Skip to main content
SpringerLink
Log in

Ionomics and metabolomics analysis reveal the molecular mechanism of metal tolerance of Pteris vittata L. dominating in a mining site in Thai Nguyen province, Vietnam

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

Abstract

This study aims to find the interaction between ionome and metabolome profiles of Pteris vittata L., an arsenic hyperaccumulator plant, to reveal its metal tolerance mechanism. Therefore, at the Pb–Zn mining sites located in Thai Nguyen province, Vietnam, where these species dominate, soil and plant samples were collected. Their multi-element compositions were analyzed using inductively coupled plasma mass spectrometry (ICP-MS) and thus referred to as the “ionomics” approach. In parallel, the widely targeted metabolomics profiles of these plant samples were performed using liquid chromatography-tandem mass spectrometry (UPLC-QqQ-MS). Nineteen elements, including both metals and nonmetals, were detected and quantified in both tissues of thirty-five plant individuals. A comparison of these elements’ levels in two tissues showed that above-ground parts accumulated more As and inorganic P, whereas Zn, Pb, and Sb were raised mostly in the under-ground samples. The partial least squares regression (PLSR) model predicting the level of each element by the whole metabolome indicated that the enhancement of flavonoids content plays an essential contribution in adaptation with the higher levels of Pb, Ag, and Ni accumulated in the aerial part, and Mn, Pb in subterranean part. Moreover, the models also highlighted the effect of Mn and Pb on the metabolic induction of adenosine derivatives in subterranean parts. At the same time, the model presented the most contribution of As to the metabolisms of the amino acids of this tissue. On those accounts, the developed integration approach linking the ionomics and metabolomics data of P. vittata improved the understanding of the molecular mechanism of hyperaccumulation characteristics and provided markers that could be targeted in future investigations.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article (and its supplementary information files).

References

  • Abin S, Ashwini N, Majeti NVP, Ladawan R, Woranan N (2019) Cadmium toxicity and tolerance in micro- and phytobiomes. In: Mirza H, Majeti NVP, Masayuki F (eds) Cadmium toxicity and tolerance in plants. Academic Press, Massachusetts, pp 19–46

    Google Scholar 

  • Aitor V, Markel SN, Mara G, Pierre-Antoine A, Maitane O, Aresatz U, Nestor E, Oier AO (2021) Metabolomics as a prediction tool for plants performance under environmental stress. Plant Sci 303:110789

    Article  Google Scholar 

  • Ali B, Xu X, Gill RA, Yang S, Ali S, Tahir M et al (2014) Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. Ind Crop Prod 52:617–626

    Article  CAS  Google Scholar 

  • Alkorta I, Hernández-Allica J, Becerril JM, Amezaga I, Albizu I, Garbisu C (2004) Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic. Rev Environ Sci Biotechnol 3(1):71–90

    Article  CAS  Google Scholar 

  • An ZZ, Huang ZC, Lei M, Liao XY, Zheng YM, Chen TB (2006) Zinc tolerance and accumulation in Pteris vittata L. and its potential for phytoremediation of Zn- and As-contaminated soil. Chemosphere 62(5):796–802

    Article  CAS  Google Scholar 

  • Anguita-Maeso M, Haro C, Montes-Borrego M, Fuente LDL, Navas-Cortes JA, Landa BB (2021) Metabolomic, ionomic and microbial characterization of olive xylem sap reveals differences according to plant age and genotype. Argon 11(6):1179

    CAS  Google Scholar 

  • Bagherzadeh-Homaee M, Ehsanpour AA (2016) Silver nanoparticles and silver ions: oxidative stress responses and toxicity in potato (Solanum tuberosum L) grown in vitro. Hortic Environ Biotechnol 57:544–553

    Article  CAS  Google Scholar 

  • Banci L, Bertini I (2013) Metallomics and the cell: some definitions and general comments. Met Ions Life Sci 12:1–13

    Article  Google Scholar 

  • Bohm BA (1968) Phenolic compounds in ferns-III. An examination of some ferns for caffeic acid derivatives. Phytochem 7:1825–1830

    Article  CAS  Google Scholar 

  • Bohm BA, Tyron RM (1967) Phenolic compounds in ferns. I. A survey of some ferns for cinnamic and benzoic acid derivatives. Canad J Bot 45:585–593

