Abstract
Stress is inevitable in the life cycle of living organisms, including plants. Being sessile, plants are more prone to the deleterious effects of environmental stress . Therefore, plants have developed complex mechanisms to survive under these challenging conditions. Tolerance , avoidance, and resistance are the three major strategies followed by plants to counter the recurring biotic and abiotic stresses . These mechanisms involve genes associated with several interconnected pathways, which lead them towards better stress tolerance . Plants resort to various modifications in their morphological traits, physiology, and so forth in response to stress. Modulations in various regulatory mechanisms, including epigenetic modifications, play a pivotal role in developing stress tolerance in plants. These involve changes in either the plant homeostasis or heritable changes in gene expression pattern. The trans-generational changes are brought about, more often, by dynamic changes in epigenetic marks rather than development of stress resistant alleles via gene mutation. A large number of stress resistant transgenics have been developed over the years all over the world. However, the traditional breeding has remained indispensable. Much emphasis has been laid on identification and characterization of stress resistance genes and developing transgenic crop varieties, while the epigenomic aspects have been given less importance. The present chapter focuses on the essential components of epigenetic machinery, different epigenetic alterations involved in conversion of active euchromatin to silent heterochromatin and vice versa during stress, and integration of epigenetic data with breeding programs to devise better strategies towards development of stress resistant crops.
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References
Ali GS, Reddy ASN (2008) Regulation of alternative splicing of pre-mRNAs by stresses. Nuclear pre-mRNA. Process plants. Springer, Berlin Heidelberg, pp 257–275
Ball MP, Li J, Gao Y, Lee J, Leproust E, Park IH, Xie B, Daley GQ, Church G (2009) Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat Biotechnol 27:361–368
Bezhani S, Winter C, Hershman S, Wagner JD, Kennedy JF, Kwon CS, Pfluger J, Su Y, Wagner D (2007) Unique, shared, and redundant roles for the Arabidopsis SWI/SNF chromatin remodeling ATPases BRAHMA and SPLAYED. Plant Cell 19:403–416
Bhardwaj AR, Joshi G, Kukreja B, Malik V, Arora P, Pandey R, Shukla RN et al (2015) Global insights into high temperature and drought stress regulated genes by RNA-Seq in economically important oilseed crop Brassica juncea. BMC Plant Biol 15:1–15
Bock C (2012) Analysing and interpreting DNA methylation data. Nat Rev Genetics 13:705–719
Bonasio R, Tu S, Reinberg D (2010) Molecular signals of epigenetic states. Science 330:612–616
Bourchis D, Voinnet O (2010) A small-RNA perspective on gametogenesis, fertilization, and early zygotic development. Science 330:617–622
Brzeski J, Jerzmanowski A (2003) Deficient in DNA methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors. J Biol Chem 278:823–828
Chen M, Lv S, Meng Y (2010) Epigenetic performers in plants. Dev Growth Differ 52:555–566
Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139
Chodavarapu RK, Feng S, Bernatavichute YV, Chen PY, Stroud H, Yu Y, Hetzel JA et al (2010) Relationship between nucleosome positioning and DNA methylation. Nature 466:388–392
Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S et al (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–219
Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161
Diekman J, Petracek M, Heard JE (2012) Drought tolerance through biotechnology: improving translation from the laboratory to farmers’ fields. Curr Opin Biotechnol 23:243–250
