IJSTR

International Journal of Scientific & Technology Research

Home About Us Scope Editorial Board Blog/Latest News Contact Us
0.2
2019CiteScore
 
10th percentile
Powered by  Scopus
Scopus coverage:
Nov 2018 to May 2020

CALL FOR PAPERS
AUTHORS
DOWNLOADS
CONTACT

IJSTR >> Volume 3- Issue 11, November 2014 Edition



International Journal of Scientific & Technology Research  
International Journal of Scientific & Technology Research

Website: http://www.ijstr.org

ISSN 2277-8616



Heat Shock Proteins: Functions And Response Against Heat Stress In Plants

[Full Text]

 

AUTHOR(S)

Magaji G. Usman, M. Y. Rafii, M. R. Ismail, M. A. Malek, Mohammad Abdul Latif, Yusuff Oladosu

 

KEYWORDS

Keywords: Heat Stress; Heat Shock Proteins; Crop Plants; Heat Tolerance

 

ABSTRACT

Abstract: Heat stress has significant effect on protein metabolism, including degradation of proteins, inhibition of protein accumulation and induction of certain protein synthesis. It also poses a serious damage to the growth and development of the plant. The ability of the plants to respond to this stress by maintaining protein in their functional conformation as well as preventing the accumulation of non-native proteins are highly important for the cell survival. Heat shock proteins are involved in signaling, translation, host-defence mechanisms, carbohydrate metabolism and amino acid metabolism. In fact, these proteins are now understood to mediate signaling, translation, host-defence mechanisms, carbohydrate metabolism and amino acid metabolism by playing a significant function in controlling the genome and ultimately features that are obvious. Several reviews have reported the tolerance of plants to different abiotic stresses. The topic of enhancing protection mechanisms (including HSPs) to induce heat resistance is very interesting and research in this area has many repercussions for the understanding of heat stress response. However, this review reports Heat Shock Proteins (HSPs) and their function, research progress on the association of HSPs with plant tolerance to heat stress as well as the response of the HSPs under heat stress as an adaptive defence mechanism.

 

REFERENCES

[1] Vierling, E. The roles of heat shock proteins in plants Annu. Rev. Plant Biol. 1991, 42, 579-620.

[2] Lindquist, S.; Craig, E. The heat-shock proteins. Annu. Rev. Genet. 1988, 22, 631-677.

[3] Efeoğlu, B. Heat Shock Proteins and Heat Shock Response in Plants. Gazi University J. Science. 2009, 22.

[4] Young, J. C. Mechanisms of the Hsp70 chaperone system This paper is one of a selection of papers published in this special issue entitled “Canadian Society of Biochemistry, Molecular & Cellular Biology 52nd Annual Meeting-Protein Folding: Principles and Diseases” and has undergone the Journal's usual peer review process. Biochemistry and Cell Biology, 2010, 88, 291-300.

[5] Pratt, W. B.; Krishna, P.; Olsen, L. J. Hsp90-binding immunophilins in plants: The protein movers. Trends Plant Sci. 2001, 6, 54-58.

[6] De Souza, M. A.; Pimentel, A. J. B.; Ribeiro, G. Breeding for heat-stress tolerance. Plant breeding for abiotic stress tolerance 2012, 137-156, Springer.

[7] Shah, F.; Huang, J.; Cui, K.; Nie, L.; Shah, T.; Chen, C.; Wang, K. Impact of high-temperature stress on rice plant and its traits related to tolerance. The Journal of Agricultural Science, 2011, 149, 545-556.

[8] Singh Rishi, P.; Prasad, P. V.; Sunita, K.; Giri, S. N.; Raja Reddy, K. "Influence of high temperature and breeding for heat tolerance in cotton: a review." Adv. Agron. 2007, 93, 313-385.

[9] Feder, M. Integrative biology of stress: Molecular actors, the ecological theater, and the evolutionary play. International Symposium on Environmental Factors, Cellular Stress and Evolution, Varanasi, India. 2006, 21.

[10] Morimoto, R. I. Cells in stress: Transcriptional activation of heat shock genes. Science-New York then Washington. 1993, 259, 1409-1409.

[11] Gupta, S. C.; Sharma, A.; Mishra, M.; Mishra, R. K.; Chowdhuri, D. K. Heat shock proteins in toxicology: How close and how far? Life Sciences 2010, 86, 377-384.

[12] Iqbal, N.; Farooq, S.; Arshad, R.; Hameed, A. Differential accumulation of high and low molecular weight heat shock proteins in Basmati rice (Oryza sativa L.) cultivars. Genetic resources and crop evolution, 2010, 57, 65-70.

[13] Westerheide, S. D; Anckar, J.; Stevens, S. M.; Sistonen, L.; Morimoto, R. I. Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science, 2009, 323, 1063-1066.

[14] Swindell, W. R.; Huebner, M.; Weber, A. P. Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 2007, 8, 125.

[15] Biamonti, G.; Caceres, J. F. Cellular stress and RNA splicing. Trends Biochem. Sci. 2009, 34,146-153.

