Skip to main content
SpringerLink
Log in

Effect of mitochondria-targeted antioxidant SkQ1 on programmed cell death induced by viral proteins in tobacco plants

  • Phenoptosis
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Programmed cell death (PCD) is the main defense mechanism in plants to fight various pathogens including viruses. The best-studied example of virus-induced PCD in plants is Tobacco mosaic virus (TMV)-elicited hypersensitive response in tobacco plants containing the N resistance gene. It was previously reported that the animal mitochondrial protein Bcl-xL, which lacks a homolog in plants, effectively suppresses plant PCD induced by TMV p50 — the elicitor of hyper-sensitive response in Nicotiana tabacum carrying the N gene. Our studies show that the mitochondria-targeted antioxidant SkQ1 effectively suppresses p50-induced PCD in tobacco plants. On the other hand, SkQ1 did not affect Poa semilatent virus TGB3-induced endoplasmic reticulum stress, which is followed by PCD, in Nicotiana benthamiana epidermal cells. These data suggest that mitochondria-targeted antioxidant SkQ1 can be used to study molecular mechanisms of PCD suppression in plants.

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

Similar content being viewed by others

Abbreviations

C12TPP:

dodecyl triphenylphosphonium

dpi:

day post infiltration

ER:

endoplasmic reticulum

PCD:

programmed cell death

PSLV:

Poa semilatent virus

PVX:

potato virus X

ROS:

reactive oxygen species

TMV:

tobacco mosaic virus

UPR:

unfolded protein response

References

  1. Shapiguzov, A., Vainonen, J. P., Wrzaczek, M., and Kangasjarvi, J. (2012) Front. Plant Sci., 3, 292.

    Article  PubMed  CAS  Google Scholar 

  2. Janitza, P., Ullrich, K. K., and Quint, M. (2012) Front. Plant Sci., 3, 271.

    Article  PubMed  Google Scholar 

  3. Eichmann, R., and Schafer, P. (2012) Front. Plant Sci., 3, 200.

    Article  PubMed  Google Scholar 

  4. Howell, S. H. (2013) Annu. Rev. Plant Biol., 64, 477–499.

    Article  PubMed  CAS  Google Scholar 

  5. Tripathy, B., and Oelmuller, R. (2012) Plant Signal. Behav., 7, 1621–1633.

    Article  PubMed  CAS  Google Scholar 

  6. Robson, C. A., and Vanlerberghe, G. C. (2002) Plant Physiol., 129, 1908–1920.

    Article  PubMed  CAS  Google Scholar 

  7. Murphy, M. P. (2009) Biochem. J., 417, 1–17.

    Article  PubMed  CAS  Google Scholar 

  8. Venditti, P., Di Stefano, L., and Di Meo, S. (2013) Mitochondrion, 13, 71–82.

    Article  PubMed  CAS  Google Scholar 

  9. Korshunov, S. S., Skulachev, V. P., and Starkov, A. A. (1997) FEBS Lett., 416, 15–18.

    Article  PubMed  CAS  Google Scholar 

  10. Petrov, V. D., and Van Breusegem, F. (2012) AoB Plants, 2012, pls014.

  11. Balazadeh, S., Jaspert, N., Arif, M., Mueller-Roeber, B., and Maurino, V. G. (2012) Front. Plant Sci., 3, 234.

    Article  PubMed  Google Scholar 

  12. Maruta, T., Noshi, M., Tanouchi, A., Tamoi, M., Yabuta, Y., Yoshimura, K., Ishikawa, T., and Shigeoka, S. (2012) J. Biol. Chem., 287, 11717–11729.

