[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content

Advertisement

Log in

Epigenetic mechanisms of plant stress responses and adaptation

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Epigenetics has become one of the hottest topics of research in plant functional genomics since it appears promising in deciphering and imparting stress-adaptive potential in crops and other plant species. Recently, numerous studies have provided new insights into the epigenetic control of stress adaptation. Epigenetic control of stress-induced phenotypic response of plants involves gene regulation. Growing evidence suggest that methylation of DNA in response to stress leads to the variation in phenotype. Transposon mobility, siRNA-mediated methylation and host methyltransferase activation have been implicated in this process. This review presents the current status of epigenetics of plant stress responses with a view to use this knowledge towards engineering plants for stress tolerance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Agius F, Kapoor A, Zhu JK (2006) Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation. Proc Natl Acad Sci USA 103:11796–11801

    Article  PubMed  CAS  Google Scholar 

  • Akimoto K, Katakami H, Kim HJ, Ogawa E, Sano CM, Wada Y, Sano H (2007) Epigenetic inheritance in rice plants. Ann Bot 100:205–217

    Article  PubMed  CAS  Google Scholar 

  • Angaji SA, Hedayati SS, Hoseinpoor R, Poor SS, Shiravi S, Madani SD (2010) Application of RNA interference in plants. Plant Omics J 3:77–84

    CAS  Google Scholar 

  • Angers B, Castonguay E, Massicotte R (2010) Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Mol Ecol 19:1283–1295

    Article  PubMed  CAS  Google Scholar 

  • Baek D, Jiang J, Chung JS, Wang B, Chen J, Xin Z, Shi H (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

    Article  PubMed  CAS  Google Scholar 

  • Bian XY, Rasheed MS, Seemanpillai MJ, Ali Rezaian M (2006) Analysis of silencing escape of tomato leaf curl virus: an evaluation of the role of DNA methylation. Mol Plant Microbe Interact 19:614–624

    Article  PubMed  CAS  Google Scholar 

  • Boyko A, Blevins T, Yao Y, Golubov A, Bilichak A, Ilnytskyy Y, Hollunder J, Meins F Jr, Kovalchuk I (2010) Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins. PLoS ONE 5(3):e9514

    Article  PubMed  Google Scholar 

  • Cao X, Jacobsen SE (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12:1138–1144

    Article  PubMed  CAS  Google Scholar 

  • Cao X, Aufsatz W, Zilberman D, Mette MF, Huang MS, Matzke M, Jacobsen SE (2003) Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr Biol 13:2212–2217

    Google Scholar 

  • Chan SWL, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Genetics 6:351–360

    PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Gong Z, Zhu JK (2008) Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol 50:1187–1195

    Article  PubMed  CAS  Google Scholar 

  • Choi CS, 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

    Article  PubMed  CAS  Google Scholar 

  • Correia B, Valledor L, Meijon M, Rodriguez JL, Dias MC, Santos C, Canal MJ, Rodriguez R, Pinto G (2013) Is the interplay between epigenetic markers related to the acclimation of cork oak plants to high temperatures? PLoS ONE 8(1):e53543

    Article  PubMed  CAS  Google Scholar 

  • 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(32):E2183–E2191

    Article  PubMed  CAS  Google Scholar 

  • 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 71:461–465

    CAS  Google Scholar 

  • El-Shami M, Pontier D, Lahmy S, Braun L, Picart C, Vega D, Hakimi MA, Jacobsen SE, Cooke R, Lagrange T (2007) Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE binding platforms in RNAi-related components. Genes Dev 21:2539–2544

    Article  PubMed  CAS  Google Scholar 

  • Emran AM, Tabei Y, Kobayashi K, Yamaoka N, Nishiguchi M (2012) Molecular analysis of transgenic melon plants showing virus resistance conferred by direct repeat of movement gene of Cucumber green mottle mosaic virus. Plant Cell Rep 31:1371–1377

    Article  PubMed  Google Scholar 

  • Feng Q, Yang C, Lin X, Wang J, Ou X, Zhang C, Chenand Y, Liu B (2012) Salt and alkaline stress induced transgenerational alteration in DNA methylation of rice (Oryza sativa). Aus J Crop Sci 6:877–883

    CAS  Google Scholar 

  • Finnegan EJ, Genger RK, Kovac K, Peacock WJ, Dennis ES (1998) DNA methylation and the promotion of flowering by vernalization. Proc Natl Acad Sci USA 95:5824–5829

