Biologia Plantarum

, Volume 62, Issue 3, pp 409–420 | Cite as

Mechanisms of heat sensing and responses in plants. It is not all about Ca2+ ions

  • M. Sajid
  • B. Rashid
  • Q. AliEmail author
  • T. Husnain


The climate shift has resulted in frequent heat waves, which cause damaging effects on plant growth and development at different life stages. All cellular processes in plants are highly sensitive to a high temperature. The plasma membrane heat receptors usually sense temperature variations directly or via a change in membrane fluidity. The accumulation of damaged proteins and reactive oxygen species also aid in heat perception. Calcium ions and heat sensors transfer signals to transcription factors through a series of signaling cascades. The heat stress transcription factors (HSFs) effectively regulate expression of heat induced genes. The members of the heat shock transcription factor A1 (HsfA1s) family are master regulators of a heat stress response. Different HSFs interact with each other at different levels and simultaneously operate heat induced gene expression. Interaction of HSFs with each other on multiple levels provides chances for manipulation to improve plant heat stress tolerance.

Additional key words

calcium heat sensors heat stress transcription factors membrane receptors reactive oxygen species 



abscisic Acid


acyl CoA binding-protein


ABA responsive-element bindingfactors/ABRE binding-factors


actin related protein 6


binding immunoglobulin protein


basic leucine zipper


calmodulin 3


calcium/calmodulin binding protein-kinases


cyclin dependent-kinase A1


calcium dependent protein-kinase


cyclic nucleotide-gated channels


DNA polymerase II subunit B3


dehydration responsive element-binding protein-2A


ethylene responsive factors


growth regulation-factor 7


Grim Reaper


histone cluster 1 family member Z


histone cluster 1 family member A


heat stress


heat stress transcription factors


heat shock transcription factor A1


Jungbrunnen 1


mitogen activated proteinkinase 6


multiprotein bridging factor 1C




NAC domain containing Protein 19


nuclear factor Y, subunit A2 or B3


natriuretic peptide receptor 1


negative regulatory domain


phosphatidic acid


phosphoenolpyruvate carboxylase


plasma membrane


protein-phosphatase 7


protein-protein interaction


radical induced cell-death 1


C-repeat binding factor gene expression 2


RCD1 interacting motif


rotamase FKBP 1


rotamase FKBP 2


reactive oxygen species


stromal-interaction molecules


Swi2/Snf2-related ATPase


synaptotagmin A


temperature dependent-repression


transcription factor IIB


transcription factors


transient receptor-potential cation channel subfamily V


unfolded protein response


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  1. Agarwal, P., Agarwal, P. K., Nair, S., Sopory, S., Reddy, M.: Stress-inducible DREB2A transcription factor from Pennisetum glaucum is a phosphoprotein and its phosphorylation negatively regulates its DNA-binding activity. - Mol. Genet. Genom. 277: 189–198, 2007.CrossRefGoogle Scholar
  2. Ahanger, M.A., Akram, N.A., Ashraf, M., Alyemeni, M.N., Wijaya, L., Ahmad, P.: Signal trasduction and biotechnology in response to environmental stresses. - Biol. Plant. 61: 401–416, 2017.CrossRefGoogle Scholar
  3. Anckar, J., Sistonen, L.: Regulation of HSF1 function in the heat stress response: implications in aging and disease. - Ann. Rev. Biochem. 80: 1089–1115, 2011.CrossRefPubMedGoogle Scholar
  4. Blomberg, J., Aguilar, X., Brännström, K., Rautio, L., Olofsson, A., Wittung-Stafshede, P., Björklund, S.: Interactions between DNA, transcriptional regulator Dreb2a and the Med25 mediator subunit from Arabidopsis thaliana involve conformational changes. - Nucl. Acids Res. 40: 5938–5950, 2012.CrossRefPubMedGoogle Scholar