    Article  PubMed  CAS  Google Scholar 

  13. Zechmann, B. (2011) Plant Signal. Behav., 6, 360–363.

    Article  PubMed  CAS  Google Scholar 

  14. Koffler, B. E., Bloem, E., Zellnig, G., and Zechmann, B. (2013) Micron, 45, 119–128.

    Article  PubMed  CAS  Google Scholar 

  15. Skulachev, V. P. (2007) Biochemistry (Moscow), 72, 1385–1396.

    Article  CAS  Google Scholar 

  16. Antonenko, Y. N., Avetisyan, A. V., Bakeeva, L. E., Chernyak, B. V., Chertkov, V. A., Domnina, L. V., Ivanova, O. Yu., Izyumov, D. S., Khailova, L. S., Klishin, S. S., Korshunova, G. A., Lyamzaev, K. G., Muntyan, M. S., Nipryakhina, O. K., Pashkovskaya, A. A., Pletyushkina, O. Yu., Pustovidko, A. V., Roginsky, V. A., Rokitskaya, T. I., Ruuge, E. K., Saprunova, V. B., Severina, I. I., Simonyan, R. A., Skulachev, I. V., Skulachev, M. V., Sumbatyan, N. V., Sviryaeva, I. V., Tashlitsky, V. N., Vassiliev, J. M., Vysokikh, M. Yu., Yaguzhinsky, L. S., Zamyatnin, A. A., Jr., and Skulachev, V. P. (2008) Biochemistry (Moscow), 73, 1273–1287.

    Article  CAS  Google Scholar 

  17. Skulachev, V. P., Anisimov, V. N., Antonenko, Y. N., Bakeeva, L. E., Chernyak, B. V., Erichev, V. P., Filenko, O. F., Kalinina, N. I., Kapelko, V. I., Kolosova, N. G., Kopnin, B. P., Korshunova, G. A., Lichinitser, M. R., Obukhova, L. A., Pasyukova, E. G., Pisarenko, O. I., Roginsky, V. A., Ruuge, E. K., Senin, I. I., Severina, I. I., Skulachev, M. V., Spivak, I. M., Tashlitsky, V. N., Tkachuk, V. A., Vyssokikh, M. Y., Yaguzhinsky, L. S., and Zorov, D. B. (2009) Biochim. Biophys. Acta, 1787, 437–461.

    Article  PubMed  CAS  Google Scholar 

  18. Skulachev, M. V., Antonenko, Y. N., Anisimov, V. N., Chernyak, B. V., Cherepanov, D. A., Chistyakov, V. A., Egorov, M. V., Kolosova, N. G., Korshunova, G. A., Lyamzaev, K. G., Plotnikov, E. Y., Roginsky, V. A., Savchenko, A. Y., Severina, I. I., Severin, F. F., Shkurat, T. P., Tashlitsky, V. N., Shidlovsky, K. M., Vyssokikh, M. Y., Zamyatnin, A. A., Jr., Zorov, D. B., and Skulachev, V. P. (2011) Curr. Drug Targets, 12, 800–826.

    Article  PubMed  CAS  Google Scholar 

  19. Severin, F. F., Severina, I. I., Antonenko, Y. N., Rokitskaya, T. I., Cherepanov, D. A., Mokhova, E. N., Vyssokikh, M. Y., Pustovidko, A. V., Markova, O. V., Yaguzhinsky, L. S., Korshunova, G. A., Sumbatyan, N. V., Skulachev, M. V., and Skulachev, V. P. (2010) Proc. Natl. Acad. Sci. USA, 107, 663–668.

    Article  PubMed  CAS  Google Scholar 

  20. Yani, Ye. V., Katargina, L. A., Chesnokova, N. B., Beznos, O. V., Savchenko, A. Yu., Vygodin, V. A., Gudkova, Ye. Yu., Zamyatnin, A. A., Jr., and Skulachev, M. V. (2012) Prakticheskaya Meditsina, 59, 134–137.

    Google Scholar 

  21. Vasil’ev, L. A., Dzyubinskaya, E. V., Kiselevsky, D. B., Shestak, A. A., and Samuilov, V. D. (2011) Biochemistry (Moscow), 76, 1120–1130.

    Article  Google Scholar 

  22. Vasil’ev, L. A., Kiselevsky, D. B., Dzyubinskaya, E. V., Nesov, A. V., and Samuilov, V. D. (2012) Biochemistry (Moscow), 77, 354–361.

    Article  Google Scholar 

  23. Dzyubinskaya, E. V., Ionenko, I. F., Kiselevsky, D. B., Samuilov, V. D., and Samuilov, F. D. (2013) Biochemistry (Moscow), 78, 68–74.

