Abstract
Due to possible climate changes, heat stress has obtained a serious concern all over the world. Tolerance to this stress via knowledge of metabolic pathways will help us in engineering heat tolerant plants. A group of proteins called heat shock proteins are synthesized following stress and their synthesis is regulated by transcription factors. Under high temperature (HT), reactive oxygen species (ROS) are often induced and can cause damage to lipids, proteins, and nucleic acids. To scavenge the ROS and maintain cell membrane stability, synthesis of antioxidants, osmolytes, and heat shock proteins is of a vital importance. In view of above mentioned, this review highlights the detailed mechanism of pathways involving crucial steps that change during HT stress.
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Abbreviations
- AA:
-
ascorbic acid
- APX:
-
ascorbate peroxidase
- AsA:
-
ascorbate
- CAT:
-
catalase
- DHAR:
-
dehydroascorbate reductase
- GPX:
-
guaiacol peroxidase
- GR:
-
glutathione reductase
- GSH:
-
reduced glutathione
- GSSG:
-
oxidized glutathione
- GST:
-
glutathione-S-transferase
- Hsfs:
-
heat stress transcription factors
- Hsps:
-
heat shock proteins
- HT:
-
high temperature
- LMM:
-
low molecular mass
- LPO:
-
lipid peroxidation
- MDA:
-
malondialdehyde
- MDHAR:
-
monodehydroascorbate reductase
- MTS:
-
membrane thermal stability
- O2 − :
-
superoxide anion
- ·OH:
-
hydroxyl radical
- PS:
-
photosystem
- ROS:
-
reactive oxygen species
- SOD:
-
superoxide dismutase
References
Agarwal, M., Sarkar, N., Grover, A.: Low molecular weight heat shock proteins in plants. — J. Plant Biol. 30: 141–149, 2003.
Ahmad, P., Prasad, M.N.V. (ed.): Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. — Springer, New York 2012.
Almeselmani, M., Deshmukh, P.S., Sairam, R.K., Kushwaha, S.R., Singh, T.P.: Protective role of antioxidant enzymes under high temperature stress. — Plant Sci. 171: 382–388, 2006.
Baniwal, S.K., Bharti, K., Chan, K.Y., Fauth, M., Ganguli, A., Kotak, S., Mishra, S.K., Nover, L., Port, M., Scharf, K., Tripp, L., Weber, C., Zielinski, D., Von Koskull-Doring, P.: Heat stress response in plants: a complex game with chaperones and more than 20 heat stress transcription factors. — J. Biosci. 29: 471–487, 2004.
Biamonti, G., Caceres, J.F.: Cellular stress and RNA splicing. — Trends Biochem. Sci. 34: 146–153, 2009.
Bohnert, H.J., Gong, Q.Q., Li, P.H., Ma, S.S.: Unraveling abiotic stress tolerance mechanisms-getting genomics going. — Curr. Opin. Plant Biol. 9: 180–188, 2006.
Bokszczanin, K.L., Fragkostefanakis, S.: Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. — Front. Plant Sci. 4: 315–335, 2013.
Bosch, S.M.: The role of α-tocopherol in plant stress tolerance. — J. Plant Physiol. 162: 743–748, 2005.
Breusegem, F.V.E., Vranova, J.F., Dat, D.I.: The role of active oxygen species in plant signal transduction. — Plant Sci. 16: 405–414, 2001.
Chakraborty, U., Pradhan, D.: High temperature-induced oxidative stress in Lens culinaris, role of antioxidants and amelioration of stress by chemical pre-treatments. — J. Plant Interact. 6: 43–52, 2011.
Chandrasekar, V., Sairam, R.K., Srivastava, G.C.: Physiological and biochemical responses of hexaploid and tetraploid wheat to drought stress. — J. Agron. Crop Sci. 185: 219–227, 2000.
Charng, Y.Y., Liu, H.C., Liu, N.Y., Chi, W.T., Wang, C.N., Chang, S.H., Wang, T.T.: A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. — Plant Physiol. 143: 251–262, 2007.
Chhabra, M.L., Dhawan, A., Sangwan, N., Dhawan, K., Singh, D.: Phytohormones induced amelioration of high temperature stress in Brassica juncea (L.) Czern & Coss. — In: Proceedings of 16th Australian Research Assembly on Brassicas. Pp. 9–11. Ballarat, Victoria 2009.
Czarnecka-Verner, E., Yuan, C.X., Scharf, K.-D., Englich, G., Gurley, W.B.: Plants contain a novel multi-member class of heat shock factors without transcriptional activator potential. — Plant mol. Biol. 43: 459–471, 2000.
