Skip to main content
Log in

Genetic improvement of rice crop under high temperature stress: bridging plant physiology with molecular biology

  • Review Article
  • Published:
Indian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Rice crop meets the calorific needs of the masses. High temperature stress has negative effects on the physiology and biochemistry of this crop. This is amply reflected from studies showing that heat stress has strong detrimental effects on photosynthetic efficiency, electrolyte leakage, lipid peroxidation, enzyme (superoxide dismutase, peroxidase, catalase, etc.) activities and transpiration rate at varied growth stages, ultimately affecting the total harvest of this crop. The macro cellular- and plant-level changes as of aboveare rooted inalterations at the molecular level, affecting the gene expression profiles, protein abundance and their interaction at the genomic level. With global warming at its pace, the cultivation of rice under field conditions is greatly threatened. Molecular analyses show that the response of rice to heat stress involves a host of genes including transcription factors, genes involved in calcium and hormonal signalling, reactive oxygen species metabolism genes and chaperones. Heat shock proteins (Hsps) are considered the key players with role in maintaining proteostasis under heat and related stresses. The expression of Hsps is centrally governed by heat shock factors (Hsfs). Hsps and Hsfs have emerged as the potential candidates for engineering stress tolerance in crop plants. Several attempts have been made in which rice genes have been incorporated in varied hosts and concurrently rice has been used as trans-host with various genes cloned from rice and other plant species. In this review, we provide an account of physiological, biochemical, transcriptomic and proteomic responses of rice crop to heat stress. The importance of ClpB-C/Hsp100 gene in heat stress tolerance and the potential heat shock factor(s) governing regulation of ClpB-C/Hsp100 for engineering heat stress tolerance in rice has been discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Agarwal, M., Katiyar-Agarwal, S., Sahi, C., Gallie, D. R., & Grover, A. (2001). Arabidopsis thaliana Hsp100 protein: Kith and kin. Cell Stress and Chaperones, 6(3), 219–224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agarwal, M., Sahi, C., Katiyar-Agarwal, S., et al. (2003). Rice Hsp100 protein complements yeast hsp104 mutation by promoting disaggregation of protein granules and shows differential expression in indica and japonica rice types. Plant Molecular Biology, 51(4), 543–553.

    Article  CAS  PubMed  Google Scholar 

  • Åkerfelt, M., Morimoto, R. I., & Sistonen, L. (2010). Heat shock factors: integrators of cell stress, development and lifespan. Nature Reviews Molecular Cell Biology, 11(8), 545–555.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Akman, Z. (2009). Comparison of high temperature tolerance in maize, rice and sorghum seeds by plant growth regulators. Journal of Animal and Veterinary Advances, 8(2), 358–361.

    CAS  Google Scholar 

  • Ali, M. K., Azhar, A., & Galani, S. (2013). Response of rice (Oryza sativa L.) under elevated temperature at early growth stage: Physiological markers. Russian Journal of Agricultural and Socio-Economic Sciences, 20(8), 11–19.

    Google Scholar 

  • Almoguera, C., Rojas, A., Díaz-Martín, J., Prieto-Dapena, P., Carranco, R., & Jordano, J. (2002). A seed-specific heat-shock transcription factor involved in developmental regulation during embryogenesis in sunflower. The Journalof Biological Chemistry, 277(46), 43866–43872.

    Article  CAS  Google Scholar 

  • Baldoni, E., Genga, A., & Cominelli, E. (2015). Plant MYB transcription factors: Their role in drought response mechanisms. International Journal of Molecular Sciences, 16(7), 15811–15851.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boscheinen, O., Lyck, R., Queitsch, C., Treuter, E., Zimarino, V., & Scharf, K. D. (1997). Heat stress transcription factors from tomato can functionally replace HSF1 in the yeast Saccharomyces cerevisiae. Molecular Genetics and Genomics, 255(3), 322–331.

    Article  CAS  Google Scholar 

  • Burke, J. J., & Chen, J. (2015). Enhancement of reproductive heat tolerance in plants. PLoS ONE, 10(4), e0122933.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Century, K., Reuber, T. L., & Ratcliffe, O. J. (2008). Regulating the regulators: The future prospects for transcription-factor-based agricultural biotechnology products. Plant Physiology, 147(1), 20–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang, C. C., Huang, P. S., Lin, H. R., & Lu, C. H. (2007). Transactivation of protein expression by rice HSP101 in planta and using Hsp101 as a selection marker for transformation. Plant and Cell Physiology, 48(8), 1098–1107.

