Skip to main content
Log in

Influence of Nanoparticles of Metals and Their Oxides on the Photosynthetic Apparatus of Plants

  • PLANT PHYSIOLOGY
  • Published:
Biology Bulletin Aims and scope Submit manuscript

Abstract

A comparative survey of the published data concerning the effects of the most frequently used metal nanoparticles and their oxides on the main parameters of the photosynthetic apparatus activity and the chloroplast ultrastructure of higher plants is presented. It is demonstrated that metal nanoparticles are capable of both stimulating and suppressing activities towards the photosynthetic apparatus. Possible mechanisms of the effects of metal nanoparticles on the plant organism are discussed.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

REFERENCES

  1. Almutairi, Z.M., Influence of silver nano-particles on the salt resistance of tomato (Solanum lycopersicum) during germination, Int. J. Agric. Biol., 2016, vol. 18, pp. 449–457.

    Article  CAS  Google Scholar 

  2. An, J., Zhang, M., Wang, S., and Tang, J., Physical, chemical and microbiological changes in stored green asparagus spears as affected by coating of silver nanoparticles-PVP, LWT—Food Sci. Technol., 2008, vol. 41, pp. 1100–1107.

    Article  CAS  Google Scholar 

  3. Arora, S., Sharma, P., Kumar, S., Nayan, R., Khanna, P.K., and Zaidi, M.G.H., Gold-nanoparticle induced enhancement in growth and seed yield of Brassica juncea, Plant Growth Regul., 2012, vol. 66, pp. 303–310.

    Article  CAS  Google Scholar 

  4. Astafurova, T.P., Morgalev, Yu.N., Zotikova, A.P., Verkhoturova, G.S., Mikhailova, S.I., Burenina, A.A., Zaitseva, T.A., Postovalova, V.M., Tsytsareva, L.K., and Borovikova, G.V., Effect of titanium dioxide and aluminum oxide nanoparticles on morphophysiological parameters of plants, Vestn. Tomsk. Gos. Univ., Ser. Biol., 2011, vol. 1, pp. 113–122.

    Google Scholar 

  5. Baier, M. and Dietz, K.-J., Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology, J. Exp. Bot., 2005, vol. 56, pp. 1449–1462.

    Article  CAS  PubMed  Google Scholar 

  6. Barazzouk, S., Bekalé, L., Kamat, P.V., and Hotchandani, S., Enhanced photostability of chlorophyll-a using gold nanoparticles as an efficient photoprotector, J. Mater. Chem., 2012, vol. 22, pp. 2516–2534.

    Article  Google Scholar 

  7. Barrios, A.C., Rico, C.M., Trujillo-Reyes, J., Medina-Velo, I.A., Peralta-Videa, J.R., and Gardea-Torresdey, J.L., Effects of uncoated and citric acid coated cerium oxide nanoparticles, bulk cerium oxide, cerium acetate, and citric acid on tomato plants, Sci. Total Environ., 2016, vols. 563–564, pp. 956–964.

    Article  PubMed  Google Scholar 

  8. Bertrand, M. and Poirier, I., Photosynthetic organisms and excess of metals, Photosynthetica, 2005, vol. 43, pp. 345–353.

    Article  CAS  Google Scholar 

  9. Bourett, T.M., Czymmek, K.J., and Howard, R.J., Ultrastructure of chloroplast protuberances in rice leaves preserved by high-pressure freezing, Planta, 1999, vol. 208, pp. 472–479.

    Article  CAS  Google Scholar 

  10. Chen, X., O’Halloran, J., and Jansen, M.A., The toxicity of zinc oxide nanoparticles to Lemna minor (L.) is predominantly caused by dissolved Zn, Aquat. Toxicol., 2016, vol. 174, pp. 46–53.

    Article  CAS  PubMed  Google Scholar 

  11. Crosatti, C., Rizza, F., Badeck, F.W., Mazzucotelli, E., and Cattivelli, L., Harden the chloroplast to protect the plant, Physiol. Plant., 2013, vol. 147, pp. 55–63.

    Article  CAS  PubMed  Google Scholar 

  12. Da Costa, M.V.J. and Sharma, P.K., Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa, Photosynthetica, 2016, vol. 54, pp. 110–119.

    Article  CAS  Google Scholar 

  13. Das, S., Debnath, N., Pradhan, S., and Goswami, A., Enhancement of photon absorption in the light-harvesting complex of isolated chloroplast in the presence of plasmonic gold nanosol—a nanobionic approach towards photosynthesis and plant primary growth augmentation, Gold Bull., 2017, vol. 50, pp. 247–257.

    Article  CAS  Google Scholar 

  14. Dimkpa, C.O., McLean, J.E., Latta, D.E., Manangón, E., Britt, D.W., Johnson, W.P., Boyanov, M.I., and Anderson, A.J., CuO and ZnO nanoparticles: phytotoxicity, metal speciation, and induction of oxidative stress in sand-grown wheat, J. Nanopart. Res., 2012, vol. 14, pp. 1–15. https://doi.org/10.1007/s11051-012-1125-9

    Article  CAS  Google Scholar 

  15. Du, W., Gardea-Torresdey, J.L., Ji, R., Yin, Y., Zhu, J., Peralta-Videa, J.R., and Guo, H., Physiological and biochemical changes imposed by CeO2 nanoparticles on wheat: a life cycle field study, Environ. Sci. Technol., 2015, vol. 49, pp. 11884–11893.

