Pharmaceuticals belong to pseudo-persistent pollutants because of constant entry into the environment and hazardous potential for non-target organisms, including plants, in which they can influence biochemical and physiological processes. Detailed analysis of results obtained by microscopic observations using fluorescent dyes (berberine hemisulphate, Fluorol Yellow 088), detection of phytohormone levels (radioimmunoassay, enzyme-linked immune sorbent assay) and thermogravimetric analysis of lignin content proved that the drug naproxen (NPX) can stimulate the formation of root structural barriers. In the primary root of plants treated with 0.5, 1, and 10 mg/L NPX, earlier Casparian strip formation and development of the whole endodermis circle closer to its apex were found after five days of cultivation (by 9-20% as compared to control) and after ten days from 0.1 mg/L NPX (by 8-63%). Suberin lamellae (SL) were deposited in endodermal cells significantly closer to the apex under 10 mg/L NPX by up to 75%. Structural barrier formation under NPX treatment can be influenced indirectly by auxin-supported cell division and differentiation caused by its eight-times higher level under 10 mg/L NPX and directly by stimulated SL deposition induced by abscisic acid (higher from 0.5 mg/L NPX), as proved by the higher proportion of cells with SL in the primary root base (by 8-44%). The earlier modification of endodermis in plant roots can help to limit the drug transfer and maintain the homeostasis of the plant.

Department of Plant Physiology Faculty of Natural Science Comenius University in Bratislava Mlynská dolina B2 842 15 Bratislava Slovakia

Institute of Plant Biology Faculty of Agronomy Mendel University Brno Zemědělská 1 613 00 Brno Czech Republic

Laboratory of Metabolomics and Isotope Analyses Global Change Research Institute Czech Academy of Sciences Bělidla 986 4a 603 00 Brno Czech Republic

Section of Experimental Plant Biology Department of Experimental Biology Faculty of Science Masaryk University Brno Kotlářská 2 611 37 Brno Czech Republic

Zobrazit více v PubMed

Andersen TG, Barberon M, Geldner N (2015) Suberization - the second life of an endodermal cell. Curr Opin Plant Biol 28:9–15. https://doi.org/10.1016/j.pbi.2015.08.004 DOI

Armand T, Cullen M, Boiziot F, Li L, Fricke W (2019) Cortex cell hydraulic conductivity, endodermal apoplastic barriers and root hydraulics change in barley (Hordeum vulgare L.) in response to a low supply of N and P. Ann Bot-London 124(6):1091–1107. https://doi.org/10.1093/aob/mcz113 DOI

Barberon M, Vermeer JEM, De Bellis D, Wang P, Naseer S, Andersen TG, Humbel BM, Nawrath C, Takano J, Salt DE et al. (2016) Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164(3):447–459. https://doi.org/10.1016/j.cell.2015.12.021 DOI

Barrieu P, Simonneau T (2000) The monoclonal antibody MAC 252 does not react with the (-) enantiomer of abscisic acid. J Exp Bot 51(343):305–307. https://doi.org/10.1093/jexbot/51.343.305 DOI

Bártíková H, Podlipná R, Skálová L (2016) Veterinary drugs in the environment and their toxicity to plants. Chemosphere 144:2290–2301. https://doi.org/10.1016/j.chemosphere.2015.10.137 DOI

Bellver-Domingo A, Fuentes R, Hernandez-Sancho F (2017) Shadow prices of emerging pollutants in wastewater treatment plants: quantification of environmental externalities. J Environ Manag 203:439–447. https://doi.org/10.1016/j.jenvman.2017.08.025 DOI

Bo LL, Feng L, Fu JT, Li XG, Li P, Zhang YH (2015) The fate of typical pharmaceuticals in wastewater treatment plants of Xi’an city in China. J Environ Chem Eng 3(3):2203–2211. https://doi.org/10.1016/j.jece.2015.08.001 DOI

Brundrett MC, Enstone DE, Peterson CA (1988) A berberine-aniline blue fluorescent staining procedure for suberin, lignin, and callose in plant tissue. Protoplasma 146(2-3):133–142. https://doi.org/10.1007/BF01405922 DOI