    Article  CAS  PubMed  Google Scholar 

  • Chen, X., Zhang, W., Zhang, B., et al. (2011). Phosphoproteins regulated by heat stress in rice leaves. Proteome Science, 9(1), 1.

    Article  CAS  Google Scholar 

  • Díaz-Martín, J., Almoguera, C., Prieto-Dapena, P., Espinosa, J. M., & Jordano, J. (2005). Functional interaction between two transcription factors involved in the developmental regulation of a small heat shock protein gene promoter. Plant Physiology, 139(3), 1483–1494.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • El-kereamy, A., Bi, Y. M., Ranathunge, K., Beatty, P. H., Good, A. G., & Rothstein, S. J. (2012). The rice R2R3-MYB transcription factor OsMYB55 is involved in the tolerance to high temperature and modulates amino acid metabolism. PLoS ONE, 7(12), e52030.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellis, R. J., van der Vies, S. M., & Hemmingsen, S. M. (1989). The molecular chaperone concept. Biochemical Society Symposia, 55, 145–153.

    CAS  Google Scholar 

  • Endo, M., Tsuchiya, T., Hamada, K., et al. (2009). High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development. Plant and Cell Physiology, 50(11), 1911–1922.

    Article  CAS  PubMed  Google Scholar 

  • Feng, L., Wang, K., Li, Y., Tan, Y., Kong, J., Li, H., et al. (2007). Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants. Plant Cell Reports, 26(9), 1635–1646.

    Article  CAS  PubMed  Google Scholar 

  • Finka, A., Mattoo, R. U., & Goloubinoff, P. (2010). Meta-analysis of heat- and chemically upregulated chaperone genes in plant and human cells. Cell Stress and Chaperones, 16(1), 15–31.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 and Environment, 38(9), 1881–1895.

    Article  CAS  PubMed  Google Scholar 

  • González-Schain, N., Dreni, L., Lawas, L. M., et al. (2016). Genome-wide transcriptome analysis during anthesis reveals new insights into the molecular basis of heat stress responses in tolerant and sensitive rice varieties. Plant and Cell Physiology, 57(1), 57–68.

    Article  PubMed  CAS  Google Scholar 

  • Grover, A. (2002). Molecular biology of stress responses. Cell Stress and Chaperones, 7(1), 1–5.

    Article  PubMed  PubMed Central  Google Scholar 

  • Grover, A., Aggarwal, P. K., Kapoor, A., Katiyar-Agarwal, S., & Agarwal, M. (2003). Production of abiotic stress tolerant transgenic crops: Present accomplishments and future needs. Current Science, 84, 355–367.

    Google Scholar 

  • Grover, A., Chandramouli, A., Agarwal, S., Katiyar-Agarwal, S., Agarwal, M., & Sahi, C. (2009). Transgenic rice for tolerance against abiotic stresses. In S. K. Datta (Ed.), Rice improvement in the genomics era (pp. 237–267). Philadelphia: Haworth Press.

    Google Scholar 

  • Grover, A., Sabat, S. C., & Mohanty, P. (1986a). Effect of high temperature on photosynthetic activities of detached senescing wheat leaves. Plant Cell Physiology, 27, 117–126.

    CAS  Google Scholar 

  • Grover, A., Sabat, S. C., & Mohanty, P. (1986b). Relative sensitivity of various spectral forms of photosynthetic pigments to leaf senescence in wheat (Triticum aestivum L.). Photosynthesis Research (Butler Memorial Volume), 10(3), 223–229.

    Article  CAS  Google Scholar 

  • Guan, J. C., Yeh, C. H., Lin, Y. P., et al. (2010). A 9 bp cis-element in the promoters of class I small heat shock protein genes on chromosome 3 in rice mediates L-azetidine-2-carboxylic acid and heat shock responses. Journal of Experimental Botany, 61(15), 4249–4261.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo, L., Chen, S., Liu, K., et al. (2008). Isolation of heat shock factor HsfA1a-binding sites in vitro revealed variations of heat shock elements in Arabidopsis thaliana. Plant and Cell Physiology, 49(9), 1306–1315.

    Article  CAS  PubMed  Google Scholar 

  • Hahn, J. S., Hu, Z., Thiele, D. J., & Iyer, V. R. (2004). Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Molecular and Cellular Biology, 24(12), 5249–5256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han, F., Chen, H., Li, X. J., Yang, M. F., Liu, G. S., & Shen, S. H. (2009). A comparative proteomic analysis of rice seedlings under various high-temperature stresses. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics, 1794(11), 1625–1634.

