Advertisement

Heat Shock Proteins and Abiotic Stress Tolerance in Plants

  • Divya Mishra
  • Shubhendu Shekhar
  • Deepika Singh
  • Subhra Chakraborty
  • Niranjan Chakraborty
Chapter
Part of the Heat Shock Proteins book series (HESP, volume 13)

Abstract

Abiotic stresses restrict plant growth and development, and reduce harvest index of many crop species worldwide. Maintenance of native conformation of proteins and reducing the accumulation of non-native proteins are imperative for survival under stress conditions as such stresses frequently lead to protein aggregation causing metabolic dysfunction. Heat shock proteins (HSP) play a key role in conferring abiotic stress tolerance. Plants protect themselves from numerous stresses by inducing HSP, besides some stress-responsive proteins, suggesting analogous response mechanisms. A close association between the HSP and ROS also co-exists, indicating that plants have evolved to gain a higher degree of regulation over ROS toxicity and can use ROS as elicitor to induce HSP for better adaptations through activating an array of molecules. Therefore, unraveling the mechanisms of plant response against various stress and the role of HSP in acquired stress tolerance is utmost important to delineate their specific function as a part of stress-responsive module. The HSP have been well characterized in different crop species, albeit the knowledge about their correlation with genome sequence information as well as their functional plasticity is limited.

Keywords

Abiotic Stress Chaperones Co-chaperones Heat shock factor Heat shock protein Protein folding Stress tolerance 

Notes

Acknowledgements

This work was supported by the National Institute of Plant Genome Research (NIPGR). We kindly acknowledge the University Grant Commission (UGC), Govt. of India for providing predoctoral fellowship to D.M, Department of Biotechnology (DBT), Govt. of India for providing predoctoral fellowship to D.S., and DST-SERB for providing postdoctoral fellowship to S.S.

References

  1. Adam, Z., & Clarke, A. K. (2002). Cutting edge of chloroplast proteolysis. Trends in Plant Science, 7, 451–456.PubMedCrossRefGoogle Scholar
  2. Adam, Z., Adamska, I., Nakabayashi, K., Ostersetzer, O., Haussuhl, K., Manuell, A., Zheng, B., Vallon, O., Rodermel, S. R., Shinozaki, K., & Clarke, A. K. (2001). Chloroplast and mitochondrial proteases in Arabidopsis. A proposed nomenclature. Plant Physiology, 125, 1912–1918.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Agrawal, L., Chakraborty, S., Jaiswal, D., Gupta, S., Datta, A., & Chakraborty, N. (2008). Comparative proteomics of tuber induction, development and maturation reveal the complexity of tuberization process in potato (Solanum tuberosum L.) Journal of Proteome Research, 7, 3803–3817.PubMedCrossRefGoogle Scholar
  4. Agrawal, L., Narula, K., Basu, S., Shekhar, S., Ghosh, S., Datta, A., Chakraborty, N., & Chakraborty, S. (2013). Comparative proteomics reveals a role for seed storage protein, AmA1 in cellular growth, development and nutrient accumulation. Journal of Proteome Research, 12, 4904–4930.PubMedCrossRefGoogle Scholar
  5. Agrawal, L., Gupta, S., Mishra, S. K., Pandey, G., Kumar, S., Chauhan, P., Chakrabarty, D., & Nautiyal, C. (2016). Elucidation of complex nature of PEG induced drought-stress response in Rice root using comparative proteomics approach. Frontiers in Plant Science, 7, 1466.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Ahn, Y. J., & Song, N. H. (2012). A cytosolic heat shock protein expressed in carrot (Daucus carota L.) enhances cell viability under oxidative and osmotic stress conditions. Hortscience, 47, 143–148.Google Scholar
  7. Ahuja, I., de Vos, R. C., Bones, A. M., & Hall, R. D. (2010). Plant molecular stress responses face climate change. Trends in Plant Science, 15, 664–674.PubMedCrossRefGoogle Scholar
  8. Alvim, F. C., Carolino, S. M., Cascardo, J. C., Nunes, C. C., Martinez, C. A., Otoni, W. C., & Fontes, E. P. (2001). Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiology, 126, 1042–1054.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Al-Whaibi, M. H. (2011). Plant heat-shock proteins: A mini review. Journal of King Saud University – Science, 23, 139–150.CrossRefGoogle Scholar
  10. Bae, M. S., Cho, E. J., Choi, E.-Y., & Park, O. K. (2003). Analysis of the Arabidopsis nuclear proteome and its response to cold stress. The Plant Journal, 36, 652–663.PubMedCrossRefGoogle Scholar
  11. Balbuena, T. S., Salas, J. J., Martínez-Force, E., Garcés, R., & Thelen, J. J. (2011). Proteome analysis of cold acclimation in sunflower. Journal of Proteome Research, 10, 2330–2346.PubMedCrossRefGoogle Scholar
  12. Baniwal, S. K., Bharti, K., Chan, K. Y., Fauth, M., Ganguli, A., Kotak, S., Mishra, S. K., Nover, L., Port, M., Scharf, K. D., Tripp, J., Weber, C., Zielinski, D., & von Koskull-Döring, P. (2004). Heat stress response in plants: A complex game with chaperones and more than twenty heat stress transcription factors. Journal of Biosciences, 29, 471–487.PubMedCrossRefGoogle Scholar
  13. Banti, V., Mafessoni, F., Loreti, E., Alpi, A., & Perata, P. (2010). The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiology, 152, 1471–1483.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Banzet, N., Richaud, C., Deveaux, Y., Kazmaier, M., Gagnon, J., & Triantaphylides, C. (1998). Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. The Plant Journal, 13, 519–527.PubMedCrossRefGoogle Scholar
  15. Benešová, M., Holá, D., Fischer, L., Jedelský, P. L., Hnilička, F., Wilhelmová, N., Rothová, O., Kočová, M., Procházková, D., Honnerová, J., Fridrichová, L., & Hniličková, H. (2012). The physiology and proteomics of drought tolerance in maize: Early stomatal closure as a cause of lower tolerance to short-term dehydration? PLoS One, 7, e38017.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bharti, K., & Nover, L. (2002). Heat stress-induced signaling. In D. Scheel & C. Wasternack (Eds.), Plant signal transduction: Frontiers in molecular biology (pp. 74–115). Oxford., 2002: Oxford University Press.Google Scholar
