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The reduction of Cr(VI) in Salvinia minima, possible involvement of an h-type thioredoxin

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Abstract

Hexavalent chromium [Cr(VI)] is extremely toxic to plant cells and has been recognized to possess a high redox potential. Tolerant plant species have shown the ability to reduce Cr(VI), but the operating mechanism involved in this process is not elucidated. Thus, the aim of this study was to investigate the possible involvement of thiolic and phenolic compounds and thioredoxin expression during Cr(VI) reduction in S. minima. In addition, a probable enzymatic reduction of Cr(VI) was investigated. Plants were exposed to 20 mg L−1 Cr(VI) concentration during 7 days under controlled conditions. The amount of metal accumulated in lacinias (root-like submerged leaves) and fronds (floating leaves) indicated that a low percentage of absorbed Cr(VI) was mobilized from lacinias to fronds. X-ray absorption near-edge structure (XANES) analysis revealed that Cr(III) was the only chromium species occurring in S. minima plants. Thiols and phenolics of lacinias and fronds were increased significantly by Cr(VI) treatment, but accumulation patterns were different. The expression of an h-type thioredoxin (Trx h) was demonstrated for the first time in Cr-exposed lacinias. Enzymatic reduction showed a low contribution to the Cr(VI) reduction. Data of this study provide evidences on the involvement of thiols, thioredoxin, and phenolics in the reduction of Cr(VI) to Cr(III) in S. minima tissues.

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References

  • Ahemad M (2014) Bacterial mechanisms for Cr(VI) resistance and reduction: an overview and recent advances. Folia Microbiol 59:321–332

    CAS  Google Scholar 

  • Aldrich MV, Gardea-Torresdey JL, Peralta-Videa JR, Parsons JG (2003) Uptake and reduction of Cr(VI) to Cr(III) by mesquite (Prosopis spp.): chromate-plant interaction in hydroponics and solid media studied using XAS. Environ Sci Technol 37:1859–1864

    CAS  Google Scholar 

  • Ali S, Abbas Z, Rizwan M, Zaheer IE, Yavaş I, Ünay A, Abdel-Daim MM, Bin-Jumah M, Hasanuzzaman M, Kalderis D (2020) Application of floating aquatic plants in phytoremediation of heavy metals polluted water: a review. Sustainability 12:1927. https://doi.org/10.3390/su12051927

    Article  CAS  Google Scholar 

  • Assabgui RA, Reid LM, Hamilton RI, Arnason T (1993) Correlation of kernel (E)-ferulic acid content of maize with resistance to Fusarium graminearum. Phytopathology 83:949–953

    CAS  Google Scholar 

  • Augustynowicz J, Kołton AM, Baran AM, Kostecka-Gugała AM, Lasek WW (2013a) Strategy of Cr detoxification by Callitriche cophocarpa. Cent Eur J Chem 11:295–303

    CAS  Google Scholar 

  • Augustynowicz J, Kyzioł-Komosińska J, Smoleń S, Waloszek A (2013b) Study on chromium-binding capacity of Callitriche cophocarpa in an aquatic environment. Arch Environ Contam Toxicol 64:410–418

    CAS  Google Scholar 

  • Augustynowicz J, Sitek E, Bryniarski T, Baran A, Ostachowicz B, Urbańska-Stopa M, Szklarczyk M (2020) The use of Callitriche cophocarpa Sendtn. for the reclamation of Cr-contaminated freshwater habitat: benefits and limitations. Environ Sci Pollut Res 27:25510–25522

    CAS  Google Scholar 

  • Baldiris R, Acosta-Tapia N, Montes A, Hernández J, Vivas-Reyes R (2018) Reduction of hexavalent chromium and detection of chromate reductase (ChrR) in Stenotrophomonas maltophilia. Molecules 23:406–425

    Google Scholar 

  • Boubakri H, Saidi MN, Barhoumi F, Kamoun H, Jebara M, Brini F (2019) Identification and characterization of thioredoxin H-type gene family in Triticum turgidum ssp. Durum in response to natural and environmental factor-induced oxidative stress. Plant Mol Biol Report 37:464–476

    CAS  Google Scholar 

  • Caldelas C, Bort J, Febrero A (2012) Ultrastructure and subcellular distribution of Cr in Iris pseudacorus L. using TEM and X-ray microanalysis. Cell Biol Toxicol 28:57–68

