Theoretical and Experimental Plant Physiology

, Volume 30, Issue 4, pp 275–286 | Cite as

Phytoremediation potential of Salvinia molesta for arsenite contaminated water: role of antioxidant enzymes

  • Adinan Alves da SilvaEmail author
  • Juraci Alves de Oliveira
  • Fernanda Vidal de Campos
  • Cleberson Ribeiro
  • Fernanda dos Santos Farnese
  • Alan Carlos Costa


Antioxidant enzymes are important components in the defense against arsenic (As) stress in plants. Here, we tested the hypothesis that Salvinia molesta, an aquatic fern, counteracts the harmful arsenite (AsIII) effects by activating scavenging reactive oxygen species (ROS) enzymes. Thus, our objective was to investigate the role of the superoxide dismutase (SOD), catalase (CAT), peroxidase (POX), and ascorbate peroxidase (APX) in S. molesta tolerance to AsIII and indicate the use of this plant in remediation of contaminated water. Plants were grown in nutrient solution at pH 6.5 and exposed to 0, 5, 10, or 20 µM AsIII for 96 h (analyses of As absorption, mineral nutrient content, and relative growth rate) and for 24 h (analyses of oxidative stress indicators and enzymatic antioxidant defenses). In the floating leaves, there was a greater basal activity of the antioxidant enzymes and less accumulation of As than in submerged leaves. The submerged leaves, which function as roots in S. molesta, accumulated more As than floating leaves, and SOD and CAT activities were inhibited. Thus, there was a greater production of ROS and oxidative stress. Our results show that S. molesta presents enzymatic antioxidant defenses to alleviate AsIII toxicity and are more effectives in the floating leaves. These results are important to elucidate the AsIII tolerance mechanisms in S. molesta and the possibility of their use in contamined water phytoremediation. Additional studies exposing plants to more prolonged stress and using AsIII concentrations closer to those found in contaminated environments will confirm this claim.


Arsenic Macrophytes Phytoremediator species Water contamination 



The authors acknowledge the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Federal University of Viçosa for financial support.