  17. Bhushan, D., Jaiswal, D. K., Ray, D., Basu, D., Data, A., Chakraborty, S., & Chakraborty, N. (2011). Dehydration-responsive reversible and irreversible changes in the extracellular matrix: Comparative proteomics of chickpea genotypes with contrasting tolerance. Journal of Proteome Research, 10, 2027–2046.PubMedCrossRefGoogle Scholar
  18. Bonhomme, L., Monclus, R., Vincent, D., Carpin, S., Lomenech, A. M., Plomion, C., Brignolas, F., & Morabito, D. (2009). Leaf proteome analysis of eight Populus ×euramericana genotypes: Genetic variation in drought response and in water-use efficiency involves photosynthesis-related proteins. Proteomics, 9, 41211–41242.CrossRefGoogle Scholar
  19. Boston, R. S., Viitanen, P. V., & Vierling, E. (1996). Molecular chaperones and protein folding in plants. Plant Molecular Biology, 32, 191–222.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Breiman, A. (2014). Plant Hsp90 and its co-chaperones. Current Protein & Peptide Science, 15, 232–244.CrossRefGoogle Scholar
  21. Burke, J. J., Hatfield, J. L., Klein, R. P., & Mullet, J. E. (1985). Accumulation of heat shock proteins in field-grown cotton. Plant Physiology, 78, 394–398.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chandel, G., Dubey, M., & Meena, R. (2013). Differential expression of heat shock proteins and heat stress transcription factor genes in rice exposed to different levels of heat stress. Journal of Plant Biochemistry and Biotechnology, 22, 277–285.CrossRefGoogle Scholar
  23. Chankova, S. G., Dimova, E. G., Mitrovska, Z., Miteva, D., Mokerova, D. V., Yonova, P. A., & Yurina, N. P. (2014). Antioxidant and HSP70B responses in Chlamydomonas reinhardtii genotypes with different resistance to oxidative stress. Ecotoxicology and Environmental Safety, 101, 131–137.PubMedCrossRefGoogle Scholar
  24. Chen, Q., & Vierling, E. (1991). Analysis of conserved domains identifies a unique structural feature of a chloroplast heat shock protein. Molecular & General Genetics, 226, 425–431.CrossRefGoogle Scholar
  25. Chen, X., Lin, S., Liu, Q., Huang, J., Zhang, W., Lin, J., Wang, Y., Ke, Y., & He, H. (2014a). Expression and interaction of small heat shock proteins (sHsps) in rice in response to heat stress. Biochimica et Biophysica Acta, 1844, 818–828.PubMedCrossRefGoogle Scholar
  26. Chen, Y., Chen, X., Wang, H., Bao, Y., & Zhang, W. (2014b). Examination of the leaf proteome during flooding stress and the induction of programmed cell death in maize. Proteome Science, 12, 33.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Choudhary, M. K., Basu, D., Datta, A., Chakraborty, N., & Chakraborty, S. (2009). Dehydration-responsive nuclear proteome of rice (Oryza sativa L.) illustrates protein network, novel regulators of cellular adaptation, and evolutionary perspective. Molecular & Cellular Proteomics, 8, 1579–1598.CrossRefGoogle Scholar
  28. Cruz de carvalho, R., Bernardes DA Silva, A., Soares, R., Almeida, A. M., Coelho, A. V., Marques DA Silva, J., & Branquinho, C. (2014). Differential proteomics of dehydration and rehydration in bryophytes: Evidence towards a common desiccation tolerance mechanism. Plant, Cell & Environment, 37, 1499–1515.CrossRefGoogle Scholar
  29. Czarnecka, E., Nagao, R. T., Key, J. L., & Gurley, W. B. (1988). Characterization of Gmhsp26-A, a stress gene encoding a divergent heat shock protein of soybean: Heavy-metal-induced inhibition of intron processing. Molecular and Cellular Biology, 8, 1113–1122.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Downs, C. A., Ryan, S. L., & Heckathorn, S. A. (1999). The chloroplast small heat-shock protein: Evidence for a general role in protecting photosystem II against oxidative stress and photoinhibition. Journal of Plant Physiology, 155, 488–496.CrossRefGoogle Scholar
  31. Duck, N. B., & Folk, W. R. (1994). Hsp70 heat shock protein cognate is expressed and stored in developing tomato pollen. Plant Molecular Biology, 26, 1031–1039.PubMedCrossRefGoogle Scholar
  32. Dumont, E., Bahrman, N., Goulas, E., Valot, B., Sellier, H., Hilbert, J. L., Vuylsteker, C., Lejeune-Hénaut, I., & Delbreil, B. (2011). A proteomic approach to decipher chilling response from cold acclimation in pea (Pisum sativum L.) Plant Science, 180, 86–98.PubMedCrossRefGoogle Scholar
  33. Dupuis, I., & Dumas, C. (1990). Influence of temperature stress on in vitro fertilization and heat shock protein synthesis in maize (Zea mays L.) reproductive tissues. Plant Physiology, 94, 665–670.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Duressa, D., Soliman, K., Taylor, R., & Senwo, Z. (2011). Proteomic analysis of soybean roots under aluminum stress. International Journal of Plant Genomics, 2011, 1–12.CrossRefGoogle Scholar
  35. Echevarría-Zomeño, S., Fernández-Calvino, L., Castro-Sanz, A. B., López, J. A., Vázquez, J., & Castellano, M. M. (2016). Dissecting the proteome dynamics of the early heat stress response leading to plant survival or death in Arabidopsis. Plant, Cell & Environment, 39, 1264–1278.CrossRefGoogle Scholar
  36. Fragkostefanakis, S., Röth, S., Schleiff, E., & Scharf, K. D. (2015). Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. Plant, Cell & Environment, 38, 1881–1895.CrossRefGoogle Scholar
  37. Giacomelli, L., Rudella, A., & van Wijk, K. J. (2006). High light response of the thylakoid proteome in Arabidopsis wild type and the ascorbate-deficient mutant vtc2-2. A comparative proteomics study. Plant Physiology, 141, 685–701.PubMedPubMedCentralCrossRefGoogle Scholar
  38. Guo, S. J., Zhou, H. Y., Zhang, X. S., Li, X. G., & Meng, Q. W. (2007). Overexpression of CaHSP26 in transgenic tobacco alleviates photoinhibition of PSII and PSI during chilling stress under low irradiance. Journal of Plant Physiology, 164, 126–136.PubMedCrossRefGoogle Scholar
  39. Guo, M., Liu, J. H., Lu, J. P., Zhai, Y. F., Wang, H., Gong, Z. H., Wang, S. B., & Lu, M. H. (2015). Genome-wide analysis of the CaHsp20 gene family in pepper: Comprehensive sequence and expression profile analysis under heat stress. Frontiers in Plant Science, 6, 806.PubMedPubMedCentralGoogle Scholar
