Skip to main content
Log in

Role of mitochondria in the operation of calcium signaling system in heat-stressed plants

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

Abstract

Mild heat stress induces the expression of heat shock proteins (HSPs) that protect plants from death during damaging heat treatments. It was assumed that the appearance in the cell of denatured proteins triggers the expression of HSP; however, recent results show that protein denaturation is not a prerequisite for this process. In this work we discuss a hypothetical mechanism for activation under heat stress of HSP expression promoted by short-term elevation of cytosolic Ca2+ level. According to our hypothesis, a prolonged elevation of Ca2+ has a negative influence on HSP expression. Therefore, calcium is transported from the cytosol into intracellular compartments, including mitochondria. The Ca2+ entry into mitochondria is accompanied by hyperpolarization of the inner mitochondrial membrane and by the increased production of reactive oxygen species (ROS). The increased ROS production contributes to the activation of HSP expression under mild heat stress but leads to plant death under severe heat shock. Thus, mitochondria and, possibly, other organelles play the crucial role in determining life or death fate of heat-treated plant cells by controlling the cytosolic Ca2+ content and ROS production.

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.

Similar content being viewed by others

Abbreviations

[Ca2+]cyt :

cytoplasmic Ca2+ concentration

[Ca2+]mit :

mitochondrial Ca2+ concentration

CaM:

calmodulin

CCCP:

carbonyl cyanide m-chlorophenylhydrazone

ER:

endoplasmic reticulum

HSE:

heat shock element

HSF:

heat shock factor

HSP:

heat shock protein

mtΔψ:

potential difference across the inner mitochondrial membrane

pmΔψ:

potential difference across the plasma membrane

PCD:

programmed cell death

ROS:

reactive oxygen species

References

  1. Vierling, E., The roles of heat-shock proteins in plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1991, vol. 42, pp. 579–620.

    Article  CAS  Google Scholar 

  2. Saidi, Y., Finka, A., and Goloubinoff, P., Heat perception and signalling in plants: a tortuous path to thermotolerance, New Phytol., 2011, vol. 190, pp. 556–565.

    Article  CAS  PubMed  Google Scholar 

  3. Mittler, R., Finka, A., and Goloubinoff, P., How do plants feel the heat? Trends Biochem. Sci., 2012, vol. 37, pp. 118–125.

    Article  CAS  PubMed  Google Scholar 

  4. Voellmy, R. and Boellmann, F., Chaperone regulation of the heat shock protein response, Adv. Exp. Med. Biol., 2007, vol. 594, pp. 89–99.

    Article  PubMed  Google Scholar 

  5. Scharf, K.D., Berberich, T., Ebersberger, I., and Nover, L., The plant heat stress transcription factor (Hsf) family: structure, function and evolution, Biochim. Biophys. Acta, 2012, vol. 1819, pp. 104–119.

    Article  CAS  PubMed  Google Scholar 

  6. Balogh, G., Horvath, I., Nagy, E., Hoyk, Z., Benko, S., Bensaude, O., and Vigh, L., The hyperfluidization of mammalian cell membrane acts as a signal to initiate the heat shock protein response, FEBS J., 2005, vol. 272, pp. 6077–6086.

    Article  CAS  PubMed  Google Scholar 

  7. Saidi, Y., Finka, A., Muriset, M., Bromberg, Z., Weiss, Y.G., Maathuis, F.J., and Goloubinoff, P., The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane, Plant Cell, 2009, vol. 21, pp. 2829–2843.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Finka, A., Mattoo, R.U., and Goloubinoff, P., Meta-analysis of heat- and chemically-upregulated chaperone genes in plant and human cells, Cell Stress Chaperones, 2011, vol. 16, pp. 15–31.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Volkov, R.A., Panchuk, I.I., Mullineaux, P.M., and Schoffl, F., Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis, Plant Mol. Biol., 2006, vol. 61, pp. 733–746.

    Article  CAS  PubMed  Google Scholar 

  10. Miller, G. and Mittler, R., Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann. Bot., 2006, vol. 98, pp. 279–288.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Pucciariello, C., Banti, V., and Perata, P., ROS signaling as common element in low oxygen and heat stresses, Plant Physiol. Biochem., 2012, vol. 59, pp. 3–10.