  1. Afzal Z, Howton TC, Sun Y, Mukhtar MS (2016) The roles of aquaporins in plant stress responses. J Dev Biol. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ahammed GJ, Choudhary SP, Chen S, Xia X, Shi K, Zhou Y, Yu J (2013) Role of brassinosteroids in alleviation of phenanthrene–cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64:199–213CrossRefPubMedGoogle Scholar
  3. Ahmad P, Sarwat M, Bhat NA, Wani MR, Kazi AG, LSP Tran (2015) Alleviation of cadmium toxicity in Brassica juncea L.(Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS ONE. CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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 60:173–180CrossRefGoogle Scholar
  5. Anjum NA, Sofo A, Scopa A et al (2015) Lipids and proteins–major targets of oxidative modifications in abiotic stressed plants. Environ Sci Pollut Res 22:4099–4121CrossRefGoogle Scholar
  6. Anjum NA, Sharma P, Gill SS et al (2016) Catalase and ascorbate peroxidase-representative H2O2-detoxifying heme enzymes in plants. Environ Sci Pollut Res 23:19002–19029CrossRefGoogle Scholar
  7. Barros JPA, Henares MNP (2015) Biomass reduction of Salvinia molesta exposed to copper sulfate pentahydrate (CuSO4.5H2O). Rev Ambient Água. CrossRefGoogle Scholar
  8. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay aplicable to acrylamide gels. Anal Biochem 44:276–287CrossRefPubMedGoogle Scholar
  9. Begum MC, Islam MS, Islam M, Amin R, Parvez MS, Kabir AH (2016) Biochemical and molecular responses underlying differential arsenic tolerance in rice (Oryza sativa L.). Plant Physiol Biochem 104:266–277CrossRefPubMedGoogle Scholar
  10. 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 349:280–287CrossRefPubMedGoogle Scholar
  11. Chakraborti D, Rahmana MM, Chatterjeea A et al (2016) Fate of over 480 million inhabitants living in arsenic and fluoride endemic Indian districts: magnitude, health, socio-economic effects and mitigation approaches. J Trace Elem Med Biol 38:33–45CrossRefPubMedGoogle Scholar
  12. Chance B, Maehley AC (1955) Assay of catalase and peroxidase. Methods Enzymol 2:755–764CrossRefGoogle Scholar
  13. Chen Z, Zhu YG, Liu WJ, Meharg AA (2005) Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa) roots. New Phytol 165:91–97CrossRefPubMedGoogle Scholar
  14. Clark RB (1975) Characterization of phosphatase of intact maize roots. J Agric Food Chem 23:458–460CrossRefPubMedGoogle Scholar
  15. Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci. CrossRefGoogle Scholar
  16. da-Silva CJ, Canatto RA, Cardoso AA, Ribeiro C, de Oliveira JA (2018) Oxidative stress triggered by arsenic in a tropical macrophyte is alleviated by endogenous and exogenous nitric oxide. Braz J Bot 41:21–28CrossRefGoogle Scholar
  17. Dave R, Singh PK, Tripathi P et al (2013) Arsenite tolerance is related to proportional thiolic metabolite synthesis in rice (Oryza sativa L.). Arch Environ Contam Toxicol 64:235–242CrossRefPubMedGoogle Scholar
  18. Del Río LA, López-Huertas E (2016) ROS generation in peroxisomes and its role in cell signaling. Plant Cell Physiol 57:1364–1376PubMedGoogle Scholar
  19. Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228CrossRefGoogle Scholar
  20. Dixit G, Singh AP, Kumar A et al (2015) Sulfur mediated reduction of arsenic toxicity involves efficient thiol metabolism and the antioxidant defense system in rice. J Hazard Mater 298:241–251CrossRefPubMedGoogle Scholar
  21. Du L, Xia X, Lan X, Liu M, Zhao L, Zhang P, Wu Y (2017) Influence of arsenic stress on physiological, biochemical, and morphological characteristics in seedlings of two cultivars of maize (Zea mays L.). Water Air Soil Pollut 228:255CrossRefGoogle Scholar
  22. Edel KH, Marchadier E, Brownlee C, Kudla J, Hetherington AM (2017) The evolution of calcium-based signalling in plants. Curr Biol 27:667–679CrossRefGoogle Scholar
  23. Faria AP, Lemos-Filho JP, Modolo LV, França MGC (2013) Electrolyte leakage and chlorophyll a fluorescence among castor bean cultivars under induced water deficit. Acta Physiol Plant 35:119–128CrossRefGoogle Scholar
  24. Farnese FS, Oliveira JA, Lima F, Leão GA, Gusman GS, Silva LC (2014) Evaluation of the potential of Pistia stratiotes L. (water lettuce) for bioindication and phytoremediation of aquatic environments contaminated with arsenic. Braz J Biol 74:108–112CrossRefGoogle Scholar