[16] Zou, J.; Liu, A.; Chen, X.; Zhou, X.; Gao, G.; Wang, W.; Zhang, X. Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J. Plant Physiol. 2009, 166, 851-861.

[17] Wahid, A.; Gelani, S.; Ashraf, M.; Foolad, M. Heat tolerance in plants: An overview. Environ. Exp. Bot. 2007, 61, 199-223.

[18] Mitra, R.; Bhatia, C. Bioenergetic cost of heat tolerance in wheat crop. Curr. Sci. 2008, 94, 1049-1053.

[19] Huang, B.; Xu, C. Identification and characterization of proteins associated with plant tolerance to heat stress. Journal of integrative plant biology, 2008, 50, 1230-1237.

[20] Palta, J. P. Stress interactions at the cellular and membrane levels. Hortscience. 1990, 25, 1377-1381.

[21] Lyons, J. (Ed.). Low temperature stress in crop plants: the role of the membrane. Elsevier, 2012.

[22] Ferguson, D. L.; Guikema, J. A.; Paulsen, G. M. Ubiquitin pool modulation and protein degradation in wheat roots during high temperature stress. Plant Physiol. 1990, 92, 740-746.

[23] Essemine, J.; Ammar, S.; Bouzid, S. Impact of heat stress on germination and growth in higher plants: Physiological, biochemical and molecular repercussions and mechanisms of defence. J. Biol. Sci, 2010, 10, 565-572.

[24] Babiychuk, E.; Vandepoele, K.; Wissing, J.; Garcia-Diaz, M.; De Rycke, R.; Akbari, H.; ... Kushnir, S. Plastid gene expression and plant development require a plastidic protein of the mitochondrial transcription termination factor family. Proceedings of the National Academy of Sciences, 2011, 108, 6674-6679.

[25] Guy, C. L.; Li, Q. The organization and evolution of the spinach stress 70 molecular chaperone gene family. The Plant Cell Online. 1998, 10, 539-556.

[26] Feder, M. E.; Hofmann, G. E. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annu. Rev. Physiol. 1999, 61, 243-282.

[27] Kalmar, B.; Greensmith, L. Induction of heat shock proteins for protection against oxidative stress. Advanced drug delivery reviews, 2009, 61, 310-318.

[28] 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. 2004, 9, 244-252.

[29] Craig, E. A.; Gross, C. A.; Is hsp70 the cellular thermometer? Trends Biochem. Sci. 1991, 16, 135-140.

[30] Banilas, G.; Korkas, E.; Englezos, V.; Nisiotou, A. A.; Hatzopoulos, P. Genome‐wide analysis of the heat shock protein 90 gene family in grapevine (Vitis vinifera L.). Australian Journal of Grape and Wine Research, 2012, 18, 29-38.

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

[32] Krivokapich, S. J.; Molina, V.; Bergagna, H. F. J.; Guarnera, E. A. Epidemiological survey of Trichinella infection in domestic, synanthropic and sylvatic animals from Argentina. Journal of helminthology, 2006, 80, 267-269.

[33] Nover, L. Heat shock response CRC PressI Llc, 1991.

[34] Tsan, M. F.; Gao, B. Heat shock protein and innate immunity. Cell Mol Immunol, 2004, 1, 274-279.

[35] Gorski, S. M.; Chittaranjan, S.; Pleasance, E. D.; Freeman, J. D.; Anderson, C. L.; Varhol, R. J., ... Marra, M. A. A SAGE approach to discovery of genes involved in autophagic cell death. Current Biology, 2003, 13, 358-363.

[36] Sharma, P.; Sharma, N.; Deswal, R. The molecular biology of the low‐temperature response in plants. Bioessays 2005, 27, 1048-1059.

[37] Åkerfelt, M.; Morimoto, R. I.; Sistonen, L. Heat shock factors: integrators of cell stress, development and lifespan. Nature reviews Molecular cell biology, 2010, 11, 545-555.

[38] Li, G. C.; Mak, J. Y. Re-induction of hsp70 synthesis: an assay for thermotolerance. International journal of hyperthermia, 2009, 25, 249-257.

[39] Whaibi, M. H. Plant heat-shock proteins: A mini review. Journal of King Saud University-Science 2011, 23, 139-150.

[40] Neznanov, N.; Komarov, A. P.; Neznanova, L.; Stanhope-Baker, P.; Gudkov, A. V. Proteotoxic stress targeted therapy (PSTT): induction of protein misfolding enhances the antitumor effect of the proteasome inhibitor bortezomib. Oncotarget, 2011, 2, 209.

[41] Tang, D.; Khaleque, M. A.; Jones, E. L.; Theriault, J. R.; Li, C.; Wong, W. H.; ...Calderwood, S. K. Expression of heat shock proteins and heat shock protein messenger ribonucleic acid in human prostate carcinoma in vitro and in tumors in vivo. Cell stress & chaperones, 2005, 10, 46.

[42] Daugaard, M.; Rohde, M.; Jäättelä, M. The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS letters, 2007, 581, 3702-3710.

[43] Ding, D.; Zhang, L.; Wang, H.; Liu, Z.; Zhang, Z.; Zheng, Y. Differential expression of miRNAs in response to salt stress in maize roots. Annals of Botany,2009, 103, 29-38.