    Article  CAS  Google Scholar 

  24. Solovyev, A. G., Minina, E. A., Makarova, S. S., Erokhina, T. N., Makarov, V. V., Kaplan, I. B., Kopertekh, L., Schiemann, J., Richert-Poggeler, K. R., and Morozov, S. Y. (2013) Biochimie, 95, 1360–7130.

    Article  PubMed  CAS  Google Scholar 

  25. Zamyatnin, A. A., Jr., Solovyev, A. G., Sablina, A. A., Agranovsky, A. A., Katul, L., Vetten, H. J., Schiemann, J., Hinkkanen, A. E., Lehto, K., and Morozov, S. Y. (2002) J. Gen. Virol., 83, 651–662.

    PubMed  Google Scholar 

  26. Solovyev, A. G., Stroganova, T. A., Zamyatnin, A. A., Jr., Fedorkin, O. N., Schiemann, J., and Morozov, S. Y. (2000) Virology, 269, 113–127.

    Article  PubMed  CAS  Google Scholar 

  27. Sambrook, J., Fritsch, E. F., and Maniatis, T. A. (1989) Molecular Cloning: A Laboratory Manual, 2nd Edn., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

    Google Scholar 

  28. Zamyatnin, A. A., Jr., Solovyev, A. G., Bozhkov, P. V., Valkonen, J. P., Morozov, S. Y., and Savenkov, E. I. (2006) Plant J., 46, 145–154.

    Article  PubMed  CAS  Google Scholar 

  29. Morozov, S. Yu., Fedorkin, O. N., Juttner, G., Schiemann, J., Baulcombe, D. C., and Atabekov, J. G. (1997) J. Gen. Virol., 78, 2077–2083.

    PubMed  CAS  Google Scholar 

  30. Erickson, F. L., Dinesh-Kumar, S. P., Holzberg, S., Ustach, C. V., Dutton, M., Handley, V., Corr, C., and Baker, B. J. (1999) Philos. Trans. R. Soc. Lond. B Biol. Sci., 354, 653–658.

    Article  PubMed  CAS  Google Scholar 

  31. Jin, H., Liu, Y., Yang, K. Y., Kim, C. Y., Baker, B., and Zhang, S. (2003) Plant J., 33, 719–731.

    Article  PubMed  CAS  Google Scholar 

  32. Takabatake, R., Ando, Y., Seo, S., Katou, S., Tsuda, S., Ohashi, Y., and Mitsuhara, I. (2007) Plant Cell Physiol., 48, 498–510.

    Article  PubMed  CAS  Google Scholar 

  33. Ye, C. M., Chen, S., Payton, M., Dickman, M. B., and Verchot, J. (2013) Mol. Plant. Pathol., 14, 241–255.

    Article  PubMed  CAS  Google Scholar 

  34. Lacomme, C., and Santa Cruz, S. (1999) Proc. Natl. Acad. Sci. USA, 96, 7956–7961.

    Article  PubMed  CAS  Google Scholar 

  35. Kawai-Yamada, M., Jin, L., Yoshinaga, K., Hirata, A., and Uchimiya, H. (2001) Proc. Natl. Acad. Sci. USA, 98, 12295–12300.

    Article  PubMed  CAS  Google Scholar 

  36. Mitsuhara, I., Malik, K. A., Miura, M., and Ohashi, Y. (1999) Curr. Biol., 15, 775–778.

    Article  Google Scholar 

  37. Qiao, J., Mitsuhara, I., Yazaki, Y., Sakano, K., Gotoh, Y., Miura, M., and Ohashi, Y. (2002) Plant Cell Physiol., 43, 992–1005.