    Article  CAS  PubMed  Google Scholar 

  12. Rikhvanov, E.G., Gamburg, K.Z., Varakina, N.N., Rusaleva, T.M., Fedoseeva, I.V., Tauson, E.L., Stupnikova, I.V., Stepanov, A.V., Borovskii, G.B., and Voinikov, V.K., Nuclear-mitochondrial cross-talk during heat shock in Arabidopsis cell culture, Plant J., 2007, vol. 52, pp. 763–778.

    Article  CAS  PubMed  Google Scholar 

  13. Queitsch, C., Hong, S.W., Vierling, E., and Lindquist, S., Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis, Plant Cell, 2000, vol. 12, pp. 479–492.

    CAS  PubMed Central  PubMed  Google Scholar 

  14. Rikhvanov, E.G., Romanova, N.V., and Chernoff, Y.O., Chaperone effects on prion and nonprion aggregates, Prion, 2007, vol. 1, pp. 217–222.

    Article  PubMed Central  PubMed  Google Scholar 

  15. Medvedev, S.S., Calcium signaling system in plants, Russ. J. Plant Physiol., 2005, vol. 52, pp. 249–274.

    Article  CAS  Google Scholar 

  16. Reddy, A.S., Ali, G.S., Celesnik, H., and Day, I.S., Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression, Plant Cell, 2011, vol. 23, pp. 2010–2032.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Biyasheva, A.E., Molotkovskii, Yu.G., and Mamonov, L.K., Increase of free Ca2+ in the cytosol of plant protoplasts in response to heat stress as related to Ca2+ homeostasis, Russ. Plant Physiol., 1993, vol. 40, pp. 540–544.

    Google Scholar 

  18. Gong, M., van der Luit, A., Knight, M., and Trewavas, A., Heat-shock-induced changes in intracellular Ca2+ level in tobacco seedlings in relation to thermotolerance, Plant Physiol., 1998, vol. 116, pp. 429–437.

    Article  CAS  PubMed Central  Google Scholar 

  19. Liu, H.T., Li, B., Shang, Z.L., Li, X.Z., Mu, R.L., Sun, D.Y., and Zhou, R.G., Calmodulin is involved in heat shock signal transduction in wheat, Plant Physiol., 2003, vol. 132, pp. 1186–1195.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Wu, H.C. and Jinn, T.L., Heat shock-triggered Ca2+ mobilization accompanied by pectin methylesterase activity and cytosolic Ca2+ oscillation are crucial for plant thermotolerance, Plant Signal Behav., 2010, vol. 5, pp. 1252–1256.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Wu, H.C., Luo, D.L., Vignols, F., and Jinn, T.L., Heat shock-induced biphasic Ca2+ signature and OsCaM1-1 nuclear localization mediate downstream signalling in acquisition of thermotolerance in rice (Oryza sativa L.), Plant Cell Environ., 2012, vol. 35, pp. 1543–1557.

    Article  CAS  PubMed  Google Scholar 

  22. Gao, F., Han, X., Wu, J., Zheng, S., Shang, Z., Sun, D., Zhou, R., and Li, B., A heat-activated calcium-permeable channel — Arabidopsis cyclic nucleotide-gated ion channel 6 — is involved in heat shock responses, Plant J., 2012, vol. 70, pp. 1056–1069.

    Article  CAS  PubMed  Google Scholar 

  23. Liu, H.T., Sun, D.Y., and Zhou, R.G., Ca2+ and AtCAM3 are involved in the expression of heat shock protein gene in Arabidopsis, Plant Cell Environ., 2005, vol. 28, pp. 1276–1284.

    Article  CAS  Google Scholar 

  24. Suri, S.S. and Dhindsa, R.S., A heat-activated map kinase (HAMK) as a mediator of heat shock response in tobacco cells, Plant Cell Environ., 2008, vol. 31, pp. 218–226.

    Article  CAS  PubMed  Google Scholar 

  25. Tunc-Ozdemir, M., Tang, C., Ishka, M.R., Brown, E., Groves, N.R., Myers, C.T., Rato, C., Poulsen, L.R., McDowell, S., Miller, G., Mittler, R., and Harper, J.F., A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development, Plant Physiol., 2013, vol. 161, pp. 1010–1020.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Kuznetsov, V.V., Andreev, I.M., and Trofimova, M.S., The synthesis of Hsps in sugar beet suspension culture cells under hyperthermia exhibits differential sensitivity to calcium, Biochem. Mol. Biol. Int., 1998, vol. 45, pp. 269–278.