  25. Farooq MA, Li L, Ali B et al (2015) Oxidative injury and antioxidant enzymes regulation in arsenic-exposed seedlings of four Brassica napus L. cultivars. Environ Sci Pollut Res 22:10699–10712CrossRefGoogle Scholar
  26. Farooq AM, Islam F, Ali B (2016a) Arsenic toxicity in plants: cellular and molecular mechanisms of its transport and metabolism. Environ Exp Bot. CrossRefGoogle Scholar
  27. Farooq MA, Gill RA, Ali B, Wang J, Islam F, Ali S, Zhou W (2016b) Subcellular distribution, modulation of antioxidant and stress-related genes response to arsenic in Brassica napus L. Ecotoxicology 25:350–366CrossRefPubMedGoogle Scholar
  28. Fayiga AO, Saha KU (2016) Arsenic hyperaccumulating fern: implications for remediation of arsenic contaminated soils. Geoderma 284:132–143CrossRefGoogle Scholar
  29. Fazi S, Amalfitano S, Casentini B et al (2016) Arsenic removal from naturally contaminated waters: a review of methods combining chemical and biological treatments. Rend Fis Acc Lincei 27:51–58CrossRefGoogle Scholar
  30. Finnegan PM, Chen W (2012) Arsenic toxicity: the effects on plant metabolism. Front Physiol. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Freitas-Silva LD, de Araújo TO, da Silva LC, Oliveira JA, Araújo JM (2016) Arsenic accumulation in Brassicaceae seedlings and its effects on growth and plant anatomy. Ecotoxicol Environ Saf 124:1–9CrossRefPubMedGoogle Scholar
  32. Fresno T, Peñalosa JM, Santner J, Puschenreiter M, Prohaska T, Moreno-Jiménez E (2016) Iron plaque formed under aerobic conditions efficiently immobilizes arsenic in Lupinus albus L roots. Environ Pollut 216:215–222CrossRefPubMedGoogle Scholar
  33. Gay C, Gebicki JM (2000) A critical evaluation of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. Anal Biochem 284:217–220CrossRefPubMedGoogle Scholar
  34. Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314CrossRefPubMedPubMedCentralGoogle Scholar
  35. Gill SS, Anjum NA, Gill R (2015) Superoxide dismutase–mentor of abiotic stress tolerance in crop plants. Environ Sci Pollut Res Int 22:10375–10394CrossRefPubMedGoogle Scholar
  36. Gomes MP, Carvalho M, Marques TCLLSM, Duarte DM, Nogueira COG, Soares AM, Garcia QS (2012) Arsenic-sensitivity in Anadenanthera peregrina due to arsenic-induced lipid peroxidation. Int J Appl Sci Technol 2:55–63Google Scholar
  37. Gupta DK, Inouhe M, Rodríguez-Serrano M, Romero-Puertas MC, Sandalio LM (2013) Oxidative stress and arsenic toxicity: role of NADPH oxidases. Chemosphere 90:1987–1996CrossRefPubMedGoogle Scholar
  38. 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 35:1201–1209CrossRefGoogle Scholar
  39. Hajiboland R (2014) Reactive oxygen species and photosynthesis. In: Ahmad P (ed) Oxidative damage to plants, 3rd edn. Academic Press, India, pp 1–63Google Scholar
  40. Halliwell B, Gutteridge JMC (2015) Free radicals in biology and medicine. Oxford University Press, OxfordCrossRefGoogle Scholar
  41. Han YH, Fu JW, Chen Y, Rathinasabapathi B, Ma LQ (2016) Arsenic uptake, arsenite efflux and plant growth in hyperaccumulator Pteris vittata: role of arsenic-resistant bacteria. Chemosphere 144:1937–1942CrossRefPubMedGoogle Scholar
  42. Hariyadi, Yanuwiadi B, Polii B, Soemarno (2013) Phytoremediation of arsenic from geothermal power plant waste water using Monochoria vaginalis, Salvinia molesta and Colocasia esculenta. Int J Biosci 3:104–111Google Scholar
  43. Havir EA, Mchale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455CrossRefPubMedPubMedCentralGoogle Scholar
  44. Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155CrossRefPubMedPubMedCentralGoogle Scholar
  45. Hettick BE, Cañas-Carrell JE, French AD, Klein DM (2015) Arsenic: a review of the element’s toxicity, plant interactions, and potential methods of remediation. J Agric Food Chem 19:7097–7107CrossRefGoogle Scholar
  46. Hofffman H, Schenk M (2011) Arsenite toxicity and uptake rate of rice (Oryza sativa L.) in vivo. Environ Pollut 159:2398–2404CrossRefGoogle Scholar
  47. Hu M, Li F, Liu C, Wu W (2015) The diversity and abundance of As(III) oxidizers on root iron plaque is critical for arsenic bioavailability to rice. Sci Rep 5:13611. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Hunt R (1978) Plant growth analysis (Studies in Biology). Edward Arnold Ltd., LondonGoogle Scholar
  49. Jasrotia S, Kansal A, Mehra A (2017) Performance of aquatic plant species for phytoremediation of arsenic-contaminated water. Appl Water Sci. 7:889–896CrossRefGoogle Scholar
