Skip to main content
SpringerLink
Log in

Significant induction by drought of HvPKDM7-1, a gene encoding a jumonji-like histone demethylase homologue in barley (H. vulgare)

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Reversible histone methylations of the fourth lysine on histone 3 (H3K4) are key epigenetic marks, involved in establishing and maintaining epigenetic transcriptional states of genes during normal development and in response to environmental stresses like drought. Their dynamic regulation is modulated by a complex mechanism employing specific epigenetic factors such as histone lysine methyltransferases and the counteracting histone demethylases. The identification and characterization of such drought-responsive epigenetic factors involved in H3K4 methylation in temperate cereal crops would provide a major advantage in their breeding for higher yield. For better understanding these mechanisms and their implication in drought stress tolerance in the annual cereal crop barley (Hordeum vulgare L.), we have isolated, cloned and characterized a drought-induced PKDM7 subfamily-like H3K4 demethylase homologue, designated HvPKDM7-1. The complete cDNA clone obtained using the RCA-RACE (Rolling Circle Amplification-RACE) method, contained a 3,861 bp ORF encoding the 1,287 a.a. putative protein, which includes conserved residues compatible with the demethylation activity. Comparative genomic analysis enabled us to locate the gene on locus 3260 on the long arm of the barley chromosome 1H. Constant transcript accumulation in early barley seed development was followed by almost complete silencing, coinciding with the stage of active storage of proteins. Transcript induction by drought stress was observed in two barley cultivars and was considerably higher in the drought-tolerant cultivar, indicating that HvPKDM7-1 may be actively involved in drought tolerance control, an agronomically very important trait.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alvarez-Venegas R, Avramova Z (2001) Two Arabidopsis homologs of the animal trithorax genes: a new structural domain is a signature feature of the trithorax gene family. Gene 271:215–221

    Article  PubMed  CAS  Google Scholar 

  • Avramova Z (2009) Evolution and pleiotropy of TRITHORAX function in Arabidopsis. Int J Dev Biol 53:371–381

    Article  PubMed  CAS  Google Scholar 

  • Boavida LC, Shuai B, Yu H-J, Pagnussat GC, Sundaresan V, Mccormick S (2009) A collection of Ds insertional mutants associated with defects in male gametophyte development and function in Arabidopsis thaliana. Genetics 181:1369–1385

    Article  PubMed  CAS  Google Scholar 

  • Chen G, Krugman T, Fahima T, Chen K, Hu Y, Röder M, Nevo E, Korol A (2010) Chromosomal regions controlling seedling drought resistance in Israeli wild barley, Hordeum spontaneum C. Koch. Genet Resour Crop Evol 57:85–99

    Article  Google Scholar 

  • Close TJ, Wing R, Kleinhofs A, Wise R (2001) Establishment of genetically and physically anchored EST resources for barley genomics. Barley Genet Newslett 31:29–30

    Google Scholar 

  • Comadran J, Russell J, Van Eeuwijk F, Ceccarelli S, Grando S, Baum M, Stanca A, Pecchioni N, Mastrangelo A, Akar T, Al-Yassin A, Benbelkacem A, Choumane W, Ouabbou H, Dahan R, Bort J, Araus JL, Pswarayi A, Romagosa I, Hackett C, Thomas W (2008) Mapping adaptation of barley to droughted environments. Euphytica 161:35–45

    Article  Google Scholar 

  • Deleris A, Greenberg MVC, Ausin I, Law RWY, Moissiard G, Schubert D, Jacobsen SE (2010) Involvement of a Jumonji-C domain-containing histone demethylase in DRM2-mediated maintenance of DNA methylation. EMBO Rep 11:950–955

    Article  PubMed  CAS  Google Scholar 

  • Demetriou K, Kapazoglou A, Bladenopoulos K, Tsaftaris A (2010) Epigenetic chromatin modifiers in barley: II. characterization and expression analysis of the HDA1 family of barley histone deacetylases during development and in response to jasmonic acid. Plant Mol Biol Rep 28:9–21

    Article  CAS  Google Scholar 

  • Demetriou K, Kapazoglou A, Tondelli A, Francia E, Stanca MA, Bladenopoulos K, Tsaftaris AS (2009) Epigenetic chromatin modifiers in barley: I. cloning, mapping and expression analysis of the plant specific HD2 family of histone deacetylases from barley, during seed development and after hormonal treatment. Physiol Plant 136:358–368

    Article  PubMed  CAS  Google Scholar 

  • Dong Q, Lawrence CJ, Schlueter SD, Wilkerson MD, Kurtz S, Lushbough C, Brendel V (2005) Comparative plant genomics resources at PlantGDB. Plant Physiol 139:610–618