  5. Bokszczanin, K.L., Fragkostefanakis, S., Bostan, H., Bovy, A., Chaturvedi, P., Chiusano, M. L., Firon, N., Iannacone, R., Jegadeesan, S. Klaczynskid, K.: Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. - Front. Plant Sci. 4: 1–20, 2013.CrossRefGoogle Scholar
  6. Brestic, M., Zivcak, M., Olsovska, K., Kalaji, H. M., Shao, H., Hakeem, K.R.: Heat signaling and stress responses in photosynthesis. In: Hakeem, K.R., Reiaz, R.Ul. Tahir, I. (ed.): Plant signaling: Understanding the Molecular Crosstalk. Pp. 241–256. Springer, New Delhi 2014.CrossRefGoogle Scholar
  7. Chen, H., Hwang, J. E., Lim, C. J., Kim, D. Y., Lee, S. Y., Lim, C.O.: Arabidopsis DREB2C functions as a transcriptional activator of HsfA3 during the heat stress response. - Biochem. biophysic. Res. Commun. 401: 238–244, 2010.CrossRefGoogle Scholar
  8. Daudi, A., Cheng, Z., O’Brien, J. A., Mammarella, N., Khan, S., Ausubel, F. M., Bolwell, G. P.: The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. - Plant Cell. 24: 275–287, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Evrard, A., Kumar, M., Lecourieux, D., Lucks, J., Von Koskull-Döring, P., Hirt, H.: Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. - Peer J. 1: e59, 2013.CrossRefPubMedGoogle Scholar
  10. Fragkostefanakis, S., Roeth, S., Schleiff, E., Scharf, K.D.: Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. - Plant Cell Environ. 38: 1881–1895, 2015.CrossRefPubMedGoogle Scholar
  11. Guan, Q., Yue, X., Zeng, H., Zhu, J. The protein phosphatase RCF2 and its interacting partner NAC019 are critical for heat stress-responsive gene regulation and thermotolerance in Arabidopsis. - Plant Cell. 26: 438–453, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Hahn, A., Bublak, D., Schleiff, E., Scharf, K.D.: Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. - Plant Cell 23: 741–755, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Hassan, Z., Sajid, M., Nadeem, T., Sehrai, G.H., Salman, S.: CRISPR CAS9: a noval genome editing tool. - Science Int. 29: 639–644, 2017.Google Scholar
  14. Ikeda, M., Mitsuda, N., Ohme-Takagi, M.: Arabidopsis HsfB1 and HsfB2b act as repressors of the expression of heatinducible Hsfs but positively regulate the acquired thermotolerance. - Plant Physiol. 157: 1243–1254, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Jiao, Y., Sun, L., Song, Y., Wang, L., Liu, L., Zhang, L., Liu, B., Li, N., Miao, C., Hao, F.: AtrbohD and AtrbohF positively regulate abscisic acid-inhibited primary root growth by affecting Ca2+ signalling and auxin response of roots in Arabidopsis. - J. exp. Bot. 64: 4183–4192, 2013.CrossRefPubMedGoogle Scholar
  16. Kim, J.-S., Mizoi, J., Yoshida, T., Fujita, Y., Nakajima, J., Ohori, T., Todaka, D., Nakashima, K., Hirayama, T., Shinozaki, K.: An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating droughtinducible genes in Arabidopsis. - Plant Cell Physiol. 52: 2136–2146, 2011.CrossRefPubMedGoogle Scholar
  17. Königshofer, H., Tromballa, H.W., 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. 31: 1771–1780, 2008.CrossRefPubMedGoogle Scholar
  18. Larkindale, J., Hall, J. D., Knight, M R., Vierling, E.: Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. - Plant Physiol. 138: 882–897, 2005.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Li, M., Berendzen, K. W., Schöffl, F. Promoter specificity and interactions between early and late Arabidopsis heat shock factors. - Plant mol. Biol. 73: 559–567, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Li, N., Sun, L., Zhang, L., Song, Y., Hu, P., Li, C., Hao, F.S.: AtrbohD and AtrbohF negatively regulate lateral root development by changing the localized accumulation of superoxide in primary roots of Arabidopsis. - Planta 241: 591–602, 2015.CrossRefPubMedGoogle Scholar
