Abstract
Plant immunity relies on two cell autonomous immune pathways present in each cell and on systemic signals emanating from local challenged sites, which enhance immunity in distal unchallenged cells. Activation of these different immune branches entails extensive transcriptional reprogramming of a largely common set of defense-related genes, leading to the termination or restriction of pathogen propagation at the cost of plant growth. Emerging evidence points to a role of chromatin remodeling and dynamics as a key mechanistic basis for timely and appropriate activation of immune response in plants. One such phenomenon that appears to be under epigenetic control involves defense priming that is conditioned upon immune activation or interactions with beneficial microbes. In defense priming, target defense-related genes are not actively transcribed but poised for a greater and/or faster activation upon second stimulation. Moreover, a growing list of nuclear-localized pathogen effectors also implies their possible role in the alteration of host chromatin configuration for virulence promotion. Epigenetic control of defense-related genes seems to represent an as-yet-underexplored interface during plant–pathogen interactions.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Aichinger E, Villar CB, Di Mambro R, Sabatini S, Kohler C (2011) The CHD3 chromatin remodeler PICKLE and polycomb group proteins antagonistically regulate meristem activity in the Arabidopsis root. Plant Cell 23:1047–1060
Alvarez ME, Nota F, Cambiagno DA (2010) Epigenetic control of plant immunity. Mol Plant Pathol 11:563–576
Alvarez-Venegas R, Sadder M, Hlavacka A, Baluska F, Xia Y, Lu G, Firsov A, Sarath G, Moriyama H, Dubrovsky JG, Avramova Z (2006) The Arabidopsis homolog of trithorax, ATX1, binds phosphatidylinositol 5-phosphate, and the two regulate a common set of target genes. Proc Natl Acad Sci U S A 103:6049–6054
Alvarez-Venegas R, Abdallat AA, Guo M, Alfano JR, Avramova Z (2007) Epigenetic control of a transcription factor at the cross section of two antagonistic pathways. Epigenetics 2:106–113
Baumgarten A, Cannon S, Spangler R, May G (2003) Genome-level evolution of resistance genes in Arabidopsis thaliana. Genetics 165:309–319
Berr A, McCallum EJ, Alioua A, Heintz D, Heitz T, Shen WH (2010) Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi. Plant Physiol 154:1403–1414
Berr A, Shafiq S, Shen WH (2011) Histone modifications in transcriptional activation during plant development. Biochim Biophys Acta 1809:567–576
Berr A, Menard R, Heitz T, Shen WH (2012) Chromatin modification and remodelling: a regulatory landscape for the control of Arabidopsis defence responses upon pathogen attack. Cell Microbiol 14:829–839
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
Bhattacharjee S, Halane MK, Kim SH, Gassmann W (2011) Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science 334:1405–1408
Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48:419–436
Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406
Burch-Smith TM, Dinesh-Kumar SP (2007) The functions of plant TIR domains. Sci STKE 2007:pe46
Butenko Y, Ohad N (2011) Polycomb-group mediated epigenetic mechanisms through plant evolution. Biochim Biophys Acta 1809:395–406
Cai Y, Jin J, Florens L, Swanson SK, Kusch T, Li B, Workman JL, Washburn MP, Conaway RC, Conaway JW (2005) The mammalian YL1 protein is a shared subunit of the TRRAP/TIP60 histone acetyltransferase and SRCAP complexes. J Biol Chem 280:13665–13670
Caldo RA, Nettleton D, Wise RP (2004) Interaction-dependent gene expression in Mla-specified response to barley powdery mildew. Plant Cell 16:2514–2528
Cazzonelli CI, Cuttriss AJ, Cossetto SB, Pye W, Crisp P, Whelan J, Finnegan EJ, Turnbull C, Pogson BJ (2009) Regulation of carotenoid composition and shoot branching in Arabidopsis by a chromatin modifying histone methyltransferase, SDG8. Plant Cell 21:39–53
Cheng YT, Germain H, Wiermer M, Bi D, Xu F, Garcia AV, Wirthmueller L, Despres C, Parker JE, Zhang Y, Li X (2009) Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell 21:2503–2516
Chinnusamy V, Zhu JK (2009) RNA-directed DNA methylation and demethylation in plants. Sci China C Life Sci 52:331–343
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814
Clayton AL, Mahadevan LC (2003) MAP kinase-mediated phosphoacetylation of histone H3 and inducible gene regulation. FEBS Lett 546:51–58
Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531
De-La-Pena C, Rangel-Cano A, Alvarez-Venegas R (2012) Regulation of disease-responsive genes mediated by epigenetic factors: interaction of Arabidopsis-Pseudomonas. Mol Plant Pathol 13:388–398
Dempsey DA, Klessig DF (2012) SOS - too many signals for systemic acquired resistance? Trends Plant Sci 17:538–545