    Article  CAS  Google Scholar 

  • Hong, S. W., & Vierling, E. (2001). Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. The Plant Journal, 27(1), 25–35.

    Article  CAS  PubMed  Google Scholar 

  • 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(4), 583–590.

    Article  CAS  PubMed  Google Scholar 

  • Hussain, S. S., Kayani, M. A., & Amjad, M. (2011). Transcription factors as tools to engineer enhanced drought stress tolerance in plants. Biotechnology Progress, 27(2), 297–306.

    Article  CAS  PubMed  Google Scholar 

  • IPCC. (2013). Summary for policymakers. In T.F., Stocker, D., Qin, G.-K., Plattner, M.M.B., Tignor, S.K., Allen, J., Boschung, A., Nauels, Y., Xia, V., Bex, & P.M., Midgley (Eds.), Climate change 2013: The physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, New York: Cambridge University Press

  • Jagadish, S. V. K., Craufurd, P. Q., & Wheeler, T. R. (2007). High temperature stress and spikelet fertility in rice (Oryza sativa L.). Journal of Experimental Botany, 58(7), 1627–1635.

    Article  CAS  PubMed  Google Scholar 

  • Jagadish, S. V. K., Murty, M. V. R., & Quick, W. P. (2015). Rice responses to rising temperatures—challenges, perspectives and future directions. Plant, Cell and Environment, 38(9), 1686–1698.

    Article  CAS  PubMed  Google Scholar 

  • Jagadish, S. V. K., Muthurajan, R., Oane, R., et al. (2010). Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). Journal of Experimental Botany, 61(1), 143–156.

    Article  CAS  PubMed  Google Scholar 

  • Jung, K. H., Ko, H. J., Nguyen, M. X., Kim, S. R., Ronald, P., & An, G. (2012). Genome-wide identification and analysis of early heat stress responsive genes in rice. Journal of Plant Biology, 55(6), 458–468.

    Article  CAS  Google Scholar 

  • Kaneko, K., Sasaki, M., Kuribayashi, N., et al. (2016). Proteomic and glycomic characterization of rice chalky grains produced under moderate and high-temperature conditions in field system. Rice, 9(1), 1–16.

    Article  Google Scholar 

  • Katiyar-Agarwal, S., Agarwal, M., Gallie, D., & Grover, A. (2001). Search for the cellular functions of plant Hsp100/Clp family proteins. Critical Reviews in Plant Sciences, 20, 277–295.

    Article  CAS  Google Scholar 

  • Katiyar-Agarwal, S., Agarwal, M., & Grover, A. (2003). Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant Molecular Biology, 51(5), 677–686.

    Article  CAS  PubMed  Google Scholar 

  • Ke, Y. T., Lu, C. A., Wu, S. J., & Yeh, C. H. (2016). Characterization of rice group 3 LEA genes in developmental stages and under abiotic stress. Plant Molecular Biology Reporter, 1, 1–13.

    Google Scholar 

  • Kim, K. H., Alam, I., Kim, Y. G., et al. (2012). Overexpression of a chloroplast-localized small heat shock protein OsHSP26 confers enhanced tolerance against oxidative and heat stresses in tall fescue. Biotechnology Letters, 34(2), 371–377.

    Article  CAS  PubMed  Google Scholar 

  • Kim, M., Kim, H., Lee, W., Lee, Y., Kwon, S. W., & Lee, J. (2015). Quantitative shotgun proteomics analysis of rice anther proteins after exposure to high temperature. International Journal of Genomics, 2015. doi: 10.1155/2015/238704.

    Google Scholar 

  • Lavania, D., Dhingra, A., Siddiqui, M. H., Al-Whaibi, M. H., & Grover, A. (2015). Current status of the production of high temperature tolerant transgenic crops for cultivation in warmer climates. Plant Physiology and Biochemistry, 86, 100–108.

    Article  CAS  PubMed  Google Scholar 

  • Lee, D. G., Ahsan, N., Lee, S. H., et al. (2007). A proteomic approach in analyzing heat-responsive proteins in rice leaves. Proteomics, 7(18), 3369–3383.

    Article  CAS  PubMed  Google Scholar 

  • Li, X.-M., Chao, D.-Y., Wu, Y., et al. (2015a). Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice. Nature Genetics, 47(7), 827–833.