    Article  PubMed  CAS  Google Scholar 

  • Feuillet C, Langridge P, Waugh R (2008) Cereal breeding takes a walk on the wild side. Trends Genet 24:24–32

    Article  PubMed  CAS  Google Scholar 

  • Fortschegger K, Shiekhattar R (2011) Plant homeodomain fingers form a helping hand for transcription. Epigenetics 6:4–8

    Article  PubMed  CAS  Google Scholar 

  • Govind G, Vokkaliga Thammegowda H, Jayaker Kalaiarasi P, Iyer D, Muthappa S, Nese S, Makarla U (2009) Identification and functional validation of a unique set of drought induced genes preferentially expressed in response to gradual water stress in peanut. Mol Genet Genomics 281:591–605

    Article  PubMed  CAS  Google Scholar 

  • Guo P, Baum M, Grando S, Ceccarelli S, Bai G, Li R, Von Korff M, Varshney RK, Graner A, Valkoun J (2009) Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. J Exp Bot 60:3531–3544

    Article  PubMed  CAS  Google Scholar 

  • Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447:418–424

    Article  PubMed  CAS  Google Scholar 

  • Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bork P, Das U, Daugherty L, Duquenne L, Finn RD, Gough J, Haft D, Hulo N, Kahn D, Kelly E, Laugraud A, Letunic I, Lonsdale D, Lopez R, Madera M, Maslen J, Mcanulla C, Mcdowall J, Mistry J, Mitchell A, Mulder N, Natale D, Orengo C, Quinn AF, Selengut JD, Sigrist CJA, Thimma M, Thomas PD, Valentin F, Wilson D, Wu CH, Yeats C (2009) InterPro: the integrative protein signature database. Nucl Acids Res 37:D211–D215

    Article  PubMed  CAS  Google Scholar 

  • Jaiswal P (2006) Gramene: a bird’s eye view of cereal genomes. Nucl Acids Res 34:D717–D723

    Article  PubMed  CAS  Google Scholar 

  • Jarillo JA, Piñeiro M, Cubas P, Martínez-Zapater JM (2009) Chromatin remodeling in plant development. Int J Dev Biol 53:1581–1596

    Article  PubMed  CAS  Google Scholar 

  • Jeong J-H, Song H-R, Ko J-H, Jeong Y-M, Kwon YE, Seol JH, Amasino RM, Noh B, Noh Y-S (2009) Repression of FLOWERING LOCUS T chromatin by functionally redundant histone H3 lysine 4 demethylases in Arabidopsis. PLoS One 4:e8033

    Article  PubMed  Google Scholar 

  • Jiang D, Kong NC, Gu X, Li Z, He Y (2011) Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet 7:e1001330

    Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    PubMed  CAS  Google Scholar 

  • Kapazoglou A, Papaefthimiou D, Tsaftaris AS (in print) Histone modifiers in cereals. In: Shen C-H (ed) Histones: class, structure and function, chap 6. Nova Science Publishers, Hauppauge

  • Kapazoglou A, Tondelli A, Papaefthimiou D, Ampatzidou H, Francia E, Stanca M, Bladenopoulos K, Tsaftaris A (2010) Epigenetic chromatin modifiers in barley: IV. The study of barley Polycomb group (PcG) genes during seed development and in response to external ABA. BMC Plant Biol 10:73

    Google Scholar 

  • Karlić R, Chung H-R, Lasserre J, Vlahoviček K, Vingron M (2010) Histone modification levels are predictive for gene expression. Proc Natl Acad Sci USA 107:2926–2931

    Article  PubMed  Google Scholar 

  • Kim J-M, To TK, Ishida J, Morosawa T, Kawashima M, Matsui A, Toyoda T, Kimura H, Shinozaki K, Seki M (2008) Alterations of lysine modifications on the histone H3N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol 49:1580–1588

    Article  PubMed  CAS  Google Scholar 

  • Klose RJ, Kallin EM, Zhang Y (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7:715–727

    Article  PubMed  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA, Mcwilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Lu F, Cui X, Zhang S, Liu C, Cao X (2010) JMJ14 is an H3K4 demethylase regulating flowering time in Arabidopsis. Cell Res 20:387–390

    Article  PubMed  Google Scholar 

  • Lu F, Li G, Cui X, Liu C, Wang X-J, Cao X (2008) Comparative analysis of JmjC domain-containing proteins reveals the potential histone demethylases in Arabidopsis and rice. J Integr Plant Biol 50:886–896

