Skip to main content
Log in

Comparative Genome-Wide Analysis and Expression Profiling of Histone Acetyltransferases and Histone Deacetylases Involved in the Response to Drought in Wheat

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Histone acetyltransferases (HATs) and histone deacetylases (HDACs) contribute to plant growth, development, and stress responses. A number of HAT and HDAC genes have been identified in several plants. However, wheat HATs and HDACs have not been comprehensively characterized. In this study, 30 TaHAT genes and 53 TaHDAC genes were detected in the wheat genome. As described in other plants, TaHATs were classified into four subfamilies (i.e., GNAT, p300/CBP, MYST, and TAFII250) and TaHDACs were divided into three subfamilies (i.e., RPD3/HDA1, HD2, and SIR2). Phylogenetic and conserved domain analyses showed that TaHATs and TaHDACs are highly similar to those in Arabidopsis and rice; however, divergence and expansion from Arabidopsis and rice were also observed. We detected many stress-related cis-regulatory elements in the promoter regions of these genes (i.e., ABRE, STRE, MYB, etc.). Further, based on a comparative expression analyses of three varieties with different degrees of drought resistance under drought stress, we found that TaHAG2, TaHAG3, TaHAC2, TaHDA18, TaHDT1, and TaHDT2 are likely regulate drought stress in wheat.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

HATs:

Histone acetyltransferases

HDACs:

Histone deacetylases

GNAT:

GCN5-related N-terminal acetyltransferase

p300/CBP:

CREB-binding protein

MYST:

MOZ, Ybf2/Sas3, Sas2, and Tip60

TAFII250:

TATA-binding protein-associated factors

RPD3/HDA1:

Reduced Potassium Dependency 3/Histone DeAcetylase 1

SIR2:

Silent Information Regulator 2

HD2:

Histone Deacetylase 2

pI:

The theoretical isoelectronic point

ABRE:

Abscisic acid-responsive element

STRE:

Stress-responsive element

ARE:

Essential for anaerobic induction

CCGTCC-box:

Meristem-specific activation

G-Box:

Light responsiveness

MYB:

MYB-related binding sites

TGA-element:

Auxin-responsive element

PSII:

Photosystem II

LHCb:

Light-harvesting chlorophyll a/b-binding proteins

References

  • Allis CD, Jenuwein T (2016) The molecular hallmarks of epigenetic control. Nat Rev Genet 17:487–500

    Article  CAS  PubMed  Google Scholar 

  • Aquea F, Timmermann T, Arce-Johnson P (2010) Analysis of histone acetyltransferase and deacetylase families of Vitis vinifera. Plant Physiol Bioch 48:194–199

    Article  CAS  Google Scholar 

  • Bienz M (2006) The PHD finger, a nuclear protein-interaction domain. Trends Biochem Sci 31:35–40

    Article  CAS  PubMed  Google Scholar 

  • Chen LT, Wu K (2010) Role of histone deacetylases HDA6 and HDA19 in ABA and abiotic stress response. Plant Signal Behav 5:1318–1320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, HeY XR (2020) TBtools-an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Cohen R, Schocken J, Kaldis A, Vlachonasios KE, Hark AT, McCain ER (2009) The histone acetyltransferase GCN5 affects the inflorescence meristem and stamen development in Arabidopsis. Planta 230:1207–1221

    Article  CAS  PubMed  Google Scholar 

  • Ekwall K (2005) Genome-wide analysis of HDAC function. Trends Genet 21:608–615

    Article  CAS  PubMed  Google Scholar 

  • Gamsjaeger R, Liew CK, Loughlin FE, Crossley M, Mackay JP (2007) Sticky fingers: zinc-fingers as protein-recognition motifs. Trends Biochem Sci 32:63–70

    Article  CAS  PubMed  Google Scholar 

  • Garrido J, Aguilar M, Prieto P (2020) Identification and validation of reference genes for RT-qPCR normalization in wheat meiosis. Sci Rep 10:1–12

    Article  CAS  Google Scholar 

  • Gasteiger E, Hoogland C, Gattiker A, Wilkins M, Appel R, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, Totowa, pp 571–607

    Chapter  Google Scholar 

  • Hassig CA, Schreiber SL (1997) Nuclear histone acetylases and deacetylases and transcriptional regulation: HATs off to HDACs. Curr Opin Chem Biol 1:300–308

    Article  CAS  PubMed  Google Scholar 

  • Hollender C, Liu Z (2008) Histone deacetylase genes in Arabidopsis development. J Integr Plant Biol 50:875–885

    Article  CAS  PubMed  Google Scholar 

  • Horton P, Park K, Obayashi T, Fujita N, Harada H, Adams-Collier C, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35(suppl_2):585–587

    Article  Google Scholar 

  • Hu Y, Qin F, Huang L, Sun Q, Li C, Zhao Y, Zhou DX (2009) Rice histone deacetylase genes display specific expression patterns and developmental functions. Biochem Bioph Res Co 388:266–271

