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Improvement of the rice photosynthetic apparatus defence under cadmium stress modulated by salicylic acid supply to roots

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Abstract

The present study was conducted to investigate the effect of exogenous salicylic acid (SA) added to the nutrient solution on the growth parameters and the functions of the photosynthetic apparatus of rice plants under cadmium (Cd) stress. Our investigations have shown that 10 µM SA has an optimal effect in rice plants grown hydroponically. Pulse amplitude modulated chlorophyll fluorescence, low-temperature chlorophyll fluorescence, oxygen evolution (measured with Clark-type and Joliot-type electrodes) and P700 photo-oxidation measurements were carried out to assess the effect of SA on the activity of the photosynthetic apparatus. The levels of three important parameters associated with oxidative stress (hydrogen peroxide, lipid peroxidation and proline content) were measured. The application of low concentration of SA significantly decreased the levels of hydrogen peroxide, lipid peroxidation and proline under Cd stress. The results revealed that low concentration of SA, applied in plants exposed to 150 µM CdCl2, significantly improves plant growth, photochemical activities of both photosystems, the electron flow from QA to plastoquinone, energetic distribution between pigment-protein complexes and the kinetic parameters of oxygen-evolving reactions. This study suggests that exogenous application of 10 µM SA through the rooting medium has a protective effect against Cd toxicity in rice plants. The possible molecular mechanisms involved in the defence effect of SA on the function of photosynthetic apparatus are discussed.

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References

  • Albertsson PA (1995) The structure and function of the chloroplast photosynthetic membrane—a model for the domain organization. Photosynth Res 46:141–149

    Article  CAS  PubMed  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Apostolova EL, Dobrikova AG, Ivanova PI, Petkanchin IB, Taneva SG (2006) Relationship between the organization of the PSII supercomplex and the functions of the photosynthetic apparatus. J Photochem Photobiol B 83:114–122

    Article  CAS  PubMed  Google Scholar 

  • Arivazhagan V, Sharavanan PS (2015) Effect of cadmium on photosynthetic responses and biochemical contents of maize plants. Am J Environ Eng Sci 2:32–36

    Google Scholar 

  • Atal N, Saradhi PP, Mohanty P (1991) Inhibition of the chloroplast photochemical reactions by treatment of wheat seedlings with low concentrations of cadmium: analysis of electron transport activities and changes in fluorescence yield. Plant Cell Physiol 32:943–951

    Article  CAS  Google Scholar 

  • Barkosky RR, Einhellig FA (1993) Effects of salicylic acid on plant water relationship. J Chem Ecol 19:237–247

    Article  CAS  PubMed  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bukhov N, Samson G, Carpentier R (2001) Non photosynthetic reduction of the intersystem electron transport chain of chloroplasts following heat stress. The pool size of stromal reductants. Photochem Photobiol 74:438–443

    Article  CAS  PubMed  Google Scholar 

  • Bukhov N, Egorova E, Carpentier R (2002) Electron flow to photosystem I from stromal reductants in vivo: the size of the pool of stromal reductants controls the rate of electron donation to both rapidly and slowly reducing photosystem I units. Planta 215:812–820

    Article  CAS  PubMed  Google Scholar 

  • Chugh LK, Sawhney SK (1999) Photosynthetic activities of Pisum sativum seedlings grown in presence of cadmium. Plant Physiol Biochem 37:297–303

    Article  CAS  Google Scholar 

  • Croce R, van Amerongen H (2011) Light-harvesting and structural organization of photosystem II: from individual complexes to thylakoid membrane. J Photochem Biochem B Biol 104:142–153

    Article  CAS  Google Scholar 

  • Cutt JR, Klessing DF (1992) Salicylic acid in plants: a changing perspective. Pharm Technol 16:25–34

    Google Scholar 

  • Dąbrowski P, Pawluśkiewicz B, Baczewska-Dąbrowska A, Oglecki P, Kalaji HM (2015) Chlorophyll a fluorescence of perennial ryegrass (Lolium perenne L.) varieties under long term exposure to shade. Zemdirbyste-Agriculture 102(3):305–312

