The effect of bisphenol A on growth, pigment composition and photosystem II activity of Arabidopsis thaliana

  • Michał Rąpała Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology Jagiellonian University
  • Bartosz Plucinski Bartosz Plucinski, M.Sc., Ph.D. candidate, Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University
  • Paweł Jedynak Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University

Abstract

Bisphenol A (BPA) is a widely used chemical, that can potentially be toxic to plants. In this study we examined the toxicity of 5-50 mg/l of BPA on Arabidopsis thaliana. Additionally, the effects of 0.5-5 mg/l of BPA were examined after four weeks of development.

                BPA had no effect on the germination rate and the chlorophyll a/b ratio. The chlorophyll a and carotenoid content was significantly elevated in seedlings treated with 5 mg/l of BPA.

In 4-week-old plants there was no change in the chlorophyll and carotenoid content and photosynthetic parameters (Fv/Fm, Fv/F0 and PI) were unaffected, which suggests no photoinhibition. No oxidative stress symptoms were observed. BPA significantly decreased leaf protein content. A low concentration of BPA seems to have no significant effect on A. thaliana flowering, but further investigation is needed. The results obtained indicate that a low concentration of BPA has no negative effect on the growth and development of A. thaliana.

Author Biographies

Michał Rąpała, Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology Jagiellonian University

Michal Rapala, Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University

Bartosz Plucinski, Bartosz Plucinski, M.Sc., Ph.D. candidate, Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University
Bartosz Plucinski, M.Sc., Ph.D. candidate, Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University
Paweł Jedynak, Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University

Pawel Jedynak, M.Sc., Ph.D. candidate, Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University

References

Azymi S, Sofalian O, Jahanbakhsh G, Khomari S (2012) Effect of chilling stress on Soluble Protein, sugar and Prolin accumulation in cotton (Gossypium hirsutum L.) genotypes. Intl J Agri Crop Sci 4: 825–830.

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254. http://dx.doi.org/10.1016/0003–2697(76)90527–3

Burridge E (2003) Bisphenol A: product profile. European Chemical News 17: 14–20.

ChemSpider, http://www.chemspider.com/Chemical-Structure.1906.html, accessed 13.04.2017

Ding L, Wang KJ, Jiang GM, Biswas DK, Xu H, Li LF, Li YH (2005). Effects of Nitrogen Deficiency on Photosynthetic Traits of Maize Hybrids Released in Different Years. Annals of Botany 96: 925–930. http://doi.org/10.1093/aob/mci244

Dogan M, Yumrutas O, Saygideger S, Korkunc M, Gulnaz O, Sokmen A (2010) Effects of bisphenol A and tetrabromobisphenol A on chickpea roots in germination stage. Am-Eurasian J Agric Environ Sci 9: 186–192

Dogan M, Korkunc M, Yumrutas O (2012) Effects of bisphenol A and tetrabromobisphenol A on bread and durum wheat varieties. Ekoloji 21: 114–122. 10.5053/ekoloji.2012.8513

Ferrara G, Loffredo E, Senesi N (2006) Phytotoxic, clastogenic and bioaccumulation effects of the environmental endocrine disruptor bisphenol A in various crops grown hydroponically. Planta 223: 910–916. 910. 10.1007/s00425-005-0147-2

Ferrario-Méry S, Valadier M-H, Foyer CH (1998). Overexpression of Nitrate Reductase in Tobacco Delays Drought-Induced Decreases in Nitrate Reductase Activity and mRNA. Plant Physiology 117: 293–302.

Frejd D, Dunaway K, Hill J, van Maanen J, Carlson C (2016) The Genomic and Morphological Effects of Bisphenol A on Arabidopsis thaliana. PLoSOne 11: e0163028. 10.1371/journal.pone.0163028

Fromme H, Küchler T, Otto T, Pilz K, Müller J, Wenzel A (2002) Occurrence of phthalates and bisphenol A and F in the environment. Water Res 36: 1429–1438. http://dx.doi.org/10.1016/S0043–1354(01)00367–0

Gattullo CE, Bährs H, Steinberg CE, Loffredo E (2012) Removal of bisphenol A by the freshwater green alga Monoraphidiumbraunii and the role of natural organic matter. Sci Total Environ 416: 501–506. 10.1016/j.scitotenv.2011.11.033.

Gonçalves JF, Becker AG, Cargnelutti D, Tabaldi LA, Pereira LB, Battisti V, Spanevello RM, Morsch VM, Nicoloso FT, Schetinger MRC (2007) Cadmium toxicity causes oxidative stress and induces response of the antioxidant system in cucumber seedlings. Brazilian Journal of Plant Physiology 19: 223–232. https://dx.doi.org/10.1590/S1677-04202007000300006

Goodson A, Summerfield W, Cooper I (2002) Survey of bisphenol A and bisphenol F in canned foods. Food Addi Contam 19: 796–802. 10.1080/02652030210146837

Hodges, D, DeLong, J, Forney, C, Prange R (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207: 604–611. 10.1007/s004250050524

Hu H, Wang L, Wang Q, Jiao L, Hua W, Zhou Q, Huang X (2014) Photosynthesis, chlorophyll fluorescence characteristics, and chlorophyll content of soybean seedlings under combined stress of bisphenol A and cadmium. Environ Toxicol Chem 33: 2455–2462. 10.1002/etc.2720.