    Article  PubMed  CAS  Google Scholar 

  • Gohlke J, Scholz CJ, Kneitz S, Weber D, Fuchs J, Hedrich R, Deeken R (2013) DNA methylation mediated control of gene expression is critical for development of crown gall tumors. PLoS Genet 9(2):e1003267

    Article  PubMed  CAS  Google Scholar 

  • Golldack D, Lüking I, Yang O (2011) Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep 30:1383–1391

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Gowher H, Jeltsch A (2002) Molecular enzymology of the catalytic domains of the Dnmt3a and Dnmt3b DNA methyltransferases. J Biol Chem 277:20409–20414

    Article  PubMed  CAS  Google Scholar 

  • Grativol C, Hemerly AS, Ferreira PC (2012) Genetic and epigenetic regulation of stress responses in natural plant populations. Biochim Biophys Acta 1819:176–185

    Article  PubMed  CAS  Google Scholar 

  • Hashida SN, 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 18:104–118

    Article  PubMed  CAS  Google Scholar 

  • Hauser MT, Aufsatz W, Jonak C, Luschnig C (2011) Transgenerational epigenetic inheritance in plants. Biochim Biophys Acta 1809:459–468

    Article  PubMed  CAS  Google Scholar 

  • Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556–560

    Article  PubMed  CAS  Google Scholar 

  • Jasencakova Z, Soppe WJ, Meister A, Gernand D, Turner BM, Schubert I (2003) Histone modifications in Arabidopsis-high methylation of H3 lysine 9 are dispensable for constitutive heterochromatin. Plant J 33:471–480

    Article  PubMed  CAS  Google Scholar 

  • Kanazawa A, Inaba J, Shimura H, Otagaki S, Tsukahara S, Matsuzawa A, Kim BM, Goto K, Masuta C (2011) Virus-mediated efficient induction of epigenetic modifications of 5 endogenous genes with phenotypic changes in plants. Plant J 65:156–168

    Article  PubMed  CAS  Google Scholar 

  • Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, Riddle NC, Verbsky ML, Richards EJ (2003) Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163:1109–1122

    PubMed  CAS  Google Scholar 

  • Karan R, DeLeon T, Biradar H, Subudhi PK (2012) Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. PLoS ONE 7(6):e40203

    Article  PubMed  CAS  Google Scholar 

  • Karlsson M, Weber W, Fussenegger M (2011) De novo design and construction of an inducible gene expression system in mammalian cells. Methods Enzymol 497:239–253

    Article  PubMed  CAS  Google Scholar 

  • Kato M, Miura A, Bender J, Jacobsen SE, Kakutani T (2003) Role of CG, non-CG methylation in immobilization of transposons in Arabidopsis. Curr Biol 13:421–426

    Article  PubMed  CAS  Google Scholar 

  • Khraiwesh B, Arif MA, Seumel GI, Ossowski S, Weigel D, Reski R, Frank W (2010) Transcriptional control of gene expression by MicroRNAs. Cell 140:111–122

    Article  PubMed  CAS  Google Scholar 

  • Kou HP, Li Y, Song XX, Ou XF, Xing SC, Ma J, Von Wettstein D, Liu B (2011) Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. J Plant Physiol 168:1685–1693

    Article  PubMed  CAS  Google Scholar 

  • Kovarik A, Koukalova B, Bezdek M, Opatrny Z (1997) Hypermethylation of tobacco heterochromatic loci in response to osmotic stress. Theor Appl Genet 95:301–306

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, Jacobsen SE (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292:2077–2080

    Article  PubMed  CAS  Google Scholar 

  • Lira-Medeiros CF, Parisod C, Fernandes RA, Mata CS, Cardoso MA, Ferreira PCG (2010) Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS ONE 5(4):e10326

    Google Scholar 

  • Luna E, Ton J (2012) The epigenetic machinery controlling transgenerational systemic acquired resistance. Plant Signal Behav 7:615–618

    Article  PubMed  CAS  Google Scholar 

  • Madlung A, Comai L (2004) The effect of stress on genome regulation and structure. Ann Bot 94:481–495

    Article  PubMed  CAS  Google Scholar 

  • Mirouze M, Paszkowski J (2011) Epigenetic contribution to stress adaptation in plants. Curr Opin Plant Biol 14:267–274

    Article  PubMed  CAS  Google Scholar 

  • Morales-Ruiz T, Ortega-Galisteo AP, Ponferrada-Marin MI, Martinez-Macias MI, Ariza RR, Roldan-Arjona T (2006) DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases. Proc Natl Acad Sci USA 103:6853–6858

