Abstract
Bisphenol A (BPA) is considered a contaminant of emerging concern and interferes with the normal activities of living organisms. The toxicity of BPA is evident in animals and terrestrial plants. However, the response of aquatic plants to low BPA concentrations is still unclear. In the present study, effects of varying BPA loadings (targeting at 0.01, 0.1, and 1 mg/L) on the growth and reproductive traits of the dioecious annual submerged macrophyte Vallisneria natans were assessed through a 5-month experiment. The results showed that BPA inhibited the elongation of V. natans leaves but resulted in an increase in leaf number and ramet number under the highest BPA loading treatment (targeting at 1 mg/L). In addition, detectable biochemical changes in the total carbon and soluble sugar contents were found, which both were significantly higher at the highest BPA loading treatment. However, the total biomass did not alter significantly after the BPA treatments, indicating that BPA did not induce direct toxic effects on the growth of V. natans. At the highest BPA loading treatment, female individuals of V. natans allocated less number for ramet than male ones, showing a clear sexual dimorphism. No significant differences between the five treatments were found for the flower or fruit traits, while the germination rate was significantly inhibited for the seeds collected from the highest BPA loading treatment. In conclusion, V. natans tolerated low concentrations of BPA by making a trade-off between ramet (leaf) number and leaf elongation, as well as modulating the total carbon and soluble sugar contents. However, serious consequence of decline in seed viability implied that the impact of BPA on plant reproduction were usually underestimated.
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Data sets in the current study are available from the corresponding authors upon reasonable request.
References
Alexander HC, Dill DC, Smith LW et al (1988) Bisphenol A: acute aquatic toxicity. Environ Toxicol Chem 7(1):19–26
Bhatnagar A, Anastopoulos I (2017) Adsorptive removal of bisphenol A (BPA) from aqueous solution: A review. Chemosphere 168:885–902. https://doi.org/10.1016/j.chemosphere.2016.10.121
Buysse JAN, Merckx R (1993) An improved colorimetric method to quantify sugar content of plant tissue. J Exp Bot 44:1627–1629
Cano-Nicolau J, Vaillant C, Pellegrini E et al (2016) Estrogenic effects of several BPA analogs in the developing zebrafish brain. Front Neurosci 10:112. https://doi.org/10.3389/fnins.2016.00112
Cao Y, Li W, Jeppesen E (2014) The response of two submerged macrophytes and periphyton to elevated temperatures in the presence and absence of snails: a microcosm approach. Hydrobiologia 738:49–59. https://doi.org/10.1007/s10750-014-1914-5
Careghini A, Mastorgio AF, Saponaro S, Sezenna E (2015) Bisphenol A, nonylphenols, benzophenones, and benzotriazoles in soils, groundwater, surface water, sediments, and food: a review. Environ Sci Pollut Res 22:5711–5741. https://doi.org/10.1007/s11356-014-3974-5
Cariati F, D’Uonno N, Borrillo F et al (2019) Bisphenol a: an emerging threat to male fertility. Reprod Biol Endocrinol 17(1):1–8. https://doi.org/10.1186/s12958-018-0447-6
Casals-Casas C, Desvergne B (2011) Endocrine disruptors: from endocrine to metabolic disruption. Annu Rev Physiol 73:135–162. https://doi.org/10.1146/annurev-physiol-012110-142200
Chou Q, Zhang W, Chen J et al (2022) Phenotypic responses of a submerged macrophyte (Vallisneria natans) to low light combined with water depth. Aquat Bot 176:103462. https://doi.org/10.1016/j.aquabot.2021.103462
Cousins IT, Staples CA, Klečka GM, Mackay D (2002) A multimedia assessment of the environmental fate of bisphenol A. Hum Ecol Risk Assess 8:1107–1135. https://doi.org/10.1080/1080-700291905846
Dou Y, Wang B, Chen L, Yin D (2013) Alleviating versus stimulating effects of bicarbonate on the growth of Vallisneria natans under ammonia stress. Environ Sci Pollut Res 20:5281–5288
Duby RS, Sing A (1999) Salinity induced accumulation of soluble sugars and salts the activity sugar metabolizing enzymes in rice plant. Biol Plantarum 42:233–239
Ebina J, Tsutsui T, Shirai T (1983) Simultaneous determination of total nitrogen and total phosphorus in water using peroxodisulfate oxidation. Water Res 17:1721–1726. https://doi.org/10.1016/0043-1354(83)90192-6
Foyer CH, Valadier M-H, Migge A, Becker TW (1998) Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. Plant Physiol 117:283–292
