doi: 10.15389/agrobiology.2018.1.38eng

UDC 631.8:546.26:581.1

Acknowledgements:
Supported financially by Russian Foundation for Basic Research
(project 15-29-05837 ofi_m)

 

FULLERENE DERIVATIVES INFLUENCE PRODUCTION PROCESS,
GROWTH AND RESISTANCE TO OXIDATIVE STRESS IN BARLEY
AND WHEAT PLANTS

G.G. Panova1, E.V. Kanash1, K.N. Semenov2, N.A. Charykov3,
Yu.V. Khomyakov1, L.M. Anikina1, A.M. Artemeva4, D.L. Kornyukhin4,
V.E. Vertebnyi1, N.G. Sinyavina1, O.R. Udalova1, N.A. Kulenova5,
S.Yu. Blokhina1

1Agrophysical Research Institute, Federal Agency for Scientific Organizations, 14, Grazhdanskii prosp., St. Petersburg, 195220 Russia, e-mail gaiane@inbox.ru (✉ corresponding author), ykanash@yandex.ru, himlabafi@yandex.ru, lanikina@yandex.ru, verteb22@mail.ru, sinad@inbox.ru, udal59@inbox.ru, sblokhina@agrophys.ru;
2Saint Petersburg State University, 26, Universitetskii pr., St. Petersburg—Petrodvorets, 198504 Russia, e-mail k.semenov@spbu.ru;
3Saint-Petersburg State Institute of Technology (Technical University), 26, Moskovskii pr., St. Petersburg, 190013 Russia, e-mail ncharykov@yandex.ru;
4Federal Research Center the Vavilov All-Russian Institute of Plant Genetic Resources, Federal Agency for Scientific Organizations, 42-44, ul. Bol’shaya Morskaya, St. Petersburg, 190000 Russia, e-mail akme11@yandex.ru, dkor4@yandex.ru;
5Serikbayev East Kazakhstan State Technical University, 69, ul. A.K. Protozanova, Ust-Kamenogorsk, 070004 Republic of Kazakhstan, e-mail nkulenova@ektu.kz

ORCID:
Panova G.G. orcid.org/0000-0002-1132-9915
Kornyukhin D.L. orcid.org/0000-0001-9181-5368
Kanash E.V. orcid.org/0000-0002-8214-8193
Vertebnyi V.E. orcid.org/0000-0002-7817-2721
Semenov K.N. orcid.org/0000-0003-2239-2044
Sinyavina N.G. orcid.org/0000-0003-0378-7331
Charykov N.A. orcid.org/0000-0002-4744-7083
Udalova O.R. orcid.org/0000-0003-3521-0254
Khomyakov Yu.V. orcid.org/0000-0003-3245-8801
Kulenova N.A. orcid.org/0000-0002-7063-4899
Anikina L.M. orcid.org/0000-0001-5217-174X
Blokhina S.Yu. orcid.org/0000-0003-3492-6808
Artemyeva A.M. orcid.org/0000-0002-6551-5203

Received March 28, 2017

 

Creation of effective environment-friendly preparations to improve productivity and sustainability of agro- and ecosystems is of current interest. Carbon nanostructures, such as the water-soluble 60 and 70 fullerene derivatives presently used in biomedicine and pharmacology, are considered perspective agents for agriculture. It was shown that they can penetrate into the cell membranes owing to lipophylicity and nanosize, transport medicinal substances to target cells and have antioxidant activity. The mechanism underlying the influence of water-soluble fullerene derivatives on plants in agroecosystems remains unclear. In the paper, we for the first time report the effects of C60 fullerene derivatives on the processes that determine the net productivity and plant resistance to oxidative stress. In the study we used fullerenol and the fullerene C60 adducts with the three essential amino acids, threonine, lysine, arginine, and also with the amino acid hydroxyproline, which were previously synthesized following a one-step procedure. Stimulating effects of these fullerene derivatives on the growth of spring wheat and barley were observed in two vegetation experiments carried out in controlled conditions (aerated nutrient solution, plant growing light equipment) when the compounds were added to the root habited medium and under non-root treatment. It was shown that the biomass of leaves, stems, and roots in plants increased by 27-226 % (p < 0.05). Statistical analysis using the Wilcoxon test confirmed the reliability of the differences found. Fullerenol, fullerene C60-hydroxyproline, and fullerene C60-threonine caused the greatest increase when compared to the control. Obviously, the observed effect was associated with the established ability of fullerenol and C60 fullerene amino acid derivatives to exert regulatory activity on the synthesis of photosynthetic pigments and, as a consequence, on the efficiency of photosynthesis. A comparison of the reflection indexes characterizing the content of chlorophylls (ChlRI) and anthocyanins (ARI) in leaves showed that the photosynthetic apparatus with a greater potential is generally formed under the influence of fullerene derivatives. Under the influence of these derivatives, the lipid peroxidation intensity also decreased and superoxide dismutase was activated while reactive oxygen species generation in leaves and (or) roots increased (predominantly in barley) or decreased. These changes in plants were the most expressed at fullerenol, C60-threonine and C60-hydroxyproline action. Under stress modeling (UV-B irradiation, 20 kJ/m2), the UV-resistance of barley plants after not-root treatment with fullerenol, C60-threonine and C60-hydroxyproline, when estimated by the dry weight of the above ground parts and roots, was 10-20 % higher compared to that of the control irradiated plants which were of less weight (by ≈ 33 % for stems and leaves, and by 10-20 % for roots). Thus, the study revealed the positive influence of synthesized amino acid derivatives of fullerene C60 and fullerenol on the plant production process and resistance to oxidative stress. High efficiency in small concentrations, low expenses for application and environmental friendliness indicate the perspectiveness of these compounds and necessitate further studying the mechanisms of their action on the soil—plant system to create preparations for use in plant growing.