DeRocher, A.E., Vierling, E.: Developmental control of small heat shock protein expression during pea seed maturation. — Plant J. 5: 93–102, 1994.
Dixon, D.P., Cole, D.J., Edward, R.: Cloning and characterization of plant theta and zeta class GSTs: implication for plant GST classification. — Chem. Biol. Interact. 133: 33–36, 2001.
Dixon, D.P., Cumminis, I., Cole, D.J., Edwards, R.: Glutathione mediated detoxification system in plants. — Curr. Opin. Plant Biol. 1: 258–266, 1998.
Eitzinger, J., Orlandini, S., Stefanski, R., Naylor, R.E.L.: Climate change and agriculture: introductory editorial. — J. agr. Sci. 148: 499–500, 2010.
Esfandiari, E., Shekari, F., Esfandiar, M.: The effect of salt stress on antioxidant enzymes activity and lipid peroxidation on the wheat seedlings. — Not. Bot. Hort. Agrobot. Cluj 35: 48–56, 2007.
Feder, M.E., Hofmann, G.E.: Heat-shock proteins, molecular chaperones, and stress response: evolutionary and ecological physiology. — Annu. Rev. Physiol. 61: 243–282, 1999.
Garg, N., Manchanda, G.: ROS generation in plants: boon or bane? — Plant Biosystem. 143: 3788–3796, 2009.
Giorno, F., Wolters-Arts, M., Grillo, S., Scharf, K., Vriezen, W.H., Mariani, C.: Developmental and heat stress-regulated expression of HsfA2 and small heat shock proteins in tomato anthers. — J. exp. Bot. 61: 453–462, 2010.
Goyal, M., Asthir, B.: Polyamine catabolism influences antioxidative defense mechanism in shoots and roots of five wheat genotypes under high temperature stress. — Plant Growth Regul. 60: 13–25, 2010.
Gupta, S.C., Sharma, A., Mishra, M., Mishra, R., Chowdhuri, D.K.: Heat shock proteins in toxicology: how close and how far? — Life Sci. 86: 377–384, 2010.
Gupta, N.K., Agarwal, S., Agarwal, V.P., Nathawat, N.S., Gupta, S., Singh, G.: Effect of short-term heat stress on growth, physiology and antioxidative defence system in wheat seedlings. — Acta Physiol. Plant. 35: 1837–1842, 2013.
Hameed, A., Goher, M., Iqbal, N.: Heat stress-induced cell death, changes in antioxidants, lipid peroxidation and protease activity in wheat leaves. — J. Plant Growth Regul. 31: 283–291, 2012.
Hasanuzzaman, M., Hossain, M.A., Fujita, M.: Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. — Plant Biotechnol. Rep. 5: 353–365, 2011.
Heckathorn, S.A., Downs, C.A., Sharkey, T.D., Coleman, J.S.: The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. — Plant Physiol. 116: 439–444, 1998.
Hemantaranjan, A., Nishant Bhanu, A., Singh, M.N., Yadav, D.K., Patel, P.K.: Heat stress responses and thermotolerance. — Adv. Plant agr. Res. 1: 1–10, 2014.
Hu, W., Hu, G., Han, B.: Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. — Plant Sci. 176: 583–590, 2009.
Kanwischer, M., Porfirova, S., Bergmüller, E., Dörmann, P.: Alterations in tocopherol cyclase activity in transgenic and mutant plants of Arabidopsis affect tocopherol content, tocopherol composition, and oxidative stress. — Plant Physiol. 137: 713–723, 2005.
Kaushal, N., Gupta, K., Bhandhari, K., Kumar, S., Thakur, P., Nayyar, H.: Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism. — Physiol. mol. Biol. Plants 17: 203–213, 2011.
Kumar, M.S., Kumar, G., Srikanthbabu, V., Udayakumar, M.: Assessment of variability in acquired thermotolerance: potential option to study genotypic response and the relevance of stress genes. — J. Plant Physiol. 164: 111–125, 2007.
Kurek, I., Chang, T.K., Bertain, S.M., Madrigal, A., Liu, L., Lassner, M.W., Zhu, G.: Enhanced thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. — Plant Cell 19: 3230–3241, 2007.
Larkindale, J., Knight, M.R.: Protection against heat stress induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene and salicylic acid. — Plant Physiol. 128: 682–695, 2002.
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.
Levitt, M., Gerstein, M., Huang, E., Subbiah, S. Tsai, J.: Protein folding: the endgame. — Annu. Rev. Biochem. 66: 549–579, 1997.
Lindquist, S., Crig, E.A.: The heat-shock proteins. — Annu. Rev. Genet. 22: 631–677, 1988.