  40. Guo, M., Liu, J. H., Ma, X., Luo, D. X., Gong, Z. H., & Lu, M. H. (2016). The plant Heat Stress Transcription Factors (HSFs): Structure, regulation, and function in response to abiotic stresses. Frontiers in Plant Science, 7, 114.PubMedPubMedCentralGoogle Scholar
  41. Gurley, W. B. (2000). HSP101: A key component for the acquisition of thermotolerance in plants. Plant Cell, 12, 457–460.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hahn, M., & Walbot, V. (1989). Effects of cold-treatment on protein synthesis and mRNA levels in rice leaves. Plant Physiology, 91, 930–938.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Hamilton, E. W., & Heckathorn, S. A. (2001). Mitochondrial adaptations to NaCl complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiology, 126, 1266–1274.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hartl, F. U. (1996). Molecular chaperones in cellular protein folding. Nature, 381, 571–580.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Helm, K. W., Lafayete, P. R., Nago, R. T., Key, J. L., & Vierling, E. (1993). Localization of small heat shock proteins to the higher plant endomembrane system. Molecular and Cellular Biology, 13, 238–247.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hlaváčková, I., Vítámvás, P., Šantrůček, J., Kosová, K., Zelenková, S., Prášil, I. T., Ovesná, J., Hynek, R., & Kodíček, M. (2013). Proteins involved in distinct phases of cold hardening process in frost resistant winter barley (Hordeum vulgare L.) cv Luxor. International Journal of Molecular Sciences, 14, 8000–8024.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Hoang, T. M. L., Moghaddam, L., Williams, B., Khanna, H., Dale, J., & Mundree, S. G. (2015). Development of salinity tolerance in rice by constitutive-overexpression of genes involved in the regulation of programmed cell death. Frontiers in Plant Science, 6, 175.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Hu, W., Hu, G., & Han, B. (2009). 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 Science, 176, 583–590.PubMedCrossRefGoogle Scholar
  49. Hu, X., Li, Y., Li, C., Yang, H., Wang, W., & Lu, M. (2010). Characterization of small heat shock proteins associated with maize tolerance to combined drought and heat stress. Journal of Plant Growth Regulation, 29, 455–464.CrossRefGoogle Scholar
  50. Huang, S., Ratliff, K. S., Schwartz, M. P., Spenner, J. M., & Matouschek, A. (1999). Mitochondrial unfold precursor proteins by unraveling them from their N-termini. Nature Structural Biology, 6, 1132–1138.PubMedCrossRefGoogle Scholar
  51. Hubert, D. A., Tornero, P., Belkhadir, Y., Krishna, P., Takahashi, A., Shirasu, K., & Dangl, J. L. (2003). Cytosolic HSP90 associates with and modulates the ARABIDOPSIS RPM1 disease resistance protein. The EMBO Journal, 22, 5679–5689.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hüther, C. M., Martinazzo, E. G., Rombaldi, C. V., & Bacarin, M. A. (2017). Effects of flooding stress in ‘Micro-Tom’ tomato plants transformed with different levels of mitochondrial sHSP23.6. Brazilian Journal of Biology, 77, 43–51.CrossRefGoogle Scholar
  53. Jackson-Constan, D., Akita, M., & Keegstra, K. (2001). Molecular chaperones involved in chloroplast protein import. Biochimica et Biophysica Acta, 1541, 102–113.PubMedCrossRefGoogle Scholar
  54. Jaiswal, D. K., Ray, D., Choudhary, M. K., Subba, P., Kumar, A., Verma, J., Kumar, R., Datta, A., Chakraborty, S., & Chakraborty, N. (2013). Comparative proteomics of dehydration response in the rice nucleus: New insights into the molecular basis of genotype-specific adaptation. Proteomics, 13, 3478–3497.PubMedCrossRefGoogle Scholar
  55. Jiang, C., Xu, J., Zhang, H., , Zhang, X., Shi, J., Li, M. and Ming, F. (2009) A cytosolic class I small heat shock protein, RcHSP17.8, of Rosa chinensis confers resistance to a variety of stresses to Escherichia coli, yeast and Arabidopsis thaliana. Plant, Cell & Environment 32, 1046–1059.CrossRefGoogle Scholar
  56. Jin, Y., Zhang, C., Yang, H., Yang, Y., Huang, C., Tian, Y., & Lu, X. (2011). Proteomic analysis of cold stress responses in tobacco seedlings. African Journal of Biotechnology, 10, 18991–19004.CrossRefGoogle Scholar
  57. Jung, Y. J., Nou, S. I., & Kang, K. K. (2014). Overexpression of Oshsp16.9 gene encoding small heat shock protein enhances tolerance to abiotic stresses in rice. Plant Breeding and Biotechnology, 2, 370–379.CrossRefGoogle Scholar
  58. Jungkunz, I., Link, K., Vogel, F., Voll, L. M., Sonnewald, S., & Sonnewald, U. (2011). AtHsp70-15-deficient Arabidopsis plants are characterized by reduced growth, a constitutive cytosolic protein response and enhanced resistance to TuMV. The Plant Journal, 66, 983–995.PubMedCrossRefGoogle Scholar
  59. Kaufman, R. J. (1999). Stress signaling from the lumen of the endoplasmic reticulum: Coordination of gene transcriptional and translational controls. Genes & Development, 13, 1211–1233.CrossRefGoogle Scholar
  60. Keeler, S., Boettger, C. M., Haynes, J. G., Kuches, K. A., Johnson, M. M., Thureen, D. L., Keeler, C. L., Jr., & Kitto, S. L. (2000). Acquired thermotolerance and expression of the HSP100/ClpB genes of Lima bean. Plant Physiology, 123, 1121–1132.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., D’Angelo, C., Bornberg-Bauer, E., Kudla, J., & Harter, K. (2007). The AtGenExpress global stress expression data set: Protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. The Plant Journal, 50, 347–363.PubMedCrossRefGoogle Scholar
  62. Kim, S. R., & An, G. (2013). Rice chloroplast-localized heat shock protein 70, OsHsp70CP1, is essential for chloroplast development under high-temperature conditions. Journal of Plant Physiology, 170, 854–863.PubMedCrossRefGoogle Scholar
  63. Kim, B. H., & Schöffl, F. (2002). Interaction between Arabidopsis heat shock transcription factor 1 and 70 kDa heat shock proteins. Journal of Experimental Botany, 53, 371–375.PubMedCrossRefGoogle Scholar
  64. Kollipara, K. P., Saab, I. N., Wych, R. D., Lauer, M. J., & Singletary, G. W. (2002). Expression profiling of reciprocal maize hybrids divergent for cold germination and desiccation tolerance. Plant Physiology, 129, 974–992.PubMedPubMedCentralCrossRefGoogle Scholar