Garcia AB, Engler JDA, Iyer S et al (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol 115:159–169
Geens T, Goeyens L, Covaci A (2011) Are potential sources for human exposure to bisphenol-A overlooked? Int J Hyg Environ Heal 214:339–347. https://doi.org/10.1016/j.ijheh.2011.04.005
Greco M, Chiappetta A, Bruno L, Bitonti MB (2013) Sexual dimorphism in flowering plants. J Exp Bot 64:67–82. https://doi.org/10.1093/JXB/ERS308
Hercog K, Maisanaba S, Filipič M et al (2019) Genotoxic activity of bisphenol A and its analogues bisphenol S, bisphenol F and bisphenol AF and their mixtures in human hepatocellular carcinoma (HepG2) cells. Sci Total Environ 687:267–276. https://doi.org/10.1016/j.scitotenv.2019.05.486
Hing-Biu L, Peart TE (2000) Bisphenol A contamination in Canadian municipal and industrial wastewater and sludge samples. Water Qual Res J 35:283–298. https://doi.org/10.2166/WQRJ.2000.018
Huang W, Han S, Wang L, Li W (2022) Carbon and nitrogen metabolic regulation in freshwater plant Ottelia alismoides in response to carbon limitation: a metabolite perspective. Front Plant Sci 13:962622
Hultine KR, Grady KC, Wood TE et al (2016) Climate change perils for dioecious plant species. Nat Plants 2(8):1–8. https://doi.org/10.1038/NPLANTS.2016.109
Keri RA, Ho SM, Hunt PA et al (2007) An evaluation of evidence for the carcinogenic activity of bisphenol A. Reprod Toxicol 24(2):240–252. https://doi.org/10.1016/j.reprotox.2007.06.008
Khryanin VN (2002) Role of phytohormones in sex differentiation in plants. Russ J Plant Physl 49(4):545–551
Li X, Wang L, Shen F et al (2018) Impacts of exogenous pollutant bisphenol A on characteristics of soybeans. Ecotox Environ Safe 157:463–471. https://doi.org/10.1016/j.ecoenv.2018.04.013
Li Q, Tian X, Gu P et al (2022) Transcriptomic analysis reveals phytohormone and photosynthetic molecular mechanisms of a submerged macrophyte in response to microcystin-LR stress. Aquat toxicol 245:106119. https://doi.org/10.1016/j.aquatox.2022.106119
Liang J, Li Y, Xie P et al (2022) Dualistic effects of bisphenol A on growth, photosynthetic and oxidative stress of duckweed (Lemna minor). Environ Sci Pollut Res 29:87717–87729
Liu Q, Wang W, Zhang Y et al (2020) Bisphenol A regulates cytochrome P450 1B1 through miR-27b-3p and induces carp lymphocyte oxidative stress leading to apoptosis. Fish Shellfish Immun 102:489–498. https://doi.org/10.1016/j.fsi.2020.05.009
Lu C, Warchol KM, Callahan RA (2012) In situ replication of honey bee colony collapse disorder. Bull Insectology 65(1):99–106
Ma Y, Liu H, Wu J et al (2019) The adverse health effects of bisphenol A and related toxicity mechanisms. Environ Res 176:108575. https://doi.org/10.1016/j.envres.2019.108575
Malea P, Kokkinidi D, Kevrekidou A, Adamakis IDS (2020) Environmentally relevant bisphenol A concentrations effects on the seagrass Cymodocea nodosa different parts elongation: perceptive assessors of toxicity. Environ Sci Pollut Res 27:7267–7279. https://doi.org/10.1007/s11356-019-07443-6
McCready RM, Guggolz J, Silviera V et al (1950) Determination of starch and amylose in vegetables. Anal Chem 22:1156–1158
Michałowicz J (2014) Bisphenol A - Sources, toxicity and biotransformation. Environ Toxicol Phar 37:738–758. https://doi.org/10.1016/j.etap.2014.02.003
Naveira C, Rodrigues N, Santos FS et al (2021) Acute toxicity of bisphenol A (BPA) to tropical marine and estuarine species from different trophic groups. Environ Pollut 268:115911. https://doi.org/10.1016/j.envpol.2020.115911
Oehlmann J, Schulte-oehlmann U, Tillmann M, Markert B (2000) Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part I: bisphenol A and octylphenol as xeno-estrogens. Ecotoxicology 9(6):383–397
Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. J Exp Bot 54:539–547
Petrie B, Lopardo L, Proctor K et al (2019) Assessment of bisphenol-A in the urban water cycle. Sci Total Environ 650:900–907. https://doi.org/10.1016/j.scitotenv.2018.09.011
Plaxton WC (1996) The organization and regulation of plant glycolysis. Annu Rev Plant Biol 47:185–214
Puijalon S, Bouma TJ, Douady CJ et al (2011) Plant resistance to mechanical stress: evidence of an avoidance-tolerance trade-off. New Phytol 191:1141–1149. https://doi.org/10.1111/j.1469-8137.2011.03763.x
Richter CA, Birnbaum LS, Farabollini F et al (2007) In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 24:199–224. https://doi.org/10.1016/j.reprotox.2007.06.004
Robionek A, Banaś K, Chmara R, Szmeja J (2015) The avoidance strategy of environmental constraints by an aquatic plant Potamogeton alpinus in running waters. Ecol Evol 5:3327–3337. https://doi.org/10.1002/ece3.1598