    Article  CAS  Google Scholar 

  • Burke DG, Watkins K, Scott BJ (1990) Manganese toxicity effects on visible symptoms, yield, manganese levels, and organic acid levels in tolerant and sensitive wheat cultivars. Crop Sci. https://doi.org/10.2135/cropsci1990.0011183X003000020007x

    Article  Google Scholar 

  • Cai Y, Ma LQ (2003) Metal tolerance, accumulation, and detoxification in plants with emphasis on arsenic in terrestrial plants. In: Cai Y, Braids OC (eds) Biogeochemistry of environmentally important trace elements. American Chemical Society, Washington, pp 95–114

    Google Scholar 

  • Cao X, Ma LQ, Tu C (2004) Antioxidative responses to arsenic in the arsenic-hyperaccumulator Chinese brake fern (Pteris vittata L.). Environ Pollut 128(3):317–25

    Article  CAS  Google Scholar 

  • Cao H, Chai TT, Wang X, Morais-Braga MFB, Yang JH, Wong FC, Coutinho HDM (2017) Phytochemicals from fern species: potential for medicine applications. Phytochem Rev 16(3):379–440

    Article  CAS  Google Scholar 

  • Catarecha P, Segura MD, Franco-Zorrilla JM, García-Ponce B, Lanza M, Solano R, Paz-Ares J, Leyva A (2007) A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell 19:1123–1133

    Article  CAS  Google Scholar 

  • Chatterjee C, Dube BK, Sinha P, Srivastava P (2004) Detrimental effects of lead phytotoxicity on growth, yield, and metabolism of rice. Commun Soil Sci Plant Anal 35:255–265

    Article  CAS  Google Scholar 

  • Da ES, Lessl JT, Wilkie AC, Liu X, Liu Y, Ma LQ (2018) Arsenic removal by As hyperaccumulator Pteris vittata from two contaminated soils: a 5-year study. Chemosphere 206:736–741

    Article  Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097

    Article  CAS  Google Scholar 

  • Dubey S, Misra P, Dwivedi S, Chatterjee S, Bag SK, Mantri S, Asif MH, Rai A, Kumar S, Shri M, Tripathi P, Tripathi RD, Trivedi PK, Chakrabarty D, Tuli R (2010) Transcriptomic and metabolomic shifts in rice roots in response to Cr (VI) stress. BMC Genomics 11(1):648

    Article  Google Scholar 

  • Escande V, Olszewski TK, Grison C (2014) Preparation of ecological catalysts derived from Zn hyperaccumulating plants and their catalytic activity in Diels-Alder reaction. Compt Rend Chimie 17:731–737

    Article  CAS  Google Scholar 

  • Escande V, Olszewski TK, Grison C (2015) From biodiversity to catalytic diversity: how to control the reaction mechanism by the nature of metallophytes. Environ Sci Pollut Res 22:5653–5666

    Article  CAS  Google Scholar 

  • Farres M, Pina B, Tauler R (2016) LC-MS based metabolomics and chemometrics study of the toxic effects of copper on Saccharomyces cerevisiae. Metallomics 8:790–798

    Article  CAS  Google Scholar 

  • Fu JW, Liu X, Han YH, Mei H, Cao Y, Oliveira LMD, Liu Y, Rathinasabapathi B, Chen Y, Ma LQ (2017) Arsenic-hyperaccumulator Pteris vittata efficiently solubilized phosphate rock to sustain plant growth and As uptake. J Hazard Mater 330:68–75

    Article  CAS  Google Scholar 

  • Gajewska E, Skłodowska M (2007) Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. Biometals 20:27–36

    Article  CAS  Google Scholar 

  • González E, Solano R, Rubio V, Leyva A, Paz-Ares J (2005) Phosphate transporter traffic facilitator1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. Plant Cell 17:3500–3512

    Article  Google Scholar 

  • Hair JF, Ringle CM, Sarstedt M (2011) PLS-SEM: indeed a silver bullet. J Mark Theory Pract 19(2):139–151

    Article  Google Scholar 

  • Hediji H, Djebali W, Cabasson C, Maucourt M, Baldet P, Bertrand A, Boulila ZL, Deborde C, Moing A, Brouquisse R, Chaıbi W, Gallusci P (2010) Effects of long-term cadmium exposure on growth and metabolomic profile of tomato plants. Ecotoxicol Environ Saf 73:1965–1974