  65. Komatsu, S., Yamamoto, A., Nakamura, T., Nouri, M. Z., Nanjo, Y., Nishizawa, K., & Furukawa, K. (2011). Comprehensive analysis of mitochondria in roots and hypocotyls of soybean under flooding stress using proteomics and metabolomics techniques. Journal of Proteome Research, 10, 3993–4004.PubMedCrossRefGoogle Scholar
  66. Komatsu, S., Makino, T., & Yasue, H. (2013). Proteomic and biochemical analyses of the cotyledon and root of flooding-stressed soybean plants. PLoS One, 8, e65301.PubMedPubMedCentralCrossRefGoogle Scholar
  67. Koo, H. J., Park, S. M., Kim, K. P., Suh, M. C., Lee, M. O., Lee, S. K., Xinli, X., & Hong, C. B. (2015). Small heat shock proteins can release light dependence of tobacco seed during germination. Plant Physiology, 167, 1030–1038.PubMedPubMedCentralCrossRefGoogle Scholar
  68. Korotaeva, N. E., Antipina, A. I., Grabelnykh, O. I., Varakina, N. N., Borovskii, G. B., & Voinikov, V. K. (2001). Mitochondrial low-molecular-weight heat-shock proteins and the tolerance of cereal mitochondria to hyperthermia. Russian Journal of Plant Physiology, 48, 798–803.CrossRefGoogle Scholar
  69. Kosová, K., Vítámvás, P., Planchon, S., Renaut, J., Vanková, R., & Prášil, I. T. (2013). Proteome analysis of cold response in spring and winter wheat (Triticum aestivum) crowns reveals similarities in stress adaptation and differences in regulatory processes between the growth habits. Journal of Proteome Research, 12, 4830–4845.PubMedCrossRefGoogle Scholar
  70. Kotak, S., Larkindale, J., Lee, U., von Koskull-Doring, P., Vierling, E., & Scharf, K. D. (2007). Complexity of the heat stress response in plants. Current Opinion in Plant Biology, 10, 310–316.PubMedCrossRefGoogle Scholar
  71. Krishna, P., & Gloor, G. (2001). The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress & Chaperones, 6, 238–246.CrossRefGoogle Scholar
  72. Kropat, J., Oster, U., Rüdiger, W., & Beck, C. F. (1997). Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proceedings of the National Academy of Sciences, 94, 14168–14172.CrossRefGoogle Scholar
  73. Kumar, M., Padula, M. P., Davey, P., Pernice, M., Jiang, Z., Sablok, G., Contreras-Porcia, L., & Ralph, P. J. (2017a). Proteome analysis reveals extensive light stress-response reprogramming in the seagrass Zostera muelleri (Alismatales, Zosteraceae) metabolism. Frontiers in Plant Science, 17, 2023.Google Scholar
  74. Kumar, N., Suyal, D. C., Sharma, I. P., Verma, A., & Singh, H. (2017b). Elucidating stress proteins in rice (Oryza sativa L.) genotype under elevated temperature: A proteomic approach to understand heat stress response. 3 Biotech, 7, 205.PubMedCrossRefPubMedCentralGoogle Scholar
  75. Larkindale, J., Mishkind, M., & Vierling, E. (2005). Plant responses to high temperature. In M. A. Jenks & P. M. Hasegawa (Eds.), Plant Abiotic Stress (pp. 100–144). Oxford: Blackwell Publishing Ltd.CrossRefGoogle Scholar
  76. Lee, J., & Ahn, Y.-J. (2013). Heterologous expression of a carrot small heat shock protein increased Escherichia coli viability under lead and arsenic stresses. Hortscience, 48, 1323–1326.Google Scholar
  77. Lee, U., Rioflorido, I., Hong, S.-W., Larkindale, J., Waters, E. R., & Vierling, E. (2007). The Arabidopsis ClpB/Hsp100 family of proteins: Chaperones for stress and chloroplast development. The Plant Journal, 49, 115–127.PubMedCrossRefGoogle Scholar
  78. Lee, D. G., Ahsan, N., Lee, S. H., Lee, J. J., Bahk, J. D., Kang, K. Y., & Lee, B. H. (2009). Chilling stress-induces proteomic changes in rice roots. Journal of Plant Physiology, 166, 1–11.PubMedCrossRefGoogle Scholar
  79. Lehesranta, S. J., Davies, H. V., Shepherd, L. V. T., Koistinen, K. M., Massat, N., Nunan, N., McNicol, J. W., & Kärenlampi, S. O. (2006). Proteomic analysis of the potato tuber life cycle. Proteomics, 6, 6042–6052.PubMedCrossRefGoogle Scholar
  80. Li, W., Wei, Z., Qiao, Z., Wu, Z., Cheng, L., & Wang, Y. (2013). Proteomics analysis of alfalfa response to heat stress. PLoS One, 8, e82725.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Liao, J. L., Zhou, H. W., Zhang, H. Y., Zhong, P. A., & Huang, Y. J. (2014). Comparative proteomic analysis of differentially expressed proteins in the early milky stage of rice grains during high temperature stress. Journal of Experimental Botany, 65, 655–671.PubMedCrossRefGoogle Scholar
  82. Lim, C. J., Yang, K. A., Hong, J. K., Choi, J. S., Yun, D. J., Hong, J. C., Chung, W. S., Lee, S. Y., Cho, M. J., & Lim, C. O. (2006). Gene expression profiles during heat acclimation in Arabidopsis thaliana suspension-culture cells. Journal of Plant Research, 119, 373–383.PubMedCrossRefGoogle Scholar
  83. Lin, S. K., Chang, M. C., Tsai, Y. G., & Lur, H. S. (2005). Proteomic analysis of the expression of proteins related to rice quality during caryopsis development and the effect of high temperature on expression. Proteomics, 5, 2140–2156.PubMedCrossRefGoogle Scholar
  84. Lin, C. J., Li, C. Y., Lin, S. K., Yang, F. H., Huang, J. J., Liu, Y. H., & Lur, H. S. (2010). Influence of high temperature during grain filling on the accumulation of storage proteins and grain quality in Rice (Oryza sativa L.) Journal of Agricultural and Food Chemistry, 58, 10545–10552.PubMedCrossRefGoogle Scholar
  85. Liu, Y., Burch-Smith, T., Schiff, M., Feng, S., & Dinesh-Kumar, S. P. (2004). Molecular chaperone hsp90 associates with resistance protein n and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. The Journal of Biological Chemistry, 279, 2101–2108.PubMedCrossRefGoogle Scholar
  86. Lopes-Caitar, V. S., de Carvalho, M. C. C. G., Darben, L. M., Kuwahara, M. K., Nepomuceno, A. L., Dias, W. P., Abdelnoor, R. V., & Marcelino-Guimarães, F. C. (2013). Genome-wide analysis of the Hsp20 gene family in soybean: Comprehensive sequence, genomic organization and expression profile analysis under abiotic and biotic stresses. BMC Genomics, 14, 577.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Low, D., Brandle, K., Nover, L., & Forreiter, C. (2000). Cytosolic heat stress proteins Hsp17.7 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo. Planta, 211, 575–582.PubMedCrossRefGoogle Scholar
