biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 59:620-628, 2015 | DOI: 10.1007/s10535-015-0539-5

Mechanisms of heat tolerance in crop plants

B. Asthir1,*
1 Punjab Agricultural University, Ludhiana, India

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.

Keywords: antioxidant defence system; cell membrane stability; heat shock proteins; osmolytes; reactive oxygen species
Subjects: heat tolerance; antioxidants; cell membrane stability; heat shock proteins; osmolytes; reactive oxygen species

Received: February 11, 2015; Revised: April 17, 2015; Accepted: April 20, 2015; Published: December 1, 2015  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Asthir, B. (2015). Mechanisms of heat tolerance in crop plants. Biologia plantarum, 59(4), 620-628. doi: 10.1007/s10535-015-0539-5
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Agarwal, M., Sarkar, N., Grover, A.: Low molecular weight heat shock proteins in plants. - J. Plant Biol. 30: 141-149, 2003. Go to original source...
    2. Ahmad, P., Prasad, M.N.V. (ed.): Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. - Springer, New York 2012. Go to original source...
    3. 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. Go to original source...
    4. 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. Go to original source...
    5. Biamonti, G., Caceres, J.F.: Cellular stress and RNA splicing. - Trends Biochem. Sci. 34: 146-153, 2009. Go to original source...
    6. 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. Go to original source...
    7. Bokszczanin, K.L., Fragkostefanakis, S.: Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. - Front. Plant Sci. 4: 315-335, 2013. Go to original source...
    8. Bosch, S.M.: The role of α-tocopherol in plant stress tolerance. - J. Plant Physiol. 162: 743-748, 2005. Go to original source...
    9. 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. Go to original source...
    10. 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. Go to original source...
    11. 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. Go to original source...
    12. 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. Go to original source...
    13. 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.
    14. 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. Go to original source...
    15. DeRocher, A.E., Vierling, E.: Developmental control of small heat shock protein expression during pea seed maturation. - Plant J. 5: 93-102, 1994. Go to original source...
    16. 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.
    17. Dixon, D.P., Cumminis, I., Cole, D.J., Edwards, R.: Glutathione mediated detoxification system in plants. - Curr. Opin. Plant Biol. 1: 258-266, 1998. Go to original source...
    18. Eitzinger, J., Orlandini, S., Stefanski, R., Naylor, R.E.L.: Climate change and agriculture: introductory editorial. - J. agr. Sci. 148: 499-500, 2010. Go to original source...
    19. 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.
    20. 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. Go to original source...
    21. Garg, N., Manchanda, G.: ROS generation in plants: boon or bane? - Plant Biosystem. 143: 3788-3796, 2009. Go to original source...
    22. 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. Go to original source...
    23. 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. Go to original source...
    24. 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. Go to original source...
    25. 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. Go to original source...
    26. 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. Go to original source...
    27. 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. Go to original source...
    28. 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. Go to original source...
    29. 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. Go to original source...
    30. 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. Go to original source...
    31. 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. Go to original source...
    32. 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. Go to original source...
    33. 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. Go to original source...
    34. 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. Go to original source...
    35. 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. Go to original source...
    36. 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...
    37. Levitt, M., Gerstein, M., Huang, E., Subbiah, S. Tsai, J.: Protein folding: the endgame. - Annu. Rev. Biochem. 66: 549-579, 1997. Go to original source...
    38. Lindquist, S., Crig, E.A.: The heat-shock proteins. - Annu. Rev. Genet. 22: 631-677, 1988. Go to original source...
    39. 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. Go to original source...
    40. 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. Go to original source...
    41. Mittler, R.: Oxidative stress, antioxidants and stress tolerance. - Trends Plant Sci. 7: 405-410, 2002. Go to original source...
    42. 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. Go to original source...