    Article  PubMed  CAS  Google Scholar 

  38. Xu, C., Bailly-Maitre, B., and Reed, J. C. (2005) J. Clin. Invest., 115, 2656–2664.

    Article  PubMed  CAS  Google Scholar 

  39. Zhang, K., and Kaufman, R. J. (2006) Neurology, 66, S102-S109.

  40. Oh, D. H., Kwon, C. S., Sano, H., Chung, W. I., and Koizumi, N. (2003) Biochem. Biophys. Res. Commun., 301, 225–230.

    Article  PubMed  CAS  Google Scholar 

  41. Urade, R. (2009) Biofactors, 35, 326–331.

    Article  PubMed  CAS  Google Scholar 

  42. Ye, C., Dickman, M. B., Whitham, S. A., Payton, M., and Verchot, J. (2011) Plant Physiol., 156, 741–755.

    Article  PubMed  CAS  Google Scholar 

  43. Ye, C. M., Kelly, V., Payton, M., Dickman, M. B., and Verchot, J. (2012) Mol. Plant, 5, 1151–1153.

    Article  PubMed  CAS  Google Scholar 

  44. Tabas, I., and Ron, D. (2011) Nat. Cell Biol., 13, 184–190.

    Article  PubMed  CAS  Google Scholar 

  45. Solovyev, A. G., Schiemann, J., and Morozov, S. Y. (2012) Sci. World J., 2012, 416076.

    Article  Google Scholar 

  46. Brigneti, G., Voinnet, O., Li, W. X., Ji, L. H., Ding, S. W., and Baulcombe, D. C. (1998) EMBO J., 17, 6739–6746.

    Article  PubMed  CAS  Google Scholar 

  47. Scholthof, H. B., Scholthof, K. B., and Jackson, A. O. (1995) Plant Cell, 7, 1157–1172.

    PubMed  CAS  Google Scholar 

  48. Yelina, N. E., Savenkov, E. I., Solovyev, A. G., Morozov, S. Y., and Valkonen, J. P. (2002) J. Virol., 76, 12981–12991.

    Article  PubMed  CAS  Google Scholar 

  49. Lukhovitskaya, N. I., Solovieva, A. D., Boddeti, S. K., Thaduri, S., Solovyev, A. G., and Savenkov, E. I. (2013) Plant Cell, 25, 960–973.

    Article  PubMed  CAS  Google Scholar 

  50. Canto, T., MacFarlane, S. A., and Palukaitis, P. (2004) J. Gen. Virol., 85, 3123–3133.

    Article  PubMed  CAS  Google Scholar 

  51. Lukhovitskaya, N. I., Yelina, N. E., Zamyatnin, A. A., Jr., Schepetilnikov, M. V., Solovyev, A. G., Sandgren, M., Morozov, S. Y., Valkonen, J. P., and Savenkov, E. I. (2005) J. Gen. Virol., 86, 2879–2889.

    Article  PubMed  CAS  Google Scholar 

  52. Gushchin, V. A., Lukhovitskaya, N. I., Andreev, D. E., Wright, K. M., Taliansky, M. E., Solovyev, A. G., Morozov, S. Y., and MacFarlane, S. A. (2013) J. Gen. Virol., 94, 230–240.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Biology, Lomonosov Moscow State University, Leninsky Gory 1/12, 119234, Moscow, Russia

    A. D. Solovieva

  2. Institute of Mitoengineering, Lomonosov Moscow State University, Vorobyevy Gory 1/73a, 119992, Moscow, Russia

    O. Yu. Frolova

  3. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Leninsky Gory 1/40, 119992, Moscow, Russia

    A. G. Solovyev, S. Yu. Morozov & A. A. Zamyatnin Jr.

  4. Institute of Agricultural Biotechnology, Russian Academy of Agricultural Sciences, ul. Timiryazevskaya 42, 127550, Moscow, Russia

    A. G. Solovyev

  5. Institute of Molecular Medicine, Sechenov First Moscow State Medical University, ul. Trubetskaya 8, 119991, Moscow, Russia

    A. A. Zamyatnin Jr.

Authors
  1. A. D. Solovieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. O. Yu. Frolova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. G. Solovyev
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Yu. Morozov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. A. Zamyatnin Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. A. Zamyatnin Jr..

Additional information

Original Russian Text © A. D. Solovieva, O. Yu. Frolova, A. G. Solovyev, S. Yu. Morozov, A. A. Zamyatnin, Jr., 2013, published in Biokhimiya, 2013, Vol. 78, No. 9, pp. 1284–1292.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Solovieva, A.D., Frolova, O.Y., Solovyev, A.G. et al. Effect of mitochondria-targeted antioxidant SkQ1 on programmed cell death induced by viral proteins in tobacco plants. Biochemistry Moscow 78, 1006–1012 (2013). https://doi.org/10.1134/S000629791309006X

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S000629791309006X

Key words

Search

Navigation