Brundrett MC, Kendrick B, Peterson CA (1991) Efficient lipid staining in plant material with Sudan Red 7B or Fluoral Yellow 088 in polyethylene glycol-glycerol. Biotech Histochem 66(3):111–116. https://doi.org/10.3109/10520299109110562 DOI

Carrier M, Loppinet-Serani A, Denux D, Lasnier JM, Ham-Pichavant F, Cansell F, Aymonier C (2011) Thermogravimetric analysis as a new method to determine the lignocellulosic composition of biomass. Biomass Bioenerg 35(1):298–307. https://doi.org/10.1016/j.biombioe.2010.08.067 DOI

Caspary R (1865) Bemerkungen über die Schutzscheide und die Bildung des Stammes und der Wurzel. Jahrbücher Für Wissenschaftliche Botanik 4:101–124

Cheng H, Inyang A, Li CD, Fei J, Zhou YW, Wang YS (2020) Salt tolerance and exclusion in the mangrove plant Avicennia marina in relation to root apoplastic barriers. Ecotoxicology 26(6):676–683. https://doi.org/10.1007/s10646-020-02203-6 DOI

Conaghan PG (2012) A turbulent decade for NSAIDs: update on current concepts of classification, epidemiology, comparative efficacy, and toxicity. Rheumat Int 32(6):1491–1502. https://doi.org/10.1007/s00296-011-2263-6 DOI

Cohen JD (1984) Convenient apparatus for the generation of small amounts of diazomethane. J Chromatogr 303(1):193–196. https://doi.org/10.1016/S0021-9673(01)96061-3 DOI

Creelman RA, Mason HS, Bensen RJ, Boyer JS, Mullet JE (1990) Water deficit and abscisic acid cause differential inhibition of shoot versus root growth in soybean seedlings: Analysis of growth, sugar accumulation, and gene expression. Plant Physiol 92(1):205–214. https://doi.org/10.1104/pp.92.1.205 DOI

Dampanaboina L, Yuan N, Mendu V (2021) Estimation of plant biomass lignin content using thioglycolic acid (TGA). J Vis Exp 173:e62055. https://doi.org/10.3791/62055 DOI

Duan L, Dietrich D, Ng CH, Chan PMY, Bhalerao R, Bennett MJ, Dinneny JR (2013) Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell 25(1):324–341. https://doi.org/10.1105/tpc.112.107227 DOI

Eder J, Rovenská J, Kutáček M, Čermák V (1988) HPLC analysis of indoles in Agrobacterium and transformed tobacco cells. In: Kutáček M, Bandurski RS, Krekule J (Eds.) Physiology and biochemistry of auxins in plants. Academia Praha and SPB Acad, Hague, p 389–390

Enders TA, Strader LC (2015) Auxin activity: Past, present, and future. Am J Bot 102(2):180–196. https://doi.org/10.3732/ajb.1400285 DOI

Enstone DE, Peterson CA, Ma FS (2003) Root endodermis and exodermis: Structure, function, and responses to the environment. J Plant Growth Regul 21(4):335–351. https://doi.org/10.1007/s00344-003-0002-2 DOI

Friero I, Alarcón MV, Gordillo L, Salguero J (2022) Abscisic acid is involved in several processes associated with root system architecture in maize. Acta Physiol Plant 44:28. https://doi.org/10.1007/s11738-022-03360-3 DOI

Geldner N (2013) The Endodermis. Annu Rev Plant Biol 64:531–558. https://doi.org/10.1146/annurev-arplant-050312-120050 DOI

Ghetti P, Ricca L, Angelini L (1996) Thermal analysis of biomass and corresponding pyrolysis products. Fuel 75(5):565–73. https://doi.org/10.1016/0016-2361(95)00296-0 DOI

Guo D, Liang J, Li L (2009) Abscisic acid (ABA) inhibition of lateral root formation involves endogenous ABA biosynthesis in Arachis hypogaea L. Plant Growth Regul 58(2):173–179. https://doi.org/10.1007/s10725-009-9365-0 DOI

