Skip to main content
Log in

Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Histone modifications affect gene expression level. Several studies have shown that they may play key roles in regulating gene expression in plants under abiotic stress, but genome-wide surveys of such stress-related modifications are very limited, especially for crops. By using ChIP-Seq and RNA-Seq, we investigated the genome-wide distribution pattern of histone H3 lysine4 tri-methylation (H3K4me3) and the pattern’s association with whole genome expression profiles of rice (Oryza sativa L.) under drought stress, one of the major and representative abiotic stresses. We detected 51.1 and 48 % of annotated genes with H3K4me3 modification in rice seedlings under normal growth (control) and drought stress conditions, respectively. By RNA-Seq, 76.7 and 79 % of annotated genes were detected with expression in rice seedlings under the control and drought stress conditions, respectively. Furthermore, 4,837 genes were differentially H3K4me3-modified (H3M), (3,927 genes with increased H3M; 910 genes with decreased H3M) and 5,866 genes were differentially expressed (2,145 up-regulated; 3,721 down-regulated) in drought stress. Differential H3K4me3 methylation only affects a small proportion of stress-responsive genes, and the H3K4me3 modification level was significantly and positively correlated with transcript level only for a subset of genes showing changes both in modification and expression with drought stress. Moreover, for the H3K4me3-regulated stress-related genes, the H3K4me3 modification level was mainly increased in genes with low expression and decreased in genes with high expression under drought stress. The comprehensive data of H3K4me3 and gene expression profiles in rice under drought stress provide a useful resource for future epigenomic regulation studies in plants under abiotic stresses.

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
Fig. 6

Similar content being viewed by others

Abbreviations

ChIP-Seq:

Chromatin immunoprecipitation sequencing

DEGs:

Differentially expressed genes

DH3M:

Differentially H3K4me3-modified

FDR:

False discovery rate

H3M:

H3K4me3 modification levels

RNA-Seq:

RNA sequencing

RPKM:

Reads per kb per million reads

TSS:

Transcription start site

References

  • Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129:823–837

    Article  PubMed  CAS  Google Scholar 

  • Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV, Tariq M, Paszkowski J (2004) Chromatin techniques for plant cells. Plant J 39:776–789

    Article  PubMed  CAS  Google Scholar 

  • Brusslan JA, Rus Alvarez-Canterbury AM, Nair NU, Rice JC, Hitchler MJ, Pellegrini M (2012) Genome-wide evaluation of histone methylation changes associated with leaf senescence in Arabidopsis. PLoS ONE 7:e33151

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139

    Article  PubMed  CAS  Google Scholar 

  • Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163

    Article  PubMed  Google Scholar 

  • Ding Y, Lapko H, Ndamukong I, Xia Y, Al-Abdallat A, Lalithambika S, Sadder M, Saleh A, Fromm M, Riethoven JJ, Lu G, Avramova Z (2009) The Arabidopsis chromatin modifier ATX1, the myotubularin-like AtMTM and the response to drought. Plant Signal Behav 4:1049–1058

    Article  PubMed  CAS  Google Scholar 

  • Ding Y, Avramova Z, Fromm M (2011) The Arabidopsis trithorax-like factor ATX1 functions in dehydration stress responses via ABA-dependent and ABA-independent pathways. Plant J 66:735–744

    Article  PubMed  CAS  Google Scholar 

  • He GM, Zhu XP, Elling AA, Chen LB, Wang XF, Guo L, Liang MZ, He H, Zhang HY, Chen FF, Qi YJ, Chen RS, Deng XW (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33

    Article  PubMed  CAS  Google Scholar 

  • He G, Elling AA, Deng XW (2011) The epigenome and plant development. Annu Rev Plant Biol 62:411–435

    Article  PubMed  CAS  Google Scholar 

  • Henikoff S, Shilatifard A (2011) Histone modification: cause or cog? Trends Genet 27:389–396

    Article  PubMed  CAS  Google Scholar 

  • Hou X, Xie K, Yao J, Qi Z, Xiong L (2009) A homolog of human ski-interacting protein in rice positively regulates cell viability and stress tolerance. Proc Natl Acad Sci USA 106:6410–6415

