Skip to main content
Log in

Amelioration of sodium and arsenic toxicity in Salvinia natans L. with 2,4-D priming through physiological responses

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Sodium (Na) and arsenic (As) toxicity were monitored by hyperaccumulation of metals in Salvinia natans L. with 2,4-dichlorophenoxyacetic acid (2,4-D) induction. Salvinia was recorded with significant bioaccumulation of those metals with de-folding of cellular attributes in sustenance under toxic environment. 2,4-D priming has revised the growth components like net assimilation rate and relative water content to register initial plants’ survival against Na and As. Proline biosynthesis supported in the maintenance of osmotic adjustment and plants sustained better activity through subdued electrolytic leakage. Oxidative stress due to both Na and As exposure is responsible for induction under significant moderation of lipid peroxidation and protein carbonization by 2,4-D application was evident to release the stress from metal and metalloids. Reactive oxygen species (ROS) like superoxide and hydrogen peroxide accumulation were monitored with activity of NADP(H)-oxidase. However, it was downregulated by 2,4-D to check the oxidative damages. Superoxide dismutase and peroxidases were significantly moderated to reduce the oxidative degradation for both metals with 2,4-D induction. Glutathione metabolism and recycling of ascorbate with monodehydroascorbate activity were other features to maintain the redox homeostasis for metal toxicity. At the molecular level, polymorphic variations of concern genes in redox cascades demarked significantly for those two metals and established the biomarker for those metals, respectively. As a whole, the biocompatibility of auxin herbicide in Salvinia may raise the possibility for auxin metabolism and thereby, the bioaccumulation to Na and As vis-à-vis tolerance for ecological safety is established.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article.

References

  • Abbas G, Murtaza B, Bibi I, Shahid M, Niazi NK, Khan MI, Amjad M, Hussain M (2018) Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health 15:59

    Google Scholar 

  • Adhikari ND, Simko I, Mou B (2019) Phenomic and physiological analysis of salinity effects on lettuce. Sensors. 19(21):4814

    CAS  Google Scholar 

  • Ahmed B, Solanki B, Zaidi A, Khan MS, Musarrat J (2019) Bacterial toxicity of biomimetic green zinc oxide nanoantibiotic: insights into ZnONP uptake and nanocolloid–bacteria interface. Toxicol Res 8:246–261

    CAS  Google Scholar 

  • Amir W, Farid M, Ishaq HK, Farid S, Zubair M, Alharby HF, Bamagoos AA, Rizwan M, Raza N, Hakeem KR, Ali S (2020) Accumulation potential and tolerance response of Typha latifolia L. under citric acid assisted phytoextraction of lead and mercury. Chemosphere 257:127247

    CAS  Google Scholar 

  • Angelos E, Brandizzi F (2018) NADPH oxidase activity is required for ER stress survival in plants. Plant J 96:1106–1120

    CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

  • Behari JR, Prakash R (2006) Determination of total arsenic content in water by atomic absorption spectroscopy (AAS) using vapour generation assembly (VGA). Chemosphere 63:17–21

    CAS  Google Scholar 

  • Berni R, Luyckx M, Xu X, Legay S, Sergeant K, Hausman JF, Lutts S, Cai G, Guerriero G (2019) Reactive oxygen species and heavy metal stress in plants: impact on the cell wall and secondary metabolism. Environ Exp Bot 161:98–106

    CAS  Google Scholar 

  • Chin DC, Kumar RS, Suen CS, Chien CY, Hwang MJ, Hsu CH, Xuhan X, Lai ZX, Yeh KW (2019) Plant cytosolic ascorbate peroxidase with dual catalytic activity modulates abiotic stress tolerances. iScience 16:31–49

    CAS  Google Scholar 

  • Da Silva AA, de Oliveira JA, de Campos FV, Ribeiro C, dos Santos FF, Costa AC (2018) Phytoremediation potential of Salvinia molesta for arsenite contaminated water: role of antioxidant enzymes. Theor Exp Plant Physiol 30:275–286

    Google Scholar 

  • De AK, Dey N, Adak MK (2016) Bio indices for 2,4-D sensitivity between two plant species: Azollapinnata R. Br. and Vernonia cinerea L. with their cellular responses. Physiol Mol Biol Plants 22:371–380

    CAS  Google Scholar 

  • Deb CR, Gangmei PK (2020) In vitro morphogenesis of foliar explants and plant regeneration of Actinidia deliciosa A. Chev.–a horticultural important plant. Plant Cell Biotechnol Mol Biol 21:114–123

