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PMID: 25171199 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Transcriptional regulation of cell cycle genes in response to abiotic stresses correlates with dynamic changes in histone modifications in maize.

PloS one ·Vol. 9 ·No. 8 ·2014-00-00 ·Pages e106070

Zhao L, Wang P, Hou H, Zhang H, Wang Y, Yan S, Huang Y, Li H, Tan J, Hu A, Gao F, Zhang Q, Li Y, Zhou H, Zhang W, Li L

Abstract

The histone modification level has been shown to be related with gene activation and repression in stress-responsive process, but there is little information on the relationship between histone modification and cell cycle gene expression responsive to environmental cues. In this study, the function of histone modifications in mediating the transcriptional regulation of cell cycle genes under various types of stress was investigated in maize (Zea mays L.). Abiotic stresses all inhibit the growth of maize seedlings, and induce total acetylation level increase compared with the control group in maize roots. The positive and negative regulation of the expression of some cell cycle genes leads to perturbation of cell cycle progression in response to abiotic stresses. Chromatin immunoprecipitation analysis reveals that dynamic histone acetylation change in the promoter region of cell cycle genes is involved in the control of gene expression in response to external stress and different cell cycle genes have their own characteristic patterns for histone acetylation. The data also showed that the combinations of hyperacetylation and hypoacetylation states of specific lysine sites on the H3 and H4 tails on the promoter regions of cell cycle genes regulate specific cell cycle gene expression under abiotic stress conditions, thus resulting in prolonged cell cycle duration and an inhibitory effect on growth and development in maize seedlings.