  21. Li, X.D., Wang, X.L., Cai, Y.M., Wu, J.H., Mo, B.T., Yu, E.-R.: Arabidopsis heat stress transcription factors A2 (HSFA2) and A3 (HSFA3) function in the same heat regulation pathway. - Acta Physiol. Plant. 39: 67, 2017.CrossRefGoogle Scholar
  22. Licausi, F., Kosmacz, M., Weits, D A., Giuntoli, B., Giorgi, F. M., Voesenek, L. A., Perata, P., Van Dongen, J.T.: Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. - Nature 479: 419, 2011.CrossRefPubMedGoogle Scholar
  23. Liu, H. C., Liao, H. T., Charng, Y.Y.: The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. - Plant Cell Environ. 34: 738–751, 2011.CrossRefPubMedGoogle Scholar
  24. Liu, J.X., Howell, S.H.: Managing the protein folding demands in the endoplasmic reticulum of plants. - New Phytol. 211: 418–428, 2016.CrossRefPubMedGoogle Scholar
  25. Maruta, T., Inoue, T., Tamoi, M., Yabuta, Y., Yoshimura, K., Ishikawa, T., Shigeoka, S.: Arabidopsis NADPH oxidases, AtrbohD and AtrbohF, are essential for jasmonic acidinduced expression of genes regulated by MYC2 transcription factor. - Plant Sci. 180: 655–660, 2011.CrossRefPubMedGoogle Scholar
  26. Meiri, D., Tazat, K., Cohen-Peer, R., Farchi-Pisanty, O., Aviezer-Hagai, K., Avni, A., Breiman, A.: Involvement of Arabidopsis ROF2 (FKBP65) in thermotolerance. - Plant mol. Biol. 72: 191, 2010.CrossRefPubMedGoogle Scholar
  27. Mishkind, M., Vermeer, J.E., Darwish, E., Munnik, T.: Heat stress activates phospholipase D and triggers PIP2 accumulation at the plasma membrane and nucleus. - Plant J. 60: 10–21, 2009.CrossRefPubMedGoogle Scholar
  28. Mittler, R., Finka, A., Goloubinoff, P.: How do plants feel the heat? Trends Biochem. Sci. 37: 118–125, 2012.CrossRefPubMedGoogle Scholar
  29. Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V.B., Vandepoele, K., Gollery, M., Shulaev, V., Van Breusegem, F.: ROS signaling: the new wave? - Trends Plant Sci. 16: 300–309, 2011.CrossRefPubMedGoogle Scholar
  30. Mizoi, J., Ohori, T., Moriwaki, T., Kidokoro, S., Todaka, D., Maruyama, K., Kusakabe, K., Osakabe, Y., Shinozaki, K., Yamaguchi-Shinozaki, K.: GmDREB2A; 2, a canonical dehydration-responsive element-binding protein 2-type transcription factor in soybean, is posttranslationally regulated and mediates dependent gene expression. - Plant Physiol. 161: 346–361, 2013.CrossRefPubMedGoogle Scholar
  31. Moreno, A.A., Orellana, A.: The physiological role of the unfolded protein response in plants. - Biol. Res. 44: 75–80, 2011.CrossRefPubMedGoogle Scholar
  32. Morimoto, K., Mizoi, J., Qin, F., Kim, J.-S., Sato, H., Osakabe, Y., Shinozaki, K., Yamaguchi-Shinozaki, K.: Stabilization of Arabidopsis DREB2A is required but not sufficient for the induction of target genes under conditions of stress. - PLoS ONE 8(12): e80457, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Nishizawa-Yokoi, A., Nosaka, R., Hayashi, H., Tainaka, H., Maruta, T., Tamoi, M., Ikeda, M., Ohme-Takagi, M., Yoshimura, K., Yabuta, Y.: HsfA1d and HsfA1e involved in the transcriptional regulation of HsfA2 function as key regulators for the Hsf signaling network in response to environmental stress. Plant Cell Physiol. 52: 933–945, 2011.CrossRefPubMedGoogle Scholar
  34. Ohama, N., Kusakabe, K., Mizoi, J., Zhao, H., Kidokoro, S., Koizumi, S., Takahashi, F., Ishida, T., Yanagisawa, S., Shinozaki, K.: The transcriptional cascade in the heat stress response of Arabidopsis is strictly regulated at the level of transcription factor expression. - Plant Cell 28: 181–201, 2016.PubMedGoogle Scholar
