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Mitochondria and Cell Death in Suspension Culture of Saccharum officinarum L. under Subzero Temperature Treatment

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Abstract

The process of cell death in sugarcane suspension culture (Saccharum officinarum L.) after exposure to a subzero temperature of –8°С and features of the mitochondria functioning during this period were studied. It was revealed that the cause of cell death after the end of the stress factor action was the development of oxidative stress and damage to individual components of mitochondrial ETC: subunit II of cytochrome c oxidase and α- and β-subunits of ATP synthase. Under these conditions, the activity of the alternative pathway (AP) of respiration remained at the control level much longer and decreased more slowly than the activity of the cytochrome pathway. The collapse of respiration occurred 6 h after exposure to subzero temperature after the release of cytochrome c from mitochondria. At the same time, the contribution of AP to the respiration of whole cells and isolated mitochondria in the S. officinarum suspension culture increased to 70%. Thus, the functioning of AP contributed to the maintenance of respiratory metabolism in S. officinarum cells after stress treatment and contributed to the survival of almost 20% of cells in culture.

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REFERENCES

  1. Samygin, G.A., Causes of plant freezing, Moscow: Nauka, 1974, 192 p.

    Google Scholar 

  2. Nievola, C.C., Carvalho, C.P., Carvalho, V., and Rodrigues, E., Rapid responses of plants to temperature changes, Temperature, 2017, vol. 4, p. 371. https://doi.org/10.1080/23328940.2017.1377812

    Article  Google Scholar 

  3. Ding, Y., Shi, Y., and Yang, S., Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants, New Phytol., 2019, vol. 222, p. 1690. https://doi.org/10.1111/nph.15696

    Article  PubMed  Google Scholar 

  4. Semikhatova, O.A. and Chirkova, T.V., Physiology of plant respiration, St. Petersburg: Publishing House of St. Petersburg University, 2001, 224 p.

    Google Scholar 

  5. Atkin, O.K. and Tjoelker, M.G., Thermal acclimation and the dynamic response of plant respiration to temperature, TRENDS in Plant Sci., 2003, vol. 8, p. 343. https://doi.org/10.1016/S1360-1385(03)00136-5

    Article  CAS  Google Scholar 

  6. Hacker, J., Ladinig, U., Wagner, J., and Neuner, G., Inflorescences of alpine cushion plants freeze autonomously and may survive subzero temperatures by supercooling, Plant Sci., 2011, vol. 180, p. 149. https://doi.org/10.1016/j.plantsci.2010.07.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Baek, K.-H. and Skinner, D.Z., Production of reactive oxygen species by freezing stress and the protective roles of antioxidant enzymes in plants, JACEN, 2012, vol. 1, p. 43. https://doi.org/10.4236/jacen.2012.11006

    Article  CAS  Google Scholar 

  8. Sperling, O., Earles, J.M., Secchi, F., Godfrey, J., and Zwieniecki, M.A., Frost induces respiration and accelerates carbon depletion in trees, PLoS ONE, 2015, vol. 10, e0144124. https://doi.org/10.1371/journal.pone.0144124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Vyse, K., Penzlin, J., Sergeant, K., Hincha, D.K., Arora, R., and Zuther, E., Repair of sub-lethal freezing damage in leaves of Arabidopsis thaliana, BMC Plant Bio-l., 2020, vol. 20, p. 35. https://doi.org/10.1186/s12870-020-2247-3

    Article  CAS  Google Scholar 

  10. Lyubushkina, I.V., Grabelnych, O.I., Pobezhimova, T.P., Stepanov, A.V., Fedyaeva, A.V., Fedoseeva, I.V., and Voinikov, V.K., Winter wheat cells subjected to freezing temperature undergo death process with features of programmed cell death, Protoplasma, 2014, vol. 251, p. 615. https://doi.org/10.1007/s00709-013-0562-3

    Article  PubMed  Google Scholar 

  11. Grabelnykh, O.I., Kirichenko, K.A., Pobezhimova, T.P., Borovik, O.A., Pavlovskaya, N.S., Lyubushkina, I.V., Koroleva, N.A., and Voinikov, V.K., The effect of cold shock on the fatty acid composition and functional state of mitochondria in hardened and unhardened winter wheat seedlings, Biol. membr., 2014, vol. 31, p. 204. https://doi.org/10.7868/S0233475514020029

