Skip to main content
SpringerLink
Log in

Ultrastructural Reorganization of Chloroplasts during Plant Adaptation to Abiotic Stress Factors

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

Abstract

This review presents a comparative analysis of the literature and the authors’ data on the ultrastructural reorganization of plant chloroplasts adapting to abiotic factors of different nature—low temperature (factor of a physical nature) and chloride salinity (factor of a chemical nature). All ultrastructural changes in chloroplasts are considered in close relationship to the physiological, biochemical, and functional adaptive changes of the photosynthetic apparatus (PSA). The review discusses the adaptive value and emphasizes the nonspecific nature of ultrastructural transformations occurring in plant chloroplasts under abiotic stress. A separate section considers the effect of metal nanoparticles on the PSA and the nanoparticle-aided modeling of the PSA responses to stresses.

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.

Similar content being viewed by others

REFERENCES

  1. Biswal, B. and Biswal, U.C., Photosynthesis under stress: stress signals and adaptive response of chloroplasts, in Handbook of Plant and Crop Stress, Pessarakli, M., Ed., New York: Marcel Dekker, 1999, pp. 315–336.

    Google Scholar 

  2. 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 

  3. 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 N-aCl, Russ. J. Plant Physiol., 2004, vol. 51, pp. 86–96.

    Article  CAS  Google Scholar 

  4. 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  CAS  Google Scholar 

  5. Venzhik, Yu.V., Titov, A.F., Talanova, V.V., Miroslavov, E.A., and Koteeva, N.K., Structural and functional reorganization of the photosynthetic apparatus in adaptation to cold of wheat plants, Cell Tissue Biol., 2013, vol. 7, pp. 168–176.

    Article  Google Scholar 

  6. Astakhova, N.V., Popov, V.N., Selivanov, A.A., Burakhanova, E.A., Alieva, G.P., and Moshkov, I.E., Reorganization of chloroplast ultrastructure associated with low-temperature hardening of Arabidopsis plants, Russ. J. Plant Physiol., 2014, vol. 61, pp. 744–750.

    Article  CAS  Google Scholar 

  7. Ivanova, T.V., Maiorova, O.V., Orlova, Yu.V., Kuznetsova, E.I., Khalilova, L.A., Myasoedov, N.A., Balnokin, Yu.V., and Tsydendambaev, V.D., Cell ultrastructure and fatty acid composition of lipids in vegetative organs of Chenopodium album L. under salt stress conditions, Russ. J. Plant Physiol., 2016, vol. 63, pp. 763–775.

    Article  CAS  Google Scholar 

  8. 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 

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

  10. Rozentsvet, O.A., Nesterov, V.N., and Bogdanova, E.S., Structural, physiological, and biochemical aspects of salinity tolerance of halophytes, Russ. J. Plant Physiol., 2017, vol. 64, pp. 464–477.

    Article  CAS  Google Scholar 

  11. Gong, M., Chen, B., Li, Z.G., and Guo, L.H., Heat-shock-induced cross adaptation to heat, chilling, drought and salt stress in maize seedlings and involvement of H2O2, J. Plant Physiol., 2001, vol. 158, pp. 1125–1130.

    Article  CAS  Google Scholar 

  12. Beck, E.H., Fettig, S., Knake, C., Hartigi, K., and Bhattarai, T., Specific and unspecific responses of plants to cold and drought stress, J. Biosci., 2007, vol. 32, pp. 501–510.

    Article  CAS  PubMed  Google Scholar 

  13. Dykman, L.A. and Shchyogolev, S.Yu., Interactions of plants with noble metal nanoparticles (Review), S.-kh.Biol., 2017, vol. 52, pp. 13–24.

    Google Scholar 

  14. 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 

  15. 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 

  16. Taylor, A.O. and Craig, A.S., Plants under climatic stress. II. Low temperature, high light effects on chloroplast ultrastructure, Plant Physiol., 1971, vol. 47, pp. 719–725.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ma, S., Lin, C., and Chen, Y., Comparative studies of chilling stress on alterations of chloroplast ultrastructure and protein synthesis in the leaves of chilling-sensitive (mung bean) and -insensitive (pea) seedlings, Bot. Bull. Acad. Sin., 1990, vol. 31, pp. 263–272.

