Skip to main content
SpringerLink
Log in

Corona discharge plasma stimulated production of atropine in callus of Datura inoxia by DNA hypomethylation and gene regulation: a novel technology for plant cell and tissue culture

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Few investigations have tested the practical use of cold plasma as a novel technology to meet the requirements in the plant cell and tissue culture field. To fill the knowledge gap, we intend to respond to the question of whether plasma priming influenced DNA ultrastructure and the production of atropine (a tropane alkaloid) in Datura inoxia. Calluses were treated with the corona discharge plasma at time durations ranging from 0 to 300 s. Significant increases (about 60%) in biomass were observed in the plasma-primed calluses. The plasma priming of calluses enhanced the accumulation of atropine about 2-fold. The plasma treatments increased proline concentrations and soluble phenols. The drastic increases in the activity of the phenylalanine ammonia-lyase (PAL) enzyme resulted from the applied treatments. Likewise, the plasma treatment of 180 s upregulated the expression of the PAL gene by 8-fold. Also, the expression of the ornithine decarboxylase (ODC) and tropinone reductase I (TR I) genes were stimulated by 4.3-fold and 3.2-fold, respectively, in response to the plasma treatment. The putrescine N-methyltransferase gene displayed a similar trend to that of TR I and ODC genes following the plasma priming. Methylation sensitive amplification polymorphism method was employed to explore the plasma-associated epigenetic changes in DNA ultrastructure. The molecular assessment referred to DNA hypomethylation, validating an epigenetic response. This biological assessment study validates the hypothesis that plasma priming of callus is an efficient, cost-effective, and eco-friendly tool to enhance callogenesis efficiency, elicit metabolism, affect gene regulation, and modify chromatin ultrastructure in D. inoxia.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The datasets used in this study are available upon reasonable request from the corresponding author.

References

  • Amini M, Momeni M, Jahandideh A, Ghoranneviss M, Soudmand S, Yousefi P, Khandan S, Amini M (2021) Tendon repair by plasma jet treatment. J Diabetes Metab Disord 20(1):621–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asgari-Targhi G, Iranbakhsh A, Ardebili ZO, Tooski AH (2021) Synthesis and characterization of chitosan encapsulated zinc oxide (ZnO) nanocomposite and its biological assessment in pepper (Capsicum annuum) as an elicitor for in vitro tissue culture applications. Int J Biol Macromol 189:170–182. https://doi.org/10.1016/j.ijbiomac.2021.08.117

    Article  CAS  PubMed  Google Scholar 

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

  • Darigh F, Iranbakhsh A, OraghiArdebili Z, Ebadi M (2022) Non-thermal plasma improved callogenesis performance and elicited the production of cannabinoids by modifying DNA methylome, expression of WRKY1 and ERF1B transcription factors, and expression of genes that contributed to biosynthesis of cannabinoids. Protoplasma. https://doi.org/10.1007/s00709-022-01769-8

    Article  PubMed  Google Scholar 

  • Ebrahimibasabi E, Ebrahimi A, Momeni M and reza Amerian M (2020) Elevated expression of diosgenin-related genes and stimulation of the defense system in Trigonella foenum-graecum (Fenugreek) by cold plasma treatment. Scientia Horticulturae. 271. https://doi.org/10.1016/j.scienta.2020.109494

  • Ghasempour M, Iranbakhsh A, Ebadi M, OraghiArdebili Z (2020) Seed priming with cold plasma improved seedling performance, secondary metabolism, and expression of deacetylvindoline O-acetyltransferase gene in Catharanthus roseus. Contrib Plasma Phys. https://doi.org/10.1002/ctpp.201900159

    Article  Google Scholar 

  • Guevara MÁ, de María N, Sáez-Laguna E, Vélez MD, Cervera MT, Cabezas JA (2017) Analysis of DNA cytosine methylation patterns using methylation-sensitive amplification polymorphism (MSAP). Plant Epigenetics: Methods and Protocols 99-112

  • Han B, Yu NN, Zheng W, Zhang LN, Liu Y, Yu JB, Zhang YQ, Park G, Sun HN, Kwon T (2021) Effect of non-thermal plasma (NTP) on common sunflower (Helianthus annus L.) seed growth via upregulation of antioxidant activity and energy metabolism-related gene expression. Plant Growth Regul 95(2):271–281

    Article  CAS  Google Scholar 

  • Harfi B, Khelifi L, Khelifi-Slaoui M et al (2018) Tropane alkaloids GC/MS analysis and low dose elicitors’ effects on hyoscyamine biosynthetic pathway in hairy roots of Algerian Datura species. Sci Rep 8:17951. https://doi.org/10.1038/s41598-018-36625-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He F, Shen H, Lin C, Fu H, Sheteiwy MS, Guan Y, Huang Y, Hu J (2017) Transcriptome analysis of chilling-imbibed embryo revealed membrane recovery related genes in maize. Front Plant Sci 7:1978

