-exposed cells (Kataria et al. 2014). al. 2016; Parihar et al. 2017). ATPase complex: The ATPase is a large (400 kDa) • Plastoquinone: It is the mobile charge carrier re- enzyme complex responsible for adenosine triphos- sponsible for the electron transport from PSII to phate (ATP) synthesis. It consists of two parts: a hy- /f (Cyt b /f). PQ is double reduced cytochrome b 6 6 drophobic membrane-bound portion called coupling and takes up two protons from the stroma to be- factor O (CFo) and another portion that sticks out come quinol (PQH2). Then, the lipophilic PQH2 into the stroma called coupling factor 1 (CF1). CFo is separated from protein D1 and moves within forms a channel across the membrane for protons the lipid bilayer of the thylakoid membrane, to pass through. CF1 is responsible for binding in- transferring the electrons to Cyt b /f, releasing organic phosphate (P) to adenosine diphosphate protons into the lumen, and returning to the oxi- (ADP) to produce ATP. It is made up of several dized form (PQ) (Eerden et al. 2017). Since main peptides; including three copies of each of α and ß absorption of quinones in the UV region (oxi- peptides arranged alternately (Taiz & Zeiger 2010). dized PQ: 250 nm, redox PQ; quinol (PQH2): ATPase is significantly affected by UV-B, as the 280 nm and semiquinone (PQH): 320 nm), amount of coupling factor (CF1) decreases, as well they can be destroyed, modified, or lost in the as the activity of the whole complex (photophos- thylakoids exposed to UV, preventing protons phorylation). The later can be due to minimizing the from binding to them (Melis et al. 1992; Vass et difference of the proton concentrations between the al. 2005; Rensen et al. 2007). two sides of the thylakoid membrane (stroma and Cytochrome b /f: The Cyt b /f complex (217 6 6 lumen), caused by the changes in the thylakoid per- kDa) consists of four large subunits (18 to 32 kDa), meability (Zhang et al. 1994; Yu et al. 2013; Parihar including cytochrome f, cytochrome b , the Rieske et al. 2017). iron-sulfur protein (ISP), and subunit IV, together Effect of UV-B in Calvin cycle enzymes: with four small hydrophobic subunits (PetG, PetL, The Calvin cycle is the primary cyclic pathway PetM and PetN) (Kurisu et al. 2003). This complex of carbon fixation and in higher plants is located mediates the electron transport chain between pho- in the stroma. The light reactions provide reducing tosystems II and I; it oxidizes PQH2 produced by 7 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 −15 power represented by the reduced form of nicotina- Increasing the dermal tissue thickness, which blocks and prevents the harmful UV-B from reach- mide adenine dinucleotide phosphate NADPH+H ing the photosynthetically active mesophyll (Roze- and energy as ATP (Heineke & Scheibe 2007). ma et al. 1997; Kakani et al. 2003; Qi et al. 2003; The Calvin cycle can be subdivided into three Rai & Agrawal 2017; Neugart & Schreiner 2018). phases: (i) the carboxylation of ribulose 1,5-bis- In addition to increasing wax production and/or the phosphate (RuBP), leading to the formation of two number of trichomes on the surface of some plants molecules of 3-phosphoglycerate (3PGA), (ii) the (Skaltsa et al. 1994; Barnes et al. 1996; Liakoura et reduction of 3PGA, and (iii) the regeneration RuBP. al. 1997; Long et al. 2003; Chen et al. 2020). The products of these reactions are triose phos- phates, which are exported into the cytosol by a spe- Enhancing the concentrations of secondary cific transporter to be converted to sucrose (Heineke metabolites & Scheibe 2007). Phenolic compounds UV-B adversely affects all Calvin cycle enzymes The phenylpropanoid pathway is ubiquitous in including ribulose-1,5-biphosphate carboxylase/ox- plants for secondary metabolites biosynthesis. It ygenase (RubisCO). RubisCO is the key enzyme in leads to the biosynthesis of various phenolic com- photosynthesis in algae and C3-plants, as it is re- pounds, which play an important role in plant adap- sponsible for the initial carbon dioxide (CO ) fixa- tation to abiotic stresses and survival, not to mention tion. Each RubisCO holoenzyme consists of eight its essential role in plant health and nutrition (Tak- large subunits (LSU, 53 kDa) and eight small subu- shak & Agrawal 2016). These compounds often ac- nits (SSU, 14 kDa). Both subunit types contain tryp- cumulate within the vacuoles of the upper epidermis tophans (Trp) that are the potential sites for UV-B leaves and effectively absorb UV radiation thus pre- induced photochemistry. Hence, UV-B causes a de- venting it from penetrating the leaf mesophyll cells cline in RubisCO activity as well as the amounts (Xu et al. 2008; Piri et al. 2011; Germ et al. 2015; of both subunits (Xiong & Day 2001; Lidon et al. Surjadinata et al. 2017). 2012; Reboredo & Lidon 2012; Kataria et al. 2014; Flavonoids are important natural products with Parihar et al. 2017). A previous study attributed the polyphenolic structure. They belong to a group of reduction of RubisCO to the lack of nitrogen supply low-molecular-weight phenolic compounds that are for protein biosynthesis; thus suppression of protein sub-divided into flavones, flavonols, flavanones, fla- biosynthesis and/or enhancement of protein degra- vanonols, flavanols (catechins), anthocyanins, and dation (Takeuchi et al. 2002). chalcones (Panche et al. 2016). In conclusion, the decrease in CO fixation rates It`s worth noting that flavonoids are sensitive to under UV-B can be attributed to several reasons, light quality, thus their concentrations are higher including thylakoid membranes rupture and photo- in plant cells exposed UV radiation (Olsson et al. electron transport disruption, in