    Article  CAS  PubMed  Google Scholar 

  16. Du, W., Tan, W., Peralta-Videa, J.R., Gardea-Torresdey, J.L., Ji, R., Yin, Y., and Guo, H., Interaction of metal oxide nanoparticles with higher terrestrial plants: physiological and biochemical aspects, Plant Physiol. Biochem., 2017, vol. 110, pp. 210–225.

    Article  CAS  PubMed  Google Scholar 

  17. Dutta Gupta, S., Agarwal, A., and Pradhan, S., Phytostimulatory effect of silver nanoparticles (AgNPs) on rice seedling growth: an insight from antioxidative enzyme activities and gene expression patterns, Ecotoxicol. Environ. Saf., 2018, vol. 161, pp. 624–633.

    Article  Google Scholar 

  18. Dykman, L.A. and Khlebtsov, N.G., Biomedical application of multifunctional gold nanocomposites, Usp. Sovrem. Biol., 2016, vol. 516, pp. 411–450.

    Google Scholar 

  19. Dykman, L. and Khlebtsov, N., Gold Nanoparticles in Biomedical Applications, Boca Raton, FL: CRC Press, 2017.

    Book  Google Scholar 

  20. Dykman, L.A. and Shchegolev, S.Yu., The interaction of plants with noble metal nanoparticles, S.-Kh. Biol., 2017, vol. 52, pp. 13–24.

    Google Scholar 

  21. Dykman, L.A. and Shchyogolev, S.Y., The effect of gold and silver nanoparticles on plant growth and development, in Metal Nanoparticles: Properties, Synthesis and Applications, Saylor, Y. and Irby, V., Eds., New York: Nova Sci. Publ., 2018, pp. 263–300.

    Google Scholar 

  22. Dykman, L.A., Bogatyrev, V.A., Shchegolev, S.Yu., and Khlebtsov, N.G., Zolotye nanochastitsy: sintez, svoistva, biomeditsinskoe primenenie (Gold Nanoparticles: Synthesis, Properties, and Biomedical Applications), Moscow: Nauka, 2008.

  23. Dykman, L.A., Bogatyrev, V.A., Sokolov, O.I., Plotnikov, V.K., Repko, N.V., and Salfetnikov, A.A., Interaction of gold, silver, and magnesium nanoparticles with plant objects, Nauchn. Zh. Kuban. Gos. Agr. Univ., 2016, no. 6, pp. 675–705.

  24. Elemike, E., Uzoh, I.M., Onwudiwe, D.C., and Babalola, O.O., The role of nanotechnology in the fortification of plant nutrients and improvement of crop production, Appl. Sci., 2019, vol. 9. https://doi.org/10.3390/app9030499

  25. Faizan, M., Faraz, A., Yusuf, M., Khan, S.T., and Hayat, S., Zinc oxide nanoparticles-mediated changes in photosynthetic efficiency and antioxidant system of tomato plants, Photosynthetica, 2018, vol. 56, pp. 678–686.

    Article  CAS  Google Scholar 

  26. Falco, W.F., Botero, E.R., Santiago, E.F., Bagnato, V.S., and Caires, A.R.L., In vivo observation of chlorophyll fluorescence quenching induced by gold nanoparticles, J. Photochem. Photobiol. Chem., 2011, vol. 225, pp. 65–71.

    Article  CAS  Google Scholar 

  27. Faraz, A., Faizan, M., Sami, F., Siddiqui, H., Pichtel, J., and Hayat, S., Nanoparticles: biosynthesis, translocation and role in plant metabolism, IET Nanobiotechnol., 2019, vol. 13, pp. 345–352.

    Article  PubMed  Google Scholar 

  28. Fayez, K.A., El-Deeb, B.A., and Mostafa, N.Y., Toxicity of biosynthetic silver nanoparticles on the growth, cell ultrastructure and physiological activities of barley plant, Acta Physiol. Plant., 2017, vol. 39. https://doi.org/10.1007/s11738-017-2452-3

  29. Fernández, A.P. and Strand, A., Retrograde signaling and plant stress: plastid signals initiate cellular stress responses, Curr. Opin. Plant Biol., 2008, vol. 11, pp. 509–513.

    Article  PubMed  Google Scholar 

  30. Gao, J., Xu, G., Qian, H., Liu, P., Zhao, P., and Hu, Y., Effects of nano-TiO2 on photosynthetic characteristics of Ulmus elongata seedlings, Environ. Pollut., 2013, vol. 176, pp. 63–70.

    Article  CAS  PubMed  Google Scholar 

  31. Gomez-Garay, A., Pintos, B., Manzanera, J.A., Lobo, C., Villalobos, N., and Martin, L., Uptake of CeO2 nanoparticles and its effect on growth of Medicago arborea in vitro plantlets, Biol. Trace Elem. Res., 2014, vol. 161, pp. 143–150.