    Article  CAS  Google Scholar 

  • Hu Z, Song N, Zheng M, Liu X, Liu Z, Xing J et al (2015) Histone acetyltransferase GCN 5 is essential for heat stress-responsive gene activation and thermotolerance in Arabidopsis. Plant J 84:1178–1191

    Article  CAS  PubMed  Google Scholar 

  • Imran M, Shafiq S, Farooq MA, Naeem MK, Widemann E, Bakhsh A et al (2019) Comparative genome-wide analysis and expression profiling of histone acetyltransferase (HAT) gene family in response to hormonal applications, metal and abiotic stresses in cotton. Int J Mol Sci 20:5311

    Article  CAS  PubMed Central  Google Scholar 

  • Imran M, Shafiq S, Naeem MK, Widemann E, Munir MZ, Jensen KB, Wang R (2020) Histone Deacetylase (HDAC) gene family in Allotetraploid cotton and its diploid progenitors silico identification molecular characterization, and gene expression analysis under multiple abiotic stresses DNA damage and phytohormone treatments. Int J Mol Sci 21(1):321

    Article  CAS  PubMed Central  Google Scholar 

  • Jiang J, Ding AB, Liu F, Zhong X (2020) Linking signaling pathways to histone acetylation dynamics in plants. J Exp Bot 71:5179–5190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705

    Article  CAS  PubMed  Google Scholar 

  • Li S, Lin Y, Wang P, Zhang B, Li M, Chen S et al (2019) The AREB1 transcription factor influences histone acetylation to regulate drought responses and tolerance in Populus trichocarpa. Plant Cell 31:663–686

    Article  CAS  PubMed  Google Scholar 

  • Liew LC, Singh MB, Bhalla PL (2013) An RNA-seq transcriptome analysis of histone modifiers and RNA silencing genes in soybean during floral initiation process. PLoS ONE 8:e77502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Luo M, Zhang W, Zhao J, Zhang J, Wu K et al (2012) Histone acetyltransferases in rice (Oryza sativa L.): phylogenetic analysis subcellular localization and expression. BMC Plant Biol 12(1):145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma X, Zhang B, Liu C, Tong B, Guan T, Xia D (2017) Expression of a populus histone deacetylase gene 84KHDA903 in tobacco enhances drought tolerance. Plant Sci 265:1–11

    Article  CAS  PubMed  Google Scholar 

  • Marmorstein R, Berger SL (2001) Structure and function of bromodomains in chromatin-regulating complexes. Gene 272:1–9

    Article  CAS  PubMed  Google Scholar 

  • Mehdi S, Derkacheva M, Ramström M, Kralemann L, Bergquist J, Hennig L (2016) The WD40 domain protein MSI1 functions in a histone deacetylase complex to fine-tune abscisic acid signaling. Plant Cell 28:42–54

    Article  CAS  PubMed  Google Scholar 

  • Nallamilli BR, Edelmann MJ, Zhong X, Tan F, Mujahid H, Zhang J, Nanduri B, Peng Z (2014) Global analysis of lysine acetylation suggests the involvement of protein acetylation in diverse biological processes in rice (Oryza sativa). PLoS ONE 9:e89283

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Onufriev AV, Schiessel H (2019) The nucleosome: from structure to function through physics. Curr Opin Struc Biol 56:119–130

    Article  CAS  Google Scholar 

  • Pandey R, MuÈller A, Napoli CA, Selinger DA, Pikaard CS, Richards EJ et al (2002) Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic acids Res 30:5036–5055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng M, Ying P, Liu X, Li C, Xia R, Li J, Zhao M (2017) Genome-wide identification of histone modifiers and their expression patterns during fruit abscission in Litchi. Front Plant Sci 8:639

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L et al (2018) The transcriptional landscape of polyploid wheat. Science 361:662

    Article  CAS  Google Scholar 

  • Servet C, Silva NCe, Zhou DX (2010) Histone acetyltransferase AtGCN5/HAG1 is a versatile regulator of developmental and inducible gene expression in Arabidopsis. Mol Plant 3:670–677

    Article  CAS  PubMed  Google Scholar 

  • Shahbazian M, Grunstein M (2007) Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 76:75–100

    Article  CAS  PubMed  Google Scholar 

  • Song J, Henry HA, Tian L (2019) Brachypodium histone deacetylase BdHD1 positively regulates ABA and drought stress responses. Plant Sci 283:355–365

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan S, Gao L, Li T, Chen L (2019) Phylogenetic and expression analysis of histone acetyltransferases in Brachypodium distachyon. Genomics 111:1966–1976

    Article  CAS  PubMed  Google Scholar 

  • Ueda M, Seki M (2020) Histone modifications form epigenetic regulatory networks to regulate abiotic stress response. Plant Physiol 182:15–26