    Article  Google Scholar 

  • Dąbrowski P, Baczewska AH, Pawluśkiewicz B, Paunov M, Alexantrov V, Goltsev V, Kalaji MH (2016) Prompt chlorophyll a fluorescence as a rapid tool for diagnostic changes in PSII structure inhibited by salt stress in Perennial ryegrass. J Photochem Photobiol B 157:22–31

    Article  PubMed  Google Scholar 

  • Djebali W, Zarrouk M, Brouquisse R, Kahoui ES, Limam F, Ghorbel MH, Chaïbi W (2005) Ultrastructure and lipid alterations induced by cadmium in tomato (Lycopersicon esculentum) chloroplast membranes. Plant Biol 7:358–368

    Article  CAS  PubMed  Google Scholar 

  • Dobrikova AG, Yotsova EK, Börner A, Landjeva SP, Apostolova EL (2017) The wheat mutant DELLA-encoding gene (Rht-B1c) affects plant photosynthetic responses to cadmium stress. Plant Physiol Biochem 114:10–18

    Article  CAS  PubMed  Google Scholar 

  • Drazic G, Mihailovic N (2005) Modification of cadmium toxicity in soybean seedlings by salicylic acid. Plant Sci 168:511–517

    Article  CAS  Google Scholar 

  • El-Tayeb MA (2005) Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul 45:215–224

    Article  CAS  Google Scholar 

  • Faller P, Kienzler K, Krieger-Liszkay A (2005) Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of Photosystem II by competitive binding to the essential Ca2+ site. Biochim Biophys Acta 1706(1–2):158–164

    Article  CAS  PubMed  Google Scholar 

  • Fatima RN, Javed F, Wahid A (2014) Salicylic acid modifies growth performance and nutrient status of rice (Oryza sativa) under cadmium stress. Int J Agric Biol 16(6):1083–1090

    CAS  Google Scholar 

  • Genty B, Briantals G, Baker N (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Guo B, Liang YC, Zhu YG, Zhao FJ (2007) Role of salicylic acidin alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. Environ Pollut 147:743–749

    Article  CAS  PubMed  Google Scholar 

  • Hakmaoui A, Ater M, Bóka K, Barón M (2007) Copper and cadmium tolerance, uptake and effect on chloroplast ultrastructure. Studies on Salix purpurea and Phragmites australis. Z Naturforsch C 62:417–426

    Article  CAS  PubMed  Google Scholar 

  • Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68(1):14–25

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast, I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  PubMed  Google Scholar 

  • Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26(3):290–300

    Article  Google Scholar 

  • Hou W, Chen X, Song G, Wang Q, Chang CC (2007) Effect of copper and cadmium on heavy metal polluted water body restoration by duckweed (Lemna minor). Plant Physiol Biochem 45:62–69

    Article  CAS  PubMed  Google Scholar 

  • Hsu YT, Kao CH (2007) Toxicity in leaves of rice exposed to cadmium is due to hydrogen peroxide accumulation. Plant Soil 298:231–241

    Article  CAS  Google Scholar 

  • Kalaji HM, Schansker G, Brestic M, Bussotti F, Calatayud A, Ferroni L et al (2017) Frequently asked questions about chlorophyll fluorescence, the sequel. Photosyn Res 132:13–66

    Article  CAS  PubMed  Google Scholar 

  • Khan W, Prithiviraj B, Smith DL (2003) Photosynthetic responses of corn and soybean to foliar application of salicylates. J Plant Physiol 160:485–492

    Article  CAS  PubMed  Google Scholar 

  • Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18

    Article  CAS  PubMed  Google Scholar 

  • Khodary SEA (2004) Effect of salicylic acid on growth, photosynthesis and carbohydrate metabolism in salt stressed maize plants. Int J Agric Biol 6:5–8

    CAS  Google Scholar 

  • Kitajima M, Butler W (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115

    Article  CAS  PubMed  Google Scholar 

  • Kok B, Forbush B, McGloin M (1970) Co-operation of charges in photosynthetic O2 evolution. I. A linear four step mechanism. Photochem Photobiol 11:457–475