    Article  CAS  PubMed  Google Scholar 

  32. Gorczyca, A., Pociecha, E., Kasprowicz, M., and Niemiec, M., Effect of nanosilver in wheat seedlings and Fusarium culmorum culture systems, Eur. J. Plant Pathol., 2015, vol. 142. https://doi.org/10.1007/s10658-015-0608-9

  33. Goswami, P., Yadav, S., and Mathur, J., Positive and negative effects of nanoparticles on plants and their applications in agriculture, Plant Sci. Today, 2019, vol. 6, pp. 232–242.

    Article  CAS  Google Scholar 

  34. Gray, C.G., Hansen, M.R., Shau, D.J., Graham, K., Dale, R., Natesan, S.K.A., and Newell, C.A., Plastid stromules are induced by stress treatments acting through abscisic acid, Plant J., 2012, vol. 69, pp. 387–398.

    Article  CAS  PubMed  Google Scholar 

  35. Hasanpour, H., Maali-Amiri, R., and Zeinali, H., Effect of TiO2 nanoparticles on metabolic limitations to photosynthesis under cold in chickpea, Russ. J. Plant Physiol., 2015, vol. 62, pp. 779–787.

    Article  CAS  Google Scholar 

  36. Hatami, M. and Ghorbanpour, M., Effect of nanosilver on physiological performance of pelargonium plants exposed to dark storage, J. Hortic. Res., 2013, vol. 21, pp. 15–20.

    Article  CAS  Google Scholar 

  37. Hong, F., Yang, F., Liu, Ch., Gao, Q., Wan, Zh., Gu, F., Wu, Ch., Ma, Zh., Zhou, J., and Yang, P., Influences of nano-TiO2 on the chloroplast aging of spinach under light, Biol. Trace Elem. Res., 2005a, vol. 104, pp. 249–260.

    Article  CAS  PubMed  Google Scholar 

  38. Hong, F., Zhou, J., Liu, Ch., Yang, F., Wu, Ch., Zheng, L., and Yang, P., Effect of nano-TiO2 on photochemical reaction of chloroplasts of spinach, Biol. Trace Elem. Res., 2005b, vol. 105, pp. 269–279.

    Article  CAS  PubMed  Google Scholar 

  39. Hong, J., Wang, L., Sun, Y., Zhao, L., Niu, G., Tan, W., Rico, C.M., Peralta-Videa, J.R., and Gardea-Torresdey, J.L., Foliar applied nanoscale and microscale CeO2 and CuO alter cucumber (Cucumis sativus) fruit quality, Sci. Total Environ., 2016, vols. 563–564, pp. 904–911.

    Article  PubMed  Google Scholar 

  40. Hossain, Z., Mustafa, G., and Komatsu, S., Plant responses to nanoparticle stress, Int. J. Mol. Sci., 2015, vol. 16, pp. 26644–26653.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Huner, N.P.M., Öquist, G., and Sarhan, F., Energy balance and acclimation to light and cold, Trends Plant Sci., 1998, vol. 3, pp. 1360–1385.

    Article  Google Scholar 

  42. Jayakannan, M., Bose, J., Babourina, O., Rengel, Z., and Shabala, S., Salicylic acid in plant salinity stress signalling and tolerance, Plant Growth Regul., 2015, vol. 76, pp. 25–40.

    Article  CAS  Google Scholar 

  43. Jiang, H.-S., Qiu, X.-N., Li, G.-B., Li, W., and Yin, L.-Y., Silver nanoparticles induced accumulation of reactive oxygen species and alteration of antioxidant systems in the aquatic plant Spirodela polyrhiza, Environ. Toxicol. Chem., 2014, vol. 33, pp. 1398–1405.

    Article  CAS  PubMed  Google Scholar 

  44. Joshi, H., Somdutt Choudhary, P., and Mundra, S.L., Future prospects of nanotechnology in agriculture, Int. J. Chem. Stud., 2019, vol. 7, pp. 957–963.

    CAS  Google Scholar 

  45. Khan, M.R., Adam, V., Rizvi, T.F., Zhang, B., Ahamad, F., Josko, I., Zhu, Y., Yang, M., and Mao, C., Nanoparticle–plant interactions: two-way traffic, Small, 2019, vol. 15. https://doi.org/10.1002/smll.201901794

  46. Klimov, S.V., Plant adaptation to stress through changes in donor–acceptor relations at different levels of structural organization, Usp. Sovrem. Biol., 2008, vol. 128, pp. 281–299.

    Google Scholar 

  47. Van Koetsem, F., Xiao, Y., Luo, Z., and Laing, G.D., Impact of water composition on association of Ag and CeO2 nanoparticles with aquatic macrophyte Elodea canadensis, Environ. Sci. Pollut. Res., 2016, vol. 23, pp. 5277–5287.

    Article  CAS  Google Scholar 

  48. Kӧhler, R.H., Schwille, P., Webb, W.W., and Hanson, M.R., Active protein transport through plastid tubules: velocity quantified by fluorescence correlation spectroscopy, J. Cell Sci., 2000, vol. 113, pp. 3921–3930.

    Article  Google Scholar 

  49. Koshkin, E.I., Fiziologiya ustoichivosti sel’skokhozyaistvennykh rastenii (Physiology of Agricultural Plant Resistance), Moscow: Kolos, 2010.

  50. Kratsch, H.A. and Wise, R.R., The ultrastructure of chilling stress, Plant, Cell Environ., 2000, vol. 23, pp. 337–350.

