Skip to main content
SpringerLink
Log in

Influence of Pseudomonas japonica and organic amendments on the growth and metal tolerance of Celosia argentea L.

  • Recent Advances and Novel Concepts in Environmental Technologies
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

In this study, a pot experiment was piloted in a greenhouse to evaluate the potential of Celosia argentea var. cristata L. for tolerating/accumulating heavy metals in synthetic wastewater in the presence of Pseudomonas japonica and organic amendment, i.e., moss and compost. Two-week-old seedlings were transferred to pots, and after 4 weeks, the bacterial strain was inoculated, then watered with synthetic wastewater for 5 weeks and harvested after 9 weeks. After harvesting, physiological and biochemical parameters, as well as metal contents of plants, were quantified. The results indicated highest growth and biomass production in moss- and compost-associated plants while highest metal uptake has been found in the presence of P. japonica and synthetic wastewater–irrigated plants. Synthetic wastewater–irrigated plants have shown highest Pb uptake of 2899 mg kg−1 DW, while with P. japonica in soil those plants have shown highest Cd, Cu, Ni, and Cr uptake of 962, 1479, 1042, and 956 mg kg−1 DW, respectively. The production of antioxidant enzymes, i.e., catalase (CAT), ascorbate peroxidase (APX), guaiacol peroxidase (GPX), and glutathione-s-transferase (GST), was high in P. japonica–amended plants because of increased uptake of metals. It is concluded that moss and compost have improved growth while P. japonica improved metal accumulation and translocation to aerial parts with little involvement in plant growth.

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
Fig. 3

Similar content being viewed by others

References

  • Adeleke R, Nwangburuka C, Oboirien B (2017) Origins, roles, and the fate of organic acids in soils: a review. S Afr J Bot 108:393–406

    CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    CAS  Google Scholar 

  • Arshad M, Khan AH, Hussain I, Anees M, Iqbal M, Soja G, Linde C, Yousaf S (2017) The reduction of chromium (VI) phytotoxicity and phytoavailability to wheat (Triticum aestivum L.) using biochar and bacteria. Appl Soil Ecol 114:90–98

    Google Scholar 

  • Bao T, Sun T, Sun L (2011) Low molecular weight organic acids in root exudates and cadmium accumulation in cadmium hyperaccumulator Solanum nigrum L. and non hyperaccumulator Solanum lycopersicum L. Afr J Biotechnol 10:17180–17185

    CAS  Google Scholar 

  • Boechat CL, Giovanella P, Amorim MB, de Sá ELS, de Oliveira Camargo FA (2017) Metal-resistant rhizobacteria isolates improve Mucuna deeringiana phytoextraction capacity in multi-metal contaminated soils from a gold mining area. Environ Sci Pollut Res 24:3063–3073

    CAS  Google Scholar 

  • Bücker-Neto L, Paiva ALS, Machado RD, Arenhart RA, Margis-Pinheiro M (2017) Interactions between plant hormones and heavy metals responses. Genet Mol Biol 40:373–386

    Google Scholar 

  • Chaudhary K, Agarwal S, Khan S (2018) Role of phytochelatins (PCs), metallothioneins (MTs), and heavy metal ATPase (HMA) genes in heavy metal tolerance. In: Mycoremediation and Environmental Sustainability. Springer, pp 39–60

  • Chen G-X, Asada K (1989) Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol 30:987–998

    CAS  Google Scholar 

  • Davenport SB, Gallego SM, Benavides MP, Tomaro ML (2003) Behaviour of antioxidant defense system in the adaptive response to salt stress in Helianthus annuus L. cells. Plant Growth Regul 40:81–88

  • Ding W, Clode PL, Lambers H (2019) Effects of pH and bicarbonate on the nutrient status and growth of three Lupinus species. Plant Soil:1–20

  • Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1109

    CAS  Google Scholar 

  • Dzantor EK (2007) Phytoremediation: the state of rhizosphere ‘engineering’ for accelerated rhizodegradation of xenobiotic contaminants. J Chem Technol Biotechnol 82:228–232