Ding Y, Avramova Z, Fromm M (2011) The Arabidopsis trithorax-like factor ATX1 functions in dehydration stress responses via ABA-dependent and ABA-independent pathways. Plant J 66:735–744
Dong X (2004) NPR1, all things considered. Curr Opin Plant Biol 7:547–552
Dong G, Ma DP, Li J (2008) The histone methyltransferase SDG8 regulates shoot branching in Arabidopsis. Biochem Biophys Res Commun 373:659–664
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 U S A 109:E2183–E2191
Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
Farrona S, Hurtado L, Reyes JC (2007) A nucleosome interaction module is required for normal function of Arabidopsis thaliana BRAHMA. J Mol Biol 373:240–250
Feilner T, Hultschig C, Lee J, Meyer S, Immink RG, Koenig A, Possling A, Seitz H, Beveridge A, Scheel D, Cahill DJ, Lehrach H, Kreutzberger J, Kersten B (2005) High throughput identification of potential Arabidopsis mitogen-activated protein kinases substrates. Mol Cell Proteomics 4:1558–1568
Fuchs J, Demidov D, Houben A, Schubert I (2006) Chromosomal histone modification patterns–from conservation to diversity. Trends Plant Sci 11:199–208
Garcia AV, Parker JE (2009) Heaven’s gate: nuclear accessibility and activities of plant immune regulators. Trends Plant Sci 14:479–487
Garcia AV, Blanvillain-Baufume S, Huibers RP, Wiermer M, Li G, Gobbato E, Rietz S, Parker JE (2010) Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLoS Pathog 6:e1000970
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227
Grini PE, Thorstensen T, Alm V, Vizcay-Barrena G, Windju SS, Jorstad TS, Wilson ZA, Aalen RB (2009) The ASH1 HOMOLOG 2 (ASHH2) histone H3 methyltransferase is required for ovule and anther development in Arabidopsis. PLoS One 4:e7817
Heidrich K, Wirthmueller L, Tasset C, Pouzet C, Deslandes L, Parker JE (2011) Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334:1401–1404
Hennig L, Derkacheva M (2009) Diversity of Polycomb group complexes in plants: same rules, different players? Trends Genet 25:414–423
Holec S, Berger F (2012) Polycomb group complexes mediate developmental transitions in plants. Plant Physiol 158:35–43
Jaskiewicz M, Conrath U, Peterhansel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12:50–55
Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22:94–97
Jeong CW, Roh H, Dang TV, Choi YD, Fischer RL, Lee JS, Choi Y (2011) An E3 ligase complex regulates SET-domain polycomb group protein activity in Arabidopsis thaliana. Proc Natl Acad Sci U S A 108:8036–8041
Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329
Kanno T, Habu Y (2011) siRNA-mediated chromatin maintenance and its function in Arabidopsis thaliana. Biochim Biophys Acta 1809:444–451
Kohler C, Aichinger E (2010) Antagonizing Polycomb group-mediated gene repression by chromatin remodelers. Epigenetics 5:20–23
Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705
Krogan NJ, Keogh MC, Datta N, Sawa C, Ryan OW, Ding H, Haw RA, Pootoolal J, Tong A, Canadien V, Richards DP, Wu X, Emili A, Hughes TR, Buratowski S, Greenblatt JF (2003) A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell 12:1565–1576
Li X, Zhang Y, Clarke JD, Li Y, Dong X (1999) Identification and cloning of a negative regulator of systemic acquired resistance, SNI1, through a screen for suppressors of npr1-1. Cell 98:329–339
Li G, Chandrasekharan MB, Wolffe AP, Hall TC (2001) Chromatin structure and phaseolin gene regulation. Plant Mol Biol 46:121–129
Li Y, Tessaro MJ, Li X, Zhang Y (2010) Regulation of the expression of plant resistance gene SNC1 by a protein with a conserved BAT2 domain. Plant Physiol 153:1425–1434
Liu C, Lu F, Cui X, Cao X (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61:395–420
Lu X, Tintor N, Mentzel T, Kombrink E, Boller T, Robatzek S, Schulze-Lefert P, Saijo Y (2009) Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc Natl Acad Sci U S A 106:22522–22527
Luna E, Bruce TJ, Roberts MR, Flors V, Ton J (2012) Next-generation systemic acquired resistance. Plant Physiol 158:844–853
Ma KW, Flores C, Ma W (2011) Chromatin configuration as a battlefield in plant-bacteria interactions. Plant Physiol 157:535–543
March-Diaz R, Garcia-Dominguez M, Lozano-Juste J, Leon J, Florencio FJ, Reyes JC (2008) Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J 53:475–487
Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469:343–349
Mas G, de Nadal E, Dechant R, Rodriguez de la Concepcion ML, Logie C, Jimeno-Gonzalez S, Chavez S, Ammerer G, Posas F (2009) Recruitment of a chromatin remodelling complex by the Hog1 MAP kinase to stress genes. EMBO J 28:326–336
Meier I, Somers DE (2011) Regulation of nucleocytoplasmic trafficking in plants. Curr Opin Plant Biol 14:538–546
Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834
Mizuguchi G, Shen X, Landry J, Wu WH, Sen S, Wu C (2004) ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303:343–348