    Google Scholar 

  18. Klimov, S.V., Davydenko, S.V., Novitskaya, G.V., Astakhova, N.V., Karasev, G.S., Suvorova, T.A., and Trunova, T.I., On the nature of the different frost resistance of winter rye and wheat plants. 2. Chloroplast ultrastructure, photosynthesis, protein, lipid, and fatty acid composition of the first leaf under cold hardening, Russ. Plant Physiol., 1993, vol. 40, pp. 627–635.

    CAS  Google Scholar 

  19. Klimov, S.V., Astakhova, N.V., and Trunova, T.I., Relationship between plant cold tolerance, photosynthesis and ultrastructural modifications of cells and chloroplasts, Russ. J. Plant Physiol., 1997, vol. 44, pp. 759–765.

    CAS  Google Scholar 

  20. Trunova, T.I. and Astakhova, N.I., The role of cell ultrastructure in the formation of frost resistance in winter wheat, Dokl. Akad. Nauk, 1998, vol. 359, pp. 120–122.

    CAS  Google Scholar 

  21. Vella, N.G.F., Joss, T.V., and Roberts, T.H., Chilling-induced ultrastructural changes to mesophyll cells of Arabidopsis grown under short days are almost completely reversible by plant re-warming, Protoplasma, 2012, vol. 249, pp. 1137–1149.

    Article  CAS  PubMed  Google Scholar 

  22. Venzhik, Yu.V., Titov, A.F., Talanova, V.V., and Miroslavov, E.A., Ultrastructure and functional activity of chloroplasts in wheat leaves under root chilling, Acta Physiol. Plant., 2014, vol. 36, pp. 323–330.

    Article  CAS  Google Scholar 

  23. 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: 63. https://doi.org/10.1007/s11738-016-2082-1

    Article  CAS  Google Scholar 

  24. Huner, N.P.A., Elfman, B., Krol, M., and McIntosh, A., Growth and development at cold-hardening temperatures. Chloroplast ultrastructure, pigment content and composition, Can. J. Bot., 1984, vol. 62, pp. 53–60.

    Article  CAS  Google Scholar 

  25. Huner, N.P.A., Morphological, anatomical, and molecular consequences of growth and development at low temperature in Secale cereale L. cv. Puma, Am. J. Bot., 1985, vol. 72, pp. 1290–1306.

    Article  CAS  Google Scholar 

  26. O'Neil, S.D., Priestley, D.A., and Chabot, B.F., Temperature and aging effects on leaf membranes of a cold hardy perennial, Fragaria virginiana,Plant Physiol., 1981, vol. 68, pp. 1409–1415.

    Article  Google Scholar 

  27. Guy, C.L., Cold acclimation and freezing stress tolerance: role of protein metabolism, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1990, vol. 41, pp. 187–223.

    Article  CAS  Google Scholar 

  28. Los, D.A., Molecular mechanisms of cold tolerance in plants, Her. Russ. Acad. Sci., 2005, vol. 75, pp. 149–155.

    Google Scholar 

  29. Ensminger, I., Busch, F., and Huner, N., Photostasis and cold acclimation: sensing low temperature through photosynthesis, Physiol. Plant., 2006, vol. 126, pp. 28–44.

    Article  CAS  Google Scholar 

  30. Uemura, M., Tominaga, Y., Nakagawara, C., Shigematsu, S., Minami, A., and Kowamura, Y., Responses of the plasma membrane to low temperatures, Physiol. Plant., 2006, vol. 126, pp. 81–89.

    Article  CAS  Google Scholar 

  31. Kreslavski, V.D., Carpentier, R., Klimov, V.V., Murata, N., and Allakhverdiev, S.I., Molecular mechanisms of stress resistance of the photosynthetic apparatus, Biochemistry (Moscow), Suppl. Ser. A: Membr. Cell B-iol., 2007, vol. 1, pp. 185–205.