addition to the nega- 1998; Izaguirre et al. 2007; Katerova et al. 2012; tive impact of the enzymes involved in Calvin cy- Inostroza-Blancheteau et al. 2014; Li et al. 2014; cle. Accordingly, UV-B causes a steep drop in total Singh & Singh, 2014; Suleman et al. 2014; Köhler carbohydrate content either directly by inhibition of et al. 2017; Bilodeau et al. 2019; Liu et al. 2020). enzymes involved in the Calvin cycle, or indirect- Increased flavonoid content under lower expo- ly by inhibition of the photochemical reactions re- sure correlates well with higher activity of pheny- quired to produce NADPH + H and ATP needed for lalanine ammonia-lyase (PAL), a key enzyme of the Calvin cycle (Prasad et al. 1998; Gwynn-Jones flavonoid biosynthesis (Kolb et al. 2001; Kumari et 2001; Bhandari & Sharma 2006; Ganapathy et al. al. 2009; Singh & Singh, 2014; Suleman et al. 2014; 2017; Ayash et al. 2018; Kurinjimalar et al. 2019). Azarafshan et al. 2020). Concerning anthocyanins, they are phytopig- DEFENCE MECHANISMS AGAINST UV-B ments responsible for attractive colours in many Photosynthetic organisms have developed vari- plant tissues, principally flowers, leaves, and fruits ous protective mechanisms against UV-B such as: (Vermerris & Nicholson 2006; Panche et al. 2016). 8 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 − 15 Several studies implied the rise in anthocyanins un- tion centres of the photosystems and thermal dis- der UV-B stress (Tsormpatsidis et al. 2008; Inostro- sipating of the excess energy, thus preventing the za-Blancheteau et al. 2014; Singh & Singh 2014; formation of reactive oxygen species. They may Reyes-Díaz et al. 2016; Sebastian et al. 2018; Del also scavenge any evolved singlet-oxygen ( O ) Valle et al. 2020). directly (Müller et al. 2001; Mozzo et al. 2008; La- UV-B induces the down-regulation of photosyn- towski et al. 2011; Bilodeau et al. 2019; Bhatt & thesis and other essential processes as mentioned Patel 2020). That is accomplished by carotenes and above, thereby increasing the plant’s susceptibility xanthophylls, but the latter to a greater extent via to photo-inhibition. It is conceivable that anthocya- xanthophyll cycle (the violaxanthin cycle in plants nins protect the plant cells against photo-damage by and higher algae and diadinoxanthin cycle in lower reducing the penetration of UV-B to the photosyn- algae) (Müller et al. 2001). It is worth noting that thetic mesophyll tissue since these pigments con- some carotenoids, such as astaxanthin, have anti- centrate in the epidermal tissues (Steyn et al. 2002; oxidant power 500 times higher than vitamin E, Mahdavian et al. 2008; Goto et al. 2016). which is found in aquatic animals and algae (Mez- These compounds are potent antioxidants, even zomo & Ferreira 2016). though that they are located away from oxidant gen- eration sites in the chloroplast and mitochondria. Many ROS (especially H O ) may leak to the vacuole CONCLUSIONS 2 2 during severe stress and then it could be quenched by anthocyanin and other phenolics (Yamasaki Intensive researches during the last four dec- 1997; Steyn et al. 2002; Takshak & Agrawal 2014; ades have yielded significant improvement in the Panche et al. 2016; Zhou et al. 2016). understanding of the molecular and physiological Certain flavonoids, including the more common background of ultraviolet radiation and its effects anthocyanin pigments, have ROS-scavenging ca- on plant physiology. The most sensitive sites for pacities up to four times greater than those of vi- ultraviolet-B (UV-B) radiation in the plant cell are tamin E and C analogues (Rice-Evans et al. 1997; the biomolecules; deoxyribonucleic acid (DNA), Wang et al. 1997; Hatier & Gould 2009; Agati et proteins, and lipids. On the other hand, UV-B`s al. 2007), helping to reduce photooxidative damage adverse effects on photosynthesis gained a lot of (Cechin et al. 2012; Tsurunaga et al. 2013). attention in the last few years, considering the im- portance of this process for life on Earth. The main Carotenoids targets of UV-B in the photosynthetic apparatus are Carotenoids are photosynthetic accessory pig- the thylakoid membranes, which affect both photo- ments that absorb visible light between 400 – 550 nm systems and the electron carriers attached to them. (Frank & Cogdell 1996). They are hydrocarbons Plants developed different mechanisms to cope containing 40 carbon atoms and are resulting from with UV-B stress, including the leaf dermal tissue the polymerization of eight units of isoprene. In increment and enhancing the concentrations of general, they are subdivided into two basic classes secondary metabolites like carotenoids and antho- 1) carotenes (linear lacking oxygen hydrocarbons) cyanins. Although information about the different such as α-carotene, β-carotene, and lycopene and effects of UV-B on plant physiology and defence 2) xanthophylls (oxygenated derivatives of caro- systems have accumulated in the last few decades, tenes) such as lutein, violaxanthin, neoxanthin, and further studies are necessary to fully understand the zeaxanthin (Mezzomo & Ferreira 2016; Bhatt & Pa- mechanism of these effects. tel 2020). Carotenoids act as protective compounds against Acknowledgement: Al-Andalus University for photo-oxidative damage of the photosynthetic ap- Medical Sciences supported this work. paratus and other cell components by quenching the single excited chlorophyll (1Chl*) and possibly a triplet excited chlorophyll (3Chl*) within reac- 9 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 − 15 cies with contrasting leaf anatomy subjected to supplemen- REFERENCES tal UV-B radiation. Forest Science, 49, 176 – 187. Bassman, J.H. and Robberecht, R. (2006). 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Effects of Ultraviolet-B Radiation in Plant Physiology

