Skip to main content
SpringerLink
Log in

Enhancing Wheat Seedling Tolerance to Cypermethrin through Azospirillum thiophilum Pretreatment

  • RESEARCH PAPERS
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Pesticide treatment leads to a significant increase in wheat yield and enhances pest resistance. However, pesticides, particularly the insecticide cypermethrin, which is used for wheat Triticum aestivum L. field and grain storage treatment, are toxic xenobiotics. To reduce their toxicity, it is possible to pre-treat seeds with plant growth-promoting rhizobacteria (PGPR), which can enhance plant resistance to adverse environmental factors. In this study, we used a previously unused as PGPR representative of the genus Azospirillum, A. thiophilum BV-ST, isolated in Russia, which makes it interesting for agricultural use in the same climatic zone. We optimized the detection method of A. thiophilum using PCR. Then, we demonstrated that this bacterium successfully inoculates to wheat roots. We showed that cypermethrin treatment of one- and two-week-old wheat seedlings caused an increase in mtDNA damage, and in one-week-old seedlings, it induced a decrease in chlorophyll levels. However, three- and four-week-old seedlings were more resistant to damage, possibly due to their approximately 5-fold higher expression of NDOR-1 and GST genes, which play an important role in xenobiotic detoxification. Pre-treatment of wheat seeds with A. thiophilum contributed to the upregulation of NDOR-1 and GST gene expression in one- and two-week-old seedlings, resulting in the protection of mtDNA from cypermethrin-induced damage and prevented the decrease in chlorophyll levels.

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.

REFERENCES

  1. Tudi, M., Daniel Ruan, H., Wang, L., Lyu, J., Sadler, R., Connell, D., Chu, C., and Phung, D.T., Agriculture development, pesticide application and its impact on the environment, Int. J. Environ. Res. Public Health, 2021, vol. 18, p. 1112. https://doi.org/10.3390/ijerph18031112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Riedo, J., Wächter, D., Gubler, A., Wettstein, F.E., Meuli, R.G., and Bucheli, T.D., Pesticide residues in agricultural soils in light of their on-farm application history, Environ. Pollut., 2023, vol. 331, p. 121892. https://doi.org/10.1016/j.envpol.2023.121892

    Article  CAS  PubMed  Google Scholar 

  3. Hossard, L., Philibert, A., Bertrand, M., Colnenne-David, C., Debaeke, P., Munier-Jolain, N., Jeuffroy M.H., Richard G., and Makowski, D., Effects of halving pesticide use on wheat production, Sci. Rep., 2014, vol. 4, p. 4405. https://doi.org/10.1038/srep04405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Rudoy, E.V., Petukhova, M.S., Ryumkin, S.V., Dobryanskaya, S.L., and Molyavko, A.V., Crop production in Russia 2030: Scenarios based on data from the scientific and technological development of the sector, Data Brief, 2019, vol. 29, p. 103980. https://doi.org/10.1016/j.dib.2019.103980

    Article  Google Scholar 

  5. Bockus, W.W., Bowden, R.L., Hunger, R.M., Murray, T.D., and Smiley, R.W., Compendium of wheat diseases and pests, in Diseases and Pests Compendium Series, St. Paul: APS Press, 2010. https://doi.org/10.1094/9780890546604

    Book  Google Scholar 

  6. Syromyatnikov, M.Y., Gureev, A.P., Starkova, N.N., Savinkova, O.V., Starkov, A.A., Lopatin, A.V., and Popov, V.N., Method for detection of mtDNA damages for evaluating of pesticides toxicity for bumblebees (Bombus terrestris L.), Pestic. Biochem. Physiol., 2020, vol. 169, p. 104675. https://doi.org/10.1016/j.pestbp.2020.104675

    Article  CAS  PubMed  Google Scholar 

  7. Katagi, T. and Fujisawa, T., Acute toxicity and metabolism of pesticides in birds, J. Pestic. Sci., 2021, vol. 46, p. 305. https://doi.org/10.1584/jpestics.D21-028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Yang, C., Lim, W., and Song, G., Mediation of oxidative stress toxicity induced by pyrethroid pesticides in fish, Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol., 2020, vol. 234, p. 108758. https://doi.org/10.1016/j.cbpc.2020.108758