Liu, H.C., Liao, H.Y., 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.
Maestri, E., Klueva, N., Perrotta, C., Gulli, M., Nguyen, H.T., Marmiroli, N.: Molecular genetics of heat tolerance and heat shock proteins in cereals. — Plant mol. Biol. 48: 667–681, 2002.
Mittler, R.: Oxidative stress, antioxidants and stress tolerance. — Trends Plant Sci. 7: 405–410, 2002.
Montillet, J.L., Chamnongpol, S, Rustérucci, C., Dat, J., Van de Cotte, B., Agnel, J.P., Battesti, C., Inzé, D., Van Breusegem, F., Triantaphylides, C.: Fatty acid hydroperoxides and H2O2 in the execution of hypersensitive cell death in tobacco leaves. — Plant Physiol. 138: 1516–1526, 2005.
Morimoto, R.I.: Cells in stress: the transcriptional activation of heat shock genes. — Science 259: 1409–1410, 1993.
Morimoto, R.I.: Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. — Gene 12: 3788–3796, 1998.
Morimoto, R.I., Santoro, M.G.: Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. — Nat. Biotechnol. 16: 833–838, 1998.
Morimoto, R.I., Tissieres, A., Georgopoulos, C. (ed): The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor — New York 1994.
Morrow, G., Inaguma, Y., Kato, K., Tanguay, R.M.: The small heat shock protein Hsp 22 of Drosophila melanogaster is a mitochondrial protein displaying oligomeric organization. — J. biol. Chem. 275: 31204–31210, 2000.
Morrow, G., Tanguay, R.M.: Small heat shock protein expression and functions during development. — Int. J. Biochem. Cell Biol. 44: 1613–1621, 2012.
Noctor, G., Foyer, C.H.: Ascorbate and glutathione: keeping active oxygen under control. — Annu. Rev. Plant Physiol. Plant mol. Biol. 49: 249–279, 1998.
Nover, L., Baniwal, S.K.: Multiplicity of heat stress transcription factors controlling the complex heat stress response of plants. — In: Proccedings of International Symposium on Environmental Factors, Cellular Stress and Evolution. P. 15. Varanasi 2006.
Panaretou, B., Zhai, C.: The heat shock proteins: their roles as multi-component machines for protein folding. — Fungal Biol. Rev. 22: 110–119, 2008.
Pastore, A., Martin, S.R., Politou, A., Kondapalli, K.C., Stemmler, T.: Unbiased cold denaturation: low- and high-temperature unfolding of yeast frataxin under physiological conditions. — J. amer. chem. Soc. 129: 5374–5375, 2007.
Preiss, J., Sivak, M.N.: Starch synthesis in sinks and sources. — In: Zamski, E., Schaffer, A.A. (ed.): Photoassimilate Distribution in Plants and Crops. Pp. 63–96. Marcel Dekker, New York 1996.
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.
Rasheed, R., Wahid, A., Farooq, M., Hussain, I., Basra, S.M.A.: Role of proline and glycine betaine pretreatments in improving heat tolerance of sprouting sugarcane (Saccharum sp.) buds. — Plant Growth Regul. 65: 35–45, 2011.
Rodriguez, M., Canales, E., Borras-Hidalgo, O.: Molecular aspects of abiotic stress in plants. — Biotechnol. Appl. 22: 1–10, 2005.
Roxas, V.P., Lodhi, S.A., Garrett, D.K., Mahan, J.R., Allen, R.D.: Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/guaiacol peroxidase. — Plant Cell Physiol. 41: 1229–1234, 2000.
Sairam, R.K., Deshmukh, P.S., Saxena, D.C.: Role of antioxidant systems in wheat genotypes tolerance to water stress. — Biol. Plant. 41: 384–394, 1998.
Sairam, R.K., Srivastava, G.C., Sexena, D.C.: Increased antioxidant activity under elevated temperature: a mechanism of heat stress tolerance in wheat genotypes. — Biol. Plant. 43: 245–251, 2000.
Sakamoto, A., Murata, N.: The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. — Plant Cell Environ. 25: 163–171, 2002.
Sandorf, I., Holländer-Czytko, H.: Jasmonate is involved in the induction of tyrosine aminotransferase and tocopherol biosynthesis in Arabidopsis thaliana. — Planta 216: 173–179, 2002.
Schöffl, F., Prändl, R., Reindl, A.: Regulation of the heat shock response. — Plant Physiol. 117: 1135–1141, 1998.