  35. Ohama, N., Sato, H., Shinozaki, K., Yamaguchi-Shinozaki, K.: Transcriptional regulatory network of plant heat stress response. - Trends Plant Sci. 22: 53–65, 2017.CrossRefPubMedGoogle Scholar
  36. Phukan, U.J., Jeena, G.S., Tripathi, V., Shukla, R.K.: Regulation of apetala2eEthylene response factors in plants. - Front. Plant Sci. 8: 150, 2017.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Qu, A.L., Ding, Y.F., Jiang, Q., Zhu, C.: Molecular mechanisms of the plant heat stress response. - Biochem. biophys. Res. Commun. 432: 203–207, 2013.CrossRefPubMedGoogle Scholar
  38. Rao, D. E., Chaitanya, K. Photosynthesis and antioxidative defense mechanisms in deciphering drought stress tolerance of crop plants. - Biol. Plant. 60: 201–218, 2016.CrossRefGoogle Scholar
  39. Rasmussen, S., Barah, P., Suarez-Rodriguez, M.C., Bressendorff, S., Friis, P., Costantino, P., Bones, A.M., Nielsen, H.B., Mundy, J.: Transcriptome responses to combinations of stresses in Arabidopsis. - Plant Physiol. 161: 1783–1794, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Röth, S., Mirus, O., Bublak, D., Scharf, K.D., Schleiff, E.: DNA-binding and repressor function are prerequisites for the turnover of the tomato heat stress transcription factor HsfB1. - Plant J. 89: 31–44, 2017.CrossRefPubMedGoogle Scholar
  41. Sajid, M., Hassan, Z., Sehrai, G.H., Rana, M.A., Puchta, H., Rao, A.Q.: Plant genome editing using engineered nucleases and success of CRISPR/Cas9 system. - Adv. Life Sci. 4: 127–136, 2017.Google Scholar
  42. Sato, H., Mizoi, J., Tanaka, H., Maruyama, K., Qin, F., Osakabe, Y., Morimoto, K., Ohori, T., Kusakabe, K., Nagata, M.: Arabidopsis DPB3-1, a DREB2A interactor, specifically enhances heat stress-induced gene expression by forming a heat stress-specific transcriptional complex with NF-Y subunits. - Plant Cell 26: 4954–4973, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Sato, H., Todaka, D., Kudo, M., Mizoi, J., Kidokoro, S., Zhao, Y., Shinozaki, K., Yamaguchi-Shinozaki, K.: The Arabidopsis transcriptional regulator DPB3-1 enhances heat stress tolerance without growth retardation in rice. - Plant Biotechnol. J. 14: 1756–1767, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Scharf, K.D., Berberich, T., Ebersberger, I., Nover, L.: The plant heat stress transcription factor (Hsf) family: structure, function and evolution. - Biochim. biophysic. Acta 1819: 104–119, 2012.CrossRefGoogle Scholar
  45. Schmollinger, S., Schulz-Raffelt, M., Strenkert, D., Veyel, D., Vallon, O., Schroda, M.: Dissecting the heat stress response in Chlamydomonas by pharmaceutical and RNAi approaches reveals conserved and novel aspects. - Mol. Plant. 6: 1795–1813, 2013.CrossRefPubMedGoogle Scholar
  46. Seo, P.J.: Recent advances in plant membrane-bound transcription factor research: emphasis on intracellular movement. - J. Integr. Plant Biol. 56: 334–342, 2014.CrossRefPubMedGoogle Scholar
  47. Singh, D., Laxmi, A.: Transcriptional regulation of drought response: a tortuous network of transcriptional factors. - Front. Plant Sci. 6: 895, 2015.PubMedPubMedCentralGoogle Scholar
  48. Song, Z.T., Sun, L., Lu, S.J., Tian, Y., Ding, Y., Liu, J.X.: Transcription factor interaction with COMPASS-like complex regulates histone H3K4 trimethylation for specific gene expression in plants. - Proc. nat. Acad. Sci. USA 112: 2900–2905, 2015.CrossRefPubMedGoogle Scholar
  49. Suzuki, N., Miller, G., Morales, J., Shulaev, V., Torres, M.A., Mittler, R.: Respiratory burst oxidases: the engines of ROS signaling.–Curr. Opin. Plant Biol. 14: 691–699, 2011.CrossRefPubMedGoogle Scholar
