Abstract
Overall transcriptomic activity of an organism is determined not only by its genetic makeup but also by epigenetic regulations. Reprogramming by epigenetic modification triggered by various environmental challenges contributes to the phenotypic diversity and defense against these challenges. Different stresses acts as stimulus and changes genic expression level by various mechanisms namely DNA methylation, histone modifications and miRNA. Epigenetics is a continuously progressing branch since the past two decades. Improvement of crop varieties with traditional breeding methods is tedious, time consuming, expensive and is unable to meet progressive living standards and demand in today’s world whereas epigenetics holds great potential for the improvement of plant varieties with respect to yield and nutritional quality by creation of novel epialleles, transgenic RNAi. RNA interference has been used for the improvement of several crops like barley, wheat, soybean etc by reduction of various anti-nutritive factors or enhancement of flavor. Silencing of Omega–3 fatty acid desaturase gene is achieved using RNAi technology for the reduction of linoleic acid and improvement of flavor. HvTX1 from barley shows increased expression during drought stress indicating its active role in drought tolerance which further can be exploited for the development of improved crop variety with increased drought tolerance. Also multiple HAT genes in rice are reported to be actively expressed under heat and water stress. Studies of epigenetic responses to different stresses can increase our understanding of plant stress adaptation and mechanism underlying them which can be further exploited for the development of improved crop varieties.
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Alexandre C, Möller-Steinbach Y, Schönrock N, Gruissem W, Hennig L (2009) Arabidopsis MSI1 Is Required for Negative Regulation of the Response to Drought Stress. Mol Plant 2:675–687
An J, Lai J, Lehman ML, Nelson CC (2013) miRDeep *: an integrated application tool for miRNA identification from RNA sequencing data. Nucleic Acids Res 41:727–737
Barrera-Figueroa BE, Gao L, Diop NN, Wu Z, Ehlers JD, Roberts PA, Close TJ, Zhu J, Liu R (2011) Identification and comparative analysis of drought-associated microRNAs in two cowpea genotypes. BMC Plant Biol 11:127
Berr A, Ménard R, Heitz T, Shen W-H (2012) Chromatin modification and remodelling: a regulatory landscape for the control of Arabidopsis defence responses upon pathogen attack. Cell Microbiol 14:829–839
Budak H, Akpinar BA (2015) Plant miRNAs: biogenesis, organization and origins. Funct Integr Genomics 15:523–531
Butardo VM, Fitzgerald MA, Bird AR, Gidley MJ, Flanagan BM, Larroque O, Resurreccion AP, Laidlaw HKC, Jobling SA, Morell MK, Rahman S (2011) Impact of down-regulation of starch branching enzyme IIb in rice by artificial microRNA-and hairpin RNA-mediated RNA silencing. J Exp Bot 62:4927–4941
Camporeale G, Oommen AM, Griffin JB, Sarath G, Zempleni J (2007) K12-biotinylated histone H4 marks heterochromatin in human lymphoblastoma cells. J Nutr Biochem 18:760–768
Centomani I, Sgobba A, D’Addabbo P, Dipierro N, Paradiso A, de Gara L, Dipierro S, Viggiano L, de Pinto MC (2015) Involvement of DNA methylation in the control of cell growth during heat stress in tobacco BY-2 cells. Protoplasma 252:1451–1459
Chen L, Wu K (2010) Role of histone deacetylases HDA6 and HDA19 in ABA and abiotic stress response. Plant Signalling & Behaviour 5:1318–1320
Chen LT, Luo M, Wang YY, Wu K (2010) Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot 61:3345–3353
Chen Z, Zhang H, Jablonowski D, Zhou X, Ren X, Hong X, Schaffrath R, Zhu JK, Gong Z (2006) Mutations in ABO1/ELO2, a Subunit of Holo-Elongator, Increase Abscisic Acid Sensitivity and Drought Tolerance in Arabidopsis thaliana. Mol Cell Biol 26:6902–6912
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 277:589–600
Da-hong L, Hui LIU, Yan-li YANG, Ping-ping ZHEN, Jian-sheng LI (2009) Down-Regulated Expression of RACK1 Gene by RNA Interference Enhances Drought Tolerance in Rice 16:14–20
Deleris A, Stroud H, Bernatavichute Y, Johnson E, Klein G, Schubert D, Jacobsen SE (2012) Loss of the DNA Methyltransferase MET1 Induces H3K9 Hypermethylation at PcG Target Genes and Redistribution of H3K27 Trimethylation to Transposons in Arabidopsis thaliana. PLoS Genet. 8, e1003062
