Plant growth and crop production are highly reduced by adverse environmental conditions and rice is particularly sensitive to abiotic stresses. Plants have developed a number of different mechanisms to respond and try to adapt to abiotic stress. Plant response to stress such as drought, cold, and high salinity, implies rapid and coordinated changes at transcriptional level of entire gene networks. During the last decade many transcription factors, belonging to different families, have been shown to act as positive or negative regulators of stress responsive genes, thus playing an extremely important role in stress signaling. More recently, epigenetic mechanisms have been also involved in the regulation of the stress responsive genes. In this review, we have performed a comprehensive analysis of the rice transcription factors reported so far as being involved in abiotic stress responses. The impact of abiotic stresses on epigenomes is also addressed. Finally, we update the connections made so far between DNA-binding transcription factors (TFs), and epigenetic mechanisms (DNA methylation and histones methylation or acetylation) emphasizing an integrative view of transcription regulation.
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References
1.
AgalouA., PurwantomoS., OvernasE., JohannessonH., ZhuX., EstiatiA.et al.2008. A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members. Plant Mol Biol, 66:87–103.
2.
AgarwalP.K., JhaB.2010. Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol Plant, 54:201–212.
3.
AgarwalP.K., AgarwalP., ReddyM.K., SoporyS.K.2006. Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep, 25:1263–1274.
4.
AgarwalP., AroraR., RayS., SinghA.K., SinghV.P., TakatsujiH.et al.2007. Genome-wide identification of C2H2 zinc-finger gene family in rice and their phylogeny and expression analysis. Plant Mol Biol, 65:467–485.
5.
AhringerJ.2000. NuRD and SIN3 histone deacetylase complexes in development. Trends Genet, 16:351–356.
6.
AidaM., IshidaT., FukakiH., FujisawaH., TasakaM.1997. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell, 9:841–857.
7.
AidaM., IshidaT., TasakaM.1999. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development, 126:1563–1570.
8.
AinaR., SgorbatiS., SantagostinoA., LabraM., GhianiA., CitterioS.2004. Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol Plant, 121:472–480.
9.
Alvarez-VenegasR., AbdallatA.A., GuoM., AlfanoJ.R., AvramovaZ.2007. Epigenetic control of a transcription factor at the cross section of two antagonistic pathways. Epigenetics, 2:106–113.
10.
Arnholdt-SchmittB.2004. Stress-induced cell reprogramming. A role for global genome regulation?Plant Physiol, 136:2579–2586.
11.
BaekD., JiangJ., ChungJ.S., WangB., ChenJ., XinZ.et al.2011. Regulated AtHKT1 gene expression by a distal enhancer element and DNA methylation in the promoter plays an important role in salt tolerance. Plant Cell Physiol, 52:149–161.
12.
BaniwalS.K., BhartiK., ChanK.Y., FauthM., GanguliA., KotakS.et al.2004. Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci, 29:471–487.
13.
BannisterA.J., KouzaridesT.2011. Regulation of chromatin by histone modifications. Cell Res, 21:381–395.
14.
BergerS.L.2007. The complex language of chromatin regulation during transcription. Nature, 447:407–412.
15.
BerriS., AbbruscatoP., Faivre-RampantO., BrasileiroA.C.M., FumasoniI., SatohK.et al.2009. Characterization of WRKY co-regulatory networks in rice and Arabidopsis. BMC Plant Biol, 9:120.
16.
CaiM., QiuD., YuanT., DingX., LiH., DuanL.et al.2008. Identification of novel pathogen-responsive cis-elements and their binding proteins in the promoter of OsWRKY13, a gene regulating rice disease resistance. Plant Cell Environ, 31:86–96.
17.
CaoY., SongF., GoodmanR.M., ZhengZ.2006. Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress. J Plant Physiol, 163:1167–1178.
18.
CaoY.F., WuY.F., ZhengZ., SongF.M.2005. Overexpression of the rice EREBP-like gene OsBIERF3 enhances disease resistance and salt tolerance in transgenic tobacco. Physiol Mol Plant Pathol., 67:202–211.
19.
CasarettoJ., HoT.H.2003. The transcription factors HvABI5 and HvVP1 are required for the abscisic acid induction of gene expression in barley aleurone cells. Plant Cell, 15:271–284.
20.
CenturyK., ReuberT.L., RatcliffeO.J.2008. Regulating the regulators: the future prospects for transcription-factor-based agricultural biotechnology products. Plant Physiol, 147:20–29.
21.
ChanS.W.-L., HendersonI.R., JacobsenS.E.2005. Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Gen, 6:351–360.
22.
CharngY.Y., LiuH.C., LiuN.Y., ChiW.T., WangC.N., ChangS.H.et al.2007. A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol, 143:251–262.
23.
ChattopadhyayS., AngL.H., PuenteP., DengX.W., WeiN.1998. Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell, 10:673–683.