    Article  PubMed  CAS  Google Scholar 

  • Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992

    Article  PubMed  CAS  Google Scholar 

  • Hu Y, Liu D, Zhong X, Zhang C, Zhang Q, Zhou DX (2012) CHD3 protein recognizes and regulates methylated histone H3 lysines 4 and 27 over a subset of targets in the rice genome. Proc Natl Acad Sci USA 109:5773–5778

    Article  PubMed  CAS  Google Scholar 

  • Huang XY, Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23:1805–1817

    Article  PubMed  CAS  Google Scholar 

  • Kim JM, 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 

  • Kim JM, To TK, Nishioka T, Seki M (2010) Chromatin regulation functions in plant abiotic stress responses. Plant Cell Environ 33:604–611

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in arabidopsis. Cell 140:136–147

    Article  PubMed  CAS  Google Scholar 

  • Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967

    Article  PubMed  CAS  Google Scholar 

  • Liu CY, Lu FL, Cui X, Cao XF (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61:395–420

    Article  PubMed  CAS  Google Scholar 

  • Luo M, Liu X, Singh P, Cui Y, Zimmerli L, Wu K (2012) Chromatin modifications and remodeling in plant abiotic stress responses. Biochim Biophys Acta 1819:129–136

    Article  PubMed  CAS  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  PubMed  CAS  Google Scholar 

  • Ndamukong I, Jones DR, Lapko H, Divecha N, Avramova Z (2010) Phosphatidylinositol 5-phosphate links dehydration stress to the activity of ARABIDOPSIS TRITHORAX-LIKE factor ATX1. PLoS ONE 5:e13396

    Article  PubMed  Google Scholar 

  • Ning J, Li XH, Hicks LM, Xiong LZ (2010) A raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol 152:876–890

    Article  PubMed  CAS  Google Scholar 

  • Petesch SJ, Lis JT (2012) Overcoming the nucleosome barrier during transcript elongation. Trends Genet 28:285–294

    Article  PubMed  CAS  Google Scholar 

  • Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, Bell GW, Walker K, Rolfe PA, Herbolsheimer E, Zeitlinger J, Lewitter F, Gifford DK, Young RA (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122:517–527

    Article  PubMed  CAS  Google Scholar 

  • Sanchez MD, Gutierrez C (2009) Arabidopsis ORC1 is a PHD-containing H3K4me3 effector that regulates transcription. Proc Natl Acad Sci USA 106:2065–2070

    Article  Google Scholar 

  • Shen H, He H, Li J, Chen W, Wang X, Guo L, Peng Z, He G, Zhong S, Qi Y, Terzaghi W, Deng XW (2012) Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 24:875–892

    Article  PubMed  CAS  Google Scholar 

  • Sokol A, Kwiatkowska A, Jerzmanowski A, Prymakowska-Bosak M (2007) Up-regulation of stress-inducible genes in tobacco and Arabidopsis cells in response to abiotic stresses and ABA treatment correlates with dynamic changes in histone H3 and H4 modifications. Planta 227:245–254

    Article  PubMed  CAS  Google Scholar 

  • Stroud H, Otero S, Desvoyes B, Ramirez-Parra E, Jacobsen SE, Gutierrez C (2012) Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proc Natl Acad Sci USA 109:5370–5375

    Article  PubMed  CAS  Google Scholar 

  • Tan MJ, Luo H, Lee S, Jin FL, Yang JS, Montellier E, Buchou T, Cheng ZY, Rousseaux S, Rajagopal N, Lu ZK, Ye Z, Zhu Q, Wysocka J, Ye Y, Khochbin S, Ren B, Zhao YM (2011) Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146:1015–1027

    Article  Google Scholar 

  • Tsuji H, Saika H, Tsutsumi N, Hirai A, Nakazono M (2006) Dynamic and reversible changes in histone H3-Lys4 methylation and H3 acetylation occurring at submergence-inducible genes in rice. Plant Cell Physiol 47:995–1003

