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Modulations of physiological responses and possible involvement of defense-related secondary metabolites in acclimation of Artemisia annua L. against short-term UV-B radiation

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Main conclusion

UV - B radiation exposure for upto 3 h did not cause direct damage to physiology, but adjusted secondary metabolism and metabolites accumulation as an effective acclimation mechanism to mitigate the adverse effects of radiation.

Artemisia annua L. plants were irradiated with UV-B radiation (280–315 nm; 2.8 Wm−2) for different short-term (1, 2, 3 and 4 h) durations. UV-B irradiation of 3 h reduced the photosynthetic rate, stomatal conductance and transpiration rate. However, F v/F m, a sensitive indicator of photosynthetic inhibition, remained stable (0.78) upto 3 h, thereafter it declined sharply (0.72). Interestingly, transcript level of LHCB1, PSBA and PSBO genes related to photosystem II (PSII) were induced under UV-B exposure. In addition, genes coding for Rubisco small (RBCS1B) and large (RBCL) subunits were also upregulated upto 3 h. To mitigate the adverse effects of UV-B radiation, plants tremendously induced defense-related secondary metabolites such as antioxidative phenolics, UV-B absorbing flavonoids, anthocyanins and protective terpenes. The GC–MS analysis of essential oils revealed relatively higher production of monoterpenes over sesquiterpenes as well as 1.2-folds higher total oil yield under UV-B radiation. Owing to its diverse biological activities, the altered quantity and quality of essential oil of A. annua may contribute towards improving its therapeutic properties. The results suggest that UV-B irradiation upto 3 h reduced photosynthesis, probably due to stomatal limitations rather than any direct injury to photosynthetic apparatus as evident from stable F v/F m value, upregulated genes and greater accumulation of their corresponding proteins which gauge PSII health, elevated UV-B absorbing compounds and other protective metabolites. Correlation analysis indicates a significant positive correlation of photosynthetic rate with stomatal conductance while a negative correlation with anthocyanin and monoterpene contents under UV-B radiation. The present study provides first hand information regarding photosynthesis, related physiological parameters and essential oil profiling in response to UV-B radiation in A. annua.

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References

  • Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition—a historical perspective. Photosynth Res 76:343–370

    Article  CAS  PubMed  Google Scholar 

  • A-H-Mackerness S, Surplus SL, Jordan BR, Thomas B (1998) Effects of supplementary ultraviolet-B radiation on photosynthetic transcripts at different stages of leaf development and light levels in pea (Pisum sativum L.): role of active oxygen species and antioxidant enzymes. Photochem Photobiol 68:88–96. doi:10.1111/j.1751-1097.1998.tb03257.x

    Article  Google Scholar 

  • Allen DJ, Nogués S, Baker NR (1998) Ozone depletion and increased UV-B radiation: is there a real threat to photosynthesis? J Exp Bot 49:1775–1788. doi:10.1093/jxb/49.328.1775

    Article  CAS  Google Scholar 

  • Andersson J, Wentworth M, Walters RG, Howard CA, Ruban AV, Horton P, Jansson S (2003) Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of the photosystem II—effects on photosynthesis, grana stacking and fitness. Plant J 35:350–361. doi:10.1046/j.1365-313X.2003.01811.x

    Article  CAS  PubMed  Google Scholar 

  • Benderradji L, Brini F, Kellou K, Ykhlef N, Djekoun A, Masmoudi K, Bouzerzour H (2012) Callus induction, proliferation, and plantlets regeneration of two bread wheat (Triticum aestivum L.) genotypes under saline and heat stress conditions. ISRN Agron 2012:1–8. doi:10.5402/2012/367851

    Google Scholar 

  • Bricker TM, Frankel LK (2011) Auxiliary functions of the PsbO, PsbP and PsbQ proteins of higher plant photosystem II: a critical analysis. J Photochem Photobiol B 104:165–178. doi:10.1016/j.jphotobiol.2011.01.025

