Differential Antioxidant Response to Supplemental UV-B Irradiation and Sunlight in Three Basil Varieties
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
Contracts No: 451-03-47/2023-011200053; 451-03-47/2023-01/ 200042
University of Belgrade
Centre for Green Technologies
University of Belgrade
Green Program of Cooperation between Science and Industry, grant No 5661
Science Fund of the Republic of Serbia
KOROLID", CZ.02.1.01/0.0/0.0/15_003/0000336
MEYS, CZ with co-funding from EU
PubMed
37895033
PubMed Central
PMC10607338
DOI
10.3390/ijms242015350
PII: ijms242015350
Knihovny.cz E-zdroje
- Klíčová slova
- Ocimum basilicum var. Genovese, Ocimum basilicum var. purpurascens, Ocimum × citriodorum, ascorbate, epidermal flavonoids, hydrogen peroxide, polyphenols, supplemented and ecologically relevant UV-B irradiation, total leaf antioxidant capacity,
- MeSH
- antioxidancia * farmakologie MeSH
- bazalka pravá * MeSH
- flavonoidy MeSH
- kyselina askorbová MeSH
- listy rostlin MeSH
- peroxid vodíku MeSH
- sluneční záření MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- antioxidancia * MeSH
- flavonoidy MeSH
- kyselina askorbová MeSH
- peroxid vodíku MeSH
Three basil plant varieties (Ocimum basilicum var. Genovese, Ocimum × citriodorum, and Ocimum basilicum var. purpurascens) were grown under moderate light (about 300 µmol photons m-2 s-1) in a glasshouse or growth chamber and then either transferred to an open field (average daily dose: 29.2 kJ m-2 d-1) or additionally exposed to UV-B irradiation in a growth chamber (29.16 kJ m-2 d-1), to reveal the variety-specific and light-specific acclimation responses. Total antioxidant capacity (TAC), phenolic profile, ascorbate content, and class III peroxidase (POD) activity were used to determine the antioxidant status of leaves under all four light regimes. Exposure to high solar irradiation at the open field resulted in an increase in TAC, total hydroxycinnamic acids (HCAs, especially caffeic acid), flavonoids, and epidermal UV-absorbing substances in all three varieties, as well as a two-fold increase in the leaf dry/fresh weight ratio. The supplemental UV-B irradiation induced preferential accumulation of HCAs (rosmarinic acid) over flavonoids, increased TAC and POD activity, but decreased the ascorbate content in the leaves, and inhibited the accumulation of epidermal flavonoids in all basil varieties. Furthermore, characteristic leaf curling and UV-B-induced inhibition of plant growth were observed in all basil varieties, while a pro-oxidant effect of UV-B was indicated with H2O2 accumulation in the leaves and spotty leaf browning. The extent of these morphological changes, and oxidative damage depended on the basil cultivar, implies a genotype-specific tolerance mechanism to high doses of UV-B irradiation.
Department of Analytical Chemistry Faculty of Chemistry University of Belgrade 11158 Belgrade Serbia
Institute of Physics Belgrade University of Belgrade 11080 Belgrade Serbia
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Favory J.J., Stec A., Gruber H., Rizzini L., Oravecz A., Funk M., Albert A., Cloix C., Jenkins G.I., Oakeley E.J., et al. Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J. 2009;28:591–601. doi: 10.1038/emboj.2009.4. PubMed DOI PMC
Vidović M., Morina F., Veljović Jovanović S. Stimulation of various phenolics in plants under ambient UV-B radiation. In: Singh V.P., Singh S., Prasad S.M., Parihar P., editors. UV-B Radiation: From Environmental Stressor to Regulator of Plant Growth. Wiley-Blackwell; Hoboken, NJ, USA: 2017. pp. 9–56.