[44] Baszczynski, C. L.; Walden, D. B.; Atkinson, B. G. Maize genome response to thermal shifts. Changes in Eukaryotic Gene Expression in Response to Environmental Stress. 1985, 349-371.

[45] Ma, C.; Haslbeck, M.; Babujee, L.; Jahn, O.; Reumann, S. Identification and characterization of a stress-inducible and a constitutive small heat-shock protein targeted to the matrix of plant peroxisomes. Plant physiology, 2006, 141, 47-60.

[46] Wu, H. C.; Hsu, S. F.; Luo, D. L.; Chen, S. J.; Huang, W. D.; Lur, H. S.; Jinn, T. L. Recovery of heat shock-triggered released apoplastic Ca2+ accompanied by pectin methylesterase activity is required for thermotolerance in soybean seedlings. Journal of experimental botany, 2010, 61, 2843-2852.

[47] Cottee, N. S.; Wilson, I. W.; Tan, D. K.; Bange, M. P. Understanding the molecular events underpinning cultivar differences in the physiological performance and heat tolerance of cotton (Gossypium hirsutum). Funct. Plant Biol. 2014, 41, 56-67.

[48] De Ronde, J. A.; Van Der Mescht, A.; Cress, W. A. Heat-shock protein synthesis in cotton is cultivar dependent. S. Afr. J. Plant Soil 1993, 10, 95-97.

[49] Snider, J. L.; Oosterhuis, D. M.; Skulman, B. W.; Kawakami, E. M. Heat stress‐induced limitations to reproductive success in Gossypium hirsutum. Physiologia plantarum, 2009, 137, 125-138.

[50] Fender, S. E.; O'Connell, M. A. Heat shock protein expression in thermotolerant and thermo-sensitive lines of cotton. Plant Cell Reports. 1989, 8, 37-40.

[51] Grigorova, B.; Vaseva, I.; Demirevska, K.; Feller, U. Combined drought and heat stress in wheat: changes in some heat shock proteins. Biologia Plantarum, 2011, 55, 105-111.

[52] Süle, A.; Vanrobaeys, F.; Hajos, G. Y.; Van Beeumen, J.; Devreese, B. Proteomic analysis of small heat shock protein isoforms in barley shoots. Phytochemistry, 2004, 65, 1853-1863.

[53] Zubo, Y. O.; Lysenko, E. A.; Aleinikova, A. Y.; Kusnetsov, V. V.; Pshibytko, N. L. Changes in the transcriptional activity of barley plastome genes under heat shock. Russian Journal of Plant Physiology, 2008, 55, 293-300.

[54] Senthil-Kumar, M.; Kumar, G.; Srikanthbabu, V.; Udayakumar, M. Assessment of variability in acquired thermotolerance: potential option to study genotypic response and the relevance of stress genes. Journal of plant physiology, 2007, 164, 111-125.

[55] Weber, C.; Nover, L.; Fauth, M. Plant stress granules and mRNA processing bodies are distinct from heat stress granules. The Plant Journal, 2008, 56, 517-530.

[56] Sun, Y.; MacRae, T. H. Small heat shock proteins: molecular structure and chaperone function. Cellular and Molecular Life Sciences CMLS, 2005, 62, 2460-2476.

[57] Weeden, N. F.; Wendel, J. F. Genetics of plant isozymes. Isozymes plant biol. Springer. 1994, 46-72.

[58] Manitašević Jovanović, S.; Tucić, B.; Matić, G. Differential expression of heat-shock proteins Hsp70 and Hsp90 in vegetative and reproductive tissues of Iris pumila. Acta physiologiae plantarum, 2011, 33, 233-240.

[59] Krishna, M. Plant responses to heat stress. Topics in Current Genetics. 2003, 4, 101.

[60] Boorstein, W. R.; Ziegelhoffer, T.; Craig, E. A. Molecular evolution of the HSP70 multigene family. J. Mol. Evol. 1994, 38, 1-17.

[61] Tompa, P.; Kovacs, D. Intrinsically disordered chaperones in plants and animals This paper is one of a selection of papers published in this special issue entitled “Canadian Society of Biochemistry, Molecular & Cellular Biology 52nd Annual Meeting-Protein Folding: Principles and Diseases” and has undergone the Journal's usual peer review process. Biochemistry and Cell Biology, 2010, 88, 167-174.

[62] Fink, A. L. Chaperone-mediated protein folding. Physiol. Rev. 1999, 79, 425-449.

[63] Hartl, F. U. Molecular chaperones in cellular protein folding. Nature. 1996, 381, 571-580.

[64] Sung, D. Y.; Vierling, E.; Guy, C. L. Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol. 2001, 126, 789-800.

[65] Montero-Barrientos, M.; Hermosa, R.; Cardoza, R. E.; Gutiérrez, S.; Nicolás, C.; Monte, E. Transgenic expression of the< i> Trichoderma harzianum hsp70 gene increases< i> Arabidopsis resistance to heat and other abiotic stresses. Journal of plant physiology, 2010, 167, 659-665.