    Article  CAS  Google Scholar 

  51. Kuznetsov, V.V. and Dmitrieva, G.D., Fiziologiya rastenii (Plant Physiology), Moscow: Abris, 2011.

  52. Lalau, C.M., Mohedano, R.D.A., Schmidt, É.C., Bouzon, Z.L., Ouriques, L.C., Dos Santos, R.W., Da Costa, C.H., Vicentini, D.S., and Matias, W.G., Toxicological effects of copper oxide nanoparticles on the growth rate, photosynthetic pigment content, and cell morphology of the duckweed Landoltia punctata, Protoplasma, 2015, vol. 252, pp. 221–229.

    Article  CAS  PubMed  Google Scholar 

  53. Lei, Z., Mingyu, S., Xiao, W., Chao, L., Chunxiang, Q., Liang, C., Hao, H., Xiaoqing, L., and Fashui, H., Antioxidant stress is promoted by nano-anatase in spinach chloroplasts under UV-B radiation, Biol. Trace Elem. Res., 2008, vol. 121, pp. 69–79.

    Article  PubMed  Google Scholar 

  54. Liu, X., Wang, F., Shi, Z., Tong, R., and Shi, X., Bioavailability of Zn in ZnO nanoparticle-spiked soil and the implications to maize plants, J. Nanopart. Res., 2015, vol. 17. https://doi.org/10.1007/s11051-015-2989-2

  55. Lütz, C. and Engel, L., Changes in chloroplast ultrastructure in some high-alpine plants: adaptation to metabolic demands and climate?, Protoplasma, 2007, vol. 231, pp. 183–192.

    Article  PubMed  Google Scholar 

  56. Ma, C.X., Chhikara, S., Xing, B.S., Musante, C., White, J.C., and Dhankher, O.P., Physiological and molecular response of Arabidopsis thaliana (L.) to nanoparticle cerium and indium oxide exposure, ACS Sustain. Chem. Eng., 2013, vol. 1, pp. 768–778.

    Article  CAS  Google Scholar 

  57. Mahakham, W., Theerakulpisut, P., Maensiri, S., Phumying, S., and Sarmah, A.K., Environmentally benign synthesis of phytochemicals-capped gold nanoparticles as nanopriming agent for promoting maize seed germination, Sci. Total Environ., 2016, vol. 573, pp. 1089–1102.

    Article  CAS  PubMed  Google Scholar 

  58. Majumdar, S., Peralta-Videa, J.R., Trujillo-Reyes, J., Sun, Y., Barrios, A.C., Niu, G., Margez, J.P.F., and Gardea-Torresdey, J.L., Soil organic matter influences cerium translocation and physiological processes in kidney bean plants exposed to cerium oxide nanoparticles, Sci. Total Environ., 2016, vols. 569–570, pp. 201–211.

    Article  PubMed  Google Scholar 

  59. Martínez-Peñalver, A., Graña, E., Reigosa, M.J., and Sánchez-Moreiras, A.M., Early photosynthetic response of Arabidopsis thaliana to temperature and salt stress conditions, Russ. J. Plant Physiol., 2012, vol. 59, pp. 640–647.

    Article  Google Scholar 

  60. Marusenko, Y., Shipp, J., Hamilton, G.A., Morgan, J.L.L., Keebaugh, M., Hil, H., Dutta, A., Zhuo, X., Upadhyay, N., Hutchings, J., Herckes, P., Anbar, A.D., Shock, E., and Hartnett, H.E., Bioavailability of nanoparticulate hematite to Arabidopsis thaliana, Environ. Pollut., 2013, vol. 174, pp. 150–156.

    Article  CAS  PubMed  Google Scholar 

  61. Medvedev, S.S. and Sharova, E.I., Biologiya razvitiya rastenii (Plant Developmental Biology), vol. 1: Nachala biologii razvitiya rastenii. Fitogormony (Fundamentals of Plant Biology. Phytohormones), St. Petersburg: St.-Peterb. Gos. Univ., 2011.

  62. Mingyu, S., Fashui, H., Chao, L., Xiao, W., Xiaoqing, L., Liang, C., Fengqing, G., and Zhongrui, L., Effects of nano-anatase TiO2 on absorption, distribution of light, and photoreduction activities of chloroplast membrane of spinach, Biol. Trace Elem. Res., 2007, vol. 118, pp. 120–130.

    Article  PubMed  Google Scholar 

  63. Mohamed, A.K.S.H., Qayyum, M.F., Abdel-Hadi, A.M., Rehman, R.A., Ali, S., and Rizwan, M., Interactive effect of salinity and silver nanoparticles on photosynthetic and biochemical parameters of wheat, Arch. Agron. Soil Sci., 2017, vol. 63, pp. 1736–1747.

    Article  CAS  Google Scholar 

  64. Mokronosov, A.T., Gavrilenko, V.F., and Zhigalova, T.V., Fotosintez. Fiziologo-ekologicheskie i biokhimicheskie aspekty (Photosynthesis: Physiological, Ecological, and Biochemical Aspects), Moscow: Akademiya, 2006.

  65. Mukherjee, A., Peralta-Videa, J.R., Bandyopadhyay, S., Rico, C.M., Zhao, L., and Gardea-Torresdey, J.L., Physiological effects of nanoparticulate ZnO in green peas (Pisum sativum L.) cultivated in soil, Metallomics, 2014, vol. 6, pp. 132–138.