  88. Lubben, T. H., Donaldson, G. K., Viitanen, P. V., & Gatenby, A. A. (1989). Severa1 proteins imported into chloroplasts form stable complexes with the GroEL-related chloroplast molecular chaperone. Plant Cell, 1, 1223–1230.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Maimbo, M., Ohnishi, K., Hikichi, Y., Yoshioka, H., & Kiba, A. (2007). Induction of a small heat shock protein and its functional roles in nicotiana plants in the defense response against Ralstonia solanacearum. Plant Physiology, 145, 1588–1599.PubMedPubMedCentralCrossRefGoogle Scholar
  90. Majoul, T., Bancel, E., Triboï, E., Ben Hamida, J., & Branlard, G. (2004). Proteomic analysis of the effect of heat stress on hexaploid wheat grain: Characterization of heat-responsive proteins from non-prolamins fraction. Proteomics, 4, 505–513.PubMedCrossRefGoogle Scholar
  91. Malik, M. K., Slovin, J. P., Hwang, C. H., & Zimmerman, J. L. (1999). Modified expression of a carrot small heat shock protein gene, Hsp17.7, results in increased or decreased thermotolerance. The Plant Journal, 20, 89–99.PubMedCrossRefGoogle Scholar
  92. Manaa, A., Ben Ahmed, H., Valot, B., Bouchet, J. P., Aschi-Smiti, S., Causse, M., & Faurobert, M. (2011). Salt and genotype impact on plant physiology and root proteome variations in tomato. Journal of Experimental Botany, 62, 2797–2813.PubMedCrossRefGoogle Scholar
  93. Merret, R., Carpentier, M. C., Favory, J. J., Picart, C., Descombin, J., Bousquet-Antonelli, C., Tillard, P., Lejay, L., Deragon, J. M., & Charng, Y. Y. (2017). Heat shock protein HSP101 affects the release of ribosomal protein mRNAs for recovery after heat shock. Plant Physiology, 174, 1216–1225.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Mertz-Henning, L. M., Pegoraro, C., Maia, L. C., Venske, E., Rombaldi, C. V., & Costa de Oliveira, A. (2016). Expression profile of rice Hsp genes under anoxic stress. Genetics and Molecular Research, 15(2.) gmr.15027954.Google Scholar
  95. Mishra, R. C., Richa, M. R. C., & Grover, A. (2016). Constitutive over-expression of rice ClpD1 protein enhances tolerance to salt and desiccation stresses in transgenic Arabidopsis plants. Plant Science, 250, 69–78.PubMedCrossRefGoogle Scholar
  96. Mishra, D., Shekhar, S., Agrawal, L., Chakraborty, S., & Chakraborty, N. (2017). Cultivar-specific high temperature stress responses in bread wheat (Triticum aestivum L.) associated with physicochemical traits and defense pathways. Food Chemistry, 221, 1077–1087.PubMedCrossRefGoogle Scholar
  97. Mittler, R. (2006). Abiotic stress, the field environment and stress combination. Trends in Plant Science, 11, 15–19.PubMedCrossRefGoogle Scholar
  98. Mu, C., Zhang, S., Yu, G., Chen, N., Li, X., & Liu, H. (2013). Overexpression of small heat shock protein LimHSP16.45 in Arabidopsis enhances tolerance to abiotic stresses. PLoS One, 8, e82264.PubMedPubMedCentralCrossRefGoogle Scholar
  99. Murakami, T., Matsuba, S., Funatsuki, H., Kawaguchi, K., Saruyama, H., Tanida, M., & Sato, Y. (2004). Over-expression of a small heat shock protein, sHSP17.7, confers both heat tolerance and UV-B resistance to rice plants. Molecular Breeding, 13, 165–175.CrossRefGoogle Scholar
  100. Muthusamy, S. K., Dalal, M., Chinnusamy, V., & Bansal, K. C. (2016). Differential regulation of genes coding for organelle and cytosolic Clp ATPases under biotic and abiotic stresses in wheat. Frontiers in Plant Science, 7, 929.PubMedPubMedCentralGoogle Scholar
  101. Muthusamy, S. K., Dalala, M., Chinnusamy, V., & Bansal, K. C. (2017). Genome-wide identification and analysis of biotic and abiotic stress regulation of small heat shock protein (HSP20) family genes in bread wheat. Journal of Plant Physiology, 211, 100–113.PubMedCrossRefGoogle Scholar
  102. Nakamoto, H., & Vigh, L. (2007). The small heat shock proteins and their clients. Cellular and Molecular Life Sciences, 64, 294–306.PubMedCrossRefGoogle Scholar
  103. Navascués, J., Pérez-Rontomé, C., Sánchez, D. H., Staudinger, C., Wienkoop, S., Rellán-Álvarez, R., & Becana, M. (2012). Oxidative stress is a consequence, not a cause, of aluminum toxicity in the forage legume Lotus corniculatus. The New Phytologist, 193, 625–636.PubMedCrossRefGoogle Scholar
  104. Neumann, D., Lichtenberger, O., Günther, D., Tschiersch, K., & Nover, L. (1994). Heat-shock proteins induce heavy-metal tolerance in higher plants. Planta, 194, 360–370.CrossRefGoogle Scholar
  105. Nieto-Sotelo, J., Martínez, L. M., Ponce, G., Cassab, G. I., Alagón, A., Meeley, R. B., Ribau, J. M., & Yang, R. (2002). Maize HSP101 plays important roles in both induced and basal Thermotolerance and primary root growth. Plant Cell, 14, 1621–1633.PubMedPubMedCentralCrossRefGoogle Scholar
  106. Nishizawa-Yokoi, A., Tainaka, H., Yoshida, E., Tamoi, M., Yabuta, Y., & Shigeoka, S. (2010). The 26S proteasome function and Hsp90 activity involved in the regulation of HsfA2 expression in response to oxidative stress. Plant & Cell Physiology, 51, 486–496.CrossRefGoogle Scholar
  107. Ogawa, I., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2009). Time course analysis of gene regulation under cadmium stress in rice. Plant and Soil, 325, 97.CrossRefGoogle Scholar
  108. Ono, K., Hibino, T., Kohinata, T., Suzuki, S., Tanaka, Y., Nakamura, T., Takabe, T., & Takabe, T. (2001). Overexpression of DnaK from a halotolerant cyanobacterium Aphanothece halophytica enhances the high-temperature tolerance of tobacco during germination and early growth. Plant Science, 160, 455–461.PubMedCrossRefGoogle Scholar
  109. Pandey, A., Chakraborty, S., Datta, A., & Chakraborty, N. (2008). Proteomics approach to identify dehydration responsive nuclear proteins from chickpea (Cicer arietinum L.) Molecular & Cellular Proteomics, 7, 88–107.CrossRefGoogle Scholar
  110. Pandey, A., Rajamani, U., Verma, J., Subba, P., Chakraborty, N., Data, A., Chakraborty, S., & Chakraborty, N. (2010). Identification of extracellular matrix proteins of rice (Oryza sativa L.) involved in dehydration-responsive network: A proteomic approach. Journal of Proteome Research, 9, 3443–3464.PubMedCrossRefGoogle Scholar
  111. Pareek, A., Singla, S. L., & Grover, A. (1998). Plant Hsp90 family with special reference to rice. Journal of Biosciences, 23, 361–367.CrossRefGoogle Scholar