Keywords: amino acid fullerene C60 derivatives, fullerenol, plant production processes, optimization, oxidative stress, resistance, ecologically safe preparations, plant growing.

 

Full article (Rus)

Full article (Eng)

 

REFERENCES

  1. Piotrovskii L.B., Kiselev O.I. Fullereny v biologii [Fullerenes in biology]. St. Petersburg, 2006 (in Russ.).
  2. Semenov K.N., Charykov N.A., Keskinov V.A. Fullerenol synthesis and identification. Rroperties of fullerenol water solutions. J. Chem. Eng. Data, 2011, 56: 230-239 CrossRef
  3. Piotrovskii L.B. Rossiiskie nanotekhnologii, 2007, 2(7-8): 6-18 (in Russ.).
  4. Andreev I., Petrukhina A., Garmanova A., Babakhin A., Andreev S., Romanova V., Troshin P., Troshina O., DuBuske L. Penetration of fullerene C60 derivatives through biological membranes. Fullerenes, Nanotubes, and Carbon Nanostructures, 2008, 16: 89-102 CrossRef
  5. Kornev A.B., Troshina O.A., Troshin P.A. Biologicheski aktivnye proizvodnye fullerenov, metody ikh polucheniya i primenenie v meditsine. V knige: Organicheskie i gibridnye nanomaterialy: tendentsii i perspektivy /Pod redaktsiei V.F. Razumova, M.V. Klyueva [Organic and hybrid nanomaterials: trends and prospects. V.F. Razumov, M.V. Klyuev (eds.)]. Ivanovo, 2013: 392-485 (in Russ.).
  6. Gao J., Wang Y., Folta K.M., Krishna V., Bai W., Indeglia P., Georgieva A., Nakamura H., Koopman B., Moudgi B. Polyhydroxy fullerenes (fullerols or fullerenols): beneficial effects on growth and lifespan in diverse biological models. PLoS ONE, 2011, 6(5): e19976 CrossRef
  7. Zhao Y.Y., Yang B., Tang M.L. Guo Q-Ch., Chen Ju-T., Wen L-P., Wang M. Concentration-dependent effects of fullerenol on cultured hippocampal neuron viability. Int. J. Nanomed., 2012, 7: 3099-3109 CrossRef
  8. Kole C., Kole P., Randunu K.M., Choudhary P., Podila R., Ke P.C., Rao A.M., Marcus R.K. Nanobiotechnology can boost crop production and quality: first evidence from increased plant biomass, fruit yield and phytomedicine content in bitter melon (Momordica charantia). BMC Biotechnol., 2013, 13: 37-58 CrossRef
  9. Panova G.G., Ktitorova I.N., Skobeleva O.V., Sinjavina N.G., Charykov N.A., Semenov K.N. Impact of polyhydroxy fullerene (fullerol or fullerenol) on growth and biophysical characteristics of barley seedlings in favourable and stressful conditions. Plant Growth Regul., 2016, 79: 309-317 CrossRef
  10. Chen R., Ratnikova T.A., Stone M.B., Lin S., Lard M., Huang G., Hudson J.S., Ke P. C. Differential uptake of carbon nanoparticles by plant and Mammalian cells. Small, 2010, 6: 612-617 CrossRef
  11. Dugan L.L., Lovett E.G., Quick K.L., Lotharius J., Lin T.T., O’Malley K.L. Fullerene-based antioxidants and neurodegenerative disorders. Parkinsonism Relat. Disord., 2001, 7: 243-246 CrossRef
  12. Gharbi N., Pressac M., Hadchouel M., Szwarc H., Wilson S.R., Moussa F. [60]Fullerene is a powerful antioxidant in vivo with no acute or subacute toxicity. Nano Lett., 2005, 5: 2578-2585 CrossRef
