Abstract
Key message
Vanadium compounds increased the content and release of distinct isoflavones in a Trifolium pratense suspension culture. Regarding transport-mechanism inhibitors, the process was mostly facilitated by ABC proteins and vesicular transport.
Abstract
The transport of isoflavones and other secondary metabolites is an important part of metabolism within plants and cultures in vitro regarding their role in defence against various abiotic and biotic stressors. This research focuses on the way how to increase production and exudation of isoflavones by application of chemical elicitor and the basic identification of their transport mechanisms across cell membranes. The release of five isoflavones (genistin, genistein, biochanin A, daidzein, and formononetin) into a nutrient medium was determined in a Trifolium pratense var. DO-8 suspension culture after two vanadium compound treatments and cultivation for 24 and 48 h. The NH4VO3 solution caused a higher concentration of isoflavones in the medium after 24 h. This increased content of secondary metabolites was subsequently suppressed by distinct transport-mechanism inhibitors. The transport of isoflavones in T. pratense was mostly affected by ABC inhibitors from the multidrug-resistance-associated protein subfamily, but the genistein concentration in the medium was lower after treatment with multidrug-resistance protein subfamily inhibitors. Brefeldin A, which blocks vesicular transport, also decreased the concentration of some isoflavones in the nutrient medium.
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Abbreviations
- ABC:
-
ATP-binding cassette protein
- MATE:
-
Multidrug and toxin extrusion protein
- MDR:
-
Multidrug-resistance protein
- MRP:
-
Multidrug-resistance-associated protein
- PAL:
-
Phenylalanine ammonia-lyase
- PDR:
-
Pleiotropic drug-resistance protein
- ROS:
-
Reactive oxygen species
References
Agati G, Azzarello E, Pollastri S, Tattini M (2012) Flavonoids as antioxidants in plants: location and functional significance. Plant Sci 196:67–76. https://doi.org/10.1016/j.plantsci.2012.07.014
Armero J, Tena M (2001) Possible role of plasma membrane H+-ATPase in the elicitation of phytoalexin and related isoflavone root secretion in chickpea (Cicer arietinum L.) seedlings. Plant Sci 161:791–798. https://doi.org/10.1016/S0168-9452(01)00472-1
Arora A, Byrem TM, Nair MG, Strasburg GM (2000) Modulation of liposomal membrane fluidity by flavonoids and isoflavonoids. Arch Biochem Biophys 373:102–109. https://doi.org/10.1006/abbi.1999.1525
Banasiak J, Biała W, Staszków A et al (2013) A Medicago truncatula ABC transporter belonging to subfamily G modulates the level of isoflavonoids. J Exp Bot 64:1005–1015. https://doi.org/10.1093/jxb/ers380
Bewaji CO (1993) Studies on vanadium interactions with the membrane-bound calcium-pumping ATPase from porcine erythrocytes. Niger J Biochem Mol Biol 8:18–22
Borgnia MJ, Eytan GD, Assaraf YG (1996) Competition of hydrophobic peptides, cytotoxic drugs, and chemosensitizers on a common P-glycoprotein pharmacophore as revealed by its ATPase activity. J Biol Chem 271:3163–3171. https://doi.org/10.1074/jbc.271.6.3163
Buer CS, Muday GK, Djordjevic MA (2007) Flavonoids are differentially taken up and transported long distances in arabidopsis. Plant Physiol 145:478–490. https://doi.org/10.1104/pp.107.101824
Chen L, Liu Y, Liu H et al (2015) Identification and expression analysis of MATE genes involved in flavonoid transport in blueberry plants. PLoS One 10:e0118578. https://doi.org/10.1371/journal.pone.0118578
Crans DC, Smee JJ, Gaidamauskas E, Yang L (2004) The chemistry and biochemistry of vanadium and the biological activities exerted by vanadium compounds. Chem Rev 104:849–902. https://doi.org/10.1021/cr020607t
Forestier C, Frangne N, Eggmann T, Klein M (2003) Differential sensitivity of plant and yeast MRP (ABCC)-mediated organic anion transport processes towards sulfonylureas. FEBS Lett 554:23–29. https://doi.org/10.1016/S0014-5793(03)01064-0