    Google Scholar 

  • Dijoo ZK, Ali R, Hameed M (2020) Role of free-floating aquatic macrophytes in abatement of the disturbed environs. In: Bhat RA, Hakeem KR (eds) Bioremediation and biotechnology, Vol. 4. Springer, Cham, 259-274. https://doi.org/10.1007/978-3-030-48690-7_12

  • Dolui D, Saha I, Adak MK (2021) 2, 4-D removal efficiency of Salvinia natans L. and its tolerance to oxidative stresses through glutathione metabolism under induction of light and darkness. Ecotoxicol Environ Saf 208:111708

    CAS  Google Scholar 

  • Drzewiecka-Antonik A, Ferenc W, Wolska A, Klepka MT, Barboza CA, Cristóvão B, Osypiuk D, Sarzyński J, Tarasiuk B, Grosicka-Maciąg E, Kurpios-Piec D (2019) Structural characterization and cytotoxic evaluation of Cu (II), Co (II) and Ni (II) complexes with herbicide 4-chloro-2-methylphenoxyacetic acid. Polyhedron 165:86–96

    CAS  Google Scholar 

  • Dumanović J, Nepovimova E, Natić M, Kuča K, Jaćević V (2020) The significance of reactive oxygen species and antioxidant defense system in plants: a concise overview. Front Plant Sci 11:552969

    Google Scholar 

  • El-Beltagi HS, Mohamed HI, Sofy MR (2020) Role of ascorbic acid, glutathione and proline applied as singly or in sequence combination in improving chickpea plant through physiological change and antioxidant defense under different levels of irrigation intervals. Molecules 25:1702

    CAS  Google Scholar 

  • Emiliani J, LlatanceOyarce WG, Bergara CD, Salvatierra LM, Novo LA, Pérez LM (2020) Variations in the phytoremediation efficiency of metal-polluted water with Salvinia biloba: prospects and toxicological impacts. Water 12:1737

    CAS  Google Scholar 

  • Etesami H, Beattie GA (2017) Plant-microbe interactions in adaptation of agricultural crops to abiotic stress conditions. In: Kumar V, Kumar M, Sharma S, Prasad R (eds) Probiotics and Plant Health. Springer, Singapore, pp. 163-200. https://doi.org/10.1007/978-981-10-3473-2_7

  • Gao Y, Pan X, Sun X, Li J, Dong L (2019) Is the protection of photosynthesis related to the mechanism of quinclorac resistance in Echinochloa crusgalli var. zelayensis? Gene 683:133–148

    CAS  Google Scholar 

  • Hasanuzzaman M, Bhuyan MHM, Nahar K, Hossain M, Mahmud JA, Hossen M, Masud AAC, Moumita FM (2018) Potassium: a vital regulator of plant responses and tolerance to abiotic stresses. Agronomy 8(3):31

    Google Scholar 

  • Hasanuzzaman M, Bhuyan MHM, Anee TI, Parvin K, Nahar K, Mahmud JA, Fujita M (2019) Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants 8(9):384

    CAS  Google Scholar 

  • Hniličková H, Hnilička F, Orsák M, Hejnák V (2019) Effect of salt stress on growth, electrolyte leakage, Na+ and K+ content in selected plant species. Plant Soil Environ 65:90–96

    Google Scholar 

  • Islam F, Farooq MA, Gill RA, Wang J, Yang C, Ali B, Wang GX, Zhou W (2017) 2,4-D attenuates salinity-induced toxicity by mediating anatomical changes, antioxidant capacity and cation transporters in the roots of rice cultivars. Sci Rep 7:1–23

    Google Scholar 

  • Jahan B, AlAjmi MF, Rehman MT, Khan NA (2020) Treatment of nitric oxide supplemented with nitrogen and sulfur regulates photosynthetic performance and stomatal behavior in mustard under salt stress. Physiol Plant 168:490–510

    CAS  Google Scholar 

  • Janků M, Luhová L, Petřivalský M (2019) On the origin and fate of reactive oxygen species in plant cell compartments. Antioxidants 8(4):105

    Google Scholar 

  • Javaid T, Farooq MA, Akhtar J, Saqib ZA, Anwar-ul-Haq M (2019) Silicon nutrition improves growth of salt-stressed wheat by modulating flows and partitioning of Na+, Cl− and mineral ions. Plant Physiol Biochem 141:291–299

    CAS  Google Scholar 

  • Kamanga RM (2020) Screening and differential physiological responses of tomato (Solanum lycopersicum L.) to drought stress. Plant Physiol Rep 25:472–482

    CAS  Google Scholar 

  • Kavishe RA, Koenderink JB, Alifrangis M (2017) Oxidative stress in malaria and artemisinin combination therapy: pros and cons. FEBS J284:2579–2591