    Article  CAS  PubMed  Google Scholar 

  • Li, H., Chen, Z., Hu, M., et al. (2011). Different effects of night versus day high temperature on rice quality and accumulation profiling of rice grain proteins during grain filling. Plant Cell Reports, 30(9), 1641–1659.

    Article  CAS  PubMed  Google Scholar 

  • Li, Z., Hu, Q., Zhou, M., Vandenbrink, J., et al. (2013). Heterologous expression of OsSIZ1, a rice SUMO E3 ligase, enhances broad abiotic stress tolerance in transgenic creeping bentgrass. Plant Biotechnology Journal, 11(4), 432–445.

    Article  CAS  PubMed  Google Scholar 

  • Li, X., Lawas, L. M., Malo, R., et al. (2015b). Metabolic and transcriptomic signatures of rice floral organs reveal sugar starvation as a factor in reproductive failure under heat and drought stress. Plant, Cell and Environment, 38(10), 2171–2192.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., Wu, L. Q., Zheng, W. Y., Wang, R. F., & Yang, L. X. (2015c). Genome-wide identification of microRNAs responsive to high temperature in rice (Oryza sativa) by high-throughput deep sequencing. Journal of Agronomy and Crop Science, 201(5), 379–388.

    Article  CAS  Google Scholar 

  • 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(2), 655–671.

    Article  CAS  PubMed  Google Scholar 

  • Lim, S. D., Cho, H. Y., Park, Y. C., Ham, D. J., Lee, J. K., & Jang, C. S. (2013). The rice RING finger E3 ligase, OsHCI1, drives nuclear export of multiple substrate proteins and its heterogeneous overexpression enhances acquired thermotolerance. Journal of Experimental Botany, 64(10), 2899–2914.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin, M. Y., Chai, K. H., Ko, S. S., Kuang, L. Y., Lur, H. S., & Charng, Y. Y. (2014). A positive feedback loop between HEAT SHOCK PROTEIN101 and HEAT STRESS-ASSOCIATED 32-KD PROTEIN modulates long-term acquired thermotolerance illustrating diverse heat stress responses in rice varieties. Plant Physiology, 164(4), 2045–2053.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(8), 2140–2156.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H. C., Liao, H. T., & Charng, Y. Y. (2011). The role of class A1 heat shock factors (HSFA1 s) in response to heat and other stresses in Arabidopsis. Plant, Cell and Environment, 34(5), 738–751.

    Article  CAS  PubMed  Google Scholar 

  • Liu, J. G., Qin, Q. L., Zhang, Z., et al. (2009). OsHSF7 gene in rice, Oryza sativa L., encodes a transcription factor that functions as a high temperature receptive and responsive factor. BMB Reports, 42(1), 16–21.

    Article  PubMed  Google Scholar 

  • Liu, Z. B., Wang, J. M., Yang, F. X., et al. (2014). A novel membrane-bound E3 ubiquitin ligase enhances the thermal resistance in plants. Plant Biotechnology Journal, 12(1), 93–104.

    Article  PubMed  CAS  Google Scholar 

  • Liu, A. L., Zou, J., Liu, C. F., et al. (2013). Overexpression of OsHsfA7 enhanced salt and drought tolerance in transgenic rice. BMB Reports, 46(1), 31–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mangrauthia, S. K., Agarwal, S., Sailaja, B., Sarla, N., & Voleti, S. R. (2016). Transcriptome analysis of Oryza sativa (Rice) seed germination at high temperature shows dynamics of genome expression associated with hormones signalling and abiotic stress pathways. Tropical Plant Biology. doi: 10.1007/s12042-016-9170-7.

    Google Scholar 

  • Mishra, R. C., & Grover, A. (2016). ClpB/Hsp100 proteins and heat stress tolerance in plants. Critical Reviews in Biotechnology, 36(5), 862–874.

    CAS  PubMed  Google Scholar 

  • Mishra, R. C., Singh, A. R., Tiwari, L. D., & Grover, A. (2016). Characterization of 5′UTR of rice ClB-C/Hsp100 gene: Evidence of its involvement in post-transcriptional regulation. Cell Stress and Chaperones, 21(2), 271–283.

    Article  CAS  PubMed  Google Scholar 

  • Mishra, S. K., Tripp, J., Winkelhaus, S., et al. (2002). In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes & Devlopment, 16(12), 1555–1567.

    Article  CAS  Google Scholar 

  • Mittal, D., Chakrabarti, S., Sarkar, A., Singh, A., & Grover, A. (2009). Heat shock factor gene family in rice: Genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiology and Biochemistry, 47(9), 785–795.