Frangne N, Eggmann T, Koblischke C et al (2002) 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. https://doi.org/10.1104/pp.010590
Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158. https://doi.org/10.1016/0014-4827(68)90403-5
Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204–2214. https://doi.org/10.1016/j.febslet.2007.03.050
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Hattori T, Ohta Y (1985) Induction of phenylalanine ammonia-lyase activation and isoflavone glucoside accumulation in suspension-cultured cells of red bean, Vigna angularis, by phytoalexin elicitors, vanadate, and elevation of medium ph. Plant Cell Physiol 26:1101–1110. https://doi.org/10.1093/oxfordjournals.pcp.a077006
Huang C, Zhong JJ (2013) Elicitation of ginsenoside biosynthesis in cell cultures of Panax ginseng by vanadate. Process Biochem 48:1227–1234. https://doi.org/10.1016/j.procbio.2013.05.019
Imtiaz M, Mushtaq MA, Nawaz MA et al (2018) Physiological and anthocyanin biosynthesis genes response induced by vanadium stress in mustard genotypes with distinct photosynthetic activity. Environ Toxicol Pharmacol 62:20–29. https://doi.org/10.1016/j.etap.2018.06.003
Jeandet P, Hébrard C, Deville M-A et al (2014) Deciphering the role of phytoalexins in plant–microorganism interactions and human health. Molecules 19:18033–18056. https://doi.org/10.3390/molecules191118033
Kang J, Hwang J-U, Lee M et al (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci 107:2355–2360. https://doi.org/10.1073/pnas.0909222107
Karuppanapandian T, Moon JC, Kim C, Manoharan K, Kim W (2011) Reactive oxygen species in plants: their generation, signal transduction, and scavenging mechanisms. Aust J Crop Sci 5:709–725. https://doi.org/10.1007/s11046-014-9801-1
Kasparova M, Siatka T, Klimesova V, Dusek J (2012) New synthetic pyridine derivate as potential elicitor in production of isoflavonoids and flavonoids in Trifolium pratense L. suspension culture. Sci World J 2012:746412. https://doi.org/10.1100/2012/746412
Klein M, Martinoia E, Hoffmann-Thoma G, Weissenböck G (2000) A membrane-potential dependent ABC-like transporter mediates the vacuolar uptake of rye flavone glucuronides: regulation of glucuronide uptake by glutathione and its conjugates. Plant J 21:289–304. https://doi.org/10.1046/j.1365-313X.2000.00684.x
Kneer R, Poulev AA, Olesinski A, Raskin I (1999) Characterization of the elicitor-induced biosynthesis and secretion of genistein from roots of Lupinus luteus L. J Exp Bot 50:1553–1559. https://doi.org/10.1093/jxb/50.339.1553
Korbecki J, Baranowska-Bosiacka I, Gutowska I, Chlubek D (2012) Biochemical and medical importance of vanadium compounds. Acta Biochim Pol 59:195–200
Kubes J, Tumova L, Martin J et al (2014) The production of isoflavonoids in Genista tinctoria L. cell suspension culture after abiotic stressors treatment. Nat Prod Res 28:2253–2263. https://doi.org/10.1080/14786419.2014.938336
Kubes J, Skalicky M, Hejnak V et al (2018) The first genistin absorption screening into vacuoles of Trifolium pratense L. Plant Soil Environ 64:290–296. https://doi.org/10.17221/134/2018-PSE
Kuiper GGJM, Lemmen JG, Carlsson B et al (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology. https://doi.org/10.1210/endo.139.10.6216
Marinova K, Pourcel L, Weder B et al (2007) The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 19:2023–2038. https://doi.org/10.1105/tpc.106.046029
Matsouka I, Beri D, Chinou I et al (2011) Metals and selenium induce medicarpin accumulation and excretion from the roots of fenugreek seedlings: a potential detoxification mechanism. Plant Soil 343:235–245. https://doi.org/10.1007/s11104-010-0714-6
Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15:523–530
Mierziak J, Kostyn K, Kulma A (2014) Flavonoids as important molecules of plant interactions with the environment. Molecules 19:16240–16265. https://doi.org/10.3390/molecules191016240
Mithöfer A, Schulze B, Boland W (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett 566:1–5. https://doi.org/10.1016/j.febslet.2004.04.011