Ding Y, Avramova Z, Fromm M (2011) The Arabidopsis trithoraxlike factor ATX1 functions in dehydration stress responses via ABA-dependent and ABA-independent pathways. Plant J 66:735–744
Dyachenko O V, Zakharchenko NS, Shevchuk T V, Bohnert HJ, Cushman JC, Buryanov YI (2006) Effect of hypermethylation of CCWGG sequences in DNA of Mesembryanthemum crystallinum plants on their adaptation to salt stress. Biochem Biokhimiia 71:461–465
Earley KW, Shook MS, Brower-Toland B, Hicks L, Pikaard CS (2007) In vitro specificities of Arabidopsis co-activator histone acetyltransferases: implications for histone hyperacetylation in gene activation. Plant J 52:615–626
Fang H, Liu X, Thorn G, Duan J, Tian L (2014) Biochemical and Biophysical Research Communications Expression analysis of histone acetyltransferases in rice under drought. Biochem Biophys Res Commun 443:400–405
Feng S, Jacobsen SE, Reik W (2010) Epigenetic Reprogramming in Plant and Animal Development. Science (80-) 330:622–627
Ferdous J, Sanchez-Ferrero JC, Langridge P, Milne L, Chowdhury J, Brien C, Tricker PJ (2016) Differential expression of microRNAs and potential targets under drought stress in barley. Plant Cell Environ 40:11–24
Ferreira H, Gentile A, Vilela RD, Gilson G, Costa L (2012) microRNAs Associated with Drought Response in the Bioenergy Crop Sugarcane (Saccharum spp.). PLoS One 7:14
Flores T, Karpova O, Su X, Zeng P, Bilyeu K, Sleper DA, Nguyen HT, Zhang ZJ (2008) Silencing ofGmFAD3 gene by siRNA leads to low a-linolenic acids (18:3) of fad3-mutant phenotype in soybean [Glycine max (Merr.)]. Transgenic Res 17:839–850
Folsom JJ, Begcy K, Hao X, Wang D, Walia H (2014) Rice Fertilization-Independent Endosperm1 Regulates Seed Size under Heat Stress by Controlling Early. Plant Physiol 165:238–248
González RM, Ricardi MM, Iusem ND (2013) Epigenetic marks in an adaptive water stress-responsive gene in tomato roots under normal and drought conditions. Epigenetics 8:1–9
González RM, Ricardi MM, Iusem ND (2011) Atypical epigenetic mark in an atypical location: cytosine methylation at asymmetric (CNN) sites within the body of a non-repetitive tomato gene. BMC Plant Biol 11:94
Guan Q, Lu X, Zeng H, Zhang Y, Zhu J (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. plant J 74:12
Hajyzadeh M, Turktas M, Mahmood K, Unver T (2015) miR408 overexpression causes increased drought tolerance in chickpea. Gene 555:186–193
Hu Y, Qin F, Huang L, Sun Q, Li C, Zhao Y, Zhou D (2009) Biochemical and Biophysical Research Communications Rice histone deacetylase genes display specific expression patterns and developmental functions. Biochem Biophys Res Commun 388:266–271
Kantar M, Lucas SJ, Budak H (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233:471–484
Kim J, To TK, 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 49:1580–1588
Kozomara A, Griffiths-jones S (2010) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 1–6
Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci U S A 101:12753–12758
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 4:694–699
Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220
Lee RC, Feinbaum RL, Harvard VA (1993) The C. elegans Heterochronic Gene lin-4 Encodes Small RNAs with Antisense Complementarity to & II-14. Cell 75:843–854
Li W, Oono Y, Zhu J, He X, Wu J, Iida K, Lu X, Cui X, Jin H, Zhu J (2008) The Arabidopsis NFYA5 Transcription Factor Is Regulated Transcriptionally and Posttranscriptionally to Promote Drought Resistance. Plant Cell 20:2238–2251
Li X, Zhu J, Hu F, Ge S, Ye M, Xiang H, Zhang G, Zheng X, Zhang H, Zhang S, Li Q, Luo R, Yu C, Yu J, Sun J, Zou X, Cao X, Xie X, Wang J, Wang W (2012) Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genomics 13:300
Liang D, Zhang Z, Wu H, Huang C, Shuai P, Ye CY, Tang S, Wang Y, Yang L, Wang J, Yin W, Xia X (2014) Single-base-resolution methylomes of populus trichocarpa reveal the association between DNA methylation and drought stress. BMC Genet 15:S9
Liu C, Lu F, Cui X, Cao X (2010) Histone Methylation in Higher Plants. Annu Rev Plant Biol 61:395–420. doi: 10.1146/annurev. arplant.043008.091939
