Skip to main content
SpringerLink
Log in

Dynamic changes in histone modification are associated with upregulation of Hsf and rRNA genes during heat stress in maize seedlings

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Histone modification plays a significant role in plant responses to abiotic stress. However, there are little scientific studies available on the involvement of dynamic changes in histone modification in the heat stress response in maize. The present investigation was aimed to analyze the epigenetic mechanisms involved in regulating the physiological and biochemical alterations in maize seedlings under heat stress. Our results and observations indicated an increase in electrolyte leakage and hydrolytic activity of the plasma membrane H+-ATPase as well as the high pigment content and reactive oxygen species (ROS) content under high temperature. Furthermore, decondensation of ribosomal DNA (rDNA) chromatin and a simultaneous increase in rRNA gene expression were observed during heat stress, accompanied by a genome-wide increase in the levels of histone H3K4me2 and H3K9ac. Additionally, chromatin immunoprecipitation (ChIP) analysis revealed that alterations in H3K4me2 and H3K9ac levels occurred in promoter regions, which were found to be associated with the upregulation of heat stress factor (Hsf) and rRNA genes. In conclusion, short-term heat stress induces dynamic histone alterations which are associated with Hsf and rRNA gene transcription, accompanied by perturbations of cell membranes and an increase in ROS during acclimation in maize seedlings.

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
Fig. 6

Similar content being viewed by others

References

  • Ahuja I, de Vos RC, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15:664–674

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-venegas R, Avramova Z (2005) Methylation patterns of histone H3 Lys 4, Lys 9 and Lys 27 in transcriptionally active and inactive Arabidopsis genes and in atx1 mutants. Nucleic Acids Res 33:5199–5220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aufsatz W, Mette MF, van der Winden J, Matzke M, Matzke AJ (2002) HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J 21:6832–6841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baerenfaller K, Shu H, Hirsch-Hoffmann M, Fütterer J, Opitz L, Rehrauer H (2016) Diurnal changes in the histone h3 signature h3k9ac|h3k27ac|h3s28p are associated with diurnal gene expression in Arabidopsis. Plant Cell Environ 39:2557–2569

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Beers RF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    CAS  PubMed  Google Scholar 

  • Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273–284

    Article  PubMed  PubMed Central  Google Scholar 

  • Blum A, Ebercon A (1981) Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Sci 21:43–47

    Article  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Briantais JM, Dacosta J, Goulas Y, Ducruet JM, Moya I (1996) Heat stress induces in leaves an increase of the minimum level of chlorophyll fluorescence, Fo: a time-resolved analysis. Photosynth Res 48:189–196

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conde A, Chaves MM, Gerós H (2011) Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol 52:1583–1602

    Article  CAS  PubMed  Google Scholar 

  • Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plants in drying soil. Annu Rev Plant Biol 42:55–76

    Article  CAS  Google Scholar 

  • Gajewska E, Skłodowska M (2007) Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. BioMetals 20:27–36

    Article  CAS  PubMed  Google Scholar 

  • Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28:1091–1101

    Article  CAS  PubMed  Google Scholar 

  • Gitelson AA, Gritz Y, Merzlyak MN (2003) Relationships between leaf chlorophyll content and spectral reflectance and algorithms for non-destructive chlorophyll assessment in higher plant leaves. J Plant Physiol 160:271–282

    Article  CAS  PubMed  Google Scholar 

  • He Y, Xiao H, Wang H, Chen YJ, Yu M (2010a) Effect of silicon on chilling-induced changes of solutes, antioxidants, and membrane stability in seashore paspalum turfgrass. Acta Physiol Plant 32:487–494

    Article  CAS  Google Scholar 

  • He G, Zhu X, Elling AA, Chen L, Wang X, Guo L, Liang M, He H, Zhang H, Chen F, Qi Y, Chen R, Deng X (2010b) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou H, Wang P, Zhang H, Wen H, Gao F, Ma N, Wang Q, Li L (2015) Histone acetylation is involved in gibberellin-regulated sodCp gene expression in maize aleurone layers. Plant Cell Physiol 56:2139–2149

    CAS  PubMed  Google Scholar 

  • Hou H, Zheng X, Zhang H, Yue M, Hu Y, Zhou H, Wang Q, Xie C, Wang P, Li L (2017) Histone deacetylase is required for GA-induced programmed cell death in maize aleurone layers. Plant Physiol 175:1484–1496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Zhang L, He S, Huang M, Tan J, Zhao L, Yan S, Li H, Zhou K, Li L (2012) Cold stress selectively unsilences tandem repeats in heterochromatin associated with accumulation of H3K9ac. Plant Cell Environ 5:2130–2142