Namdeo AG (2007) Plant Cell elicitation for production of secondary metabolites: a review. Pharmacogn Rev 1:69–79
North P, Post RL (1984) Inhibition of (Na,K)-ATPase by tetravalent vanadium. J Biol Chem 259:4971–4978
O’Neill SD, Spanswick RM (1984) Effects of vanadate on the plasma membrane ATPase of red beet and corn. Plant Physiol 75:586–591. https://doi.org/10.1104/pp.75.3.586
Palazón J, Cusidó RM, Bonfill M et al (2003) Elicitation of different Panax ginseng transformed root phenotypes for an improved ginsenoside production. Plant Physiol Biochem 41:1019–1025. https://doi.org/10.1016/j.plaphy.2003.09.002
Panichev N, Mandiwana K, Moema D et al (2006) Distribution of vanadium (V) species between soil and plants in the vicinity of vanadium mine. J Hazard Mater 137:649–653. https://doi.org/10.1016/j.jhazmat.2006.03.006
Pawlak-Sprada S, Arasimowicz-Jelonek M, Podgórska M, Deckert J (2011a) Activation of phenylpropanoid pathway in legume plants exposed to heavy metals. Part I. Effects of cadmium and lead on phenylalanine ammonia-lyase gene expression, enzyme activity and lignin content. Acta Biochim Pol 58:211–216
Pawlak-Sprada S, Stobiecki M, Deckert J (2011b) Activation of phenylpropanoid pathway in legume plants exposed to heavy metals. Part II. Profiling of isoflavonoids and their glycoconjugates induced in roots of lupine (Lupinus luteus) seedlings treated with cadmium and lead. Acta Biochim Pol 58:217–223
Payen L, Delugin L, Courtois A et al (2001) The sulphonylurea glibenclamide inhibits multidrug resistance protein (MRP1) activity in human lung cancer cells. Br J Pharmacol 132:778–784. https://doi.org/10.1038/sj.bjp.0703863
Pessoa JC, Etcheverry S, Gambino D (2015) Vanadium compounds in medicine. Coord Chem Rev 301–302:24–48. https://doi.org/10.1016/j.ccr.2014.12.002
Potschka H, Baltes S, Löscher W (2004) Inhibition of multidrug transporters by verapamil or probenecid does not alter blood-brain barrier penetration of levetiracetam in rats. Epilepsy Res 58:85–91. https://doi.org/10.1016/j.eplepsyres.2003.12.007
Prieto D, Corchete P (2014) Transport of flavonolignans to the culture medium of elicited cell suspensions of Silybum marianum. J Plant Physiol 171:63–68. https://doi.org/10.1016/j.jplph.2013.10.005
Prochazkova D, Bousova I, Wilhelmova N (2011) Antioxidant and prooxidant properties of flavonoids. Fitoterapia 82:513–523. https://doi.org/10.1016/j.fitote.2011.01.018
Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375. https://doi.org/10.1146/annurev.arplant.57.032905.105406
Sabudak T, Guler N (2009) Trifolium L.—a review on its phytochemical and pharmacological profile. Phyther Res 23:439–446. https://doi.org/10.1002/ptr.2709
Saito K, Yonekura-Sakakibara K, Nakabayashi R et al (2013) The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. Plant Physiol Biochem 72:21–34. https://doi.org/10.1016/j.plaphy.2013.02.001
Sánchez T, Martín S, Saco D (2014) Some responses of two Nicotiana tabacum L. cultivars exposed to vanadium. J Plant Nutr 37:777–784. https://doi.org/10.1080/01904167.2013.873456
Searle BM, Higashino H, Khalil F et al (1983) Vanadate effect on the Na,K-ATPase and the Na–K pump in in vitro-grown rat vascular smooth muscle cells. Circ Res 53:186–191. https://doi.org/10.1161/01.RES.53.2.186
Selvaraj S, Krishnaswamy S, Devashya V et al (2015) Influence of membrane lipid composition on flavonoid–membrane interactions: implications on their biological activity. Prog Lipid Res 58:1–13. https://doi.org/10.1016/j.plipres.2014.11.002
Shi X, Dalal NS (1990) NADPH-dependent flavoenzymes catalyze one electron reduction of metal ions and molecular oxygen and generate hydroxyl radicals. FEBS Lett 276:189–191. https://doi.org/10.1016/0014-5793(90)80539-U
Shi X, Jiang H, Mao Y et al (1996) Vanadium (IV)-mediated free radical generation and related 2′-deoxyguanosine hydroxylation and DNA damage. Toxicology 106:27–38. https://doi.org/10.1016/0300-483x(95)03151-5