    Google Scholar 

  32. Kreslavski, V.D., Los, D.A., Allakhverdiev, S.I., and Kuznetsov, Vl.V., Signaling role of reactive oxygen species in plants under stress, Russ. J. Plant Physiol., 2012, vol. 59, pp. 141–154.

    Article  CAS  Google Scholar 

  33. Theocharis, A., Clément, C., and Barka, E.A., Physiological and molecular changes in plants grown at low temperatures, Planta, 2012, vol. 235, pp. 1091–1105.

    Article  CAS  PubMed  Google Scholar 

  34. Holzinger, A., Wasteneys, G.O., and Lütz, C., Investigating cytoskeletal function in chloroplast protrusion formation in the arctic-alpine plant Oxyria digyna,Plant Biol. (Stuttgart), 2007, vol. 9, pp. 400–410.

    Article  CAS  PubMed  Google Scholar 

  35. 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 

  36. 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 

  37. Lichtenthaler, H.K., Biosynthesis, accumulation and emission of carotenoids, α-tocopherol, plastoquinone, and isoprene in leaves under high photosynthetic irradiance, Photosynth. Res., 2007, vol. 92, pp. 163–179.

    Article  CAS  PubMed  Google Scholar 

  38. Anderson, J.M., Insights into the consequences of grana stacking of thylakoid membranes in vascular plants: a personal perspective, Aust. J. Plant Physiol., 1999, vol. 26, pp. 625–639.

    CAS  Google Scholar 

  39. Bobylev, G.S., Timonina, V.N., and Sorokin, E.M., The lability of the chloroplast membranes in the plant adapting to temperature alteration, Sov. Plant Physiol., 1992, vol. 39, pp. 541–551.

    Google Scholar 

  40. Orlov, V.P., Sokolova, M.K., and Sokolov, O.I., F-actin and actin-associated protein 56 kD organization in plant cells during cold-shock conditions, Proc. All-Russian Sci. Conf. “Resistance of Organisms to Adverse Environmental Factors,” Irkutsk: Irkutsk Nauch. Tsentr Surgery and Traumatol., Sib. Otd., Russ. Akad. Med. Nauk, 2009, p. 340.

  41. Miyasaka, S.C. and Grunes, D.L., Root zone temperature and calcium effects on phosphorus, sulfur, and micronutrients in winter wheat forage, Agronomy J., 1997, vol. 89, pp. 743–748.

    Article  Google Scholar 

  42. Bigot, J. and Boucaud, J., Short-term responses of Brassica rapa plants to low root temperature: effects on nitrate uptake and its translocation to the shoot, Physiol. Plant., 2006, vol. 96, pp. 646–654.

    Article  Google Scholar 

  43. Luo, H.Y., Lee, S.K., and He, J., Integrated effects of root-zone temperatures and phosphorus levels on aeroponically-grown lettuce (Lactuca sativa L.) in the tropics, Open Hortic. J., 2009, vol. 2, pp. 6–12.

    Article  CAS  Google Scholar 

  44. Plotnikov, V.K., Evtushenko, Ya.Yu., and Serkin, N.V., Analysis of frost resistance of winter barley cultivars by comparing freezing survival of whole plants and the hygroscopicity of mature grain, Russ. J. Plant Physiol., 2012, vol. 59, pp. 287–289.

    Article  CAS  Google Scholar 

  45. Parvaiz, A. and Satyawati, S., Salt stress and phyto-biochemical responses of plants—A review, Plant Soil Environ., 2008, vol. 54, pp. 89–99.

    Article  CAS  Google Scholar 

  46. Hasegawa, P.M., Bressan, R.A., Zhu, J.K., and Bognert, H.J., Plant cellular and molecular responses to high salinity, Annu. Rev. Plant Physiol. Plant Mol. Biol., 2000, vol. 51, pp. 463–499.