Agriculture , Volume 67 (1): 15 – Apr 1, 2021

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Abstract

Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 − 15 Review DOI: 10.2478/agri-2021-0001 RANA NASSOUR , ABDULKARIM AYASH Al-Andalus University for Medical Sciences, Tartous, Syria Nassour, R. and Ayash, A. (2021). Effects of ultraviolet-B radiation in plant physiology. Agriculture (Poľnohospodárstvo), 67(1), 1 – 15. Over the past few decades, anthropogenic activities contributed to the depletion of the ozone layer, which increased the levels of solar ultraviolet-B (UV-B) radiation reaching the Earth`s surface. Generally, UV-B is harmful to all living organisms. It damages the cell`s Deoxyribonucleic acid (DNA), proteins, and lipids, and as a consequence, it affects the bio-membranes negatively. In this review, we summarize the major effects of UV-B in the plant`s main molecules and physiological reactions, in addition to the possible defence mechanisms against UV-B including accumulating UV-B absorbing pigments to alleviate the harmful impact of UV-B. Key words: ultraviolet-B radiation, reactive oxygen species, respiration, photosynthesis, phenolic compounds Solar radiation is a part of the electromagnetic field Ultraviolet (UV) radiation comprises three types and is considered an essential condition for life on of waves varying by their wavelengths and energy: Earth. The electromagnetic spectrum includes differ- UV-C (100 ‒ 280 nm), UV-B (280 ‒ 320 nm), and ent types of waves; gamma radiation (<0.1 nm), X-rays UV-A (320 ‒ 390 nm). UV-C has the highest energy (0.1 ‒ 100 nm), ultraviolet radiation (100 ‒ 390 nm), level and it is the most hazardous part of the ultravi- visible waves (390 ‒ 780 nm), infrared radiation olet radiation. Luckily, it is completely absorbed by (780 nm ‒ 1 mm), microwaves (1 mm ‒ 1 cm) and ra- the atmospheric oxygen (O ) and stratospheric ozone dio waves (1 cm – 100 km) (Sliney & Chaney 2006; (O ), while most of the UV-B radiation is absorbed Mandi 2016; Zwinkels 2016). efficiently by O , and UV-A is fully transmitted to Although visible light forms only a very small the Earth’s surface to a large extend (Madronich et part of the entire sun`s electromagnetic spectrum, it al. 1998; Mandi 2016). In this context, the ozone provides the energy needed for plants to perform pho- acts as a natural barrier to the Earth from sunlight tosynthesis, the most important process for the pro- and its effects. It blocks and isolates harmful UV duction of reduced carbon (e.g. carbohydrates, amino radiation before it reaches the surface of our planet, acids, fatty acids, etc.) and oxygen. That makes pho- damaging the cells of humans and other organisms. tosynthesis the main source of building blocks and The stratospheric ozone is continuously pro- energy-supplying molecules in living organisms. duced and broken down according to a natural pro- Rana Nassour (*Corresponding author), Department of Basic Science, Faculty of Pharmacy, Al-Andalus University for Medical Sciences, Tartous, Syria. E-mail: ranahn1985@gmail.com Abdulkarim Ayash, Department of Basic Science, Faculty of Pharmacy, Al-Andalus University for Medical Sciences, Tartous, Syria. E-mail: abdulkarimayash@gmail.com © 2021 Authors. This is an open access article licensed under the Creative Commons Attribution-NonComercial-NoDerivs License (http://creativecommons.org/licenses/by-nc-nd/4.0/). 1 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 − 15 cess with dynamic equilibrium, via oxygen pho- in various subcellular sites, including mitochondrial tolysis by short ultraviolet radiation (UV-C shorter respiration, photosynthesis, and photo-respiratory than 250 nm). The released atomic oxygen (O) reactions (Mhamdi & Breusegem 2018). then bonds with molecular oxygen (O ), resulting Plants possess an antioxidant system to protect in ozone (O ). The O is then broken down by long their cells from ROS. The major antioxidants are en- 3 3 ultraviolet radiation (UV-B) to produce O and O, zymes, including superoxide dismutase (SOD), cat- according to the following equations (Häder 1991; alase (CAT), various peroxidases like ascorbate per- Mandi 2016): oxidase (APX), and glutathione peroxidase (GPX). Besides, there are some low molecular weight anti- short UV radiation (>250 mm) O 2O oxidants (LMWAs) in plant cells, such as ascorbate (vitamin C), tocopherols (vitamin E), β-carotene, 2O 2O + 2O 2 3 and phenolic compounds such as the flavonoids (Ren et al. 2006; Hatier & Gould 2009; Reboredo long UV radiation (UV-B) & Lidon 2012; Zlatev et al. 2012; Fu & Shen 2017; 2O 2O + 2O Zhang et al. 2017; Bhattacharjee 2019). Unfortunately, the ozone layer has been undergo- ROS formation increases in the plant cell under ing a gradual decline in its quantity for nearly four stress conditions, such as ultraviolet radiation due to decades due to gaseous pollutants, such as chlo- their high-energy photons that damage the cell struc- rinated fluorocarbons (CFCs), chloroform, hydro- ture (oxidize proteins, lipids, and other biomole- chlorofluorocarbons (HCFCs), carbon tetrachloride, cules), disrupt the functionality and integrity of en- methyl bromide, and reactive nitrogen species (ni- zymes and cell membranes, and cause an imbalance tric oxide, nitrous oxide, etc.) (Rastogi et al. 2014; in the redox reactions. So, a considerable part of the Sreelakshmi & Raza 2014; Mandi 2016). These sta- electrons leaks from electron transport systems to ble compounds can remain in the upper atmosphere ), reducing it to superoxide free radical oxygen (O •- for