    Article  CAS  PubMed  Google Scholar 

  • Cai Y, Jiaa JW, Crockb J, Linc ZX, Chena XY, Croteau R (2002) A cDNA clone for b-caryophyllene synthase from Artemisia annua. Phytochemistry 61:523–529. doi:10.1016/S0031-9422(02)00265-0

    Article  CAS  PubMed  Google Scholar 

  • Carvalho IS, Cavaco T, Brodelius M (2011) Phenolic composition and antioxidant capacity of six Artemisia species. Ind crops prod 33:382–388. doi:10.1016/j.indcrop.2010.11.005

    Article  CAS  Google Scholar 

  • Cechin I, Rocha VJ, Fumis TF (2012) Sensitivity of yellow passion fruit to ultraviolet-B radiation. Pesq agropec bras 47(10):1422–1427. doi:10.1590/S0100-204X2012001000002

    Article  Google Scholar 

  • Chang C, Yang M, Wen H, Chern J (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Analysis 10:178–182

    CAS  Google Scholar 

  • Chang X, Alderson PG, Wright CJ (2009) Enhanced UV-B radiation alters basil (Ocimum basilicum L) growth and stimulates the synthesis of volatile oils. J Hortic For 1:027–031

    Google Scholar 

  • Clark RJ, Menary RC (1980) Environmental effects on peppermint, I. Effect of day length, photon flux density, night temperature and day temperature on yield and composition of peppermint oil. Aust J Plant Physiol 7:685–692. doi:10.1071/PP9800685

    CAS  Google Scholar 

  • Close DC, McArthor C (2002) Rethinking the role of many plant phenolics—protection against photodamage not herbivores? Oikos 99:166–172. doi:10.1034/j.1600-0706.2002.990117.x

    Article  CAS  Google Scholar 

  • Fedina I, Hidema J, Velitchkova M, Georgieva K, Nedeva D (2010) UV-B induced stress responses in three rice cultivars. Biol Plant 54(3):571–574. doi:10.1007/s10535-010-0102-3

    Article  CAS  Google Scholar 

  • Fu BY, Xiong JH, Zhu LH, Zhao XQ, Xu HX, Gao YM, Li YS, Xu JL, Li ZK (2007) Identification of functional candidate genes for drought tolerance in rice. Mol Genet Genomics 278:599–609. doi:10.1007/s00438-007-0276-3

    CAS  PubMed  Google Scholar 

  • Gil M, Bottini R, Berli F, Pontin M, Silva MF, Piccoli P (2013) Volatile organic compounds characterized from grapevine (Vitis vinifera L. cv. Malbec) berries increase at pre-harvest and in response to UV-B radiation. Phytochemistry 96:148–157. doi:10.1016/j.phytochem.2013.08.011

    Article  CAS  PubMed  Google Scholar 

  • Greenberg BMMI, Wilson X, Huang CL, Duxbury KE, Gerhardt RW, Gensener (1997) The effects of ultraviolet-B radiation on higher plants. In: Wang W, Gorsuch JW, Hughes JS (eds) Plants for environmental studies. Lewis Publishers, New York, pp 1–36

    Google Scholar 

  • Gwynn-Jones D (2001) Short-term impacts of enhanced UV-B radiation on photoassimilate allocation and metabolism: a possible interpretation for time-dependent inhibition of growth. Plant Ecol 154:67–73. doi:10.1023/A:1012963021074

    Article  Google Scholar 

  • Hideg E, Jansen MA, Strid A (2013) UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends Plant Sci 18(2):107–115. doi:10.1016/j.tplants.2012.09.003

    Article  CAS  PubMed  Google Scholar 

  • Holopainen JK (2004) Multiple functions of inducible plant volatiles. Trends Plant Sci 9:529–533. doi:10.1016/j.tplants.2004.09.006

    Article  CAS  PubMed  Google Scholar 

  • Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J, Tholl D (2012) The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-b-caryophyllene, is a defense against a bacterial pathogen. New Phytol 193(4):997–1008. doi:10.1111/j.1469-8137.2011.04001