Liu X, Luo M, Zhang W, Zhao J, Zhang J, Wu K, Tian L, Duan J (2012) Histone acetyltransferases in rice (Oryza sativa L.): phylogenetic analysis, subcellular localization and expression. BMC Plant Biol 12:145
Liya Wei, Danfeng Zhang (2009) Differentially Expressed miRNAs Potentially Involved in the Regulation of Defense Mechanism to Drought Stress in Maize Seedlings. Int J Plant 170:979–989
Lu X, Wang W, Ren W, Chai Z, Guo W (2015) Genome-Wide Epigenetic Regulation of Gene Transcription in Maize Seeds. PLoS One 10:1–20. doi: 10.1371/journal.pone.0139582
Luo M, Wang YY, Liu X, Yang S, Lu Q, Cui Y, Wu K (2012) HD2C interacts with HDA6 and is involved in ABA and salt stress response in Arabidopsis. J Exp Bot 63:3297–3306
Mengel A, Ageeva A, Georgii E, Bernhardt J, Wu K, Durner J, Lindermayr C (2016) Nitric oxide modulates histone acetylation at stress genes by inhibition of histone deacetylases. Plant Physiol 1734
Nathan D, Ingvarsdottir K, Sterner DE, Bylebyl GR, Dokmanovic M, Dorsey JA, Whelan KA, Krsmanovic M, Lane WS, Meluh PB, Johnson ES, Berger SL (2006) Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev 20:966–976
Ni Z, Hu Z, Jiang Q, Zhang H (2013) GmNFYA3, a target gene of miR169, is a positive regulator of plant tolerance to drought stress. Plant Mol Biol 82:113–129
Papaefthimiou D, Tsaftaris AS (2012) Significant induction by drought of HvPKDM7-1, a gene encoding a jumonji-like histone demethylase homologue in barley (H. vulgare). Acta Physiol Plant 1187–1198
Park G, Park J, Yoon J, Yu S-N, An G (2010) A RING finger E3 ligase gene, Oryza sativa Delayed Seed Germination 1 (OsDSG1), controls seed germination and stress responses in rice. Plant Mol Biol 74:467–478
Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer Homolog, and HEN1, a Novel Protein, Act in microRNA Metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495
Qian Y, Xi Y, Cheng B, Zhu S, Kan X (2014) Identification and characterization of the SET domain gene family in maize. Mol Biol Report 3:1341–1354
Ragupathy R, Ravichandran S, Mahdi SR, Huang D, Reimer E, Domaratzki M, Cloutier S (2016) Deep sequencing of wheat sRNA transcriptome reveals distinct temporal expression pattern of miRNAs in response to heat, light and UV. Sci Rep 6:39373
Regina A, Bird A, Topping D, Bowden S, Freeman J, Barsby T, Kosar-Hashemi B, Li Z, Rahman S, Morell M (2010) Increasing the amylose content of durum wheat through silencing of the SBEIIa genes. BMC Plant Biol 10:144
Ruiz-ferrer V, Voinnet O (2009) Roles of Plant Small RNAs in Biotic Stress Responses. Annu Rev Plant Biol 60:485–510
Schijlen EGWM, Vos CHR De, Martens S, Jonker HH, Rosin FM, Molthoff JW, Tikunov YM, Angenent GC, Tunen AJ Van, Bovy AG (2007) RNA Interference Silencing of Chalcone Synthase, the First Step in the Flavonoid Biosynthesis Pathway, Leads to Parthenocarpic Tomato Fruits [C]. Plant Physiol 144:1520–1530
Schwartz YB, Kahn TG, Pirrotta V (2010) Polycomb and Trithorax Control Genome Expression by Determining the Alternative Chromatin Epigenetic States for Key Developmental Regulators. Russ J Genet 46:1247–1249
Scippa GS, Michele M Di, Onelli E, Patrignani G, Chiatante D, Bray EA, Studi Á (2004) The histone-like protein H1-S and the response of tomato leaves to water deficit. J Exp Bot 55:99–109
Shahbazian MD, Grunstein M (2007) Functions of Site-Specific Histone Acetylation and Deacetylation. Annu Rev Biochem 76:75–100
Shan X, Wang X, Yang G, Wu Y, Su S, Li S, Liu H, Yuan Y (2013) Analysis of the DNA methylation of maize (Zea mays L.) in response to cold stress based on methylation-sensitive amplified polymorphisms. J Plant Biol 56:32–38
Sharma R, Mohan Singh RK, Malik G, Deveshwar P, Tyagi AK, Kapoor S, Kapoor M (2009) Rice cytosine DNA methyltransferases -Gene expression profiling during reproductive development and abiotic stress. FEBS J 276:6301–6311
Song Y, Ji D, Li S, Wang P, Li Q, Xiang F (2012) The Dynamic Changes of DNA Methylation and Histone Modifications of Salt Responsive Transcription Factor Genes in Soybean. PLoS Genet 7:e41274
Sosa-valencia G, Palomar M, Covarrubias AA, Reyes JL (2016) The Legume miR1514a modulates a NAC transcription factor transcript to trigger phasiRNA formation in response to drought. J Exp Bot erw 380