    CAS  PubMed  Google Scholar 

  27. Trofimova, M.S., Andreev, I.M., and Kuznetsov, V.V., Calcium is involved in regulation of the synthesis of HSPs in suspension-cultured sugar beet cells under hyperthermia, Physiol. Plant., 1999, vol. 105, pp. 67–73.

    Article  CAS  Google Scholar 

  28. Larkindale, J. and Knight, M.R., Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid, Plant Physiol., 2002, vol. 128, pp. 682–695.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Kolupaev, Yu.E., Akinina, G.E., and Mokrousov, A.V., Induction of heat tolerance in wheat coleoptiles by calcium ions and its relation to oxidative stress, Russ. J. Plant Physiol., 2005, vol. 52, pp. 199–204.

    Article  CAS  Google Scholar 

  30. Pyatrikas, D.V., Rikhvanov, E.G., Fedoseeva, I.V., Varakina, N.N., Rusaleva, T.M., Tauson, E.L., Stepanov, A.V., Borovskii, G.B., and Voinikov, V.K., Mitochondrial Retrograde Regulation of HSP101 Expression in Arabidopsis thaliana under Heat Stress and Amiodarone Action, Russ. J. Plant Physiol., 2014, vol. 61, pp. 80–89.

    Article  CAS  Google Scholar 

  31. Spalding, E.P. and Harper, J.F., The ins and outs of cellular Ca2+ transport, Curr. Opin. Plant Biol., 2011, vol. 14, pp. 715–720.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Li, Z., Yue, H., and Xing, D., MAP kinase 6-mediated activation of vacuolar processing enzyme modulates heat shock-induced programmed cell death in Arabidopsis, New Phytol., 2012, vol. 195, pp. 85–96.

    Article  CAS  PubMed  Google Scholar 

  33. Scott, I. and Logan, D.C., Mitochondrial morphology transition is an early indicator of subsequent cell death in Arabidopsis, New Phytol., 2008, vol. 177, pp. 90–101.

    CAS  PubMed  Google Scholar 

  34. Kim, M.C., Calcium and calmodulin-mediated regulation of gene expression in plants, Mol. Plant, 2009, vol. 2, pp. 13–21.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Sun, X.T., Li, B., Zhou, G.M., Tang, W.Q., Bai, J., Sun, D.Y., and Zhou, R.G., Binding of the maize cytosolic Hsp70 to calmodulin, and identification of calmodulin-binding site in Hsp70, Plant Cell Physiol., 2000, vol. 41, pp. 804–810.

    Article  CAS  PubMed  Google Scholar 

  36. Reddy, V.S., Ali, G.S., and Reddy, A.S., Genes encoding calmodulin-binding proteins in the Arabidopsis genome, J. Biol. Chem., 2002, vol. 277, pp. 9840–9852.

    Article  CAS  PubMed  Google Scholar 

  37. Meiri, D. and Breiman, A., Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs, Plant J., 2009, vol. 59, pp. 387–399.

    Article  CAS  PubMed  Google Scholar 

  38. Al-Quraan, N.A., Locy, R.D., and Singh, N.K., Expression of calmodulin genes in wild type and calmodulin mutants of Arabidopsis thaliana under heat stress, Plant Physiol. Biochem., 2010, vol. 48, pp. 697–702.

    Article  CAS  PubMed  Google Scholar 

  39. Königshofer, H., Tromballa, H.W., and Löppert, H.G., Early events in signalling high-temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production, Plant Cell Environ., 2008, vol. 31, pp. 1771–1780.

    Article  PubMed  Google Scholar 

  40. Zhang, W., Zhou, R.G., Gao, Y.J., Zheng, S.Z., Xu, P., Zhang, S.Q., and Sun, D.Y., Molecular and genetic evidence for the key role of AtCAM3 in heat-shock signal transduction in Arabidopsis, Plant Physiol., 2009, vol. 149, pp. 1773–1784.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Liu, H.T., Li, G.L., Chang, H., Sun, D.Y., Zhou, R.G., and Li, B., Calmodulin-binding protein phosphatase PP7 is involved in thermotolerance in Arabidopsis, Plant Cell Environ., 2007, vol. 30, pp. 156–164.