Hong JH, Seah SW, Xu J (2013) The root of ABA action in environmental stress response. Plant Cell Rep 32(7):971–983. https://doi.org/10.1007/s00299-013-1439-9 DOI

Huang L, Li WC, Tam NFY, Ye Z (2019) Effects of root morphology and anatomy on cadmium uptake and translocation in rice (Oryza sativa L.). J Environ Sci 75:296–306. https://doi.org/10.1016/j.jes.2018.04.005 DOI

Kaashyap M, Ford R, Kudapa H, Jain M, Edwards D, Varshney R, Mantri N (2018) Differential regulation of genes involved in root morphogenesis and cell wall modification is associated with salinity tolerance in chickpea. Sci Rep-UK 8:4855. https://doi.org/10.1038/s41598-018-23116-9 DOI

Karahara I, Ikeda A, Kondo T, Uetake Y (2004) Development of the Casparian strip in primary roots of maize under salt stress. Planta 219(1):41–47. https://doi.org/10.1007/s00425-004-1208-7 DOI

Kibuye FA, Gall HE, Elkin KR, Ayers B, Veith TL, Miller M, Jacob S, Hayden KR, Watson JE, Elliott HA (2019) Fate of pharmaceuticals in a spray-irrigation system: From wastewater to groundwater. Sci Total Environ 654:197–208. https://doi.org/10.1016/j.scitotenv.2018.10.442 DOI

Kosma DK, Murmu J, Razeq FM, Santos P, Bourgault R, Molina I, Rowland O (2014) AtMYB41 activates ectopic suberin synthesis and assembly in multiple plant species and cell types. Plant J 80:216–229. https://doi.org/10.1111/tpj.12624 DOI

Kreszies T, Shellakkutti N, Osthoff A, Yu P, Baldauf JA, Zeisler-Diehl VV, Ranathunge K, Hochholdinger F, Schreiber L (2019) Osmotic stress enhances suberization of apoplastic barriers in barley seminal roots: analysis of chemical, transcriptomic and physiological responses. New Phytol 221:180–194. https://doi.org/10.1111/nph.1535 DOI

Kummerová M, Zezulka Š, Babula P, Váňová L (2013) Root response in Pisum sativum and Zea mays under fluoranthene stress: Morphological and anatomical traits. Chemosphere 90:665–673. https://doi.org/10.1016/j.chemosphere.2012.09.047 DOI

Kummerová M, Zezulka Š, Babula P, Tříska J (2016) Possible ecological risk of two pharmaceuticals diclofenac and paracetamol demonstrated on a model plant Lemna minor. J Hazard Mater 302:351–361. https://doi.org/10.1016/j.jhazmat.2015.09.057 DOI

Kuromori T, Seo M, Shinozaki K (2018) ABA transport and plant water stress responses. Trends Plant Sci 23(6):513–522. https://doi.org/10.1016/j.tplants.2018.04.001 DOI

Landa P, Přerostová S, Langhansová L, Maršík P, Vaňková R, Vaněk T (2018) Transcriptomic response of Arabidopsis thaliana roots to naproxen and praziquantel. Ecotox Environ Safe 166:301–310. https://doi.org/10.1016/j.ecoenv.2018.09.081 DOI

Li R, Tan H, Zhu Y, Zhang Y (2017) The retention and distribution of parent, alkylated, and N/O/S-containing polycyclic aromatic hydrocarbons on the epidermal tissue of mangrove seedlings. Environ Pollut 226:135–142. https://doi.org/10.1016/j.envpol.2017.04.025 DOI

Li WC (2014) Occurrence, sources, and fate of pharmaceuticals in aquatic environment and soil. Environ Pollut 187:193–201. https://doi.org/10.1016/j.envpol.2014.01.015 DOI

López-Pacheco IY, Silva-Núñez A, Salinas-Salazar C, Arévalo-Gallegos A, Lizarazo-Holguin LA, Barceló D, Iqbal HMN, Parra-Saldívar R (2019) Anthropogenic contaminants of high concern: Existence in water resources and their adverse effects. Sci Total Environ 690:1068–1088. https://doi.org/10.1016/j.scitotenv.2019.07.052 DOI

