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Europium improves the transport of quercetin through Arabidopsis thaliana

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Biologia Plantarum

Abstract

The effect of a rare earth element europium (Eu) on the long-distance transport of a plant defence compound quercetin (Q) was investigated. The complex Q/Eu3+ was synthesized in a HEPES buffer and tested for its transport ability through Arabidopsis thaliana and its ability to interact with target molecules in plant cells. Our results show that complexation with Eu3+ enhanced the transport of Q through Arabidopsis roots. During the transport, the complex degraded and released a free Q to tissues where Q was originally not available. Thus, the plant became better supplied with the defensive compound Q. The obtained spectrophotometric data imply that one of the reasons for the Q/Eu3+ degradation was the interaction of the complex with double stranded RNAs (dsRNAs) present in Arabidopsis. Since dsRNAs are replicative forms of plant RNA viruses, the ability of Q/Eu3+ to release a free Q in their presence suggests further investigation of this complex as a potential antiviral agent.

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Abbreviations

CMVsat:

satellite-associated Cucumber mosaic virus

DPBA:

diphenylboric acid-2 aminoethyl ester

dsRNA:

double-stranded RNA

Eu:

europium

HEPES:

4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid

Q:

quercetin

ssRNA:

single-stranded RNA

References

  • Ahmed, N., Maekawa, M., Noda, K.: Anthocyanin accumulation and expression pattern of anthocyanin biosynthesis genes in developing wheat coleoptiles. — Biol. Plant. 53: 223–228, 2009.

    Article  CAS  Google Scholar 

  • Ahn, S.Y., Kim, S.A., Cho, K.S., Yun, H.K.: Expression of genes related to flavonoid and stilbene synthesis as affected by signaling chemicals and Botrytis cinerea in grapevines. — Biol. Plant. 58: 758–767, 2014.

    Article  CAS  Google Scholar 

  • Anderegg, G., Ripperger, H.: Correlation between metal complex formation and biological activity of nicotianamine analogues. — J. chem. Soc. chem. Commun. 10: 647–650, 1989.

    Article  Google Scholar 

  • Benes, I., Schreiber, K., Ripperger, H., Kirsceiss, A.: Metal complex formation of nicotianamine, a possible phytosiderophore. — Experientia 39: 261–262, 1983.

    Article  CAS  Google Scholar 

  • Buer, C.S., Muday, G.K.: The transparent testa 4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. — Plant Cell 16: 1191–1205, 2004.

  • Buer, C.S., Muday, G.K., Djordjevic, M.A.: Flavonoids are differentially taken up and transported long distances in Arabidopsis. — Plant Physiol. 145: 478–490, 2007.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Carlson, E.E.: Natural products as chemical probes. — ACS Chem. Biol. 5: 639–653, 2010.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen, S.M., Li, C.H., Zhu, X.R., Deng, Y.M., Sun, W., Wang, L.S., Chen, F.D., Zhang, Z.: The identification of flavonoids and the expression of genes of anthocyanin biosynthesis in the chrysanthemum flowers. — Biol. Plant. 56: 458–464, 2012.

    Article  CAS  Google Scholar 

  • Curie, C., Cassin, G., Couch, D., Divol, F., Higuchi, K., Le Jean, M., Misson, J., Schikora, A., Czernic, P., Mari, S.: Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. — Ann. Bot. 103: 1–11, 2009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dodds, J.A., Morris, T.J., Jordan, R.L.: Plant viral doublestranded RNA. — Annu. Rev. Phytopathol. 22: 151–168, 1984.

    Article  CAS  Google Scholar 

  • Dolatabadi, J.E.N.: Molecular aspects on the interaction of quercetin and its metal complexes with DNA. — Int. J. biol. Macromol. 48: 227–233, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Emsley, J.: An A-Z guide to the elements. — In: Emsley, J. (ed.): Nature’s Building Blocks. Pp. 141–142. Oxford University Press, Oxford 2003.

    Google Scholar 

  • Erlund, I.: Review of the flavonoids quercetin, hesperetin, and naringenin. Dietary sources, bioactivities, and epidemiology. — Nutr. Res. 24: 851–874, 2004.

