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Global epigenetic changes of histone modification under environmental stresses in rice root

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Abstract

Abiotic stresses are non-living factors with negative morphological and physiological effects on living organisms. Substantial evidence exists that gene expression changes during plant cell growth are regulated by chromatin reconfiguration and histone modification. Several types of histone modifications are dramatically transformed in stress-responsive gene regions under drought stress conditions. Environmental stresses also cause the root apical meristem (RAM) region to decelerate root growth. In this study, we investigated how quantitative changes in epigenetic markers in this region influence rice morphology and physiology. Both iron and salinity treatments changed the epigenetic landscape from euchromatic to heterochromatic according to heterochromatin (H3K9me2) and euchromatin (H3K4me) markers, especially in the proximal meristem region. Moreover, supplementation with external abscisic acid (ABA) was able to mimic the effect of environmental stresses on global epigenetic changes. In contrast, the addition of external auxin (IAA) to rice under saline conditions affected heterochromatin formation without influencing euchromatin transformation. Chromatin dynamics is therefore believed to be directly connected to plant growth regulator signaling. We discuss insights into the role of plant growth regulators: ABA and IAA, peroxide signaling, and their effects on the global epigenetic change of histone modification under abiotic stresses.

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Abbreviations

ABA:

Abscisic acid

IAA:

Indole-3-acetic acid

RAM:

Root apical meristem

H3K9me2:

Histone H3 dimethylation at lysine 9

H3K4me2:

Histone H3 dimethylation at lysine 4

References

  • Atulba SL, Gutierrez J, Kim GW, Kim SY, Khan MI, Lee YB, Kim PJ (2015) Evaluation of rice root oxidizing potential using digital image analysis. J Korean Soc Appl Biol Chem 58:463–471

    CAS  Google Scholar 

  • Berger SL (2002) Histone modifications in transcriptional regulation. Curr Opin Genet Dev 12:142–148

    CAS  PubMed  Google Scholar 

  • Braszewska-Zalewska A, Hasterok R (2013) Epigenetic modifications of nuclei differ between root meristematic tissues of Hordeum vulgare. Plant Signal Behav 8:2–4

    Google Scholar 

  • Chen CC, Dixon JB, Turner FT (1980) Iron coatings on rice roots: morphology and models of development1. Soil Sci Soc Am J 44:1113–1119

    CAS  Google Scholar 

  • Chen Z, Zang J, Whetstine J, Hong X, Davrazou F, Kutateladze TG, Zhang G (2006) Structural insights into histone demethylation by JMJD2 family members. Cell 125:691–702

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chinnusamy V, Gong Z, Zhu J-K (2008) Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol 50:1187–1195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Costas C, Desvoyes B, Gutierrez C (2011) A chromatin perspective of plant cell cycle progression. Biochim Biophys Acta - Gene Regul Mech 1809(8):379–387

    CAS  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. In Annual Review of Plant Biology 61:651–679

    CAS  PubMed  Google Scholar 

  • Fernández-Marcos M, Sanz L, Lewis DR, Muday GK, Lorenzo O (2011) Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc Natl Acad Sci 108:18506–18511

    PubMed  Google Scholar 

  • Fischle W, Wang Y, Allis CD (2003) Histone and chromatin cross-talk. Curr Opin Cell Biol 15:172–183

    CAS  PubMed  Google Scholar 

  • Fuchs J, Demidov D, Houben A, Schubert I (2006) Chromosomal histone modification patterns—from conservation to diversity. Trends Plant Sci 11:199–208

    CAS  PubMed  Google Scholar 

  • Grafi G, Florentin A, Ransbotyn V, Morgenstern Y (2011) The stem cell state in plant development and in response to stress. Front Plant Sci 2:1–10

    Google Scholar 

  • Gulnaz A, Iqbal J, Azam F (1999) Seed treatment with growth regulators and crop produktivity. II. Response of critical growth stages of wheat (Triticum aestivum L.) under salinity stress. Cereal Res 27:419–426

    CAS  Google Scholar 

  • Jasencakova Z, Meister A, Schubert I (2001) Chromatin organization and its relation to replication and histone acetylation during the cell cycle in barley. Chromosoma 110:83–92

    CAS  PubMed  Google Scholar 

  • Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080

    CAS  PubMed  Google Scholar 

  • Ji H, Liu L, Li K, Xie Q, Wang Z, Zhao X, Li X (2014) PEG-mediated osmotic stress induces premature differentiation of the root apical meristem and outgrowth of lateral roots in wheat. J Exp Bot 65:4863–4872

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J-M, Sasaki T, Ueda M, Sako K, Seki M (2015) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6:1–12

    Google Scholar 

  • Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ 35:53–60

    Google Scholar 

  • Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates (O2˙−, H2O2, and ˙OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol 136:3114–3123

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lobréaux S, Hardy T, Briat JF (1993) Abscisic acid is involved in the iron-induced synthesis of maize ferritin. EMBO J 12:651–657