  112. Parsell, P. A., & Lindquist, S. (1993). The function of heat-shock proteins in stress tolerance: Degradation and reactivation of damaged proteins. Annual Review of Genetics, 27, 437–496.PubMedCrossRefGoogle Scholar
  113. Pi, E., Qu, L., Hu, J., Huang, Y., Qiu, L., Jiang, B., Liu, C., Peng, T., Zhao, Y., Wang, H., Tsai, S. T., Ngai, S., & Du, L. (2016). Mechanisms of soybean roots tolerances to salinity revealed by proteomic and phosphoproteomic comparisons between two cultivars. Molecular & Cellular Proteomics, 15, 266–288.CrossRefGoogle Scholar
  114. Prasad, B. D., Goel, S., & Krishna, P. (2010). In Silico identification of carboxylate clamp type tetratricopeptide repeat proteins in Arabidopsis and Rice as putative co-chaperones of Hsp90/Hsp70. PLoS One, 5, e12761.PubMedPubMedCentralCrossRefGoogle Scholar
  115. Pratt, W. B., & Toft, D. O. (2003). Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Experimental Biology and Medicine, 228, 111–133.PubMedCrossRefGoogle Scholar
  116. Pratt, W. B., Galigniana, M. D., Harrell, J. M., & Deranco, D. B. (2004). Role of hsp90 and the hsp90-binding immunophilins in signaling protein movement. Cellular Signalling, 16, 857–872.PubMedCrossRefGoogle Scholar
  117. Pyatrikas, D. V., Rikhvanov, E. G., Fedoseeva, I. V., Varakina, N. N., Rusaleva, T. M., Tauson, E. L., Stepanov, A. V., Borovskii, G. B., & Voinikov, V. K. (2014). Mitochondrial retrograde regulation of HSP101 expression in Arabidopsis thaliana under heat stress and amiodarone action. Russian Journal of Plant Physiology, 61, 80–89.CrossRefGoogle Scholar
  118. Qi, Y., Wang, H., Zou, Y., Liu, C., Wang, Y., & Zhang, W. (2011). Over-expression of mitochondrial heat shock protein 70 suppresses programmed cell death in rice. FEBS Letters, 585, 231–239.PubMedCrossRefGoogle Scholar
  119. Queitsch, C., Hong, S. W., Vierling, E., & Lindquist, S. (2000). Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell, 12, 479–492.PubMedPubMedCentralCrossRefGoogle Scholar
  120. Reddy, R., Chaudhary, S., Patil, P., & Krishna, P. (1998). The 90 kDa heat shock protein (Hsp90) is expressed throughout Brassica napus seed development and germination. Plant Science, 131, 131–137.CrossRefGoogle Scholar
  121. Reddy, P. S., Kavi Kishor, P. B., Seiler, C., Kuhlmann, M., Eschen-Lippold, L., Lee, J., Reddy, M. K., & Sreenivasulu, N. (2014). Unraveling regulation of the small heat shock proteins by the heat shock factor HvHsfB2c in barley: Its implications in drought stress response and seed development. PLoS One, 9, e89125.PubMedPubMedCentralCrossRefGoogle Scholar
  122. Rensink, W. A., Lobst, S., Hart, A., Stegalkina, S., Liu, J., & Buell, C. R. (2005). Gene expression profiling of potato responses to cold, heat, and salt stress. Functional & Integrative Genomics, 5, 201–207.CrossRefGoogle Scholar
  123. Rinalducci, S., Egidi, M. G., Mahfoozi, S., Godehkahriz, S. J., & Zolla, L. (2011). The influence of temperature on plant development in a vernalization-requiring winter wheat: A 2-DE based proteomic investigation. Journal of Proteomics, 74, 643–659.PubMedCrossRefGoogle Scholar
  124. Ristic, Z., Gifford, D. J., & Cass, D. D. (1991). Heat shock proteins in two lines of Zea mays L. that differ in drought and heat resistance. Plant Physiology, 97, 1430–1434.PubMedPubMedCentralCrossRefGoogle Scholar
  125. Rizhsky, L., Liang, H., & Mittler, R. (2002). The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiology, 130, 1143–1151.PubMedPubMedCentralCrossRefGoogle Scholar
  126. Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S., & Mittler, R. (2004). When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology, 134, 1683–1696.PubMedPubMedCentralCrossRefGoogle Scholar
  127. Rollins, J. A., Habte, E., Templer, S. E., Colby, T., Schmidt, J. and von Korff M. (2013) Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). Journal of Experimental Botany 64, 3201–3212.PubMedPubMedCentralCrossRefGoogle Scholar
  128. Rossel, J. B., Wilson, I. W., & Pogson, B. J. (2002). Global changes in gene expression in response to high light in Arabidopsis. Plant Physiology, 130, 1109–1120.PubMedPubMedCentralCrossRefGoogle Scholar
  129. Rozenzvieg, D., Elmaci, C., Samach, A., Lurie, S., & Porat, R. (2004). Isolation of four heat shock protein cDNAs from grapefruit peel tissue and characterization of their expression in response to heat and chilling temperature stresses. Physiologia Plantarum, 121, 421–428.CrossRefGoogle Scholar
  130. Ruibal, C., Castro, A., Carballo, V., Szabados, L., & Vidal, S. (2013). Recovery from heat, salt and osmotic stress in Physcomitrella patens requires a functional small heat shock protein PpHsp16.4. BMC Plant Biology, 13, 174.PubMedPubMedCentralCrossRefGoogle Scholar
  131. Sabehat, A., Lurie, S., & Weiss, D. (1998). Expression of small heat-shock proteins at low temperatures: A possible role in protecting against chilling injuries. Plant Physiology, 117, 651–658.PubMedPubMedCentralCrossRefGoogle Scholar
  132. Sanchez-Bel, P., Egea, I., Sanchez-Ballesta, M. T., Sevillano, L., del Carmen Bolarin, M., & Flores, F. B. (2012). Proteome changes in tomato fruits prior to visible symptoms of chilling injury are linked to defensive mechanisms, uncoupling of photosynthetic processes and protein degradation machinery. Plant & Cell Physiology, 53, 470–484.CrossRefGoogle Scholar
  133. Sarkar, N. K., Kim, Y. K., & Grover, A. (2009). Rice sHsp genes: Genomic organization and expression profiling under stress and development. BMC Genomics, 10, 393.PubMedPubMedCentralCrossRefGoogle Scholar
  134. Sarry, J. E., Kuhn, L., Ducruix, C., Lafaye, A., Junot, C., Hugouvieux, V., Jourdain, A., Bastien, O., Fievet, J. B., Vailhen, D., Amekraz, B., Moulin, C., Ezan, E., Garin, J., & Bourguignon, J. (2006). The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics, 6, 2180–2198.PubMedCrossRefGoogle Scholar
  135. Sato, Y., & Yokoya, S. (2008). Enhanced tolerance to drought stress in transgenic rice plants overexpressing a small heat-shock protein, sHSP17.7. Plant Cell Reports, 27, 329–334.PubMedCrossRefGoogle Scholar
  136. Scarpeci, T. E., Zanor, M. I., & Valle, E. M. (2008). Investigating the role of plant heat shock proteins during oxidative stress. Plant Signaling & Behavior, 3, 856–857.CrossRefGoogle Scholar