    Article  CAS  Google Scholar 

  12. Vanlerberge, G.C., Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants, Int. J. Mol. Sci., 2013, vol. 14, p. 6805. https://doi.org/10.3390/ijms14046805

    Article  CAS  Google Scholar 

  13. Grabelnych, O.I., Borovik, O.A., Tauson, E.L., Pobezhimova, T.P., Katyshev, A.I., Pavlovskaya, N.S., Koroleva, N.A., Lyubushkina, I.V., Bashmakov, V.Y., Popov, V.N., Borovskii, G.B., and Voinikov, V.K., Mitochondrial energy-dissipating systems (alternative oxidase, uncoupling proteins, and external NADH dehydrogenase) are involved in development of frost-resistance of winter wheat seedlings, Biochemistry (Moscow), 2014, vol. 79, p. 506. https://doi.org/10.1134/S0006297914060030

    Article  CAS  PubMed  Google Scholar 

  14. Atkin, O.K., Zhang, Q., and Wiskich, J.T., Effect of temperature on rates of alternative and cytochrome pathway respiration and their relationship with the redox poise of the quinone pool, Plant Physiol., 2002, vol. 128, p. 212.https://doi.org/10.1104/pp.010326

  15. Furuike, S., Adachi, K., Sakaki, N., Shimo-Kon, R., Itoh, H., Muneyuki, E., Yoshida, M., Kinosita, K., Temperature dependence of the rotation and hydrolysis activities of the F1-ATPase, Biophys. J., 2008, vol. 95. p. 761, https://doi.org/10.1529/biophysj.107.123307

  16. Kerbler, S.M., Taylor, N.L., and Millar, A.H., Cold sensitivity of mitochondrial ATP synthase restricts oxidative phosphorylation in Arabidopsis thaliana, New Phytol., 2019, vol. 221, p. 1776. https://doi.org/10.1111/nph.15509

    Article  CAS  PubMed  Google Scholar 

  17. Lyubushkina, I.V., Fedyaeva, A.V., Stepanov, A.V., Grabelnych, O.I., High temperatures induce ROS generation and damage to respiratory activity in Saccharum officinarum suspension cells, J. Sib. Fed. Univ. Biol., 2021, vol. 14, p. 354. https://doi.org/10.17516/1997-1389-0355

    Article  Google Scholar 

  18. Laemmli, U.K., Cleavage of structural proteins during the assembly of head bacteriophage T4, Nature, 1970, vol. 227, p. 680.

    Article  CAS  PubMed  Google Scholar 

  19. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J., Protein measurement with folin phenol reagent, J. Biol. Chem., 1951, vol. 193, p. 265.

    Article  CAS  PubMed  Google Scholar 

  20. Duval, I., Brochu, V., Simard, M., Beaulieu, C., and Beaudoin, N., Thaxtomin A induces programmed cell death in Arabidopsis thaliana suspension-cultured cells, Planta, 2005, vol. 222, p. 820. https://doi.org/10.1007/s00425-005-0016-z

    Article  CAS  PubMed  Google Scholar 

  21. Crowley, L.C., Chojnowski, G., and Waterhouse, N.J., Measuring the DNA content of cells in apoptosis and at different cell-cycle stages by propidium iodide staining and flow cytometry, Cold Spring Harb. Protoc., 2016, vol. 10. https://doi.org/10.1101/pdb.prot087247

  22. Kolupaev, Yu.E. and Karpets, Yu.V., Reactive oxygen species, antioxidants and plant resistance to stressors, Kiev: Logos, 2019, 277 p.

    Google Scholar 

  23. Simeonova, E., Garstka, M., Kozioł-Lipińska, J., Mostowska, A., Monitoring the mitochondrial transmembrane potential with the JC-1 fluorochrome in programmed cell death during mesophyll leaf senescence, Protoplasma, 2004, vol. 223, p. 143. https://doi.org/10.1007/s00709-004-0039-5

    Article  CAS  PubMed  Google Scholar 

  24. Jones, H.G., Plant and microclimate: a quantitative approach to environmental plant physiology, Cambridge University Press, 2014, 423 p.