  50. Kanwar MK, Poonam, Bhardwaj R (2015) Arsenic induced modulation of antioxidative defense system and brassinosteroids in Brassica juncea L. Ecotoxicol Environ Saf 115:119–125CrossRefPubMedGoogle Scholar
  51. Khang VH, Hatayama M, Inoue C (2012) Arsenic accumulation by aquatic macrophyte coontail (Ceratophyllum demersum L.) exposed to arsenite, and the effect of iron on the uptakeof arsenite and arsenate. Environ Exp Bot 83:47–52CrossRefGoogle Scholar
  52. Kumar S, Dubey RS, Tripathi RD, Chakrabarty D, Trivedi PK (2015) Omics and biotechnology of arsenic stress and detoxification in plants: current updates and prospective. Environ Int 74:221–230CrossRefPubMedGoogle Scholar
  53. Kumar M, Rahman MM, Ramanathan AL, Naidu R (2016) Arsenic and other elements in drinking water and dietary components from the middle Gangetic plain of Bihar, India: health risk index. Sci Total Environ 539:125–134CrossRefPubMedGoogle Scholar
  54. Kumari S, Kumar B, Sheel R (2017) Biological control of heavy metal pollutants in water by Salvinia molesta. Int J Curr Microbiol App Sci 6:2838–2843CrossRefGoogle Scholar
  55. Leão GA, Oliveira JA, Felipe RTA, Farnese FS (2017) Phytoremediation of arsenic-contaminated water: the role of antioxidant metabolism of Azolla caroliniana Willd. (Salviniales). Acta Bot Bras 31:161–168CrossRefGoogle Scholar
  56. LeBlanc MS, McKinney EC, Meagher RB, Smith AP (2013) Hijacking membrane transporters for arsenic phytoextraction. J Biotechnol 163:1–9CrossRefPubMedGoogle Scholar
  57. Li N, Wang J, Song WY (2016) Arsenic uptake and translocation in plants. Plant Cell Physiol 57:4–13CrossRefPubMedGoogle Scholar
  58. Liu WJ, Wood BA, Raab A, McGrath SP, Zhao FJ, Feldmann J (2010) Complexation of arsenite with phytochelatins reduces arsenite efflux and translocation from roots to shoots in Arabidopsis thaliana. Plant Physiol 152:2211–2221CrossRefPubMedPubMedCentralGoogle Scholar
  59. Luque GM, Bellard C, Bertelsmeier C (2014) The 100th of the world’s worst invasive alien species. Biol Invasions 16:981–985CrossRefGoogle Scholar
  60. Marin AR, Pezeshki SR, Masscheleyn PH, Choi HS (1993) Effect of dimethylarsenic acid (DMAA) on growth, tissue arsenic and photosynthesis in rice plants. J Plant Nut 16:865–880CrossRefGoogle Scholar
  61. Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot 61:4197–4220CrossRefPubMedGoogle Scholar
  62. Miranda CV, Schwartsburd PB (2016) Aquatic ferns from Viçosa (MG, Brazil): Salviniales (Filicopsida; Tracheophyta). Braz J Bot 39:935–942CrossRefGoogle Scholar
  63. Mishra S, Jha AB, Dubey RS (2011) Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma 248:565–577CrossRefPubMedGoogle Scholar
  64. Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19CrossRefPubMedGoogle Scholar
  65. Mohammadi M, Karr AL (2001) Superoxide anion generation in effective and ineffective soybean root nodules. J Plant Physiol 158:1023–1029CrossRefGoogle Scholar
  66. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-especific peroxidase en spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  67. Newete SW, Byrne MJ (2016) The capacity of aquatic macrophytes for phytoremediation and their disposal with specific reference to water hyacinth. Environ Sci Pollut Res Int 23:10630–10643CrossRefPubMedGoogle Scholar
  68. Nicomel NR, Leus K, Folens K, Voort PV, Du Laing GD (2016) Technologies for arsenic removal from water: current status and future perspectives. Int J Environ Res Public Health 13:62. CrossRefGoogle Scholar
  69. Ozturk F, Duman F, Leblebici Z, Temizgul R (2010) Arsenic accumulation and biological responses of watercress (Nasturtium officinale R. Br.) exposed to arsenite. Environ Exp Bot 69:167–174CrossRefGoogle Scholar
  70. Parrotta L, Guerriero G, Sergeant K, Cai G, Hausman JF (2015) Target or barrier? The cell wall of early and later-diverging plants vs cadmium toxicity: differences in the response mechanisms. Front Plant Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Pommerrenig B, Diehn TA, Bienert GP (2015) Metalloido-porins: essentiality of Nodulin 26-like intrinsic proteins in metalloid transport. Plant Sci 238:212–227CrossRefPubMedGoogle Scholar
  72. Rahman MA, Hasegawa H (2011) Aquatic arsenic: phytoremediation using floating macrophytes. Chemosphere 83:633–646CrossRefPubMedGoogle Scholar