MeSH Terms
Acetylation Blotting, Western Cell Cycle/genetics Cell Cycle Proteins/genetics,metabolism Cold Temperature Copper Sulfate/pharmacology Flow Cytometry Gene Expression Regulation, Developmental Gene Expression Regulation, Plant Histones/metabolism Hot Temperature Lysine/metabolism Mannitol/pharmacology Plant Proteins/genetics Plant Roots/genetics,metabolism Promoter Regions, Genetic/genetics Reverse Transcriptase Polymerase Chain Reaction Sodium Chloride/pharmacology Stress, Physiological Zea mays/genetics,growth & development,metabolism
Chemicals
Cell Cycle Proteins Histones Plant Proteins Mannitol Sodium Chloride Lysine Copper Sulfate
Authors & Affiliations
16 authors, click to expand affiliations / ORCID
Zhao Lin
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Wang Pu
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Hou Haoli
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Zhang Hao
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Wang Yapei
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Yan Shihan
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Huang Yan
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Li Hui
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Tan Junjun
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Hu Ao
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Gao Fei
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Zhang Qi
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Li Yingnan
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Zhou Hong
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
Zhang Wei
Renmin Hospital, Wuhan University, Wuhan, China.
Li Lijia
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.
References (43)
43 references, click to expand
  1. Cold stress selectively unsilences tandem repeats in heterochromatin associated with accumulation of H3K9ac.
    Plant Cell Environ. 2012 Dec;35(12):2130-42 PMID: 22616903
  2. Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins.
    Plant Physiol. 2004 Jun;135(2):1084-99 PMID: 15208425
  3. 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. 2010 Aug 18;10:178 PMID: 20718950
  4. Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress.
    Plant Physiol. 2004 Jun;135(2):1050-8 PMID: 15181207
  5. Histone H4 acetylation of euchromatin and heterochromatin is cell cycle dependent and correlated with replication rather than with transcription.
    Plant Cell. 2000 Nov;12(11):2087-100 PMID: 11090211
  6. A Common histone modification code on C4 genes in maize and its conservation in Sorghum and Setaria italica.
    Plant Physiol. 2013 May;162(1):456-69 PMID: 23564230
  7. Transition of chromatin status during the process of recovery from drought stress in Arabidopsis thaliana.
    Plant Cell Physiol. 2012 May;53(5):847-56 PMID: 22505693
  8. Effect of water stress on cell division and cell-division-cycle 2-like cell-cycle kinase activity in wheat leaves
    Plant Physiol. 1998 Jun;117(2):667-78 PMID: 9625720
  9. Vernalization requires epigenetic silencing of FLC by histone methylation.
    Nature. 2004 Jan 8;427(6970):164-7 PMID: 14712277
  10. Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis.
    Plant Physiol. 2005 Jun;138(2):734-43 PMID: 15863702
  11. Genome-wide analysis of core cell cycle genes in Arabidopsis.
    Plant Cell. 2002 Apr;14(4):903-16 PMID: 11971144
  12. An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond.
    J Exp Bot. 2011 Jul;62(11):3713-25 PMID: 21617249
  13. Reversible histone acetylation and deacetylation mediate genome-wide, promoter-dependent and locus-specific changes in gene expression during plant development.
    Genetics. 2005 Jan;169(1):337-45 PMID: 15371352
  14. Single-walled carbon nanotubes selectively influence maize root tissue development accompanied by the change in the related gene expression.
    J Hazard Mater. 2013 Feb 15;246-247:110-8 PMID: 23291336
  15. Chromatin regulation functions in plant abiotic stress responses.
    Plant Cell Environ. 2010 Apr;33(4):604-11 PMID: 19930132
  16. Promoter-associated histone acetylation is involved in the osmotic stress-induced transcriptional regulation of the maize ZmDREB2A gene.
    Physiol Plant. 2014 Aug;151(4):459-67 PMID: 24299295
  17. Epigenetic regulation of stress responses in plants.
    Curr Opin Plant Biol. 2009 Apr;12(2):133-9 PMID: 19179104
  18. Mapping global histone acetylation patterns to gene expression.
    Cell. 2004 Jun 11;117(6):721-33 PMID: 15186774
  19. Control of the transition to flowering by chromatin modifications.
    Mol Plant. 2009 Jul;2(4):554-564 PMID: 19825638
  20. Identification of AtHD2C as a novel regulator of abscisic acid responses in Arabidopsis.
    Plant J. 2006 Apr;46(1):124-33 PMID: 16553900
  21. Genome-wide and organ-specific landscapes of epigenetic modifications and their relationships to mRNA and small RNA transcriptomes in maize.
    Plant Cell. 2009 Apr;21(4):1053-69 PMID: 19376930
  22. Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana.
    Plant Cell Physiol. 2008 Oct;49(10):1580-8 PMID: 18779215
  23. Trichostatin A selectively suppresses the cold-induced transcription of the ZmDREB1 gene in maize.
    PLoS One. 2011;6(7):e22132 PMID: 21811564
  24. Measurement of ozone injury by determination of leaf chlorophyll concentration.
    Plant Physiol. 1977 Oct;60(4):606-8 PMID: 16660147
  25. Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana.
    Planta. 2000 Oct;211(5):632-40 PMID: 11089675
  26. ABA treatment of germinating maize seeds induces VP1 gene expression and selective promoter-associated histone acetylation.
    Physiol Plant. 2011 Nov;143(3):287-96 PMID: 21679193
  27. Plant 45S rDNA clusters are fragile sites and their instability is associated with epigenetic alterations.
    PLoS One. 2012;7(4):e35139 PMID: 22509394
  28. A dominant negative mutant of cyclin-dependent kinase A reduces endoreduplication but not cell size or gene expression in maize endosperm.
    Plant Cell. 2004 Jul;16(7):1854-69 PMID: 15208390
  29. Arabidopsis HDA6 regulates locus-directed heterochromatin silencing in cooperation with MET1.
    PLoS Genet. 2011 Apr;7(4):e1002055 PMID: 21552333
  30. Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control.
    Plant J. 2005 Feb;41(4):546-66 PMID: 15686519
  31. Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes.
    Plant Physiol. 2007 Mar;143(3):1429-38 PMID: 17208957
  32. Genome-wide patterns of histone modifications in yeast.
    Nat Rev Mol Cell Biol. 2006 Sep;7(9):657-66 PMID: 16912715
  33. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3.
    Nature. 2004 Jan 8;427(6970):159-64 PMID: 14712276
  34. Systematic analysis of cell-cycle gene expression during Arabidopsis development.
    Plant J. 2009 Aug;59(4):645-60 PMID: 19392699
  35. Somatic embryogenesis in Solanum tuberosum L.: a histological examination of key developmental stages.
    Plant Cell Rep. 2004 Sep;23(3):115-9 PMID: 15185123
  36. Maize histone deacetylase hda101 is involved in plant development, gene transcription, and sequence-specific modulation of histone modification of genes and repeats.
    Plant Cell. 2007 Apr;19(4):1145-62 PMID: 17468264
  37. 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. 2005 Sep 12;33(16):5199-207 PMID: 16157865
  38. ABA-mediated inhibition of seed germination is associated with ribosomal DNA chromatin condensation, decreased transcription, and ribosomal RNA gene hypoacetylation.
    Plant Mol Biol. 2012 Jun;79(3):285-93 PMID: 22527753
  39. Genome-wide map of nucleosome acetylation and methylation in yeast.
    Cell. 2005 Aug 26;122(4):517-27 PMID: 16122420
  40. Complexes of D-type cyclins with CDKs during maize germination.
    J Exp Bot. 2013 Dec;64(18):5661-71 PMID: 24127516
  41. Dynamics of global histone acetylation and deacetylation in vivo: rapid restoration of normal histone acetylation status upon removal of activators and repressors.
    Genes Dev. 2002 Mar 15;16(6):743-52 PMID: 11914279
  42. Histone deacetylation is required for progression through mitosis in tobacco cells.
    Plant J. 2005 Feb;41(3):346-52 PMID: 15659094
  43. Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest.
    Plant Cell. 2011 May;23(5):1876-88 PMID: 21558544
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
DOI
10.1371/journal.pone.0106070
Published
2014-00-00
Epub
2014-00-29
Pages
e106070
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC4149478
Subset
IM
External Links
PubMed source DOI: 10.1371/journal.pone.0106070 PMC Full Text View journal details
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