    CAS  Google Scholar 

  • Chen Z, Zou L, Zhang H, Chen Y, Liu P, Li X (2014) Thioredoxin is involved in hexavalent chromium reduction in Streptomyces violaceoruber strain LZ-26-1 isolated from the Lanzhou reaches of the Yellow River. Int Biodeterior Biodegradation 94:146–151

    CAS  Google Scholar 

  • Cheung KH, Gu JD (2007) Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: a review. Int Biodeterior Biodegrad 59:8–15

    CAS  Google Scholar 

  • Coetzee JJ, Bansal N, Chirwa EMN (2020) Chromium in environment, its toxic effect from chromite-mining and ferrochrome industries, and its possible bioremediation. Expos Health 12:51–62

    Google Scholar 

  • Devi PS, Rukmini K, Himabindu SVSSSL, Savithramma NN (2015) Antibacterial activity and phytochemical screening of Salvinia auriculata Aubl. from Tirumala Hills, Tirupati. Int J Pharm Sci Rev Res 30:35–38

    Google Scholar 

  • Dhir B (2009) Salvinia: an aquatic fern with potential use in phytoremediation. Environ We Inter J Sci Technol 4:23–27

    Google Scholar 

  • Duarte B, Silva V, Caçador I (2012) Hexavalent chromium reduction, uptake and oxidative biomarkers in Halimione portulacoides. Ecotoxicol Environ Saf 83:1–7

    CAS  Google Scholar 

  • Dubey SP, Sillanpaa M, Varma RS (2017) Reduction of hexavalent chromium using Sorbaria sorbifolia aqueous leaf extract. Appl Sci 7:715. https://doi.org/10.3390/app7070715

    Article  CAS  Google Scholar 

  • Ederli L, Reale L, Ferranti F, Pasqualini S (2004) Responses induced by high concentration of cadmium in Phragmites australis roots. Physiol Plant 121:66–74

    CAS  Google Scholar 

  • Espinoza-Quiñones FR, Martin N, Stutz G, Tirao G, Palácio SM, Rizzutto MA, Módenes AN, Silva FG Jr, Szymanski N, Kroumov AD (2009) Root uptake and reduction of hexavalent chromium by aquatic macrophytes as assessed by high-resolution X-ray emission. Water Res 43:4159–4166

    Google Scholar 

  • Figueroa SJA, Mauricio JC, Murari J, Beniz DB, Piton JR, Slepicka HH, Falcão de Souza M, Espíndola AM, Levinsky APS (2016) Upgrades to the XAFS2 beamline control system and to the endstation at the LNLS. J Phys Conf Ser 712:012022. https://doi.org/10.1088/1742-6596/712/1/012022

    Article  CAS  Google Scholar 

  • Gini TG, Jothi GJ (2018) Column chromatography and HPLC analysis of phenolic compounds in the fractions of Salvinia molesta Mitchell. Egypt J Basic Appl Sci 5:197–203

    Google Scholar 

  • Gomes MAC, Hauser-Davis RA, Suzuki MS, Vitória AP (2017) Plant chromium uptake and transport, physiological effects and recent advances in molecular investigations. Ecotoxicol Environ Saf 140:55–64

    CAS  Google Scholar 

  • Hernández LE, Sobrino-Plata J, Montero-Palmero MB, Carrasco-Gil S, Flores-Cáceres ML, Ortega-Villasante C, Escobar C (2015) Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. J Exp Bot 66:2901–2911

    Google Scholar 

  • Kaszycki P, Dubicka-Lisowska A, Augustynowicz J, Piwowarczyk B, Wesołowski W (2018) Callitriche cophocarpa (water starwort) proteome under chromate stress: evidence for induction of a quinone reductase. Environ Sci Pollut Res 25:8928–8942

    CAS  Google Scholar 

  • Kováčik J, Klejdus B (2008) Dynamics of phenolic acids and lignin accumulation in metal-treated Matricaria chamomilla roots. Plant Cell Rep 27:605–615

    Google Scholar 

  • Kumari S, Kumar B, Sheel R (2016) Bioremediation of heavy metals by serious aquatic weed, Salvinia. Int J Curr Microbiol App Sci 9:355–368

    Google Scholar 

  • Levina A, Lay PA (2004) Solution structures of chromium(VI) complexes with glutathione and model thiols. Inorg Chem 43:324–335

    CAS  Google Scholar 

  • Linde AR, Garcia-Vazquez E (2006) A simple assay to quantify metallothionein helps to learn about bioindicators and environmental health. Biochem Mol Biol Educ 34:360–363