Lux A, Martinka M, Vaculík M, White PJ (2011a) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62(1):21–37. https://doi.org/10.1093/jxb/erq281 DOI

Lux A, Vaculík M, Martinka M, Lišková D, Kulkarni MJ, Stirk W, Van Staden J (2011b) Cadmium induces hypodermal periderm formation in the roots of the monocotyledonous medicinal plant Merwilla plumbea. Ann Bot-London 107(2):285–292. https://doi.org/10.1093/aob/mcq240 DOI

Lühr C, Pecenka R (2020) Development of a model for the fast analysis of polymer mixtures based on cellulose, hemicellulose (xylan), lignin using thermogravimetric analysis and application of the model to poplar wood. Fuel 277:118169. https://doi.org/10.1016/j.fuel.2020.118169 DOI

Margenat A, Matamoros V, Díez S, Cañameras N, Comas J, Bayona JM (2017) Occurrence of chemical contaminants in peri-urban agricultural irrigation waters and assessment of their phytotoxicity and crop productivity. Sci Total Environ 599:1140–1148. https://doi.org/10.1016/j.scitotenv.2017.05.025 DOI

Martinka M, Vaculík M, Lux A (2014) Plant Cell Responses to Cadmium and Zinc. In: Nick P, Opatrný Z (Eds.) Applied Plant Cell Biology: Cellular Tools and Approaches for Plant Biotechnology. Plant Cell Monographs 22. Springer-Verlag, Berlin Heidelberg, p 209–246. https://doi.org/10.1007/978-3-642-41787-0_7 DOI

McKendry P (2002) Energy production from biomass (Part 1): Overview of biomass. Bioresource Technol 83(1):37–46. https://doi.org/10.1016/S0960-8524(01)00118-3 DOI

Namyslov J, Bauriedlová Z, Janoušková J, Soukup A, Tylová E (2020) Exodermis and endodermis respond to nutrient deficiency in nutrient-specific and localized manner. Plants-Basel 9(2):201. https://doi.org/10.3390/plants9020201 DOI

Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. CSH Perspect Biol 2(6):a001537. https://doi.org/10.1101/cshperspect.a001537 DOI

Pawlak-Sprada S, Arasimowicz-Jelonek M, Podgórska M, Decker J (2011) 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(2):211–216 DOI

Pino MR, Muñiz S, Val J, Navarro E (2016) Phytotoxicity of 15 common pharmaceuticals on the germination of Lactuca sativa and photosynthesis of Chlamydomonas reinhardtii. Environ Sci Pollut Res 23(22):22530–22541. https://doi.org/10.1007/s11356-016-7446-y DOI

Piotrowicz-Cieślak AI, Adomas B, Nałęcz-Jawecki G (2012) Phytotoxicity of sulfonamide soil pollutants to legume plant species. Fresen Environ Bull 21(5a):1310–1314

Quarrie SA, Whitford PN, Appleford NEJ, Wang TL, Cook SK, Henson IE, Loveys BR (1988) A monoclonal antibody to (S)-abscisic acid: its characterisation and use in a radioimmunoassay for measuring abscisic acid in crude extracts of cereal and lupin leaves. Planta 173(3):330–339. https://doi.org/10.1007/BF00401020 DOI

Rede D, Santos LHMLM, Ramos S, Oliva-Teles F, Antão C, Sousa SR, Delerue-Matos C (2016) Ecotoxicological impact of two soil remediation treatments in Lactuca sativa seeds. Chemosphere 159:193–198. https://doi.org/10.1016/j.chemosphere.2016.06.002 DOI

Reid PH, York Jr ET (1958) Effect of nutrient deficiencies on growth and fruiting characteristics of peanuts in sand cultures. Agron J 50(2):63–67. https://doi.org/10.2134/agronj1958.00021962005000020002x DOI

Seo DH, Jeong H, Do Choi Y, Jang G (2021) Auxin controls the division of root endodermal cells. Plant Physiol 187(3):1577–1586. https://doi.org/10.1093/plphys/kiab341 DOI