  13. Yin J.J., Lao F., Fu P.P., Wamer W.G., Zhao Y., Wang P.C., Qiu Y., Sun B., Xing G., Dong J., Liang X.-J., Chen C. The scavenging of reactive oxygen species and the potential for cell protection by functionalized fullerene materials. Biomaterials, 2009, 30(4): 611-621 CrossRef
  14. Lin S., Reppert J., Hu Q., Hudson J.S., Reid M.L., Ratnikova T.A., Rao A.M., Luo H., Ke P.C. Uptake, translocation, and transmission of carbon nanomaterials in rice plants. Small, 2009, 5: 1128-1132 CrossRef
  15. Avanasi R., Jackson W.A., Sherwin B., Mudge J.F., Anderson T.A. C60 fullerene soil sorption, biodegradation, and plant uptake. Environ. Sci. Technol., 2014, 48(5): 2792-2797 CrossRef
  16. Wang C., Zhang H., Ruan L., Chen L., Li H., Chang X.-L., Zhang X., Yang S.-T. Bioaccumulation of 13C-fullerenol nanomaterials in wheat. Environ. Sci.: Nano, 2016, 4: 1-7 CrossRef
  17. Semenov K.N., Charykov N.A., Namazbaev V.I., Keskinov V.A. Sposob polucheniya smesi fullerenolov. Patent RF na izobretenie RU 2495821 C2. ZAO ILIP (RU), OOO Agrofizprodukt (RU). 2010122963/05. Zayavl. 04.06.2010. Opubl. 20.10.2013. Byul. 29 [Method for the preparation of a mixture of fullerenols. Patent RU 2495821 C2. ZAO ILIP (RU), OOO Agrophysprodukt (RU). 2010122963/05. Appl. 04.06.2010. Publ. 20.10.2013. Bul. 29 (in Russ.).
  18. Semenov K.N., Charykov N.A., Keskinov V.A., Keskinova M.V., Saf'yannikov N.M., Shubina V.A. Sposob polucheniya fullerenolov. Patent RF na izobretenie RU 2481267 C2. OOO «Biogel'tek» (RU). 2011106276/05. Zayavl. 11.02.2011. Opubl. 10.05.2013. Byul. 13 [Method for the preparation of fullerenols. Patent RU 2481267 C2. «Biogeltek» (RU). 2011106276/05. Appl. 02/11/2011. Publ. . 10.05.2013. Bul. 13] (in Russ.).
  19. Panova G.G., Chernousov I.N., Udalova O.R., Aleksandrov A.V., Karmanov I.V., Anikina L.M., Sudakov V.L. Doklady RASKHN, 2015, 4: 17-21 (in Russ.).
  20. Purvid A.C., Shewfeld R.L., Gegogeine J.W. Superoxide production in mitochondria isolated from green bell pepper fruit. Physiologia Plantarum, 1995, 94: 743-749 CrossRef
  21. Lukatkin A.S. Fiziologiya rastenii, 2002, 49: 697-702 (in Russ.).
  22. Nekrasova G.F., Kiseleva I.S. Ekologicheskaya fiziologiya rastenii [Plant ecophysiology]. Ekaterinburg, 2008 (in Russ.).
  23. Yakushev V.P., Kanash E.V., Osipov Yu.A., Yakushev V.V., Lekomtsev P.V., Voropaev V.V. [Optical criteria during contact and distant measurements sowing state of wheat and photosynthesis effectiveness on the background of deficit of mineral nutrition]. Agricultural Biology, 2010, 3: 94-101 (in Russ.).
  24. Kanash E.V., Panova G.G., Blokhina S.Yu. Optical criteria for assessment of efficiency and adaptogenic characteristics of biologically active preparations. Acta Horticulturae, 2013, 1009: 37-44 CrossRef
  25. Kanash E.V., Ermakov E.I. V sbornike: Reguliruemaya agroekosistema v rastenievodstve i ekofiziologii [Control of agroecosystems in plant growing and ecophysiology]. St. Petersburg, 2007: 232-253 (in Russ.).

back