24.
ChenJ.Q., MengX.P., ZhangY., XiaM., WangX.P.2008. Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett, 30:2191–2198.
25.
ChenL.T., LuoM., WangY.Y., WuK.2010. Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot, 61:3345–3353.
26.
ChengC., DaigenM., HirochikaH.2006. Epigenetic regulation of the rice retrotransposon Tos17. Mol Genet Genomics, 276:378–390.
27.
ChinnusamyV., ZhuJ.K.2009. Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol, 12:133–139.
28.
ChoiC.-S., SanoH.2007. Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Mol Genet Genomics, 277:589–600.
29.
ChoiH.I., HongJ.H., HaJ.O., KangJ.Y., KimS.Y.2000. ABFs, a family of ABA-responsive element binding factors. J Biol Chem, 275:1723–1730.
30.
CiolkowskiI., WankeD., BirkenbihlR.P., SomssichI.E.2008. Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol, 68:81–92.
31.
DaiX., XuY., MaQ., XuW., WangT., XueY.et al.2007. Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiol, 143:1739–1751.
32.
DengX., PhillipsJ., MeijerA.H., SalaminiF., BartelsD.2002. Characterization of five novel dehydration-responsive homeodomain leucine zipper genes from the resurrection plant Craterostigma plantagineum. Plant Mol Biol, 49:601–610.
33.
DevaiahB.N., NagarajanV.K., RaghothamaK.G.2007. Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol, 145:147–159.
34.
DezarC.A., GagoG.M., GonzalezD.H., ChanR.L.2005. Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants. Transgenic Res, 14:429–440.
35.
DietzK.J., VogelM.O., ViehhauserA.2010. AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signalling. Protoplasma, 245:3–14.
36.
DingY., WangX., SuL., ZhaiJ.X., CaoS.Y., ZhangD.F.et al.2007. SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell, 19:9–22.
37.
DubouzetJ.G., SakumaY., ItoY., KasugaM., DubouzetE.G., MiuraS.et al.2003. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J, 33:751–763.
38.
FangY.J., YouJ., XieK.B., XieW.B., XiongL.Z.2008. Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genomics, 280:547–563.
39.
FellerA., MachemerK., BraunE.L., GrotewoldE.2011. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J, 66:94–116.
40.
FeurtadoJ.A., HuangD., Wicki-StordeurL., HemstockL.E., PotentierM.S., TsangE.W.et al.2011. The Arabidopsis C2H2 Zinc Finger INDETERMINATE DOMAIN1/ENHYDROUS promotes the transition to germination by regulating light and hormonal signaling during seed maturation. Plant Cell 10.1105/tpc.111.085134
41.
FrankW., PhillipsJ., SalaminiF., BartelsD.1998. Two dehydration-inducible transcripts from the resurrection plant Craterostigma plantagineum encode interacting homeodomain-leucine zipper proteins. Plant J, 15:413–421.
42.
FranszP.F., De JongJ.H.2002. Chromatin dynamics in plants. Curr Opin Plant Biol, 5:560–567.
43.
FuW., WuK., DuanJ.2007. Sequence and expression analysis of histone deacetylases in rice. Biochem Biophys Res Commun, 356:843–850.
44.
FujitaY., FujitaM., SatohR., MaruyamaK., ParvezM.M., SekiM.et al.2005. AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell, 17:3470–3488.
45.
FukaoT., Bailey-SerresJ.2008. Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proc Natl Acad Sci USA, 105:16814–16819.
46.
FukaoT., YeungE., Bailey-SerresJ.2011. The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell, 23:412–427.
47.
FukaoT., XuK., RonaldP.C., Bailey-SerresJ.2006. A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell, 18:2021–2034.
48.
FukazawaJ., SakaiT., IshidaS., YamaguchiI., KamiyaY., TakahashiY.2000. Repression of shoot growth, a bZIP transcriptional activator, regulates cell elongation by controlling the level of gibberellins. Plant Cell, 12:901–915.
49.
GaoF., XiongA.S., PengR.H., JinX.F., XuJ., ZhuB.et al.2010. OsNAC52, a rice NAC transcription factor, potentially responds to ABA and confers drought tolerance in transgenic plants. Plant Cell Tissue Organ Culture, 100:255–262.
50.
GaoM.-J., HegedusD.D., SharpeA.G., RobinsonS.J., LydiateD.J., HannoufaA.2007. Isolation and characterization of a GCN5-interacting protein from Arabidopsis thaliana. Planta, 225:1367–1379.
51.
GaoM.J., SchaferU.A., ParkinI.A.P., HegedusD.D., LydiateD.J., HannoufaA.2003. A novel protein from Brassica napus has a putative KID domain and responds to low temperature. Plant J, 33:1073–1086.
52.