    Article  CAS  Google Scholar 

  9. Sim, J.X., Drigo, B., Doolette, C.L., Vasileiadis, S., Karpouzas, D.G., and Lombi, E., Impact of twenty pesticides on soil carbon microbial functions and community composition, Chemosphere, 2022, vol. 307, p. 135820. https://doi.org/10.1016/j.chemosphere.2022.135820

    Article  CAS  PubMed  Google Scholar 

  10. Cycoń, M., Markowicz, A., Borymski, S., Wójcik, M., and Piotrowska-Seget, Z., Imidacloprid induces changes in the structure, genetic diversity and catabolic activity of soil microbial communities, J. Environ. Manage., 2013, vol. 131, p. 55. https://doi.org/10.1016/j.jenvman.2013.09.041

    Article  CAS  PubMed  Google Scholar 

  11. Prashar, P. and Shah, S., Impact of fertilizers and pesticides on soil microflora in agriculture, in Sustainable Agriculture Reviews. Sustainable Agriculture Reviews, Lichtfouse, E., Ed., Springer: Cham, 2016, vol. 19, p. 331. https://doi.org/10.1007/978-3-319-26777-7_8

    Book  Google Scholar 

  12. Alimova, A.A., Sitnikov, V.V., Pogorelov, D.I., Boyko, O.N., Vitkalova, I.Y., Gureev, A.P., and Popov, V.N., High doses of pesticides induce mtDNA damage in intact mitochondria of potato in vitro and do not impact on mtDNA integrity of mitochondria of shoots and tubers under in vivo exposure, Int. J. Mol. Sci., 2022, vol. 23, p. 2970. https://doi.org/10.3390/ijms23062970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Wu, A.P., He, Y., Ye, S.Y., Qi, L.Y., Liu, L., Zhong, W., Wang, Y.H., and Fu, H., Negative effects of a piscicide, rotenone, on the growth and metabolism of three submerged macophytes, Chemosphere, 2020, vol. 250, p. 126246. https://doi.org/10.1016/j.chemosphere.2020.126246

    Article  CAS  PubMed  Google Scholar 

  14. Parween, T., Jan, S., Mahmooduzzafar, and Fatma T., Assessing the impact of chlorpyrifos on growth, photosynthetic pigments and yield in Vigna radiata L. at different phenological stages, Afr. J. Agric. Res., 2011, vol. 619, p. 4432.

    Google Scholar 

  15. Giménez–Moolhuyzen, M., van der Blom, J., Lorenzo–Mínguez, P., Cabello, T., and Crisol-Martínez, E., Photosynthesis Inhibiting Effects of Pesticides on Sweet Pepper Leaves, Insects, 2020, vol. 11, p. 69. https://doi.org/10.3390/insects11020069

    Article  PubMed  PubMed Central  Google Scholar 

  16. Dayan, F.E., Barker, A., and Tranel, P.J., Origins and structure of chloroplastic and mitochondrial plant protoporphyrinogen oxidases: implications for the evolution of herbicide resistance, Pest Manage. Sci., 2018, vol. 74, p. 2226. https://doi.org/10.1002/ps.4744

    Article  CAS  Google Scholar 

  17. Vitkalova, I.Y., Gureev, A.P., Shaforostova, E.A., Boyko, O.N., Igamberdiev, A.U., and Popov, V.N., The effect of pesticides on the mtDNA integrity and bioenergetic properties of potato mitochondria, Pestic. Biochem. Physiol., 2021, vol. 172, p. 104764. https://doi.org/10.1016/j.pestbp.2020.104764

    Article  CAS  PubMed  Google Scholar 

  18. Prathiksha, J., Narasimhamurthy, R.K., Dsouza, H.S., and Mumbrekar, K.D., Organophosphate pesticide-induced toxicity through DNA damage and DNA repair mechanisms, Mol. Biol. Rep., 2023, vol. 50, p. 5465. https://doi.org/10.1007/s11033-023-08424-2

    Article  CAS  PubMed  Google Scholar 

  19. Wang, C.Y. and Zhao, Z.B., Somatic mtDNA mutations in lung tissues of pesticide-exposed fruit growers, Toxicology, 2012, vol. 291, p. 51. https://doi.org/10.1016/j.tox.2011.10.018

