Biologia plantarum 62:409-420, 2018 | DOI: 10.1007/s10535-018-0795-2

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

M. Sajid1, B. Rashid1, Q. Ali1,2,*, T. Husnain1
1 Centre of Excellence for Molecular Biology, University of the Punjab, Lahore, Pakistan
2 Institute of Molecular Biology and Biotechnology, University of Lahore, Lahore, Pakistan

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.

Keywords: calcium; heat sensors; heat stress transcription factors; membrane receptors; reactive oxygen species
Subjects: heat stress; calcium; heat sensors; membranes; oxidative stress; histone modification; endoplasmatic reticulum

Received: August 29, 2017; Revised: January 11, 2018; Accepted: January 22, 2018; Published: September 1, 2018Show citation

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Sajid, M., Rashid, B., Ali, Q., & Husnain, T. (2018). Mechanisms of heat sensing and responses in plants. It is not all about Ca2+ ions. Biologia plantarum62(3), 409-420. doi: 10.1007/s10535-018-0795-2.
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References

  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  24. Liu, J.X., Howell, S.H.: Managing the protein folding demands in the endoplasmic reticulum of plants. - New Phytol. 211: 418-428, 2016. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  28. Mittler, R., Finka, A., Goloubinoff, P.: How do plants feel the heat? Trends Biochem. Sci. 37: 118-125, 2012. Go to original source...
  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. Go to original source...
  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. Go to original source...
  31. Moreno, A.A., Orellana, A.: The physiological role of the unfolded protein response in plants. - Biol. Res. 44: 75-80, 2011. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  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. Go to original source...
  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.
  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.
  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. Go to original source...
  47. Singh, D., Laxmi, A.: Transcriptional regulation of drought response: a tortuous network of transcriptional factors. - Front. Plant Sci. 6: 895, 2015. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  62. Zhu, J.-K.: Abiotic stress signaling and responses in plants. - Cell 167: 313-324, 2016. Go to original source...
  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. Go to original source...