[66] Morimoto, R. I.; Santoro, M. G. Stress–inducible responses and heat shock proteins: New pharmacologic targets for cytoprotection. Nature Biotech. 1998, 16, 833-838.

[67] Kim, B.; Schöffl, F. Interaction between arabidopsis heat shock transcription factor 1 and 70 kDa heat shock proteins. J. Exp. Bot. 2002, 53, 371-375.

[68] Vigh, L.; Horváth, I.; Maresca, B.; Harwood, J. L. Can the stress protein response be controlled by ‘membrane-lipid therapy’?. Trends in biochemical sciences, 2007, 32, 357-363.

[69] Richter, K.; Haslbeck, M.; Buchner, J. The heat shock response: Life on the verge of death. Mol. Cell 2010, 40, 253-266.

[70] Czar, M. J.; Galigniana, M. D.; Silverstein, A. M.; Pratt, W. B.; Geldanamycin, W. B. A heat shock protein 90-binding benzoquinone ansamycin, inhibits steroid-dependent translocation of the glucocorticoid receptor from the cytoplasm to the nucleus. Biochem. 1997, 36, 7776-7785.

[71] García-Cardeña, G.; Fan, R.; Shah, V.; Sorrentino, R.; Cirino, G.; Papapetropoulos, A.; Sessa, W. C. Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature. 1998, 392, 821-824.

[72] Prasinos, C.; Krampis, K.; Samakovli, D.; Hatzopoulos, P. Tight regulation of expression of two Arabidopsis cytosolic Hsp90 genes during embryo development. J. Exp. Bot. 2005, 56, 633-644.

[73] Holt, S. E.; Aisner, D. L.; Baur, J.; Tesmer, V. M.; Dy, M.; Ouellette, M.; Shay, J. W. Functional requirement of p23 and Hsp90 in telomerase complexes. Genes Dev. 1991, 13, 817-826.

[74] Nathan, D. F.; Vos, M. H.; Lindquist, S. In vivo functions of the saccharomyces cerevisiae Hsp90 chaperone. Proc. Natl. Acad. Sci. 1997, 94, 12949-12956.

[75] Berardini, T. Z.; Bollman, K.; Sun, H.; Scott Poethig, R. Regulation of vegetative phase change in Arabidopsis thaliana by cyclophilin 40. Science Signaling. 2001, 291, 2405.

[76] Ludwig-Müller, J.; Krishna, P.; Forreiter, C. A glucosinolate mutant of arabidopsis is thermosensitive and defective in cytosolic Hsp90 expression after heat stress,” Plant Physiol. 2000, 123, 949-958.

[77] Müssig, C.; Fischer, S.; Altmann, T. Brassinosteroid-regulated gene expression. Plant Physiol. 2002, 129, 1241-1251.

[78] Taipale, M.; Jarosz, D. F.; Lindquist, D. S. HSP90 at the hub of protein homeostasis: Emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 2010, 11, 515-528.

[79] Liu, D.L.; Zhang, X.X.; Cheng, Y.X.; Takano, T.; Liu, S.K. Cloning and characterization of the rHsp90 gene in rice (Oryza sativa. L) under environmental stress. Mol. Plant Breed. 2006, 4, 317–322.

[80] Yamada, K.; Fukao, Y.; Hayashi, M.; Fukazawa, M.; Suzuki, I.; Nishimura, M. Cytosolic HSP90 regulates the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana. J. Biol. Chem. 2007, 282, 37794–37804.

[81] Nishizawa-Yokoi, A.; Tainaka, H.; Yoshida, E.; Tamoi, M.; Yabuta, Y.; Shigeoka, S. The 26S proteasome function and Hsp90 activity involved in the regulation of HsfA2 expression in response to oxidative stress. Plant Cell Physiol. 2010, 51, 486–496.

[82] McLellan, C.A.; Turbyville, T.J.; Wijeratne, E.M.; Kerschen, A.; Vierling, E.; Queitsch, C.; Whitesell, L.; Gunatilaka, A.A. A rhizosphere fungus enhances Arabidopsis thermotolerance through production of an HSP90 inhibitor. Plant Physiol. 2007, 145, 174–182.

[83] Ahsan, N.; Komatsu, S. Comparative analyses of the proteomes of leaves and flowers at various stages of development reveal organ‐specific functional differentiation of proteins in soybean. Proteomics, 2009, 9, 4889-4907.

[84] Jackson-Constan, D.; Akita, M.; Keegstra, K. Molecular chaperones involved in chloroplast protein import. Biochimica Et Biophysica Acta (BBA)-Mol. Cell Res. 2001, 1541, 102-113.

[85] Young, J. C.; Agashe, V. R.; Siegers, K.; Hartl, F. U. Pathways of chaperone-mediated protein folding in the cytosol. Nature Reviews Molecular Cell Biology, 2004, 5, 781-791.

[86] Apuya, N.; Yadegari, R.; Fischer, R. L.; Harada, J. J.; Zimmerman, J. L.; Goldberg, R. B. The Arabidopsis embryo mutant schlepperless has a defect in the chaperonin-60α gene. Plant Physiol. 2001, 126, 717-730.