  50. Vainonen, J. P., Jaspers, P., Wrzaczek, M., Lamminmäki, A., Reddy, R. A., Vaahtera, L., Brosché, M., Kangasjärvi, J.: RCD1–DREB2A interaction in leaf senescence and stress responses in Arabidopsis thaliana. - Biochem. J. 442: 573–581, 2012.CrossRefPubMedGoogle Scholar
  51. Wang, C., Zhang, Q., Shou, H.X.: Identification and expression analysis of OsHsfs in rice. - J. Zhejiang Univ. Sci. B. 10: 291–300, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Wang, X., Huang, B.: Lipid-and calcium-signaling regulation of HsfA2c-mediated heat tolerance in tall fescue. - Environ. exp. Bot. 136: 59–67, 2017.CrossRefGoogle Scholar
  53. Wrzaczek, M., Vainonen, J. P., Gauthier, A., Overmyer, K., Kangasjärvi, J.: Reactive oxygen in abiotic stress perception-from genes to proteins. - In: Shanker, A. (ed): Abiotic Stress Response in Plants. Physiological, Biochemical and Genetic Perspectives. Pp. 27–54. InTech, London 2011.Google Scholar
  54. Wu, A., Allu, A. D., Garapati, P., Siddiqui, H., Dortay, H., Zanor, M.-I., Asensi-Fabado, M A., Munné-Bosch, S., Antonio, C., Tohge, T.: JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. - Plant Cell 24: 482–506, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Xie, Z., Li, D., Wang, L., Sack, F.D., Grotewold, E.: Role of the stomatal development regulators FLP/MYB88 in abiotic stress responses. - Plant J. 64: 731–739, 2010.CrossRefPubMedGoogle Scholar
  56. Yan, Q., Huang, Q., Chen, J., Li, J., Liu, Z., Yang, Y., Li, X., Wang, J.: SYTA has positive effects on the heat resistance of Arabidopsis. - Plant Growth Regul. 81: 467–476, 2017.CrossRefGoogle Scholar
  57. Yang, G.Y., Zhang, W.H., Sun, Y.D., Zhang, T.T., Hu, D., Zhai, M.Z.: Two novel WRKY genes from Juglans regia, JrWRKY6 and JrWRKY53, are involved in abscisic aciddependent stress responses. - Biol. Plant. 61: 611–621, 2017.CrossRefGoogle Scholar
  58. Yao, J., Liu, B., Qin, F.: Modular thermal sensors in temperature-gated transient receptor potential (TRP) channels. - Proc. nat. Acad. Sci. USA 108: 11109–11114, 2011.CrossRefPubMedGoogle Scholar
  59. Yao, Y., He, R. J., Xie, Q. L., Song, L., He, J., Marchant, A., Chen, X. Y., Wu, A.M.: ETHYLENE RESPONSE FACTOR 74 (ERF74) plays an essential role in controlling a respiratory burst oxidase homolog D (RbohD)-dependent mechanism in response to different stresses in Arabidopsis. - New Phytol. 213: 1667–1681, 2017.CrossRefPubMedGoogle Scholar
  60. Yoshida, T., Ohama, N., Nakajima, J., Kidokoro, S., Mizoi, J., Nakashima, K., Maruyama, K., Kim, J.-M., Seki, M., Todaka, D.: Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shockresponsive gene expression. - Mol. Genet. Genom. 286: 321–332, 2011.CrossRefGoogle Scholar
  61. Zhang, S.S., Yang, H., Ding, L., Song, Z.T., Ma, H., Chang, F., Liu, J.X.: Tissue-specific transcriptomics reveals an important role of the unfolded protein response in maintaining fertility upon heat stress in Arabidopsis. - Plant Cell 29: 1007–1023, 2017.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Zhu, J.-K.: Abiotic stress signaling and responses in plants. - Cell 167: 313–324, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Zhu, X., Thalor, S. K., Takahashi, Y., Berberich, T., Kusano, T.: An inhibitory effect of the sequence-conserved upstream open-reading frame on the translation of the main openreading frame of HsfB1 transcripts in Arabidopsis. - Plant Cell Environ. 35: 2014–2030, 2012.CrossRefPubMedGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  1. 1.Centre of Excellence for Molecular BiologyUniversity of the PunjabLahorePakistan
  2. 2.Institute of Molecular Biology and BiotechnologyUniversity of LahoreLahorePakistan

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