    Article  CAS  Google Scholar 

  • Ho R, Teai T, Bianchini JP, Lafont R, Raharivelomanana P (2011) Ferns: from traditional uses to pharmaceutical development, chemical identification of active principles. In: Fernández H, Kumar A, Revilla MA (eds) Working with ferns. Springer, New York, pp 321–346

    Chapter  Google Scholar 

  • Hong J, Yang L, Zhang D, Shi J (2016) Plant metabolomics: an indispensable system biology tool for plant science. Int J Mol Sci 17(6):767

    Article  Google Scholar 

  • Knowles V, Plaxton W (2013) Quantification of total and soluble inorganic phosphate. Bio Protoc 3(17):e890

    Article  Google Scholar 

  • Kochian LV, Pineros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274(1–2):175–195

    Article  CAS  Google Scholar 

  • Kohda YHT, Qian Z, Chien MF, Miyauchi K, Endo G, Suzui N, Yin YG, Kawachi N, Ikwda H, Watabe H, Kikunaga H, Kitajima N, Inoue C (2021) New evidence of arsenic translocation and accumulation in Pteris vittata from real-time imaging using positron-emitting 74As tracer. Sci Rep 11:12149

    Article  CAS  Google Scholar 

  • Kohli SK, Handa N, Bali S, Khanna K, Arora S., Sharma A, Bhardwaj R (2019) Current scenario of Pb toxicity in plants: unraveling plethora of physiological responses. In: De-Voogt P (ed) Reviews of environmental contamination and toxicology, volume 249. Reviews of environmental contamination and toxicology (continuation of residue reviews), Springer, Cham. https://doi.org/10.1007/398_2019_25

  • Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25(1):1–18

    Article  Google Scholar 

  • Liu C, Mm L, Ek He, Aj Y, Gb W, Yt T (2021) Phenomic and metabolomic responses of roots to cadmium reveal contrasting resistance strategies in two rice cultivars (Oryza sativa L.). Soil Ecol Lett 3:220–229

    Article  CAS  Google Scholar 

  • Luo X, Meng J, Chen X, Cheng L, Yan S, Gao L, Xue M, Yang Y (2020) Metabolomics-based study reveals the effect of lead (Pb) in the culture environment on Whitmania pigra. Sci Rep 10:4794

    Article  CAS  Google Scholar 

  • Ma LQ, Komar KM, Tu C, Zhang W, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579. https://doi.org/10.1038/35054664

    Article  CAS  Google Scholar 

  • Macfie SM, Cossins EA, Taylor GJ (1994) Effects of excess manganese on production of organic acids in Mn-tolerant and Mn-sensitive cultivars of Triticum aestivum L. (wheat). J Plant Physiol 143(2):135–144. https://doi.org/10.1016/S0176-1617(11)81677-9

    Article  CAS  Google Scholar 

  • Mendoza-Wilson AM, Castro-Arredondo SI, Espinosa-Plascencia A et al (2016) Chemical composition and antioxidant-prooxidant potential of a polyphenolic extract and a proanthocyanidin-rich fraction of apple skin. Heliyon 2:e00073. https://doi.org/10.1016/j.heliyon.2016.e00073

    Article  Google Scholar 

  • Munne-Bosch S, Penuelas J (2003) Photo and antioxidative protection, and a role for salicylic acid during drought and recovery in field grown Phillyrea angustifolia plants. Planta 217:758–766

    Article  CAS  Google Scholar 

  • Navarro-Reig M, Jaumot J, Piña B, Moyano E, Galceran MT, Tauler R (2017) Metabolomic analysis of the effects of cadmium and copper treatment in Oryza sativa L. using untargeted liquid chromatography coupled to high resolution mass spectrometry and all-ion fragmentation. Metallomics 9(6):660–675 (21)

    Article  CAS  Google Scholar 

  • Nguyen NL, Vu CT, To HM, Pham HN, Nguyen HD, Nguyen TD, Nguyen TKO (2020) The interactions among the heavy metals in soils and in weeds and their antioxidant capacity under the mining activities in Thai Nguyen province, Vietnam. J Chem 8010376

  • Nguyen TKO, Nguyen NL, Pham HN et al (2021) Development of a Pteris vittata L. compound database by widely targeted metabolomics profiling. Biomed Chromatogr. https://doi.org/10.1002/bmc.5110

    Article  Google Scholar 

  • Noel JP, Austin MB, Bomati EK (2005) Structure–function relationships in plant phenylpropanoid biosynthesis. Curr Opin Plant Biol 8:249–253