    Article  PubMed  PubMed Central  Google Scholar 

  • Hirano I, Iida H, Ito Y, Park HD, Takahashi K (2019) Effects of light conditions on growth and defense compound contents of Datura inoxia and D. stramonium. J Plant Res 132(4):473–480

    Article  CAS  PubMed  Google Scholar 

  • Hu Q, Fu Y, Guan Y, Lin C, Cao D, Hu W, Sheteiwy M, Hu J (2016) Inhibitory effect of chemical combinations on seed germination and pre-harvest sprouting in hybrid rice. Plant Growth Regul 80:281–289

    Article  CAS  Google Scholar 

  • Hu Q, Lin C, Guan Y, Sheteiwy MS, Hu W, Hu J (2017) Inhibitory effect of eugenol on seed germination and pre-harvest sprouting of hybrid rice (Oryza sativa L.). Scientific Reports 7(1):1–9

    Google Scholar 

  • Iranbakhsh A, Ardebili ZO, Ardebili NO (2021) Gene regulation by NO in plants. In: Singh, Durgesh Tripathi, Maria Romero-Puertas, Luisa Sandalio (ed) Nitric Oxide in Plant Biology, 1st edn. Academic Press, Elsevier, Chapter 27; https://doi.org/10.1016/B978-0-12-818797-5.00006-6

  • Judickaitė A, Lyushkevich V, Filatova I, Mildažienė V, Žūkienė R (2022) The potential of cold plasma and electromagnetic field as stimulators of natural sweeteners biosynthesis in Stevia rebaudiana Bertoni. Plants 11(5):611. https://doi.org/10.3390/plants11050611

  • Lee Y, Lee YY, Kim YS, Balaraju K, Mok YS, Yoo SJ, Jeon Y (2021) Enhancement of seed germination and microbial disinfection on ginseng by cold plasma treatment. J Ginseng Res 45(4):519–526

    Article  PubMed  Google Scholar 

  • Li K, Zhong C, Shi Q, Bi H, Gong B (2021) Cold plasma seed treatment improves chilling resistance of tomato plants through hydrogen peroxide and abscisic acid signaling pathway. Free Radical Biol Med 172:286–297. https://doi.org/10.1016/j.freeradbiomed.2021.06.011

    Article  CAS  Google Scholar 

  • Mildažienė V, Aleknavičiūtė V, Žūkienė R, Paužaitė G, Naučienė Z, Filatova I, Lyushkevich V, Haimi P, Tamošiūnė I, Baniulis D (2019) Treatment of common sunflower (Helianthus annus L.) seeds with radio-frequency electromagnetic field and cold plasma induces changes in seed phytohormone balance, seedling development and leaf protein expression. Sci Rep 9(1):1–12. https://doi.org/10.1038/s41598-019-42893-5

    Article  CAS  Google Scholar 

  • Mirakhorli T, Ardebili ZO, Ladan-Moghadam A, Danaee E (2021) Nitric oxide improved growth and yield in soybean (Glycine max) by mediating physiological, anatomical, and transcriptional modifications. J Plant Growth Regul. https://doi.org/10.1007/s00344-021-10389-0

    Article  Google Scholar 

  • Moghanloo M, Iranbakhsh A, Ebadi M, OraghiArdebili Z (2019) Differential physiology and expression of phenylalanine ammonia lyase (PAL) and universal stress protein (USP) in the endangered species Astragalus fridae following seed priming with cold plasma and manipulation of culture medium with silica nanoparticles. 3 Biotech 9(7):1–13

    Article  Google Scholar 

  • Mravlje J, Regvar M, Starič P, Mozetič M, Vogel-Mikuš K (2021) Cold plasma affects germination and fungal community structure of buckwheat seeds. Plants 10(5):851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niazi A, Iranbakhsh A, Esmaeel Zadeh M, Ebadi M, OraghiArdebili Z (2022) Zinc oxide nanoparticles (ZnONPs) influenced seed development, grain quality, and remobilization by affecting the transcription of microRNA 171 (miR171), miR156, NAM, and SUT genes in wheat (Triticum aestivum): a biological advantage and risk assessment study. Protoplasma. https://doi.org/10.1007/s00709-022-01817-3

    Article  PubMed  Google Scholar 

  • Pavasupree S, Chanchula N, Bootchanont A, Wattanawikkam C, Jitjing P, Boonyawan D, Porjai P (2021) Enhancement propagation of protocorms in orchid (Cymbidium tracyanum L. Castle) by cold atmospheric pressure air plasma jet. Plasma Chem Plasma Process 41(2):573–589. https://doi.org/10.1007/s11090-020-10148-1

