Abstract
Heat shock factors (HSFs) in plants regulate heat stress response by mediating expression of a set of heat shock protein (HSP) genes. In the present study, we isolated a novel heat shock gene, TaHSF3, encoding a protein of 315 amino acids in wheat. Phylogenetic analysis showed that TaHSF3 belonged to HSF class B2. Subcellular localization analysis indicated that TaHSF3 localized in nuclei. TaHSF3 was highly expressed in wheat spikes and showed intermediate expression levels in roots, stems, and leaves under normal conditions. It was highly upregulated in wheat seedlings by heat and cold and to a lesser extent by drought and NaCl and ABA treatments. Overexpression of TaHSF3 in Arabidopsis enhanced tolerance to extreme temperatures. Frequency of survival of three TaHSF3 transgenic Arabidopsis lines was 75–91 % after heat treatment and 85–95 % after freezing treatment compared to 25 and 10 %, respectively, in wild-type plants (WT). Leaf chlorophyll contents of the transformants were higher (0.52–0.67 mg/g) than WT (0.35 mg/g) after heat treatment, and the relative electrical conductivities of the transformants after freezing treatment were lower (from 17.56 to 18.6 %) than those of WT (37.5 %). The TaHSF3 gene from wheat therefore confers tolerance to extreme temperatures in transgenic Arabidopsis by activating HSPs, such as HSP70.
Similar content being viewed by others
Abbreviations
- ABA:
-
abscisic acid
- DBD:
-
DNA-binding domain
- HSE:
-
heat shock element
- HSF:
-
heat shock factor
- HSP:
-
heat shock protein
- NLS:
-
nuclear localization signal domain
- QRT-PCR:
-
quantitative real-time PCR
- WT:
-
wild type
References
Aono M, Kubo A, Saji H, Tanaka K, Kondo N (1993) Enhanced tolerance to photooxidative stress of transgenic Nicotiana tabacum with high chloroplastic glutathione reductase activity. Plant Cell Physiol 34:129–136
Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf KD, Tripp J, Weber C, Zielinski D, von Koskull-Doring P (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29:471–487
Boscheinen O, Lyck R, Queitsch C, Treuter E, Zimarino V, Scharf KD (1997) Heat stress transcription factors from tomato can functionally replace HSF1 in the yeast Saccharomyces cerevisiae. Mol Gen Genet 255:322–331
Boston RS, Vitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222
Breeze E, Harrison E, Page T, Warner N, Shen C, Zhang C, Buchanan-Wollaston V (2008) Transcriptional regulation of plant senescence: from functional genomics to systems biology. Plant Biol 10:99–109
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:725–743
Czarnecka-Verner E, Gurley WB (1999) Plant heat shock transcription factors: divergence in structure and function. Biotechnologia 3:125–142
Czarnecka-Verner E, Yuan CX, Fox PC, Gurley WB (1995) Isolation and characterization of six heat shock transcription factor cDNA clones from soybean. Plant Mol Biol 29:37–51
Czarnecka-Verner E, Yuan CX, Scharf KD, Englich G, Gurley WB (2000) Plants contain a novel multi-member class of heat shock factors without transcriptional activator potential. Plant Mol Biol 43:459–471
Donghwan S, Hwang JU, Lee J, Lee SL, Choi Y, Gynheung A, Martinoia E, Youngsook L (2009) Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell 21:4031–4043
Duan YH, Guo J, Ding K, Wang SJ, Zhang H, Dai XW, Chen YY, Govers F, Li-Li H, Kang ZS (2011) Characterization of a wheat HSP70 gene and its expression in response to stripe rust infection and abiotic stresses. Mol Biol Rep 38:301–307
Ferrigno P, Silver PA (1999) Regulated nuclear localization of stress-responsive factors: how the nuclear tracking of protein kinases and transcription factors contributes to cell survival. Oncogene 18:6129–6134
Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449
Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70:603–647
Guo JK, Wu J, Ji Q, Wang C, Luo L, Yuan Y, Wang YH, Wang J (2008) Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. J Genet Genomics 35:105–118
Haq NU, Raza S, Luthe DS, Heckathorn SA, Shakeel SN (2012) A dual role for the chloroplast small heat shock protein of Chenopodium album including protection from both heat and metal stress. Plant Mol Biol Rep. doi:10.1007/s11105-012-0516-5
Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–580
Hu DG, Ming L, Luo H, Dong QL, Yao YX, You CX, Hao YJ (2012) Molecular cloning and functional characterization of MdSOS2 reveals its involvement in salt tolerance in apple callus and Arabidopsis. Plant Cell Rep 31:713–722
Ikeda M, Mitsuda N, Ohme-Takagi M (2011) Arabidopsis HsfB1 and HsfB2b act as repressors of the expression of heat-inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiol 157:1243–1254
Kanchiswamy CN, Muroi A, Maffei ME, Yoshioka H, Sawasaki T, Arimura G (2010) Ca2+-dependent protein kinases and their substrate HsfB2a are differently involved in the heat response signaling pathway in Arabidopsis. Plant Biotech 27:469–473
Kotak S, Port M, Ganguli A, Bicker F, Von Koskull-Dǒring P (2004) Characterization of C-terminal domains of Aradidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant Class A Hsfs with AHA and NES motifs essential for activator function and intrancellular localization. Plant J 39:98–112
Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–897
Li HY, Chang CS, Lu LS, Liu CA, Chan MT, Chang YY (2003) Over-expression of Arabidopsis thaliana heat shock factor gene (AtHsfA1b) enhances chilling tolerance in transgenic tomato. Botbull Acad Sin 44:A129–A140
Li CG, Chen QJ, Gao XQ, Qi BS, Chen NZ, Xu SM, Chen J, Wang XC (2005) AtHsfA2 modulates expression of stress responsive genes and enhances tolerance to heat and oxidative stress in Arabidopsis. Sci China C Life Sci 48:540–550