Dhar MK, Vishal P, Sharma R, Kaul S (2014) Epigenetic dynamics: role of epimarks and underlying machinery in plants exposed to abiotic stress. Int J Genomics 2014:187146. https://doi.org/10.1155/2014/187146
Dhar PK, Thwin CS, Tun K, Tsumoto Y, Maurer-Stroh S, Eisenhaber F, Surana U (2009) Synthesizing non-natural parts from natural genomic template. J Biol Eng 3(3):2. https://doi.org/10.1186/1754-1611-3-2
Dhawan R, Luo H, Foerster AM, Abu Qamar S, Du HN, Briggs SD, Scheid OM, Mengiste T (2009) HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis. Plant Cell 21:1000–1019
Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, Dixon JE, Ecker JR (2012) Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci USA 109:E2183–E2191
Dyachenko OV, Zakharchenko NS, Shevchuk TV, 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 (Mosc) 71:461–465
Eichten SR, Briskine R, Song J, Li Q, Swanson-Wagner R, Hermanson PJ, Waters AJ et al (2013) Epigenetic and genetic influences on DNA methylation variation in maize populations. Plant Cell 25:2783–2797
Feng S, Cokus SJ, Zhang X, Chen PY, Bostick M, Goll MG, Hetzel J et al (2010) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci 107:8689–8694
Fujimoto R, Sasaki T, Inoue H, Nishio T (2008) Hypomethylation and transcriptional reactivation of retrotransposon-like sequences in ddm1 transgenic plants of Brassica rapa. Plant Mol Biol 66:463–473
Gendrel A, Lippman Z, Yordan C, Colot V, Martienssen RA (2002) Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297:1871–1873
Gutzat R, Scheid OM (2012) Epigenetic responses to stress: triple defense? Curr Opin Plant Biol 15:568–573
Houben A, Demidov D, Caperta AD, Karimi R, Agueci F, Vlasenko L (2007) Phosphorylation of histone H3 in plants–a dynamic affair. Biochim Biophys Acta 1769(5–6):308–315
Jeggo PA, Holliday R (1986) Azacytidine-induced reactivation of a DNA repair gene in Chinese hamster ovary cells. Mol Cell Biol 6:2944–2949
Ji L, Neumann DA, Schmitz RJ (2015) Crop epigenomics: identifying, unlocking and harnessing cryptic variation in crop genomes. Mol Plant 8(6):860–870
Ji L, Sasaki T, Sun X, Ma P, Lewis ZA, Schmitz RJ (2014) Methylated DNA is over-represented in whole-genome bisulfite sequencing data. Front Genet 5:341
Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J et al (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5:e1000530
Johnson TB, Coghill RD (1925) Researches on pyrimidines. C111. The discovery of 5-methyl-cytosine in tuberculinic acid, the nucleic acid of the tubercle Bacillus1. J American Chem Soc 47:2838–2844
Khorasanizadeh S (2004) The nucleosome: from genomic organization to genomic regulation. Cell 116:259–272
Keqiang Wu, Zhang L, Zhou C, Chun-Wei Y, Chaikam V (2008) HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J Exp Bot 59(2):225–234
Kim K-C, Lai Z, Fan B, Chen Z (2008) Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20:2357–2371
Kim DH, Sung S (2012) Environmentaly coordinated epigenetic silencing of FLC by protein and long noncoding RNA components. Curr Opin Plant Biol 15:51–56
Kim JM, To TK, Ishida J, Matsui A, Kimura H, Seki M (2012) Transition of chromatin status during the process of recovery from drought stress in Arabidopsis thaliana. Plant Cell Physiol 53:847–856
Kosuke N, Kawagishi Y, Kawabe A, Sato M, Masuta Y, Kato A, Ito H (2017) Epigenetic regulation of a heat-activated retrotransposon in cruciferous vegetables. Epigenomes 1(1):7
Laird PW (2010) Principles and challenges of genome wide DNA methylation analysis. Nat Rev Genet 11:191–203
Lane AK, Niederhuth CE, Ji L, Schmitz RJ (2014) pENCODE: a plant encyclopedia of DNA elements. Annu Rev Genet 48:49–70
Lauria M, Rossi V (2011) Epigenetic control of gene regulation in plants. Biochimica et Biophysica Acta (BBA) 1809:369–378
Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220