[87] Zabaleta, Eduardo, et al. "Antisense expression of chaperonin 60β in transgenic tobacco plants leads to abnormal phenotypes and altered distribution of photoassimilates." The Plant Journal 1994, 6.3, 425-432.

[88] Mayer, M. P. Gymnastics of molecular chaperones. Mol. Cell 2010, 39, 321–331.

[89] Bukau, B.; Weissman, J.; Horwich, A. Molecular chaperones and protein quality control. Cell 2006, 125, 443–451.

[90] Boston, R. S.; Viitanen, P.V.; Vierling, E. Molecular chaperones and protein folding in plants. Plant Mol. Biol. 1996, 32, 191–222.

[91] Weiss, C.; Bonshtien, A.; Farchi-Pisanty, O.; Vitlin, A.; Azem, A. Cpn20: Siamese twins of the chaperonin world. Plant Mol. Biol. 2009, 69, 227–238.

[92] Kessler, F.; Blobel, G. Interaction of the protein import and folding machineries of the chloroplast. Proc. Natl. Acad. Sci. U. S. A. 1996, 93, 7684–7689.

[93] Madueño, F.; Napier, J. A.; Gray, J.C. Newly imported Rieske iron–sulfur protein associates with both Cpn60 and Hsp70 in the chloroplast stroma. Plant Cell 1993, 5, 1865–1876.

[94] Tsugeki, R.; Nishimura, M. Interaction of homologues of Hsp70 and Cpn60 with ferredoxin-NADP+ reductase upon its import into chloroplasts. FEBS Lett. 1993, 320, 198–202.

[95] Jaru-Ampornpan, P.; Shen, K.; Lam, V.Q.; Ali, M.; Doniach, S.; Jia, T.Z.; Shan, S.O. ATP-independent reversal of a membrane protein aggregate by a chloroplast SRP subunit, Nat. Struct. Mol. Biol. 2010, 17, 696–702.

[96] Falk, S.; Sinning, I. cpSRP43 is a novel chaperone specific for light-harvesting chlorophyll a, b-binding proteins. J. Biol. Chem. 2010, 285, 21655–21661.

[97] Agarwal, M.; Katiyar-Agarwal, S.; Sahi, C.; Gallie, D.; Grover, A. Arabidopsis thaliana Hsp100 proteins: Kith and kin. Cell Stress Chaperon. 2001, 63, 219.

[98] Schirmer, E. C.; Glover, J. R.; Singer, M. A.; Lindquist, S. HSP100/Clp proteins: A common mechanism explains diverse functions. Trends Biochem. Sci. 1996, 21, 289-296.

[99] Bösl, B.; Grimminger, V.; Walter, S. The molecular chaperone Hsp104: A molecular machine for protein disaggregation. J. Struct. Biol. 2006, 156, 139-148.

[100] Adam, Z.; Adamska, I.; Nakabayashi, K.; Ostersetzer, O.; Haussuhl, K.; Manuell, A.; Shinozaki, K. Chloroplast and mitochondrial proteases in arabidopsis. A proposed nomenclature. Plant Physiol. 2001, 125(4), 1912-1918.

[101] Keeler, S. J.; Boettger, C. M.; Haynes, J. G.; Kuches, K. A.; Johnson, M. M.; Thureen, D. L.; Kitto, S. L. Acquired thermotolerance and expression of the HSP100/ClpB genes of lima bean. Plant Physiol. 2000, 123, 1121-1132.

[102] Queitsch, C.; Hong, S.; Vierling, E.; Lindquist, S. Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Sci. Signal. 2000, 12, 479-492

[103] Agarwal, M.; Sahi, C.; Katiyar-Agarwal, S.; Agarwal, S.; Young, T.; Gallie, D.; Grover, A. Molecular characterization of rice hsp101: Complementation of yeast hsp104 mutation by disaggregation of protein granules and differential expression in indica and japonica rice types. Plant Mol. Biol. 2003, 51, 543-553.

[104] Queitsch, C.; Hong, S. W.; Vierling, E.; Lindquist, S. Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. The Plant Cell Online 2000, 12, 479-492.

[105] Sun, W.; Van Montagu, M.; Verbruggen, N. Small heat shock proteins and stress tolerance in plants. Biochimica Et Biophysica Acta. 2002, 1577, 1.

[106] Jaya, N.; Garcia, V.; Vierling, E. Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc. Natl. Acad. Sci. 2009, 106, 15604-15609.

[107] Löw, D.; Brändle, K.; Nover, L.; Forreiter, C. Cytosolic heat-stress proteins Hsp17. 7 class I and Hsp17. 3 class II of tomato act as molecular chaperones in vivo. Planta. 2000, 211, 575-582.

[108] Yu, J. H.; Kim, K. P.; Park, S. M.; Hong, C. Biochemical analysis of a cytosolic small heat shock protein, NtHSP18. 3, from Nicotiana tabacum. Mol. Cells 2005, 19, 328-333.