  73. Rahman A, Mostofa MG, Alam MM, Nahar K, Hasanuzzaman M, Fujita M (2015) Calcium mitigates arsenic toxicity in rice seedlings by reducing arsenic uptake and modulating the antioxidante defense and glyoxalase systems and stress markers. BioMed Res Int. CrossRefPubMedPubMedCentralGoogle Scholar
  74. Reed ST, Ayala-Silva T, Dunn CB, Gordon GG (2015) Effects of arsenic on nutrient accumulation and distribution in selected ornamental plants. Agric Sci 6:1513–1531Google Scholar
  75. Rezania S, Taib SM, Md Din MF, Dahalan FA, Kamyab H (2016) Comprehensive review on phytotechnology: heavy metals removal by diverse aquatic plants species from wastewater. J Hazard Mater 318:587–599CrossRefPubMedGoogle Scholar
  76. Rout JR, Sahoo SL (2013) Antioxidant enzyme gene expression in response to copper stress in Withania somnifera L. Plant Growth Regul 71:95–99CrossRefGoogle Scholar
  77. Sarwar N, Imran M, Shaheen MR, Ishaque W, Kamran MA, Matloob A, Hussain S (2017) Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere 171:710–721CrossRefPubMedGoogle Scholar
  78. Shaibur MR, Kawai S (2009) Effect of arsenic on visible symptom and arsenic concentration in hydroponic Japanese mustard spinach. Environ Exp Bot 67:65–70CrossRefGoogle Scholar
  79. Sharma I (2012) Arsenic induced oxidative stress in plants. Biologia 67:447–453CrossRefGoogle Scholar
  80. Sharma I (2013) Arsenic-induced oxidative stress and antioxidant defense system of Pisum sativum and Pennisetum typhoides: a comparative study. Res J Biotech 8:48–56Google Scholar
  81. Shen S, Li XF, Cullen WR, Weinfeld M, Le XC (2013) Arsenic binding to proteins. Chem Rev 113:7769–7792CrossRefPubMedPubMedCentralGoogle Scholar
  82. Shen J, Song L, Müller K et al (2016) Magnesium alleviates adverse effects of lead on growth, photosynthesis, and ultrastructural alterations of Torreya grandis seedlings. Front Plant Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  83. Silva AA, Oliveira JA, Campos FV, Ribeiro C, Farnese FS (2017) Role of glutathione in tolerance to arsenite in Salvinia molesta, an aquatic fern. Acta Bot Bras. CrossRefGoogle Scholar
  84. Singh AP, Dixit G, Kumar A (2015a) Nitric oxide alleviated arsenic toxicity by modulation of antioxidants and thiol metabolism in rice (Oryza sativa L.). Front Plant Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  85. Singh VP, Singh S, Kumar J, Prasad SM (2015b) Investigating the roles of ascorbate-glutathione cycle and thiol metabolism in arsenate tolerance in ridged Luffa seedlings. Protoplasma 252:1217–1229CrossRefPubMedGoogle Scholar
  86. Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 16:13561–13578CrossRefPubMedPubMedCentralGoogle Scholar
  87. Talukdar D (2013) Arsenic-induced oxidative stress in the common bean legume, Phaseolus vulgaris L. seedlings and its amelioration by exogenous nitric oxide. Physiol Mol Biol Plants 19:69–79CrossRefPubMedGoogle Scholar
  88. Talukdar D, Talukdar T (2013) Superoxide-dismutase deficient mutants in common beans (Phaseolus vulgaris L.): genetic control, differential expressions of isozymes, and sensitivity to arsenic. BioMed Res Int. CrossRefPubMedPubMedCentralGoogle Scholar
  89. Upadhyaya H, Shome S, Roy D, Bhattacharya MK (2014) Arsenic induced changes in growth and physiological responses in Vigna radiata seedling: effect of curcumin interaction. Am J Plant Sci 5:3609–3618CrossRefGoogle Scholar
  90. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511CrossRefPubMedPubMedCentralGoogle Scholar
  91. Xu W, Dai W, Yan H et al (2015) Arabidopsis NIP3;1 plays an important role in arsenic uptake and root-to-shoot translocation under arsenite stress conditions. Mol Plant 8:722–733CrossRefPubMedGoogle Scholar
  92. Yamaguchi N, Ohkura T, Takahashi Y, Maejima Y, Arao T (2014) Arsenic distribution and speciation near rice roots influenced by iron plaques and redox conditions of the soil matrix. Environ Sci Technol 48:1549–1556CrossRefPubMedGoogle Scholar
  93. Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794CrossRefPubMedGoogle Scholar

Copyright information

© Brazilian Society of Plant Physiology 2018

Authors and Affiliations

  1. 1.Laboratório de Ecofisiologia e Produtividade VegetalInstituto Federal de Educação, Ciência e Tecnologia Goiano/Campus Rio VerdeRio VerdeBrazil
  2. 2.Departamento de Biologia VegetalUniversidade Federal de ViçosaViçosaBrazil
  3. 3.Instituto Federal Fluminense/Campus Avançado de São João da BarraSão João da BarraBrazil

Personalised recommendations