Skip to main content
SpringerLink
Log in

Specific Features of the Ultrastructure and Biochemical Composition of Triticum spelta L. Leaf Mesophile Cells in the Initial Period of Stress Temperature Action

  • Published:
Cell and Tissue Biology Aims and scope Submit manuscript

Abstract

Under controlled conditions, the effect of high (40°C, 2 h) and positive low (4°C, 2 h) temperatures on the ultrastructure of mesophyll cells of the leaf and the content of photosynthetic pigments, phenols, and flavonoids in 2-week-old Triticum spelta plants was studied. The ultrastructure of the mesophyll cells of the leaf of the control plants was typical: a developed thylakoid system was clearly seen that was immersed in a fine-grained stroma in the chloroplasts of regular lenticular shape. Short-term hyperthermia caused a partial destruction of thylakoid membranes. Wave-shaped packing of grana thylakoids, significant expansion of lumen intervals, disturbance of the structural bond between the grana thylacoids and stroma thylakoids was noted. With hyperthermia, the mitochondria noticeably “swelled,” while the cristae membranes became less contrasting. The number of lipid droplets increased in the cytoplasm of cells. In the leaves, the content of chlorophylls and carotenoids decreased, however, the number of common phenols and flavonoids increased. Short-term hypothermia caused intense formation of plastoglobules, and an increase in the number and size of starch grains. Destruction of thylakoid membranes was not observed. Some of the mitochondria were rounded (40%), with their size being close to the control values, and some organelles were lenticular, “dumbbell,” and “cup-shaped.” Under hyper- and hypothermia, the T. spelta leaf mesophyll cells showed a tendency to increase the degree of chromatin condensation in the nucleus. Under hypothermia, the content and ratio of chlorophylls and carotenoids in leaves did not differ much from the control plants, and no significant quantitative changes in the total phenols and flavonoids were recorded.

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.

Similar content being viewed by others

REFERENCES

  1. Amarowicz, R., Weidner, S., Wojtowicz, I., Karmacґ, M., Kosinґska, A., and Rybarczyk, A., Influence of low-temperature stress on changes in the composition of grapevine leaf phenolic compounds and their antioxidant properties, Funct. Plant Sci. Biotechnol., 2010, vol. 4, pp. 90–96.

    Google Scholar 

  2. Armstrong, A.F., Logan, D.C., Tobin, A.K., O’Toole, P., and Atkin, O.K., Heterogeneity of plant mitochondrial responses underpinning respiratory acclimation to the cold in Arabidopsis thaliana Leaves, Plant Cell Environ., 2006, vol. 29, pp. 940–949.

    Article  PubMed  Google Scholar 

  3. Asada, K., Production and scavenging of reactive oxygen species in chloroplasts and their functions, Plant Physiol., 2006, vol. 141, pp. 391–396.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Austin, J.R., Frost, E., Vidi, P.A, Kessler, F., and Staehelin, L.A., Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes, Plant Cell, 2006, vol. 18, pp. 1693–1703.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Babenko, L.M., The effect of stress temperatures on the activity of lipoxygenases in Triticum spelta, Bull. Kharkiv Nat. Agrar. Univ., Ser. Biol., 2018, vol. 1, no. 43, pp. 40–46.

  6. Babenko, L.M., Kosakivska, I.V., Akimov, Yu.A., Klymchuk, D.O., and Skaternya, T.D., Effect of temperature stresses on pigment content, lipoxygenase activity and cell ultrastructure of winter wheat seedlings, Gen. Plant Physiol., 2014, vol. 4, pp. 117–125.

    Google Scholar 

  7. Babenko, L.M., Scherbatiuk, N.N., Klimchuk, D.A, and Kosakovskaya, I.V., Structural-functional peculiarities of leaf mesophyll cells of Triticum aestivum cultivars with different cold/heat tolerance under short-term temperature stresses, Tsitologiia, 2018, vol. 60, no. 2, pp. 128–135.

    Article  Google Scholar 

  8. Bobo-García, G., Davidov-Pardo, G., Arroqui, C., Vírseda, P., Marín-Arroyo, M.R., and Navarro, M., Intra-laboratory validation of microplate methods for total phenolic content and antioxidant activity on polyphenolic extracts, and comparison with conventional spectrophotometric methods, J. Sci. Food Agric., 2015, vol. 95, pp. 204–209.

    Article  CAS  PubMed  Google Scholar 

  9. Brüggemann, W., Klaucke, S., and Maas-Kantel, K., Long-term chilling of young tomato plants under low light. V. Kinetic and molecular properties of two key enzymes of the Calvin cycle in Lycopersicon esculentum Mill. and L. peruvianum Mill, Planta, 1994, vol. 194, pp. 160–168.

