Abstract
In order to evaluate the differential absorption and toxicity of arsenate (AsV) and arsenite (AsIII), Lemna valdiviana plants were grown in a nutrient solution and subjected to 0.0 (control); 0.5; 1.0; 1.5; 2.0; 3.0; 4.0; 5.0 and 7.5 mg L−1 of AsIII or AsV for three days. Exposure to both chemical forms resulted in As bioaccumulation, although AsIII-grown plants showed higher As content in tissues. In AsV-grown plants, the relative growth rate (RGR) decreased to 50%, at a concentration of 4.0 mg L−1, while for treatments with AsIII, the same decrease was observed at 1.0 mg L−1. The tolerance index decreased with increasing concentrations, with lower values for AsIII. Plants treated with AsIII showed increased superoxide anion levels, whilst higher levels of hydrogen peroxide were present in AsV-treated plants. Moreover, malondialdehyde (MDA) levels were higher for plants subjected to AsIII when compared to AsV at lower concentrations. Concentrations of 1 mg L−1 of AsIII and 4 mg L−1 of AsV showed equivalent MDA levels. Superoxide dismutase and catalase activities were increased at low concentrations and were inhibited at higher concentrations of AsIII and AsV, whereas peroxidase activity was positively modulated by increased AsIII or AsV concentrations. In conclusion, L. valdiviana plants took up and accumulated arsenic as AsIII or AsV, demonstrating the potential for phytoremediation of this metalloid. Furthermore, AsIII-exposed plants showed enhanced toxicity when compared to AsV, at the same applied concentration, although toxicity was more related to internal As concentrations, regardless of the chemical form applied.
References
Abbas G, Murtaza B, Bibi I, Shahid M, Niazi NK, Khan MI, Amjad M, Hussain M, Tahir N (2018) Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health 15:59. https://doi.org/10.3390/ijerph15010059
Abedin MJ, Feldmann J, Meharg AA (2002) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128:1120–1128. https://doi.org/10.1104/pp.010733
Aguiar-Silva C, Brandão SE, Domingos M, Bulbovas P (2016) Antioxidant responses of Atlantic Forest native tree species as indicators of increasing tolerance to oxidative stress when they are exposed to air pollutants and seasonal tropical climate. Ecol Indic 63:154–164. https://doi.org/10.1016/j.ecolind.2015.11.060
Andrade HM, Oliveira JA, Farnese FS, Ribeiro C, Silva AA, Campos FV, Neto JL (2016) Arsenic toxicity: cell signalling and the attenuating effect of nitric oxide in Eichhornia crassipes. Biol Plant 60:173–180. https://doi.org/10.1007/s10535-015-0572-4
Beauchamp C, Fridovich I (1971) Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:267–287. https://doi.org/10.1016/0003-2697(71)90370-8
Boveris A, Alvarez S, Bustamante J, Valdez L (2002) Measurement of superoxide radical and hydrogen peroxide production in isolated cells and subcellular organelles. Methods Enzymol 105:280–287. https://doi.org/10.1016/S0076-6879(02)49342-1
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
Campos FV, Oliveira JA, Silva AA, Ribeiro C, Farnese FS (2019) Phytoremediation of arsenite-contaminated environments: is Pistia stratiotes L. a useful tool? Ecol Indic 104:794–801. https://doi.org/10.1016/j.ecolind.2019.04.048
Cao Y, Sun D, Ai H, Mei H, Liu X, Sun S, Xu G, Liu Y, Chen Y, Ma LQ (2017) Knocking out OsPT4 gene decreases arsenate uptake by rice plants and inorganic arsenic accumulation in rice grains. Environ Sci Technol 51:12131–12138. https://doi.org/10.1021/acs.est.7b03028
Chen Y, Sun SK, Tang Z, Liu G, Moore KL, Maathuis FJ, Miller AJ, MacGrath SP, Zhao FJ (2017) The Nodulin 26-like intrinsic membrane protein OsNIP3; 2 is involved in arsenite uptake by lateral roots in rice. J Exp Bot 68:3007–3016. https://doi.org/10.1093/jxb/erx165
Duman F, Ozturk F, Aydin Z (2010) Biological responses of duckweed (Lemna minor L.) exposed to the inorganic arsenic species As (III) and As (V): effects of concentration and duration of exposure. Ecotoxicology 19:983–993. https://doi.org/10.1007/s10646-010-0480-5
Farnese FS, Oliveira JA, Paiva EA, Menezes-Silva PE, da Silva AA, Campos FV, Ribeiro C (2017) The involvement of nitric oxide in integration of plant physiological and ultrastructural adjustments in response to arsenic. Front Plant Sci 8:516. https://doi.org/10.3389/fpls.2017.00516
Farooq MA, Islam F, Ali B, Najeeb U, Mao B, Gill RA et al. (2016) Arsenic toxicity in plants: cellular and molecular mechanisms of its transport and metabolism. Environ Exp Bot 132:42–52. https://doi.org/10.1016/j.envexpbot.2016.08.004
Finnegan PM, Chen W (2012) Arsenic toxicity: The effects on plant metabolism. Front Physiol 3:1–18. https://doi.org/10.3389/fphys.2012.00182
Gay C, Gebicki JM (2000) A critical evaluation of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. Anal Biochem 284:217–220. https://doi.org/10.1006/abio.2000.4696
Geng CN, Zhu YG, Liu WJ, Smith SE (2005) Arsenate uptake and translocation in seedlings of two genotypes of rice is affected by external phosphate concentrations. Aquat Bot 83:321–331. https://doi.org/10.1016/j.aquabot.2005.07.003
Ghosh P, Banerjee M, Giri AK, Ray K (2008) Toxicogenomics of arsenic: classical ideas and recent advances. Mutat Res Rev Mutat 659:293–301. https://doi.org/10.1016/j.mrrev.2008.06.003
