Abstract
Heat stress transcription factors (Hsfs) are known to play a vital role in protecting plants against various abiotic stresses. Among the wild wheat relatives, Aegilops tauschii offers an excellent source of abiotic stress tolerance genes for improvement of bread wheat. However, little is known about its stress tolerance mechanisms. In this study, 22 AetHsf genes were identified in the genome of Aegilops tauschii and their chromosomal location, exon–intron structures, sub-cellular localization, phylogenetic and syntenic relationship were analyzed. Based on the conserved motif analysis, these Hsfs were further divided into group A, B and C. The interaction network analysis and expression profile of AetHsfs in different tissues predicted their interaction with diverse types of proteins and suggested their involvement in different developmental processes of the plant. The promoter analysis of AetHsfs showed the presence of abiotic stress-responsive, phytohormone-responsive, plant development-related and light-related cis-elements. Thus, we investigated the expression of Hsfs in Aegilops tauchii seedlings under various abiotic stress conditions and irradiated with different monochromatic lights. Most of the AetHsfs were found to be upregulated by heat stress, while some showed expression in drought, salinity and high light stress as well. Notably, the expression pattern of various AetHsfs showed their responsiveness toward dark and various light conditions (blue red and far-red) as well. Thus, this study provides novel insights into the potential role of AetHsfs in stress and light signaling pathways, which can further facilitate understanding of the stress tolerance mechanisms in Aegilops tauschii.
Similar content being viewed by others
References
Agarwal P, Mitra M, Banerjee S, Roy S (2020) MYB4 transcription factor, a member of R2R3-subfamily of MYB domain protein, regulates cadmium tolerance via enhanced protection against oxidative damage and increases expression of PCS1 and MT1C in Arabidopsis. Plant Sci 297:110501
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. J Biol Chem 277:43866–43872
Alptekin B, Budak H (2017) Wheat miRNA ancestors: evident by transcriptome analysis of A, B, and D genome donors. Funct Integr Genomics 17:171–187
Andrási N, Pettkó-Szandtner A, Szabados L (2021) Diversity of plant heat shock factors: regulation, interactions, and functions. J Exp Bot 72:1558–1575
Arico D, Legris M, Castro L, Garcia CF, Laino A, Casal JJ, Mazzella MA (2019) Neighbour signals perceived by phytochrome B increase thermotolerance in Arabidopsis. Plant Cell Environ 42:2554–2566
Balfagón D, Sengupta S, Gómez-Cadenas A, Fritschi FB, Azad RK, Mittler R, Zandalinasc SI (2019) Jasmonic acid is required for plant acclimation to a combination of high light and heat stress. Plant Physiol 181:1668–1682
Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf K-D et al (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29:471–487
Bechtold U, Albihlal WS, Lawson T, Fryer MJ, Sparrow PAC, Richard F, Persad R, Bowden L, Hickman R, Martin C et al (2013) Arabidopsis Heat shock transcription factora1b overexpression enhances water productivity, resistance to drought, and infection. J Exp Bot 64:3467–3481
Begum T, Reuter R, Schöffl F (2013) Overexpression of AtHsfB4 induces specific effects on root development of Arabidopsis. Mech Dev 130:54–60
Bharti S, Kumar P, Tintschl-ko A, Bharti K, Treuter E, Nover L (2004) Tomato heat stress transcription factor HsfB1 represents a novel type of general transcription coactivator with a histone-like motif interacting with the plant CREB binding protein ortholog HAC1. Plant Cell 16:1521–1535
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
Casal JJ, Balasubramanian S (2019) Thermomorphogenesis. Annu Rev Plant Biol 70:321–346
Charng YY, Liu HC, Liu NY, Chi WT, Wang CN, Chang SH, Wang TT (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol 143:251–262
Chauhan H, Khurana N, Agarwal P, Khurana P (2011a) Heat shock factors in rice (Oryza sativa L.): Genome-wide expression analysis during reproductive development and abiotic stress. Mol Genet Genomics 286:171–187
Chauhan H, Khurana N, Tyagi AK, Khurana JP, Khurana P (2011b) Identification and characterization of high temperature stress responsive genes in bread wheat (Triticum aestivum L.) and their regulation at various stages of development. Plant Mol Biol 75:35–51