    Article  CAS  PubMed  Google Scholar 

  • Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165:920–931

    Article  CAS  PubMed  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Biol 42:313–349

    Article  CAS  Google Scholar 

  • Larqué-Saavedra A (1979) Stomatal closure in response to acetylsalicylic acid treatment. Z Pflannzenphysiol 93:371–375

    Article  Google Scholar 

  • Li H, Luo N, Li YW, Cai QY, Li HY, Mo CH, Wong NH (2017) Cadmium in rice: Transport mechanisms, influencing factors, and minimizing measures. Environ Pollut 224:622–630

    Article  CAS  PubMed  Google Scholar 

  • Lichtentaler HK (1987) Chlorophyll and carotenoids: pigments of photosynthetic biomembranes. Methods Enzym 148:350–382

    Article  Google Scholar 

  • Lichtenthaler HK, Buschmann C, Knapp M (2005) How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica 43:379–393

    Article  CAS  Google Scholar 

  • Liu JG, Liang JS, Li KQ, Zhang ZJ, Yu BY, Lu XL, Yang JC, Zhu QS (2003) Correlations between cadmium and mineral nutrients in absorption and accumulation in various genotypes of rice under cadmium stress. Chemosphere 52:1467–1473

    Article  CAS  PubMed  Google Scholar 

  • Lu Q, Zhang T, Zhang W, Su C, Yang Y, Hu D, Xu Q (2018) Alleviation of cadmium toxicity in Lemna minor by exogenous salicylic acid. Ecotoxicol Environ Saf 147:500–508

    Article  CAS  PubMed  Google Scholar 

  • Maksymiec W, Krupa Z (2006) The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57:187–194

    Article  CAS  Google Scholar 

  • Maslenkova L, Peeva V, Stojnova Zh, Popova L (2009) Salicylic acid-induced changes in photosystem II reactions in barley plants. Biotechnol Biotechnol Equip 23(1):297–300

    Article  Google Scholar 

  • Maurya R, Prasad SM, Gopal R (2008) LIF technique offers the potential for the detection of cadmium-induced alteration in photosynthetic activities of Zea Mays L. J Photochem Photobiol C 9:29–35

    Article  CAS  Google Scholar 

  • Metwally A, Finkmemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra A, Choudhuri MA (1999) Effects of salicylic acid on heavy metal-induced membrane degradation mediated by lipoxygenase in rice. Biol Plant 42:409–415

    Article  CAS  Google Scholar 

  • Moussa H, El-Gamal S (2010) Effect of salicylic acid pretreatment on cadmium toxicity in wheat. Biol Plant 54:315–320

    Article  CAS  Google Scholar 

  • Nouairi I, Ben Ammar W, Ben Youssef N, Ben Miled Daoud D, Habib Ghorbal M, Zarrouk M (2006) Comparative study of cadmium effects on membrane lipid composition of Brassica juncea and Brassica napus leaves. Plant Sci 170:511–519

    Article  CAS  Google Scholar 

  • Parmar P, Kumari N, Sharma V (2013) Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Bot Studies 54:45–51

    Article  Google Scholar 

  • Popova LP, Maslenkova LT, Yordanova RY, Ivanova AP, Krantev AP, Szalai G, Janda T (2009) Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem 47:224–231

    Article  CAS  PubMed  Google Scholar 

  • Prasad MN (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35:525–545

    Article  CAS  Google Scholar 

  • Rai VK, Sharma SS, Sharma S (1986) Reversal of ABA-induced stomatal closure by phenolic compounds. J Exp Bot 37:129–134

    Article  CAS  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, Del Río LA et al (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544

    Article  PubMed  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testillano PS, Risueno MC, Del Río LA et al (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229–243

    Article  PubMed  PubMed Central  Google Scholar 

  • Roháček K (2002) Chlorophyll fluorescence parameters: the definitions, photosynthetic measuring and mutual relationships. Photosynthetica 40:13–29