    PubMed  PubMed Central  Google Scholar 

  • Miller GAD, Suzuki N, Ciftci-yilmaz S, Mittler RON (2010) Reactive oxygen species homeostasis and signalling. Plant Cell Environ 33:453–467

    CAS  Google Scholar 

  • Molina O, Vargiu G, Abad MA, Zhiteneva A, Jeyaprakash AA, Masumoto H, Earnshaw WC (2016) Epigenetic engineering reveals a balance between histone modifications and transcription in kinetochore maintenance. Nat Commun 7:13334

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pekowska A, Benoukraf T, Ferrier P, Spicuglia S (2010) A unique H3K4me2 profile marks tissue-specific gene regulation. Genome Res 20:1493–1502

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petruk S, Sedkov Y, Johnston DM, Hodgson JW, Black KL, Kovermann SK, Mazo A (2012) TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell 150:922–933

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosa S, Ntoukakis V, Ohmido N, Pendle A, Abranches R, Shaw P (2014) Cell differentiation and development in Arabidopsis are associated with changes in histone dynamics at the single-cell level. Plant Cell 26:4821–4833

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sacks MM, Silk WK, Burman P (1997) Effect of water stress on cortical cell division rates within the apical meristem of primary roots of maize. Plant Physiol 114:519–527

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seto E, Yoshida M (2014) Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb Perspect Biol 6:18713–18713

    Google Scholar 

  • Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Shi Y (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941–953

    CAS  PubMed  Google Scholar 

  • Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45

    CAS  PubMed  Google Scholar 

  • Turner BM (2002) Cellular memory and the histone code. Cell 111:285–291

    CAS  PubMed  Google Scholar 

  • Vaughn MW, Dedhia N, Mccombie WR, Lavine K, Mittal V, May B, Martienssen R (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476

    PubMed  Google Scholar 

  • Verslues PE, Zhu J-K (2005) Before and beyond ABA: upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress. Biochem Soc Trans 33:375–379

    CAS  PubMed  Google Scholar 

  • Veselov D, Akhiyarova G, Kudoyarova G, Fricke W (2004) Rapid and tissue-specific changes in ABA and in growth rate in response to salinity in barley leaves. J Exp Bot 55:1115–1123

    PubMed  Google Scholar 

  • West G, Inzé D, Beemster GTS (2004) Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol 135:1050–1058

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yan S, Zhang Q, Li Y, Huang Y, Zhao L, Tan J, Li L (2014) Comparison of chromatin epigenetic modification patterns among root meristem, elongation and maturation zones in maize (Zea mays L.). Cytogenet Genome Res 143:179–188

    CAS  PubMed  Google Scholar 

  • Yang F, Zhang L, Li J, Huang J, Wen R, Ma L, 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

    PubMed  PubMed Central  Google Scholar 

  • Yang L, Zhang J, He J, Qin Y, Hua D, Duan Y, Gong Z (2014) ABA-mediated ROS in mitochondria regulate root meristem activity by controlling PLETHORA expression in Arabidopsis. PLoS Genet 10(12):e1004791

    PubMed  PubMed Central  Google Scholar 

  • Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 21:133–139

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Zhao K, Tung C-W, Eizenga GC, Wright MH, Ali ML, Price AH, McCouch SR (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2:467

    PubMed  PubMed Central  Google Scholar 

  • Zheng C, Halaly T, Acheampong AK, Takebayashi Y, Jikumaru Y, Kamiya Y, Or E (2015) Abscisic acid (ABA) regulates grape bud dormancy, and dormancy release stimuli may act through modification of ABA metabolism. J Exp Bot 66:1527–1542

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by the SmartD program (IAARD-Indonesian Ministry of Agriculture) to AP, and JSPS and CAS under the Japan-Czech Research Cooperative Program to NO. We thank Edanz Group (www.edanzediting.com/ac) for editing the English text of a draft of this manuscript.

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Authors and Affiliations

  1. Indonesian Center for Agricultural Biotechnology and Genetic Resource Research and Development (ICABIOGRD), Bogor, Indonesia

    Aqwin Polosoro & Wening Enggarini

  2. Graduate School of Human Development and Environment, Kobe University, Kobe, Japan

    Aqwin Polosoro & Nobuko Ohmido

Authors
  1. Aqwin Polosoro
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  2. Wening Enggarini
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  3. Nobuko Ohmido
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Contributions

NO conceived of the study, participated in its design and coordination, and drafted the manuscript. AP carried out collected experiments, assembly of data, performed statistical analysis studies, and drafted the manuscript. WE prepared the rice materials and assisted with data interpretation. All authors read and NO approved the final manuscript.

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Correspondence to Nobuko Ohmido.

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Responsible Editor: Hans de Jong

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Polosoro, A., Enggarini, W. & Ohmido, N. Global epigenetic changes of histone modification under environmental stresses in rice root. Chromosome Res 27, 287–298 (2019). https://doi.org/10.1007/s10577-019-09611-3

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  • DOI: https://doi.org/10.1007/s10577-019-09611-3

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