Schuetz, T.J., Gallo, G.J., Sheldon, L., Tempst, P., Kingston, R.E.: Isolation of a cDNA for HSF2: evidence for two heat shock factor genes in humans. — Proc. nat. Acad. Sci. USA 88: 6911–6915, 1991.
Schulze-Lefert, P.: Plant immunity: the origami of receptor activation. — Curr. Biol. 14: R22–R24, 2004.
Sharma-Natu, P., Sumesh, K.V., Ghildiyal, M.C. Heat shock protein in developing grains in relation to thermotolerance for grain growth in wheat. — Agron. Crop Sci. 196: 76–80, 2010.
Smirnoff, N. (ed.): Environment and Plant Metabolism: Flexibility and Acclimation. — Bios Scientific Publishers, Oxford 1995.
Smith, P., Olesen, J.E.: Synergies between the mitigation of, and adaptation to, climate change in agriculture. — J. agr. Sci. 148: 543–552, 2010.
Snyman, M., Cronje, M.J.: Modulation of heat shock factors accompanies salicylic acid-mediated potentiation of Hsp70 in tomato seedlings. — J. exp. Bot. 59: 2125–2132, 2008.
Sorger, P.K., Nelson, H.C.M.: Trimerization of a yeast transcriptional activator via a coiled-coil motif. — Cell 59: 807–813, 1989.
Stone, P.J., Nicolas, M.E.: Wheat cultivars vary widely in their responses of grain yield and quality to short periods of postanthesis heat stress. — Aust. J. Plant Physiol. 21: 887–900, 1994.
Sumesh, K.V., Sharma-Natu, P., Ghildiyal, M.C.: Starch synthase activity and heat shock protein in relation to thermal tolerance of developing wheat grains. — Biol. Plant. 52: 749–753, 2008.
Sun, W., Montagu, M.V., Verbruggen, N.: Small heat shock proteins and stress tolerance in plants. — Biochim. biophys. Acta 1577: 1–9, 2002.
Sung, D.-Y., Kaplan, F., Lee, K.-J., Guy, C.L.: Acquired tolerance to temperature extremes. — Trends Plant Sci. 8: 179–187, 2003.
Suzuki, N., Mittler, R.: Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. — Physiol. Plant. 126: 45–51, 2006.
Suzuki, N., Miller, G., Morales, J., Shulaev, V., Torres, M.A.: Respiratory burst oxidases: the engines of ROS signaling. — Curr. Opin. Plant Biol. 14: 691–699, 2011.
Suzuki, N., Koussevitzky, S., Mittler, R., Miller, G.: ROS and redox signalling in the response of plants to abiotic stress. — Plant Cell Environ. 35: 259–270, 2012.
Timperio, A.M., Egid, M.G., Zolla, L.: Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). — J. Proteomics 71: 391–411, 2008.
Tripathy, B.C., Oelmüller, R.: Reactive oxygen species generation and signaling in plants. — Plant Signal. Behavior 7: 1621–1633, 2012.
Tripp, J., Mishra, S.K., Scharf, K.-D.: Functional dissection of the cytosolic chaperone network in tomato mesophyll protoplasts. — Plant Cell Environ. 32: 123–133, 2009.
Vierling, E.: The roles of heat shock proteins in plants. — Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 579–620, 1991.
Vinocur, B., Altman, A.: Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. — Curr. Opin. Biotechnol. 16: 123–132, 2005.
Von Koskull-Doring, P., Scharf, K.D., Nover, L.: The diversity of plant heat stress transcription factors. — Trends Plant Sci. 12: 452–457, 2007.
Wagner, D., Przybyla, D., Op den Camp, R., Kim, C., Landgraf, F., Lee, K.P., Wursch, M., Laloi, C., Nater, M., Hideg, E., Apel, K.: The genetic basis of singlet oxygen induced stress responses of Arabidopsis thaliana. — Science 306: 1183–1185, 2004.
Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R.: Heat tolerance in plants: an overview. — Environ. exp. Bot. 61: 199–223, 2007.
Wang, W., Vinocur, B., Shoseyov, O., Altman, A.: Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. — Trends Plant Sci. 9: 244–252, 2004.
Xu, S., Li, J., Zhang, X., Wei, H., Cui, L.: Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. — Environ. exp. Bot. 56: 274–285, 2006.
Yamada, K., Fukao, Y., Hayashi, M., Fukazawa, M., Suzuki, I.: Cytosolic HSP90 regulated the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana. — J. biol. Chem. 282: 37794–37804, 2007.
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Asthir, B. Mechanisms of heat tolerance in crop plants. Biol Plant 59, 620–628 (2015). https://doi.org/10.1007/s10535-015-0539-5
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DOI: https://doi.org/10.1007/s10535-015-0539-5