    Article  PubMed  CAS  Google Scholar 

  • Mayer KFX, Martis M, Hedley PE, Šimková H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, Kubaláková M, Suchánková P, Murat F, Felder M, Nussbaumer T, Graner A, Salse J, Endo T, Sakai H, Tanaka T, Itoh T, Sato K, Platzer M, Matsumoto T, Scholz U, Doležel J, Waugh R, Stein N (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23(4):1249–1263

    Google Scholar 

  • Mayer KFX, Taudien S, Martis M, Simkova H, Suchankova P, Gundlach H, Wicker T, Petzold A, Felder M, Steuernagel B, Scholz U, Graner A, Platzer M, Dolezel J, Stein N (2009) Gene content and virtual gene order of barley chromosome 1H. Plant Physiol 151:496–505

    Article  PubMed  CAS  Google Scholar 

  • Mazzucotelli E, Mastrangelo AM, Crosatti C, Guerra D, Stanca AM, Cattivelli L (2008) Abiotic stress response in plants: when post-transcriptional and post-translational regulations control transcription. Plant Sci 174:420–431

    Article  CAS  Google Scholar 

  • Nottke A, Colaiacovo MP, Shi Y (2009) Developmental roles of the histone lysine demethylases. Development 136:879–889

    Article  PubMed  CAS  Google Scholar 

  • Ozturk ZN, Talamé V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551–573

    Article  CAS  Google Scholar 

  • Page RDM (2002) Visualizing phylogenetic trees using TreeView. Curr Protoc Bioinformatics 6.2.1–6.2.15

  • Papaefthimiou D, Likotrafiti E, Kapazoglou A, Bladenopoulos K, Tsaftaris A (2010) Epigenetic chromatin modifiers in barley: III. isolation and characterization of the barley GNAT-MYST family of histone acetyltransferases and responses to exogenous ABA. Plant Physiol Biochem 48:98–107

    Article  PubMed  CAS  Google Scholar 

  • Papaefthimiou D,Tsaftaris A (in print) Characterization of a drought inducible trithorax-like H3K4 methyltransferase from barley. Biol Plant (Prague)

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucl Acids Res 30:e36

    Article  PubMed  Google Scholar 

  • Pfluger J, Wagner D (2007) Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol 10:645–652

    Article  PubMed  CAS  Google Scholar 

  • Pien S, Fleury D, Mylne JS, Crevillen P, Inze D, Avramova Z, Dean C, Grossniklaus U (2008) ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20:580–588

    Article  PubMed  CAS  Google Scholar 

  • Polidoros AN, Pasentsis K, Tsaftaris AS (2006) Rolling circle amplification-RACE: a method for simultaneous isolation of 5′ and 3′ cDNA ends from amplified cDNA templates. BioTechniques 41:35–42

    Article  PubMed  CAS  Google Scholar 

  • Prioul JL, Méchin V, Lessard P, Thévenot C, Grimmer M, Chateau-Joubert S, Coates S, Hartings H, Kloiber-Maitz M, Murigneux A, Sarda X, Damerval C, Edwards KJ (2008) A joint transcriptomic, proteomic and metabolic analysis of maize endosperm development and starch filling. Plant Biotechnol J 6:855–869

    Article  PubMed  CAS  Google Scholar 

  • Proost S, Van Bel M, Sterck L, Billiau K, Van Parys T, Van De Peer Y, Vandepoele K (2009) PLAZA: a comparative genomics resource to study gene and genome evolution in plants. Plant Cell 21:3718–3731

    Article  PubMed  CAS  Google Scholar 

  • Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X (2009) DOG 1.0: illustrator of protein domain structures. Cell Res 19:271–273

    Article  PubMed  CAS  Google Scholar 

  • Rolletschek H, Weschke W, Weber H, Wobus U, Borisjuk L (2004) Energy state and its control on seed development: starch accumulation is associated with high ATP and steep oxygen gradients within barley grains. J Exp Bot 55:1351–1359

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Ruthenburg AJ, Allis CD, Wysocka J (2007) Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol Cell 25:15–30

    Article  PubMed  CAS  Google Scholar 

  • Sabelli PA, Larkins BA (2009) The development of endosperm in grasses. Plant Physiol 149:14–26

    Article  PubMed  CAS  Google Scholar 

  • Schulte D, Close TJ, Graner A, Langridge P, Matsumoto T, Muehlbauer G, Sato K, Schulman AH, Waugh R, Wise RP, Stein N (2009) The International Barley Sequencing Consortium-at the threshold of efficient access to the barley genome. Plant Physiol 149:142–147

    Article  PubMed  CAS  Google Scholar 

  • Searle IR, Pontes O, Melnyk CW, Smith LM, Baulcombe DC (2010) JMJ14, a JmjC domain protein, is required for RNA silencing and cell-to-cell movement of an RNA silencing signal in Arabidopsis. Genes Dev 24:986–991