millions of years (20 ‒ 100 million years), where (O ) (Hideg et al. 2013; Bhattacharjee 2019; Dmi- chlorine and bromine atoms are released from them trieva et al. 2020). via UV. Each atom, which acts as a free radical, is In general, it is agreed that chloroplasts are the capable of initiating a series of reactions that can major sources of ROS in the plant cell, particular- destroy more than 100,000 ozone molecules. This ly under illumination, while the mitochondria are significant destruction of O reduces the UV absorp- the main source of ROS in the darkness and non- tion efficiency, so more of this radiation reaches green parts of the plant. The excitation of oxygen the surface of the Earth (1% reduction of O causes (O ) produces singlet oxygen ( O ), while reduction 3 2 2 •- 1.3 ‒ 1.8% increase of UV-B on the Earth’s surface) produces superoxide radicals (O ), hydrogen per- (Caldwell & Flint 1994; Sivasakthivel & Reddy oxide (H O ), and hydroxyl radicals (OH ), (Fig- 2 2 2011; Lidon et al. 2012). ure 1) (Mhamdi & Breusegem 2018). Chloroplasts 1 •- It`s worth noting that due to the ban of hydro- produce O , O and H O during photosynthetic 2 2 2 2 chlorofluorocarbons according to the 1987 Mon- electron transport, whereas mitochondria produce •- treal Protocol, the ozone layer is about to recover, O mainly at complex I and III of electron transport although there is still a long way to go (Chipperfield chain (Bhattacharjee 2019; Huang et al. 2019). The et al. 2017). Still, latitudes between 60° S and 60° N latter can be explained by the direct reduction of oxy- •- did not show recovery for unclear reasons (Ball et gen to O in complex I (the flavoprotein region of al. 2018). NADH (reduced nicotinamide adenine dinucleotide) dehydrogenase segment). Regarding complex III UV-B INDUCES REACTIVE OXYGEN SPECIES (the ubiquinone-cytochrome region), it is believed PRODUCTION that fully reduced ubiquinone donates an electron to Reactive oxygen species (ROS) are toxic cytochrome C1 and leaves an unstable highly reduc- by-products generated during metabolism, even un- ing ubisemiquinone radical that is favourable for the •- der natural conditions. They are produced in plants electron leakage to O and, hence, to O formation 2 2 2 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 − 15 (Bhattacharjee 2019). The increased production of posed to UV exhibit a decline in photosynthesis, ROS in living organisms under stress conditions is protein synthesis, and other biochemical processes. very toxic because it can react with vital biomol- These impairments lead to the reductions in plant ecules, altering and reducing their biochemical ac- height, dry weight, leaf area, relative growth rate, tivities, causing oxidative damage and eventually and total biomass (Caldwell et al. 2007; Kumari et resulting in cell death (Jithesh et al. 2006; Piri et al. al. 2009; Piri et al. 2011; Reddy et al. 2013; Bacelar 2011; Pessoa 2012; Zlatev et al. 2012; Kataria et al. et al. 2015; Reyes-Díaz et al. 2016; Fina et al. 2017; 2014; Yokawa et al. 2016) Fu & Shen 2017; Rai & Agrawal 2017; Neugart & Schreiner 2018; Parani & Vidhya 2018; Alves & De- UV-B EFFECTS IN PLANTS schamps 2019; Alemu & Gebre 2020), an increase Although UV-B is just a small fraction of the in the leaf thickness and downward leaf curling (Go- electromagnetic field, it adversely affects the lives laszewska et al. 2003; Bacelar et al. 2015; Rai & of all living organisms, including plants. Plants ex- Agrawal 2017), and a decline in transpiration rate, Figure 1. Oxygen-derived reactive oxygen species (Mhamdi & Breusegem 2018) ‒ + 2+ Note: e ‒ electron; 2H ‒ 2 protons; Fe ‒ iron divalent ion; t ‒ the half-life time; µs ‒ microsecond; ns ‒ nanosecond; 1/2 ms ‒ millisecond 3 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 −15 beside a delay in flowering and fruiting (Bassman et sensitive to ROS; since hydroxyl radical and singlet al. 2003; Reddy et al. 2013; Rai & Agrawal 2017). oxygen can react with methylene groups of PUFA In addition, many studies referred to the negative and form lipid peroxy radicals and hydroperoxide. impact of UV-B on stomatal conductance, which re- In their turn, the peroxy radicals can abstract hydro- duces the amount of CO available for photosynthe- gen from other unsaturated fatty acids, leading to sis (Cechin et al. 2007; Lidon et al. 2012; Bacelar a chain reaction of peroxidation (Nasibi & M-Kalan- et al. 2015; Cechin et al. 2018; Reyes et al. 2018; tari 2005; Vass et al. 2005; Rastogi et al. 2014; Shar- Reyes et al. 2019). ma et al. 2014; Kumar et al. 2018). Based on the above, the negative impact of UV-B effects in cellular compounds UV-B causes destruction of biomembranes (cellu- UV-B forms a small part of the electromagnetic lar membranes, mitochondrial membranes (cris- field, yet it is very energetic affecting and modifying tae), thylakoids, tonoplast, etc.), because each one a wide range of important biochemicals and break- of these membranes consists of a bilayer of phos- ing them into smaller molecules. That makes it de- pholipids with proteins interspersed throughout. structive for the organism’s life in general. Therefore, any damage to the components of these Proteins: UV-B has negative effects on structur- membranes will lead to rupture them and disrupt the al and functional proteins. It destroys the peptide biochemical reactions in them (Bidlack & Jansky bonds in the protein and breaks them into polypep- 2018). tides. Proteins highly absorbance to UV-B (around Carbohydrates: they are the main product of pho- 280 nm) is due to the absorbance of their aromatic tosynthesis. Carbon is fixed in C3-plants within Cal- amino acids (such as