    Article  CAS  Google Scholar 

  • Fellows, R.J., Wang, Z.M., Ainsworth, C.C.: Europium uptake and partitioning in oat (Avena sativa) roots as studied by laser-induced fluorescence spectroscopy and confocal microscopy profiling technique. — Environ. Sci. Technol. 37: 5247–5253, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Frangne, N., Eggmann, T., Koblischke, C., Weissenbock, G., Martinoia, E., Klein, M.: Flavone glucoside uptake into barley mesophyll and Arabidopsis cell culture vacuoles. Energization occurs by H+-antiport and ATP-binding cassette-type mechanisms. — Plant Physiol. 128: 726–733, 2002.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • French, C.J., Towers, G.H.N.: Inhibition of infectivity of potatovirus X by flavonoids. — Phytochemistry 31: 3017–3020, 1992.

    Article  CAS  Google Scholar 

  • Gao, Y.S., Zeng, F.L., Yi, A., Ping, S., Jing, L.H.: Research of the entry of rare earth elements Eu3+ and La3+ into plant cell. — Biol. Trace Element Res. 91: 253–265, 2003.

    Article  CAS  Google Scholar 

  • González-Álvarez, M., Alzuet, G., Garcia-Gimenez, J.L., Macias, B., Borras, J.: Biological activity of flavonoids copper complexes. — Zeit. anorg. allg. Chem. 631: 2181–2187, 2005.

    Article  Google Scholar 

  • Jacobs, M., Rubery, P.H.: Naturally-occurring auxin transport regulators. — Science 241: 346–349, 1988.

    Article  CAS  PubMed  Google Scholar 

  • Kearney, C.M., Gonsalves, D., Provvidenti, R.: A severe strain of Cucumber mosaic virus from China and its associated satellite RNA. — Plant Dis. 74: 819–823, 1990.

    Article  CAS  Google Scholar 

  • Kostyuk, V.A., Potapovich, A.I., Strigunova, E.N., Kostyuk, T.V., Afanas’ev, I.B.; Experimental evidence that flavonoid metal complexes may act as mimics of superoxide dismutase. — Arch. Biochem. Biophys. 428: 204–208, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Kostyuk, V.A., Potapovich, A.I., Vladykovskaya, E.N., Korkina, L.G., Afanas’ev, I.B.: Influence of metal ions on flavonoid protection against asbestos-induced cell injury. — Arch. Biochem. Biophys. 385: 129–137, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Krcatović, E., Rusak, G., Bezić, N., Krajačić, M.: Inhibition of tobacco mosaic virus infection by quercetin and vitexin. — Acta virol. 52: 119–124, 2008.

    PubMed  Google Scholar 

  • Leif, R.C., Vallarino, L.M., Becker, M.C., Yang, S.: Increasing the luminescence of lanthanide complexes. — Cytometry Part A 69: 767–778, 2006.

    Article  Google Scholar 

  • Levizou, E., Karageorgou, P., Petropoulou, Y., Grammatikopoulos, G, Manetas, Y.: Induction of ageotropic response in lettuce radicle growth by epicuticular flavonoid aglycons of Dittrichia viscosa. — Biol. Plant. 48: 305–307, 2004.

    Article  CAS  Google Scholar 

  • Maeder, M., Zuberbühler, A.D.: Non linear least-squares fitting of multivariate absorption data. — Anal. Chem. 62: 2220–2224, 1990.

    Article  CAS  Google Scholar 

  • Malhotra, B., Onyilagha, J.C., Bohm, B.A., Towers, G.H.N., James, D., Harborne, J.B., French, C.J.: Inhibition of tomato ring spot virus by flavonoids. — Phytochemistry 43: 1271–1276, 1996.

    Article  CAS  Google Scholar 

  • Marinić, M., Piantanida, I., Rusak, G., Žinić, M.: Interactions of quercetin and its lanthane complex with double stranded DNA/RNA and single stranded RNA: spectrophotometric sensing of poly G. — J. Inorg. Biochem. 100: 288–298, 2006.

    Article  PubMed  Google Scholar 

  • Quideau, S., Deffieux, D., Douat-Casassus, C., Pouysegu, L.: Plant polyphenols: chemical properties, biological activities, and synthesis. — Angew. Chem. Int. Edit. 50: 586–621, 2011.

    Article  CAS  Google Scholar 

  • Rusak, G., Černi, S., Polančec, D.S., Ludwig-Müller, J.: The responsiveness of the IAA2 promoter to IAA and IBA is differentially affected in Arabidopsis roots and shoots by flavonoids. — Biol. Plant. 54: 403–414, 2010.