    Article  CAS  PubMed  Google Scholar 

  • Imeh U, Khokhar S (2002) Distribution of conjugated and free phenols in fruits: antioxidant activity and cultivar variations. J Agric Food Chem 50:6301–6306. doi:10.1021/jf020342j

    Article  CAS  PubMed  Google Scholar 

  • Jansen MAK, Gaba V, Greenberg BM, Mattoo AK, Edelman M (1996a) Low threshold levels of ultraviolet-B in a background of photosynthetically active radiation trigger rapid degradation of the D2 protein of photosystem II. Plant J 9:693–699. doi:10.1046/j.1365-313X.1996.9050693.x

    Article  CAS  Google Scholar 

  • Jansen MAK, Greenberg BM, Edelman M, Mattoo AK, Gaba V (1996b) Accelerated degradation of the D2 protein of photosystem II under ultraviolet radiation. Photochem Photobiol 63:814–817. doi:10.1111/j.1751-1097.1996.tb09636.x

    Article  CAS  Google Scholar 

  • Juteau F, Masotti V, Bessière JM, Dherbomez M, Viano J (2002) Antibacterial and antioxidant activities of Artemisia annua essential oil. Fitoterapia 73:532–535. doi:10.1016/S0367-326X(02)00175-2

    Article  CAS  PubMed  Google Scholar 

  • Kalbina I, Strid A (2006) Supplementary ultraviolet-B irradiation reveals differences in stress responses between Arabidopsis thaliana ecotypes. Plant, Cell Environ 29:754–763. doi:10.1111/j.1365-3040.2005.01436.x

    Article  CAS  Google Scholar 

  • Koltermann D, Schreiner M, Krumbein A, Mewis I, Ulrichs C, Huyskens-Keil S (2007) UV-B radiation mediated changes of bioactive compounds Brassica juncea L. Proceedings of Eco Summit (ES’07), China, pp 1–161

  • Lawlor DW, Tezara W (2009) Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Ann Bot 103:561–579. doi:10.1093/aob/mcn244

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li L, Huang Q, Zhang S, Zhao S (2013) Effect of enhanced UV-B radiation and low-energy N+ ion beam radiation on the response of photosynthesis, antioxidant enzymes, and lipid peroxidation in rice (Oryza sativa) seedlings. Appl Biochem Biotechnol 171(4):1072–1083. doi:10.1007/s12010-013-0361-5

    Article  CAS  PubMed  Google Scholar 

  • Lilley JM, Ludlow MM, McCouch SR, O’Toole JC (1996) Locating QTL for osmotic adjustment and dehydration tolerance in rice. J Exp Bot 47:1427–1436. doi:10.1093/jxb/47.9.1427

    Article  CAS  Google Scholar 

  • Loreto F, Pinelli P, Manes F, Kollist H (2004) Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex leaves. Tree Physiol 24:361–367. doi:10.1093/treephys/24.4.361

    Article  CAS  PubMed  Google Scholar 

  • Maffei M, Codignola A (1990) Photosynthesis, photorespiration and herbicide effect on terpene production in peppermint (Mentha piperita L.). J Essent Oil Res 2:275–286. doi:10.1080/10412905.1990.9697886

    Article  CAS  Google Scholar 

  • Mancinelli AL, Yang CH, Lindquist P, Anderson OR, Rabino I (1975) Photocontrol of anthocyanin synthesis: III. The action of streptomycin on the synthesis of chlorophyll and anthocyanin. Plant Physiol 55:251–257. doi:10.1104/pp.55.2.251

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martínez-Lüscher J, Morales F, Delrot S, Sánchez-Díaz M, Gomés E, Aguirreolea J, Pascual I (2013) Short- and long-term physiological responses of grapevine leaves to UV-B radiation. Plant Sci 213:114–122. doi:10.1016/j.plantsci.2013.08.010

    Article  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence––a practical guide. J Expt Bot 51:659–668. doi:10.1093/jexbot/51.345.659