    Article  PubMed  CAS  Google Scholar 

  • Sreenivasulu N, Usadel B, Winter A, Radchuk V, Scholz U, Stein N, Weschke W, Strickert M, Close TJ, Stitt M, Graner A, Wobus U (2008) Barley grain maturation and germination: metabolic pathway and regulatory network commonalities and differences highlighted by new MapMan/PageMan profiling tools. Plant Physiol 146:1738–1758

    Article  PubMed  CAS  Google Scholar 

  • Suprunova T, Krugman T, Distelfeld A, Fahima T, Nevo E, Korol A (2007) Identification of a novel gene (Hsdr4) involved in water-stress tolerance in wild barley. Plant Mol Biol 64:17–34

    Article  PubMed  CAS  Google Scholar 

  • Talame V, Ozturk NZ, Bohnert HJ, Tuberosa R (2007) Barley transcript profiles under dehydration shock and drought stress treatments: a comparative analysis. J Exp Bot 58:229–240

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822

    Article  PubMed  CAS  Google Scholar 

  • Teulat B, Borries C, This D (2001) New QTLs identified for plant water status, water-soluble carbohydrate and osmotic adjustment in a barley population grown in a growth-chamber under two water regimes. Theor Appl Genet 103:161–170

    Article  CAS  Google Scholar 

  • Teulat B, Monneveux P, Wery J, Borries C, Souyris I, Charrier A, This D (1997) Relationships between relative water content and growth parameters under water stress in barley: a QTL study. New Phytol 137:99–107

    Article  Google Scholar 

  • Teulat B, Zoumarou-Wallis N, Rotter B, Ben Salem M, Bahri H, This D (2003) QTL for relative water content in field-grown barley and their stability across Mediterranean environments. Theor Appl Genet 108:181–188

    Article  PubMed  CAS  Google Scholar 

  • Von Korff M, Grando S, Del Greco A, This D, Baum M, Ceccarelli S (2008) Quantitative trait loci associated with adaptation to Mediterranean dryland conditions in barley. Theor Appl Genet 117:653–669

    Article  Google Scholar 

  • Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191

    Article  PubMed  CAS  Google Scholar 

  • Yang W, Jiang D, Jiang J, He Y (2010) A plant-specific histone H3 lysine 4 demethylase represses the floral transition in Arabidopsis. Plant J 62:663–673

    Article  PubMed  CAS  Google Scholar 

  • Zhou X, Ma H (2008) Evolutionary history of histone demethylase families: distinct evolutionary patterns suggest functional divergence. BMC Evol Biol 8:294

    Google Scholar 

Download references

Acknowledgments

We would like to thank Dr. Bladenopoulos (NAGREF) for kindly providing plant material, Dr. Kapazoglou (INA) for useful discussions and Mr. Pasentzis (INA) for all his help and advice in this work. This work was supported by a PENED grant (Ο3ΕΔ402/2003). Continuous support for INA/CERTH from the General Secretariat of Research and Technology of Greece is also acknowledged.

Author information

Author notes

  1. Dimitra Papaefthimiou

    Present address: Department of Pharmaceutical Sciences, Aristotle University of Thessaloniki, 54124, Thessaloniki, Greece

Authors and Affiliations

  1. Institute of Agrobiotechnology (INA), CERTH, Thermi-Thessaloniki, 57001, Greece

    Dimitra Papaefthimiou & Athanasios S. Tsaftaris

  2. Department of Genetics and Plant Breeding, Aristotle University of Thessaloniki, Thessaloniki, 54124, Greece

    Athanasios S. Tsaftaris

Authors
  1. Dimitra Papaefthimiou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Athanasios S. Tsaftaris
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Athanasios S. Tsaftaris.

Additional information

Communicated by Y. Wang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Figure S1 Illustration of the barley chromosome 1H with locus 3260 containing hvpkdm7-1 highlighted. (TIFF 120 kb)

11738_2011_915_MOESM2_ESM.tif

Supplementary material Figure S2 Graphs illustrating the relative expression of the barley transcripts HvPKDM7-1 and Hsdr4 under drought stress in the cultivars Demetra (drought tolerant) and Caresse (intermediate drought tolerance) during a 10 day period, plotted against relative water content. (TIFF 459 kb)

Supplementary Table (DOC 49 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Papaefthimiou, D., Tsaftaris, A.S. Significant induction by drought of HvPKDM7-1, a gene encoding a jumonji-like histone demethylase homologue in barley (H. vulgare). Acta Physiol Plant 34, 1187–1198 (2012). https://doi.org/10.1007/s11738-011-0915-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-011-0915-5

Keywords

Search

Navigation