GendrelA.V., LippmanZ., YordanC., ColotV., MartienssenR.A.2002. Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science, 297:1871–1873.
53.
GuiltinanM.J., MarcotteW.R., QuatranoR.S.1990. A plant leucine zipper protein that recognizes an abscisic-acid response element. Science, 250:267–271.
54.
GuthaL.R., ReddyA.R.2008. Rice DREB1B promoter shows distinct stress-specific responses, and the overexpression of cDNA in tobacco confers improved abiotic and biotic stress tolerance. Plant Mol Biol, 68:533–555.
55.
GuttersonN., ReuberT.L.2004. Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol, 7:465–471.
56.
HaakeV., CookD., RiechmannJ.L., PinedaO., ThomashowM.F., ZhangJ.Z.2002. Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol, 130:639–648.
57.
HashidaS.-N., UchiyamaT., MartinC., KishimaY., SanoY., MikamiT.2006. The temperature-dependent change in methylation of the Antirrhinum transposon Tam3 is controlled by the activity of its transposase. Plant Cell, 18:104–118.
58.
HirayamaT., ShinozakiK.2010. Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J, 61:1041–1052.
59.
HoboT., KowyamaY., HattoriT.1999a. A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA, 96:15348–15353.
60.
HoboT., AsadaM., KowyamaY., HattoriT.1999b. ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J, 19:679–689.
61.
HossainM.A., ChoJ.I., HanM., AhnC.H., JeonJ.S., AnG.et al.2010a. The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice. J. Plant Physiol, 167:1512–1520.
62.
HossainM.A., LeeY., ChoJ.I., AhnC.H., LeeS.K., JeonJ.S.et al.2010b. The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signaling in rice. Plant Mol Biol, 72:557–566.
63.
HuH.H., DaiM.Q., YaoJ.L., XiaoB.Z., LiX.H., ZhangQ.F.et al.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.
64.
HuH.H., YouJ., FangY.J., ZhuX.Y., QiZ.Y., XiongL.Z.2008a. Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol, 67:169–181.
65.
HuY., ChongK., WangT.2008b. OsRAF is an ethylene responsive and root abundant factor gene of rice. Plant Growth Reg, 54:55–61.
66.
HuY., QinF., HuangL., SunQ., LiC., ZhaoY.et al.2009. Rice histone deacetylase genes display specific expression patterns and developmental functions. Biochem Biophys Res Commun, 388:266–271.
67.
HuangJ., YangX., WangM.M., TangH.J., DingL.Y., ShenY.et al.2007. A novel rice C2H2-type zinc finger protein lacking DLN-box/EAR-motif plays a role in salt tolerance. Biochim Biophys Acta, 1769:220–227.
68.
HuangJ., SunS.J., XuD.Q., YangX., BaoY.M., WangZ.F.et al.2009a. Increased tolerance of rice to cold, drought and oxidative stresses mediated by the overexpression of a gene that encodes the zinc finger protein ZFP245. Biochem Biophys Res Commun, 389:556–561.
69.
HuangX.Y., ChaoD.Y., GaoJ.P., ZhuM.Z., ShiM., LinH.X.2009b. A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev, 23:1805–1817.
70.
IkedaY., KinoshitaT.2009. DNA demethylation: a lesson from the garden. Chromosoma, 118:37–41.
71.
IlegemsM., DouetV., Meylan-BettexM., UyttewaalM., BrandL., BowmanJ.L.et al.2010. Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation. Development, 137:975–984.
72.
IshiguroS., NakamuraK.1994. Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 5′ upstream regions of genes coding for sporamin and beta-amylase from sweet potato. Mol Gen Genet, 244:563–571.
73.
ItoY., KatsuraK., MaruyamaK., TajiT., KobayashiM., SekiM.et al.2006. Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol, 47:141–153.
74.
IvenT., StrathmannA., BottnerS., ZwafinkT., HeinekampT., Guivarc'hA.et al.2010. Homo- and heterodimers of tobacco bZIP proteins counteract as positive or negative regulators of transcription during pollen development. Plant J, 63:155–166.
75.
JainM., TyagiA.K., KhuranaJ.P.2008. Genome-wide identification, classification, evolutionary expansion and expression analyses of homeobox genes in rice. FEBS J, 275:2845–2861.
JayaniR.S., RamanujamP.L., GalandeS.2010. Studying histone modifications and their genomic functions by employing chromatin immunoprecipitation and immunoblotting. Methods Cell Biol, 98:35–56.
78.
JeB.I., PiaoH.L., ParkS.J., ParkS.H., KimC.M., XuanY.H.et al.2010. RAV-Like1 maintains brassinosteroid homeostasis via the coordinated activation of BRI1 and biosynthetic genes in rice. Plant Cell, 22:1777–1791.
79.
JenuweinT., AllisC.D.2001. Translating the histone code. Science, 293:1074–1080.