  137. Schöffl, F., Prändl, R., & Reindl, A. (1999). Molecular responses to heat stress. In Molecular responses to cold, drought, heat and salt stress in higher plants (Vol. 1). Texas: Biotechnology intelligence unit.Google Scholar
  138. Schroda, M., Vallon, V., Wlollman, F., & Beck, C. F. (1999). A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of photosystem II during and after photoinhibition. Plant Cell, 11, 11165–11178.CrossRefGoogle Scholar
  139. Shekhar, S., Mishra, D., Gayali, S., Buragohain, A. K., Chakraborty, S., & Chakraborty, N. (2016). Comparison of proteomic and metabolomic profiles of two contrasting ecotypes of sweetpotato (Ipomoea batata L.) Journal of Proteomics, 143, 306–317.PubMedCrossRefGoogle Scholar
  140. Siddique, M., Gernhard, S., von Koskull-Döring P, ., Vierling, E. and Scharf, K. D. (2008) The plant sHSP superfamily: Five new members in Arabidopsis thaliana with unexpected properties. Cell Stress & Chaperones 13, 183–197.CrossRefGoogle Scholar
  141. Singh, A., Singh, U., Mittal, D., & Grover, A. (2010). Genome-wide analysis of rice ClpB/HSP100, ClpC and ClpD genes. BMC Genomics, 11, 95.PubMedPubMedCentralCrossRefGoogle Scholar
  142. Singh, R. K., Jaishankar, J., Muthamilarasan, M., Shweta, S., Dangi, A., & Prasad, M. (2016). Genome-wide analysis of heat shock proteins in C4 model, foxtail millet identifies potential candidates for crop improvement under abiotic stress. Scientific Reports, 6, 32641.PubMedPubMedCentralCrossRefGoogle Scholar
  143. Singla, S. L., Pareek, A., & Grover, A. (1997). Yeast HSP104 homologue rice HSP110 is developmentally- and stress-regulated. Plant Science, 125, 211–219.CrossRefGoogle Scholar
  144. Singla, S. L., Pareek, A., & Grover, A. (1998). Plant Hsp100 family with special reference to rice. Journal of Biosciences, 23, 337–345.CrossRefGoogle Scholar
  145. Soll, J. (2002). Protein import into chloroplasts. Current Opinion in Plant Biology, 5, 529–535.PubMedCrossRefGoogle Scholar
  146. Song, H., Fan, P., & Li, Y. (2009a). Overexpression of organellar and cytosolic AtHSP90 in Arabidopsis thaliana impairs plant tolerance to oxidative stress. Plant Molecular Biology Reporter, 27, 342–349.CrossRefGoogle Scholar
  147. Song, H., Zhao, R., Fan, P., Wang, X., Chen, X., & Li, Y. (2009b). Overexpression of AtHsp90.2, AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses. Planta, 229, 955–964.PubMedCrossRefGoogle Scholar
  148. Song, H. M., Wang, H. Z., & Xu, X. B. (2012). Overexpression of AtHsp90.3 in Arabidopsis thaliana impairs plant tolerance to heavy metal stress. Biologia Plantarum, 56, 197–199.CrossRefGoogle Scholar
  149. Soto, A., Allona, I., Collada, C., Guevara, M., Casado, R., Emilio, R., Aragoncillo, C., & Gomez, L. (1999). Heterologous expression of a plant small heat-shock protein enhances Escherichia coli viability under heat and cold stress. Plant Physiology, 120, 521–528.PubMedPubMedCentralCrossRefGoogle Scholar
  150. Su, P. H., & Li, H. M. (2008). Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiology, 146, 1231–1241.PubMedPubMedCentralCrossRefGoogle Scholar
  151. Subba, P., Barua, P., Kumar, R., Data, A., Soni, K. K., Chakraborty, S., & Chakraborty, N. (2013a). Phosphoproteomic dynamics of chickpea (Cicer arietinum L.) reveals shared and distinct components of dehydration response. Journal of Proteome Research, 12, 5025–5047.PubMedCrossRefGoogle Scholar
  152. Subba, P., Kumar, R., Gayali, S., Shekhar, S., Parveen, S., Pandey, A., Data, A., Chakraborty, S., & Chakraborty, N. (2013b). Characterisation of the nuclear proteome of a dehydration-sensitive cultivar of chickpea and comparative proteomic analysis with a tolerant cultivar. Proteomics, 13, 1973–1992.PubMedCrossRefGoogle Scholar
  153. Sugino, M., Hibino, T., Tanaka, Y., Nii, N., & Takabe, T. (1999). Overexpression of DnaK from a halotolerant cyanobacterium Aphanothece halophytic acquires resistance to salt stress in transgenic tobacco plants. Plant Science, 146, 81–88.CrossRefGoogle Scholar
  154. Süle, A., Vanrobaeys, F., Hajós, G., Van Beeumen, J., & Devreese, B. (2004). Proteomic analysis of small heat shock protein isoforms in barley shoots. Phytochemistry, 65, 1853–1863.PubMedCrossRefGoogle Scholar
  155. Sun, W., Bernard, C., Van de Cotte, B., Van Montagu, M., & Verbruggen, N. (2001). At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. The Plant Journal, 27, 407–415.PubMedPubMedCentralCrossRefGoogle Scholar
  156. Sun, J. H., Chen, J. Y., Kuang, J., Chen, W., & Lu, W. (2010). Expression of sHSP genes as affected by heat shock and cold acclimation in relation to chilling tolerance in plum fruit. Postharvest Biology and Technology, 55, 91–96.CrossRefGoogle Scholar
  157. Sung, D. Y., Vierling, E., & Guy, C. L. (2001). Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiology, 126, 789–800.PubMedPubMedCentralCrossRefGoogle Scholar
  158. Swindell, W. R., Huebner, M., & Weber, A. P. (2007). Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics, 8, 125.PubMedPubMedCentralCrossRefGoogle Scholar
  159. Talamè, V., Ozturk, N. Z., Bohnert, H. J., & Tuberosa, R. (2007). Barley transcript profiles under dehydration shock and drought stress treatments: A comparative analysis. Journal of Experimental Botany, 58, 229–240.PubMedCrossRefGoogle Scholar
  160. Thao, N. P., Chen, L., Nakashima, A., Hara, S., Umemura, K., Takahashi, A., Shirasu, K., Kawasaki, T., & Shimamoto, K. (2007). RAR1 and HSP90 form a complex with Rac/Rop GTPase and function2 in innate-immune responses in rice. Plant Cell, 19, 4035–4045.PubMedPubMedCentralCrossRefGoogle Scholar
  161. Vierling, E. (1991). The roles of heat shock proteins in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 42, 579–620.CrossRefGoogle Scholar
  162. Vinocur, B., & Altman, A. (2005). Recent advances in engineering plant tolerance to abiotic stress: Achievements and limitations. Current Opinion in Biotechnology, 16, 123–132.PubMedCrossRefGoogle Scholar