    Article  CAS  PubMed  Google Scholar 

  20. Knuteson, S.L., Whitwell, T., and Klaine, S.J., Influence of plant age and size on simazine toxicity and uptake, J. Environ. Qual., 2002, vol. 31, p. 2096. https://doi.org/10.2134/jeq2002.2096

    Article  CAS  PubMed  Google Scholar 

  21. Cummins, I., Dixon, D.P., Freitag-Pohl, S., Skipsey, M., and Edwards, R., Multiple roles for plant glutathione transferases in xenobiotic detoxification, Drug Metab. Rev., 2011, vol. 43, p. 266. https://doi.org/10.3109/03602532.2011.552910

    Article  CAS  PubMed  Google Scholar 

  22. Alori, E.T. and Babalola O.O., Microbial Inoculants for Improving Crop Quality and Human Health in Africa, Front. Microbiol., 2018, vol. 19, p. 2213. https://doi.org/10.3389/fmicb.2018.02213

    Article  Google Scholar 

  23. Vocciante, M., Grifoni, M., Fusini, D., Petruzzelli, G., and Franchi, E., The role of plant growth-promoting rhizobacteria (PGPR) in mitigating plant’s environmental stresses, Appl. Sci., 2022, vol. 12, p. 1231. https://doi.org/10.3390/app12031231

    Article  CAS  Google Scholar 

  24. Nievas, S., Coniglio, A., Takahashi, W.Y., López, G.A., Larama, G., Torres, D., Rosas, S., Etto, R.M., Galvão C.W., Mora V., and Cassán F., Unraveling Azospirillum’s colonization ability through microbiological and molecular evidence, J. Appl. Microbiol., 2023, vol. 134, p. lxad071. https://doi.org/10.1093/jambio/lxad071

  25. Gureev, A.P., Mashkina, O.S., Shabanova, E.A., Vitkalova, I.Y., Sitnikov, V.V., and Popov, V.N., Study of the amount of oxidative damage to mitochondrial and chloroplast DNA in clones of white poplar (Populus alba L.) during long-term in vitro cultivation for 26 years, Plant Mol. Biol., 2021, vol. 106, p. 479. https://doi.org/10.1007/s11103-021-01157-5

    Article  CAS  PubMed  Google Scholar 

  26. Gureeva, M.V. and Gureev, A.P., Molecular mechanisms determining the role of bacteria from the genus Azospirillum in plant adaptation to damaging environmental factors, Int. J. Mol. Sci., 2023, vol. 24, p. 9122. https://doi.org/10.3390/ijms24119122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Marrs, K.A., The functions and regulation of glutathione S-transferases in plants, Annu. Rev. Plant Biol., 1996, vol. 47, p. 127. https://doi.org/10.1146/annurev.arplant.47.1.127

    Article  CAS  Google Scholar 

  28. Seckin Dinler, B., Cetinkaya, H., and Secgin, Z., The regulation of glutathione s-transferases by gibberellic acid application in salt treated maize leaves, Physiol. Mol. Biol. Plants, 2023, vol. 29, p. 69. https://doi.org/10.1007/s12298-022-01269-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Xu, N., Chu, Y., Chen, H., Li, X., Wu, Q., Jin, L., Wang, G., and Huang, J., Rice transcription factor OsMA-DS25 modulates root growth and confers salinity tolerance via the ABA–mediated regulatory pathway and ROS scavenging, PLoS Genet., 2018, vol. 14, p. e1007662. https://doi.org/10.1371/journal.pgen.1007662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Lavrinenko, K., Chernousova, E., Gridneva, E., Dubinina, G., Akimov, V., Kuever, J., Lysenko, A., and Grabovich, M., Azospirillum thiophilum sp. nov., a diazotrophic bacterium isolated from a sulfide spring, Int. J. Syst. Evol. Microbiol., 2010, vol. 60, p. 2832. https://doi.org/10.1099/ijs.0.018853-0

    Article  CAS  PubMed  Google Scholar 

  31. Tikhonova, E.N., Grouzdev, D.S., and Kravchenko, I.K., Azospirillum palustre sp. nov., a methylotrophic nitrogen-fixing species isolated from raised bog, Int. J. Syst. Evol. Microbiol., 2019, vol. 69, p. 2787. https://doi.org/10.1099/ijsem.0.003560