Mosher RA, Durrant WE, Wang D, Song J, Dong X (2006) A comprehensive structure-function analysis of Arabidopsis SNI1 defines essential regions and transcriptional repressor activity. Plant Cell 18:1750–1765
Naqvi AR, Sarwat M, Hasan S, Roychodhury N (2012) Biogenesis, functions and fate of plant microRNAs. J Cell Physiol 227:3163–3168
Palma K, Thorgrimsen S, Malinovsky FG, Fiil BK, Nielsen HB, Brodersen P, Hofius D, Petersen M, Mundy J (2010) Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor. PLoS Pathog 6:e1001137
Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V (2012) Primed plants do not forget. Environ Exp Bot [Epub ahead of print]
Pecinka A, Mittelsten Scheid O (2012) Stress-induced chromatin changes: a critical view on their heritability. Plant Cell Physiol 53:801–808
Pfluger J, Wagner D (2007) Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol 10:645–652
Pieterse CM, van der Does D, Zamioudis C, Leon-Reyes A, van Wees SC (2012) Hormonal Modulation of Plant Immunity. Annu Rev Cell Dev Biol. [Epub ahead of print]
Pontvianne F, Blevins T, Pikaard CS (2010) Arabidopsis Histone Lysine Methyltransferases. Adv Bot Res 53:1–22
Rasmann S, De Vos M, Jander G (2012) Ecological role of transgenerational resistance against biotic threats. Plant Signal Behav 7:447–449
Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343
Roudier F, Teixeira FK, Colot V (2009) Chromatin indexing in Arabidopsis: an epigenomic tale of tails and more. Trends Genet 25:511–517
Roudier F, Ahmed I, Bérard C, Sarazin A, Mary-Huard T, Cortijo S, Bouyer D, Caillieux E, Duvernois-Berthet E, Al-Shikhley L, Giraut L, Després B, Drevensek S, Barneche F, Dèrozier S, Brunaud V, Aubourg S, Schnittger A, Bowler C, Martin-Magniette ML, Robin S, Caboche M, Colot V (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30:1928–1938
Saleh A, Alvarez-Venegas R, Yilmaz M, Le O, Hou G, Sadder M, Al-Abdallat A, Xia Y, Lu G, Ladunga I, Avramova Z (2008) The highly similar Arabidopsis homologs of trithorax ATX1 and ATX2 encode proteins with divergent biochemical functions. Plant Cell 20:568–579
Sang Y, Wu MF, Wagner D (2009) The stem cell–chromatin connection. Semin Cell Dev Biol 20:1143–1148
Segonzac C, Zipfel C (2011) Activation of plant pattern-recognition receptors by bacteria. Curr Opin Microbiol 14:54–61
Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, Seki H, Ulker B, Somssich IE, Schulze-Lefert P (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315:1098–1103
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
Spoel SH, Dong X (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3:348–351
Tamada Y, Yun JY, Woo SC, Amasino RM (2009) ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. Plant Cell 21:3257–3269
Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330
Tena G, Boudsocq M, Sheen J (2011) Protein kinase signaling networks in plant innate immunity. Curr Opin Plant Biol 14:519–529
van den Burg HA, Takken FL (2009) Does chromatin remodeling mark systemic acquired resistance? Trends Plant Sci 14:286–294
van Hulten M, Pelser M, van Loon LC, Pieterse CM, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci U S A 103:5602–5607
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
Wiermer M, Feys BJ, Parker JE (2005) Plant immunity: the EDS1 regulatory node. Curr Opin Plant Biol 8:383–389
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
Yi H, Richards EJ (2007) A cluster of disease resistance genes in Arabidopsis is coordinately regulated by transcriptional activation and RNA silencing. Plant Cell 19:2929–2939
Yi H, Richards EJ (2009) Gene duplication and hypermutation of the pathogen Resistance gene SNC1 in the Arabidopsis bal variant. Genetics 183:1227–1234
Zhang Y, Reinberg D (2001) Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 15:2343–2360
Zhang Y, Goritschnig S, Dong X, Li X (2003) A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15:2636–2646
Zhang K, Sridhar VV, Zhu J, Kapoor A, Zhu JK (2007) Distinctive core histone post-translational modification patterns in Arabidopsis thaliana. PLoS One 2:e1210
Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10:R62
Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S (2008) Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456:125–129
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Saijo, Y., Reimer-Michalski, EM. (2013). Epigenetic Control of Plant Immunity. In: Grafi, G., Ohad, N. (eds) Epigenetic Memory and Control in Plants. Signaling and Communication in Plants, vol 18. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-35227-0_4
Download citation
DOI: https://doi.org/10.1007/978-3-642-35227-0_4
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-35226-3
Online ISBN: 978-3-642-35227-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)