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Functional & Integrative Genomics

, Volume 19, Issue 3, pp 497–513 | Cite as

Functional characterization of HSFs from wheat in response to heat and other abiotic stress conditions

  • Preeti Agarwal
  • Paramjit KhuranaEmail author
Original Article
  • 318 Downloads

Abstract

High temperature stress is known to be one of the major limiting factors for wheat productivity worldwide. HSFs are known to play a central role in heat stress response in plants. Hence, the current study is an attempt to explore an in-depth involvement of TaHSFs in stress responses mainly in heat and other abiotic responses like salinity, drought, and cold stress. Effort was made to understand as how the expression of HSF is able to define the differential robustness of wheat varieties. Subsequent studies were done to establish the involvement of any temporal or spatial cue on the behavior of these TaHSFs under heat stress conditions. A total of 53 HSFs have been reported until date and out of these, few TaHSFs including one identified in our library, i.e., TaHsfA2d (Traes_4AS_52EB860E7.2), were selected for the expression analysis studies. The expressions of these HSFs were found to differ in both magnitude and sensitivity to the heat as well as other abiotic stresses. Moreover, these TaHSFs displayed wide range of expression in different tissues like anther, ovary, lemma, palea, awn, glume, and different stages of seed development. Thus, TaHSFs appear to be under dynamic expression as they respond in a unique manner to spatial, temporal, and environmental cues. Therefore, these HSFs can be used as candidate genes for understanding the molecular mechanism under heat stress and can be utilized for improving crop yield by enhancing the tolerance and survival of the crop plants under adverse environment conditions.

Keywords

Abiotic stress Days After Anthesis HSFs Heat stress Triticum aestivum 

Abbreviations

CTAD

C-terminal activation domains

DAA

Days after anthesis

HSF

Heat shock factor

HSP

Heat shock proteins

HT

High temperature

NES

Nuclear export signal

NLS

Nuclear localization signal

Notes

Author contribution

PA and PK planned the experiment. PA wrote the manuscript. PA and PK read and approved the manuscript.

Funding information

This work was funded by the Department of Biotechnology, Government of India, New Delhi, and Council of Scientific and Industrial Research, New Delhi, for awarding the Senior Research Fellowship.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10142_2019_666_Fig10_ESM.png (1.5 mb)
Supplementary Figure S1

The multiple alignments for TaHSF and its homologous members were done using ClustalW2 showing conservation of a HSF. b coiled-coil domain (PNG 1567 kb)

10142_2019_666_MOESM1_ESM.tif (2.3 mb)
High resolution image (TIF 2320 kb)
10142_2019_666_Fig11_ESM.png (1.7 mb)
Supplementary Figure S2

The multiple alignment of TaHSF transcription factor with its orthologue members from other plant species were done by ClustalW2 showing conservation of the HSF domain (PNG 1776 kb)

10142_2019_666_MOESM2_ESM.tif (2.7 mb)
High resolution image (TIF 2744 kb)
10142_2019_666_MOESM3_ESM.xls (32 kb)
Supplementary Table S1 List of primers used in the study (XLS 32 kb)
10142_2019_666_MOESM4_ESM.xls (35 kb)
Supplementary Table S2 Distribution of HSF transcription factor in various species retrieved from Plant Transcription Factor Database. A total of 4574 HSFs have been reported in database (XLS 35 kb)
10142_2019_666_MOESM5_ESM.xls (20 kb)
Supplementary Table S3 Details of TaHSFs reported in Triticum aestivum retrieved from Plant Transcription Factor Database along with their protein length, motifs with their positions, Gene Ontology (GO) terms and etc (XLS 19 kb)
10142_2019_666_MOESM6_ESM.xls (32 kb)
Supplementary Table S4 Details of TaHSF (Traes_4AS_52EB860E7.2) and its homologous members retrieved from Plant Transcription Factor Database w.r.t. to HSF domain and motif derived from SMART and MEME online tool (XLS 32 kb)
10142_2019_666_MOESM7_ESM.xls (20 kb)
Supplementary Table S5 Details of TaHSF (Traes_4AS_52EB860E7.2) and its orthologous members retrieved from Plant Transcription Factor Database w.r.t. to HSF domain and motif derived from SMART and MEME online tool (XLS 19 kb)