80.
JeongJ.S., KimY.S., BaekK.H., JungH., HaS.H., Do ChoiY.et al.2010. Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol, 153:185–197.
81.
JinH., MartinC.1999. Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol, 41:577–585.
82.
JohannessonH., WangY., HansonJ., EngstromP.2003. The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings. Plant Mol Biol, 51:719–729.
83.
JohnsonL.M., BostickM., ZhangX., KraftE., HendersonI., CallisJ.et al.2007. The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol, 17:379–384.
KimJ.M., ToT.K., IshidaJ., MorosawaT., KawashimaM., MatsuiA.et al.2008a. Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol, 49:1580–1588.
87.
KimK.C., LaiZ., FanB., ChenZ.2008b. Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell, 20:2357–2371.
88.
KotakS., PortM., GanguliA., BickerF., Von Koskull-DoringP.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.
89.
KwonC.S., LeeD., ChoiG., ChungW.I.2009. Histone occupancy-dependent and -independent removal of H3K27 trimethylation at cold-responsive genes in Arabidopsis. Plant J, 60:112–121.
90.
LabraM., GhianiA., CitterioS., SgorbatiS., SalaF., VanniniC.et al.2002. Analysis of cytosine methylation pattern in response to water deficit in pea root tips. Plant Biol, 4:694–699.
91.
Lang-MladekC., PopovaO., KiokK., BerlingerM., RakicB., AufsatzW.et al.2010. Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in Arabidopsis. Mol Plant, 3:594–602.
92.
LiC., ChenQ., GaoX., QiB., ChenN., XuS.et al.2005. AtHsfA2 modulates expression of stress responsive genes and enhances tolerance to heat and oxidative stress in Arabidopsis. Sci China C Life Sci, 48:540–550.
LiH.Y., ChangC.S., LuL.S., LiuC.A., ChanM.T., CharngY.Y.2003. Over-expression of Arabidopsis thaliana heat shock factor gene (AtHsf1b) enhances chilling tolerance in transgenic tomato. Botan Bull Acad Sin, 44:129–140.
95.
LiX., WangX., HeK., MaY., SuN., HeH.et al.2008. High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell, 20:259–276.
LinR.M., ZhaoW.S., MengX.B., WangM., PengY.L.2007. Rice gene OsNAC19 encodes a novel NAC-domain transcription factor and responds to infection by Magnaporthe grisea. Plant Sci, 172:120–130.
98.
Lira-MedeirosC.F., ParisodC., FernandesR.A., MataC.S., CardosoM.A., FerreiraP.C.G.2010. Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS ONE, 5:e10326.
99.
LiuA.L., ZouJ., ZhangX.W., ZhouX.Y., WangW.F., XiongX.Y.et al.2010. Expression profiles of Class A rice heat shock transcription factor genes under abiotic stresses. J Plant Biol, 53:142–149.
100.
LiuJ.G., QinQ.L., ZhangZ., PengR.H., XiongA.S., ChenJ.M.et al.2009. OsHSF7 gene in rice, Oryza sativa L., encodes a transcription factor that functions as a high temperature receptive and responsive factor. BMB Rep, 42:16–21.
101.
LuG., GaoC.X., ZhengX.N., HanB.2009. Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta, 229:605–615.
102.
LusserA., BroschG., LoidlA., HaasH., LoidlP.1997. Identification of maize histone deacetylase HD2 as an acidic nucleolar phosphoprotein. Science, 277:88–91.
103.
MaQ., DaiX., XuY., GuoJ., LiuY., ChenN.et al.2009. Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. Plant Physiol, 150:244–256.
104.
MadlungA., ComaiL.2004. The effect of stress on genome regulation and structure. Ann Bot, 94:481–495.
105.
MagnaniE., SjolanderK., HakeS.2004. From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. Plant Cell, 16:2265–2277.
106.
MaierA.T., Stehling-SunS., WollmannH., DemarM., HongR.L., HaubeissS.et al.2009. Dual roles of the bZIP transcription factor PERIANTHIA in the control of floral architecture and homeotic gene expression. Development, 136:1613–1620.
107.
MaruyamaK., SakumaY., KasugaM., ItoY., SekiM., GodaH.et al.2004. Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J, 38:982–993.
108.
MatsukuraS., MizoiJ., YoshidaT., TodakaD., ItoY., MaruyamaK.et al.2010. Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol Genet Genomics, 283:185–196.
109.
MattanaM., BiazziE., ConsonniR., LocatelliF., VanniniC., ProveraS.et al.2005. Overexpression of Osmyb4 enhances compatible solute accumulation and increases stress tolerance of Arabidopsis thaliana. Physiol Plant, 125:212–223.
110.
McClintockB.1984. The significance of responses of the genome to challenge. Science, 226:792–801.
111.