Kataria S., Jajoo A., Guruprasad K.N. Impact of increasing Ultraviolet-B (UV-B) radiation on photosynthetic processes. J. Photochem. Photobiol. B Biol. 2014;137:55–66. doi: 10.1016/j.jphotobiol.2014.02.004. PubMed DOI
Barnes P.W., Robson T.M., Zepp R.G., Bornman J.F., Jansen M.A.K., Ossola R., Wang Q.W., Robinson S.A., Foereid B., Klekociuk A.R., et al. Interactive effects of changes in UV radiation and climate on terrestrial ecosystems, biogeochemical cycles, and feedbacks to the climate system. Photochem. Photobiol. Sci. 2023;22:1049–1091. doi: 10.1007/s43630-023-00376-7. PubMed DOI PMC
Bernhard G.H., Bais A.F., Aucamp P.J., Klekociuk A.R., Liley J.B., McKenzie R.L. Stratospheric ozone, UV radiation, and climate interactions. Photochem. Photobiol. Sci. 2023;22:937–989. doi: 10.1007/s43630-023-00371-y. PubMed DOI PMC
Lamy K., Portafaix T., Josse B., Brogniez C., Godin-Beekmann S., Bencherif H., Revell L., Akiyoshi H., Bekki S., Hegglin M.I., et al. Clear-sky ultraviolet radiation modelling using output from the Chemistry Climate Model Initiative. Atmos. Chem. Phys. 2019;19:10087–10110. doi: 10.5194/acp-19-10087-2019. PubMed DOI PMC
Sanchez-Lorenzo A., Enriquez-Alonso A., Calbó J., González J.A., Wild M., Folini D., Norris J.R., Vicente-Serrano S.M. Fewer clouds in the Mediterranean: Consistency of observations and climate simulations. Sci. Rep. 2017;7:41475. doi: 10.1038/srep41475. PubMed DOI PMC
Malinovic-Milicevic S., Mihailovic D.T., Lalic B., Dreskovic N. Thermal environment and UV-B radiation indices in the Vojvodina region, Serbia. Clim. Res. 2013;57:111–121. doi: 10.3354/cr01163. DOI
Pashiardis S., Kalogirou S.A., Pelengaris A. Statistical Analysis and Inter-Comparison of Solar UVB and Global Radiation for Athalassa and Larnaca, Cyprus. SM J. Biometr. Biostat. 2017;2:1006
Podolec R., Demarsy E., Ulm R. Perception and signaling of ultraviolet-B radiation in plants. Annu. Rev. Plant Biol. 2021;72:793–822. doi: 10.1146/annurev-arplant-050718-095946. PubMed DOI
Hideg É., Jansen M.A., Strid Å. UV-B exposure, ROS, and stress: Inseparable companions or loosely linked associates? Trends Plant Sci. 2013;18:107–115. doi: 10.1016/j.tplants.2012.09.003. PubMed DOI
Yadav A., Singh D., Lingwan M., Yadukrishnan P., Masakapalli S.K., Datta S. Light signaling and UV-B-mediated plant growth regulation. J. Integr. Plant Biol. 2020;62:1270–1292. doi: 10.1111/jipb.12932. PubMed DOI
Asada K. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 2006;141:391–396. doi: 10.1104/pp.106.082040. PubMed DOI PMC
Fischer B.B., Hideg É., Krieger-Liszkay A. Production, detection, and signaling of singlet oxygen in photosynthetic organisms. Antioxid. Redox Signal. 2013;18:2145–2162. doi: 10.1089/ars.2012.5124. PubMed DOI
Foyer C.H., Shigeoka S. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol. 2011;155:93–100. doi: 10.1104/pp.110.166181. PubMed DOI PMC
Vidović M., Morina F., Prokić L., Milić Komić S., Živanović B., Veljović Jovanović S. Antioxidative response in variegated Pelargonium zonale leaves and generation of extracellular H2O2 in (peri) vascular tissue induced by sunlight and paraquat. J. Plant Physiol. 2016;206:25–39. doi: 10.1016/j.jplph.2016.07.017. PubMed DOI
Krause G.H. The high-energy state of the thylakoid system as indicated by chlorophyll fluorescence and chloroplast shrinkage. Biochim. Biophys. Acta Bioenerg. 1973;292:715–728. doi: 10.1016/0005-2728(73)90019-4. PubMed DOI
Briantais J.M., Vernotte C., Picaud M., Krause G.H. Chlorophyll fluorescence as a probe for the determination of the photo-induced proton gradient in isolated chloroplasts. Biochim. Biophys. Acta Bioenerg. 1980;591:198–202. doi: 10.1016/0005-2728(80)90233-9. PubMed DOI
Hernández I., Van Breusegem F. Opinion on the possible role of flavonoids as energy escape valves: Novel tools for nature’s Swiss army knife? Plant Sci. 2010;179:297–301. doi: 10.1016/j.plantsci.2010.06.001. DOI
Golovatskaya I.F., Laptev N.I. Plants and Their Interaction to Environmental Pollution. Elsevier; Amsterdam, The Netherlands: 2023. Effect of UV-B radiation on plants growth, active constituents, and productivity; pp. 25–60.