    Article  Google Scholar 

  • Sárvári É, Cseh E, Balczer T, Szigeti Z, Záray G, Fodor F (2008) Effect of Cd on the iron re-supply-induced formation of chlorophyll-protein complexes in cucumber. Acta Biol Szeged 52(1):183–186

    Google Scholar 

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    Article  CAS  PubMed  Google Scholar 

  • Schützendübel A, Nikolova P, Rudolf C, Polle A (2002) Cadmium and H2O2-induced oxidative stress in Populus canescens roots. Plant Physiol Biochem 40:577–584

    Article  Google Scholar 

  • Shaff JE, Schultz BA, Craft EJ, Clark RT, Kochian LV (2010) GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant Soil 330:207–214

    Article  CAS  Google Scholar 

  • Shirao M, Takahashi S, Kaneko K, Badger M, Kinjo Y, Forster B, Tsuyama M, Kuroki S (2013) Gymnosperms have increased capacity for electron leakage to oxygen (Mehler and PTOX reactions) in photosynthesis compared with angiosperms. Plant Cell Physiol 54:1152–1163

    Article  CAS  PubMed  Google Scholar 

  • Sigfridsson KGV, Bernát G, Mamedov F, Styring S (2004) Molecular interference of Cd2+ with Photosystem II. Biochim Biophys Acta 1659:19–31

    Article  CAS  PubMed  Google Scholar 

  • Singh S, Eapen S, Souza SFD (2006) Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere 62:233–246

    Article  CAS  PubMed  Google Scholar 

  • Singh PK, Chaturvedi VK, Bose B (2010) Effects of salicylic acid on seedling growth and nitrogen metabolism in cucumber (Cucumis sativus L.). J Stress Physiol Biochem 6(3):102–113

    Google Scholar 

  • Singh AP, Dixit G, Kumar A, Mishra S, Kumar N et al (2017) A protective role for nitric oxide and salicylic acid for arsenite phytotoxicity in rice (Oryza sativa L.). Plant Physiol Biochem 115:163–173

    Article  CAS  PubMed  Google Scholar 

  • Stefanov M, Yotsova K, Rashkov G, Ivanova K, Markovska Y, Apostolova E (2016) Effects of salinity on the photosynthetic apparatus of two Paulownia lines. Plant Physiol Biochem 101:54–59

    Article  CAS  PubMed  Google Scholar 

  • Stefanov M, Yotsova E, Markovska Y, Apostolova EL (2017) Effect of high light intensity on the photosynthetic apparatus of two hybrid lines of Paulownia grown on soils with different salinity. Photosyntetica 55:1–9 (in press)

    Article  Google Scholar 

  • Stoichkova K, Busheva M, Apostolova E, Andreeva A (2006) Changes in the energy distribution in mutant thylakoid membranes of pea with modified pigment content II. Changes due to magnesium ions concentration. J Photochem Photobiol B 83:11–20

    Article  Google Scholar 

  • Tamás L, Mistrík I, Alemayehu A, Zelinová V, Bočová B, Huttová J (2015) Salicylic acid alleviates cadmium-induced stress responses through the inhibition of Cd-induced auxin-mediated reactive oxygen species production in barley root tips. J Plant Physiol 173:1–8

    Article  PubMed  Google Scholar 

  • Tang Y, Sun X, Wen T, Liu M, Yang M, Chen X (2017) Implications of terminal oxidase function in regulation of salicylic acid on soybean seedling photosynthetic performance under water stress. Plant Physiol Biochem 112:19–28

    Article  CAS  PubMed  Google Scholar 

  • Tran TA, Popova L (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turk J Bot 37:1–13

    CAS  Google Scholar 

  • Vassilev A, Lidon F, Scotti P, Da Graca M, Yordanov I (2004) Cadmium-induced changes in chloroplast lipids and photosystem activities in barley plants. Biol Plant 48:153–156

    Article  CAS  Google Scholar 

  • Vestena S, Cambraia J, Ribeiro C, Oliveira JA, Oliva MA (2011) Cadmium induced oxidative stress and antioxidative enzyme response in Water Hyacinth and Salvinia. Braz J Plant Physiol 23:131–139