Rosa M, Prado C, Podazza G et al (2009) Soluble sugars: metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4:388–393
Sarkar A, Gogoi N, Roy S (2022) Bisphenol‑A incite dose‑dependent dissimilitude in the growth pattern, physiology, oxidative status, and metabolite profile of Azolla filiculoides. Environ Sci Pollut Res: 1–20. https://doi.org/10.1007/s11356-022-22107-8
Seoane M, Cid Á, Esperanza M (2021) Toxicity of bisphenol A on marine microalgae: single- and multispecies bioassays based on equivalent initial cell biovolume. Sci Total Environ 767:144363. https://doi.org/10.1016/j.scitotenv.2020.144363
Shao H, Gontero B, Maberly SC et al (2017) Responses of Ottelia alismoides, an aquatic plant with three CCMs, to variable CO2 and light. J Exp Bot 68:3985–3995. https://doi.org/10.1093/jxb/erx064
Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Biol 51:49–81
Tayama S, Nakagawa Y, Tayama K (2008) Genotoxic effects of environmental estrogen-like compounds in CHO-K1 cells. Mutat Res - Gen Tox En 649:114–125. https://doi.org/10.1016/j.mrgentox.2007.08.006
USEPA (1997) Special report on environmental endocrine disruption: an effects assessment and analysis. EPA/630/R-96/012 (und im Internet unter www.epa.gov/endocrine)
Wang B, Song Z, Liu G et al (2010) Comparison of the extent of genetic variation of Vallisneria natans and its sympatric congener V. spinulosa in lakes of the middle–lower reaches of the Yangtze River. Aquat Bot 92:233–238. https://doi.org/10.1016/j.aquabot.2009.12.006
Wang S, Wang L, Hua W et al (2015) Effects of bisphenol A, an environmental endocrine disruptor, on the endogenous hormones of plants. Environ Sci Pollut Res 22:17653–17662. https://doi.org/10.1007/s11356-015-4972-y
Wu NC, Seebacher F (2020) Effect of the plastic pollutant bisphenol A on the biology of aquatic organisms: A meta-analysis. Glob Chang Biol 26:3821–3833. https://doi.org/10.1111/gcb.15127
Xiao C, Xing W, Liu G (2010) Seed germination of 14 wetland species in response to duration of cold-wet stratification and outdoor burial depth. Aquat Biol 11:169–177
Xiao C, Wang L, Zhou Q, Huang X (2020) Hazards of bisphenol A (BPA) exposure: a systematic review of plant toxicology studies. J Hazard Mater 384:121488. https://doi.org/10.1016/j.jhazmat.2019.121488
Yamamoto T, Yasuhara A, Shiraishi H, Nakasugi O (2001) Bisphenol A in hazardous waste landfill leachates. Chemosphere 42:415–418. https://doi.org/10.1016/S0045-6535(00)00079-5
Zhang C, Li Y, Wang C et al (2016) Occurrence of endocrine disrupting compounds in aqueous environment and their bacterial degradation: a review. Crit Rev Environ Sci Technol 46:1–59. https://doi.org/10.1080/10643389.2015.1061881
Zhang H, Zhang Y, Li J, Yang M (2019) Occurrence and exposure assessment of bisphenol analogues in source water and drinking water in China. Sci Total Environ 655:607–613. https://doi.org/10.1016/j.scitotenv.2018.11.053
Zhi Y, Cao Y, Sun J et al (2018) Indirect effects of extreme precipitation on the growth of Vallisneria denseserrulata Makino. Environ Exp Bot 153:229–235. https://doi.org/10.1016/j.envexpbot.2018.06.003
Zhou Y, Li X, Zhao Y et al (2016) Divergences in reproductive strategy explain the distribution ranges of Vallisneria species in China. Aquat Bot 132:41–48. https://doi.org/10.1016/j.aquabot.2016.04.005
Zhou Y, Li L, Song Z (2019) Plasticity in sexual dimorphism enhances adaptation of dioecious Vallisneria natans plants to water depth change. Front Plant Sci 10:826. https://doi.org/10.3389/fpls.2019.00826
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Thanks to Dr. Aitian Ren for her writing assistance.
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This work was supported by the Knowledge Innovation Program of Wuhan-Shuguang Project.
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Experimental design: Huiying Han, Longyi Yuan and Yu Cao; research activities: Huiying Han, Hang Wu, Yu Cao, Yongwei Zhi and Jingzhe Zhou; writing—original draft preparation: Huiying Han, Wei Li and Yu Cao; writing—review and editing: Huiying Han, Longyi Yuan, Yu Cao and Jingzhe Zhou.
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Han, H., Wu, H., Zhi, Y. et al. Impacts of bisphenol A on growth and reproductive traits of submerged macrophyte Vallisneria natans. Environ Sci Pollut Res 30, 46383–46393 (2023). https://doi.org/10.1007/s11356-023-25521-8
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DOI: https://doi.org/10.1007/s11356-023-25521-8