Epigenetics, a mode for plants to respond to abiotic stresses
Epigenetics, a mode for plants to respond to abiotic stresses
Weihua QIAO1(), Liumin FAN2()
1. Insititute of Crop Sciences/National Key Facility for Crop Resources and Genetic Improvement, Chinese Academy of Agricultural Sciences, Beijing 100081, China; 2. State Key Laboratory of Protein and Plant Gene Research, Genetic Engineering Peking-Yale Joint Center of Plant Molecular Genetics and Agro-biotechnology, College of Life Sciences, Peking University, Beijing 100871, China
Epigenetics has been becoming a hot topic in recent years. It can be mechanisms that regulate gene expression without changing DNA base sequence. In plants epigenetic regulation has been implicated to be a very important phenomenon and mechanism for the regulation of responses to environmental stresses. Environmental signals induce various epigenetic modifications in the genome, and these epigenetic modifications might likely be inherited to the next generation that behaves with enhanced ability to tolerate stresses. This review highlights recent advances in the study of epigenetics in plant stress responses.
Corresponding Author(s):
QIAO Weihua,Email:qiao@caas.net.cn; FAN Liumin,Email:lmfan@pku.edu.cn
引用本文:
. Epigenetics, a mode for plants to respond to abiotic stresses[J]. Frontiers in Biology, 2011, 6(6): 477-481.
Weihua QIAO, Liumin FAN. Epigenetics, a mode for plants to respond to abiotic stresses. Front Biol, 2011, 6(6): 477-481.
Domains rearranged methyltransferase (DRM) (CG, CNG and CNN)
Contributes to de novo methylation in all sequence contexts
Tabacoo
Wada et al., 2003; Wada 2005
Chromomethylase (CMT)
Maintain CNG methylation in heterochromatin and silencing of methylated loci
Arabidopsis; maize
Bartee et al., 2001; Papa et al., 2001
Methyltransferase (MET1)
DNA methylation at CG sites
Arabidopsis; carrot; pea; tomato and maize
Finnegan and Kovac, 2000
Glycerophosphodiesterase-like protein (NtGPDL)
Aluminum, low temperature and salt stress can induce DNA demethylation in the coding region
Tabacoo
Choi and Sano, 2007
Histone H3K9 methyltransferase; SDG33
Histone methylation of Lys 9
Tabacoo; Arabidopsis
Shen, 2001; Johnson et al., 2002
Methyl binding domain protein; MBD1 to 13
Associated with histone and Some MBDs recognize methyl-cytosine
Arabidopsis
Zemach and Grafi, 2003
Histone deacetylase 19 HDA19; AtRPD3A
Response to Jasmonic Acid and Ethylene Signaling induced by stress
Arabidopsis
Zhou et al., 2005
DICER; DICER-LIKE; (DCL) 1, 2, 3, 4
Cuts dsRNA into small fragments
Arabidopsis
Schauer et al., 2002
RNA-denpendent RNA polymerase; RDR 1 to 6; SDE1/SGS2
Amplifies microRNAs
Arabidopsis; Tabacoo (Nicotiana benthamiana)
Dalmay et al., 2000; Mourrain et al., 2000; Vaistij et al., 2002
Tab.1
1
Ascenzi R, Gantt J S (1997). A drought-stress-inducible histone gene in Arabidopsis thaliana is a member of a distinct class of plant linker histone variants. Plant Mol Biol , 34(4): 629–641 doi: 10.1023/A:1005886011722 pmid:9247544
2
Aufsatz W, Mette M F, van der Winden J, Matzke M, Matzke A J (2002). HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J , 21(24): 6832–6841 doi: 10.1093/emboj/cdf663 pmid:12486004
3
Bartee L, Malagnac F, Bender J (2001). Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev , 15(14): 1753–1758 doi: 10.1101/gad.905701 pmid:11459824
4
Borsani O, Zhu J, Verslues P E, Sunkar R, Zhu J K (2005). Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell , 123(7): 1279–1291 doi: 10.1016/j.cell.2005.11.035 pmid:16377568
5
Camporeale G, Oommen A M, Griffin J B, Sarath G, Zempleni J (2007). K12-biotinylated histone H4 marks heterochromatin in human lymphoblastoma cells. J Nutr Biochem , 18(11): 760–768 doi: 10.1016/j.jnutbio.2006.12.014 pmid:17434721
6
Chen L T, Luo M, Wang Y Y, Wu K (2010). Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot , 61(12): 3345–3353 doi: 10.1093/jxb/erq154 pmid:20519338
7
Chinnusamy E, Zhu J K (2009). Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol , 12(2): 1–7 doi: 10.1016/j.pbi.2008.12.006 pmid:19112043