References

  1. Akpinar BA, Avsar B, Lucas SJ, Budak H (2012) Plant abiotic stress signaling. Plant Signal Behav 7(11):1450–1455CrossRefPubMedPubMedCentralGoogle Scholar
  2. Banti V, Mafessoni F, Loreti E, Alpi A, Perata P (2010) The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol 152(3):1471–1483CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bechtold U, Albihlal WS, Lawson L, 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(11):3467–3481CrossRefPubMedPubMedCentralGoogle Scholar
  4. Budak H, Kantar M, Kurtoglu KY (2013) Drought tolerance in modern and wild wheat. Sci World J 2013:548246CrossRefGoogle Scholar
  5. Budak H, Hussain B, Khan Z, Ozturk NZ, Ullah N (2015) From genetics to functional genomics: improvement in drought signaling and tolerance in wheat. Front Plant Sci 6:1012CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chauhan H, Khurana N, Tyagi AK, Khurana JP, Khurana P (2011a) Identification and characterization of high temperatures stress responsive genes in bread wheat (Triticum aestivum L.) and their regulation at various stages of development. Plant Mol Biol 75(1–2):35–51CrossRefPubMedGoogle Scholar
  7. Chauhan H, Khurana N, Agarwal P, Khurana P (2011b) Heat shock factors in rice (Oryza sativa L.): genome-wide expression analysis during reproductive development and abiotic stress. Mol Gen Genomics 286(2):171–187CrossRefGoogle Scholar
  8. Chauhan H, Khurana N, Agarwal P, Khurana P (2013) A seed preferential heat shock transcription factor from wheat provides abiotic stress tolerance and yield enhancement in transgenic Arabidopsis under heat tress environment. PLoS One 8(11):1–13Google Scholar
  9. Doring P (2000) The role of AHA motifs in the activator function of tomato heat stress transcription factors HsfA1 and HsfA2. Plant Cell 12(2):265–278CrossRefPubMedPubMedCentralGoogle Scholar
  10. Ergen NZ, Thimmapuram J, Bohnert HJ, Budak H (2009) Transcriptome pathways unique to dehydration tolerant relatives of modern wheat. Functional and Integrative Genomics 9(3):377–396CrossRefPubMedGoogle Scholar
  11. Fragkostefanakis S, Röth S, Schleiff E, Scharf KD (2015) Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. Plant Cell Environ 38(9):1881–1895CrossRefPubMedGoogle Scholar
  12. Giorno F, Wolters-Arts M, Grillo S, Scharf KD, Vriezen WH, Mariani C (2010) Developmental and heat stress-regulated expression of HsfA2 and small heat shock proteins in tomato anthers. J Exp Bot 61(2):453–462CrossRefGoogle Scholar
  13. Giorno F, Guerriero G, Baric S, Mariani C (2012) Heat shock transcriptional factors in Malus domestica: identification, classification and expression analysis. BMC Genomics 13:639CrossRefPubMedPubMedCentralGoogle Scholar
  14. Guo M, Lu LP, Zhai YF, Chai WG, Gong ZH, Lu MH (2015) Genome-wide analysis, expression profile of heat shock factor gene family (CaHsfs) and characterisation of CaHsfA2 in pepper (Capsicum annuum L.). BMC Plant Biol 15:151CrossRefPubMedPubMedCentralGoogle Scholar
  15. Guo M, Liu JH, Ma X, Luo DX, Gong ZH, Lu MH (2016) The plant heat stress transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses. Front Plant Sci 7:114PubMedPubMedCentralGoogle Scholar
  16. Hairat S, Khurana P (2015) Improving photosynthetic responses during recovery from heat treatments with brassinosteroids and calcium chloride in Indian bread wheat cultivars. Am J Plant Sci 6(11):1827–1849CrossRefGoogle Scholar
  17. Hu B, Jin J, Guo AY, Zhang H, Luo L, Gao G (2015a) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297CrossRefPubMedGoogle Scholar
  18. Hu Y, Han YT, Wei W, Li YJ, Zhang K, Gao YR, Zhao FL, Feng JY (2015b) Identification, isolation and expression analysis of heat shock transcription factors in the diploid woodland strawberry Fragaria vesca. Front Plant Sci 6:736PubMedPubMedCentralGoogle Scholar