    Article  CAS  Google Scholar 

  • Huang M, Li H, Zhang L, Gao F, Wang P, Hu Y, Yan S, Zhao L, Zhang Q, Tan J, Liu X, He S, Li L (2012) Plant 45S rDNA clusters are fragile sites and their instability is associated with epigenetic alterations. PLoS One 7:e35139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janicka-Russak M, Kabała K (2012) Abscisic acid and hydrogen peroxide induce modification of plasma membrane H+-ATPase from Cucumis sativus L. roots under heat shock. J Plant Physiol 169:1607–1614

    Article  CAS  PubMed  Google Scholar 

  • Jin J, Shi J, Liu B, Liu Y, Huang Y, Yu Y (2015) Mrg702, a reader protein of H3K4me3 and H3K36me3, is involved in brassinosteroid-regulated growth and flowering time control in rice. Plant Physiol 168:1–27

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kim JM, To TK, Ishida J, Matsui A, Kimura H, Seki M (2012) Transition of chromatin status during the process of recovery from drought stress in Arabidopsis thaliana. Plant Cell Physiol 53:847–856

    Article  CAS  PubMed  Google Scholar 

  • Komarova NY, Grabe T, Huigen DJ, Hemleben V, Volkov RA (2004) Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids. Plant Mol Biol 56:439–463

    Article  CAS  PubMed  Google Scholar 

  • Kooten O, Snel JF (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Article  PubMed  Google Scholar 

  • Kotak S, Port M, Ganguli A, Bicker F, Koskull-Döring V (2004) Characterization of C-terminal domains of Arabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class A Hsfs with AHA and NES motifs essential for activator function and intracellular localization. Plant J 39:98–112

    Article  CAS  PubMed  Google Scholar 

  • Kotak S, Larkindale J, Lee U, Von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:10–316

    Article  CAS  Google Scholar 

  • Kurdistani SK, Grunstein M (2003) Histone acetylation and deacetylation in yeast. Nat Rev Mol Cell Biol 4:276–284

    Article  CAS  PubMed  Google Scholar 

  • Lennartsson A, Ekwall K (2009) Histone modification patterns and epigenetic codes. Biochim Biophys Acta Gen Subj 1790:863–868

    Article  CAS  Google Scholar 

  • Li JY, Jiang AL, Zhang W (2007) Salt stress-induced programmed cell death in rice root tip cells. J Integr Plant Biol 49:481–486

    Article  CAS  Google Scholar 

  • Li Q, Gent J, Zynda G, Song J, Makarevitch I, Hirsch CD, Hirsch CN, Dawe RK, Madzima TF, McGinnis KM, Lisch D, Schmitz RJ, Vaughn MW, Springer NM (2015) RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome. Proc Natl Acad Sci U S A 112:14728–14733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Huang B (2000) Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. Crop Sci 40:503–510

    Article  CAS  Google Scholar 

  • Liu K, Yu Y, Dong A, Shen WH (2017) Set domain group701 encodes a h3k4-methytransferase and regulates multiple key processes of rice plant development. New Phytol 215:609–620

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125

    Article  CAS  PubMed  Google Scholar 

  • Morsomme P, Boutry M (2000) The plant plasma membrane H+-ATPase: structure, function and regulation. Biochim Biophys Acta Biomembr 1465:1–16

    Article  CAS  Google Scholar 

  • Niogret M, Culia ez-Macia F, Goday A, Alba M, Pages M (1996) Expression and cellular localization of rab28 mRNA and Rab28 protein during maize embryogenesis. Plant J 9:549–557

    Article  CAS  PubMed  Google Scholar 

  • Pecinka A, Dinh HQ, Baubec T, Rosa M, Lettner N, Scheid OM (2010) Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell 22:3118–3129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng JC, Karpen GH (2007) H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability. Nat Cell Biol 9:25–35

    Article  CAS  PubMed  Google Scholar 

  • Pontes O, Lawrence RJ, Neves N, Silva M, Lee J-H, Chen ZJ, Viegas W, Pikaard CS (2003) Natural variation in nucleolar dominance reveals the relationship between nucleolus organizer chromatin topology and rRNA gene transcription in Arabidopsis. Proc Natl Acad Sci U S A 100:11418–11423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Probst AV, Fagard M, Proux F, Mourrain P, Boutet S, Earley K, Lawrence RJ, Pikaard CS, Murfett J, Furner I (2004) Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16:1021–1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santoro R, Li J, Grummt I (2002) The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat Genet 32:393–396