[109] Ahn, Y.; Zimmerman, J. Introduction of the carrot HSP17. 7 into potato (Solanum tuberosum L.) enhances cellular membrane stability and tuberization in vitro. Plant Cell Environ. 2006, 29, 95-104,.

[110] Charng, Y.; Liu, H.; Liu, N.; Hsu, F.; Ko, S. Arabidopsis Hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiol. 2006, 140, 1297-1305.

[111] Volkov, R. A.; Panchuk, I. I.; Mullineaux, P. M.; Schöffl, F. Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol. Biol. 2006, 61, 733-746.

[112] Sato, Y.; Yokoya, S. Enhanced tolerance to drought stress in transgenic rice plants over expressing a small heat-shock protein, sHSP17. 7. Plant Cell Reports 2008, 27, 329-334.

[113] Zahur, M.; Maqbool, A.; Irfan, M.; Barozai, M. Y. K.; Qaiser, U.; Rashid, B.; Riazuddin, S. Functional analysis of cotton small heat shock protein promoter region in response to abiotic stresses in tobacco using agrobacterium-mediated transient assay. Mol. Biol. Reports 2009, 36, 1915-1921.

[114] Neta-Sharir, I.; Isaacson, T.; Lurie, S.; Weiss, D. Dual role for tomato heat shock protein 21: Protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. The Plant Cell Online. 2005, 17, 1829-1838.

[115] Guo, S.; Zhou, H.; Zhang, X.; Li, X.; Meng, Q. Overexpression of< i> CaHSP26 in transgenic tobacco alleviates photoinhibition of PSII and PSI during chilling stress under low irradiance. J. Plant Physiol. 2007, 164, 126-136.

[116] Sun, W.; Bernard, C.; Van De Cotte, B.; Van Montagu, M.; Verbruggen, N. At‐HSP17. 6A, encoding a small heat‐shock protein in arabidopsis, can enhance osmotolerance upon overexpression. Plant J. 2001, 27, 407-415.

[117] Timperio, A. M.; Egidi, M. G; Zolla, L. Proteomics applied on plant abiotic stresses: Role of heat shock proteins (HSP). J. Proteomics. 2008, 71, 391-411.

[118] Mogk, A.; Schlieker, C.; Friedrich, K. L.; Schönfeld, H.; Vierling, E.; Bukau, B. Refolding of substrates bound to small hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. J. Biol. Chem. 2003, 278, 31033-31042.

[119] Downs, C. A.; Heckathorn, S. A. The mitochondrial small heat shock protein protects NADH:ubiquinone oxidoreductase of the electron transport chain during heat stress in plants. Febs Lett. 1998, 430, 246–250.

[120] Snyman, M.; Cronje, M. Modulation of heat shock factors accompanies salicylic acid-mediated potentiation of Hsp70 in tomato seedlings. J. Exp. Bot. 2008, 59, 2125-2132.

[121] Liming, Y.; Qian, Y.; Pigang, L.; Sen, L. Expression of the HSP24 gene from Trichoderma harzianum in Saccharomyces cerevisiae. J. Therm. Biol. 2008, 33, 1–6.

[122] Sun, W.; Bernard, C.; van de Cotte, B.; Montagu, M.V.; Verbruggen, N. At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J. 2001, 27, 407–415.

[123] Wang, Y.; Ying, J.; Kuzma, M.; Chalifoux, M.; Sample, A.; McArthur, C.; Uchacz, T.; Sarvas, C.; Wan, J.; Dennis, D.T.; et al. Molecular tailoring of farnesylation for plant drought tolerance and yield protection. Plant J. 2005, 43, 413–424.

[124] Miroshnichenko, S.; Tripp, J.; Nieden, U.Z.; Neumann, D.; Conrad, U.; Manteuffel, R. Immunomodulation of function of small heat shock proteins prevents their assembly into heat stress granules and results in cell death at sub-lethal temperatures. Plant J. 2005, 41, 269–281.

[125] Bukau, B.; Weissman, J.; Horwich, A. Molecular chaperones and protein quality control. Cell. 2006, 125, 443-451.

[126] Hartl, F. U.; Hayer-Hartl, M. Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 2009, 16, 574-581.

[127] Morimoto, R. I. Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes and Development. 2008, 22, 1427-1438.

[128] Fender, S. E.; O'Connell, M. A. Expression of the heat shock response in a tomato interspecific hybrid is not intermediate between the two parental responses.” Plant Physiol. 1990, 93, 1140-1146.

[129] Haddadi, F. Development of A Plant Regeneration System and Analysis of 101 Heat Shock Protein in Strawberry Cv.Camarosa Following Gene Bombardment. Msc thesis, 2009, 30-35

[130] Ortiz, C.; Cardemil, L. Heat‐shock responses in two leguminous plants: a comparative study. J. Exp. Bot. 2001, 52, 1711-1719.

[131] Campbell, J.L.; Klueva, N.Y.; Zheng, H.G.; Nieto-Sotelo, J.; Ho, T.H.; Nguyen, H.T. “Cloning of new members of heat shock protein HSP101 gene family in wheat (Triticum aestivum (L.) Moench) inducible by heat, dehydration, and ABA,” Biochimica et Biophysica Acta 2001, 1517, 270–277.