    Article  PubMed  CAS  Google Scholar 

  • van Dijk K, Ding Y, Malkaram S, Riethoven JJ, Liu R, Yang J, Laczko P, Chen H, Xia Y, Ladunga I, Avramova Z, Fromm M (2010) Dynamic changes in genome-wide histone H3 lysine 4 methylation patterns in response to dehydration stress in Arabidopsis thaliana. BMC Plant Biol 10:238

    Article  PubMed  Google Scholar 

  • van Steensel B (2011) Chromatin: constructing the big picture. EMBO J 30:1885–1895

    Article  PubMed  Google Scholar 

  • Vining KJ, Pomraning KR, Wilhelm LJ, Priest HD, Pellegrini M, Mockler TC, Freitag M, Strauss SH (2012) Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression. BMC Genomics 13:27

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Elling AA, Li X, Li N, Peng Z, He G, Sun H, Qi Y, Liu XS, Deng XW (2009) Genome-wide and organ-specific landscapes of epigenetic modifications and their relationships to mRNA and small RNA transcriptomes in maize. Plant Cell 21:1053–1069

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Xie W, Chen Y, Tang W, Yang J, Ye R, Liu L, Lin Y, Xu C, Xiao J, Zhang Q (2010) A dynamic gene expression atlas covering the entire life cycle of rice. Plant J 61:752–766

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Zhang Y, Zhang H, Huang H, Folta KM, Lu J (2010) Whole genome wide expression profiles of Vitis amurensis grape responding to downy mildew by using Solexa sequencing technology. BMC Plant Biol 10:234

    Article  PubMed  Google Scholar 

  • Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952

    Article  PubMed  CAS  Google Scholar 

  • Xiao B, Huang Y, Tang N, Xiong L (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor Appl Genet 115:35–46

    Article  PubMed  CAS  Google Scholar 

  • Yang S, Vanderbeld B, Wan J, Huang Y (2010) Narrowing down the targets: towards successful genetic engineering of drought-tolerant crops. Mol Plant 3:469–490

    Article  PubMed  CAS  Google Scholar 

  • Yun MY, Wu J, Workman JL, Li B (2011) Readers of histone modifications. Cell Res 21:564–578

    Article  PubMed  CAS  Google Scholar 

  • Zhang QF (2007) Strategies for developing green super rice. Proc Natl Acad Sci USA 104:16402–16409

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126:1189–1201

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9:R137

    Article  PubMed  Google Scholar 

  • Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE (2009) Genome-wide analysis of mono-, di- and tri-methylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10:R62

    Article  PubMed  Google Scholar 

  • Zhang Z, Zhang S, Zhang Y, Wang X, Li D, Li Q, Yue M, Zhang YE, Xu Y, Xue Y, Chong K, Bao S (2011) Arabidopsis floral initiator SKB1 confers high salt tolerance by regulating transcription and pre-mRNA splicing through altering histone H4R3 and small nuclear ribonucleoprotein LSM4 methylation. Plant Cell 23:396–411

    Article  PubMed  Google Scholar 

  • Zhang W, Wu Y, Schnable JC, Zeng Z, Freeling M, Crawford GE, Jiang J (2012a) High-resolution mapping of open chromatin in the rice genome. Genome Res 22:151–162

    Article  PubMed  CAS  Google Scholar 

  • Zhang W, Zhang T, Wu Y, Jiang J (2012b) Genome-wide identification of regulatory DNA elements and protein-binding footprints using signatures of open chromatin in Arabidopsis. Plant Cell 24:2719–2731

    Article  PubMed  CAS  Google Scholar 

  • Zhou DX (2009) Regulatory mechanism of histone epigenetic modifications in plants. Epigenetics 4:15–18

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Professor Dao-Xiu Zhou for constructive suggestions. This work was supported by grants from the National Program for Basic Research of China (2012CB114305), the National Program on High Technology Development (2012AA10A303), and the National Natural Science Foundation of China (30725021 and 30921091).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lizhong Xiong.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zong, W., Zhong, X., You, J. et al. Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress. Plant Mol Biol 81, 175–188 (2013). https://doi.org/10.1007/s11103-012-9990-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-012-9990-2

Keywords

Navigation