8
Choi C S, Sano H (2007). Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Mol Genet Genomics , 277(5): 589–600 doi: 10.1007/s00438-007-0209-1 pmid:17273870
9
Dalmay T, Hamilton A, Rudd S, Angell S, Baulcombe D C (2000). An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell , 101(5): 543–553 doi: 10.1016/S0092-8674(00)80864-8 pmid:10850496
10
Dyachenko O V, Zakharchenko N S, Shevchuk T V, Bohnert H J, Cushman J C, Buryanov Y I (2006). Effect of hypermethylation of CCWGG sequences in DNA of Mesembryanthemum crystallinum plants on their adaptation to salt stress. Biochemistry (Mosc) , 71(4): 461–465 doi: 10.1134/S000629790604016X pmid:16615868
11
Finnegan E J, Kovac K A (2000). Plant DNA methyltransferases. Plant Mol Biol , 43(2–3): 189–201 doi: 10.1023/A:1006427226972 pmid:10999404
12
Fu W Q, Wu K Q, Duan J (2007). Sequence and expression analysis of histone deacetylases in rice. Biochem Biophys Res Commun , 356(4): 843–850 doi: 10.1016/j.bbrc.2007.03.010 pmid:17399684
13
Hashida S N, Uchiyama T, Martin C, Kishima Y, Sano Y, Mikami T (2006). The temperature-dependent change in methylation of the Antirrhinum transposon Tam3 is controlled by the activity of its transposase. Plant Cell , 18(1): 104–118 doi: 10.1105/tpc.105.037655 pmid:16326924
14
Henderson I R, Jacobsen S E (2007). Epigenetic inheritance in plants.Nature , 447(7143): 418–424
15
Johnson L, Cao X, Jacobsen S (2002). Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol , 12(16): 1360–1367 doi: 10.1016/S0960-9822(02)00976-4 pmid:12194816
16
Kim J M, To T K, Ishida J, Morosawa T, Kawashima M, Matsui A, Toyoda T, Kimura H, Shinozaki K, Seki M (2008). Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol , 49(10): 1580–1588 doi: 10.1093/pcp/pcn133 pmid:18779215
17
Kovarik A, Koukalova B, Bezdek M, Opatrn Z (1997). Hypermethylation of tobacco heterochromatic loci in response to osmotic stress. Theor Appl Genet , 95(1–2): 301–306 doi: 10.1007/s001220050563
18
Labra M, Ghiani A, Citterio S, Sgorbati S, Sala F, Vannini C, Ruffini-Castiglione M, Bracale M (2002). Analysis of cytosine methylation pattern in response to water deficit in pea root tips. Plant Biol (Stuttgart) , 4(6): 694–699 doi: 10.1055/s-2002-37398
19
Lister R, O’Malley R C, Tonti-Filippini J, Gregory B D, Berry C C, Millar A H, Ecker J R (2008). Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell , 133(3): 523–536 doi: 10.1016/j.cell.2008.03.029 pmid:18423832
20
Martienssen R (1998). Transposons, DNA methylation and gene control. Trends Genet , 14(7): 263–264 doi: 10.1016/S0168-9525(98)01518-2 pmid:9676527
21
Mourrain P, Béclin C, Elmayan T, Feuerbach F, Godon C, Morel J B, Jouette D, Lacombe A M, Nikic S, Picault N, Rémoué K, Sanial M, Vo T A, Vaucheret H (2000). ArabidopsisSGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell , 101(5): 533–542 doi: 10.1016/S0092-8674(00)80863-6 pmid:10850495
22
Nathan D, Ingvarsdottir K, Sterner D E, Bylebyl G R, Dokmanovic M, Dorsey J A, Whelan K A, Krsmanovic M, Lane W S, Meluh P B, Johnson E S, Berger S L (2006). Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev , 20(8): 966–976 doi: 10.1101/gad.1404206 pmid:16598039
23
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones J D G (2006). A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science , 312(5772): 436–439 doi: 10.1126/science.1126088 pmid:16627744
24
Papa C M, Springer N M, Muszynski M G, Meeley R, Kaeppler S M (2001). Maize chromomethylase Zea methyltransferase2 is required for CpNpG methylation. Plant Cell , 13(8): 1919–1928 pmid:11487702
25
Phillips J R, Dalmay T, Bartels D (2007). The role of small RNAs in abiotic stress. FEBS Lett , 581(19): 3592–3597 doi: 10.1016/j.febslet.2007.04.007 pmid:17451688
26
Probst A V, Fagard M, Proux F, Mourrain P, Boutet S, Earley K, Lawrence R J, Pikaard C S, Murfett J, Furner I, Vaucheret H, Mittelsten Scheid O (2004). Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell , 16(4): 1021–1034 doi: 10.1105/tpc.018754 pmid:15037732