    Article  CAS  PubMed  Google Scholar 

  • Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819:104–119

    Article  CAS  PubMed  Google Scholar 

  • Schumb WC, Satterfield CN, Wentworth RL (1955) Hydrogen peroxide. Wiley, New York

    Google Scholar 

  • Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270

    Article  CAS  PubMed  Google Scholar 

  • Thompson W, Beven A, Wells B, Shaw P (1997) Sites of rDNA transcription are widely dispersed through the nucleolus in Pisum sativum and can comprise single genes. Plant J 12:571–581

    Article  CAS  PubMed  Google Scholar 

  • Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signal Behav 7:1621–1633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Von Koskull-Döring P, Scharf KD, Nover L (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci 12:452–457

    Article  CAS  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Zhao L, Hou H, Zhang H, Huang Y, Wang Y, Li H, Gao F, Yan S, Li L (2015) Epigenetic changes are associated with programmed cell death induced by heat stress in seedling leaves of Zea mays. Plant Cell Physiol 211:646–657

    Google Scholar 

  • Yang F, Zhang L, Li J, Huang J, Wen R, Ma L, Zhou D, Li L (2010) Trichostatin A and 5-azacytidine both cause an increase in global histone H4 acetylation and a decrease in global DNA and H3K9 methylation during mitosis in maize. BMC Plant Biol 10:178–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yordanov I, Velikova V, Tsonev T (2000) Plant responses to drought, acclimation, and stress tolerance. Photosynthetica 38:171–186

    Article  CAS  Google Scholar 

  • Zhang L, Hu Y, Yan S, Li H, He S, Huang M, Li L (2012) ABA-mediated inhibition of seed germination is associated with ribosomal DNA chromatin condensation, decreased transcription, and ribosomal RNA gene hypoacetylation. Plant Mol Biol 79:285–293

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Wang P, Hou H, Zhang H, Wang Y, Yan S, Huang Y, Li H, Tan J, Hu A (2014) Transcriptional regulation of cell cycle genes in response to abiotic stresses correlates with dynamic changes in histone modifications in maize. PLoS One 9:e106070

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng X, Hou H, Zhang H, Yue M, Hu Y, Li L (2017) Histone acetylation is involved in GA-mediated rDNA decondensation in maize layers. Plant Cell Rep 15:1–9

    Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (Nos. 31571265 and 31801026) and the Fundamental Research Funds for Central Public Welfare Research Institutes (562018Y-5949).

Author information

Author notes

  1. Haoli Hou and Lin Zhao contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, 430072, China

    Haoli Hou, Lin Zhao, Xueke Zheng, Mayank Gautam, Mengxia Yue, Jiaqi Hou, Zhenfei Chen, Pu Wang & Lijia Li

  2. School of electrical engineering and Automation, Wuhan University, Wuhan, 430072, China

    Haoli Hou

  3. Institute of Food and Agriculture Standardization, China National Institute of Standardization, Beijing, 100191, China

    Lin Zhao

Authors
  1. Haoli Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lin Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xueke Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mayank Gautam
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mengxia Yue
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiaqi Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhenfei Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Pu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lijia Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Pu Wang or Lijia Li.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Heiti Paves

Publisher’s note

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

Key Message

Short-term heat stress induces dynamic changes of histone H3K9ac and H3K4me2 which may participate in the physiological changes, rDNA chromatin decondensation, and gene transcriptional regulation.

Electronic supplementary material

ESM 1

(DOC 39 kb)

Fig. S1.

Alteration in maize leaf growth during heat stress treatment and recovery. (a) Growth status of seedling leaves under heat stress. (b) Relative weight. (c) Relative length. One hundred seedlings were measured at each time point. The x-axis represented different time points: 0, the control value was defined as 1.0; H1, 1 h of heat treatment; H2, 2 h of heat treatment; H5, 5 h of heat treatment; H24, 24 h of heat treatment; R1, 1 h recovery after 24 h of heat treatment; R2, 2 h recovery after 24 h of heat treatment; R5, 5 h recovery after 24 h of heat treatment; R24, 24 h recovery period after 24 h of heat treatment. Samples were collected from three independent experiments and assays for each sample were repeated three times. All data were represented as the mean ± SD. Error bars represent standard error (n=3). Asterisk (*) represented p<0.05 as compared to control by Student’s t-test. (PNG 172 kb)

High resolution image

(TIF 11012 kb)

Fig. S2.