Janeczko A, Budziszewska B, Skoczowski A, Dybała M (2008) Specific binding sites for progesterone and 17β-estradiol in cells of Triticum aestivum L. Acta Biochimica Polonica 55: 707–711. 10.1.1.337.2839

Janeczko A, Skoczowski A (2005) Mammalian sex hormones in plants. Folia Histochem Cytobiol 43: 71–79.

Jiao L, Ding H, Wang L, Zhou Q, Huang X. (2017) Bisphenol A effects on the chlorophyll contents in soybean at different growth stages. Environmental Pollution 223: 426–434 http://dx.doi.org/10.1016/j.envpol.2017.01.042

Jiao L, Wang L, Qiu Z, Wang Q, Zhou Q, Huang X (2015) Effects of bisphenol A on chlorophyll synthesis in soybean seedlings. Environ Sci Pollut Res Int 22: 5877–5886. 10.1007/s11356-014-3764-0.

Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud, Dąbrowski P, Elsheery NI, Ferroni L, Guidi L, Hogewoning SW, Jajoo A, Misra AN, Nebauer SG, Pancaldi S, Penella C, Poli D, Pollastrini M, Romanowska-Duda ZB, Rutkowska B, Serôdio J, Suresh K, Szulc W, Tambussi E, Yanniccari M, Zivcak M (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res Nov 122: 121–158. 10.1007/s11120-014-0024-6.

Kitajima K, Hogan KP (2003) Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ 26: 857–865.

Kopcewicz J (1970a) Influence of estrogens on the flower formation in Cichorium intybus L. Naturwissenschaften 57: 136. http://dx.doi.org/10.1007/BF00600070

Kopcewicz J (1970b) Effect of estradiol-17beta, estrone and estriol on the endogenous auxins content in plants. Acta Soc Bot Pol 39: 339–346. 10.5586/asbp.1970.02610.5586/asbp.1970.026

Kumar A, Prasad MNV (2015) Lead–induced toxicity and interference in chlorophyll fluorescence in Talinum triangulare grown hydroponically. Photosynthetica 53: 66–71. 10.1007/s11099-015-0091-8

Lemaître T, Gaufichon L, Boutet-Mercey S, Christ A, Masclaux-Daubresse C (2008) Enzymatic and Metabolic Diagnostic of Nitrogen Deficiency in Arabidopsis thaliana Wassileskija Accession. Plant Cell Physiol 49: 1056–1065. https://doi.org/10.1093/pcp/pcn081

Lichtenthaler HK, (1987) Chlorophylls and carotenoids: pigments of photosynthetic membranes. Methods Enzymol 148: 350–382. http://dx.doi.org/10.1016/0076–6879(87)48036–1

Malec P, Yahalom A, Chamovitz DA (2002) Identification of a light–regulated protein kinase activity from seedlings of Arabidopsis thaliana. Photochem Photobiol 75: 178–183. 10.1562/0031-8655(2002)0750178IOALRP2.0.CO2

Maleva MG, Nekrasova GF, Malec P, Prasad MN, Strzałka K (2009) Ecophysiological tolerance of Elodea canadensis to nickel exposure. Chemosphere 77: 392–398. 10.1016/j.chemosphere.2009.07.024.

Mandich A, Bottero S, Benfenati E, Cevasco A, Erratico C, Maggioni S, Massari A, Pedemonte F, Vigano L (2007) In vivo exposure of carp to graded concentrations of bisphenol A. Gen Comp Endocrinol 153: 15–24. http://dx.doi.org/10.1016/j.ygcen.2007.01.004

Mate CJ, Hudson GS, von Caemmerer S, Evans J R, Andrews TJ (1993). Reduction of ribulose biphosphate carboxylase activase levels in tobacco (Nicotiana tabacum) by antisense RNA reduces ribulose biphosphate carboxylase carbamylation and impairs photosynthesis. Plant Physiology 102: 1119–1128.

Matsumura Y, Akahira-Moriya A, Sasaki-Mori M (2015) Bioremediation of bisphenol A polluted soil by Sphingomonas bisphenolicum AO1 and the microbial community existing in the soil. Biocontrol Sci 20: 35–42. 10.4265/bio.20.35.

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. J Exp Bot 51: 659–68.

Misra AN, Misra M, Singh R (2012) Chlorophyll fluorescence in plant biology. In Biophysics (Misra, AN, ed.), pp. 171–192. Rijeka, Croatia: InTech. 10.5772/1877

Molina AM, Lora AJ, Blanco A, Monterde JG, Ayala N, Moyano R (2013) Endocrine–active compound evaluation: qualitative and quantitative histomorphological assessment of zebrafish gonads after bisphenol A exposure. Ecotoxicol Environ Saf 88: 155–162. 10.1016/j.ecoenv.2012.11.010.