Liang D, Zhang Z, Wu H, Huang C, Shuai P, Ye CY, Tang S et al (2014) Single-base-resolution methylomes of Populus trichocarpa reveal the association between DNA methylation and drought stress. BMC Genet 15:S9
Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133:523–536
Long Y, Xia W, Li R, Wang J, Shao M, Feng J, King GJ et al (2011) Epigenetic QTL mapping in Brassica napus. Genetics 189:1093–1102
Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–952
Margueron R, Trojer P, Reinberg D (2005) The key to development: interpreting the histone code? Curr Opin Genet Dev 15:163–176
McGhee JD, Felsenfeld G (1980) Nucleosome structure. Ann Rev Biochem 49:1115–1156
Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P et al (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553–560
Misook H, Danny W-KN, Wen-Hsiung L, Chen ZJ (2011) Coordinated histone modifications are associated with gene expression variation within and between species. Genome Res 21(4):590–598
Mlynarova L, Nap JP, Bisseling T (2007) The SWI/SNF chromatin remodelling gene AtCHR12 mediates temporary growth arrest in Arabidopsis thaliana upon perceiving environmental stress. Plant J 51:874–885
Narlikar GJ, Sundaramoorthy R, Owen-Hughes T (2013) Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154:490–503
Niederhuth CE, Schmitz RJ (2014) Covering your bases: inheritance of DNA methylation in plant genomes. Mol Plant 7:472–480
Osakabe Y, Osakabe K, Shinozaki K, Tran LSP (2014) Response of plants to water stress. Front Plant Sci 5:86
Parkin IAP, Koh C, Tang H, Robinson SJ, Kagale S, Clarke WE, Town CD et al (2014) Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol 15:R77
Pecinka A, Dinh HQ, Baubec T, Rosa M, Lettner N, Scheid OM (2010) Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell 22:3118–3129
Rando OJ (2012) Combinatorial complexity in chromatin structure and function: revisiting the histone code. Curr Opin Genet Dev 22:148–155
Reyna-Lopez GE, Simpson J, Ruiz-Herrera J (1997) Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Mol Gen Genet 253:703–710
Richards EJ (2006) Inherited epigenetic variation-revisiting soft inheritance. Nat Rev Genet 7:395–401
Robinson MD, Kahraman A, Law CW, Lindsay H, Nowicka M, Weber LM, Zhou X (2014) Statistical methods for detecting differentially methylated loci and regions. Front Genet 5:324
Roudier F, Ahmed I, Sarazin A, Mary-Huard T, Cortijo S, Bouyer D et al (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBOJ 30(10):1928–1938
Saze H (2008) Epigenetic memory transmission through mitosis and meiosis in plants. Semin Cell Dev Biol 19:527–536
Saze H, Tsugane K, Kanno T, Nishimura T (2012) DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation. Plant Cell Physiol 53:766–784
Schmitz RJ, He Y, Valdes-Lopez O, Khan SM, Joshi T, Urich MA, Nery JR et al (2013) Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Res 23:1663–1674
Schmitz RJ, Schultz MD, Lewsey MG, O’Malley RC, Urich MA, Libiger O, Schork NJ et al (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334:369–373
Schmitz RJ, Zhang X (2011) High-throughput approaches for plant epigenomic studies. Curr Opin Plant Biol 14:130–136
Sharma R, Vishal P, Kaul S, Dhar MK (2017) Epiallelic changes in known stress-responsive genes under extreme drought conditions in Brassica juncea (L.) Czern. Plant Cell Rep 36(1):203–217
Slaughter A, Daniel X, Flors V, Luna E, Hohn B, Mauch-Mani B (2012) Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol 158:835–843
Slotkin RK, Vaughn M, Borges F, Tanurdžić M, Becker JD, Feijó JA, Martienssen RA (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472
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 227:245–254
Springer NM (2013) Epigenetics and crop improvement. Trends Genet 29:241–247
Stelpflug SC, Eichten SR, Hermanson PJ, Springer NM, Kaeppler SM (2014) Consistent and heritable alterations of DNA methylation are induced by tissue culture in maize. Genetics 198:209–218