  19. Huang Y, Li MY, Wang F, Xu ZS, Huang W, Wang GL, Ma J, Xiong AS (2015) Heat shock factors in carrot: genome-wide identification, classification, and expression profiles response to abiotic stress. Mol Biol Rep 42(5):893–905CrossRefPubMedGoogle Scholar
  20. Kantar M, Lucas SJ, Budak H (2011) Drought stress: molecular genetics and genomics approaches. Adv Bot Res 57:445–493CrossRefGoogle Scholar
  21. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) 1000 genome project data processing subgroup the sequence alignment/map format and SAM tools. Bioinformatics 25(16):2078–2079CrossRefPubMedPubMedCentralGoogle Scholar
  22. Lin YX, Jiang HYZX, 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 12:76CrossRefPubMedPubMedCentralGoogle Scholar
  23. Liu HC, Liao HT, Charng YY (2011) The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis: master heat shock factors in Arabidopsis. Plant Cell Environ 34(5):738–751CrossRefPubMedGoogle Scholar
  24. Lucas S, Durmaz E, Akpnar BA, Budak H (2011) The drought response displayed by a DRE-binding protein from Triticum dicoccoides. Plant Physiol Biochem 49(3):346–351CrossRefPubMedGoogle Scholar
  25. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH (2011) CDD. A Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39(Database issue):D225–D229CrossRefGoogle Scholar
  26. Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L (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(12):1555–1567CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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 Physiol Biochem 47(9):785–795CrossRefPubMedGoogle Scholar
  28. Ogawa D, Yamaguchi K, Nishiuchi T (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased thermotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J Exp Bot 58(12):3373–3383CrossRefPubMedGoogle Scholar
  29. Perez DE, Hoyer JS, Johnson AI, Moody ZR, Lopez L, Kaplinsky NJ (2009) BOBBER1 is an on canonical Arabidopsis small heat shock protein required for both development and thermotolerance. Plant Physiol 151(1):241–252CrossRefPubMedPubMedCentralGoogle Scholar
  30. Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819(2):104–119CrossRefGoogle Scholar
  31. Ullah N, Yüce M, Neslihan OGZ, Budak H (2017) Comparative metabolite profiling of drought stress in roots and leaves of seven Triticeae species. BMC Genomics 18(1):969CrossRefPubMedPubMedCentralGoogle Scholar
  32. Von-Koskull-Doring P, Scharf KD, Nover L (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci 12(10):452–457CrossRefPubMedGoogle Scholar
  33. Wang J, Sun N, Deng T, Zhang L, Zuo K (2014) Genome-wide cloning, identification, classification and functional analysis of cotton heat shock transcription factors in cotton (Gossypium hirsutum). BMC Genomics 15:961CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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(2):539–557CrossRefPubMedGoogle Scholar
  35. 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(3):1025–1039CrossRefPubMedGoogle Scholar
  36. 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 Omics J 7(5):291–297Google Scholar
  37. 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(5):957–967CrossRefPubMedGoogle Scholar
  38. Zahedi M, Jenner C (2003) Analysis of effects in wheat of high temperature on grain filling attributes estimated from mathematical models of grain filling. J Agric Sci 141(2):203–212CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Plant Molecular BiologyUniversity of Delhi South CampusNew DelhiIndia

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