Liberek K, Lewandowska A, Zietkiewicz S (2008) Chaperones in control of protein disaggregation. EMBO J 27:328–335
Lin BL, Wang JS, Liu HC, Chen RW, Meyer Y, Barakat A, Delseny M (2001) Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress Chaperones 6:201–208
Lin YX, Jiang HY, Chu ZX, Tang XL, Zhu SW, Cheng BJ (2011) Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genomics 12:76–83
Liu AL, Zou J, Zhang XW, Zhou XY, Wang WF, Xiong XY, Chen LY, Chen XB (2010) Expression profiles of Class A rice heat shock transcription factor genes under abiotic stresses. J Plant Biol 53:142–149
Liu T, Hou X, Zhang J, Song Y, Zhang S, Li Y (2011) A cDNA clone of BcHSP81-4 from the sterility line (PolCMS) of non-heading Chinese cabbage (Brassica campestris ssp. chinensis). Plant Mol Biol Rep 29:723–732
Lohmann C, Eggers-Schumacher G, Wunderlich M, Schöffl F (2004) Two different heat shock factors regulate immediate early expression of stress genes in Arabidopsis. Mol Genet Genomics 271:11–21
Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98:279–288
Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf KD (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev 16:1555–1567
Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A (2009) Heat shock factor gene family in rice: expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiol Biochem 5:1–11
Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12:3788–3796
Morimoto RI, Sarge KD, Abravaya K (1992) Transcriptional regulation of heat shock genes: a paradigm for inducible genomic responses. J Biol Chem 31:21987–21990
Morimoto RI, Tissieres A, Georgopoulos C (1994) Progress and perspectives on the biology of heat shock proteins and molecular chaperones. In: Morimoto RI, Tissieres A, Georgopoulos C (eds) The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory, New York, pp 1–31
Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48:535–547
Nover L, Bharti K, Doring P, Mishra SK, Ganguli A, Scharf KD (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6:177–189
Ogawa D, Yamaguchi K, Nishiuchi T (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J Exp Bot 58:3373–3383
Peng SB, Zhu ZG, Zhao K, Shi JL, Yang YZ, He MY, Wang YJ (2012) A novel heat shock transcription factor, VpHsf1, from Chinese wild Vitis pseudoreticulata is involved in biotic and abiotic stresses. Plant Mol Biol Rep. doi:10.1007/s11105-012-0463-1
Peteranderl R, Rabenstein M, Shin YK, Liu CW, Wemmer DE, King DS, Nelson HC (1999) Biochemical and biophysical characterization of the trimerization domain from the heat shock transcription factor. Biochemistry 38:3559–3569
Qin DD, Wu HY, Peng HR, Yao YY, Ni ZF, Li ZX, Zhou CL, Sun QX (2008) Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using wheat genome array. BMC Genomics 9:1–19
Qin YX, Wang MC, Tian YC, He WX, Lu H, Xia GM (2012) Over-expression of TaMYB33 encoding a novel wheat MYB transcription factor increases salt and drought tolerance in Arabidopsis. Mol Biol Rep 39:7183–7192
Sacnjeev K, Kapil B, Kwan YC, Markus F, Arnab G, Sachin K, Shravan KM, Lutz N, Markus P, Klaus-Dieter S, Joanna T, Christian W, Dirk Z, Pascal VK (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 4:471–487
Scharf KD, Heider H, Hohfeld I, Lyck R, Schmidt E, Nover L (1998) The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Mol Cell Biol 18:2240–2251
Swindell WR, Huebner M, Weber AP (2007) Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 125:1–15
Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–7
Wang WX, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252
Xiao H, Lis JT (1988) Germline transformation used to define key features of heat-shock response elements. Science 239:1139–1143
Xu ZS, Xia LQ, Chen M, Cheng XG, Zhang RY, Li LC, Zhao YX, Lu Y, Ni ZY, Liu L, Qiu ZG, Ma YZ (2007) Isolation and molecular characterization of the Triticum aestivum L. Ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 65:719–732
Xu ZS, Chen M, Li LC, Ma YZ (2008) Functions of the ERF transcription factor family in plants. Botany 86:969–977
Xu ZS, Chen M, Li LC, Ma YZ (2011) Functions and application of the AP2/ERF transcription factor family in crop improvement. J Integr Plant Biol 53:570–585
Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2008) Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227:957–967
Yoshida T, Ohama N, Nakajima J, Kidokoro S, Mizoi J, Nakashima K, Maruyama K, Kim JM, Seki M, Todaka D, Osakabe Y, Sakuma Y, Schoffl F, Shinozaki K, Yamaguchi-Shinozaki K (2011) Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Genet Genomics 286:321–332
Zhu B, Ye C, Lü H, Chen X, Chai G, Chen J, Wang C (2006) Identification and characterization of a novel heat shock transcription factor gene, GmHsfA1, in soybeans (Glycine max). J Plant Res 119:247–256
Acknowledgments
This research was financially supported by the National Natural Science Foundation of China (31171546) and the National Transgenic Key Project of MOA (2011ZX08002-002). We are grateful to Drs. Ruilian Jing (Institute of Crop Science, Chinese Academy of Agricultural Sciences), for providing wheat seeds, and RA McIntosh (Plant Breeding Institute, University of Sydney), for critically reading the manuscript.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Zhang, S., Xu, ZS., Li, P. et al. Overexpression of TaHSF3 in Transgenic Arabidopsis Enhances Tolerance to Extreme Temperatures. Plant Mol Biol Rep 31, 688–697 (2013). https://doi.org/10.1007/s11105-012-0546-z
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-012-0546-z