    Article  CAS  PubMed  Google Scholar 

  • Mittal, D., Enoki, Y., Lavania, D., Singh, A., Sakurai, H., & Grover, A. (2011). Binding affinities and interactions among different heat shock element types and heat shock factors in rice (Oryza sativa L.). The FEBS Journal, 278(17), 3076–3085.

    Article  CAS  PubMed  Google Scholar 

  • Mittal, D., Madhyastha, D. A., & Grover, A. (2012a). Genome-wide transcriptional profiles during temperature and oxidative stress reveal coordinated expression patterns and overlapping regulons in rice. PLoS ONE, 7(7), e40899.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittal, D., Madhyastha, D. A., & Grover, A. (2012b). Gene expression analysis in response to low and high temperature and oxidative stresses in rice: Combination of stresses evokes different transcriptional changes as against stresses applied individually. Plant Science, 197, 102–113.

    Article  CAS  PubMed  Google Scholar 

  • Mohanty, H. K., Mallik, S., & Grover, A. (2000). Prospects of improving flooding tolerance in lowland rice varieties by conventional breeding and genetic engineering. Current Science, 78(2), 132–140.

    Google Scholar 

  • Murakami, T., Matsuba, S., Funatsuki, H., et al. (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(2), 165–175.

    Article  CAS  Google Scholar 

  • Murakami, Y., & Toriyama, K. (2008). Enhanced high temperature tolerance in transgenic rice seedlings with elevated levels of alternative oxidase, OsAOX1a. Plant Biotechnology, 25(4), 361–364.

    Article  CAS  Google Scholar 

  • Muthayya, S., Sugimoti, J. D., Montgomery, S., & Maberly, G. F. (2014). An overview of global rice production, supply trade, and consumption. Annals of the New York Academy of Sciences, 1324, 7–14.

    Article  PubMed  Google Scholar 

  • Nakashima, K., Yamaguchi-Shinozaki, K., & Shinozaki, K. (2014). The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Frontiers in Plant Science, 5(170). doi:10.3389/fpls.2014.00170.

    PubMed  PubMed Central  Google Scholar 

  • Nelson, G. C., Rosegrant, M. W., Koo, J., et al. (2009). Climate change: Impact on agriculture and costs of adaptation. Washington DC: IFPRI Food Policy Report.

    Google Scholar 

  • Nieto-Sotelo, J., Martínez, L. M., Ponce, G., et al. (2002). Maize Hsp101 plays important role in both induced and basal thermotolerance and primary root growth. The Plant Cell, 14(7), 1621–1633.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pareek, A., Singla, S. L., & Grover, A. (1995). Immunological evidence for accumulation of two high-molecular-weight (104 and 90 kDa) HSPs in response to different stresses in rice and in response to high temperature stress in different plant genera. Plant Molecular Biology, 29(2), 293–301.

    Article  CAS  PubMed  Google Scholar 

  • Pareek, A., Singla, S. L., & Grover, A. (1997). Short-term salinity and high temperature stress-associated ultrastructural alterations in young leaf cells of Oryza sativa L. Annals of Botany, 80(5), 629–639.

    Article  Google Scholar 

  • Pareek, A., Singla, S. L., & Grover, A. (1998a). Protein alterations associated with salinity, desiccation, high and low temperature stresses and abscisic acid application in seedlings of Pusa 169, a high-yielding rice (Oryza sativa L.) cultivar. Current Science, 75, 1023–1035.

    CAS  Google Scholar 

  • Pareek, A., Singla, S. L., & Grover, A. (1998b). Protein alterations associated with salinity, desiccation, high temperature and low temperature stresses and abscisic acid application in Lal nakanda, a drought tolerant rice cultivar. Current Science, 75, 1170–1174.

    CAS  Google Scholar 

  • Peng, S., Huang, J., Sheehy, J. E., et al. (2004). Rice yields decline with higher night temperatures from global warming. Proceedings of the National Academy of Sciences of the United States of America, 101(27), 9971–9975.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prasad, P. V. V., Boote, K. J., Allen, L. H., Sheehy, J. E., & Thomas, J. M. G. (2006). Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crops Research, 95(2), 398–411.

    Article  Google Scholar 

  • Qi, Y., Wang, H., Zou, Y., et al. (2011). Over-expression of mitochondrial heat shock protein 70 suppresses programmed cell death in rice. FEBS Letters, 585(1), 231–239.