  163. Vítámvás, P., Prášil, I. T., Kosová, K., Planchon, S., & Renaut, J. (2012). Analysis of proteome and frost tolerance in chromosome 5A and 5B reciprocal substitution lines between two winter wheats during long-term cold acclimation. Proteomics, 12, 68–85.PubMedCrossRefGoogle Scholar
  164. Wang, W., Vinocur, B., Shoseyov, O., & Altman, A. (2004). Role of plant heatshock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science, 9, 244–252.PubMedPubMedCentralCrossRefGoogle Scholar
  165. Wang, A., Yu, X., Mao, Y., Liu, Y., Liu, G., Liu, Y., & Niu, X. (2015). Overexpression of a small heat-shock-protein gene enhances tolerance to abiotic stresses in rice. Plant Breeding, 134, 384–393.CrossRefGoogle Scholar
  166. Wang, J., Yu, Q., Xiong, H., Wang, J., Chen, S., Yang, Z., & Dai, S. (2016). Proteomic insight into the response of Arabidopsis chloroplasts to darkness. PLoS One, 11, e0154235.PubMedPubMedCentralCrossRefGoogle Scholar
  167. Wang, M., Zou, Z., Li, Q., Sun, K., Chen, X., & Li, X. (2017). The CsHSP17.2 molecular chaperone is essential for thermotolerance in Camellia Sinensis. Scientific Reports, 7(1237).Google Scholar
  168. Waters, E. R. (2013). The evolution, function, structure, and expression of the plant sHSPs. Journal of Experimental Botany, 64, 391–403.PubMedCrossRefGoogle Scholar
  169. Waters, E. R., Lee, G. J., & Vierling, E. (1996). Evolution, structure and function of the small heat shock proteins in plants. Journal of Experimental Botany, 47, 325–338.CrossRefGoogle Scholar
  170. Waters, E. R., Lee, G. J., & Vierling, E. (2013). Evolution, structure and function of the small heat shock proteins in plants. Journal of Experimental Botany, 47, 325–338.CrossRefGoogle Scholar
  171. Xu, C., & Huang, B. (2010). Comparative analysis of drought responsive proteins in kentucky bluegrass cultivars contrasting in drought tolerance. Crop Science, 50, 2543–2552.CrossRefGoogle Scholar
  172. Xu, X. B., Song, H. M., Zhou, Z. H., Shi, N. N., Ying, Q. C., & Wang, H. Z. (2010). Functional characterization of AtHsp90.3 in Saccharomyces cerevisiae and Arabidopsis thaliana under heat stress. Biotechnology Letters, 32, 979–987.PubMedCrossRefGoogle Scholar
  173. Xu, Y., Zhan, C., & Huang, B. (2011). Heat shock proteins in association with heat tolerance in grasses. International Journal of Proteomics, 2011(529648).CrossRefGoogle Scholar
  174. Xu, J., Xue, C., Xue, D., Zhao, J., Gai, J., Guo, N., & Xing, H. (2013). Overexpression of GmHsp90s, a heat shock protein 90 (Hsp90) gene family cloning from soybean, decrease damage of abiotic stresses in Arabidopsis thaliana. PLoS One, 8, e69810.PubMedPubMedCentralCrossRefGoogle Scholar
  175. Yamada, K., Fukao, Y., Hayashi, M., Fukazawa, M., Suzuki, I., & Nishimura, M. (2007). Cytosolic HSP90 regulates the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana. The Journal of Biological Chemistry, 282, 37794–37804.PubMedPubMedCentralCrossRefGoogle Scholar
  176. Yang, Y., Li, X., Yang, S., Zhou, Y., Dong, C., Ren, J., Sun, X., & Yang, Y. (2015). Comparative physiological and proteomic analysis reveals the leaf response to cadmium-induced stress in poplar (Populus yunnanensis). PLoS One, 10, e0137396.PubMedPubMedCentralCrossRefGoogle Scholar
  177. Young, T. E., Ling, J., Geisler-Lee, C. J., Tanguay, R. L., Caldwell, C., & Gallie, D. R. (2001). Developmental and thermal regulation of the maize heat shock protein, HSP101. Plant Physiology, 127, 777–791.PubMedPubMedCentralCrossRefGoogle Scholar
  178. Young, L. W., Wilen, R. W., & Bonham-Smith, P. C. (2004). High temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production. Journal of Experimental Botany, 55, 485–495.PubMedCrossRefGoogle Scholar
  179. Yu, A., Li, P., Tang, T., Wang, J., Chen, Y., & Liu, L. (2015). Roles of Hsp70s in stress responses of microorganisms, plants, and animals. BioMed Research International, 2015, 1–8.Google Scholar
  180. Yu, J., Cheng, Y., Feng, K., Ruan, M., Ye, Q., Wang, R., Li, Z., Zhou, G., Yao, Z., Yang, Y., & Wan, H. (2016). Genome-wide identification and expression profiling of tomato Hsp20 gene family in response to biotic and abiotic stresses. Frontiers in Plant Science, 7, 1215.PubMedPubMedCentralGoogle Scholar
  181. Zhang, L., Yu, Z., Jiang, L., Jiang, J., Luo, H., & Fu, L. (2011). Effect of post-harvest heat treatment on proteome change of peach fruit during ripening. Journal of Proteomics, 74, 1135–1149.PubMedCrossRefGoogle Scholar
  182. Zhang, Y., Xu, L., Zhu, X., Gong, Y., Xiang, F., Sun, X., & Liu, L. (2013). Proteomic analysis of heat stress response in leaves of radish (Raphanus sativus L.) Plant Molecular Biology Reporter, 31, 195–203.CrossRefGoogle Scholar
  183. Zhang, L., Zhang, Q., Gao, Y., Pan, H., Shi, S., & Wang, Y. (2014a). Overexpression of heat shock protein gene PfHSP21.4 in Arabidopsis thaliana enhances heat tolerance. Acta Physiologiae Plantarum, 36, 1555–1564.CrossRefGoogle Scholar
  184. Zhang, Y., Sun, M., & Zhang, Q. (2014b). Proteomic analysis of the heat stress response in leaves of two contrasting chrysanthemum varieties. Plant OMICS, 7, 229–232.Google Scholar
  185. Zhang, Y., Pan, J., Huang, X., Guo, D., Lou, H., Hou, Z., Su, M., Liang, R., Xie, C., Mingshan You, M., & Li, B. (2017). Differential effects of a post-anthesis heat stress on wheat (Triticum aestivum L.) grain proteome determined by iTRAQ. Scientific Reports, 7, 3468.PubMedPubMedCentralCrossRefGoogle Scholar
  186. Zou, J., Liu, C., Liu, A., Zou, D., & Chen, X. (2012). Overexpression of OsHsp17.0 and OsHsp23.7 enhances drought and salt tolerance in rice. Journal of Plant Physiology, 169, 628–635.PubMedCrossRefGoogle Scholar
  187. Zhou, Y., Chen, H., Chu, P., Li, Y., Tan, B., Ding, Y., Tsang, E. W. T., Jiang, L., Wu, K., & Huang, S. (2012). NnHSP17.5, a cytosolic class II small heat shock protein gene from Nelumbo nucifera, contributes to seed germination vigor and seedling thermotolerance in transgenic Arabidopsis. Plant Cell Reports, 31, 379–389.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Divya Mishra
    • 1
  • Shubhendu Shekhar
    • 1
  • Deepika Singh
    • 1
  • Subhra Chakraborty
    • 1
  • Niranjan Chakraborty
    • 1
  1. 1.National Institute of Plant Genome Research, Jawaharlal Nehru University CampusNew DelhiIndia

Personalised recommendations