    Article  CAS  Google Scholar 

  • Rusak, G., Krajačić, M., Krsnik-Rasol, M., Gutzeit, H.O.: Quercetin influences response in Nicotiana megalosiphon infected by satellite-associated cucumber mosaic virus. — J. Plant Dis. Protect. 114: 145–150, 2007.

    CAS  Google Scholar 

  • Rusak, G., Krajačić, M., Pleše, N.: Inhibition of tomato bushy stunt virus infection using a quercetagetin flavonoid isolated from Centaurea rupestris L. — Antivir. Res. 36: 125–129, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Rusak, G., Piantanida, I., Bretschneider, S., Ludwig-Müller, J.: Complex formation of quercetin with lanthanum enhances binding to plant viral satellite double stranded RNA. — J. Inorg. Biochem. 103: 1597–1601, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Škorić, D., Krajačić, M., Barbarossa, L., Cillo, F., Grieco, F., Šarić, A., Gallitelli, D.: Occurence of Cucumber mosaic cucumovirus with satellite RNA in lethal necrosis affected tomatoes in Croatia. — J. Phytopathol. 144: 543–549, 1996.

    Article  Google Scholar 

  • Stafford, H.A.: Flavonoid evolution — an enzymatic approach. — Plant Physiol. 96: 680–685, 1991.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tian, H.E., Gao, Y.S., Li, F.M., Zeng, F.L.: Effects of europium ions (Eu3+) on the distribution and related biological activities of elements in Lathyrus sativus L. roots. — Biol. Trace Element Res. 93: 257–269, 2003.

    Article  CAS  Google Scholar 

  • Tian, H.E., Gao, Y.S., Zeng, F.L., Li, F.M., Shan, L.: Effects of Eu3+ on the metabolism of aminoacid and protein in xerophytic Lathyrus sativus L. — Biol. Trace Element. Res. 105: 257–267, 2005.

    Article  CAS  Google Scholar 

  • Wang, S.X., Zhang, F.J., Feng, Q.P., Li, Y.L.: Synthesis, characterization, and antibacterial activity of transition metal complexes with 5-hydroxy-7,4′-dimethoxyflavone. — J. Inorg. Biochem. 46: 251–257, 1992.

    Article  CAS  PubMed  Google Scholar 

  • Ward, F.E., Garling, D.L., Buckler, R.T., Lawler, D.M., Cummings, D.P.: Antimicrobial 3-methyleneflavanones. — J. Med. Chem. 24: 1073–1077, 1981.

    Article  CAS  PubMed  Google Scholar 

  • Woźnicka, E., Kopacz, M., Umbreit, M., Klos, J.: New complexes of La(III), Ce(III), Pr(III), Nd(III), Sm(III), Eu(III) and Gd(III) ions with morin. — J. Inorg. Biochem. 101: 774–782, 2007.

    Article  PubMed  Google Scholar 

  • Zeng, F.L., Tian, H.E., Wang, Z.P., An, Y., Gao, F.Y., Zhang, L.J., Li, F.M., Shan, L.: Effect of rare earth element europium on amaranthin synthesis in Amaranthus caudatus seedlings. — Biol. Trace Element Res. 93: 271–282, 2003.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Faculty of Science, University of Zagreb, Horvatovac 102a, 10000, Zagreb, Croatia

    I. Šola & G. Rusak

  2. Division of Organic Chemistry and Biochemistry, RuĐer Bošković Institute, Bijenička cesta 54, 10000, Zagreb, Croatia

    I. Piantanida & I. Crnolatac

Authors
  1. I. Šola
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  2. I. Piantanida
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  3. I. Crnolatac
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  4. G. Rusak
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Corresponding authors

Correspondence to I. Šola or I. Crnolatac.

Additional information

Acknowledgements: This work was financially supported by the Ministry of Science, Education and Sport of Croatia (098-0982914-2918 and broj Rusak projekta) The authors are grateful to Dr. M. HadŽija, the Laboratory for Molecular Endocrinology and Transplantation, Ruđer Bošković Institute, for help with a fluorescence microscope.

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Šola, I., Piantanida, I., Crnolatac, I. et al. Europium improves the transport of quercetin through Arabidopsis thaliana . Biol Plant 59, 554–559 (2015). https://doi.org/10.1007/s10535-015-0508-z

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  • DOI: https://doi.org/10.1007/s10535-015-0508-z

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