    Article  CAS  PubMed  Google Scholar 

  32. Noble, R.M. and Hamilton, D.J., Stability of cypermethrin and cyfluthrin on wheat in storage, Pestic. Sci., 1985, vol. 16, p. 179. https://doi.org/10.1002/ps.2780160212

    Article  CAS  Google Scholar 

  33. Patel, S., Pandey, A.K., Bajpayee, M., Parmar, D., and Dhawan, A., Cypermethrin-induced DNA damage in organs and tissues of the mouse: evidence from the comet assay, Mutat. Res., Genet. Toxicol. Environ. Mutagen., 2006, vol. 607, p. 176. https://doi.org/10.1016/j.mrgentox.2006.04.010

    Article  CAS  Google Scholar 

  34. Çavuşoğlu, K., Kaya, A., Yilmaz, F., and Yalçin, E., Effects of cypermethrin on Allium cepa, Environ. Toxicol., 2012, vol. 27, p. 583. https://doi.org/10.1016/10.1002/tox.20681

    Article  PubMed  Google Scholar 

  35. Tarrand, J.J., Krieg, N.R., and Döbereiner, J., A taxonomic study of the Spirillum lipoferum group, with descriptions of a new genus, Azospirillum gen. nov. and two species, Azospirillum lipoferum (Beijerinck) comb. nov. and Azospirillum brasilense sp. nov, Can. J. Microbiol., 1978, vol. 24, p. 967. https://doi.org/10.1139/m78-160

    Article  CAS  PubMed  Google Scholar 

  36. Lin, S.-Y., Young, C.C., Hupfer, H., Siering, C., Arun, A.B., Chen, W.-M., Lai, W.-A., Shen, F.-T., Rekha, P.D., and Yassin, A.F., Azospirillum picis sp. nov., isolated from discarded tar, Int. J. Syst. Evol. Microbiol., 2009, vol. 59, p. 761. https://doi.org/10.1099/ijs.0.65837-0

    Article  CAS  PubMed  Google Scholar 

  37. Lin, S.-Y., Hameed, A., Shen, F.-T., Liu, Y.-C., Hsu Y.-H., Shahina, M., Lai, W.-A., and Young, C.-C., Description of Niveispirillum fermenti gen. nov., sp. nov., isolated from a fermentor in Taiwan, transfer of Azospirillum irakense (1989) as Niveispirillum irakense comb. nov., and reclassification of Azospirillum amazonense (1983) as Nitrospirillum amazonense gen. nov., Antonie van Leeuwenhoek, 2014, vol. 105, p. 1149. https://doi.org/10.1007/s10482-014-0176-6

    Article  CAS  PubMed  Google Scholar 

  38. Reinhold, B., Hurek, T., Fendrik, I., Pot, B., Gillis, M., Kersters, K., Thielemans, S., and De Ley, J., Azospirillum halopraeferens sp. nov., a nitrogen-fixing organism associated with roots of kallar grass (Leptochloa fusca (L.) Kunth), Int. J. Syst. Bacteriol., vol. 37, p. 43. https://doi.org/10.1099/00207713-37-1-43

  39. Caraway, B.H. and Krieg, N.R., Aerotaxis in Spirillum volutans, Can. J. Microbiol., 1974, vol. 20, p. 1367. https://doi.org/10.1139/m74-211

    Article  CAS  Google Scholar 

  40. Pfennig, N. and Lippert, K.D., Über das Vitamin B12‑Bedürfnis phototropher Schwefelbakterien, Archiv für Mikrobiologie, 1966, vol. 55, p. 245. https://doi.org/10.1007/BF00410246

    Article  CAS  Google Scholar 

  41. Baudoin, E., Couillerot, O., Spaepen, S., Moënne-Loccoz, Y., and Nazaret, S., Applicability of the 16S–23S rDNA internal spacer for PCR detection of the phytostimulatory PGPR inoculant Azospirillum lipoferum CRT1 in field soil, J. Appl. Microbiol., 2010, vol. 108, p. 25. https://doi.org/10.1111/j.1365-2672.2009.04393.x