    Article  CAS  PubMed  Google Scholar 

  • Qiao, B., Zhang, Q., Liu, D., et al. (2015). A calcium-binding protein, rice annexin OsANN1, enhances heat stress tolerance by modulating the production of H2O2. Journal of Experimental Botany, 66(19), 5853–5866.

    Article  CAS  PubMed  Google Scholar 

  • Qin, D., Wang, F., Geng, X., et al. (2015). Overexpression of heat stress-responsive TaMBF1c, a wheat (Triticum aestivum L.) multiprotein bridging factor, confers heat tolerance in both yeast and rice. Plant Molecular Biology, 87(1–2), 31–45.

    Article  CAS  PubMed  Google Scholar 

  • Queitsch, C., Hong, S. W., Vierling, E., & Lindquist, S. (2000). Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. The Plant Cell, 12(4), 479–492.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rani, B. A., & Maragatham, N. (2013). Effect of elevated temperature on rice phenology and yield. Indian Journal of Science and Technology, 6(8), 5095–5097.

    Google Scholar 

  • Reddy, P. S., Kavi Kishor, P. B., Seiler, C., et al. (2014). Unravelling regulation of the small heat shock proteins by heat shock factor HvHsfB2c in barley: Its implications in drought stress response and seed development. PLoS ONE, 9(3), e89125.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Restrepo-Diaz, H., & Garces-Varon, G. (2013). Response of rice plants to heat stress during initiation of panicle primordia or grain-filling phases. Journal of Stress Physiology & Biochemistry, 9(3), 318–325.

    Google Scholar 

  • Richter, K., Haslbeck, M., & Buchner, J. (2010). The heat shock response: Life on the verge of death. Molecular Cell, 40(2), 253–266.

    Article  CAS  PubMed  Google Scholar 

  • Sailaja, B., Anjum, N., Prasanth, V. V., et al. (2014). Comparative study of susceptible and tolerant genotype reveals efficient recovery and root system contributes to heat stress tolerance in rice. Plant Molecular Biology Reporter, 32(6), 1228–1240.

    Article  CAS  Google Scholar 

  • Sailaja, B., Subrahmanyam, D., Neelamraju, S., et al. (2015). Integrated physiological, biochemical, and molecular analysis identifies important traits and mechanisms associated with differential response of rice genotypes to elevated temperature. Frontiers in Plant Science, 6. doi: 10.3389/fplz.2015.01044

    PubMed  PubMed Central  Google Scholar 

  • Sánchez-Reinoso, A. D., Garcés-Varón, G., & Restrepo-Díaz, H. (2014). Biochemical and physiological characterization of three rice cultivars under different daytime temperature conditions. Chilean journal of agricultural research, 74(4), 373–379.

    Article  Google Scholar 

  • Sarkar, N. K., Kim, Y.-K., & Grover, A. (2009). Rice sHsp genes: Genomic organization and expression profiling under stress and development. BMC Genomics,. doi:10.1186/1471-2164-10-393.

    PubMed  PubMed Central  Google Scholar 

  • Sarkar, N. K., Kim, Y.-K., & Grover, A. (2014). Coexpression network analysis associated with call of rice seedlings for encountering heat stress. Plant Molecular Biology, 84(1–2), 125–143.

    Article  CAS  PubMed  Google Scholar 

  • Sarkar, N. K., Kundnani, P., & Grover, A. (2013a). Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa). Cell Stress and Chaperones, 18(4), 427–437.

    Article  CAS  PubMed  Google Scholar 

  • Sarkar, N. K., Thapar, U., Kundnani, P., Panwar, P., & Grover, A. (2013b). Functional relevance of J-protein family of rice (Oryza sativa). Cell Stress and Chaperones, 18(3), 321–331.

    Article  CAS  PubMed  Google Scholar 

  • Scharf, K. D., Berberich, T., Ebersberger, I., & Nover, L. (2012). The plant heat stress transcription factor (Hsf) family: Structure, function and evolution. Biochimica et Biophysica Acta, 1819(2), 104–119.

    Article  CAS  PubMed  Google Scholar 

  • Shah, F., Huang, J., Cui, K., et al. (2011). Physiological and biochemical changes in rice associated with high night temperature stress and their amelioration by exogenous application of ascorbic acid (vitamin C). Australian Journal of Crop Science, 5(13), 1810.

    CAS  Google Scholar 

  • Shen, H., Zhong, X., Zhao, F., et al. (2015). Overexpression of receptor-like kinase ERECTA improves thermotolerance in rice and tomato. Nature Biotechnology, 33(9), 996–1003.