    Article  CAS  Google Scholar 

  • Mohanpuria P, Yadav SK (2009) Retardation in seedling growth and induction of early senescence in plants upon caffeine exposure is related to its negative effect on Rubisco. Photosynthetica 47(2):293–297. doi:10.1007/s11099-009-0045-0

    Article  CAS  Google Scholar 

  • Nogues S, Allen DJ, Morison JIL, Baker NR (1999) Characterization of stomatal closure caused by ultraviolet-B radiation. Plant Physiol 121:489–496. doi:10.1104/pp.121.2.489

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nogués S, Allen DJ, Morison JIL, Baker NR (1998) Ultraviolet‐B radiation effects on water relations, leaf development, and photosynthesis in droughted pea plants. Plant Physiol 117:173–181. doi:10.1104/pp.117.1.173

    Article  PubMed Central  PubMed  Google Scholar 

  • Oberhuber W, Bauer H (1991) Photoinhibition of photosynthesis under natural conditions in ivy (Hedera helix L.) growing in an understory of deciduous trees. Planta 185:545–553. doi:10.1007/BF00202965

    Article  CAS  PubMed  Google Scholar 

  • Pandey N, Pandey-Rai S (2014) Short-term UV-B radiation-mediated transcriptional responses and altered secondary metabolism of in vitro propagated plantlets of Artemisia annua L. Plant Cell Tiss Organ Cult 116:371–385. doi:10.1007/s11240-013-0413-0

    Article  CAS  Google Scholar 

  • Pawłowicz I, Kosmala A, Rapacz M (2012) Expression pattern of the psbO gene and its involvement in acclimation of the photosynthetic apparatus during abiotic stresses in Festuca arundinacea and F. Pratensis. Acta Physiol Plant 34:1915–1924. doi:10.1007/s11738-012-0992-0

    Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Radulović NS, Randjelović PJ, Stojanović NM, Blagojević PD, Stojanović-Radić ZZ, Ilić IR, Djordjević VB (2013) Toxic essential oils. Part II: Chemical, toxicological, pharmacological and microbiological profiles of Artemisia annua L. Volatiles. Food Chem Toxicol 58:37–49. doi:10.1016/j.fct.2013.04.016

    Article  PubMed  Google Scholar 

  • Romero MR, Efferth T, Serrano MA, Castano B, Macias RI, Briz O, Marin JJ (2005) Effect of artemisinin/artesunate as inhibitors of hepatitis B virus production in an “in vitro” replicative system. Antiviral Res 68:75–83. doi:10.1016/j.antiviral.2005.07.005

    Article  CAS  PubMed  Google Scholar 

  • Sangwan NS, Farooqi AHA, Shabih F, Sangwan RS (2001) Regulation of essential oil production in plants. Plant Growth Regul 34:03–21. doi:10.1023/A:1013386921596

    Article  CAS  Google Scholar 

  • Sarvikas P, Hakala M, Pa¨tsikka E, Tyystja¨rvi T, Tyystja¨rvi E (2006) Action spectrum of photoinhibition in leaves of wild type and npq1-2 and npq4-1 mutants of Arabidopsis thaliana. Plant Cell Physiol 47:391–400. doi:10.1093/pcp/pcj006

    CAS  PubMed  Google Scholar 

  • Sen R, Bandyopadhyay S, Dutta A, Mandal G, Ganguly S, Saha P, Chatterjee M (2007) Artemisinin triggers induction of cell-cycle arrest and apoptosis in Leishmania donovani promastigotes. J Med Microbiol 56:1213–1218. doi:10.1099/jmm.0.47364-0

    Article  CAS  PubMed  Google Scholar 

  • Silva RR, Caˆmara CAG, Almeida AV, Ramos CS (2012) Biotic and abiotic stress-induced phenylpropanoids in leaves of the mango tree (Mangifera indica L., Anacardiaceae). J Braz Chem Soc 23:206–211. doi:10.1590/S0103-50532012000200003

    Google Scholar 

  • Singh M (2000) Turnover of D1 protein encoded by psbA gene in higher plants and cyanobacteria sustains photosynthetic efficiency to maintain plant productivity under photoinhibitory irradiance. Photosynthetica (Prague) 38:161–169. doi:10.1023/A:1007297227403