    Article  CAS  PubMed  Google Scholar 

  66. Nair, P.M.G. and Chung, I.M., A mechanistic study on the toxic effect of copper oxide nanoparticles in soybean (Glycine max L.) root development and lignification of root cells, Biol. Trace Elem. Res., 2014a, vol. 162, pp. 342–352.

    Article  CAS  PubMed  Google Scholar 

  67. Nair, P.M.G. and Chung, I.M., Impact of copper oxide nanoparticles exposure on Arabidopsis thaliana growth, root system development, root lignification, and molecular level changes, Environ. Sci. Pollut. Res., 2014b, vol. 21, pp. 12709–12722.

    Article  CAS  Google Scholar 

  68. Nair, P.M.G. and Chung, I.M., Physiological and molecular level effects of silver nanoparticles exposure in rice (Oryza sativa L.) seedlings, Chemosphere, 2014c, vol. 112, pp. 105–113.

    Article  CAS  PubMed  Google Scholar 

  69. Nair, P.M.G. and Chung, I.M., Study on the correlation between copper oxide nanoparticles induced growth suppression and enhanced lignification in Indian mustard (Brassica juncea L.), Ecotoxicol. Environ. Saf., 2015, vol. 113, pp. 302–313.

    Article  CAS  PubMed  Google Scholar 

  70. Nair, P.M.G., Kim, S.H., and Chung, I.M., Copper oxide nanoparticle toxicity in mung bean (Vigna radiata L.) seedlings: physiological and molecular level responses of in vitro grown plants, Acta Physiol. Plant., 2014, vol. 36, pp. 2947–2958.

    Article  Google Scholar 

  71. Nayan, R., Rawat, M., Negi, B., Pande, A., and Arora, S., Zinc sulfide nanoparticle mediated alterations in growth and anti-oxidant status of Brassica juncea, Biologia, 2016, vol. 71, pp. 896–902.

    Article  CAS  Google Scholar 

  72. Nekrasova, G.F., Ushakova, O.S., Ermakov, A.E., Uimin, M.A., and Byzov, I.V., Effects of copper(II) ions and copper oxide nanoparticles on Elodea densa Planch., Russ. J. Ecol., 2011, vol. 42, no. 6, pp. 458–463.

  73. Notter, D.A., Mitrano, D.M., and Nowack, B., Are nanosized or dissolved metals more toxic in the environment? A meta-analysis, Environ. Toxicol. Chem., 2014, vol. 33, pp. 2733–2739.

    Article  CAS  PubMed  Google Scholar 

  74. Novikova, G.V., Stepanchenko, N.S., Nosov, A.V., and Moshkov, I.E., At the beginning of the route: ABA perception and signal transduction in plants, Russ. J. Plant Physiol., 2009, vol. 56, pp. 727–741.

    Article  CAS  Google Scholar 

  75. Paramonova, N.V., Shevyakova, N.I., and Kuznetsov, Vl.V., Ultrastructure of chloroplasts and their storage inclusions in the primary leaves of Mesembryanthemum crystallinum affected by putrescine and NaCl, Russ. J. Plant Physiol., 2004, vol. 51, pp. 86–96.

    Article  CAS  Google Scholar 

  76. Perreault, F., Oukarroum, A., Pirastru, L., Sirois, L., Matias, W.G., and Popovic, R., Evaluation of copper oxide nanoparticles toxicity using chlorophyll a fluorescence imaging in Lemna gibba, J. Bot, 2010, vol. 2010. https://doi.org/10.1155/2010/763142

  77. Prasad, T., Sudhakar, P., Sreenivasulu, Y., Latha, P., Munaswamy, V., Raja Reddy, K., Sreeprasad, T.S., Sajanlal, P.R., and Pradeep, T., Effect of nanoscale zinc oxide particles on the germination, growth and yield of peanut, J. Plant Nutr., 2012, vol. 35, pp. 905–927.

    Article  CAS  Google Scholar 

  78. Pribil, M., Labs, M., and Leister, D., Structure and dynamics of thylakoids in land plants, J. Exp. Bot., 2014, vol. 65, pp. 1955–1972.

    Article  CAS  PubMed  Google Scholar 

  79. Qi, M., Liu, Yu., and Li, T., Nano-TiO2 improve the photosynthesis of tomato leaves under mild heat stress, Biol. Trace Elem. Res., 2013, vol. 156, pp. 323–328.

    Article  CAS  PubMed  Google Scholar 

  80. Qian, H., Peng, X., Han, X., Ren, J., Sun, L., and Fu, Zh., Comparison of the toxicity of silver nanoparticles and silver ions on the growth of terrestrial plant model Arabidopsis thaliana, J. Environ. Sci., 2013, vol. 25, pp. 1947–1955.

    Article  CAS  Google Scholar 

  81. Raliya, R. and Tarafdar, J.C., ZnO nanoparticle biosynthesis and its effect on phosphorous-mobilizing enzyme secretion and gum contents in clusterbean (Cyamopsis tetragonoloba L.), Agric. Res., 2013, vol. 2, pp. 48–57.