MeijerA.H., De KamR.J., D'ErfurthI., ShenW., HogeJ.H.2000. HD-Zip proteins of families I and II from rice: interactions and functional properties. Mol Gen Genet, 263:12–21.
112.
MeyerP.2010. DNA methylation systems and targets in plants. FEBS Lett, 585:2008–2015.
113.
MittalD., ChakrabartiS., SarkarA., SinghA., GroverA.2009. Heat shock factor gene family in rice: genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiol Biochem, 47:785–795.
114.
MittlerR., KimY., SongL.H., CoutuJ., CoutuA., Ciftci-YilmazS.et al.2006. Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett, 580:6537–6542.
115.
MundyJ., YamaguchishinozakiK., ChuaN.H.1990. Nuclear proteins bind conserved elements in the abscisic acid-responsive promoter of a rice RAB gene. Proc Natl Acad Sci USA, 87:1406–1410.
116.
NakamuraS., LynchT.J., FinkelsteinR.R.2001. Physical interactions between ABA response loci of Arabidopsis. Plant J, 26:627–635.
117.
NakashimaK., TranL.S.P., Van NguyenD., FujitaM., MaruyamaK., TodakaD.et al.2007. Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J, 51:617–630.
118.
NakashimaK., ItoY., Yamaguchi-ShinozakiK.2009. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol, 149:88–95.
119.
NuruzzamanM., ManimekalaiR., SharoniA.M., SatohK., KondohH., OokaH.et al.2010. Genome-wide analysis of NAC transcription factor family in rice. Gene, 465:30–44.
120.
OhS.J., KimY.S., KwonC.W., ParkH.K., JeongJ.S., KimJ.K.2009. Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol, 150:1368–1379.
121.
OhmetakagiM., ShinshiH.1995. Ethylene-inducible DNA-binding proteins that interact with an ethylene-responsive element. Plant Cell, 7:173–182.
122.
OhnishiT., SugaharaS., YamadaT., KikuchiK., YoshibaY., HiranoH.Y.et al.2005. OsNAC6, a member of the NAC gene family, is induced by various stresses in rice. Genes Genet Syst, 80:135–139.
PandeyR., MullerA., NapoliC.A., SelingerD.A., PikaardC.S., RichardsE.J.et al.2002. Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res, 30:5036–5055.
125.
PasqualiG., BiricoltiS., LocatelliF., BaldoniE., MattanaM.2008. Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples. Plant Cell Rep, 27:1677–1686.
126.
PavangadkarK., ThomashowM.F., TriezenbergS.J.2010. Histone dynamics and roles of histone acetyltransferases during cold-induced gene regulation in Arabidopsis. Plant Mol Biol, 74:183–200.
127.
PavletichN.P., PaboC.O.1991. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science, 252:809–817.
128.
PecinkaA., DinhH.Q., BaubecT., RosaM., LettnerN., Mittelsten ScheidO.2010a. Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell, 22:3118–3129.
129.
PecinkaA., DinhH.Q., BaubecT., RosaM., LettnerN., ScheidO.M.2010b. Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell, 22:3118–3129.
130.
PelhamH.R.1982. A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene. Cell, 30:517–528.
131.
Pena-CastroJ.M., Van ZantenM., LeeS.C., PatelM.R., VoesenekL.A., FukaoT.et al.2011. Expression of rice SUB1A and SUB1C transcription factors in Arabidopsis uncovers flowering inhibition as a submergence-tolerance mechanism. Plant J.
132.
PengS., HuangJ., SheehyJ.E., LazaR.C., VisperasR.M., ZhongX.et al.2004. Rice yields decline with higher night temperature from global warming. Proc Natl Acad Sci USA, 101:9971–9975.
133.
QinF.J., SunQ.W., HuangL.M., ChenX.S., ZhouD.X.2010. Rice SUVH histone methyltransferase genes display specific functions in chromatin modification and retrotransposon repression. Mol Plant, 3:773–782.
134.
QinQ.L., LiuJ.G., ZhangZ., PengR.H., XiongA.S., YaoQ.H.et al.2007. Isolation, optimization, and functional analysis of the cDNA encoding transcription factor OsDREB1B in Oryza sativa L. Mol Breed, 19:329–340.
135.
QiuD., XiaoJ., DingX., XiongM., CaiM., CaoY.et al.2007. OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol Plant Microbe Interact, 20:492–499.
136.
QiuD., XiaoJ., XieW., LiuH., LiX., XiongL.et al.2008. Rice gene network inferred from expression profiling of plants overexpressing OsWRKY13, a positive regulator of disease resistance. Mol Plant, 1:538–551.
137.
QiuD.Y., XiaoJ., XieW.B., ChengH.T., LiX.H., WangS.P.2009. Exploring transcriptional signalling mediated by OsWRKY13, a potential regulator of multiple physiological processes in rice. BMC Plant Biol, 9.