    Article  CAS  Google Scholar 

  • Wang Y, Qian Y, Hu H, Xu Y, Zhang H (2011) Comparative proteomic analysis of Cd-responsive proteins in wheat roots. Acta Physiologiae Plantarum 33(2):349–357

    Article  CAS  Google Scholar 

  • Wang Q, Liang X, Dong Y, Linlin Xu, Zhang Xiuwei, Kong Jing, Liu Shuang et al (2013) Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of perennial ryegrass under cadmium stress. J Plant Growth Regul 32:721–731

    Article  CAS  Google Scholar 

  • Wodala B, Eitel G, Gyula TN, Ördög A, Horváth F (2012) Monitoring moderate Cu and Cd toxicity by chlorophyll fluorescence and P700 absorbance in pea leaves. Photosynthetica 50:380–386

    Article  CAS  Google Scholar 

  • Xu J, Wang WY, Yin HX, Liu XJ, Sun H, Mi Q (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330

    Article  CAS  Google Scholar 

  • Xue XC, Gao HY, Zhang LT (2013) Effects of cadmium on growth, photosynthetic rate and chlorophyll content in leaves of soybean seedlings. Biol Plant 57:587–590

    Article  CAS  Google Scholar 

  • Yilmaz DD, Parlak KU (2011) Changes in proline accumulation and antioxidative enzyme activities in Groenlandia densa under cadmium stress. Ecol Indic 11:417–423

    Article  CAS  Google Scholar 

  • Yotsova EK, Stefanov MA, Dobrikova AG, Apostolova EL (2017) Different sensitivities of photosystem II in green algae and cyanobacteria to phenylurea and phenol-type herbicides: effect on electron donor side. Zeitschrift für Naturforschung C 72(7–8):315–324

    CAS  Google Scholar 

  • Yotsova E, Dobrikova A, Stefanov M, Apostolova E (2018) Impact of salicylic acid on the growth and the activity of photosynthetic apparatus in rice under non-stress conditions. Compt Rend Acad Bulg Sci, http://www.proceedings.bas.bg/

  • Yuan S, Lin H (2008) Role of salicylic acid in plant abiotic stress. Z Naturforsch 63:313–320

    CAS  Google Scholar 

  • Zeinalov Y (2002) An equipment for investigations of photosynthetic oxygen production reactions. Bulg J Plant Physiol 28:57–67

    Google Scholar 

  • Zeinalov Y (2009) On the minimum quantum requirement of photosynthesis. Z Naturforsch 64:673–679

    CAS  Google Scholar 

  • Zhao FY, Han MM, Zhang SY, Wang K, Zhang CR, Liu T et al (2012) Hydrogen peroxide-mediated growth of the root system occurs via auxin signaling modification and variations in the expression of cell-cycle genes in rice seedlings exposed to cadmium stress. J Integr Plant Biol 54:991–1006

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the Project No. 137/12.05.2016 of Program for career development of young scientists, Bulgarian Academy of Sciences.

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Authors and Affiliations

  1. Institute of Biophysics and Biomedical Engineering, Bulgarian Academy of Sciences, Sofia, Bulgaria

    Ekaterina K. Yotsova, Anelia G. Dobrikova, Martin A. Stefanov & Emilia L. Apostolova

  2. Department of Biophysics and Radiobiology, Biological Faculty, Sofia University, Sofia, Bulgaria

    Margarita Kouzmanova

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  1. Ekaterina K. Yotsova
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  2. Anelia G. Dobrikova
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  3. Martin A. Stefanov
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  4. Margarita Kouzmanova
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  5. Emilia L. Apostolova
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Correspondence to Emilia L. Apostolova.

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Yotsova, E.K., Dobrikova, A.G., Stefanov, M.A. et al. Improvement of the rice photosynthetic apparatus defence under cadmium stress modulated by salicylic acid supply to roots. Theor. Exp. Plant Physiol. 30, 57–70 (2018). https://doi.org/10.1007/s40626-018-0102-9

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