    Article  CAS  Google Scholar 

  82. Raliya, R., Nair, R., Chavalmane, S., Wang, W.N., and Biswas, P., Mechanistic evaluation of translocation and physiological impact of titanium dioxide and zinc oxide nanoparticles on the tomato (Solanum lycopersicum L.) plant, Metallomics, 2015, vol. 7, pp. 1584–1594.

    Article  CAS  PubMed  Google Scholar 

  83. Ramesh, M., Palanisamy, K., and Babu, N.K., Effects of bulk and nano-titanium dioxide and zinc oxide on physiomorphological changes in Triticum aestivum Linn., J. Global Biosci., 2014, vol. 3, pp. 415–422.

    Google Scholar 

  84. Rani, P.U., Yasur, J., Loke, K.S., and Dutta, D., Effect of synthetic and biosynthesized silver nanoparticles on growth, physiology and oxidative stress of water hyacinth: Eichhornia crassipes (Mart) Solms, Acta Physiol. Plant., 2016, vol. 38. https://doi.org/10.1007/s11738-016-2074-1

  85. Rico, C.M., Morales, M.I., Barrios, A.C., McCreary, R., Hong, J., Lee, W.Y., Nunez, J., Peralta-Videa, J.R., and Gardea-Torresdey, J.L., Effect of cerium oxide nanoparticles on the quality of rice (Oryza sativa L.) grains, J. Agric. Food Chem., 2013, vol. 61, pp. 11278–11285.

    Article  CAS  PubMed  Google Scholar 

  86. Rico, C.M., Peralta-Videa, J.R., and Gardea-Torresdey, J.L., Chemistry, biochemistry of nanoparticles, and their role in antioxidant defense system in plants, in Nanotechnology and Plant Sciences: Nanoparticles and Their Impact on Plants, Siddiqui, M.H., Al-Whaibi, M.H., and Mohammad, F.N.Y, Eds., New York: Springer, 2015, pp. 1–17.

    Google Scholar 

  87. Rizwan, M., Ali, Sh., Qayyum, M.F., Ok, Y.S., Adrees, M., Ibrahim, M., Zia-ur-Rehman, M., Farid, M., and Abbas, F., Effect of metal and metal oxide nanoparticles on growth and physiology of globally important food crops: a critical review, J. Hazard. Mater., 2016, vol. 322, pp. 2–16.

    Article  PubMed  Google Scholar 

  88. Salama, H.M.H., Effects of silver nanoparticles in some crop plants, common bean (Phaseolus vulgaris L.) and corn (Zea mays L.), Int. Res. J. Biotech., 2012, vol. 3, pp. 190–197.

    Google Scholar 

  89. Sanzari, I., Leone, A., and Ambrosone, A., Nanotechnology in plant science: to make a long story short, Front. Bioeng. Biotechnol., 2019, vol. 7. https://doi.org/10.3389/fbioe.2019.00120

  90. Servin, A.D., Morales, M.I., Castillo-Michel, H., Hernandez-Viezcas, J.A., Munoz, B., Zhao, L.J., Nunez, J.E., Peralta-Videa, J.R., and Gardea-Torresdey, J.L., Synchrotron verification of TiO2 accumulation in cucumber fruit: a possible pathway of TiO2 nanoparticle transfer from soil into the food chain, Environ. Sci. Technol., 2013, vol. 47, pp. 11592–11598.

    Article  CAS  PubMed  Google Scholar 

  91. Shabnam, N., Sharmila, P., and Pardha-Saradhi, P., Impact of ionic and nanoparticle speciation states of silver on light harnessing photosynthetic events in Spirodela polyrhiza, Int. J. Phytoremediat., 2017, vol. 19, pp. 80–86.

    Article  CAS  Google Scholar 

  92. Sharma, P., Bhatt, D., Zaidi, M.G.H., Saradhi, P.P., Khanna, P.K., and Arora, S., Silver nanoparticle-mediated enhancement in growth and antioxidant status of Brassica juncea, Appl. Biochem. Biotechnol., 2012, vol. 167, pp. 2225–2233.

    Article  CAS  PubMed  Google Scholar 

  93. Shi, J., Abid, A.D., Kennedy, I.M., Hristova, K.R., and Silk, W.K., To duckweeds (Landoltia punctata), nanoparticulate copper oxide is more inhibitory than the soluble copper in the bulk solution, Environ. Pollut., 2011, vol. 159, pp. 1277–1282.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Shi, J., Peng, C., Yang, Y., Yang, J., Zhang, H., Yuan, X., Chen, Y., and Hu, T., Phytotoxicity and accumulation of copper oxide nanoparticles to the cu-tolerant plant Elsholtzia splendens, Nanotoxicology, 2014, vol. 8, pp. 179–188.

    Article  CAS  PubMed  Google Scholar 

  95. Song, U., Jun, H., Waldman, B., Roh, J., Kim, Y., Yi, J., and Lee, E.J., Functional analyses of nanoparticle toxicity: a comparative study of the effects of TiO2 and Ag on tomatoes (Lycopersicon esculentum), Ecotoxicol. Environ. Saf., 2013, vol. 93, pp. 60–67.