    Article  Google Scholar 

  10. Ciamporova, M., and Mistrik, I., The ultrastructural response of root cells to stressful conditions, Environ. Exp. Bot., 1993, vol. 33, pp. 11–26.

    Article  Google Scholar 

  11. Commuri, P.D. and Jones, R.J., Ultrastructural characterization of maize (Zea mays L.) kernels exposed to high temperature during endosperm cell division, Plant Cell Environ., 1999, vol. 22, pp. 375–385.

    Article  Google Scholar 

  12. Es-Safi, N.E., Ghidouche, S., and Ducrot, P.H., Flavonoids: hemisynthesis, reactivity, characterization and free radical scavenging activity, Molecules, 2007, vol. 12, pp. 2228–2258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hatfield, J. and Prueger, J., Temperature extremes: effect on plant growth and development, Weather Climate Extremes, 2015, vol. 10, pp. 4–10.

    Article  Google Scholar 

  14. Holaday, A.S., Martindale, W., and Alred, R., Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low temperature, Plant Physiol., 1992, vol. 98, pp. 1105–1114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hurry, V.M., Strand, Å., and Tobiæson, M., Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism, and carbohydrate content, Plant Physiol., 1995, vol. 109, pp. 697–706.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kislyuk, I.M., Bubolo, L.S., Kamentseva I.E., Kotlova, E.R., and Sherstneva, O.A., Heat shock increases thermotolerance of photosynthetic electron transport and the content of chloroplast membranes and lipids in wheat leaves, Russ. J. Plant Physiol., 2007, vol. 54, pp. 456–463.

    Article  CAS  Google Scholar 

  17. Kislyuk, I.M., Bubolo, L.S., Bykov, O.D., Kamentse-va, I.E., and Sherstneva, O.A., Protective and injuring action of visible light on photosynthetic apparatus in wheat plants during hyperthermia treatment, Russ. J. Plant Physiol., 2008, vol. 55, pp. 613–621.

    Article  CAS  Google Scholar 

  18. Kleine, T., Voigt, C., and Leister, D., Plastid signalling to the nucleus: messengers still lost in the mists?, Trends Genet., 2009, vol. 25, pp. 185–192.

    Article  CAS  PubMed  Google Scholar 

  19. Klymchuk, D.O., Kosakivska, I.V., Akimov, Yu.M., Shcherbatyuk, M.M., and Vorobyova, T.V., Structure-functional peculiarities of Brassica campestris and Amarantus caudathus leaf cells under low positive temperature, Bull. Kharkiv Nat. Agrar. Univ., Ser. Biol., 2011, vol. 3, no. 24, pp. 15–24.

  20. Klymchuk, D.O., Kosakivska, I.V., Akimov, Yu.M., Shcherbatyuk, M.M., and Vorobyova, T.V., Structural and functional peculiarities of Brassica campestris and Amaranthus caudatus leaf cells under high temperature, Bull. Kharkiv Nat. Agrar. Univ., Ser. Biol., 2012, vol. 2, no. 26, pp. 61–70.

  21. Kosakivska, I.V., Klymchuk, D.O., Negretzky, V.A., Bluma, D.A., and Ustinova, A.Yu., Stress proteins and ultrastructural characteristics of leaf cells in plants with different types of ecological strategies, Gen. Appl. Plant Physiol., 2008, vol. 34, pp. 405–418.

    CAS  Google Scholar 

  22. Kosakovskaya, I.V., Babenko, L.M, Skaternaya, T.D., and Ustinova, A.Yu., Influence of hypo- and hyperthermia on the activity and content of pigments and soluble proteins in Triticum aestivum L. seedlings of Yatran 60, Fiziol. Rast. Genet., 2014, vol. 46, no. 3, pp. 212–220.

    Google Scholar 

  23. Krol, A., Amarowiczb, R., and Weidnera, S., The effects of cold stress on the phenolic compounds and antioxidant capacity of grapevine (Vitis vinifera L.) leaves, J. Plant Physiol., 2015, vol. 189, pp. 97–104.

    Article  CAS  PubMed  Google Scholar 

  24. Li, T.A., Xu, S.L., Oses, Prieto, J.A., Putil, S., Xu, P., Wang, R.L., Li, K.H., Maltby, D.A., An, L.H., Burlingame, A.L., Deng, Z.P., and Wang, Z.Y., Proteomics analysis reveals posttranslational mechanisms for cold-induced metabolic changes in Arabidopsis, Mol. Plant., 2011, vol. 4, pp. 361–374.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Logan, D.C., Mitochondrial fusion, division and positioning in plants, Biochem. Soc. Trands., 2010, vol. 38, pp. 789–779.