    Article  CAS  PubMed  Google Scholar 

  42. Liu, H.T., Gao, F., Li, G.L., Han, J.L., Liu, D.L., Sun, D.Y., and Zhou, R.G., The calmodulin-binding protein kinase 3 is part of heat shock signal transduction in Arabidopsis thaliana, Plant J., 2008, vol. 55, pp. 760–773.

    Article  CAS  PubMed  Google Scholar 

  43. Kanchiswamy, C.N., Muroi, A., Maffei, M.E., Yoshioka, H., Sawasaki, T., and Arimura, G., Ca2+-dependent protein kinases and their substrate HsfB2a are differently involved in the heat response signaling pathway in Arabidopsis, Plant Biotechnol., 2010, vol. 27, pp. 469–473.

    Article  CAS  Google Scholar 

  44. Li, B., Liu, H.T., Sun, D.Y., and Zhou, R.G., Ca2+ and calmodulin modulate DNA-binding activity of maize heat shock transcription factor in vitro, Plant Cell Physiol., 2004, vol. 45, pp. 627–634.

    Article  CAS  PubMed  Google Scholar 

  45. Holmberg, C.I., Hietakangas, V., Mikhailov, A., Rantanen, J.O., Kallio, M., Meinander, A., Hellman, J., Morrice, N., MacKintosh, C., Morimoto, R.I., Eriksson, J.E., and Sistonen, L., phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1, EMBO J., 2001, vol. 20, pp. 3800–3810.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Kanchiswamy, C.N., Takahashi, H., Quadro, S., Maffei, M.E., Bossi, S., Bertea, C., Zebelo, S.A., Muroi, A., Ishihama, N., Yoshioka, H., Boland, W., Takabayashi, J., Endo, Y., Sawasaki, T., and Arimura, G., Regulation of Arabidopsis defense responses against Spodoptera littoralis by CPK-mediated calcium signaling, BMC Plant Biol., 2010, vol. 10, p. 97.

    Article  PubMed Central  PubMed  Google Scholar 

  47. Stael, S., Wurzinger, B., Mair, A., Mehlmer, N., Vothknecht, U.C., and Teige, M., Plant organellar calcium signalling: an emerging field, J. Exp. Bot., 2012, vol. 63, pp. 1525–1542.

    Article  CAS  PubMed  Google Scholar 

  48. Moeder, W., Urquhart, W., Ung, H., and Yoshioka, K., The role of cyclic nucleotide-gated ion channels in plant immunity, Mol. Plant, 2011, vol. 4, pp. 442–452.

    Article  CAS  PubMed  Google Scholar 

  49. McAinsh, M.R. and Pittman, J.K., Shaping the calcium signature, New Phytol., 2009, vol. 181, pp. 275–294.

    Article  CAS  PubMed  Google Scholar 

  50. Ward, J.M., Mäser, P., and Schroeder, J.I., Plant ion channels: gene families, physiology, and functional genomics analyses, Annu. Rev. Physiol., 2009, vol. 71, pp. 59–82.

    Article  CAS  PubMed  Google Scholar 

  51. Finka, A., Cuendet, A.F., Maathuis, F.J., Saidi, Y., and Goloubinoff, P., Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance, Plant Cell, 2012, vol. 24, pp. 3333–3348.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Horváth, I., Glatz, A., Nakamoto, H., Mishkind, M.L., Munnik, T., Saidi, Y., Goloubinoff, P., Harwood, J.L., and Vigh, L., Heat shock response in photosynthetic organisms: membrane and lipid connections, Prog. Lipid Res., 2012, vol. 51, pp. 208–220.

    Article  PubMed  Google Scholar 

  53. Liu, Y., Liu, H., Pan, Q., Yang, H., Zhan, J., and Huang, W., The plasma membrane H+-ATPase is related to the development of salicylic acid-induced thermotolerance in pea leaves, Planta, 2009, vol. 229, pp. 1087–1098.

    Article  CAS  PubMed  Google Scholar 

  54. Larkindale, J., Hall, J.D., Knight, M.R., and Vierling, E., Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance, Plant Physiol., 2005, vol. 138, pp. 882–897.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Liu, H.T., Gao, F., Cui, S.J., Han, J.L., Sun, D.Y., and Zhou, R.G., Primary evidence for involvement of IP3 in heat-shock signal transduction in Arabidopsis, Cell Res., 2006, vol. 16, pp. 394–400.