Rice-Evans C., Miller N., Paganga G. Antioxidant properties of phenolic compounds. Trends Plant Sci. 1997;2:152–159. doi: 10.1016/S1360-1385(97)01018-2. DOI
Neill S.O., Gould K.S. Anthocyanins in leaves: Light attenuators or antioxidants? Funct. Plant Biol. 2003;30:865–873. doi: 10.1071/FP03118. PubMed DOI
Gould K.S. Nature’s Swiss army knife: The diverse protective roles of anthocyanins in leaves. J. Biotechnol. Biomed. 2004;2004:314. doi: 10.1155/S1110724304406147. PubMed DOI PMC
Ferreres F., Figueiredo R., Bettencourt S., Carqueijeiro I., Oliveira J., Gil-Izquierdo A., Pereira D.M., Valentão P., Andrade P.B., Duarte P., et al. Identification of phenolic compounds in isolated vacuoles of the medicinal plant Catharanthus roseus and their interaction with vacuolar class III peroxidase: An H2O2 affair? J. Exp. Bot. 2011;62:2841–2854. doi: 10.1093/jxb/erq458. PubMed DOI
Agati G., Matteini P., Goti A., Tattini M. Chloroplast-located flavonoids can scavenge singlet oxygen. New Phytol. 2007;174:77–89. doi: 10.1111/j.1469-8137.2007.01986.x. PubMed DOI
Jansen M.A., Coffey A.M., Prinsen E. UV-B induced morphogenesis: Four players or a quartet? Plant Signal. Behav. 2012;7:1185–1187. doi: 10.4161/psb.21260. PubMed DOI PMC
Castronuovo D., Russo D., Libonati R., Faraone I., Candido V., Picuno P., Andrade P., Milella L. Influence of shading treatment on yield, morphological traits and phenolic profile of sweet basil (Ocimum basilicum L.) Sci. Hortic. 2019;254:91–98. doi: 10.1016/j.scienta.2019.04.077. DOI
Aldarkazali M., Rihan H.Z., Carne D., Fuller M.P. The growth and development of sweet basil (Ocimum basilicum) and bush basil (Ocimum minimum) grown under three light regimes in a controlled environment. Agronomy. 2019;9:743. doi: 10.3390/agronomy9110743. DOI
Dou H., Niu G., Gu M., Masabni J.G. Effects of light quality on growth and phytonutrient accumulation of herbs under controlled Environments. Horticulturae. 2017;3:36. doi: 10.3390/horticulturae3020036. DOI
Sipos L., Balázs L., Székely G., Jung A., Sárosi S., Radácsi P., Csambalik L. Optimization of basil (Ocimum basilicum L.) production in LED light environments—A review. Sci. Hortic. 2021;289:110486. doi: 10.1016/j.scienta.2021.110486. DOI
Taulavuori K., Pyysalo A., Taulavuori E., Julkunen-Tiitto R. Responses of phenolic acid and flavonoid synthesis to blue and blue-violet light depends on plant species. Environ. Exp. Bot. 2018;150:183–187. doi: 10.1016/j.envexpbot.2018.03.016. DOI
Stagnari F., Di Mattia C., Galieni A., Santarelli V., D’Egidio S., Pagnani G., Pisante M. Light quantity and quality supplies sharply affect growth, morphological, physiological and quality traits of basil. Ind. Crops Prod. 2018;122:277–289. doi: 10.1016/j.indcrop.2018.05.073. DOI
Pennisi G., Pistillo A., Orsini F., Cellini A., Spinelli F., Nicola S., Fernandez J.A., Crepaldi A., Gianquinto G., Marcelis L.F. Optimal light intensity for sustainable water and energy use in indoor cultivation of lettuce and basil under red and blue LEDs. Sci. Hortic. 2020;272:109508. doi: 10.1016/j.scienta.2020.109508. DOI
Sakalauskaite J., Viškelis P., Duchovskis P., Dambrauskiene E., Sakalauskiene S., Samuoliene G., Brazaityte A. Supplementary UV-B irradiation effects on basil (Ocimum basilicum L.) growth and phytochemical properties. J. Food Agric. Environ. 2012;10:342–346.