    Article  CAS  PubMed  Google Scholar 

  96. Sosan, A., Svistunenko, D., Straltsova, D., Tsiurkina, K., Smolich, I., Lawson, T., Subramaniam, S., Golovko, V., Anderson, D., Sokolik, A., Colbeck, I., and Demidchik, V., Engineered silver nanoparticles are sensed at the plasma membrane and dramatically modify the physiology of Arabidopsis thaliana plants, Plant J., 2016, vol. 85, pp. 245–257.

    Article  CAS  PubMed  Google Scholar 

  97. Syu, Y.-Y., Hung, J.-H., Chen, J.-C., and Chuang, H.-W., Impacts of size and shape of silver nanoparticles on Arabidopsis plant growth and gene expression, Plant Physiol. Biochem., 2014, vol. 83, pp. 57–64.

    Article  CAS  PubMed  Google Scholar 

  98. Tighe-Neira, R., Carmorac, E., Recioc, G., Nunes-Nesid, A., Reyes-Diaze, M., Alberdie, M., Rengelg, Z., and Inostroza-Blancheteau, C., Metallic nanoparticles influence the structure and function of the photosynthetic apparatus in plants, Plant Physiol. Biochem., 2018, vol. 130, pp. 408–417.

    Article  CAS  PubMed  Google Scholar 

  99. Titov, A.F. and Shibaeva, T.G., Brassinosteroidy (Brassinosteroids), Petrozavodsk: Karel. Nauchn. Tsentr Ross. Akad. Nauk, 2013.

    Google Scholar 

  100. Titov, A.F. and Talanova, V.V., Ustoichivost’ rastenii i fitogormony (Plant Resistance and Phytohormones), Petrozavodsk: Karel. Nauchn. Tsentr Ross. Akad. Nauk, 2009.

  101. Tombuloglu, H., Slimani, Y., Tombuloglu, G., Almessiere, M., and Baykal, A., Uptake and translocation of magnetite (Fe3O4) nanoparticles and its impact on photosynthetic genes in barley (Hordeum vulgare L.), Chemosphere, 2019, vol. 226, pp. 110–122.

    Article  CAS  PubMed  Google Scholar 

  102. Torres, R., Diz, V., and Lagorio, M.G., Effects of gold nanoparticles on the photophysical and photosynthetic parameters of leaves and chloroplasts, Photochem. Photobiol. Sci., 2018, vol. 17, pp. 505–516.

    Article  CAS  PubMed  Google Scholar 

  103. Tripathi, D.K., Gaur, S., Singh, S., Singh, S., Pandey, R., Singh, V.P., Sharma, N.C., Prasad, S.M., Dubey, N.K., and Chauhan, D.K., An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity, Plant Physiol. Biochem., 2017, vol. 110, pp. 2–12.

    Article  CAS  PubMed  Google Scholar 

  104. Trujillo-Reyes, J., Majumdar, S., Botez, C.E., Peralta-Videa, J.R., and Gardea-Torresdey, J.L., Exposure studies of core-shell Fe/Fe3O4 and Cu/CuO NPs to lettuce (Lactuca sativa) plants: are they a potential physiological and nutritional hazard?, J. Hazard. Mater., 2014, vol. 267, pp. 255–263.

    Article  CAS  PubMed  Google Scholar 

  105. Trunova, T.I., Rastenie i nizkotemperaturnyi stress. 64-e Timiryazevskoe chtenie (Plant and Low-Temperature Stress. 64th Timiryazev Memorial Lectures), Moscow: Nauka, 2007.

  106. Usmanov, I.Yu., Rakhmankulova, E.F., and Kulagin, A.Yu., Ekologicheskaya fiziologiya rastenii (Ecological Plant Physiology), Moscow: Logos, 2001.

  107. Venzhik, Yu.V., Titov, A.F., Talanova, V.V., Miroslavov, E.A., and Koteeva, N.K., Structural and functional reorganization of the photosynthetic apparatus of wheat plants during cold adaptation, Tsitologiya, 2012, vol. 54, pp. 916–924.

    Google Scholar 

  108. Venzhik, Yu., Talanova, V., and Titov, A., The effect of abscisic acid on cold tolerance and chloroplasts ultrastructure in wheat under optimal and cold stress conditions, Acta Physiol. Plant., 2016, vol. 38. https://doi.org/10.1007/s11738-016-2082-1

  109. Veselov, D.S., Kudoyarova, G.R., Kudryakova, N.V., and Kuznetsov, V.V., Role of cytokinins in stress resistance of plants, Russ. J. Plant Physiol., 2017, vol. 64, pp. 15–27.

    Article  CAS  Google Scholar 

  110. Wan, Y., Li, J., Ren, H., Huang, J., and Yuan, H., Physiological investigation of gold nanorods toward watermelon, J. Nanosci. Nanotechnol., 2014, vol. 14, pp. 6089–6094.

    Article  CAS  PubMed  Google Scholar 

  111. Wang, J., Koo, Y., Alexander, A., Yang, Y., Westerhof, S., Zhang, Q., Schnoor, J.L., Colvin, V.L., Braam, J., and Alvarez, P.J.J., Phytostimulation of poplars and Arabidopsis exposed to silver nanoparticles and Ag+ at sublethal concentrations, Environ. Sci. Technol., 2013, vol. 47, pp. 5442–5449.