Sridhar VV, Kapoor A, Zhang K, Zhu J, Zhou T, Hasegawa PM, Bressan RA, Zhu J (2007) Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature 447:735–740
Sterner DE, Berger SL (2000) Acetylation of Histones and Transcription-Related Factors. Microbiol Mol Biol Rev 64:435–459
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 277:37741–37746
Sunilkumar G, Campbell LM, Puckhaber L, Stipanovic RD, Rathore KS (2006) Engineering cottonseed for use in human nutrition by tissue-specific reduction of toxic gossypol. PNAS 103:18054–18059
Tan M (2010) Plant Physiology and Biochemistry Analysis of DNA methylation of maize in response to osmotic and salt stress based on methylation-sensitive ampli fi ed polymorphism. Plant Physiol Biochem 48:21–26
Tang N, Ma S, Zong W, Yang N, Lv Y, Yan C, Guo Z, Li J, Li X, Xiang Y, Song H, Xiao J, Li X, Xiong L (2016) MODD mediates deactivation and degradation of OsbZIP46 to negatively regulate ABA signaling and drought resistance in rice. Plant Cell 28:2161–2177
Thiebaut F, Rojas CA, Almeida KL, Grativol C, Domiciano GC, Lamb CRC, Engler JDEA, Hemerly AS, Ferreira PCG (2012) Regulation of miR319 during cold stress in sugarcane. Plant, Cell Environ 35:502–512
Versées W, Groeve S De, Lijsebettens M Van (2010) Micro Commentary Elongator, a conserved multitasking complex? Mol Microbiol 76:1065–1069
Vincenzo E, Russo A, Martienssen, A R (1998) Epigenetic Mechanisms of Gene Regulation. Q Rev Biol 73:210
Wang W, Pan Y, Zhao X, Dwivedi D, Zhu L, Ali J, Fu B, Li Z (2011) Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). J Exp Bot 62:1951–1960
Wang Y, Beaith M, Chalifoux M, Ying J, Uchacz T, Sarvas C, Griffiths R, Kuzma M, Wan J, Huang Y (2009) Shoot-Specific Down-Regulation of Protein Farnesyltransferase (a-Subunit) for Yield Protection against Drought in Canola. Mol Plant 2:191–200
Wei R, Qiu D, Wilson IW, Zhao H, Lu S, Miao J, Feng S (2015) Identification of novel and conserved microRNAs in Panax notoginseng roots by high-throughput sequencing. BMC Genomics 16:835–844
Wightman B, Ha L, Ruvkun G (1993) Posttranscriptional Regulation of the Heterochronic Gene lin-14 by W-4 Mediates Temporal Pattern Formation in C. elegans Bruce. Cell 75:855–862
Wu T, Pi E-X, Tsai S-N, Lam H-M, Sun S-M, Kwan YW, Ngai S-M (2011) GmPHD5 acts as an important regulator for crosstalk between histone H3K4 di-methylation and H3K14 acetylation in response to salinity stress in soybean. BMC Plant Biol 11:178–190
Yang C, Li D, Mao D, Ji C, Li X, Zhao X, Cheng Z, Chen C, Zhu L (2013) Change reference 6th to Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.) Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). 36:2207–2218
Yi R, Qin Y, Macara IG, Yi R, Qin Y, Macara IG, Cullen BR (2003) Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs service Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 17:3011–3016
Yu B, Yu B, Yang Z, Li J, Minakhina S, Yang M, Padgett RW, Steward R, Chen X (2012) Methylation as a Crucial Step in Plant microRNA Biogenesis. Science (80-) 932:932
Zhang X, Zou Z, Gong P, Zhang J, Ziaf K, Li H, Xiao F, Ye Z (2011) Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol Lett 33:403–409
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 (2014a) Transcriptional regulation of cell cycle genes in response to abiotic stresses correlates with dynamic changes in histone modifications in maize. PLoS One 9:e106070
Zhao L, Wang P, Yan S, Gao F, Li H, Hou H, Zhang Q, Tan J, Li L (2014b) Promoter-associated histone acetylation is involved in the osmotic stress-induced transcriptional regulation of the maize ZmDREB2A gene. Physiol Plant 151:459–467
Zheng Y, Ding Y, Sun X, Xie S, Wang D, Liu X, Su L, Wei W, Pan L (2016) Histone deacetylase HDA9 negatively regulates salt and drought stress responsiveness in Arabidopsis. J Exp Bot 5:1703–1713
Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61:4157–4168
Zong W, Zhong X, You J (2013) Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress. Plant Mol Biol 175–188
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Saraswat, S., Yadav, A.K., Sirohi, P. et al. Role of epigenetics in crop improvement: Water and heat stress. J. Plant Biol. 60, 231–240 (2017). https://doi.org/10.1007/s12374-017-0053-8
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DOI: https://doi.org/10.1007/s12374-017-0053-8