tyrosine, phenylalanine, tryp- vin cycle in the form of phosphorylated triose and tophan, histidine, and cysteine), so they are consid- then convert to glucose, which binds to each other ered as one of the main targets for UV-B (Nawkar et to be stored as polysaccharides. UV-B causes a steep al. 2013; Parihar et al. 2017). drop in total carbohydrate content either directly by Proteins may undergo photomodification direct - inhibition of enzymes involved in the Calvin cycle, ly through photooxidation reactions or indirectly by or indirectly by inhibition of the photochemical re- the photosensitized production of reactive oxygen actions required to produce NADPH + H and ATP species (ROS) and free radicals. Ultraviolet radia- needed for the Calvin cycle (Prasad et al. 1998; tion modifies the structure of amino acids, which Bhandari & Sharma 2006; Ganapathy et al. 2017; leads to protein denaturation and enzyme deactiva- Kurinjimalar et al. 2019; Reyes et al. 2019). tion. This can be due to UV-B destruction of aromat- ic amino acids (free and within proteins), or to its Deoxyribonucleic acid (DNA): UV-B damages effect on the disulphide bonds (S-S) in amino acids, nuclear, mitochondrial, and chloroplast DNA by in- which contain a sulfhydryl group in their reaction direct oxidative stress or direct absorption of purines centre (Hollosy 2002; Vass et al. 2005; Xue et al. and pyrimidines to these wavelengths (between 2005; Castenholz and Garcia-Pichel 2012; Nawkar 220 ‒ 300 nm), although pyrimidines are more af- et al. 2013; Wang et al. 2017). fected. DNA lesions induced by UV-B include di- mers between two adjacent pyrimidine bases, cis- Lipids: When exposed to UV-B, lipids under- syn cyclobutane pyrimidine dimers (CPDs), espe- go lipid peroxidation whether they are glycolipids, cially thymine dimers (TTs) and pyrimidine (6 – 4) phospholipids, or unsaturated fatty acids. UV-B pyrimidone photoproducts [(6 – 4)PPs] (Draper & exposed phospholipids are sensitive to ROS in two Hays 2000; Sinha et al. 2001; Frohnmeyer & Staiger sites: the unsaturated double bond between the car- 2003; Roleda et al. 2006; Babele et al. 2012; Pfeifer bon atoms and the ester bond between glycerol and & Besaratinia 2012; Nawkar et al. 2013; Rastogi et fatty acids (Kramer et al. 1991; Moorthy & Kathire- al. 2014; Gill et al. 2015; Li et al. 2015; Robson et san 1998; Hollosy 2002; Bhandari & Sharma 2006; al. 2019). These DNA lesions together can act as the Noaman 2007; Pérez et al. 2012; Ganapathy et al. principal cause of UV-B induced growth inhibition 2017; Wang et al. 2017). Polyunsaturated fatty acids in plants. Additionally, these photoproducts block (PUFAs) in the membrane`s phospholipids are also 4 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 − 15 the activity of DNA and RNA polymerases along the reaction centres (Bornman 1989; Takeuchi et al. the DNA strand, which inhibit replication and tran- 2002; Kataria et al. 2014). scription, respectively, and can lead to genetic code UV-B reduces the content of photosynthetic pig- misreading and causing mutations and death (Sinha ments in the chloroplast, especially chlorophyll a, et al. 2001; Takahashi et al. 2015; Jansen 2017). which is considered the principal pigment in pho- UV radiation causes a decline in the cell divi- tosynthesis (Qi et al. 2003; Gupta et al. 2008; Juo- sion rates as well as in cell number. This can be due zaityte et al. 2008; Lidon & Ramalho 2011; Singh to the genetic material destruction and disrupting & Singh 2014; Sztatelman et al. 2015; Ayash et transcription processes (as mentioned above) be- al. 2017; Fu & Shen 2017; Sebastian et al. 2018). side inhibition of protein synthesis in G1 ‒ S phases This loss in chlorophyll can be attributed to proto- of the cell cycle (Buma et al. 1996; Nogués et al. chlorophyllide photoreduction to chlorophyllide by protochlorophyllide oxidoreductase during the early 1998; Hopkins et al. 2002; Juan et al. 2005; Gill et stages of chlorophyll biosynthesis, as well as chlo- al. 2015). Jiang et al. (2011) implied that UV-B-in- rophyllase induction, which is responsible for chlo- duced G1 to S arrest may be a protective mechanism rophyll breakdown (Agrawal 1996; Marwood & that prevents cells with damaged DNA from divid- Greenberg 1996; Pradhan et al. 2006; Sakalauskaite ing and may explain the plant growth inhibition un- et al. 2013; Ganapathy et al. 2017; Rai & Agrawal der increased solar UV-B. Besides, UV-B-treated 2017). cells age more quickly than those of the controls Concerning carotenoids, they are photosynthetic (Hopkins et al. 2002). accessory pigment. They invariably increase in re- Effect of UV-B in respiration sponse to UV-B (Kurinjimalar et al. 2019). A very few studies investigated the impact of Effects of UV-B in the thylakoid membranes UV-B on respiration. Under UV-B stress, respi- The thylakoid membranes consist of a bilayer of ration increase significantly in the plant cell. This phospholipids with proteins interspersed through- increment can be explained by the rise of energy de- out. UV-B destroys the basic components of these mands, which is used in protection and repair mech- membranes (proteins and phospholipids), leading to anisms, including the increase of the leaf thickness rupture them partially or completely, thus prevent- and phenolic compounds biosynthesis (Gwynn- ing the binding of electron acceptors, and disrupting Jones 2001; Bassman & Robberecht 2006; Suchar photoelectron transport (Sinha et al. 2001; Lidon & & Robberecht 2016). Ramalho 2011; Kataria et al. 2014; Allorent et al. Effect of UV-B in photosynthesis 2016; Bidlack & Jansky 2018). Based on the mentioned above, many studies Photosynthesis is the most