138.
QiuY.P., YuD.Q.2009. Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ Exp Bot, 65:35–47.
139.
QiuY.P., JingS.J., FuJ., LiL., YuD.Q.2004. Cloning and analysis of expression profile of 13 WRKY genes in rice. Chin Sci Bull, 49:2159–2168.
140.
RamamoorthyR., JiangS.Y., KumarN., VenkateshP.N., RamachandranS.2008. A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol, 49:865–879.
141.
RubertiI., SessaG., LucchettiS., MorelliG.1991. A novel class of plant proteins containing a homeodomain with a closely linked leucine zipper motif. EMBO J, 10:1787–1791.
142.
RushtonP.J., MacDonaldH., HuttlyA.K., LazarusC.M., HooleyR.1995. Members of a new family of DNA-binding proteins bind to a conserved cis-element in the promoters of alpha-Amy2 genes. Plant Mol Biol, 29:691–702.
RyuH.S., HanM., LeeS.K., ChoJ.I., RyooN., HeuS.et al.2006. A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep, 25:836–847.
145.
SaiboN.J., LourencoT., OliveiraM.M.2009. Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot, 103:609–623.
146.
SakamotoH., MaruyamaK., SakumaY., MeshiT., IwabuchiM., ShinozakiK.et al.2004. Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol, 136:2734–2746.
147.
SakumaY., LiuQ., DubouzetJ.G., AbeH., ShinozakiK., Yamaguchi-ShinozakiK.2002. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun, 290:998–1009.
148.
SantosA.P., FerreiraL., MarocoJ., OliveiraM.M.2011. Abiotic stress and induced DNA hypomethylation cause interphase chromatin structural changes in rice rDNA loci. Cytogenet Genome Res, 132:297–303.
149.
SchrammF., LarkindaleJ., KiehlmannE., GanguliA., EnglichG., VierlingE.et al.2008. A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J, 53:264–274.
150.
ServetC., SilvaN.C.E., ZhouD.X.2010. Histone acetyltransferase AtGCN5/HAG1 is a versatile regulator of developmental and inducible gene expression in Arabidopsis. Mol Plant, 3:670–677.
151.
SharmaR., Mohan SinghR.K., MalikG., DeveshwarP., TyagiA.K., KapoorS.et al.2009. Rice cytosine DNA methyltransferases—gene expression profiling during reproductive development and abiotic stress. FEBS J, 276:6301–6311.
152.
ShimonoM., SuganoS., NakayamaA., JiangC.J., OnoK., TokiS.et al.2007. Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell, 19:2064–2076.
153.
ShobbarZ.S., OaneR., GamuyaoR., De PalmaJ., MalboobiM.A., KarimzadehG.et al.2008. Abscisic acid regulates gene expression in cortical fiber cells and silica cells of rice shoots. New Phytol, 178:68–79.
154.
SokolA., KwiatkowskaA., JerzmanowskiA., Prymakowska-BosakM.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.
155.
SongC.P., GalbraithD.W.2006. AtSAP18, an orthologue of human SAP18, is involved in the regulation of salt stress and mediates transcriptional repression in Arabidopsis. Plant Mol Biol, 60:241–257.
156.
SongC.P., AgarwalM., OhtaM., GuoY., HalfterU., WangP.et al.2005. Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell, 17:2384–2396.
157.
SongX.J., MatsuokaM.2009. Bar the windows: an optimized strategy to survive drought and salt adversities. Genes Dev, 23:1709–1713.
158.
SongY., JingS.J., YuD.Q.2009. Overexpression of the stress-induced OsWRKY08 improves osmotic stress tolerance in Arabidopsis. Chin Sci Bull, 54:4671–4678.
159.
SouerE., VanhouwelingenA., KloosD., MolJ., KoesR.1996. The no apical meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell, 85:159–170.
160.
StewardN., ItoM., YamaguchiY., KoizumiN., SanoH.2002. Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. J Biol Chem, 277:37741–37746.
161.
StockingerE.J., MaoY., RegierM.K., TriezenbergS.J., ThomashowM.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, 29:1524–1533.
162.
StrackeR., WerberM., WeisshaarB.2001. The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol, 4:447–456.
163.
StrahlB.D., AllisC.D.2000. The language of covalent histone modifications. Nature, 403:41–45.
164.
SuC.F., WangY.C., HsiehT.H., LuC.A., TsengT.H., YuS.M.2010. A novel MYBS3-dependent pathway confers cold tolerance in rice. Plant Physiol, 153:145–158.
TakasakiH., MaruyamaK., KidokoroS., ItoY., FujitaY., ShinozakiK.et al.2010. The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics, 284:173–183.
167.
TakatsujiH., MoriM., BenfeyP.N., RenL., ChuaN.H.1992. Characterization of a zinc finger DNA-binding protein expressed specifically in Petunia petals and seedlings. EMBO J, 11:241–249.