    Google Scholar 

  25. Tumanov, I.I. and Krasavtsev, O.A., Hardening of northern woody plants by negative temperatures, Rus. J. Plant Physiol., 1959, vol. 6, p. 654.

    Google Scholar 

  26. Salcheva, G. and Samygin, G.A., Microscopic observations of the freezing of winter wheat tissues, Rus. J. Plant Physiol., 1963, vol. 10, p. 65.

    Google Scholar 

  27. Vianello, A., Zancani, M., Peresson, C., Petrussa, E., Casolo, V., Krajňáková, J., Patui, S., Braidot, E., Macrì, F., Plant mitochondrial pathway leading to programmed cell death, Physiol. Plant., 2007, vol. 129, p. 242. https://doi.org/10.1111/j.1399-3054.2006.00767.x

    Article  CAS  Google Scholar 

  28. Repetto, M., Semprine, J., and Boveris, A., Lipid peroxidation: chemical mechanism, biological implications and analytical determination, in: Lipid Peroxidation, Catala, A., Ed., Rijeka: InTech, 2012, p. 3. https://doi.org/10.5772/45943

    Book  Google Scholar 

  29. Golovko T.K. Dykhanie rastenii (fiziologicheskie aspekty) (Plant respiration (physiological aspects)), St. Petersburg: Nauka, 1999, 204 p.

  30. Gibbs, J., Morrell, S., Valdez, A., Setter, T.L., Greenway, H., Regulation of alcoholic fermentation in coleoptiles of two rice cultivars differing in tolerance to anoxia, J. Exp. Bot., 2000, vol. 51, p. 785. https://doi.org/10.1093/jexbot/51.345.785

    Article  CAS  PubMed  Google Scholar 

  31. Lee, C.P., Maksaev, G., Jensen, G.S., Murcha, M.W., Wilson, M.E., Fricker, M., Hell, R., Haswell, E.S., Millar, A.H., Sweetlove, L., MSL1 is a mechanosensitive ion channel that dissipates mitochondrial membrane potential and maintains redox homeostasis in mitochondria during abiotic stress, Plant J., 2016, vol. 88, p. 809. https://doi.org/10.1111/tpj.13301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Garmash, E.V., Respiration and involvement of an alternative pathway as related to age and phenological strategy of the leaf, Rus. J. Plant Physiol., 2019, vol. 66, p. 403. https://doi.org/10.1134/S102144371903004X

    Article  CAS  Google Scholar 

  33. Amirsadeghi, S., Robson, C.A., and Vanlerberghe, G.C., The role of the mitochondrion in plant responses to biotic stress, Physiol. Plant., 2007, vol. 129, p. 253.

    Article  CAS  Google Scholar 

  34. Horn, M.E. and Mertz, D., Cyanide-resistant respiration in suspension cultures cells of Nicotiana glutinosa L., Plant Physiol., 1982, vol. 69, p. 1439.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

We are grateful to an anonymous reviewer for valuable comments and advice.

Funding

The work was carried out within the framework of the state task of the Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch, Russian Academy of Sciences (registration no. 121031300009-4) using the collections of The Core Facilities Center “Bioresource Center” and equipment of The Core Facilities Center “Bioanalytics” at The Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch, Russian Academy of Sciences.

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Authors and Affiliations

  1. Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch, Russian Academy of Sciences, Irkutsk, Russia

    I. V. Lyubushkina, A. V. Stepanov, A. V. Fedyaeva, I. V. Fedoseeva, T. P. Pobezhimova & O. I. Grabelnykh

  2. Irkutsk State University, Irkutsk, Russia

    I. V. Lyubushkina & O. I. Grabelnykh

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  1. I. V. Lyubushkina
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  2. A. V. Stepanov
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  3. A. V. Fedyaeva
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  4. I. V. Fedoseeva
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  5. T. P. Pobezhimova
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  6. O. I. Grabelnykh
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Correspondence to O. I. Grabelnykh.

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Lyubushkina, I.V., Stepanov, A.V., Fedyaeva, A.V. et al. Mitochondria and Cell Death in Suspension Culture of Saccharum officinarum L. under Subzero Temperature Treatment. Russ J Plant Physiol 69, 113 (2022). https://doi.org/10.1134/S1021443722060188

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  • DOI: https://doi.org/10.1134/S1021443722060188

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