important process in revealed that UV-B increases the permeability of the plant, because it is the main source of organic thylakoids membranes, which causes protons leak- matter on our planet, besides being responsible for age to stroma and lowers ATP synthesis rates (Sala- producing and releasing oxygen to the Earth’s at- ma et al. 2011; Zlatev et al. 2012; Rai & Agrawal mosphere, which is essential for the respiration of 2017). Also, swelled, disintegrated, and scattered aerial organisms. UV-B affects photosynthetic ap- thylakoids and the absence of grana can be noticed paratus in many sites as the following: under UV-B stress (Yu et al. 2013). Effects of UV-B in pigmentation Effects of UV-B in light reactions Photosynthetic pigments are bound to structural PSII: PSII is a multifunctional pigment-protein proteins in the thylakoid membranes in higher complex embedded in the thylakoid membranes, plants and algae to form Light-harvesting complex- especially in the grana regions of the chloroplasts. es (LHCs) within photosystem II (PSII) and photo- This complex contains more than 20 protein sub- system I (PSI). Researches indicate that high inten- units and redox components that mediate light-in- sity of UV-B leads to a functional disconnection be- duced electron transport (Vass et al. 2005). Many tween LHC and photosystems (particularly within negative effects of UV-B have been reported in dif- PSII), which impairs the absorbed energy transfer to 5 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 −15 ferent sites of PSII, including the following: to S3 due to increased susceptibility to absorp- • Oxygen evolving complex (OEC): It is located in tion of these rays, which may result in the sepa- the lumenal side of the thylakoids, and includes ration of the Mn-OH bond and the formation of four manganese atoms and one calcium atom the hydroxyl radical and thus obstruct the release forming a Mn Ca cluster (Najafpour & Govindjee of oxygen (Sicora et al. 2006; Szilárd et al. 2007; 2011). According to Kok scheme, Mn shifts be- Vass 1996; Vass 2012; Kataria et al. 2014; Allor- tween five states during water oxidation (S0, S1, ent et al. 2016; Ayash et al. 2018; Mosadegh et S2, S3, S4), releasing one proton and one elec- al. 2019). tron in each state. The outcome of this process is • D1 protein: It is one of the most important struc- the evolving of four electrons, four protons, and tural protein (38.021 kDa) of PSII, binding essen- an oxygen molecule (Figure 2). Various stud- tial electron transporters such as tyrosine (Tyr-Z) ies indicated that UV-B might inhibit the OEC (Barber 2014). Under UV-B, D1 is degraded complex directly by absorbing this radiation via to a 20 kDa fragment which is subsequently the Mn cluster, which breaks the bonds between completely degraded by proteases enzymes in the manganese atoms, or by damaging the inter- a light-dependent manner (Bergo et al. 2003). mediates of the water evolving process. There is Besides the stability decrement of D1 and imbal- a gradual increase of UV-B sensitivity from S0 ance between its synthesis and breaking down Figure 2. S-state Kok scheme (Yano & Yachandra 2014) ‒ + Note: hv ‒ light; µs ‒ microsecond; ms ‒ millisecond; e ‒ electron; H ‒ proton; F ‒ flash 6 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 −15 rates, as the amount of ROS increases (in par- PSII and reduces plastocyanin (PC ‒ the electron ticular the active atomic oxygen) (Booij-James donor for PSI) (Vass et al. 2005). The previous stud- et al. 2000; Beardall & Raven 2004; Holzinger & ies suggest that the Cyt b /f complex is the least af- Lütz 2006; Cai et al. 2016; Tilbrook et al. 2016; fected thylakoid component by UV-B, which can be Parihar et al. 2017). explained by the fact that Cyt b /f complex contains • Tyrosine: Released electrons from OEC are trans- two quinine binding sites (one of them for quinol ferred to the reaction centre (RC) of PSII (P680) oxidation and the other for quinone reduction). Be- via a redox-active tyrosine residue (Tyr-Z) of the sides the UV-B minor sensitivity for genes encoded D1 protein. PSII contains another redox-active in the chloroplast, such as subunit IV of this com- tyrosine, called Tyr-D (on the D2 subunit) which plex (Kataria et al. 2014; Parihar et al. 2017). can donate electrons to P680, but is not involved PSI: PSI of higher plants contains approximately in electron transfer from OEC (Sicora et al. 15 protein subunits. PsaA and PsaB (each ≈80 kDa) 2003). Under UV-B, tyrosine may be inactivated form the central heterodimer of the reaction centre and/or photo-oxidized to 3,4-dihydroxyphenyla- and most of the electron carriers and pigments of lanine (DOPA) and form di-tyrosine as a result LHCI are bound to them (Niyogi et al. 2015). Un- (Vass 1996; Vass et al. 2005; Parihar et al. 2017). even distribution of the effect of UV-B has been • D2 protein: It is considered an essential struc- demonstrated by various studies to display minor or tural protein (39.418 kDa) of PSII, binding cru- no effects on PSI compared to PSII (Hollosy 2002; cial electron transporters, such as plastoquinone Kataria et al. 2014; Parihar et al. 2017). This can (PQ) (Barber 2014). A significant decrease in be attributed to the significant down-regulation of D2 content is reported in the exposed to UV-B many genes encoding PS I protein subunits in UV- thylakoids (Booij-James et al. 2000; Tilbrook et B-exposed cells (Kataria et al. 2014). al. 2016; Parihar et al. 2017). ATPase complex: The ATPase is a large (400 kDa) • Plastoquinone: It is the mobile charge carrier re- enzyme complex responsible for adenosine triphos- sponsible for the electron transport from PSII to phate (ATP) synthesis. It consists of two parts: a hy- /f (Cyt b /f). PQ is double reduced cytochrome b 6 6 drophobic membrane-bound portion called coupling and takes up two protons from the stroma to be- factor O (CFo) and another portion that sticks out come quinol (PQH2). Then, the lipophilic PQH2 into the stroma called coupling factor 1 (CF1). CFo is separated from protein D1 and moves within forms a channel across the membrane for protons the lipid bilayer of the thylakoid membrane, to pass through. CF1 is responsible for binding in- transferring the electrons to Cyt b /f, releasing organic phosphate (P) to adenosine diphosphate protons into the lumen, and returning to the oxi- (ADP) to produce ATP. It is made up of several dized form (PQ) (Eerden et al. 2017). Since main peptides; including three copies of each of α and ß absorption of quinones in the UV region (oxi- peptides arranged alternately (Taiz & Zeiger 2010). dized PQ: 250 nm, redox PQ; quinol (PQH2): ATPase is significantly affected by UV-B, as the 280 nm and semiquinone (PQH): 320 nm), amount of coupling factor (CF1) decreases, as well they can be destroyed, modified, or lost in the as the activity of the whole complex (photophos- thylakoids exposed to UV, preventing protons phorylation). The later can be due to minimizing the from binding to them (Melis et al. 1992; Vass et difference of the proton concentrations between the al. 2005; Rensen et al. 2007). two sides of the thylakoid membrane (stroma and Cytochrome b /f: The Cyt b /f complex (217 6 6 lumen), caused by the changes in the thylakoid per- kDa) consists of four large subunits (18 to 32 kDa), meability (Zhang et al. 1994; Yu et al. 2013; Parihar including cytochrome f, cytochrome b , the Rieske et al. 2017). iron-sulfur protein (ISP), and subunit IV, together Effect of UV-B in Calvin cycle enzymes: with four small hydrophobic subunits (PetG, PetL, The Calvin cycle is the primary cyclic pathway PetM and PetN) (Kurisu et al. 2003). This complex of carbon fixation and in higher plants is located mediates the electron transport chain between pho- in the stroma. The light reactions provide reducing tosystems II and I; it oxidizes PQH2 produced by 7 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 −15 power represented by the reduced form of nicotina- Increasing the dermal tissue thickness, which blocks and prevents the harmful UV-B from reach- mide adenine dinucleotide phosphate NADPH+H ing the photosynthetically active mesophyll (Roze- and energy as ATP (Heineke & Scheibe 2007). ma et al. 1997; Kakani et al. 2003; Qi et al. 2003; The Calvin cycle can be subdivided into three Rai & Agrawal 2017; Neugart & Schreiner 2018). phases: (i) the carboxylation of ribulose 1,5-bis- In addition to increasing wax production and/or the phosphate (RuBP), leading to the formation of two number of trichomes on the surface of some plants molecules of 3-phosphoglycerate (3PGA), (ii) the (Skaltsa et al. 1994; Barnes et al. 1996; Liakoura et reduction of 3PGA, and (iii) the regeneration RuBP. al. 1997; Long et al. 2003; Chen et al. 2020). The products of these reactions are triose phos- phates, which are exported into the cytosol by a spe- Enhancing the concentrations of secondary cific transporter to be converted to sucrose (Heineke metabolites & Scheibe 2007). Phenolic compounds UV-B adversely affects all Calvin cycle enzymes The phenylpropanoid pathway is ubiquitous in including ribulose-1,5-biphosphate carboxylase/ox- plants for secondary metabolites biosynthesis. It ygenase (RubisCO). RubisCO is the key enzyme in leads to the biosynthesis of various phenolic com- photosynthesis in algae and C3-plants, as it is re- pounds, which play an important role in plant adap- sponsible for the initial carbon dioxide (CO ) fixa- tation to abiotic stresses and survival, not to mention tion. Each RubisCO holoenzyme consists of eight its essential role in plant health and nutrition (Tak- large subunits (LSU, 53 kDa) and eight small subu- shak & Agrawal 2016). These compounds often ac- nits (SSU, 14 kDa). Both subunit types contain tryp- cumulate within the vacuoles of the upper epidermis tophans (Trp) that are the potential sites for UV-B leaves and effectively absorb UV radiation thus pre- induced photochemistry. Hence, UV-B causes a de- venting it from penetrating the leaf mesophyll cells cline in RubisCO activity as well as the amounts (Xu et al. 2008; Piri et al. 2011; Germ et al. 2015; of both subunits (Xiong & Day 2001; Lidon et al. Surjadinata et al. 2017). 2012; Reboredo & Lidon 2012; Kataria et al. 2014; Flavonoids are important natural products with Parihar et al. 2017). A previous study attributed the polyphenolic structure. They belong to a group of reduction of RubisCO to the lack of nitrogen supply low-molecular-weight phenolic compounds that are for protein biosynthesis; thus suppression of protein sub-divided into flavones, flavonols, flavanones, fla- biosynthesis and/or enhancement of protein degra- vanonols, flavanols (catechins), anthocyanins, and dation (Takeuchi et al. 2002). chalcones (Panche et al. 2016). In conclusion, the decrease in CO fixation rates It`s worth noting that flavonoids are sensitive to under UV-B can be attributed to several reasons, light quality, thus their concentrations are higher including thylakoid membranes rupture and photo- in plant cells exposed UV radiation (Olsson et al. electron transport disruption, in addition to the nega- 1998; Izaguirre et al. 2007; Katerova et al. 2012; tive impact of the enzymes involved in Calvin cy- Inostroza-Blancheteau et al. 2014; Li et al. 2014; cle. Accordingly, UV-B causes a steep drop in total Singh & Singh, 2014; Suleman et al. 2014; Köhler