Differential Antioxidant Response to Supplemental UV-B Irradiation and Sunlight in Three Basil Varieties

. 2023 Oct 19 ; 24 (20) : . [epub] 20231019

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37895033

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

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.

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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

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