Muravyeva DA, Bubenchikova VN, Belikov V (1984) Spectrophotometric determination of the total anthocyanins amount in the flowers of cornflower blue. Pharmacy 36: 28–29.

Nakajima N, Ohshima Y, Serizawa S, Kouda T, Edmonds JS, Shiraishi F, Aono M, Kubo A, Tamaoki M, Saji H (2002) Processing of bisphenol A by plant tissues: Glucosylation by cultured BY-2 cells and glucosylation/translocation by plants of Nicotiana tabacum. Plant Cell Physiol 43: 1036–1042. https://doi.org/10.1093/pcp/pcf130

Neto AD, Prisco JT, Gomes-Filho E (2009) Changes in soluble amino-N, soluble proteins and free amino acids in leaves and roots of salt-stressed maize genotypes. Journal of Plant Interactions 4: 137–144. 10.1080/17429140902866954

Nielsen SS, Osuala CI, Brandt WE (1994) Early leaf harvest reduces yield but not protein concentration of cowpea seeds. Hort Science 29: 631–632.

Pan WJ, Xiong C, Wua QP, Liu JX, Liao HM, Chen W, Liu YS, Zheng L (2013) Effect of BPA on the germination, root development, seedling growth and leaf differentiation under different light conditions in Arabidopsis thaliana. Chemosphere 93: 2585–2592.

Pankovic D, Plesnic M, Arsenijevic-Maksimovic I, Petrovic N, Sakac Z, Kastori R (2000) Effects of Nitrogen Nutrition on Photosynthesis in Cd-treated Sunflower Plant. Annals of Botany 86: 841–847. doi:10.1006/anbo.2000.1250

Spreitzer RJ, Salvucci ME (2002) Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53: 449–75.

Qiu Z, Wang L, Zhou Q (2013) Effects of bisphenol A on growth, photosynthesis and chlorophyll fluorescence in above-ground organs of soybean seedlings. Chemosphere 90: 1274–1280. 10.1016/j.chemosphere.2012.09.085.

Quick WP, Schur U, Fichtner K, Schulze E-D, Roderme SR, Bogorad L, Stitti M (1991) The impact of decreased Rubisco on photosynthesis, growth, allocation and storage in tobacco plants which have been transformed with antisense rbcS. The Plant Journal 1: 51–58. 10.1111/j.1365-313X.1991.00051.x.

Ranciere F, Lyons JG, Loh VHY, Botton J, Galloway T, Wang T, Shaw JE, Magliano DJ (2015) Bisphenol A and the risk of cardiometabolic disorders: a systematic review with meta-analysis of the epidemiological evidence. Environ Health 14: 46. 10.1186/s12940-015-0036-5

Ren L, Jia Y, Ruth N, Shi Y, Wang J, Qiao C, Yan Y (2016) Biotransformations of bisphenols mediated by a novel Arthrobacter sp. strain YC-RL. Appl Microbiol Biotechnol 100: 1967–1976. 10.1007/s00253-015-7076-1.

Seachrist DD, Bonk KW, Ho SM, Prins GS, Soto AM, Keri RA (2016) A review of the carcinogenic potential of bisphenol A. Reprod Toxicol 59: 167–182. 10.1016/j.reprotox.2015.09.006.

Somm E, Schwitzgebel VM, Toulotte A, Cederroth CR, Combescure C, Nef S, Aubert ML, Hüppi PS (2009) Perinatal exposure to bisphenol a alters early adipogenesis in the rat. Environ Health Perspect 117: 1549–1555. 10.1289/ehp.11342.

Speranza A, Crosti P, Malerba M, Stocchi O, Scoccianti V (2011) The environmental endocrine disruptor, bisphenol A, affects germination, elicits stress response and alters steroid hormone production in kiwifruit pollen. Plant Biol (Stuttg) 13: 209–217. 10.1111/j.1438–8677.2010.00330.x.

Sun H, Wang LH, Zhou Q (2013) Effects of bisphenol A on growth and nitrogen nutrition of roots of soybean seedlings. Environ Toxicol Chem 32: 174–180.10.1002/etc.2042.

Tarapore P, Ying J, Ouyang B, Burke B, Bracken B, Ho SM (2014) Exposure to bisphenol A correlates with early-onset prostate cancer and promotes centrosome amplification and anchorage-independent growth in vitro. PLoS One 9: e90332. 10.1371/journal.pone.0090332.

Tian YS, Jin XF, Fu XY, Zhao W, Han HJ, Zhu B, Liu M, Yao QH (2014) Microarray analysis of differentially expressed gene responses to bisphenol A in Arabidopsis. J Toxicol Sci 39: 671–679.

Yamamoto T, Yasuhara A, Shiraishi H, Nakasugi O (2001) Bisphenol A in hazardous waste landfill leachates. Chemosphere 42: 415–418. http://dx.doi.org/10.1016/S0045-6535(00)00079-5

Zhang J, Wang L, Li M, Jiao L, Zhou Q, Huang X (2015) Effects of bisphenol A on chlorophyll fluorescence in five plants. Environ Sci Pollut Res Int 22: 17724–17732. 10.1007/s11356-015-5003-8.

Published
2017-07-27
Section
Articles