    Google Scholar 

  • Kumwimba MN, Dzakpasu M, Li X (2020) Potential of invasive watermilfoil (Myriophyllum spp.) to remediate eutrophic waterbodies with organic and inorganic pollutants. J Environ Manag 270:110919

    Google Scholar 

  • Leon RG, Ferrell JA, Brecke BJ (2014) Impact of exposure to 2, 4-D and dicamba on peanut injury and yield. Weed Technol 28:465–470

    Google Scholar 

  • Mandal C, Ghosh N, Maiti S, Das K, Gupta S, Dey N, Adak MK (2013) Antioxidative responses of Salvinia (Salvinia natans Linn.) to aluminium stress and it’s modulation by polyamine. Physiol Mol Biol Plants 19(1):91–103

    CAS  Google Scholar 

  • Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17(1):9–15

    CAS  Google Scholar 

  • Murmu J, Chinthapalli B, Raghavendra AS (2003) Light activation of NADP malic enzyme in leaves of maize: marginal increase in activity, but marked change in regulatory properties of enzyme. J Plant Physiol 160:51–56

    CAS  Google Scholar 

  • Ohtani S, Gon M, Tanaka K, Chujo Y (2020) The design strategy for an aggregation-and crystallization-induced emission-active molecule based on the introduction of skeletal distortion by boron complexation with a tridentate ligand. Crystals 10(7):615

    CAS  Google Scholar 

  • OriginPro (2020) Version 2020b. OriginLab Corporation, Northampton, MA, USA

  • Panda A, Rangani J, Kumari A, Parida AK (2017) Efficient regulation of arsenic translocation to shoot tissue and modulation of phytochelatin levels and antioxidative defense system confers salinity and arsenic tolerance in the halophyte Suaeda maritima. Environ Exp Bot 143:149–171

    CAS  Google Scholar 

  • Pandey PK, Singh S, Singh AK, Samanta R, Yadav RN, Singh MC (2016) Inside the plant: bacterial endophytes and abiotic stress alleviation. J Appl Nat Sci 1 8(4):1899–1904

    CAS  Google Scholar 

  • Prasad SM, Kumar S, Parihar P, Singh R (2016) Interactive effects of herbicide and enhanced UV-B on growth, oxidative damage and the ascorbate-glutathione cycle in two Azollaspecies. Ecotoxicol Environ Saf 133:341–349

    CAS  Google Scholar 

  • Rached M, Pierre B, Yves G, Matsukura C, Ariizumi T, Ezura H, Fukuda N (2018) Differences in blossom-end rot resistance in tomato cultivars is associated with total ascorbate rather than calcium concentration in the distal end part of fruits per se. Hort J87:372–381

    Google Scholar 

  • Rezania S, Taib SM, Din MFM, Dahalan FA, Kamyab H (2016) Comprehensive review on phytotechnology: heavy metals removal by diverse aquatic plants species from waste water. J Hazard Mater 318:587–599

    CAS  Google Scholar 

  • Rigal A, Doyle SM, Ritter Traub A, Raggi S, Vain T, O’Brien JA, Goossens A, Pauwels L, Robert S (2020) A network of stress-related genes regulates hypocotyl elongation downstream of selective auxin perception. Plant Physiol:kiab269. https://doi.org/10.1093/plphys/kiab269

  • Roblin G, Bonnemain JL, Chollet JF (2020) Auxinic herbicide conjugates with an α-amino acid function: structural requirements for biological activity on motor cells. Plant Physiol Biochem 155:444–454

    CAS  Google Scholar 

  • Rohman M, Islam M, Monsur MB, Amiruzzaman M, Fujita M, Hasanuzzaman M (2019) Trehalose protects maize plants from salt stress and phosphorus deficiency. Plants 8(12):568

    CAS  Google Scholar 

  • Saha I, Sarkar B, Ghosh A, De AK, Adak MK (2019) Abscisic acid induced cellular responses of sub1A QTL to aluminium toxicity in rice (Oryza sativa L.). Ecotoxicol Environ Saf 183:109600

    CAS  Google Scholar 

  • Saha I, Dolui D, Ghosh A, Adak MK (2020) Responses of sub1A quantitative trait locus in rice to salinity in modulation with silver induction. Braz J Bot 43:789–797

    Google Scholar 

  • Saha I, Hasanuzzaman M, Dolui D, Sikdar D, Debnath SC, Adak MK (2021) Silver-nanoparticle and abscisic acid modulate sub1A quantitative trait loci functioning towards submergence tolerance in rice (Oryza sativa L.). Environ Exp Bot 181:104276

    CAS  Google Scholar 

  • Sarkar RK, Bhattacharjee B (2011) Rice genotypes with SUB1 QTL differ in submergence tolerance, elongation ability during submergence and re-generation growth at re-emergence. Rice 5:1–11