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
Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, Patel DJ et al (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 21:64–72
Suji KK, Joel AJ (2010) An epigenetic change in rice cultivars under water stress conditions. Elect J Plant Breed 1:1142–1143
Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9:465–476
Terooatea TW, Pozner A, Buck-Koehntop BA (2016) PAtCh-Cap:input strategy for improving analysis of ChIP-exo data sets and beyond. Nucleic Acids Res 44(21):e159
Tran RK, Zilberman D, de Bustos C, Ditt RF, Henikoff JG, Lindroth AM, Delrow J, Boyle T, Kwong S, Bryson TD, Jacobsen SE, Henikoff S (2005) Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. Genome Biol 6:R90
Tsaftaris AS, Dickinson AN (2000) DNA methylation and plant breeding. Plant Breed Rev 18:87–176
Varshney RK, Bansal KC, Aggarwal PK, Datta SK, Craufurd PQ (2011) Agricultural biotechnology for crop improvement in a variable climate: hope or hype? Trends Plant Sci 16:363–371
Volpe TA, Kidner C, Hall IM, Teng G, Grewal SIS, Martienssen A (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833–1837
Waddington CH (1953) Epigenetics and evolution. Symp Soc Exp Biol 7:186–199
Walley JW, Rowe HC, Xiao Y, Chehab EW, Kliebenstein DJ, Wagner D, Dehesh K (2008) The chromatin remodeler SPLAYED regulates specific stress signaling pathways. PLoS Pathog 4:e1000237–e1000237
Wang W, Zhao X, Pan Y, Zhu L, Fu B, Li Z (2011) DNA methylation changes detected by methylation sensitive amplified polymorphism in two contrasting rice genotypes under salt stress. J Genet Genomics 38:419–424
Wang X, Elling AA, Li X, Li N, Peng Z, He G, Sun H et al (2009) Genome-wide and organ-specific landscapes of epigenetic modifiations and their relationships to mRNA and small RNA transcriptomes in maize. Plant Cell 21:1053–1069
West PT, Li Q, Ji L, Eichten SR, Song J, Vaughn MW, Schmitz RJ et al (2014) Genomic distribution of H3K9me2 and DNA methylation in a maize genome. PLoS ONE 9:e105267
Wu K, Zhang L, Zhou C, Yu CW, Chaikam V (2008) HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J Exper Bot 59:225–234
Yang C, Zhang M, Niu W, Yang R, Zhang Y, Qiu Z, Sun B et al (2011) Analysis of DNA methylation in various swine tissues. PLoS ONE 6:e16229
Zentner GE, Henikoff S (2013) Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol 20:259–266
Zhang X, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, Goodrich J, Jacobsen SE (2007a) Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoSBiol 5:e129
Zhang X, Henderson IR, Lu C, Green PJ, Jacobsen SE (2007b) Role of RNA polymerase IV in plant small RNA metabolism. Proc Natl Acad Sci 104:4536–4541
Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SWL, Chen H, Henderson IR et al (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201
Zhao L, Wang P, Hou H, Zhang H, Wang Y, Yan S, Huang Y et al (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 et al (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 X, Pontes O, Zhu J, Miki D, Zhang F, Li WX, Lida K et al (2008) T ROS3 is an RNA-binding protein required for DNA demethylation in Arabidopsis. Nature 455:1259–1262
Zhu JK (2009) Active DNA demethylation mediated by DNA glycosylases. Ann Rev Genet 43:143
Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61–69
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Dhar, M.K., Sharma, R., Vishal, P., Kaul, S. (2019). Epigenetic Response of Plants to Abiotic Stress: Nature, Consequences and Applications in Breeding. In: Rajpal, V., Sehgal, D., Kumar, A., Raina, S. (eds) Genetic Enhancement of Crops for Tolerance to Abiotic Stress: Mechanisms and Approaches, Vol. I. Sustainable Development and Biodiversity, vol 20. Springer, Cham. https://doi.org/10.1007/978-3-319-91956-0_3
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