27
Qiu S P, Huang J, Pan L J, Wang M M, Zhang H S (2006). Salt induces expression of RH3.2A, encoding an H3.2-type histone H3 protein in rice (Oryza sativa L.). Yi Chuan Xue Bao , 33(9): 833–840 doi: 10.1016/S0379-4172(06)60117-0 pmid:16980130
28
Schauer S E, Jacobsen S E, Meinke D W, Ray A (2002). DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci , 7(11): 487–491 12417148 doi: 10.1016/S1360-1385(02)02355-5
29
Scippa G S, Griffiths A, Chiatante D, Bray E A (2000). The H1 histone variant of tomato, H1-S, is targeted to the nucleus and accumulates in chromatin in response to water-deficit stress. Planta , 211(2): 173–181 doi: 10.1007/s004250000278 pmid:10945211
30
Shen W H (2001). NtSET1, a member of a newly identified subgroup of plant SET-domain-containing proteins, is chromatin-associated and its ectopic overexpression inhibits tobacco plant growth. Plant J , 28(4): 371–383 doi: 10.1046/j.1365-313X.2001.01135.x pmid:11737775
31
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(1): 245–254 doi: 10.1007/s00425-007-0612-1 pmid:17721787
32
Sridha S, Wu K (2006). Identification of AtHD2C as a novel regulator of abscisic acid responses in Arabidopsis. Plant J , 46(1): 124–133 doi: 10.1111/j.1365-313X.2006.02678.x pmid:16553900
33
Sridhar V V, Kapoor A, Zhang K, Zhu J, Zhou T, Hasegawa P M, Bressan R A, Zhu J K (2007). Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature , 447(7145): 735–738 doi: 10.1038/nature05864 pmid:17554311
34
Steward N, Ito M, Yamaguchi Y, Koizumi N, Sano H (2002). Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. J Biol Chem , 277(40): 37741–37746 doi: 10.1074/jbc.M204050200 pmid:12124387
35
Stockinger E J, Mao Y, Regier M K, Triezenberg S J, Thomashow M F (2001). Transcriptional adaptor and histone acetyltransferase proteins in Arabidopsis and their interactions with CBF1, a transcriptional activator involved in cold-regulated gene expression. Nucleic Acids Res , 29(7): 1524–1533 doi: 10.1093/nar/29.7.1524 pmid:11266554
36
Sunkar R, Chinnusamy V, Zhu J, Zhu J K (2007). Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci , 12(7): 310–309 doi: 10.1016/j.tplants.2007.05.001 pmid:17596996
37
Sunkar R, Kapoor A, Zhu J K (2006). Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell , 18(8): 2051–2065 doi: 10.1105/tpc.106.041673 pmid:16861386
38
Sunkar R, Zhu J K (2004). Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell , 16(8): 2001–2019 doi: 10.1105/tpc.104.022830 pmid:15258262
39
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(7): 995–1003 doi: 10.1093/pcp/pcj072 pmid:16774928
40
Vaistij F E, Jones L, Baulcombe D C (2002). Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell , 14(4): 857–867 doi: 10.1105/tpc.010480 pmid:11971140
41
Wada Y (2005). Physiological functions of plant DNA methyltransferases. Plant Biotechnol , 22: 71–80
42
Wada Y, Ohya H, Yamaguchi Y, Koizumi N, Sano H (2003). Preferential de novo methylation of cytosine residues in non-CpG sequences by a domains rearranged DNA methyltransferase from tobacco plants. J Biol Chem , 278(43): 42386–42393 doi: 10.1074/jbc.M303892200 pmid:12917429
43
Yoder J A, Walsh C P, Bestor T H (1997). Cytosine methylation and the ecology of intragenomic parasites. Trends Genet , 13(8): 335–340 doi: 10.1016/S0168-9525(97)01181-5 pmid:9260521
44
Zemach A, Grafi G (2003). Characterization of Arabidopsis thaliana methyl-CpG-binding domain (MBD) proteins. Plant J , 34(5): 565–572 doi: 10.1046/j.1365-313X.2003.01756.x pmid:12787239
45
Zhang K, Sridhar V V, Zhu J, Kapoor A, Zhu J K (2007). Distinctive core histone post-translational modification patterns in Arabidopsis thaliana. PLoS ONE , 2(11): e1210 doi: 10.1371/journal.pone.0001210 pmid:18030344
46
Zhou C, Zhang L, Duan J, Miki B, Wu K (2005). HISTONE DEACETYLASE19 is involved in jasmonic acid and ethylene signaling of pathogen response in Arabidopsis. Plant Cell , 17(4): 1196–1204 doi: 10.1105/tpc.104.028514 pmid:15749761