    CAS  Google Scholar 

  • Lytle CM, Lytle FW, Yang N, Qian JH, Hansen D, Zayed A, Terry N (1998) Reduction of Cr(VI) to Cr(III) by wetland plants: potential for in situ heavy metal detoxification. Environ Sci Technol 32:3087–3093

    CAS  Google Scholar 

  • Maine MA, Hadad HR, Sánchez GC, Caffaratti SE, Pedro MC (2016) Kinetics of Cr(III) and Cr(VI) removal from water by two floating macrophytes. Int J Phytoremediation 18:261–268

    CAS  Google Scholar 

  • Malaviya P, Singh A, Anderson TA (2020) Aquatic phytoremediation strategies for chromium removal. Rev Environ Sci Biotechnol 19:897–944

    CAS  Google Scholar 

  • McDonell MW, Simon MN, Studier FW (1977) Analysis of restriction fragments of T7 DNA and determination of molecular weights by electrophoresis in neutral and alkaline gels. J Mol Biol 110:119–146

    CAS  Google Scholar 

  • Memon SQ, Bhanger MI, Khuhawar MY (2005) Preconcentration and separation of Cr(III) and Cr(VI) using sawdust as a sorbent. Anal Bioanal Chem 383:619–624

    CAS  Google Scholar 

  • Nur-E-Alam M, Mia MAS, Ahmad F, Rahman MM (2020) An overview of chromium removal techniques from tannery effluent. Appl Water Sci 10:205. https://doi.org/10.1007/s13201-020-01286-0

    Article  CAS  Google Scholar 

  • Ouyang Y, Peng Y, Li J, Holmgren A, Lu J (2018) Modulation of thiol-dependent redox system by metal ions via thioredoxin and glutaredoxin systems. Metallomics 10:218–228

    CAS  Google Scholar 

  • Pagano EA, Chueca A, Lopez-Gorgé J (2000) Expression of thioredoxins f and m, and of their targets fructose-1,6-bisphosphatase and NADP-malate dehydrogenase, in pea plants grown under normal and light/temperature stress conditions. J Exp Bot 51:1299–1307

    CAS  Google Scholar 

  • Pivato M, Fabrega-Prats M, Masi A (2014) Low-molecular-weight thiols in plants: functional and analytical implications. Arch Biochem Biophys 560:83–99

    CAS  Google Scholar 

  • Pradas del Real AE, Pérez-Sanz A, Lobo MC, McNear DH Jr (2014) The chromium detoxification pathway in the multimetal accumulator Silene vulgaris. Environ Sci Technol 48:11479–11486

    CAS  Google Scholar 

  • Pradedova EV, Nimaeva OD, Salyaev RK (2017) Redox processes in biological systems. Russ J Plant Physiol 64:822–832

    CAS  Google Scholar 

  • Prado C, Rosa M, Pagano E, Hilal M, Prado FE (2010) Seasonal variability of physiological and biochemical aspects of chromium accumulation in outdoor-grown Salvinia minima. Chemosphere 81:584–593

    CAS  Google Scholar 

  • Prado C, Chocobar-Ponce S, Pagano E, Prado F, Rosa M (2021) Differential effects of Zn concentrations on Cr(VI) uptake by two Salvinia species: involvement of thiol compounds. Int J Phytoremediation 23:10–17

    CAS  Google Scholar 

  • Ravela B, Newville M (2005) ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J Synchrotron Radiat 12:537–541

    Google Scholar 

  • Saha R, Nandi R, Saha B (2011) Sources and toxicity of hexavalent chromium. J Coord Chem 64:1782–1806

    CAS  Google Scholar 

  • Santana KB, de Almeida AAF, Souza VL, Mangabeira PAO, Silva DC, Gomes FP, Dutruch L, Loguercio LL (2012) Physiological analyses of Genipa americana L. reveals a tree with ability as phytostabilizer and rhizofilterer of chromium ions for phytoremediation of polluted watersheds. Environ Exp Bot 80:35–42

    CAS  Google Scholar 

  • Shahid M, Shamshad S, Rafiq M, Khalid S, Bibi I, Niazi NK, Dumat C, Rashid MI (2017) Chromium speciation, bioavailability, uptake, toxicity, and detoxification in soil-plant system: a review. Chemosphere 178:513–533