Shoji T, Inai K, Yazaki Y et al (2008) Multidrug and toxic compound extrusion-type transporters implicated in vacuolar sequestration of nicotine in tobacco roots. Plant Physiol 149:708–718. https://doi.org/10.1104/pp.108.132811
Sirikantaramas S, Sudo H, Asano T et al (2007) Transport of camptothecin in hairy roots of Ophiorrhiza pumila. Phytochemistry 68:2881–2886. https://doi.org/10.1016/j.phytochem.2007.08.028
Sivesind E, Seguin P (2006) Effects of foliar application of elicitors on red clover isoflavone content. J Agron Crop Sci 192:50–54. https://doi.org/10.1111/j.1439-037X.2006.00191.x
Skalicky M, Kubes J, Hejnak V et al (2018) Isoflavones production and possible mechanism of their exudation in Genista tinctoria L. suspension culture after treatment with vanadium compounds. Molecules 23:1619. https://doi.org/10.3390/molecules23071619
Smetanska I (2008) Production of secondary metabolites using plant cell cultures. Adv Biochem Eng Biotechnol 111:187–228. https://doi.org/10.1007/10_2008_103
Steffens M, Ettl F, Kranz D, Kindl H (1989) Vanadate mimics effects of fungal cell wall in eliciting gene activation in plant cell cultures. Planta 177:160–168. https://doi.org/10.1007/BF00392804
Sugiyama A, Shitan N, Yazaki K (2007) Involvement of a soybean ATP-binding cassette-type transporter in the secretion of genistein, a signal flavonoid in legume-rhizobium symbiosis. Plant Physiol 144:2000–2008. https://doi.org/10.1104/pp.107.096727
Takanashi K, Shitan N, Yazaki K (2014) The multidrug and toxic compound extrusion (MATE) family in plants. Plant Biotechnol 31:417–430. https://doi.org/10.5511/plantbiotechnology.14.0904a
Usui T (2006) Pharmaceutical prospects of phytoestrogens. Endocr J 53:7–20. https://doi.org/10.1507/endocrj.53.7
Villegas M, Sommarin M, Brodelius PE (2000) Effects of sodium orthovanadate on benzophenanthridine alkaloid formation and distribution in cell suspension cultures of Eschscholtzia californica. Plant Physiol Biochem 38:233–241. https://doi.org/10.1016/S0981-9428(00)00736-1
Wigler PW (1996) Cellular drug efflux and reversal therapy of cancer. J Bioenerg Biomembr 28:279–284. https://doi.org/10.1007/BF02110701
Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223. https://doi.org/10.1016/S1369-5266(02)00256-X
Yazaki K, Sugiyama A, Morita M, Shitan N (2008) Secondary transport as an efficient membrane transport mechanism for plant secondary metabolites. Phytochem Rev 7:513–524. https://doi.org/10.1007/s11101-007-9079-8
Ye Y, Ding Y, Jiang Q et al (2017) The role of receptor-like protein kinases (RLKs) in abiotic stress response in plants. Plant Cell Rep 36:235–242. https://doi.org/10.1007/s00299-016-2084-x
Zhao J (2015) Flavonoid transport mechanisms: how to go, and with whom. Trends Plant Sci 20:576–585. https://doi.org/10.1016/j.tplants.2015.06.007
Zhao J, Dixon RA (2009) MATE transporters facilitate vacuolar uptake of epicatechin 3′-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell Online 21:2323–2340. https://doi.org/10.1105/tpc.109.067819
Zhao J, Dixon RA (2010) The ‘ins’ and ‘outs’ of flavonoid transport. Trends Plant Sci 15:72–80. https://doi.org/10.1016/j.tplants.2009.11.006
Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333. https://doi.org/10.1016/j.biotechadv.2005.01.003
Acknowledgements
We would like to thank Dr. Marie Kasparova (Department of Pharmacognosy, Charles University in Prague) who provided the red clover callus culture. Miroslava Karlova, Adela Kohoutkova and Marketa Simunkova also helped with the technical background.
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This research was supported by the Ministry of Education, Youth and Sports of the Czech Republic, Projects No. SVV 260 416 and Project S grant.
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Kubes, J., Skalicky, M., Tumova, L. et al. Vanadium elicitation of Trifolium pratense L. cell culture and possible pathways of produced isoflavones transport across the plasma membrane. Plant Cell Rep 38, 657–671 (2019). https://doi.org/10.1007/s00299-019-02397-y
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DOI: https://doi.org/10.1007/s00299-019-02397-y