    Article  CAS  Google Scholar 

  • Pham HN, Michalet S, Bodillis J, Nguyen TD, Nguyen TKO, Le TPQ, Haddad M, Nazaret S, Dijoux-Franca MG (2017) Impact of metal stress on the production of secondary metabolites in Pteris vittata L. and associated rhizosphere bacterial communities. Environ Science Pollut Res 24(20):16735–16750

    Article  CAS  Google Scholar 

  • Qureshi M, Abdin M, Qadir S, Iqbal M (2007) Lead-induced oxidative stress and metabolic alterations in Cassia angustifolia Vahl. Biol Plantarum 51:121–128

    Article  CAS  Google Scholar 

  • Raza A (2020) Metabolomics: a systems biology approach for enhancing heat stress tolerance in plants. Plant Cell Rep. https://doi.org/10.1007/s00299-020-02635-8

    Article  Google Scholar 

  • Reeves RD (2006) Hyperaccumulation of trace elements by plants. In: Morel JL et al (eds) Phytoremediation of metal-contaminated soils. Springer, New York, pp 25–52

    Chapter  Google Scholar 

  • Rohart F, Gautier B, Singh A, Lê Cao KA (2017) mixOmics: an R package for ‘omics feature selection and multiple data integration. PLoS Comput Biol 13(11):e1005752. https://doi.org/10.1371/journal.pcbi.1005752

    Article  CAS  Google Scholar 

  • Salido AL, Hasty KL, Lim JM, Butcher DJ (2003) Phytoremediation of arsenic and lead in contaminated soil using Chinese brake ferns (Pteris vittata) and Indian mustard (Brassica juncea). Int J Phytoremediation 5(2):89–103

    Article  CAS  Google Scholar 

  • Salt DE, Baxter I, Lahner B (2008) Ionomics and the study of the plant ionome. Annu Rev Plant Biol 59:709–733

    Article  CAS  Google Scholar 

  • Sevillano GMA, Barrera GT, Roldán NFJ, Lobato MZ, Ariza GJL (2014) A combination of metallomics and metabolomics studies to evaluate the effects of metal interactions in mammals. Application to Mus musculus mice under arsenic/cadmium exposure. J Proteom 104:66–79

    Article  Google Scholar 

  • Sheila MM, Edwin AC, Gregory JT (1994) Effects of excess manganese on production of organic acids in Mn-tolerant and Mn-sensitive cultivars of Triticum aestivum L. (Wheat). J Plant Physiol 143(2):135–144

    Article  Google Scholar 

  • Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39:629–642. https://doi.org/10.1111/j.1365-313X.2004.02161.x

    Article  CAS  Google Scholar 

  • Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci. 6:1143. Published 2016 Feb 8. https://doi.org/10.3389/fpls.2015.01143

  • Soongsombat P, Kruatrachue M, Chaiyarat R, Pokethitiyook P, Ngernsansaruay C (2009) Lead tolerance and accumulation in Pteris vittata and Pityrogramma calomelanos and their potential for phytoremediation of lead-contaminated soil. Int J Phytoremediation 11(4):396–412

    Article  CAS  Google Scholar 

  • Souri MK, Hatamian M, Tesfamariam, (2019) Plant growth stage infuences heavy metal accumulation in leafy vegetables of garden cress and sweet basil. Chem Biol Technol Agric 6:25

    Article  CAS  Google Scholar 

  • Sun X, Zhang J, Zhang H, Ni Y, Zhang Q, Chen J, Guan Y (2010) The responses of Arabidopsis thaliana to cadmium exposure explored via metabolite profiling. Chemosphere 78(7):840–845

    Article  CAS  Google Scholar 

  • Tavassoly I, Goldfarb J, Iyengar R (2018) Systems biology primer: the basic methods and approaches. Essays Biochem 62(4):487–500

    Article  Google Scholar 

  • Tu C, Ma LQ, Bhaskar B (2002) Arsenic accumulation in the hyperaccumulator Chinese brake and its utilization potential for phytoremediation. J Environ Qual 31:1671e1675

    Article  Google Scholar 

  • Wagner S, Hoefer C, Puschenreiter M, Wenzel WW, Oburger E, Hann S, Robinson B, Kretzschmar R, Santner J (2020) Arsenic redox transformations and cycling in the rhizosphere of Pteris vittata and Pteris quadriaurita. Environ Exp Bot 177:104122