    Article  PubMed  CAS  Google Scholar 

  • Muthamilarasan M, Prasad M (2013) Plant innate immunity: an updated insight in defense mechanism. J Biosci. doi:10.1007/s12038-013-9302-2

    PubMed  Google Scholar 

  • Penterman J, Zilberman D, Huh JH, Ballinger T, Henikoff S, Fischer RL (2007) DNA demethylation in the Arabidopsis genome. Proc Natl Acad Sci USA 104:6752–6757

    Article  PubMed  CAS  Google Scholar 

  • Qian Y, Cheng X, Liu Y, Jiang H, Zhu S, Cheng B (2010) An epigenetic change in rice cultivars under water stress conditions. Plant Cell Rep 29:1365–1376

    Article  PubMed  CAS  Google Scholar 

  • Ramsahoye BH, Biniszkiewicz D, Lyko F, Clrk V, Bird AP, Jaenisch R (2000) Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc Natl Acad Sci USA 97:5237–5242

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Negrete EA, Carrillo-Tripp J, Rivera-Bustamante RF (2009) RNA silencing against geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. J Virol 83:1332–1340

    Article  PubMed  Google Scholar 

  • Sabbah M, Raise M, Tal M (1995) Methylation of DNA in NaCl-adapted cells of potato. Plant Cell Rep 14:467–470

    Article  CAS  Google Scholar 

  • Sahu PP, Rai NK, Chakraborty S, Singh M, Chandrappa PH, Ramesh B, Chattopadhyay D, Prasad M (2010) Tomato cultivar tolerant to Tomato leaf curl New Delhi virus infection induces virus-specific short interfering RNA accumulation and defence-associated host gene expression. Mol Plant Pathol 11:531–544

    Article  PubMed  CAS  Google Scholar 

  • Sahu PP, Rai NK, Puranik S, Roy A, Khan M, Prasad M (2012) Dynamics of defense-related components in two contrasting genotypes of tomato upon infection with Tomato Leaf Curl New Delhi Virus. Mol Biotechnol 52:140–150

    Article  PubMed  CAS  Google Scholar 

  • Santos AP, Serra T, Figueiredo DD, Barros P, Lourenço T, Chander S, Oliveira MM, Saibo NJ (2011) Transcription regulation of abiotic stress responses in rice: a combined action of transcription factors and epigenetic mechanisms. OMICS 15:839–857

    Article  PubMed  CAS  Google Scholar 

  • Shaik R, Ramakrishna W (2012) Bioinformatic analysis of epigenetic and micro-RNA mediated regulation of drought responsive genes in rice. PLoS ONE 7(11):e49331

    Article  PubMed  CAS  Google Scholar 

  • Sharma N, Sahu PP, Puranik S, Prasad M (2012) Recent advances in plant-virus interaction with emphasis on small interfering RNAs (siRNAs). Mol Biotechnol. doi: 10.1007/s12033-012-9615-7

  • 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 ONE 7(7):e41274

    Article  PubMed  CAS  Google Scholar 

  • Soppe WJ, Jasencakova Z, Houben A, Kakutani T, Meister A, Huang MS, Jacobsen SE, Schubert I, Fransz PF (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21:6549–6559

    Article  PubMed  CAS  Google Scholar 

  • Steward N, Kusano T, Sano H (2000) Expression of ZmMET1, a gene encoding a DNA methyltransferase from maize, is associated not only with DNA replication in actively proliferating cells, but also with altered DNA methylation status in cold-stressed quiescent cells. Nuc Acids Res 28:3250–3259

    Article  CAS  Google Scholar 

  • Suji KK, John A (2010) An epigenetic change in rice cultivars under water stress conditions. Elect J Plant Breed 1:1142–1143

    Google Scholar 

  • Tariq M, Saze H, Probst AV, Lichota J, Habu Y, Paszkowski J (2003) Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci USA 100:8823–8827

    Article  PubMed  CAS  Google Scholar 

  • Tompa R, McCallum CM, Delrow J, Henikoff JG, van Steensel B, Henikoff S (2002) Genome-wide profiling of DNA methylation reveals transposon targets of CHROMOMETHYLASE3. Curr Biol 12:65–68

    Article  PubMed  CAS  Google Scholar 

  • Tougou M, Yamagishi N, Furutani N, Shizukawa Y, Takahata Y, Hidaka S (2007) Soybean dwarf virus-resistant transgenic soybeans with the sense coat protein gene. Plant Cell Rep 26:1967–1975