    Article  CAS  PubMed  Google Scholar 

  42. Shime-Hattori, A., Kobayashi, S., Ikeda, S., Asano, R., Shime, H., and Shinano, T., A rapid and simple PCR method for identifying isolates of the genus Azospirillum within populations of rhizosphere bacteria, J. Appl. Microbiol., 2011, vol. 111, p. 915. https://doi.org/10.1111/j.1365-2672.2011.05115.x

    Article  CAS  PubMed  Google Scholar 

  43. Arnon, D.I., Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris, Plant Physiol., 1949, vol. 24, p. 1. https://doi.org/10.1111/10.1104/pp.24.1.1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Lorenzen, C.J., Determination of chlorophyll and pheo-pigments: spectrophotometric equations, Limnol. Oceanogr., 1967, vol. 12, p. 343. https://doi.org/10.4319/lo.1967.12.2.0343

    Article  CAS  Google Scholar 

  45. Saxena, D.K. and Harinder, K., Chlorophyll as a biological marker of stress following application of heavy metals (Pb, Ni and Cd) in moss Thuidium cymbifolium, J. Phytol. Res., 2006, vol. 19, p. 239.

    CAS  Google Scholar 

  46. Niroula, A., Khatri, S., Timilsina, R., Khadka, D., Khadka, A., and Ojha, P., Profile of chlorophylls and carotenoids of wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.) microgreens, J. Food Sci. Technol. (New Delhi, India), 2019, vol. 56, p. 2758. https://doi.org/10.1007/s13197-019-03768-9

    Article  CAS  Google Scholar 

  47. Mikhed, Y., Daiber, A., and Steven, S., Mitochondrial oxidative stress, mitochondrial DNA damage and their role in age-related vascular dysfunction, Int. J. Mol. Sci., 2015, vol. 16, p. 15918. https://doi.org/10.3390/ijms160715918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Fukami, J., Cerezini, P., and Hungria, M., Azospirillum: benefits that go far beyond biological nitrogen fixation, AMB Expr., 2018, vol. 8, p. 73. https://doi.org/10.1186/s13568-018-0608-1

    Article  CAS  Google Scholar 

  49. Finn, R.D., Basran, J., Roitel, O., Wolf, C.R., Munro, A.W., Paine, M.J., and Scrutton, N.S., Determination of the redox potentials and electron transfer properties of the FAD- and FMN-binding domains of the human oxidoreductase NR1, Eur. J. Biochem., 2003, vol. 270, p. 1164. https://doi.org/10.1046/j.1432-1033.2003.03474.x

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the Russian Science Foundation project no. 23-24-00277.

Author information

Authors and Affiliations

  1. Voronezh State University, Department of Biochemistry and Cell Physiology, 394018, Voronezh, Russia

    M. V. Gureeva, A. A. Alimova, M. S. Kirillova, O. A. Filatova, M. I. Moskvitina & A. P. Gureev

  2. Voronezh State University, Department of Genetics, Cytology and Bioengineering, 394018, Voronezh, Russia

    A. A. Alimova, A. A. Eremina, V. A. Kryukova, E. P. Krutskikh, E. V. Chernyshova & A. P. Gureev

  3. Voronezh State University of Engineering Technology, Laboratory of Metagenomics and Food Biotechnology, 394036, Voronezh, Russia

    A. A. Alimova & A. P. Gureev

Authors
  1. M. V. Gureeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. A. Alimova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. A. Eremina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. V. A. Kryukova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. S. Kirillova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. O. A. Filatova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. I. Moskvitina
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. E. P. Krutskikh
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. E. V. Chernyshova
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. A. P. Gureev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. V. Gureeva.

Ethics declarations

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

Additional information

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Abbreviations: PGPR, plant growth-promoting rhizobacteria; NDOR, NADPH-dependent diflavin oxidoreductase; GST, glutathione S-transferase; ACC, 1-aminocyclopropane-1-carboxylate; SOD, superoxide dismutase; MDA, malondialdehyde; GA3, gibberellin A3.

Supplementary Information

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gureeva, M.V., Alimova, A.A., Eremina, A.A. et al. Enhancing Wheat Seedling Tolerance to Cypermethrin through Azospirillum thiophilum Pretreatment. Russ J Plant Physiol 70, 184 (2023). https://doi.org/10.1134/S102144372360215X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1134/S102144372360215X

Keywords:

Search

Navigation