    Article  CAS  Google Scholar 

  • Wickham H (2016). ggplot2: elegant graphics for data analysis. Springer-Verlag New York. https://ggplot2.tidyverse.org

  • Wu Z, Ren H, McGrath SP, Wu P, Zhao FJ (2011) Investigating the contribution of the phosphate transport pathway to arsenic accumulation in rice. Plant Physiol 157:498–508

    Article  CAS  Google Scholar 

  • Xia X, Cao J, Zheng Y, Wang Q, Xiao J (2014) Flavonoid concentrations and bioactivity of flavonoid extracts from 19 species of ferns from China. Ind Crops Prod 58:91–98

    Article  CAS  Google Scholar 

  • Xiao X, Chen T, An Z, Lei M, Huang Z, Liao X, Liu Y (2008) Potential of Pteris vittata L. for phytoremediation of sites co-contaminated with cadmium and arsenic: the tolerance and accumulation. J Environ Sci 20(1):62–67

    Article  Google Scholar 

  • Yasseen BT, Al-Thani RF (2013) Ecophysiology of wild plants and conservation perspectives in the State of Qatar. In: Stoytcheva M, Zlatev R (eds) Agricultural chemistry. InTech, Croatia, p 210

    Google Scholar 

  • Zhang H, Du W, Peralta-Videa JR, Gardea-Torresdey JL, White JC, Keller A, Guo H, Ji R, Zhao L (2018) Metabolomics reveals how cucumber (Cucumis sativus) reprograms metabolites to cope with silver ions and silver nanoparticle-induced oxidative stress. Environ Sci Technol 52(14):8016–8026

    Article  CAS  Google Scholar 

  • Zoghlami LB, Djebali W, Abbes Z, Hediji H, Maucourt M, Moing A, Brouquisse R, Chaıbi M (2011) Metabolite modifications in Solanum lycopersicum roots and leaves under cadmium stress. Afr J Biotechnol 10:567–579

    CAS  Google Scholar 

Download references

Acknowledgements

The corresponding author gratefully acknowledges Dr. Rebecca Dauwe (EA3900 BioPI, UFR Sciences, Université de Picardie Jules Verne, 33 rue Saint Leu, 80039 Amiens Cedex, France) for her advice in data treatment and statistical analysis and Laboratoire Mixte International—“Drug Resistance in Southeast Asia” (LMI-DRISA) for a financial contribution to the activity of our analytical platform.

Funding

This research is funded by the University of Science and Technology of Hanoi (USTH) under grant number USTH.LS.01/22–24.

Author information

Authors and Affiliations

  1. Department of Life Sciences, University of Science and Technology of Hanoi, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam

    Ngoc-Lien Nguyen, Hoang-Nam Pham, Hien-Minh To & Kieu-Oanh Thi Nguyen

  2. Department of Water, Environment, Oceanography, University of Science and Technology of Hanoi, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam

    Van-Hoi Bui & Cam-Tu Vu

  3. UMR 5557, Ecologie Microbienne, CNRS, INRA, VetagroSup, UCBL, Université de Lyon, 43 Boulevard du 11 Novembre, 69622, Villeurbanne, France

    Marie-Geneviève Dijoux-Franca

Authors
  1. Ngoc-Lien Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Van-Hoi Bui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hoang-Nam Pham
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hien-Minh To
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marie-Geneviève Dijoux-Franca
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cam-Tu Vu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kieu-Oanh Thi Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Kieu-Oanh Nguyen Thi and Marie-Geneviève Dijoux-Franca contributed to the study conception and design. Material collection, sample preparation, and analysis were performed by Ngoc-Lien Nguyen, Van-Hoi Bui, Hien-Minh To, and Hoang-Nam Pham. Data treatment and statistical analysis were done by Cam-Tu Vu and Kieu-Oanh Nguyen Thi. The first draft of the manuscript was written by Kieu-Oanh Nguyen Thi, and all authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Kieu-Oanh Thi Nguyen.

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: Gangrong Shi

Publisher's note

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

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nguyen, NL., Bui, VH., Pham, HN. et al. Ionomics and metabolomics analysis reveal the molecular mechanism of metal tolerance of Pteris vittata L. dominating in a mining site in Thai Nguyen province, Vietnam. Environ Sci Pollut Res 29, 87268–87280 (2022). https://doi.org/10.1007/s11356-022-21820-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-21820-8

Keywords

Search

Navigation