    Article  CAS  PubMed  Google Scholar 

  • Singh, A., & Grover, A. (2008). Genetic engineering for heat tolerance in plants. Physiology and Molecular Biology of Plants, 14(1–2), 155–166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh, A., & Grover, A. (2010). Plant HSP100/ClpB-like proteins: Poorly-analyzed cousins of the yeast ClpB machine. Plant Molecular Biology, 74(4–5), 395–404.

    Article  CAS  PubMed  Google Scholar 

  • Singh, A., Mittal, D., Lavania, D., Agarwal, M., Mishra, R. C., & Grover, A. (2010a). OsHsfA2c and OsHsfB4b are involved in the transcriptional regulation of cytoplasmic OsClpB (Hsp100) gene in rice (Oryza sativa L.). Cell Stress and Chaperones, 17(2), 243–254.

    Article  CAS  Google Scholar 

  • Singh, A., Singh, U., Mittal, D., & Grover, A. (2010b). Genome-wide analysis of rice ClpB/HSP100, ClpC and ClpD genes. BMC Genomics,. doi:10.1186/1471-2164-11-95.

    Google Scholar 

  • Singla, S. L., & Grover, A. (1993). Antibodies raised against a yeast heat shock protein cross-react with a heat and abscisic acid-regulated polypeptide in rice. Plant Molecular Biology, 22(6), 1177–1180.

    Article  CAS  PubMed  Google Scholar 

  • Singla, S. L., & Grover, A. (1994). Detection and quantitation of a rapidly accumulating and predominant 104 kDa heat shock polypeptide in rice. Plant Science, 97(1), 23–30.

    Article  CAS  Google Scholar 

  • Singla, S. L., Pareek, A., & Grover, A. (1997a). Yeast HSP 104 homologue rice HSP 110 is developmentally- and stress-regulated. Plant Science, 125, 211–219.

    Article  CAS  Google Scholar 

  • Singla, S. L., Pareek, A., & Grover, A. (1997b). High temperature stress. In M. N. V. Prasad (Ed.), Physiological Ecology of Plants (pp. 101–127). New Jersey: Wiley.

    Google Scholar 

  • Singla, S. L., Pareek, A., Kush, A. K., & Grover, A. (1998). Distribution patterns of the 104 kDa stress-associated protein of rice reveal its constitutive accumulation in seeds and disappearance from the just-emerged seedlings. Plant Molecular Biology, 37, 911–919.

    Article  CAS  PubMed  Google Scholar 

  • Tanamachi, K., Miyazaki, M., Matsuo, K., et al. (2016). Differential responses to high temperature during maturation in heat-stress-tolerant cultivars of Japonica rice. Plant Production Science, 19(2), 300–308.

    Article  CAS  Google Scholar 

  • Timabud, T., Yin, X., Pongdontri, P., & Komatsu, S. (2016). Gel-free/label-free proteomic analysis of developing rice grains under heat stress. Journal of Proteomics, 133, 1–19.

    Article  CAS  PubMed  Google Scholar 

  • Tran, L. S. P., Nishiyama, R., Yamaguchi-Shinozaki, K., & Shinozaki, K. (2010). Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM Crops, 1(1), 32–39.

    Article  PubMed  Google Scholar 

  • Uchida, A., Hibino, T., Shimada, T., et al. (2008). Overexpression of DnaK chaperone from a halotolerant cyanobacterium Aphanothecehalophytica increases seed yield in rice and tobacco. Plant Biotechnology, 25(2), 141–150.

    Article  CAS  Google Scholar 

  • Wang, X., Huang, W., Yang, Z., Liu, J., & Huang, B. (2016a). Transcriptional regulation of heat shock proteins and ascorbate peroxidase by CtHsfA2b from African bermudagrass conferring heat tolerance in Arabidopsis. Scientific Reports, 12(2), 1–23. doi:10.1038/srep28021.

    Google Scholar 

  • Wang, D., Li, X. F., Zhou, Z. J., Feng, X. P., Yang, W. J., & Jiang, D. A. (2010). Two Rubisco activase isoforms may play different roles in photosynthetic heat acclimation in the rice plant. Physiologia Plantarum, 139(1), 55–67.

    Article  CAS  PubMed  Google Scholar 

  • Wang, D., Qin, B., Li, X., et al. (2016b). Nucleolar DEAD-Box RNA helicase TOGR1 regulates thermotolerant growth as a pre-rRNA chaperone in rice. PLoS Genetics, 12(2), 1–23.