    CAS  Google Scholar 

  • Sharma P, Bihari V, Agarwal SK, Verma V, Kesavachandran CN, Pangtey BS, Mathur N, Singh KP, Srivastava M, Goel SK (2012) Groundwater contaminated with hexavalent chromium [Cr (VI)]: a health survey and clinical examination of community inhabitants (Kanpur, India). PLoS One 7:e47877

    CAS  Google Scholar 

  • Sharma A, Kapoor D, Wang J, Shahzad B, Kumar V, Bali AS, Jasrotia S, Zheng B, Yuan H, Yan D (2020a) Chromium bioaccumulation and its impacts on plants: an overview. Plants 9:100. https://doi.org/10.3390/plants9010100

    Article  CAS  Google Scholar 

  • Sharma M, Kumar V, Mahey S, Bhardwaj R, Thukral AK (2020b) Antagonistic effects of EDTA against biochemical toxicity induced by Cr(VI) in Hordeum vulgare L. seedlings. Physiol Mol Biol Plants 26:2487–2502

    CAS  Google Scholar 

  • Sharma M, Kumar V, Bhardwaj R, Thukral AK (2020c) Tartaric acid mediated Cr hyperaccumulation and biochemical alterations in seedlings of Hordeum vulgare L. J Plant Growth Regul 39:1–14

    CAS  Google Scholar 

  • Sharma N, Sodhi KK, Kumar M, Singh DK (2021) Heavy metals eco-toxicity with major concern to chromium and recent advancement in remediation technologies. Environ Nanotechnol Monit Manag 15:100388. https://doi.org/10.1016/j.enmm.2020.100388

    Article  Google Scholar 

  • Stephenson C, Black CR (2014) One step forward, two steps back: the evolution of phytoremediation into commercial technologies. Biosci Horiz 7:1–15

    CAS  Google Scholar 

  • Swain T, Hillis WE (1959) The phenols constituents of Prunus domestica. I. The quantitative analysis of phenolics constituents. J Sci Food Agric 10:63–68

    CAS  Google Scholar 

  • Thilakar RJ, Rathi JJ, Pillai PM (2012) Phytoaccumulation of chromium and copper by Pistia stratiotes L. and Salvinia natans (L.) All. J Nat Prod Plant Resour 2:725–730

    CAS  Google Scholar 

  • USEPA (1994) SW 846 Method 3051A: Microwave assisted acid digestion of sediments, sludges, soils, and oils. Washington (USA) [cited 2021 Jan 28].

  • Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432

    CAS  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the financial support from the Consejo de Investigaciones de la Universidad Nacional de Tucumán (grant PIUNT 26 G/623) and Consejo Nacional de Investigaciones Científicas y Técnicas (grant PIP 14/151). Our special thanks to Fundación Leloir (Buenos Aires, Argentina) for the sequence analysis of Trx h and to Dr. Fernando E. Prado for the critical reading of manuscript. This research used resources of the Brazilian Synchrotron Light Laboratory (LNLS), an open national facility operated by the Brazilian Centre for Research in Energy and Materials (CNPEM) for the Brazilian Ministry for Science, Technology, Innovations and Communications (MCTIC) (XAFS2-20170902 project).

Funding

This study was supported by Grant PIUNT 26 G/623 (Universidad Nacional de Tucumán), Argentina, and Grant PIP 14/151 (Consejo Nacional de Investigaciones Científicas y Técnicas – CONICET), Argentina.

This research used resources of the Brazilian Synchrotron Light Laboratory (LNLS), an open national facility operated by the Brazilian Centre for Research in Energy and Materials (CNPEM) for the Brazilian Ministry for Science, Technology, Innovations and Communications (MCTIC) (XAFS2-20170902 project).

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SCP and CP: Conceptualization, formal analysis, investigation, and writing—review and editing.

RT: Investigation.

NI and EP: Investigation in the metal content determination in plant tissues and performed the expression of h-type Trx.

JMRL and MDM: Investigation in the XANES analysis.

MR: Conceptualization, formal analysis, supervision, and funding acquisition.

All authors: Review and editing and gave final approval for publication.

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Correspondence to Mariana Rosa.

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Chocobar-Ponce, ., Prado, C., Tabernero, R. et al. The reduction of Cr(VI) in Salvinia minima, possible involvement of an h-type thioredoxin. Environ Sci Pollut Res 29, 3958–3966 (2022). https://doi.org/10.1007/s11356-021-15967-z

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