168.
TanakaM., TakahataY., NakayamaH., NakataniM., TaharaM.2009. Altered carbohydrate metabolism in the storage roots of sweet potato plants overexpressing the SRF1 gene, which encodes a Dof zinc finger transcription factor. Planta, 230:737–746.
169.
TaoZ., LiuH., QiuD., ZhouY., LiX., XuC.et al.2009. A pair of allelic WRKY genes play opposite roles in rice-bacteria interactions. Plant Physiol, 151:936–948.
TranL.P., NishiyamaR., Yamaguchi-ShinozakiK., ShinozakiK.2010. Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM Crops, 1:32–39.
172.
TranL.S.P., NakashimaK., SakumaY., OsakabeY., QinF., SimpsonS.D.et al.2006. Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. Plant J, 49:46–63.
173.
TsujiH., SaikaH., TsutsumiN., HiraiA., NakazonoM.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.
174.
TutejaN., SoporyS.K.2008. Chemical signaling under abiotic stress environment in plants. Plant Signal Behav, 3:525–536.
175.
UnoY., FurihataT., AbeH., YoshidaR., ShinozakIK., Yamaguchi-ShinozakiK.2000. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA, 97:11632–11637.
176.
Van DijkK., DingY., MalkaramS., RiethovenJ.J.M., LiuR., YangJ.Y.et al.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.
177.
VanniniC., LocatelliF., BracaleM., MagnaniE., MarsoniM., OsnatoM.et al.2004. Overexpression of the rice Osmyb4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants. Plant J, 37:115–127.
178.
VanniniC., IritiM., BracaleM., LocatelliF., FaorodF., CroceaP.et al.2006. The ectopic expression of the rice Osmyb4 gene in Arabidopsis increases tolerance to abiotic, environmental and biotic stresses. Physiol Mol Plant Pathol, 69:26–42.
VernoudV., LaigleG., RozierF., MeeleyR.B., PerezP., RogowskyP.M.2009. The HD-ZIP IV transcription factor OCL4 is necessary for trichome patterning and anther development in maize. Plant J, 59:883–894.
181.
VogelJ.T., ZarkaD.G., Van BuskirkH.A., FowlerS.G., ThomashowM.F.2005. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J, 41:195–211.
182.
WangD., PanY., ZhaoX., ZhuL., FuB., LiZ.2011a. Genome-wide temporal-spatial gene expression profiling of drought responsiveness in rice. BMC Genomics, 12:149.
183.
WangQ.Y., GuanY.C., WuY.R., ChenH.L., ChenF., ChuC.C.2008. Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol Biol, 67:589–602.
184.
WangW.-S., PanY.-J., ZhaoX.-Q., DwivediD., ZhuL.-H., AliJ.et al.2011b. Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.)J Exp Bot, 62:1951–1960.
185.
WangX., EllingA.A., LiX., LiN., PengZ., HeG.et al.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.
186.
WangY., HenrikssonE., SodermanE., HenrikssonK.N., SundbergE., EngstromP.2003. The Arabidopsis homeobox gene, ATHB16, regulates leaf development and the sensitivity to photoperiod in Arabidopsis. Dev Biol, 264:228–239.
187.
WindhovelA., HeinI., DabrowaR., StockhausJ.2001. Characterization of a novel class of plant homeodomain proteins that bind to the C4 phosphoenolpyruvate carboxylase gene of Flaveria trinervia. Plant Mol Biol, 45:201–214.
188.
WinterS., FischleW.2010. Epigenetic markers and their cross-talk. Essays Biochem, 48:45–61.
WuC., YouC., LiC., LongT., ChenG., ByrneM.E.et al.2008. RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice. Proc Natl Acad Sci USA, 105:12915–12920.
191.
WuL., ChenX., RenH., ZhangZ., ZhangH., WangJ.et al.2007. ERF protein JERF1 that transcriptionally modulates the expression of abscisic acid biosynthesis-related gene enhances the tolerance under salinity and cold in tobacco. Planta, 226:815–825.
192.
WuX., ShirotoY., KishitaniS., ItoY., ToriyamaK.2009. Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep, 28:21–30.
193.
XiangY., TangN., DuH., YeH.Y., XiongL.Z.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.
194.
XieZ., ZhangZ.L., ZouX., HuangJ., RuasP., ThompsonD.et al.2005. Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol, 137:176–189.
195.
XuD.Q., HuangJ., GuoS.Q., YangX., BaoY.M., TangH.J.et al.2008a. Overexpression of a TFIIIA-type zinc finger protein gene ZFP252 enhances drought and salt tolerance in rice (Oryza sativa L.)FEBS Lett, 582:1037–1043.
196.