carbohydrate content either directly by inhibition of et al. 2017; Bilodeau et al. 2019; Liu et al. 2020). enzymes involved in the Calvin cycle, or indirect- Increased flavonoid content under lower expo- ly by inhibition of the photochemical reactions re- sure correlates well with higher activity of pheny- quired to produce NADPH + H and ATP needed for lalanine ammonia-lyase (PAL), a key enzyme of the Calvin cycle (Prasad et al. 1998; Gwynn-Jones flavonoid biosynthesis (Kolb et al. 2001; Kumari et 2001; Bhandari & Sharma 2006; Ganapathy et al. al. 2009; Singh & Singh, 2014; Suleman et al. 2014; 2017; Ayash et al. 2018; Kurinjimalar et al. 2019). Azarafshan et al. 2020). Concerning anthocyanins, they are phytopig- DEFENCE MECHANISMS AGAINST UV-B ments responsible for attractive colours in many Photosynthetic organisms have developed vari- plant tissues, principally flowers, leaves, and fruits ous protective mechanisms against UV-B such as: (Vermerris & Nicholson 2006; Panche et al. 2016). 8 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 − 15 Several studies implied the rise in anthocyanins un- tion centres of the photosystems and thermal dis- der UV-B stress (Tsormpatsidis et al. 2008; Inostro- sipating of the excess energy, thus preventing the za-Blancheteau et al. 2014; Singh & Singh 2014; formation of reactive oxygen species. They may Reyes-Díaz et al. 2016; Sebastian et al. 2018; Del also scavenge any evolved singlet-oxygen ( O ) Valle et al. 2020). directly (Müller et al. 2001; Mozzo et al. 2008; La- UV-B induces the down-regulation of photosyn- towski et al. 2011; Bilodeau et al. 2019; Bhatt & thesis and other essential processes as mentioned Patel 2020). That is accomplished by carotenes and above, thereby increasing the plant’s susceptibility xanthophylls, but the latter to a greater extent via to photo-inhibition. It is conceivable that anthocya- xanthophyll cycle (the violaxanthin cycle in plants nins protect the plant cells against photo-damage by and higher algae and diadinoxanthin cycle in lower reducing the penetration of UV-B to the photosyn- algae) (Müller et al. 2001). It is worth noting that thetic mesophyll tissue since these pigments con- some carotenoids, such as astaxanthin, have anti- centrate in the epidermal tissues (Steyn et al. 2002; oxidant power 500 times higher than vitamin E, Mahdavian et al. 2008; Goto et al. 2016). which is found in aquatic animals and algae (Mez- These compounds are potent antioxidants, even zomo & Ferreira 2016). though that they are located away from oxidant gen- eration sites in the chloroplast and mitochondria. Many ROS (especially H O ) may leak to the vacuole CONCLUSIONS 2 2 during severe stress and then it could be quenched by anthocyanin and other phenolics (Yamasaki Intensive researches during the last four dec- 1997; Steyn et al. 2002; Takshak & Agrawal 2014; ades have yielded significant improvement in the Panche et al. 2016; Zhou et al. 2016). understanding of the molecular and physiological Certain flavonoids, including the more common background of ultraviolet radiation and its effects anthocyanin pigments, have ROS-scavenging ca- on plant physiology. The most sensitive sites for pacities up to four times greater than those of vi- ultraviolet-B (UV-B) radiation in the plant cell are tamin E and C analogues (Rice-Evans et al. 1997; the biomolecules; deoxyribonucleic acid (DNA), Wang et al. 1997; Hatier & Gould 2009; Agati et proteins, and lipids. On the other hand, UV-B`s al. 2007), helping to reduce photooxidative damage adverse effects on photosynthesis gained a lot of (Cechin et al. 2012; Tsurunaga et al. 2013). attention in the last few years, considering the im- portance of this process for life on Earth. The main Carotenoids targets of UV-B in the photosynthetic apparatus are Carotenoids are photosynthetic accessory pig- the thylakoid membranes, which affect both photo- ments that absorb visible light between 400 – 550 nm systems and the electron carriers attached to them. (Frank & Cogdell 1996). They are hydrocarbons Plants developed different mechanisms to cope containing 40 carbon atoms and are resulting from with UV-B stress, including the leaf dermal tissue the polymerization of eight units of isoprene. In increment and enhancing the concentrations of general, they are subdivided into two basic classes secondary metabolites like carotenoids and antho- 1) carotenes (linear lacking oxygen hydrocarbons) cyanins. Although information about the different such as α-carotene, β-carotene, and lycopene and effects of UV-B on plant physiology and defence 2) xanthophylls (oxygenated derivatives of caro- systems have accumulated in the last few decades, tenes) such as lutein, violaxanthin, neoxanthin, and further studies are necessary to fully understand the zeaxanthin (Mezzomo & Ferreira 2016; Bhatt & Pa- mechanism of these effects. tel 2020). Carotenoids act as protective compounds against Acknowledgement: Al-Andalus University for photo-oxidative damage of the photosynthetic ap- Medical Sciences supported this work. paratus and other cell components by quenching the single excited chlorophyll (1Chl*) and possibly a triplet excited chlorophyll (3Chl*) within reac- 9 Agriculture (Poľnohospodárstvo), 67, 2021 (1): 1 − 15 cies with contrasting leaf anatomy subjected to supplemen- REFERENCES tal UV-B radiation. Forest Science, 49, 176 – 187. Bassman, J.H. and Robberecht, R. (2006). 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Journal

Agriculturede Gruyter

Published: Apr 1, 2021

Keywords: ultraviolet-B radiation; reactive oxygen species; respiration; photosynthesis; phenolic compounds

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