    43. Morimoto, R.I.: Cells in stress: the transcriptional activation of heat shock genes. - Science 259: 1409-1410, 1993. Go to original source...
    44. 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. Go to original source...
    45. Morimoto, R.I., Santoro, M.G.: Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. - Nat. Biotechnol. 16: 833-838, 1998. Go to original source...
    46. 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.
    47. 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. Go to original source...
    48. Morrow, G., Tanguay, R.M.: Small heat shock protein expression and functions during development. - Int. J. Biochem. Cell Biol. 44: 1613-1621, 2012. Go to original source...
    49. Noctor, G., Foyer, C.H.: Ascorbate and glutathione: keeping active oxygen under control. - Annu. Rev. Plant Physiol. Plant mol. Biol. 49: 249-279, 1998. Go to original source...
    50. 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.
    51. Panaretou, B., Zhai, C.: The heat shock proteins: their roles as multi-component machines for protein folding. - Fungal Biol. Rev. 22: 110-119, 2008. Go to original source...
    52. 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. Go to original source...
    53. 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.
    54. 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...
    55. 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. Go to original source...
    56. Rodriguez, M., Canales, E., Borras-Hidalgo, O.: Molecular aspects of abiotic stress in plants. - Biotechnol. Appl. 22: 1-10, 2005.
    57. 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. Go to original source...
    58. 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. Go to original source...
    59. 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. Go to original source...
    60. 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. Go to original source...
    61. 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. Go to original source...
    62. Schöffl, F., Prändl, R., Reindl, A.: Regulation of the heat shock response. - Plant Physiol. 117: 1135-1141, 1998. Go to original source...
    63. 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. Go to original source...
    64. Schulze-Lefert, P.: Plant immunity: the origami of receptor activation. - Curr. Biol. 14: R22-R24, 2004. Go to original source...
    65. 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. Go to original source...
    66. Smirnoff, N. (ed.): Environment and Plant Metabolism: Flexibility and Acclimation. - Bios Scientific Publishers, Oxford 1995.
    67. Smith, P., Olesen, J.E.: Synergies between the mitigation of, and adaptation to, climate change in agriculture. - J. agr. Sci. 148: 543-552, 2010. Go to original source...
    68. 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. Go to original source...
    69. Sorger, P.K., Nelson, H.C.M.: Trimerization of a yeast transcriptional activator via a coiled-coil motif. - Cell 59: 807-813, 1989. Go to original source...
    70. 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. Go to original source...
    71. 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. Go to original source...
    72. Sun, W., Montagu, M.V., Verbruggen, N.: Small heat shock proteins and stress tolerance in plants. - Biochim. biophys. Acta 1577: 1-9, 2002. Go to original source...
    73. Sung, D.-Y., Kaplan, F., Lee, K.-J., Guy, C.L.: Acquired tolerance to temperature extremes. - Trends Plant Sci. 8: 179-187, 2003. Go to original source...
    74. Suzuki, N., Mittler, R.: Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. - Physiol. Plant. 126: 45-51, 2006. Go to original source...
    75. 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. Go to original source...
    76. 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. Go to original source...
    77. 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. Go to original source...
    78. Tripathy, B.C., Oelmüller, R.: Reactive oxygen species generation and signaling in plants. - Plant Signal. Behavior 7: 1621-1633, 2012. Go to original source...
    79. 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. Go to original source...
    80. Vierling, E.: The roles of heat shock proteins in plants. - Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 579-620, 1991. Go to original source...
    81. Vinocur, B., Altman, A.: Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. - Curr. Opin. Biotechnol. 16: 123-132, 2005. Go to original source...
    82. Von Koskull-Doring, P., Scharf, K.D., Nover, L.: The diversity of plant heat stress transcription factors. - Trends Plant Sci. 12: 452-457, 2007. Go to original source...
    83. 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. Go to original source...
    84. Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R.: Heat tolerance in plants: an overview. - Environ. exp. Bot. 61: 199-223, 2007. Go to original source...
    85. 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. Go to original source...
    86. 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. Go to original source...
    87. 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. Go to original source...

    Return to the content