    Article  CAS  PubMed  Google Scholar 

  56. Zheng, S.Z., Liu, Y.L., Li, B., Shang, Z.L., Zhou, R.G., and Sun, D.Y., Phosphoinositide-specific phospholipase C9 is involved in the thermotolerance of Arabidopsis, Plant J., 2012, vol. 69, pp. 689–700.

    Article  CAS  PubMed  Google Scholar 

  57. Kaplan, B., Davydov, O., Knight, H., Galon, Y., Knight, M.R., Fluhr, R., and Fromm, H., Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis, Plant Cell, 2006, vol. 18, pp. 2733–2748.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  58. Whalley, H.J., Sargeant, A.W., Steele, J.F., Lacoere, T., Lamb, R., Saunders, N.J., Knight, H., and Knight, M.R., Transcriptomic analysis reveals calcium regulation of specific promoter motifs in Arabidopsis, Plant Cell, 2011, vol. 23, pp. 4079–4095.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  59. Walsh, C., Barrow, S., Voronina, S., Chvanov, M., Petersen, O.H., and Tepikin, A., Modulation of calcium signalling by mitochondria, Biochim. Biophys. Acta, 2009, vol. 1787, pp. 1374–1382.

    Article  CAS  PubMed  Google Scholar 

  60. Olson, M.L., Chalmers, S., and McCarron, J.G., Mitochondrial organization and Ca2+ uptake, Biochem. Soc. Trans., 2012, vol. 40, pp. 158–167.

    Article  CAS  PubMed  Google Scholar 

  61. Kornmann, B., The molecular Hug between the ER and the mitochondria, Curr. Opin. Cell Biol., 2013, March 8, doi 10.1016/j.ceb.2013.02.010 pii: S0955-0674(13)00033-1

    Google Scholar 

  62. Subbaiah, C.C., Bush, D.S., and Sachs, M.M., Mitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells, Plant Physiol., 1998, vol. 118, pp. 759–771.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Logan, D. and Knight, M.R., Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants, Plant Physiol., 2003, vol. 133, pp. 21–24.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Sun, J., Zhang, C.L., Deng, S.R., Lu, C.F., Shen, X., Zhou, X.Y., Zheng, X.J., Hu, Z.M., and Chen, S.L., An ATP signalling pathway in plant cells: extracellular ATP triggers programmed cell death in Populus euphratica, Plant Cell Environ., 2012, vol. 35, pp. 893–916.

    Article  PubMed  Google Scholar 

  65. Arpagaus, S., Rawyler, A., and Braendle, R., Occurrence and characteristics of the mitochondrial permeability transition in plants, J. Biol. Chem., 2002, vol. 277, pp. 1780–1787.

    Article  CAS  PubMed  Google Scholar 

  66. Virolainen, E., Blokhina, O., and Fagerstedt, K., Ca2+-induced high amplitude swelling and cytochrome c release from wheat (Triticum aestivum L.) mitochondria under anoxic stress, Ann. Bot., 2002, vol. 90, pp. 509–516.

    Article  CAS  PubMed  Google Scholar 

  67. Banti, V., Mafessoni, F., Loreti, E., Alpi, A., and Perata, P., The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis, Plant Physiol., 2010, vol. 152, pp. 1471–1483.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  68. Krause, M. and Durner, J., Harpin inactivates mitochondria in Arabidopsis suspension cells, Mol. Plant-Microbe Interact., 2004, vol. 17, pp. 131–139.

    Article  CAS  PubMed  Google Scholar 

  69. Kuzmin, E.V., Karpova, O.V., Elthon, T.E., and Newton, K.J., Mitochondrial respiratory deficiencies signal up-regulation of genes for heat shock proteins, J. Biol. Chem., 2004, vol. 279, pp. 20 672–20 677.

    Article  CAS  Google Scholar 

  70. Pavlova, E.L., Rikhvanov, E.G., Tauson, E.L., Varakina, N.N., Gamburg, K.Z., Rusaleva, T.M., Borovskii, G.B., and Voinikov, V.K., Effect of salicylic acid on the development of induced thermotolerance and induction of heat shock protein synthesis in the Arabidopsis thaliana Cell Culture, Russ. J. Plant Physiol., 2009, vol. 56, pp. 68–73.