    Article  CAS  PubMed  Google Scholar 

  47. Munns, R. and Tester, M., Mechanisms of salinity tolerance, Annu. Rev. Plant Biol., 2008, vol. 59, pp. 651–681.

    Article  CAS  PubMed  Google Scholar 

  48. Chaves, M.M., Flexas, J., and Pinheiro, C., Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell, Ann. Bot., 2009, vol. 103, pp. 551–560.

    Article  CAS  PubMed  Google Scholar 

  49. Rozentsvet, O.A., Nesterov, V.N., and Bogdanova, E.S., Physiological and biochemical aspects of halophyte ecology, Biol. Bull., 2017, vol. 44, pp. 1295–1301.

    Article  CAS  Google Scholar 

  50. Rahman, S., Matsumuro, T., Miyake, H., and Takeoka, Y., Salinity-induced ultrastructural alterations in leaf cells of rice (Oryza sativa L.), Plant Prod. Sci., 2000, vol. 3, pp. 422–429.

    Article  Google Scholar 

  51. Naeem, M.S., Warusawitharana, H., Liu, H., Liu, D., Ahmad, R., Waraich, E.A., Xu, L., and Zhou, W., 5‑Aminolevulinic acid alleviates the salinity-induced changes in Brassica napus as revealed by the ultrastructural study of chloroplast, Plant Physiol. Biochem., 2012, vol. 57, pp. 84–92.

    Article  CAS  PubMed  Google Scholar 

  52. Jabeen, Z., Hussain, N., Han, Y., Shah, M.J., Zeng, F., Zeng, J., and Zhang, G., The differences in physiological responses, ultrastructure changes, and Na+ subcellular distribution under salt stress among the barley genotypes differing in salt tolerance, Acta Physiol. Plant., 2014, vol. 36, pp. 2397–2407.

    Article  CAS  Google Scholar 

  53. Hernández, J.A., Olmos, E., Corpas, F.J., Sevilla, F., and del Río, L.A., Salt-induced oxidative stress in chloroplasts of pea plants, Plant Sci., 1995, vol. 105, pp. 151–167.

    Article  Google Scholar 

  54. Mitsuya, S., Takeoka, Y., and Miyake, H., Effects of sodium chloride on foliar ultrastructure of sweet potato (Ipomoea batatas Lam.) plantlets grown under light and dark conditions in vitro, J. Plant Physiol., 2000, vol. 157, pp. 661–667.

    Article  CAS  Google Scholar 

  55. Balnokin, Y.V., Kurkova, E.B., Myasoedov, N.A., Lun’kov, R.V., Shamsutdinov, N.Z., Egorova, E.A., and Bukhov, N.G., Structural and functional state of thylakoids in a halophyte Suaeda altissima before and after disturbance of salt–water balance by extremely high concentrations of NaCl, Russ. J. Plant Physiol., 2004, vol. 51, pp. 815–821.

    Article  CAS  Google Scholar 

  56. Yamane, K., Kawasaki, M., Taniguchi, M., and M-iyake, 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 

  57. Trotta, A., Redondo-Gómez, S., Pagliano, C., Clemente, M.E., Rascio, N., La Rocca, N., Antonacci, A., Andreucci, F., and Barbato, R., Chloroplast ultrastructure and thylakoid polypeptide composition are affected by different salt concentrations in the halophytic plant Arthrocnemum macrostachyum,J. Plant Physiol., 2012, vol. 169, pp. 111–116.

    Article  CAS  PubMed  Google Scholar 

  58. Bruns, S. and Hecht-Buchholz, C., Light and electron microscope studies on the leaves of several potato cultivars after application of salt at various development stages, Potato Res., 1990, vol. 33, pp. 33–41.

    Article  Google Scholar 

  59. Yamane, K., Mitsuya, S., Taniguchi, M., and M-iyake, H., Salt-induced chloroplast protrusion is the process of exclusion of ribulose-1,5-bisphosphate carboxylase/oxygenase from chloroplasts into cytoplasm in leaves of rice, Plant Cell Environ., 2012, vol. 35, pp. 1663–1671.