    Article  CAS  Google Scholar 

  • Wigge, P. A. (2013). Ambient temperature signalling in plants. Current Opinion in Plant Biology, 16(5), 661–666.

    Article  CAS  PubMed  Google Scholar 

  • Wu, X., Shiroto, Y., Kishitani, S., Ito, Y., & Toriyama, K. (2009). Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Reports, 28(1), 21–30.

    Article  CAS  PubMed  Google Scholar 

  • Xiang, J., Ran, J., Zou, J., et al. (2013). Heat shock factor OsHsfB2b negatively regulates drought and salt tolerance in rice. Plant Cell Reports, 32(11), 1795–1806.

    Article  CAS  PubMed  Google Scholar 

  • Xue, G.-P., Drenth, J., & McIntyre, C. L. (2015). TaHsfA6f is a transcriptional activator that regulates a suite of heat stress protection genes in wheat (Triticum aestivum L.) including previously unknown Hsf targets. Journal of Experimental Botany, 66(3), 1025–1039.

    Article  CAS  PubMed  Google Scholar 

  • Yamakawa, H., Hirose, T., Kuroda, M., & Yamaguchi, T. (2007). Comprehensive expression profiling of rice grain filling-related genes under high temperature using DNA microarray. Plant Physiology, 144(1), 258–277.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, C., & Heilman, J. (1993). Response of rice (Oryza sativa L.) to short term high temperature: growth, development and yield. Journal of Agricultural Research in China, 42(1), 1–11.

    Google Scholar 

  • Yokotani, N., Higuchi, M., Kondou, Y., et al. (2011). A novel chloroplast protein, CEST induces tolerance to multiple environmental stresses and reduces photooxidative damage in transgenic Arabidopsis. Journal of Experimental Botany, 62(2), 557–569.

    Article  CAS  PubMed  Google Scholar 

  • Yokotani, N., Ichikawa, T., Kondou, Y., et al. (2008). Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta, 227(5), 957–967.

    Article  CAS  PubMed  Google Scholar 

  • Yoshida, S. (1973). Effects of temperature on growth of the rice plant (Oryza sativa L.) in a controlled environment. Soil Science and Plant Nutrition, 19(4), 299–310.

    Article  Google Scholar 

  • Yoshida, T., Ohama, N., Nakajima, J., et al. (2011). Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Molecular Genetics and Genomics, 286(5–6), 321–332.

    Article  CAS  PubMed  Google Scholar 

  • Yoshida, S., Satake, T., & Mackill, D.S. (1981). High temperature stress in rice, IRRI research paper series. No. 67, International Rice Research Institute, Los Banos, Philippines, pp. 1–15.

  • Zhang, C. X., Fu, G. F., Yang, X. Q., et al. (2016). Heat stress effects are stronger on spikelets than on flag leaves in rice due to differences in dissipation capacity. Journal of Agronomy and Crop Science, 202(5), 394–408.

    Article  CAS  Google Scholar 

  • Zhang, X., Li, J., Liu, A., et al. (2012). Expression profile in rice panicle: Insights into heat response mechanism at reproductive stage. PLoS ONE, 7(11), e49652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, X., Rerksiri, W., Liu, A., et al. (2013). Transcriptome profile reveals heat response mechanism at molecular and metabolic levels in rice flag leaf. Gene, 530(2), 185–192.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, X., Xiong, H., Liu, A., et al. (2014). Microarray data uncover the genome-wide gene expression patterns in response to heat stress in rice post-meiosis panicle. Journal of Plant Biology, 57(6), 327–336.

    Article  CAS  Google Scholar 

  • Zhao, L., Lei, J., Huang, Y., et al. (2016). Mapping quantitative trait loci for heat tolerance at anthesis in rice using chromosomal segment substitution lines. Breeding Science, 66(3), 358–366.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

DL, RK, IG and SR are respectively thankful to Centre for Advanced Research and Innovation [Department of Biotechnology (DBT), Government of India], University Grants Commission (Government of India), Bose project [Department of Science and Technology (DST), Government of India] and Science and Engineering Research Board (SERB) (DST, Government of India) for the fellowship support. AG acknowledges DBT, DST and SERB for the financial support to his laboratory.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anil Grover.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 24 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lavania, D., Kumar, R., Goyal, I. et al. Genetic improvement of rice crop under high temperature stress: bridging plant physiology with molecular biology. Ind J Plant Physiol. 21, 391–408 (2016). https://doi.org/10.1007/s40502-016-0255-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40502-016-0255-y

Keywords

Navigation