    Article  CAS  PubMed  Google Scholar 

  • Ueda M, Matsui A, Tanaka M, Nakamura T, Abe T, Sako K et al (2017) The distinct roles of class I and II RPD3-like histone deacetylases in salinity stress response. Plant Physiol 175:1760–1773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueda M, Matsui A, Nakamura T, Abe T, Sunaoshi Y, Shimada H, Seki M (2018) Versatility of HDA19-deficiency in increasing the tolerance of Arabidopsis to different environmental stresses. Plant Signal Behav 13:e1475808

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Cao H, Chen F, Liu Y (2014) The roles of histone acetylation in seed performance and plant development. Plant Physiol Bioch 84:125–133

    Article  CAS  Google Scholar 

  • Wu X, Oh MH, Schwarz EM, Larue CT, Sivaguru M, Imai BS et al (2011) Lysine acetylation is a widespread protein modification for diverse proteins in Arabidopsis. Plant Physiol 155:1769–1778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao J, Zhang H, Xing L, Xu S, Liu H, Chong K, Xu Y (2013) Requirement of histone acetyltransferases HAM1 and HAM2 for epigenetic modification of FLC in regulating flowering in Arabidopsis. J Plant Physiol 170:444–451

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Xu H, Liu Y, Wang X, Xu Q, Deng X (2015) Genome-wide identification of sweet orange (Citrus sinensis) histone modification gene families and their expression analysis during the fruit development and fruit-blue mold infection process. Front Plant Sci 6:607

    Article  PubMed  PubMed Central  Google Scholar 

  • Xue C, Liu S, Chen C, Zhu J, Yang X, Zhou Y et al (2018) Global proteome analysis links lysine acetylation to diverse functions in Oryza sativa. Proteomics 18:1700036

    Article  CAS  Google Scholar 

  • Yu X, Gao Q, Chen G, Guo JE, Guo X, Tang B, Hu Z (2018) SlHDA5, a tomato histone deacetylase gene, is involved in responding to salt, drought, and ABA. Plant Mol Biol Rep 36:36–44

    Article  CAS  Google Scholar 

  • van Zanten M, Zöll C, Wang Z, Philipp C, Carles A, Li Y et al (2014) HISTONE DEACETYLASE 9 represses seedling traits in Arabidopsis thaliana dry seeds. Plant J 80:475–488

    Article  PubMed  CAS  Google Scholar 

  • Zhang JB, He SP, Luo JW, Wang XP, Li DD, Li XB (2020) A histone deacetylase, GhHDT4D, is positively involved in cotton response to drought stress. Plant Mol Biol 104:67–79

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Lu J, Zhang J, Wu PY, Yang S, Wu K (2015) Identification and characterization of histone deacetylases in tomato (Solanum lycopersicum). Front Plant Sci 5:760

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Li M, Gu D, Liu X, Zhang J, Wu K, Zhang X, Teixeira da Silva J, Duan J (2016) Involvement of rice histone deacetylase HDA705 in seed germination and in response to ABA and abiotic stresses. Biochem Bioph Res Co 470:439–444

    Article  CAS  Google Scholar 

  • Zhao T, Zhan Z, Jiang D (2019) Histone modifications and their regulatory roles in plant development and environmental memory. J Genet Genomics 46:467–476

    Article  PubMed  Google Scholar 

  • Zheng Y, Ding Y, Sun X, Xie S, Wang D, Liu X, Su L, Lei Pan W, Zhou DX (2016) Histone deacetylase HDA9 negatively regulates salt and drought stress responsiveness in Arabidopsis. J Exp Bot 67:1703–1713

    Article  CAS  PubMed  Google Scholar 

  • Zheng M, Liu X, Lin J, Liu X, Wang Z, Xin M et al (2019) Histone acetyltransferase GCN 5 contributes to cell wall integrity and salt stress tolerance by altering the expression of cellulose synthesis genes. Plant J 97:587–602

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Key Research and Development Program of China (Grant No. 2017YFD0300408) and Natural Science Foundation of Henan Province (Grant No. 212300410352).

Author information

Authors and Affiliations

Authors

Contributions

HL designed the experiments and wrote the manuscript. HL and HJL carried out the bioinformatics analysis. XXP and HYC performed the biological experiment. XL and JRW prepared the plant sample. CYW helped revise the manuscript. All the authors read and approved the final manuscript.

Corresponding authors

Correspondence to Hua Li or Chenyang Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no competing financial interests.

Additional information

Handling Editor: Rhonda Peavy.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, H., Liu, H., Pei, X. et al. Comparative Genome-Wide Analysis and Expression Profiling of Histone Acetyltransferases and Histone Deacetylases Involved in the Response to Drought in Wheat. J Plant Growth Regul 41, 1065–1078 (2022). https://doi.org/10.1007/s00344-021-10364-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-021-10364-9

Keywords

Navigation