    Article  CAS  Google Scholar 

  • Pérez-Pizá MC, Ibañez VN, Varela A, Cejas E, Ferreyra M, Chamorro-Garces JC, Zilli C, Vallecorsa P, Fina B, Prevosto L and Marfil CF (2021) Non-thermal plasmas affect plant growth and DNA methylation patterns in glycine max. J Plant Growth Regul 41:2732–2742. https://doi.org/10.1007/s00344-021-10470-8

  • Rasooli Z, Barzin G, Mahabadi TD, Entezari M (2021) Stimulating effects of cold plasma seed priming on germination and seedling growth of cumin plant. S Afr J Bot 142:106–113

    Article  CAS  Google Scholar 

  • Rasouli M, Amini M, Khandan S, Ghoranneviss M, Nikmaram H, Ostrikov KK (2022) Arc and pulsed spark discharge inactivation of pathogenic P. aeruginosa, S. aureus, M. canis, T. mentagrophytes, and C. albicans microorganisms. Environ Sci Pollut Res 29:56442-56453. https://doi.org/10.1007/s11356-022-19847-y

  • Sheteiwy MS, An J, Yin M, Xiaowen J, Yajing G, Fei H, Jin H (2019) Cold plasma treatment and exogenous salicylic acid priming enhances salinity tolerance of Oryza sativa seedlings. Protoplasma 256:79–99. https://doi.org/10.1007/s00709-018-1279-0

    Article  CAS  PubMed  Google Scholar 

  • Sheteiwy M, Ulhassan Z, Qi W, Lu H, AbdElgawad H, Minkina T, Sushkova S, Rajput VD, El-Keblawy A, Josko I, Sulieman S (2022) Association of jasmonic acid priming with multiple defense mechanisms in wheat plants under high salt stress. Front Plant Sci 2614

  • Shi Z, Zou W, Zhu Z, Xiong Z, Li S, Dong P, Zhu Z (2022) Tropane alkaloids (hyoscyamine, scopolamine and Atropine) from genus Datura: extractions, contents, syntheses and effects. Ind Crops Prod 186:115283

    Article  CAS  Google Scholar 

  • Škoro N, Živković S, Jevremović S, Puač N (2022) Treatment of Chrysanthemum synthetic seeds by Air SDBD plasma. Plants 11(7):907

    Article  PubMed  PubMed Central  Google Scholar 

  • Suriyasak C, Hatanaka K, Tanaka H, Okumura T, Yamashita D, Attri P, Koga K, Shiratani M, Hamaoka N, Ishibashi Y (2021) Alterations of DNA methylation caused by cold plasma treatment restore delayed germination of heat-stressed rice (Oryza sativa L.) Seeds. Agric Sci Technol 1(1):5–10. https://doi.org/10.1021/acsagscitech.0c00070

    Article  CAS  Google Scholar 

  • Tabatabaee S, Iranbakhsh A, Shamili M and Ardebili ZO (2021) Copper nanoparticles mediated physiological changes and transcriptional variations in microRNA159 (miR159) and mevalonate kinase (MVK) in pepper; potential benefits and phytotoxicity assessment. J Environ Chem Eng 9(5):106151. https://doi.org/10.1016/j.jece.2021.106151

  • Twaij BM, Taha AJ, Bhuiyan FH, Hasan MN (2022) Effect of saccharides on secondary compounds production from stem derived callus of Datura inoxia. Biotechnol Rep 33:e00701

    Article  CAS  Google Scholar 

  • Vafaee Moghadam A, Iranbakhsh A, Saadatmand S, Ebadi M, Ardebili ZO (2021) New insights into the transcriptional, epigenetic, and physiological responses to zinc oxide nanoparticles in Datura stramonium; potential species for phytoremediation. J Plant Growth Regul. https://doi.org/10.1007/s00344-021-10305-6

    Article  Google Scholar 

  • Zhao L, Deng M, Teng Y, Ren W, Wang X, Ma W, Luo Y, Christie P (2021) Enhanced biomass and cadmium accumulation by three cadmium-tolerant plant species following cold plasma seed treatment. J Environ Manage 296:113212

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Science and Research Branch, Islamic Azad University, Tehran, Iran

    Zahra Tardast & Alireza Iranbakhsh

  2. Department of Biology, Damghan Branch, Islamic Azad University, Damghan, Iran

    Mostafa Ebadi

  3. Department of Biology, Garmsar Branch, Islamic Azad University, Garmsar, Iran

    Zahra Oraghi Ardebili

Authors
  1. Zahra Tardast
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alireza Iranbakhsh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mostafa Ebadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zahra Oraghi Ardebili
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alireza Iranbakhsh.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Handling Editor: Peter Nick

Publisher's note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tardast, Z., Iranbakhsh, A., Ebadi, M. et al. Corona discharge plasma stimulated production of atropine in callus of Datura inoxia by DNA hypomethylation and gene regulation: a novel technology for plant cell and tissue culture. Protoplasma 260, 1515–1525 (2023). https://doi.org/10.1007/s00709-023-01863-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-023-01863-5

Keywords

Search

Navigation