    Article  CAS  Google Scholar 

  26. Olenichenko, N.A., Zagoskina, N.V., Astakhova, N.V., Trunova, T.I., and Kuznetsov, Yu.V., Primary and secondary metabolism of winter wheat during cold hardening and the action of antioxidants, Appl. Biochem. Microbiol., 2008, vol. 44, no. 5, pp. 589–594.

    Article  CAS  Google Scholar 

  27. Pareek, A., Singla, S., and Grover, A., Short-term salinity and high temperature stress associated ultrastructural alterations in young leaf cells of Oryza sativa L., Ann. Bot., 1997, vol. 80, pp. 629–639.

    Article  Google Scholar 

  28. Pavlyuchkova, S.M., Spivak, E.A., Vershilovskaya, I.V., Nedved, E.L., and Shkraba, E.V., Effect of exogenous 5-aminolevulinic acid on the functioning of the antioxidant system of potato plants (Solanum tuberosum) under low-temperature stress, Vestsi Nat. Acad. Nauk. Belarusi, Ser. Biyal., 2014, vol. 3, pp. 46–51.

    Google Scholar 

  29. Popov, V.N., Antipina, O.V., and Astakhova, N.V., Changes in chloroplast ultrastructure of tobacco plants in the course of protection from oxidative stress under hypothermia, Russ. J. Plant Physiol., 2016, vol. 63, pp. 301–307.

    Article  CAS  Google Scholar 

  30. Posmyk, M.M., Bailly, C., Szafranґska, K., Jasan, K.M., and Corbinea, F., Antioxidant enzymes and isoflavonoids in chilled soybean (Glycine max (L.) Merr.) seedlings, J. Plant Physiol., 2005, vol. 162, pp. 403–412.

    Article  CAS  PubMed  Google Scholar 

  31. Reddy, A.R., Chaitanya, K.V., and Vivekanandan, M., Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants, J. Plant Physiol., 2004, vol. 161, pp. 1189–1202.

    Article  CAS  Google Scholar 

  32. Ristic, Z. and Ashworth, E., Changes in leaf ultrastructure and carbohydrates in Arabidopsis thaliana L. (Heynh) cv. Columbia during rapid cold acclimation, Protoplasma, 1993, vol. 172, pp. 111–123.

    Article  Google Scholar 

  33. Rivero, R., Ruiz, J., Garcıa, P., Lopez-Lefebre, L., Sanchez, E., and Romero, L., Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants, Plant Sci., 2001, vol. 160, pp. 315–321.

    Article  CAS  PubMed  Google Scholar 

  34. Rudikovskaya, E.G., Fedorova, G.A., Dudareva, L.V., Makarova, L.E., and Rudokovskij, A.V., Effect of growth temperature on the composition of phenols in pea roots, Russ. J. Plant Physiol., 2008, vol. 55, pp. 712–715.

    Article  CAS  Google Scholar 

  35. Rurek, M., Plant mitochondria under a variety of temperature stress conditions, Mitochondrion, 2014, vol. 19, pp. 289–294.

    Article  CAS  PubMed  Google Scholar 

  36. Salem-Fnayou, A.B., Bouamama, B., Ghorbel, A., and Mliki, A., Investigations on the leaf anatomy and ultrastructure of grapevine (Vitis vinifera) under heat stress, Microsc. Res. Tech., 2011, vol. 74, pp. 756–762.

    Article  PubMed  Google Scholar 

  37. Smirnov, O., Kosyan, A., Kosyk, O., and Taran, N., Response of phenolic metabolism induced by aluminium (Al3+) toxicity in Fagopyrum esculentum Moench plants, Ukr. Biochem. J., 2015, vol. 87, pp. 129–135.

    Article  CAS  PubMed  Google Scholar 

  38. Sopher, C.R., Krol, M., and Huner, N.P.A., Chloroplastic changes associated with paclobutrazol-induced stress protection in maize seedlings, Can. J. Bot., 1999, vol. 77, pp. 279–290.

    CAS  Google Scholar 

  39. Stefanowska, M., Kura, M., and Kacperska, A., Low temperature induced modifications in cell ultrastructure and localization of phenolics in winter oilseed rape (Brassica napus L, var. oleifera) leaves, Annu. Bot., 2002, vol. 90, pp. 637–645.

    Article  CAS  Google Scholar 

  40. Swigonska, S., Amarowicz, R., Kryl, A., Mostek, A., Badowiec, A., and Weidner, S., Influence of abiotic stress during soybean germination followed by recovery on the phenolic compounds of radicles and their antioxidant capacity, Acta Soc. Bot. Pol., 2014, vol. 83, pp. 209–218.