    Article  CAS  Google Scholar 

  71. Pulyaevskaya, M.A., Varakina, N.N., Gamburg, K.Z., Rusaleva, T.M., Stepanov, A.V., Voinikov, V.K., and Rikhvanov, E.G., Sodium fluoride inhibits HSP synthesis in heat-stressed cultured cells of Arabidopsis thaliana, Russ. J. Plant Physiol., 2011, vol. 58, pp. 589–596.

    Article  CAS  Google Scholar 

  72. Vanderauwera, S., Vandenbroucke, K., Inzé, A., van de Cotte, B., Mühlenbock, P., de Rycke, R., Naouar, N., van Gaever, T., van Montagu, M.C., and van Breusegem, F., AtWRKY15 perturbation abolishes the mito-chondrial stress response that steers osmotic stress tolerance in Arabidopsis, Proc. Natl. Acad. Sci. USA, 2012, vol. 109, pp. 20 113–20 118.

    Article  CAS  Google Scholar 

  73. Rikhvanov, E.G., Varakina, N.N., Rusaleva, T.M., Rachenko, E.I., Knorre, D.A., and Voinikov, V.K., Do mitochondria regulate the heat-shock response in Saccharomyces cerevisiae? Curr. Genet., 2005, vol. 48, pp. 44–59.

    Article  CAS  PubMed  Google Scholar 

  74. Fedoseeva, I.V., Pyatrikas, D.V., Varakina, N.N., Rusaleva, T.M., Stepanov, A.V., Rikhvanov, E.G., Borovskii, G.B., and Voinikov, V.K., Effect of amiodarone on thermotolerance and Hsp104p synthesis in the yeast Saccharomyces cerevisiae, Biochemistry (Moscow), 2012, vol. 77, pp. 78–86.

    Article  CAS  Google Scholar 

  75. Robb-Gaspers, L.D., Burnett, P., Rutter, G.A., Denton, R.M., Rizzuto, R., and Thomas, A.P., Integrating cytosolic calcium signals into mitochondrial metabolic responses, EMBO J., 1998, vol. 17, pp. 4987–5000.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  76. Pozniakovsky, A.I., Knorre, D.A., Markova, O.V., Hyman, A.A., Skulachev, V.P., and Severin, F.F., Role of mitochondria in the pheromone- and amiodarone-induced programmed death of yeast, J. Cell Biol., 2005, vol. 168, pp. 257–269.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  77. Suzuki, N., Koussevitzky, S., Mittler, R., and Miller, G., ROS and redox signalling in the response of plants to abiotic stress, Plant Cell Environ., 2012, vol. 35, pp. 259–270.

    Article  CAS  PubMed  Google Scholar 

  78. Kreslavskii, 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  Google Scholar 

  79. Gordeeva, A.V., Labas, Yu.A., and Zvyagil’skaya, R.A., Apoptosis in unicellular organisms: mechanisms and evolution, Biochemistry (Moscow), 2004, vol. 69, pp. 1055–1066.

    Article  CAS  Google Scholar 

  80. Korshunov, S.S., Skulachev, V.P., and Starkov, A.A., High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria, FEBS Lett., 1997, vol. 416, pp. 15–18.

    Article  CAS  PubMed  Google Scholar 

  81. Weir, I.E., Pham, N.A., and Hedley, D.W., Oxidative stress is generated via the mitochondrial respiratory chain during plant cell apoptosis, Cytometry A, 2003, vol. 54, pp. 109–117.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to I. V. Fedoseeva.

Additional information

Original Russian Text © E.G. Rikhvanov, I.V. Fedoseeva, D.V. Pyatrikas, G.B. Borovskii, V.K. Voinikov, 2014, published in Fiziologiya Rastenii, 2014, Vol. 61, No. 2, pp. 155–169.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rikhvanov, E.G., Fedoseeva, I.V., Pyatrikas, D.V. et al. Role of mitochondria in the operation of calcium signaling system in heat-stressed plants. Russ J Plant Physiol 61, 141–153 (2014). https://doi.org/10.1134/S1021443714020125

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443714020125

Keywords

Navigation