    Article  PubMed  CAS  Google Scholar 

  • Uthup TK, Ravindran M, Bini K, Thakurdas S (2011) Divergent DNA methylation patterns associated with abiotic stress in Hevea brasiliensis. Mol Plant 4:996–1013

    Google Scholar 

  • Vanyushin BF, Ashapkin VV (2011) DNA methylation in higher plants: past, present and future. Biochim Biophys Acta 1809:360–368

    Article  PubMed  CAS  Google Scholar 

  • Verhoeven KJF, Jansen JJ, Dijk PJV, Biere A (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol 185:1108–1118

    Article  PubMed  CAS  Google Scholar 

  • Wada Y, Miyamoto K, Kusano T, Sano H (2004) Association between up-regulation of stress-responsive genes and hypomethylation of genomic DNA in tobacco plants. Mol Genet Genomics 271:658–666

    Article  PubMed  CAS  Google Scholar 

  • Wang WS, Pan YJ, Zhao XQ, Dwivedi D, Zhu LH, Ali J, Fu BY, Li ZK (2011) Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). J Exp Bot 62:1951–1960

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, An C, Zhang X, Yao J, Zhang Y, Sun Y, Yu F, Amador DM, Mou Z (2013) The Arabidopsis elongator complex subunit2 epigenetically regulates plant immune responses. Plant Cell 25:762–776

    Article  PubMed  CAS  Google Scholar 

  • Yadav RK, Chattopadhyay D (2011) Enhanced viral intergenic region-specific short interfering RNA accumulation and DNA methylation correlates with resistance against a geminivirus. Mol Plant Microbe Interact 24:1189–1197

    Article  PubMed  CAS  Google Scholar 

  • Yaish MW, Colasanti J, Rothstein SJ (2011) The role of epigenetic processes in controlling flowering time in plants exposed to stress. J Exp Bot 62:3727–3735

    Article  PubMed  CAS  Google Scholar 

  • Yao Y, Bilichak A, Golubov A, Kovalchuk I (2012) ddm1 plants are sensitive to methyl methane sulfonate and NaCl stresses and are deficient in DNA repair. Plant Cell Rep 31:1549–1561

    Article  PubMed  Google Scholar 

  • Yu Y, Yang X, Wang H, Shi F, Liu Y, Liu J, Li L, Wang D, Liu B (2013a) Cytosine methylation alteration in natural populations of Leymus chinensis induced by multiple abiotic stresses. PLoS ONE 8(2):e55772

    Article  PubMed  CAS  Google Scholar 

  • Yu A, Lepère G, Jay F, Wang J, Bapaume L, Wang Y, Abraham AL, Penterman J, Fischer RL, Voinnet O, Navarro L (2013b) Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1211757110

  • Zhang L, Wang Y, Zhang X, Zhang M, Han D, Qiu C, Han Z (2012) Dynamics of phytohormone and DNA methylation patterns changes during dormancy induction in strawberry (Fragaria × ananassa Duch.). Plant Cell Rep 31:155–165

    Article  PubMed  Google Scholar 

  • Zheng Q, Rowley MJ, Böhmdorfer G, Sandhu D, Gregory BD, Wierzbicki AT (2013) RNA polymerase V targets transcriptional silencing components to promoters of protein-coding genes. Plant J 73:179–189

    CAS  Google Scholar 

  • Zhu B, Zheng Y, Angliker H, Schwarz S, Thiry S, Siegmann M, Jost JP (2000) 5-Methylcytosine DNA glycosylase activity is also present in the human MBD4 (G/T mismatch glycosylase) and in a related avian sequence. Proc Natl Acad Sci USA 28:4157–4165

    CAS  Google Scholar 

  • Zhu J, Kapoor A, Sridhar VV, Agius F, Zhu JK (2007) The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patterns in Arabidopsis. Curr Biol 17:54–59

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Authors are grateful to the Director, National Institute of Plant Genome Research (NIPGR), New Delhi, India for providing facilities. The authors’ work in this area was supported by the core grant of NIPGR. Ms Garima Pandey and Mr Mehanathan Muthamilarasan acknowledge the award of Junior Research Fellowship by University Grants Commission. Ms. Namisha Sharma acknowledges the award of Junior Research Fellowship by Department of Biotechnology, New Delhi. They are also thankful to the reviewers for their informative and constructive comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Manoj Prasad.

Additional information

Communicated by P. Lakshmanan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sahu, P.P., Pandey, G., Sharma, N. et al. Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep 32, 1151–1159 (2013). https://doi.org/10.1007/s00299-013-1462-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-013-1462-x

Keywords

Navigation