Cohen-Peer R, Schuster S, Meiri D, Breiman A, Avni A (2010) Sumoylation of Arabidopsis heat shock factor A2 (HsfA2) modifies its activity during acquired thermotholerance. Plant Mol Biol 74:33–45
Czarnecka-Verner E, Pan S, Salem T, Gurley WB (2004) Plant class B HSFs inhibit transcription and exhibit affinity for TFIIB and TBP. Plant Mol Biol 56:57–75
Duan S, Liu B, Zhang Y, Li G, Guo X (2019) Genome-wide identification and abiotic stress-responsive pattern of heat shock transcription factor family in Triticum aestivum L. BMC Genomics 20:1–20
El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, Qureshi M, Richardson LJ, Salazar GA, Smart A et al (2019) The Pfam protein families database in 2019. Nucleic Acids Res 47:D427–D432
Eremina M, Rozhon W, Yang S, Poppenberger B (2015) ENO2 activity is required for the development and reproductive success of plants, and is feedback-repressed by AtMBP-1. Plant J 81:895–906
Evrard A, Kumar M, Lecourieux D, Lucks J, von Koskull-Döring P, Hirt H (2013) Regulation of the heat stress response in arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. PeerJ 2013:1–21
Fan J, Lou Y, Shi H, Chen L, Cao L (2019) Transcriptomic analysis of dark-induced senescence in bermudagrass (Cynodon dactylon). Plants 8:1–17
Fragkostefanakis S, Mesihovic A, Simm S, Paupière MJ, Hu Y, Paul P, Mishra SK, Tschiersch B, Theres K, Bovy A et al (2016) HsfA2 controls the activity of developmentally and stress-regulated heat stress protection mechanisms in tomato male reproductive tissues. Plant Physiol 170:2461–2477
Giesguth M, Sahm A, Simon S, Dietz KJ (2015) Redox-dependent translocation of the heat shock transcription factor AtHSFA8 from the cytosol to the nucleus in Arabidopsis thaliana. FEBS Lett 589:718–725
Guo J, Wu J, Ji Q, Wang C, Luo L, Yuan Y, Wang Y, Wang J (2008) Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. J Genet Genomics 35:105–118
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. Front Plant Sci 7:114
Hahn A, Bublak D, Schleiff E, Scharf K-D (2011) Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 23:741–755
Hairat S, Khurana P (2015) Evaluation of Aegilops tauschii and Aegilops speltoides for acquired thermotolerance: Implications in wheat breeding programmes. Plant Physiol Biochem 95:65–74
Han SH, Park YJ, Park CM (2019) Light primes the thermally induced detoxification of reactive oxygen species during development of thermotolerance in Arabidopsis. Plant Cell Physiol 60:230–241
Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 80(295):1852–1858
Hasanuzzaman M, Nahar K, Alam M, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684
Hayes S, Sharma A, Fraser DP, Trevisan M, Cragg-Barber CK, Tavridou E, Fankhauser C, Jenkins GI, Franklin KA (2017) UV-B perceived by the UVR8 photoreceptor inhibits plant thermomorphogenesis. Curr Biol 27:120–127
Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:585–587
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics 31:1296–1297
Hu X-J, Chen D, Lynne Mclntyre C, Fernanda Dreccer M, Zhang Z-B, Drenth J, Kalaipandian S, Chang H, Xue G-P (2018) Heat shock factor C2a serves as a proactive mechanism for heat protection in developing grains in wheat via an ABA-mediated regulatory pathway. Plant Cell Environ 41:79–98
Huang YC, Niu CY, Yang CR, Jinn TL (2016) The heat stress factor HSFA6b connects ABA signaling and ABA-mediated heat responses. Plant Physiol 172:1182–1199
Hwang SM, Kim DW, Woo MS, Jeong HS, Son YS, Akhter S, Choi GJ, Bahk JD (2014) Functional characterization of Arabidopsis HsfA6a as a heat-shock transcription factor under high salinity and dehydration conditions. Plant, Cell Environ 37:1202–1222
Jin GH, Gho HJ, Jung KH (2013) A systematic view of rice heat shock transcription factor family using phylogenomic analysis. J Plant Physiol 170:321–329
Jung HS, Crisp PA, Estavillo GM, Cole B, Hong F, Mockler TC, Pogson BJ, Chory J (2013) Subset of heat-shock transcription factors required for the early response of Arabidopsis to excess light. Proc Natl Acad Sci USA 110:14474–14479
Jung JH, Domijan M, Klose C, Biswas S, Ezer D, Gao M, Khattak AK, Box MS, Charoensawan V, Cortijo S et al (2016) Phytochromes function as thermosensors in Arabidopsis. Science 354:886–889
Kilian B, Mammen K, Millet E, Sharma R, Graner A, Salamini F, Hammer K, Hakan O (2011) Wild crop relatives: genomic and breeding resources. Springer, Heidelberg. https://doi.org/10.1007/978-3-642-14228-4