[132] Batra, G.; Chauhan, V. S.; Singh, A.; Sarkar, N. K.; Grover, A. Complexity of rice Hsp100 gene family: lessons from rice genome sequence data. Journal of biosciences, 2007, 32, 611-619.

[133] Zhang, Q.; Denlinger, D. L. Molecular characterization of heat shock protein 90, 70 and 70 cognate cDNAs and their expression patterns during thermal stress and pupal diapause in the corn earworm. Journal of insect physiology, 2010, 56, 138-150.

[134] Duan, Y. H.; Guo, J.; Ding, K.; Wang, S. J.; Zhang, H.; Dai, X. W.; ... Kang, Z. S. Characterization of a wheat HSP70 gene and its expression in response to stripe rust infection and abiotic stresses. Molecular biology reports 2011, 38, 301-307.

[135] S¨ule, A.; Vanrobaeys, F.; Haj ´os, G.Y.; Van Beeumen, J.; Devreese, B. “Proteomic analysis of small heat shock protein isoforms in barley shoots.” Phytochemistry 2004, 65, 1853–1863.

[136] Lee, D.G.; Ahsan, N.; Lee, S.H.; et al., “A proteomic approach in analyzing heat-responsive proteins in rice leaves,” Proteomics 2007, 7, 3369–3383.

[137] Xing, J.; Xu, Y.; Tian, J.; Gianfagna, T.; Huang, B. “Suppression of shade- or heat-induced leaf senescence in creeping bentgrass through transformation with the ipt gene for cytokinin synthesis,” J. Am. Soc. Hortic. Sci.2009, 134, 602–609.

[138] Xu, Yan; Chenyang Zhan,; Bingru Huang. "Heat shock proteins in association with heat tolerance in grasses." Int. J. Proteomics 2011, 2011.

[139] Zhang, Jin, et al. "Genome-wide analysis of the Populus Hsp90 gene family reveals differential expression patterns, localization, and heat stress responses." BMC genomics 2013, 14.1, 1-14.

[140] Kumar, R. R.; Goswami, S.; Sharma, S. K.; Pathak, H.; Rai, G. K.; Rai, R. D. Genome Wide Identification of Target Heat Shock Protein90 Genes and Their Differential Expression against Heat Stress in Wheat. Int. J. Biochem. Res. Rev .2012, 2.

[141] Young, R. A. Stress proteins and immunology. Annu. Rev. Immunol. 1990, 8, 401-420.

[142] Gilliham, M.; Dayod, M.; Hocking, B. J.; Xu, B.; Conn, S. J.; Kaiser, B. N.; ...Tyerman, S. D. Calcium delivery and storage in plant leaves: exploring the link with water flow. Journal of experimental botany, 2011, 62, 2233-2250.

[143] Barbe, M. F.; Tytell, M.; Gower, D. J.; Welch, W. J. Hyperthermia protects against light damage in the rat retina. Science. 1988, 241, 1817-1820.

[144] Levitt, M.; Gerstein, M.; Huang, E.; Subbiah, S.; Tsai, J. Protein folding: The endgame. Annu. Rev. Biochem. 1997, 66, 549-579.

[145] Nakamoto, H.; Vígh, L. The small heat shock proteins and their clients. Cell. Mol. Life Sci. 2007, 64, 294-306.

[146] 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. 2009, 176, 583-590.

[147] Panaretou, B.; Zhai, C. The heat shock proteins: Their roles as multi-component machines for protein folding. Fungal Biol. Rev. 2008, 22, 110-119.

[148] Schulze-Lefert, P. Plant immunity: The origami of receptor activation. Curr. Biol. 2004, 14, R22-R24.

[149] Tripp, J.; Mishra, S. K.; Scharf, K. Functional dissection of the cytosolic chaperone network in tomato mesophyll protoplasts. Plant Cell Environ. 2009, 32, 123-133.

[150] Polla, B. A role for heat shock proteins in inflammation? Immunol. Today 1988, 9, 134-137.

[151] Miller, L.; Qureshi, M. Induction of heat-shock proteins and phagocytic function of chicken macrophage following in vitro heat exposure. Veterinary Immunology and Immunopathology. 1992, 30, 179-191.

[152] Wahid, A.,; Close, T. J.Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biologia Plantarum, 2007, 51(1), 104-109.

[153] Baler, R.; Welch, W. J.; Voellmy, R. Heat shock gene regulation by nascent polypeptides and denatured proteins: Hsp70 as a potential autoregulatory factor. J. Cell Biol. 1992, 117, 1151-1159.

[154] Åkerfelt, M.; Morimoto, R. I.; Sistonen, L. Heat shock factors: integrators of cell stress, development and lifespan. Nature reviews Molecular cell biology, 2010, 11, 545-555.

[155] Calderwood, S. K. Heat shock proteins in breast cancer progression-A suitable case for treatment?. International Journal of Hyperthermia, 2010, 26(7), 681-685.

[156] Nover, L.; Bharti, K.; Döring, P.; Mishra, S. K.; Ganguli, A.; Scharf, K. Arabidopsis and the heat stress transcription factor world: How many heat stress transcription factors do we need? Cell Stress Chaperon. 2001, 6, 177.