Semenova N.A., Smirnov A.A., Ivanitskikh A.S., Izmailov A.Y., Dorokhov A.S., Proshkin Y.A., Yanykin D.V., Sarimov R.R., Gudkov S.V., Chilingaryan N.O. Impact of Ultraviolet Radiation on the Pigment Content and Essential Oil Accumulation in Sweet Basil (Ocimum basilicum L.) Appl. Sci. 2022;12:7190. doi: 10.3390/app12147190. DOI
Tattini M., Sebastiani F., Brunetti C., Fini A., Torre S., Gori A., Centritto M., Ferrini F., Landi M., Guidi L. Dissecting molecular and physiological response mechanisms to high solar radiation in cyanic and acyanic leaves: A case study on red and green basil. J. Exp. Bot. 2017;68:2425–2437. doi: 10.1093/jxb/erx123. PubMed DOI
Torre S., Tattini M., Brunetti C., Guidi L., Gori A., Marzano C., Landi M., Sebastiani F. De novo assembly and comparative transcriptome analyses of red and green morphs of sweet basil grown in full sunlight. PLoS ONE. 2016;11:e0160370. doi: 10.1371/journal.pone.0160370. PubMed DOI PMC
Landi M., Agati G., Fini A., Guidi L., Sebastiani F., Tattini M. Unveiling the shade nature of cyanic leaves: A view from the “blue absorbing side” of anthocyanins. Plant Cell Environ. 2021;44:1119–1129. doi: 10.1111/pce.13818. PubMed DOI
Jakovljević D., Topuzović M., Stanković M. Nutrient limitation as a tool for the induction of secondary metabolites with antioxidant activity in basil cultivars. Ind. Crops Prod. 2019;138:111462. doi: 10.1016/j.indcrop.2019.06.025. DOI
Foyer C.H., Noctor G. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell. 2005;17:1866–1875. doi: 10.1105/tpc.105.033589. PubMed DOI PMC
Caldwell M.M., Bornman J.F., Ballaré C.L., Flint S.D., Kulandaivelu G. Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with other climate change factors. Photochem. Photobiol. Sci. 2007;6:252–266. doi: 10.1039/b700019g. PubMed DOI
Bidel L.P., Chomicki G., Bonini F., Mondolot L., Soulé J., Coumans M., La Fisca P., Baissac Y., Petit V., Loiseau A., et al. Dynamics of flavonol accumulation in leaf tissues under different UV-B regimes in Centella asiatica (Apiaceae) Planta. 2015;242:545–559. doi: 10.1007/s00425-015-2291-7. PubMed DOI
Vidović M., Morina F., Milić S., Zechmann B., Albert A., Winkler J.B., Veljovıć Jovanovıć S. Ultraviolet-B component of sunlight stimulates photosynthesis and flavonoid accumulation in variegated Plectranthus coleoides leaves depending on background light. Plant Cell Environ. 2015;38:968–979. doi: 10.1111/pce.12471. PubMed DOI
Jenkins G.I., Long J.C., Wade H.K., Shenton M.R., Bibikova T.N. UV and blue light signalling: Pathways regulating chalcone synthase gene expression in Arabidopsis. New Phytol. 2001;151:121–131. doi: 10.1046/j.1469-8137.2001.00151.x. PubMed DOI
Jenkins G.I. Signal transduction in responses to UV-B radiation. Annu. Rev. Plant Biol. 2009;60:407–431. doi: 10.1146/annurev.arplant.59.032607.092953. PubMed DOI