    Google Scholar 

  • Sarkar B, De AK, Saha I, Ghosh A, Dolui D, Adak MK (2020) Modalities of NADP-malic enzyme activities under light and darkness indicate its regulation with reference to C4 weed. Plant Sci Today 7:607–615

    CAS  Google Scholar 

  • Sarker U, Oba S (2018) Drought stress effects on growth, ROS markers, compatible solutes, phenolics, flavonoids, and antioxidant activity in Amaranthus tricolor. Appl Biochem Biotechnol 186(4):999–1016

    CAS  Google Scholar 

  • Sharma A, Shahzad B, Kumar V, Kohli SK, Sidhu GPS, Bali AS, Handa N, Kapoor D, Bhardwaj R, Zheng B (2019) Phytohormones regulate accumulation of osmolytes under abiotic stress. Biomolecules 9(7):285

    CAS  Google Scholar 

  • Singh D, Singh CK, Kumari S, Singh Tomar RS, Karwa S, Singh R, Singh RB, Sarkar SK, Pal M (2017) Discerning morpho-anatomical, physiological and molecular multiformity in cultivated and wild genotypes of lentil with reconciliation to salinity stress. PLoS One 12(5):e0177465

    Google Scholar 

  • Soleimani E, Moghadam RH, Ranjbar A (2015) Occupational exposure to chemicals and oxidative toxic stress. J Toxicol Environ Health Sci 7:1–24

    Google Scholar 

  • Swargiary A, Verma AK, Singh S, Roy MK, Daimari M (2021) Antioxidant and antiproliferative activity of selected medicinal plants of lower Assam, India: an in vitro and in silico study. Anti Cancer Agents Med Chem 21:267–277

    CAS  Google Scholar 

  • Wang M, Zhang S, Ding F (2020) Melatonin mitigates chilling-induced oxidative stress and photosynthesis inhibition in tomato plants. Antioxidants 9(3):218

    Google Scholar 

  • Xiao W, Loscalzo J (2020) Metabolic responses to reductive stress. Antioxid Redox Signal 32:1330–1347

    CAS  Google Scholar 

  • Xie Z, Wang J, Wang W, Wang Y, Xu J, Li Z, Zhao X, Fu B (2020) Integrated analysis of the transcriptome and metabolome revealed the molecular mechanisms underlying the enhanced salt tolerance of rice due to the application of exogenous melatonin. Front Plant Sci 11:618680

    Google Scholar 

  • Yadav S, Modi P, Dave A, Vijapura A, Patel D, Patel M (2020) Effect of abiotic stress on crops. In: Hasanuzzaman M, Fujita M, Teixeira Filho MCM (eds) Sustain Crop Prod. Intech, London. https://doi.org/10.5772/intechopen.88434

  • Yamazaki S, Ueda Y, Mukai A, Ochiai K, Matoh T (2018) Rice phytochelatin synthases Os PCS 1 and Os PCS 2 make different contributions to cadmium and arsenic tolerance. Plant Direct 2:e00034

    Google Scholar 

  • Yin L, Mano JI, Tanaka K, Wang S, Zhang M, Deng X, Zhang S (2017) High level of reduced glutathione contributes to detoxification of lipid peroxide-derived reactive carbonyl species in transgenic Arabidopsis overexpressing glutathione reductase under aluminum stress. Physiol Plant 161:211–223

    CAS  Google Scholar 

  • Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167:527–533

    CAS  Google Scholar 

Download references

Funding

This work was supported by University Research Scholarship (URS) contingency grant of University of Kalyani, West Bengal, India, and Department of Science and Technology, Govt. of India (DST-PURSE) Program, DST, New Delhi, activated to University of Kalyani, Nadias, West Bengal, India.

Author information

Authors and Affiliations

Authors

Contributions

M.K.A. and M.H. conceived and designed the experiments. D.D., I.S., and A.G. conducted the experiments. M.K.A. helped and supervised the experiments. M.H. and M.K.A analyzed the data and prepared the illustration. M.K.A. wrote the manuscript draft. M.H. revised, edited, and formatted the manuscript. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Mirza Hasanuzzaman or Malay Kumar Adak.

Ethics declarations

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Elena Maestri

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(DOCX 47 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dolui, ., Hasanuzzaman, ., Saha, I. et al. Amelioration of sodium and arsenic toxicity in Salvinia natans L. with 2,4-D priming through physiological responses. Environ Sci Pollut Res 29, 9232–9247 (2022). https://doi.org/10.1007/s11356-021-16246-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-16246-7

Keywords

Navigation