Gusman GS, Oliveira JA, Farnese FS, Cambraia J (2013) Arsenate and arsenite: the toxic effects on photosynthesis and growth of lettuce plants. Acta Physiol Plant 35:1201–1209. https://doi.org/10.1007/s11738-012-1159-8
Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455. https://doi.org/10.1104/pp.84.2.450
Hodges DM, DeLong JM, Forney CF, Prange RK (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. https://doi.org/10.1007/s004250050524
Hunt R (1982) Plant growth curves. Edward Arnold, London
Khan I, Ahmad A, Iqbal M (2009) Modulation of antioxidant defense system for arsenic detoxification in Indian mustard. Ecotoxicol Environ Saf 72:626–634. https://doi.org/10.1016/j.ecoenv.2007.11.016
Leão GA, Oliveira JO, Felipe RTA, Farnese FS, Gusman GS (2014) Anthocyanins, thiols, and antioxidant scavenging enzymes are involved in Lemna gibba tolerance to arsenic. J Plant Interact 9:143–151. https://doi.org/10.1080/17429145.2013.784815
Marin AR, Pezeshki SR, Masschelen PH, Choi HS (1993) Effect of dimethylarsenic acid (DMAA) on growth, tissue arsenic and photosynthesis in rice plants. J Plant Nutr 16:1532–4807. https://doi.org/10.1080/01904169309364580
McClintock TR, Chen Y, Bundschuh J, Oliver JT, Navoni J, Olmos V, Lepori EV, Ahsan H, Parvez F (2012) Arsenic exposure in Latin America: biomarkers, risk assessments and related health effects. Sci Total Environ 429:76–91. https://doi.org/10.1016/j.scitotenv.2011.08.051
Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. N. Phytol 154:29–43. https://doi.org/10.1046/j.1469-8137.2002.00363.x
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Pontius FW, Brown KG, Chen CJ (1994) Health implications of arsenic in drinking water. J Am Water Works Ass 86:52–63. https://doi.org/10.1002/j.1551-8833.1994.tb06246.x
Rodríguez-Ruiz M, Aparicio-Chacón MV, Palma JM, Corpas FJ (2019) Arsenate disrupts ion balance, sulfur and nitric oxide metabolisms in roots and leaves of pea (Pisum sativum L.) plants. Environ Exp Bot 161:143–156. https://doi.org/10.1016/j.envexpbot.2018.06.028
Silva AA, Oliveira JA, Campos FV, Ribeiro C, Farnese FS, Costa AC (2018) Phytoremediation potential of Salvinia molesta for arsenite contaminated water: role of antioxidant enzymes. Theor Exp Plant Phys 30:275–286. https://doi.org/10.1007/s40626-018-0121-6
Singh R, Singh S, Parihar P, Singh VP, Prasad SM (2015) Arsenic contamination, consequences and remediation techniques: a review. Ecotoxicol Environ Saf 112:247–270. https://doi.org/10.1016/j.ecoenv.2014.10.009
Souri Z, Karimi N, Oliveira LM (2018) Antioxidant enzymes responses in shoots of arsenic hyperaccumulator, Isatis cappadocica Desv., under interaction of arsenate and phosphate. Environ Technol 39:1316–1327. https://doi.org/10.1080/09593330.2017.1329349
Souza TD, Borges AC, Matos AT, Veloso RW, Braga AF (2018) Kinetics of arsenic absorption by the species Eichhornia crassipes and Lemna valdiviana under optimized conditions. Chemosphere 209:866–874. https://doi.org/10.1016/j.chemosphere.2018.06.132
Souza TD, Borges AC, Braga AF, Veloso RW, Matos AT (2019) Phytoremediation of arsenic-contaminated water by Lemna valdiviana: an optimization study. Chemosphere 234:402–408. https://doi.org/10.1016/j.chemosphere.2019.06.004
Tang X, Lim MP, McBride MB (2018) Arsenic uptake by arugula (Eruca vesicaria L.) cultivars as affected by phosphate availability. Chemosphere 195:559–566. https://doi.org/10.1016/j.chemosphere.2017.12.110
Wei C, Ge Z, Chu W, Feng R (2015) Speciation of antimony and arsenic in the soils and plants in an old antimony mine. Environ Exp Bot 109:31–39. https://doi.org/10.1016/j.envexpbot.2014.08.002
Wilkins DA (1978) The measurement of tolerance to edaphic factors by means of root growth. N. Phytol 80:623–633. https://doi.org/10.1111/j.1469-8137.1978.tb01595.x
Wu C, Huang L, Xue SG, Pan WS, Zou Q, Hartley W, Wong MH (2017) Oxic and anoxic conditions affect arsenic (As) accumulation and arsenite transporter expression in rice. Chemosphere 168:969–975. https://doi.org/10.1016/j.chemosphere.2016.10.114
Zhang J, Hwang JU, Song WY, Martinoia E, Lee Y (2017) Identification of amino acid residues important for the arsenic resistance function of Arabidopsis ABCC1. Febs Lett 591:656–666. https://doi.org/10.1002/1873-3468.12576
Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. N. Phytol 181:777–794. https://doi.org/10.1111/j.1469-8137.2008.02716.x
Zhao FJ, McGrath SP, Meharg A (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:1–25. https://doi.org/10.1146/annurev-arplant-042809-112152
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The authors are gratefull to Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) - Finance Code 001 and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) by financial support.
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Coelho, D.G., Marinato, C.S., de Matos, L.P. et al. Is arsenite more toxic than arsenate in plants?. Ecotoxicology 29, 196–202 (2020). https://doi.org/10.1007/s10646-019-02152-9
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DOI: https://doi.org/10.1007/s10646-019-02152-9