Ulm R., Baumann A., Oravecz A., Máté Z., Ádám É., Oakeley E.J., Schäfer E., Nagy F. Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. Proc. Natl. Acad. Sci. USA. 2004;101:1397–1402. doi: 10.1073/pnas.0308044100. PubMed DOI PMC
Brown B.A., Cloix C., Jiang G.H., Kaiserli E., Herzyk P., Kliebenstein D.J., Jenkins G.I. A UV-B-specific signaling component orchestrates plant UV protection. Proc. Natl. Acad. Sci. USA. 2005;102:18225–18230. doi: 10.1073/pnas.0507187102. PubMed DOI PMC
Vidović M., Morina F., Milić S., Albert A., Zechmann B., Tosti T., Winkler J.B., Veljović Jovanović S. Carbon allocation from source to sink leaf tissue in relation to flavonoid biosynthesis in variegated Pelargonium zonale under UV-B radiation and high PAR intensity. Plant Physiol. Biochem. 2015;93:44–55. doi: 10.1016/j.plaphy.2015.01.008. PubMed DOI
Potters G., Pasternak T.P., Guisez Y., Palme K.J., Jansen M.A. Stress-induced morphogenic responses: Growing out of trouble? Trends Plant Sci. 2007;12:98–105. doi: 10.1016/j.tplants.2007.01.004. PubMed DOI
Hideg É., Vass I. UV-B induced free radical production in plant leaves and isolated thylakoid membranes. Plant Sci. 1996;115:251–260. doi: 10.1016/0168-9452(96)04364-6. DOI
Takahama U., Oniki T. A peroxidase/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells. Physiol. Plant. 1997;101:845–852. doi: 10.1111/j.1399-3054.1997.tb01072.x. DOI
Smith J.L., Burritt D.J., Bannister P. Shoot dry weight, chlorophyll and UV-B-absorbing compounds as indicators of a plant’s sensitivity to UV-B radiation. Ann. Bot. 2000;86:1057–1063. doi: 10.1006/anbo.2000.1270. DOI
Živanović B., Sedlarević A., Vidović M., Morina F., Veljović Jovanović S. Differential dynamics of flavonoid biosynthesis and accumulation in five medicinal herbs under full sunlight exposure; Proceedings of the UV 4Plants, 1st Network Conference; Pecs, Hungary. 30–31 May 2016; p. 64. In Book of abstracts.
Kolb C.A., Kopecký J., Riederer M., Pfündel E.E. UV screening by phenolics in berries of grapevine (Vitis vinifera) Funct. Plant Biol. 2003;30:1177–1186. doi: 10.1071/FP03076. PubMed DOI
Hectors K., Prinsen E., De Coen W., Jansen M.A., Guisez Y. Arabidopsis thaliana plants acclimated to low dose rates of ultraviolet B radiation show specific changes in morphology and gene expression in the absence of stress symptoms. New Phytol. 2007;175:255–270. doi: 10.1111/j.1469-8137.2007.02092.x. PubMed DOI
Singh S., Agrawal S.B., Agrawal M. UVR8 mediated plant protective responses under low UV-B radiation leading to photosynthetic acclimation. J. Photochem. Photobiol. B. 2014;137:67–76. doi: 10.1016/j.jphotobiol.2014.03.026. PubMed DOI
Jenkins G.I. Plant Responses to Environmental Stress. Bios Scientific Publishers Ltd.; Oxford, UK: 1999. Regulation of phenylpropanoid and flavonoid biosynthesis genes by UV-B in Arabidopsis; pp. 9–15.