    CAS  Google Scholar 

  • Estefan G, Sommer R, Ryan J (2013) Methods of soil, plant, and water analysis. A manual for the West Asia and North Africa Region. 89:170–176

  • González-Valdez E, Alarcón A, Ferrera-Cerrato R, Vega-Carrillo HR, Maldonado-Vega M, Salas-Luévano MÁ (2016) Seed germination and seedling growth of five plant species for assessing potential strategies to stabilizing or recovering metals from mine tailings. Water Air Soil Pollut 227:1–10

    Google Scholar 

  • Gupta P, Rani R, Chandra A, Kumar V (2018) Potential applications of Pseudomonas sp.(strain CPSB21) to ameliorate Cr6+ stress and phytoremediation of tannery effluent contaminated agricultural soils. Sci Rep 8:4860

    Google Scholar 

  • Hadi F, Bano A, Fuller MP (2010) The improved phytoextraction of lead (Pb) and the growth of maize (Zea mays L.): the role of plant growth regulators (GA3 and IAA) and EDTA alone and in combinations. Chemosphere 80:457–462

    CAS  Google Scholar 

  • Hojati M, Modarres-Sanavy SAM, Enferadi ST, Majdi M, Ghanati F, Farzadfar S, Pazoki A (2017) Cadmium and copper induced changes in growth, oxidative metabolism, and terpenoids of Tanacetum parthenium. Environ Sci Pollut Res 24:12261–12272

    CAS  Google Scholar 

  • Jaskulak M, Rorat A, Grobelak A, Chaabene Z, Kacprzak M, Vandenbulcke F (2019) Bioaccumulation, antioxidative response, and metallothionein expression in Lupinus luteus L. exposed to heavy metals and silver nanoparticles. Environ Sci Pollut Res 16:1–13

    Google Scholar 

  • Kalsotra T, Khullar S, Agnihotri R, Reddy MS (2018) Metal induction of two metallothionein genes in the ectomycorrhizal fungus Suillus himalayensis and their role in metal tolerance. Microbiology 164:868–876

    CAS  Google Scholar 

  • Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2015a) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18

    CAS  Google Scholar 

  • Khan AR, Ullah I, Khan AL, Park GS, Waqas M, Hong SJ, Jung BK, Kwak Y, Lee IJ, Shin JH (2015b) Improvement in phytoremediation potential of Solanum nigrum under cadmium contamination through endophytic-assisted Serratia sp. RSC-14 inoculation. Environ Sci Pollut Res 22:14032–14042

    CAS  Google Scholar 

  • Khan AHA, Tanveer S, Anees M, Muhammad YS, Iqbal M, Yousaf S (2016a) Role of nutrients and illuminance in predicting the fate of fungal mediated petroleum hydrocarbon degradation and biomass production. J Environ Manag 176:54–60

    Google Scholar 

  • Khan AHA, Anees M, Arshad M, Muhammad YS, Iqbal M, Yousaf S (2016b) Effects of illuminance and nutrients on bacterial photo-physiology of hydrocarbon degradation. Sci Total Environ 557:705–711

    Google Scholar 

  • Khan AHA, Butt TA, Mirza CR, Yousaf S, Nawaz I, Iqbal M (2019) Combined application of selected heavy metals and EDTA reduced the growth of Petunia hybrida L. Sci Rep 9:4138

    Google Scholar 

  • Koptsik G (2014) Problems and prospects concerning the phytoremediation of heavy metal polluted soils: a review. Eurasian Soil Sci 47:923–939

    CAS  Google Scholar 

  • Lajayer BA, Moghadam NK, Maghsoodi MR, Ghorbanpour M, Kariman K (2019) Phytoextraction of heavy metals from contaminated soil, water, and atmosphere using ornamental plants: mechanisms and efficiency improvement strategies. Environ Sci Pollut Res 26:1–17

    Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    CAS  Google Scholar 

  • Liu J, Shi X, Qian M, Zheng L, Lian C, Xia Y, Shen Z (2015) Copper-induced hydrogen peroxide upregulation of a metallothionein gene, OsMT2c, from Oryza sativa L. confers copper tolerance in Arabidopsis thaliana. J Hazard Mater 294:99–108

    CAS  Google Scholar 

  • Liu J, Xin X, Zhou Q (2017) Phytoremediation of contaminated soils using ornamental plants. Environ Rev 26:43–54

    Google Scholar 

  • Maehly A, Chance B (1954) Methods of biochemical analysis by Glick D. Interscience, New York

    Google Scholar 

  • Man YB, Chung AKC, Wong MH (2016) Changes in low molecular weight organic acids and antioxidative enzyme activities of wetland plants under metal stresses. Environ Eng Manag J 15:1657–1663

    CAS  Google Scholar 

  • Marzilli M, Di Santo P, Palumbo G, Maiuro L, Paura B, Tognetti R, Cocozza C (2018) Cd, and Cu accumulation, translocation and tolerance in Populus alba clone (Villafranca) in autotrophic in vitro screening. Environ Sci Pollut Res 25:10058–10068

    CAS  Google Scholar 

  • Michael PI, Krishnaswamy M (2011) The effect of zinc stress combined with high irradiance stress on membrane damage and antioxidative response in bean seedlings. Environ Exp Bot 74:171–177

    CAS  Google Scholar 

  • Mishra R, Datta SP, Annapurna K, Meena MC, Dwivedi BS, Golui D, Bandyopadhyay K (2019) Enhancing the effectiveness of zinc, cadmium, and lead phytoextraction in polluted soils by using amendments and microorganisms. Environ Sci Pollut Res 26:1–12

    Google Scholar 

  • Nadeem SM, Imran M, Naveed M, Khan MY, Ahmad M, Zahir ZA, Crowley DE (2017) Synergistic use of biochar, compost and plant growth-promoting rhizobacteria for enhancing cucumber growth under water deficit conditions. J Sci Food Agric 97:5139–5145

    CAS  Google Scholar 

  • Singh RP, Jha PN (2018) Priming with ACC-utilizing bacterium attenuated copper toxicity, improved oxidative stress tolerance, and increased phytoextraction capacity in wheat. Environ Sci Pollut Res 25:33755–33767

    CAS  Google Scholar 

  • Stancheva I, Geneva M, Hristozkova M, Markovska Y, Salamon I (2010) Antioxidant capacity of sage grown on heavy metal-polluted soil. Russ J Plant Physiol 57:799–805

    CAS  Google Scholar 

  • Stanislawska-Glubiak E, Korzeniowska J, Kocon A (2015) Effect of peat on the accumulation and translocation of heavy metals by maize grown in contaminated soils. Environ Sci Pollut Res 22:4706–4714

    CAS  Google Scholar 

  • Sytar O, Kumari P, Yadav S, Brestic M, Rastogi A (2018) Phytohormone priming: a regulator for heavy metal stress in plants. J Plant Growth Regul 38:739–752

    Google Scholar 

  • Tandon S, Kumar R, Parsana S (2015) Auxin treatment of wetland and non-wetland plant species to enhance their phytoremediation efficiency to treat municipal wastewater. J Sci Ind Res 74:702–707

    CAS  Google Scholar 

  • Upadhyaya A, Sankhla D, Davis TD, Sankhla N, Smith B (1985) Effect of paclobutrazol on the activities of some enzymes of activated oxygen metabolism and lipid peroxidation in senescing soybean leaves. J Plant Physiol 121:453–461

    CAS  Google Scholar 

  • Venkatachalam P, Priyanka N, Manikandan K, Ganeshbabu I, Indiraarulselvi P, Geetha N, Muralikrishna K, Bhattacharya RC, Tiwari M, Sharma N, Sahi SV (2017) Enhanced plant growth promoting the role of phycomolecules coated zinc oxide nanoparticles with P supplementation in cotton (Gossypium hirsutum L.). Plant Physiol Biochem 110:118–127