    Article  Google Scholar 

  41. Theocharis, A., Clement, 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 

  42. Treutter, D., Significance of flavonoids in plant resistance: a review, Environ. Chem. Lett., 2006, vol. 4, pp. 147–157.

    Article  CAS  Google Scholar 

  43. Vassileva, V., Signarbieux, C., Anders, I., and Feller, U., Genotypic variation in drought stress response and subsequent recovery of wheat (Triticum aestivum L.), J. Plant Res., 2011, vol. 124, no. 1, pp. 147–154.

    Article  PubMed  Google Scholar 

  44. Vella, 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 rewarming, Protoplasma, 2012, vol. 249, pp. 1137–1149.

    Article  CAS  PubMed  Google Scholar 

  45. Venzhik, Yu.V., Titov, A.F., Talanova, V.V., Mirosla-vov, 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, no. 2, pp. 168–176.

    Article  Google Scholar 

  46. Venzhik, Yu.V., Titov, A.F., and Talanova, V.V., Short-term chilling of wheat seedlings or roots affects the ultrastructure of mesophyll cells, Tr. Karel. Nauch. Tsentra, Ross. Akad. Nauk, 2017, vol. 5, pp. 66–78.

    Google Scholar 

  47. Veselova, S., Farhutdinov, R., Mitrichenko, A., Symonyan, M., and Hartung, W., The effect of root cooling on hormone content and root hydraulic conductivity of durum wheat seedlings (Triticum durum L.), Bulg. J. Plant Physiol., Special Issue, 2003 pp. 360–366.

    Google Scholar 

  48. Voskresenskaya, O.L., Voskresenskiy, V.S., Sabaeva, E.V., and Yagdarova, O.A., Influence of ultraviolet radiation and microclimate parameters on the content of pigments in leaves of birch which grows under the conditions of the city, Vestn. Udmurt. Univ., Ser. Biol. Nauki Zemle, 2014, vol. 3, pp. 39–45.

    Google Scholar 

  49. Weidner, S., Kordala, E., Brosowska-Arendt, W., Karamacґ, M., Kosinґska, A., and Amarowicz, R., Phenolic compounds and properties of antioxidants in grapevine roots followed by recovery, Acta Soc. Bot. Pol., 2009, vol. 78, pp. 279–286.

    Article  CAS  Google Scholar 

  50. Wellburn, A., The spectral determination of chlorophyll a and chlorophyll b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution, J. Plant Physiol., 1994, vol. 144, pp. 307–313.

    Article  CAS  Google Scholar 

  51. Wise, R.R. and Naylor, A.W., Chilling-enhanced photooxidation. The peroxidative destruction of lipids during chilling injury to photosynthesis and ultrastructure, Plant Physiol., 1987, vol. 8, pp. 272–277.

    Article  Google Scholar 

  52. Yamada, K., and Osakabe, Y., Sugar compartmentation as an environmental stress adaptation strategy in plants, Semin. Cell Dev. Biol., 2017, vol. 72, pp. 1–10.

    Article  Google Scholar 

Download references

ACKNOWLEDGMENTS

This work was supported by the National Academy of Sciences of Ukraine, the project “The Phytohormonal System of New Genotypes of Triticum aestivum L. and Its Wild Ancestors under the Influence of Extreme Climatic Factors.”

We are thankful to D.A. Klimchuk, Ph.D., the head of the Center for Electron Microscopy, N. Kholodny Institute of Botany, National Academy of Sciences of Ukraine, for his attention and useful discussion of the results when this publication was prepared.

Author information

Authors and Affiliations

  1. Kholodny Institute of Botany, National Academy of Sciences of Ukraine, Kyiv, Ukraine

    L. M. Babenko, M. V. Vodka, Yu. N. Akimov, A. V. Babenko & I. V. Kosakovskaya

  2. Educational and Scientific Centre “Institute of Biology”, Taras Shevchenko National University of Kyiv, Kyiv, Ukraine

    A. E. Smirnov

Authors
  1. L. M. Babenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. V. Vodka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu. N. Akimov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. E. Smirnov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. V. Babenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. I. V. Kosakovskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. M. Babenko.

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 T. Borisova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Babenko, L.M., Vodka, M.V., Akimov, Y.N. et al. Specific Features of the Ultrastructure and Biochemical Composition of Triticum spelta L. Leaf Mesophile Cells in the Initial Period of Stress Temperature Action. Cell Tiss. Biol. 13, 70–78 (2019). https://doi.org/10.1134/S1990519X19010024

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990519X19010024

Keywords:

Search

Navigation