    Article  CAS  Google Scholar 

  • Smith JL, Burritt DJ, Bannister P (2000) Shoot dry weight, chlorophyll and UV-B-absorbing compounds as indicators of a plant’s sensitivity to UV-B radiation. Ann Bot 86:1057–1063. doi:10.1006/anbo.2000.1270

    Article  CAS  Google Scholar 

  • Smith WE, Shivaji R, Williams WP, Luthe DS, Sandoya GV, Smith CL, Sparks DL, Brown AE (2012) A maize line resistant to herbivory constitutively releases (E)-b-caryophyllene. J Econ Entomol 105:120–128

    Article  CAS  PubMed  Google Scholar 

  • Verma RK, Chauhan A, Verma RS, Gupta AK (2011) Influence of planting date on growth, artemisinin yield, seed and oil yield of Artemisia annua L. under temperate climatic conditions. Ind Crops Prod 34:860–864. doi:10.1016/j.indcrop.2011.02.004

    Article  CAS  Google Scholar 

  • Vuorinen T, Nerg AM, Ibrahim MA, Reddy GV, Holopainen JK (2004) Emission of Plutella xylostella-induced compounds from cabbages grown at elevated CO2 and orientation behavior of the natural enemies. Plant Physiol 135:1984–1992. doi:10.1104/pp.104.047084

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wahid A, Ghazanfar A (2006) Possible involvement of some secondary metabolites in salt tolerance of sugarcane. J Plant Physiol 163:723–730. doi:10.1016/j.jplph.2005.07.007

    Article  CAS  PubMed  Google Scholar 

  • Xiong JH, Fu BY, Xu HX, Li YS (2010) Proteomic analysis of PEG-simulated drought stress responsive proteins of rice leaves using a pyramiding rice line at the seedling stage. Bot Stud 51:137–145

    CAS  Google Scholar 

  • Xu YH, Liu R, Yan L, Liu ZQ, Jiang SC, Shen YY, Wang XF, Zhang DP (2012) Light-harvesting chlorophyll a/b-binding proteins are required for stomatal response to abscisic acid in Arabidopsis. J Exp Bot 63(3):1095–1106. doi:10.1093/jxb/err315

    Article  PubMed Central  PubMed  Google Scholar 

  • Yao X, Liu Q (2006) Changes in morphological, photosynthetic and physiological responses of Mono Maple seedlings to enhanced UV-B and to nitrogen addition. Plant Growth Regul 50:165–177. doi:10.1007/s10725-006-9116-4

    Article  CAS  Google Scholar 

  • Yu GH, Li W, Yuan ZY, Cui HY, Lv CG, Gao ZP, Han B, Gong YZ, Chen GX (2013) The effects of enhanced UV-B radiation on photosynthetic and biochemical activities in super-high-yield hybrid rice Liangyoupeijiu at the reproductive stage. Photosynthetica 51(1):33–44. doi:10.1007/s11099-012-0081-z

    Article  CAS  Google Scholar 

  • Zlatev ZS, Lidon FJC, Kaimakanova M (2012) Plant physiological responses to UV-B radiation. Emir J Food Agric 24(6):481–501. doi:10.9755/ejfa.v24i6.14669

    Google Scholar 

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Acknowledgments

The authors are thankful to CSIR (council of scientific and industrial research), India, for financial assistance, Prof. S.B. Agrawal and Dr. Hema Singh for providing facilities to conduct gas exchange and chlorophyll fluorescence analysis and Dr. Priyanka Pandey for her assistance in heat map preparation.

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Correspondence to Shashi Pandey-Rai.

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N. Pandey and S. Pandey-Rai have contributed equally.

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Pandey, N., Pandey-Rai, S. Modulations of physiological responses and possible involvement of defense-related secondary metabolites in acclimation of Artemisia annua L. against short-term UV-B radiation. Planta 240, 611–627 (2014). https://doi.org/10.1007/s00425-014-2114-2

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