Stoláriková M, Vaculík M, Lux A, Di Baccio D, Minnocci A, Andreucci A, Sebastiani L (2012) Anatomical differences of poplar (Populus × euramericana clone I-214) roots exposed to zinc excess. Biologia 67(3):483–489. https://doi.org/10.2478/s11756-012-0039-4 DOI

Svobodníková L, Kummerová M, Zezulka Š, Babula P, Sendecká K (2020) Root response in Pisum sativum under naproxen stress: Morpho-anatomical, cytological, and biochemical traits. Chemosphere 258:127411. https://doi.org/10.1016/j.chemosphere.2020.127411 DOI

Šípošová K, Kollárová K, Lišková D, Vivodová Z (2019) The effects of IBA on the composition of maize root cell walls. J Plant Physiol 239:10–17. https://doi.org/10.1016/j.jplph.2019.04.004 DOI

Tao Q, Jupa R, Luo J, Lux A, Kováč J, Wen Y, Zhou Y, Jan J, Liang Y, Li T (2017) The apoplasmic pathway via the root apex and lateral roots contributes to Cd hyperaccumulation in the hyperaccumulator Sedum alfredii. J Exp Bot 68(3):739–751. https://doi.org/10.1093/jxb/erw453 DOI

Tylová E, Pecková E, Blascheová Z, Soukup A (2017) Casparian bands and suberin lamellae in exodermis of lateral roots: an important trait of roots system response to abiotic stress factors. Ann Bot-London 120(1):71–85. https://doi.org/10.1093/aob/mcx047 DOI

Vaculík M, Lux A, Luxová M, Tanimoto E, Lichtscheidl I (2009) Silicon mitigates cadmium inhibitory effects in young maize plants. Environ Exp Bot 67(1):52–58. https://doi.org/10.1016/j.envexpbot.2009.06.012 DOI

Vitha S, Baluška F, Jasik J, Volkmann D, Barlow PW (2000) Steedman’s wax for F-Actin visualization. In: Staiger CJ, Baluška F, Volkmann D, Barlow PW (Eds.) Actin: A Dynamic Framework for Multiple Plant Cell Functions. Developments in Plant and Soil Sciences, Vol. 89. Springer, Dordrecht, https://doi.org/10.1007/978-94-015-9460-8_35 DOI

Wang X, Sun C, Gao S, Wang L, Shuokui H (2001) Validation of germination rate and root elongation as indicator to assess phytotoxicity with Cucumis sativus. Chemosphere 44(8):1711–1721. https://doi.org/10.1016/S0045-6535(00)00520-8 DOI

Wang C, Wang H, Li P, Li H, Xu C, Cohen H, Aharoni A, Wu S (2020) Developmental programs interact with abscisic acid to coordinate root suberization in Arabidopsis. Plant J 104(1):241–251. https://doi.org/10.1111/tpj.14920 DOI

Weiler EW, Jourdan PS, Conrad W (1981) Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid-phase enzyme immunoassay. Planta 153(6):561–571. https://doi.org/10.1007/BF00385542 DOI

Wild SR, Berrow ML, McGrath SP, Jones KC (1992) Polynuclear aromatic hydrocarbons in crops from long-term field experiments amended with sewage sludge. Environ Pollut 76(1):25–32. https://doi.org/10.1016/0269-7491(92)90113-O DOI

Yadav V, Molina I, Ranathunge K, Castillo IQ, Rothstein SJ, Reed JW (2014) ABCG transporters are required for suberin and pollen wall extracellular barriers in Arabidopsis. Plant Cell 26(9):3569–3588. https://doi.org/10.1105/tpc.114.129049 DOI

Yuan HM, Liu WC, Jin Y, Lu YT (2013) Role of ROS and auxin in plant response to metal-mediated stress. Plant Signaling & Behavior 8(7):e24671. https://doi.org/10.1093/pcp/pct030 DOI

Zezulka Š, Kummerová M, Babula P, Hájková M, Oravec M (2019) Sensitivity of physiological and biochemical endpoints in early ontogenetic stages of crops under diclofenac and paracetamol treatments. Environ Sci Pollut R 26(4):3965–3979. https://doi.org/10.1007/s11356-018-3930-x DOI