    Article  CAS  PubMed  Google Scholar 

  112. Wang, X., Yang, X., Chen, S., Li, Q., Wang, W., Hou, Ch., Gao, X., Wangand, L., and Wang, Sh., Zinc oxide nanoparticles affect biomass accumulation and photosynthesis in Arabidopsis, Plant Sci., 2016, vol. 6. https://doi.org/10.3389/fpls.2015.01243

  113. Wei, H. and Wang, E., Nanomaterials with enzyme-like characteristics (nanozymes): next-generation artificial enzymes, Chem. Sov. Rev., 2013, vol. 42, pp. 6060–6093.

    Article  CAS  Google Scholar 

  114. Wen, Y., Zhang, L., Chen, Z., Sheng, X., Qiu, J., and Xu, D., Co-exposure of silver nanoparticles and chiral herbicide imazethapyr to arabidopsis thaliana: enantioselective effects, Chemosphere, 2016, vol. 145, pp. 207–214.

    Article  CAS  PubMed  Google Scholar 

  115. Xiong, T., Dumat, C., Dappe, V., Vezin, H., Schreck, E., Shahid, M., Pieral, A., and Sobanska, S., Copper oxide nanoparticle foliar uptake, phytotoxicity, and consequences for sustainable urban agriculture, Environ. Sci. Technol., 2017, vol. 51, pp. 5242–5251.

    Article  CAS  PubMed  Google Scholar 

  116. Yadu, B., Chandrakar, V., Korram, J., Satnami, M.L., Kumar, M., and Keshavkant, S., Silver nanoparticle modulates gene expressions, glyoxalase system and oxidative stress markers in fluoride stressed Cajanus cajan L, J. Hazard. Mater., 2018, vol. 353, pp. 44–52.

    Article  CAS  PubMed  Google Scholar 

  117. Yamane, K., Kawasaki, M., Tanguchi, M., and Miyake, H., Correlation between chloroplast ultrastructure and chlorophyll fluorescence characteristics in the leaves of rice (Oryza sativa L.) grown under salinity, Plant Prod. Sci., 2008, vol. 11, pp. 139–145.

    Article  CAS  Google Scholar 

  118. Yang, F., Liu, Ch., Gao, F., Su, M., Wu, X., Zheng, L., Hong, F., and Yang, P., The improvement of spinach growth by nano-anatase TiO2 treatment is related to nitrogen photoreduction, Biol. Trace Elem. Res., 2007, vol. 119, pp. 77–88.

    Article  CAS  PubMed  Google Scholar 

  119. Yang, J., Cao, W., and Rui, Y., Interactions between nanoparticles and plants: phytotoxicity and defense mechanisms, J. Plant Interact., 2017, vol. 12, pp. 158–169.

    Article  CAS  Google Scholar 

  120. Yasur, J. and Rani, P.U., Environmental effects of nanosilver: impact on castor seed germination, seedling growth, and plant physiology, Environ. Sci. Pollut. Res., 2013, vol. 20, pp. 8636–8648.

    Article  CAS  Google Scholar 

  121. Zhang, W., Ebbs, S.D., Musante, C., White, J.C., Gao, C., and Ma, X., Uptake and accumulation of bulk and nanosized cerium oxide particles and ionic cerium by radish (Raphanus sativus L.), J. Agric. Food Chem., 2015, vol. 63, pp. 382–390.

    Article  CAS  PubMed  Google Scholar 

  122. Zhao, L., Sun, Y., Hernandez-Viezcas, J.A., Hong, J., Majumdar, S., Niu, G., Duarte-Gardea, J.M., Peralta-Videa, J.R., and Gardea-Torresdey, J.L., Monitoring the environmental effects of CeO2 and ZnO nanoparticles through the life cycle of corn (Zea mays) plants and in situ μ-XRF mapping of nutrients in kernels, Environ. Sci. Technol., 2015, vol. 49, pp. 2921–2928.

    Article  CAS  PubMed  Google Scholar 

  123. Zheng, L., Hong, F.S., Lu, S.P., and Liu, C., Effect of nano-TiO2 on strength of naturally aged seeds and growth of spinach, Biol. Trace Elem. Res., 2005, vol. 104, pp. 83–91.

    Article  CAS  PubMed  Google Scholar 

  124. Zou, X., Li, P., Huang, Q., and Zhang, H., The different response mechanisms of Wolffia globosa: light-induced silver nanoparticle toxicity, Aquat. Toxicol., 2016, vol. 176, pp. 97–105.

    Article  CAS  PubMed  Google Scholar 

  125. Zuverza-Mena, N., Martínez-Fernández, D., Du, W., Hernandez-Viezcas, J.A., Bonilla-Bird, N., López-Moreno, M.L., Komárek, M., Peralta-Videa, J.R., and Gardea-Torresdey, J.L., Exposure of engineered nanomaterials to plants: insights into the physiological and biochemical responses—a review, Plant Physiol. Biochem., 2017, vol. 110, pp. 236–264.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the Russian Foundation for Basic Research, project no. 18-04-00469.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yu. V. Venzhik.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by A. Aver’yanov

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Venzhik, Y.V., Moshkov, I.E. & Dykman, L.A. Influence of Nanoparticles of Metals and Their Oxides on the Photosynthetic Apparatus of Plants. Biol Bull Russ Acad Sci 48, 140–155 (2021). https://doi.org/10.1134/S106235902102014X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S106235902102014X

Navigation