XuK., XuX., FukaoT., CanlasP., Maghirang-RodriguezR., HeuerS.et al.2006. Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature, 442:705–708.
197.
XuZ.S., ChenM., LiL.C., MaY.Z.2008b. Functions of the ERF transcription factor family in plants. Botany-Botanique, 86:969–977.
198.
XuZ.S., XiaL.Q., ChenM., ChengX.G., ZhangR.Y., LiL.C.et al.2007. Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol, 65:719–732.
199.
Yamaguchi-ShinozakiK., ShinozakiK.2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol, 57:781–803.
200.
YamauchiT., MoritohS., Johzuka-HisatomiY., OnoA., TeradaR., NakamuraI.et al.2008. Alternative splicing of the rice OsMET1 genes encoding maintenance DNA methyltransferase. J Plant Physiol, 165:1774–1782.
201.
YamasakiK., KigawaT., InoueM., TatenoM., YamasakiT., YabukiT.et al.2005. Solution structure of an Arabidopsis WRKY DNA binding domain. Plant Cell, 17:944–956.
202.
YanH., KikuchiS., NeumannP., ZhangW., WuY., ChenF.et al.2010. Genome-wide mapping of cytosine methylation revealed dynamic DNA methylation patterns associated with genes and centromeres in rice. Plant J, 63:353–365.
203.
YangX.D., YangY.N.M., XueL.J.D., ZouM.J., LiuJ.J.D., ChenF.P.et al.2011. Rice ABI5-like1 Regulates ABA and auxin responses by affecting the expression of ABRE-containing genes. Plant Physiol, 156:1397–1409.
204.
YiS.Y., KimJ.H., JoungY.H., LeeS., KimW.T., YS.H.et al.2004. The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis. Plant Physiol, 136:2862–2874.
205.
YokotaniN., IchikawaT., KondouY., MatsuiM., HirochikaH., IwabuchiM.et al.2008. Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta, 227:957–967.
206.
YokotaniN., IchikawaT., KondouY., MatsuiM., HirochikaH., IwabuchiM.et al.2009. Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic Arabidopsis. Planta, 229:1065–1075.
207.
YuS., LigangC., LipingZ., DiqiuY.2010. Overexpression of OsWRKY72 gene interferes in the abscisic acid signal and auxin transport pathway of Arabidopsis. J Biosci, 35:459–471.
208.
ZhangM., KimatuJ.N., XuK., LiuB.2010. DNA cytosine methylation in plant development. J Gen Genom, 37:1–12.
209.
ZhangX.2008. The epigenetic landscape of plants. Science, 320:489–492.
210.
ZhangX., YazakiJ., SundaresanA., CokusS., ChanS.W.-L., ChenH.et al.2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell, 126:1189–1201.
211.
ZhangX., WangL., MengH., WenH., FanY., ZhaoJ.2011. Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species. Plant Mol Biol, 75:365–378.
212.
ZhangY., ChenC., JinX.F., XiongA.S., PengR.H., HongY.H.et al.2009. Expression of a rice DREB1 gene, OsDREB1D, enhances cold and high-salt tolerance in transgenic Arabidopsis. BMC Rep, 42:486–492.
213.
ZhaoL., HuY., ChongK., WangT.2010. ARAG1, an ABA-responsive DREB gene, plays a role in seed germination and drought tolerance of rice. Ann Bot, 105:401–409.
214.
ZhengX.N., ChenB., LuG.J., HanB.2009. Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem Biophys Res Commun, 379:985–989.
215.
ZhongL., XuY.-H., WangJ.-B.2009. DNA-methylation changes induced by salt stress in wheat Triticum aestivum. Afr J Biotech, 8:6201–6207.
216.
ZhouD.X.2009. Regulatory mechanism of histone epigenetic modifications in plants. Epigenetics, 4:15–18.
217.
ZhouJ., TangX., MartinG.B.1997. The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J, 16:3207–3218.
218.
ZhouJ., LiF., WangJ.L., MaY., ChongK., XuY.Y.2009. Basic helix-loop-helix transcription factor from wild rice (OrbHLH2) improves tolerance to salt- and osmotic stress in Arabidopsis. J. Plant Physiol, 166:1296–1306.
219.
ZhuJ., JeongJ.C., ZhuY., SokolchikI., MiyazakiS., ZhuJ.K.et al.2008. Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc Natl Acad Sci USA, 105:4945–4950.
220.
ZilbermanD., GehringM., TranR.K., BallingerT., HenikoffS.2007. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet, 39:61–69.
221.
ZouM.J., GuanY.C., RenH.B., ZhangF., ChenF.2007. Characterization of alternative splicing products of bZIP transcription factors OsABI5. Biochem Biophys Res Commun, 360:307–313.
222.
ZouM.J., GuanY.C., RenH.B., ZhangF., ChenF.2008. A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol Biol, 66:675–683.
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