[157] Scharf, K.; Höhfeld, I.; Nover, L. Heat stress response and heat stress transcription factors. J. Biosciences 1998, 23, 313-329.

[158] Scharf, K.; Rose, S.; Zott, W.; Schöffl, F.; Nover, L.; Schöff, F. Three tomato genes code for heat stress transcription factors with a region of remarkable homology to the DNA-binding domain of the yeast HSF. EMBO J. 1990, 9, 4495.

[159] Mishra, S. K.; Tripp, J.; Winkelhaus, S.; Tschiersch, B.; Theres, K.; Nover, L.; Scharf, K. In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev. 2002, 16, 1555-1567.

[160] Mayer, M.; Bukau, B. Hsp70 chaperones: Cellular functions and molecular mechanism. Cell. Mol. Life Sci. 2005, 62, 670-684.

[161] Hartl, F. U.; Hayer-Hartl, M. Molecular chaperones in the cytosol: From nascent chain to folded protein. Science. 2002, 295, 1852-1858.

[162] Mirus, O.; Schleiff, E. The evolution of tetratricopeptide repeat domain containing receptors involved in protein translocation. Endocytobiosis Cell Res. 2009, 19, 31-50.

[163] Zhang, X.; Glaser, E. Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends Plant Sci. 2002, 7, 14-21.

[164] Ballinge, C. A.; Connell, P.; Wu, Y.; Hu, Z.; Thompson, L. J.; Yin, L.; Patterson, C. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol. Cell. Biol. 1991, 19, 4535-4545.

[165] Lüders, J.; Demand, J.; Höhfeld, J. The ubiquitin-related BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome. J. Biol. Chem. 2000, 275, 4613-4617.

[166] Schramm, F.; Ganguli, A.; Kiehlmann, E.; Englich, G.; Walch, D.; von Koskull-Doring, P. The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol. Biol. 2006, 60, 72.

[167] Davletova, S.; Schlauch, K.; Coutu, J.; Mittler, R. The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol. 2005, 139, 56.

[168] Gallie, D. R.; Le, H.; Caldwell, C.; Tanguay, R. L.; Hoang, N. X.; Browning, K. S. The phosphorylation state of translation initiation factors is regulated developmentally and following heat shock in wheat. J. Biol. Chem. 1997, 272, 53.

[169] Ye, S.; Yu, S.; Shu, L.; Wu, J.; Wu, A.; Luo, L. Expression profile analysis of 9 heat shock protein genes throughout the life cycle and under abiotic stress in rice. Chinese Science Bulletin 2012, 57, 336-343.

[170] Miernyk, J. A. The 70 kDa stress-related proteins as molecular chaperones. Trends Plant Sci. 1997, 2, 7.

[171] Renaut, J.; Hausman, J. F.; Wisniewski, M. E. Proteomics and low-temperature studies: bridging the gap between gene expression and metabolism. Physiol. Plant 2006, 126, 109.

[172] Lee, D. G.; Ahsan, N.; Lee, S. H.; Kang, K. Y.; Bahk, J. D.; Lee, I. J. A proteomic approach in analyzing heat-responsive proteins in rice leaves,” Proteomics. 2007, 7, 83.

[173] Polenta, G. A.; Calvete, J. J.; González, C. B. Isolation and characterization of the main small heat shock proteins induced in tomato pericarp by thermal treatment. FEBS J. 2007, 274, 55.

[174] Lee, D. G.; Ahsan, N.; Lee, S. H.; Kang, K. Y.; Bahk, J. D.; Lee, I. J.; Lee, B. H. A proteomic approach in analyzing heat‐responsive proteins in rice leaves. Proteomics 2007, 7, 3369-3383.

[175] Larkindale, J.; Vierling, E. Core genome responses involved in acclimation to high temperature. Plant Physiol. 2008, 146, 61.

[176] Downs, C.A.; Heckathorn, S.A.; Bryan, J.K.; Coleman, J.S. “The methionine-rich low molecular weight chloroplast heat shock protein: Evolutionary conservation and accumulation in relation to thermotolerance”, Am. J. Bot. 1998, 85, 175-183.

[177] Krishnan, M.; Nguyen, H.T.; Burke, J.J. “Heat shock protein synthesis and thermal tolerance in wheat.” Plant Physiol. 1989, 90, 140-145.

[178] Finka, A.; Cuendet, A. F. H.; Maathuis, F. J.; Saidi, Y.; Goloubinoff, P. Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance. The Plant Cell Online, 2012, 24, 3333-3348.

[179] Weng, J.; Nguyen, H.T.; “Differences in the heat shock response between thermotolerant and thermosusceptible cultivars of hexaploid wheat”. Theor. Appl. Genet., 1992, 84, 941-946.

[180] Maestri, E.; Klueva, N.; Perrotta, C.; Gulli, M.; Nguyen, H.J.; Marmiroli, N.; “Molecular genetics of heat tolerance and heat shock proteins in cereals”. Plant Mol. Biol. 2002, 48, 667-681.