Kim T, Samraj S, Jiménez J, Gómez C, Liu T, Begcy K (2021) Genome-wide identification of heat shock factors and heat shock proteins in response to UV and high intensity light stress in lettuce. BMC Plant Biol 21:1–20
Kishii M (2019) An update of recent use of Aegilops Species in Wheat Breeding. Front Plant Sci 10:585
Kotak S, Vierling E, Bäumlein H, Von Koskull-Dörlng P (2007) A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19:182–195
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Legris M, Klose C, Burgie ES, Rojas CC, Neme M, Hiltbrunner A, Wigge PA, Schäfer E, Vierstra RD, Casal JJ (2016) Phytochrome B integrates light and temperature signals in Arabidopsis. Science 80(354):897–900
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van De Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Li PS, Yu TF, He GH, Chen M, Bin ZY, Chai SC, Xu ZS, Ma YZ (2014) Genome-wide analysis of the Hsf family in soybean and functional identification of GmHsf-34 involvement in drought and heat stresses. BMC Genomics 15:1–16
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 12:1–14
Liu B, Hu J, Zhang J (2019a) Evolutionary divergence of duplicated hsf genes in Populus. Cells 8:438
Liu M, Huang Q, Sun W, Ma Z, Huang L, Wu Q, Tang Z, Bu T, Li C, Chen H (2019b) Genome-wide investigation of the heat shock transcription factor (Hsf) gene family in Tartary buckwheat (Fagopyrum tataricum). BMC Genomics 20:1–17
Liu X, Panpan M, Guiyan Y, Mengyan Z, Shaobing P, Zhai MZ (2020) Genome-wide identification and transcript profiles of walnut heat stress transcription factor involved in abiotic stress. BMC Genomics 21:474
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408
Luo M-C, Gu YQ, Puiu D, Wang H, Twardziok SO, Deal KR, Huo N, Zhu T, Wang L, Wang Y et al (2017) Genome sequence of the progenitor of the wheat D genome Aegilops tauschii. Nature 551:498–502
Ma D, Li X, Guo Y, Chu J, Fang S, Yan C, Noel JP, Liu H (2016) Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light. Proc Natl Acad Sci USA 113:224–229
Mansouri M, Naghavi MR, Alizadeh H, Mohammadi-Nejad G, Mousavi SA, Salekdeh GH, Tada Y (2019) Transcriptomic analysis of Aegilops tauschii during long-term salinity stress. Funct Integr Genomics 19:13–28
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, Döring 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 Z, Wang M, Li F, Lv H, Li C, Xia G (2009) A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat. Mol Cell Proteomics 8:2676–2686
Pérez-Salamó I, Papdi C, Rigó G, Zsigmond L, Vilela B, Lumbreras V, Nagy I, Horváth B, Domoki M, Darula Z et al (2014) The heat shock factor A4A confers salt tolerance and is regulated by oxidative stress and the mitogen-activated protein kinases MPK3 and MPK6. Plant Physiol 165:319–334
Pierleoni A, Martelli PL, Fariselli P, Casadio R (2006) BaCelLo: a balanced subcellular localization predictor. Bioinformatics 22:408–416
Quail PH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3:85–93
Queitsch C, Hong SW, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12:479–492
Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69:225–232
Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822–18827
Samtani H, Sharma A, Khurana P (2022a) Overexpression of HVA1 enhances drought and heat stress tolerance in Triticum aestivum doubled haploid plants. Cells 11:912
Samtani H, Sharma A, Khurana P (2022b) Wheat ocs-element binding factor 1enhances thermotolerance by modulating the heat stress response pathway. Frontiers in Plant Sciences 13:914363
Scharf K-D, Heider H, Höhfeld 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
Scharf K-D, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819:104–119
Schramm F, Ganguli A, Kiehlmann E, Englich G, Walch D, Von Koskull-Döring P (2006) The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol Biol 60:759–772
Schubert R, Dobritzsch S, Gruber C, Hause G, Athmer B, Schreiber T, Marillonnet S, Okabe Y, Ezura H, Acosta IF et al (2019) Tomato MYB21 acts in ovules to mediate jasmonate-regulated fertility. Plant Cell 31:1043–1062
Singh V, Singh G, Singh V (2020) TulsiPIN: An interologous protein interactome of Ocimum tenuiflorum. J Proteome Res 19:884–899
Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, Peng W, Liu Y, Peng J, Xie D (2011) The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect Jasmonate-regulated stamen development in Arabidopsis. Plant Cell 23:1000–1013
Sorger PK, Pelham HR (1988) Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54:855–864
Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P et al (2019) STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47:D607–D613
Tang M, Xu L, Wang Y, Cheng W, Luo X, Xie Y, Fan L, Liu L (2019) Genome-wide characterization and evolutionary analysis of heat shock transcription factors (HSFs) to reveal their potential role under abiotic stresses in radish (Raphanus sativus L.). BMC Genomics 20:1–13
von Koskull-Döring P, Scharf KD, Nover L (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci 12:452–457
Wang F, Dong Q, Jiang H, Zhu S, Chen B, Xiang Y (2012) Genome-wide analysis of the heat shock transcription factors in Populus trichocarpa and Medicago truncatula. Mol Biol Rep 39:1877–1886
Wang N, Liu W, Yu L, Guo Z, Chen Z, Jiang S, Xu H, Fang H, Wang Y, Zhang Z et al (2020a) Heat shock factor A8a modulates flavonoid synthesis and drought tolerance. Plant Physiol 184:1273–1290
Wang X-C, Wu J, Guan M-L, Zhao C-H, Geng P, Zhao Q (2020b) Arabidopsis MYB4 plays dual roles in flavonoid biosynthesis. Plant J 101:637–652
Wei Y, Cao L, Huang X, Wang X, Wang H, Song Y, He Q, Lyu M, Hu X, Liu J (2020) Genome-wide characterization of early response genes to abscisic acid coordinating multiple pathways in Aegilops tauschii. Crop J 9:934–944
Xue GP, Sadat S, Drenth J, McIntyre CL (2014) The heat shock factor family from Triticum aestivum in response to heat and other major abiotic stresses and their role in regulation of heat shock protein genes. J Exp Bot 65:539–557
Xue GP, Drenth J, McIntyre CL (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. J Exp Bot 66:1025–1039
Yang W, Li J, Liu D, Sun J, He L, Zhang A (2014) Genome-wide analysis of the heat shock transcription factor family in Triticum urartu and Aegilops tauschii. Plant Omi J 7:291–297
Yee D, Goring DR (2009) The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. J Exp Bot 60:1109–1121
Yu C-S, Chen Y-C, Lu C-H, Hwang J-K (2006) Prediction of protein subcellular localization. Proteins Struct Funct Bioinforma 64:643–651
Zang D, Wang J, Zhang X, Liu Z, Wang Y (2019) Arabidopsis heat shock transcription factor HSFA7b positively mediates salt stress tolerance by binding to an E-box-like motif to regulate gene expression. J Exp Bot 70:5355–5374
Zhang J, Li Y, Jia H, Li J, Huang J, Lu M, Rhoads DM, Sun T, Gong Z (2015) The heat shock factor gene family in Salix Suchowensis : a genome-wide survey and expression profiling during development and abiotic stresses. Front Plant Sci 6:1–14
Zhang D, Zhou Y, Zhao X, Lv L, Zhang C, Li J, Sun G, Li S, Song C (2018) Development and utilization of introgression lines using synthetic octaploid wheat (Aegilops tauschii × hexaploid wheat) as Donor. Front Plant Sci 9:1113
Zhang K, Wang X, Cheng F (2019) Plant Polyploidy: Origin, evolution, and its influence on crop domestication. Hortic Plant J 5:231–239
Zhao X, Bai S, Li L, Han X, Li J, Zhu Y, Fang Y, Zhang D, Li S (2020) Comparative transcriptome analysis of two Aegilops tauschii with contrasting drought tolerance by RNA-Seq. Int J Mol Sci 21:1–20
Zhou M, Zheng S, Liu R, Lu J, Lu L, Zhang C, Liu Z, Luo C, Zhang L, Yant L et al (2019) Genome-wide identification, phylogenetic and expression analysis of the heat shock transcription factor family in bread wheat (Triticum aestivum L.). BMC Genomics 20:505
Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324
Funding
HS and AS are thankful to University Grant Commission (UGC) for fellowships. This work has been supported by a grant from JC Bose fellowship award, Science and Engineering Research Board, Government of India, for research support to JPK and PK.
Author information
Authors and Affiliations
Contributions
PK, JPK and HS conceptualized the idea of the research. HS and AS performed the experiments. PK and JPK provided all the facilities for the experiments. HS and AS wrote the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationship that could be construed as a potential conflict of interest.
Additional information
Communicated by Bing Yang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Samtani, H., Sharma, A., Khurana, J.P. et al. The heat stress transcription factor family in Aegilops tauschii: genome-wide identification and expression analysis under various abiotic stresses and light conditions. Mol Genet Genomics 297, 1689–1709 (2022). https://doi.org/10.1007/s00438-022-01952-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-022-01952-9