    Article  CAS  PubMed  Google Scholar 

  60. Paramonova, N.V., Shevyakova, N.I., and Kuznetsov, Vl.V., Ultrastructure of ferritin in the leaves of Mesembryanthemum crystallinum under stress conditions, Russ. J. Plant Physiol., 2007, vol. 54, pp. 244–256.

    Article  CAS  Google Scholar 

  61. Shevyakova, N.I., Eshinimaeva, B.Ts., and Kuznetsov, Vl.V., Expression of ferritin gene in Mesembryanthemum crystallinum plants under different supply with iron and different intensity of oxidative stress, Russ. J. Plant Physiol., 2011, vol. 58: 768.

    Article  CAS  Google Scholar 

  62. Sauer, A. and Heise, K.-P., On the light dependence of fatty acid synthesis in spinach chloroplasts, Plant Physiol., 1983, vol. 73, pp. 11–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Briat, J.F., Ravet, K., Arnaud, N., Duc, C., Boucherez, J., Tourine, B., Cellier, F., and Gaymard, F., New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants, Ann. Bot., 2010, vol. 105, pp. 811–822.

    Article  CAS  PubMed  Google Scholar 

  64. Wang, P., Lombi, E., Zhao, F.G., and Kopittke, P.M., Nanotechnology: a new opportunity in plant sciences, Trends Plant Sci., 2016, vol. 21, pp. 699–712.

    Article  CAS  PubMed  Google Scholar 

  65. Rai, P.K., Kumar, V., Lee, S.S., Raza, N., Kim, K.H., Ok, Y.S., and Tsang, D.C.W., Nanoparticle-plant interaction: implications in energy, environment, and agriculture, Environ. Int., 2018, vol. 119, pp. 1–19.

    Article  CAS  PubMed  Google Scholar 

  66. 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 

  67. 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 

  68. 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: 763142. https://doi.org/10.1155/2010/763142

    Article  CAS  Google Scholar 

  69. Lalau, C.M., de Mohedano, R.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 

  70. Nekrasova, G.F., Ushakova, O.S., Ermakov, A.E., U-imin, 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: 458. https://doi.org/10.1134/S1067413611060117

    Article  CAS  Google Scholar 

  71. 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.

  72. Huang, J., Cheng, J., and Yi, J., Impact of silver nanoparticles on marine diatom Skeletonema costatum,J. Appl. Toxicol., 2016, vol. 36, pp. 1343–1354.

    Article  CAS  PubMed  Google Scholar 

  73. 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. Phytoremediation, 2017, vol. 19, pp. 80–86.

    Article  CAS  PubMed  Google Scholar 

  74. Matorin, D.N., Todorenko, D.A., Seifullina, N.Kh., Zayadan, B.K., and Rubin, A.B., Effect of silver nanoparticles on the parameters of chlorophyll fluorescence and P700 reaction in the green alga Chlamydomonas reinhardtii,Microbiology, 2013, vol. 82, pp. 809–814.

    Article  CAS  Google Scholar 

  75. 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 

  76. 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 

  77. Zhao, L., Sun, Y., Hernandez-Viezcas, J.A., Hong, J., Majumdar, S., Niu, G., Duarte-Gardea, 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 

  78. Wang, X., Yang, X., Chen, S., Li, Q., Wang, W., Hou, Ch., Gao, X., Wangand, L., and Wang, S., Zinc oxide nanoparticles affect biomass accumulation and photosynthesis in Arabidopsis,Front. Plant Sci., 2016, vol. 6: 1243. https://doi.org/10.3389/fpls.2015.01243

    Article  PubMed  PubMed Central  Google Scholar 

  79. 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 

  80. Golubev, A.A., Prilepskii, A.Y., Dykman, L.A., K-hlebtsov, N.G., and Bogatyrev, V.A., Colorimetric evaluation of the viability of the microalga Dunaliella salina as a test tool for nanomaterial toxicity, Toxicol. Sci., 2016, vol. 151, pp. 115–125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. 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 

  82. Astafurova, T.P., Morgalev, Y.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 nanoparticles of titanium dioxide and aluminum oxide on some morphophysiological characteristics of plants, Tomsk State Univ. J. Biol., 2011, no. 1, pp. 113–122.