    CAS  Google Scholar 

  • Wang S, Zhao Y, Guo J, Liu Y (2018) Antioxidative response in leaves and allelochemical changes in root exudates of Ricinus communis under Cu, Zn, and Cd stress. Environ Sci Pollut Res 25:32747–32755

    CAS  Google Scholar 

  • Xu P, Han N, Kang T, Zhan S, Lee KS, Jin BR, Li J, Wan H (2016) SeGSTo, a novel glutathione S-transferase from the beet armyworm (Spodoptera exigua), involved in detoxification and oxidative stress. Cell Stress Chaperones 21:805–816

    CAS  Google Scholar 

  • Xu X, Yang B, Qin G, Wang H, Zhu Y, Zhang K, Yang H (2019) Growth, accumulation, and antioxidative responses of two Salix genotypes exposed to cadmium and lead in hydroponic culture. Environ Sci Pollut Res 26:19770–19784

    CAS  Google Scholar 

  • Yahmed JB, de Oliveira TM, Novillo P, Quinones A, Forner MA, Salvador A, Froelicher Y, Mimoun MB, Talon M, Ollitrault P, Morillon R (2016) A simple, fast and inexpensive method to assess salt stress tolerance of aerial plant part: Investigations in the mandarin group. J Plant Physiol 190:36–43

    Google Scholar 

  • Yang Z, Chen J, Dou R, Gao X, Mao C, Wang L (2015) Assessment of the phytotoxicity of metal oxide nanoparticles on two crop plants, maize (Zea mays L.) and rice (Oryza sativa L.). Int J Environ Res Public Health 12:15100–15109

    CAS  Google Scholar 

  • Yang Z, Liu L, Lv Y, Cheng Z, Xu X, Xian J, Zhu X, Yang Y (2018) Metal availability, soil nutrient, and enzyme activity in response to the application of organic amendments in Cd-contaminated soil. Environ Sci Pollut Res 25:2425–2435

    CAS  Google Scholar 

  • Zhang X, Li M, Yang H, Li X, Cui Z (2018) Physiological responses of Suaeda glauca and Arabidopsis thaliana in phytoremediation of heavy metals. J Environ Manag 223:132–139

    CAS  Google Scholar 

  • Zhong L, Lin L, Liao M, Wang J, Tang Y, Sun G, Liang D, Xia H, Wang X, Zhang H, Ren W (2019) Phytoremediation potential of Pterocypsela laciniata as a cadmium hyperaccumulator. Environ Sci Pollut Res 26:13311–13319

    CAS  Google Scholar 

Download references

Author information

Author notes

  1. Ameena Iqbal and Muhammad Umair Mushtaq contributed equally to this work.

Authors and Affiliations

  1. Department of Environmental Sciences, Faculty of Biological Sciences, Quaid-i-Azam University, Islamabad, 45320, Pakistan

    Ameena Iqbal, Muhammad Umair Mushtaq, Aqib Hassan Ali Khan, Sohail Yousaf & Mazhar Iqbal

  2. Department of Biotechnology, COMSATS University Islamabad, Abbottabad Campus, Abbottabad, 22060, Pakistan

    Ismat Nawaz

  3. Institute of Environmental Sciences and Engineering (IESE), School of Civil and Environmental Engineering (SCEE), National University of Sciences and Technology (NUST), Islamabad, 44000, Pakistan

    Zeshan

Authors
  1. Ameena Iqbal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Muhammad Umair Mushtaq
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aqib Hassan Ali Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ismat Nawaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sohail Yousaf
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zeshan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mazhar Iqbal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mazhar Iqbal.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Elena Maestri

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 28 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iqbal, A., Mushtaq, M.U., Khan, A.H.A. et al. Influence of Pseudomonas japonica and organic amendments on the growth and metal tolerance of Celosia argentea L.. Environ Sci Pollut Res 27, 24671–24685 (2020). https://doi.org/10.1007/s11356-019-06181-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-06181-z

Keywords

Search

Navigation