Makri O., Kintzios S. Ocimum sp.(basil): Botany, cultivation, pharmaceutical properties, and biotechnology. J. Herbs Spices Med. Plants. 2008;13:123–150. doi: 10.1300/J044v13n03_10. DOI
Kolb C.A., Kaser M.A., Kopecký J., Zotz G., Riederer M., Pfundel E.E. Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves. Plant Physiol. 2001;127:863–875. doi: 10.1104/pp.010373. PubMed DOI PMC
Tattini M., Galardi C., Pinelli P., Massai R., Remorini D., Agati G. Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress. New Phytol. 2004;163:547–561. doi: 10.1111/j.1469-8137.2004.01126.x. PubMed DOI
Li J., Ou-Lee T.M., Raba R., Amundson R.G., Last R.L. Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell. 1993;5:171–179. doi: 10.2307/3869583. PubMed DOI PMC
Grace S.C., Logan B.A., Adams W.W. Seasonal differences in foliar content of chlorogenic acid, a phenylpropanoid antioxidant, in Mahonia repens. Plant Cell Environ. 1998;21:513–521. doi: 10.1046/j.1365-3040.1998.00282.x. DOI
Clarke L.J., Robinson S.A. Cell wall-bound ultraviolet-screening compounds explain the high ultraviolet tolerance of the Antarctic moss, Ceratodon purpureus. New Phytol. 2008;179:776–783. doi: 10.1111/j.1469-8137.2008.02499.x. PubMed DOI
Zhang K.M., Yu H.J., Shi K., Zhou Y.H., Yu J.Q., Xia X.J. Photoprotective roles of anthocyanins in Begonia semperflorens. Plant Sci. 2010;179:202–208. doi: 10.1016/j.plantsci.2010.05.006. DOI
Larsen D.H., Li H., Shrestha S., Verdonk J.C., Nicole C., Marcelis L.F., Woltering E.J. Lack of blue light regulation of antioxidants and chilling tolerance in Basil. Front. Plant Sci. 2022;13:852654. doi: 10.3389/fpls.2022.852654. PubMed DOI PMC
Schmalwieser A.W., Gröbner J., Blumthaler M., Klotz B., De Backer H., Bolsée D., Werner R., Tomsic D., Metelka L., Eriksen P., et al. UV Index monitoring in Europe. Photochem. Photobiol. Sci. 2017;16:1349–1370. doi: 10.1039/c7pp00178a. PubMed DOI
McKenzie R., Smale D., Kotkamp M. Relationship between UVB and erythemally weighted radiation. Photochem. Photobiol. Sci. 2004;3:252–256. doi: 10.1039/b312985c. PubMed DOI
Cerović Z.G., Masdoumier G., Ghozlen N.B., Latouche G. A new optical leaf-clip meter for simultaneous non-destructive assessment of leaf chlorophyll and epidermal flavonoids. Physiol Plant. 2012;146:251–260. doi: 10.1111/j.1399-3054.2012.01639.x. PubMed DOI PMC
Morina F., Jovanović L., Mojović M., Vidović M., Panković D., Veljović Jovanović S. Zinc-induced oxidative stress in Verbascum thapsus is caused by an accumulation of reactive oxygen species and quinhydrone in the cell wall. Physiol. Plant. 2010;140:209–224. doi: 10.1111/j.1399-3054.2010.01399.x. PubMed DOI
Cano A., Hernández-Ruíz J., García-Cánovas F., Acosta M., Arnao M.B. An end-point method for estimation of the total antioxidant activity in plant material. Phytochem. Anal. 1998;9:196–202. doi: 10.1002/(SICI)1099-1565(199807/08)9:4<196::AID-PCA395>3.0.CO;2-W. DOI
Thordal-Christensen H., Zhang Z., Wei Y., Collinge D.B. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley powdery mildew interaction. Plant J. 1997;11:1187–1194. doi: 10.1046/j.1365-313X.1997.11061187.x. DOI