  83. Hong, F., Yang, P., Gao, F., Liu, Ch., Zheng, L., Yang, F., and Zhou, J., Effect of nano-anatase TiO2 on spectral characterization of photosystem particles from spinach, Chem. Res. Chin. Univ., 2005, vol. 21, pp. 196–200.

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  85. 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 

  86. 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 

  87. 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.

  88. Majumdar, S., Peralta-Videa, J.R., Trujillo-Reyes, J., Sun, Y., Barrios, A.C., Niu, G., Flores-Margez, J.P., 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.

  89. Cao, Z., Rossi, L., Stowers, C., Zhang, W., Lombardini, L., and Ma, X., The impact of cerium oxide nanoparticles on the physiology of soybean (Glycine max (L.) Merr.) under different soil moisture conditions, Environ. Sci. Pollut. Res. Int., 2018, vol. 25, pp. 930–939.

    Article  CAS  PubMed  Google Scholar 

  90. 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 

  91. Torres, R., Diz, V.E., 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 

  92. 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 

  93. Govorov, A.O. and Carmeli, I., Hybrid structures composed of photosynthetic system and metal nanoparticles: plasmon enhancement effect, Nano Lett., 2007, vol. 7, pp. 620–625.

    Article  CAS  PubMed  Google Scholar 

  94. Falco, W.F., Botero, E.R., Falcão, E.A., 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. A., 2011, vol. 225, pp. 65–71.

    Article  CAS  Google Scholar 

  95. Barazzouk, S., Bekalé, L., and Hotchandani, S., Enhanced photostability of chlorophyll-a using gold nanoparticles as an efficient photoprotector, J. Mater. Chem., 2012, vol. 22, pp. 25316–25324.

    Article  CAS  Google Scholar 

  96. 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., 2005, vol. 105, pp. 269–279.

    Article  CAS  PubMed  Google Scholar 

  97. Oukarroum, A., Bras, S., Perreault, F., and Popovic, R., Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta,Ecotoxicol. Environ. Saf., 2012, vol. 78, pp. 80–85.

    Article  CAS  PubMed  Google Scholar 

  98. Nair, P.M.G. and Chung, M., III, Biochemical, anatomical and molecular level changes in cucumber (C-ucumis sativus) seedlings exposed to copper oxide nanoparticles, Biologia, 2016, vol. 70, pp. 1575–1585.

    Google Scholar 

  99. 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 

  100. Dykman, L.A. and Shchyogolev, S.Yu., 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, ch. 6, pp. 263–300.

    Google Scholar 

Download references

ACKNOWLEDGMENTS

We thank Mr. D.N. Tychinin for his help in preparation of the manuscript.

Funding

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

Author information

Authors and Affiliations

  1. Institute of Biochemistry and Physiology of Plants and Microorganisms, Russian Academy of Sciences, Saratov, Russia

    Yu. V. Venzhik, S. Yu. Shchyogolev & L. A. Dykman

Authors
  1. Yu. V. Venzhik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Yu. Shchyogolev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. A. Dykman
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Yu.V. Venzhik wrote and edited the manuscript, S.Yu. Shchyogolev and L.A. Dykman advised the review process and edited the manuscript. All authors read and approved the final version of this review article.

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

Abbreviations: AOS—antioxidant defense system; PSA—photosynthetic apparatus.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Venzhik, Y.V., Shchyogolev, S.Y. & Dykman, L.A. Ultrastructural Reorganization of Chloroplasts during Plant Adaptation to Abiotic Stress Factors. Russ J Plant Physiol 66, 850–863 (2019). https://doi.org/10.1134/S102144371906013X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S102144371906013X

Keywords:

Search

Navigation