Heat-induced alterations in the plasma membrane. (a) Alterations in membrane permeability in the leaves of maize seedlings during heat stress treatment and recovery. The ion leakage rate was increased after heat treatment. (b) Alterations in plasma membrane H+-ATPase hydrolytic activity in the leaves of maize seedlings during treatment and recovery from heat stimuli. The x-axis represented different time points: 0, the control value was defined as 1.0; H1, 1 h of heat treatment; H2, 2 h of heat treatment; H5, 5 h of heat treatment; H24, 24 h of heat treatment; R1, 1 h of recovery period after 24 h of heat treatment; R2, 2 h of recovery period after 24 h of heat treatment; R5, 5 h of recovery period after 24 h heat treatment; R24, 24 h of recovery period after 24 h of heat treatment. Samples were collected from three independent experiments and assays for each sample were repeated three times. All data were represented as the mean ± SD. Error bars represented standard error (n=3). Asterisk (*) represented p<0.05 and *** represented p<0.01 in comparison to control by Student’s t-test. (PNG 206 kb)

High resolution image

(TIF 18452 kb)

Fig. S3

Changes in the contents of chlorophyll a, b and carotenoid in the leaves of maize seedlings during the process of treatment and recovery from heat stress. Time points indicated on the x-axis are as follows: 0, basal condition before stress treatment; H1, 1 h heat treatment; H2, 2 h heat treatment; H5, 5 h heat treatment; H24, 24 h heat treatment; R1, 1 h recovery after 24 h heat treatment; R2, 2 h recovery after 24 h heat treatment; R5, 5 h recovery after 24 h heat treatment; R24, 24 h recovery after 24 h heat treatment. Each assay was repeated three times for every sample from three independent experiments. The bars represent standard errors (n=3). * p<0.05, *** p<0.01, as compared with the control group with the t-test. (PNG 153 kb)

High resolution image

(TIF 7794 kb)

Fig. S4.

Alterations in ROS content and enzyme activities in the leaves of maize seedlings during treatment and recovery from heat stimulation. (a) H2O2 concentration. (b) O2- concentration. (c) MDA concentration. (d) SOD activity. (e) CAT activity. (f) POD activity. Relative concentrations and the enzyme activity of the control group (0 h) were defined as 1.0. The x-axis represented different time points: 0, the control value was defined as 1.0; H1, 1 h of heat treatment; H2, 2 h of heat treatment; H5, 5 h of heat treatment; H24, 24 h of heat treatment; R1, 1 h of recovery period after 24 h of heat treatment; R2, 2 h of recovery period after 24 h of heat treatment; R5, 5 h of recovery period after 24 h of heat treatment; R24, 24 h of recovery period after 24 h of heat treatment. Samples were collected from three independent experiments and assays for each sample were repeated three times. All data were represented as the mean ± SD. Error bars were represented as standard error (n=3). Asterisk (*) represented p<0.05 as compared to control plants by Student’s t-test. (PNG 309 kb)

High resolution image

(TIF 15209 kb)

Fig. S5.

Western blot analysis of the change in level of H3K9ac and H3K4me2 in the leaves of maize seedlings during the process of treatment and recovery from heat stress. Histone H3 was used as a loading control. The x-axis represents different time points: 0, the control value was defined as 1.0; H1, 1 h heat treatment; H2, 2 h heat treatment; H5, 5 h heat treatment; H24, 24 h heat treatment; R1, 1 h recovery after 24 h heat treatment; R2, 2 h recovery after 24 h heat treatment; R5, 5 h recovery after 24 h heat treatment; R24, 24 h recovery after 24 h heat treatment. (PNG 184 kb)

High resolution image

(TIF 8447 kb)

Fig. S6.

Immunostaining analysis of the change in levels of H3K9ac (a) and H3K4me2 (b) in the leaves of maize seedlings during the process of treatment and recovery from heat stress. DAPI was used as a counterstain. More than 500 nuclei were analyzed. Bar=10 μm. (PNG 195 kb)

High resolution image

(TIF 6977 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hou, H., Zhao, L., Zheng, X. et al. Dynamic changes in histone modification are associated with upregulation of Hsf and rRNA genes during heat stress in maize seedlings. Protoplasma 256, 1245–1256 (2019). https://doi.org/10.1007/s00709-019-01364-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-019-01364-4

Keywords

Search

Navigation