Abstract
In plants, active defense against pathogens and parasites relies substantially on the perception of danger. It has been well established that plants recognize invading microbes through the perception of microbe-associated molecular patterns(MAMPs), i.e., structures characteristic for whole classes of microbes. Among the MAMPs are highly conserved epitopes of important microbial proteins, such as bacterial flagellin or EF-Tu. These MAMPs are perceived by pattern recognition receptors (PRRs) on the plant cell surface. In Arabidopsis, the PRRs FLS2 and EFR, perceiving flagellin and EF-Tu, respectively, are leucine-rich repeat receptor-like kinases (LRR-RLKs). They bind their cognate ligands at the outside of the cell and relay the signal to the cytoplasm, inducing a potent defense response. In addition, alarm may also be caused by endogenous danger signals arising simply from cellular damage. In Arabidopsis thaliana, the small peptides AtPep1 to AtPep7 appear to act as such damage-associated molecular patterns (DAMPs), since they were found to induce various defense responses. AtPeps are perceived by two receptors, PEPR1 and PEPR2, which are surprisingly similar to FLS2 and EFR. The AtPep/PEPR system is suggested to act as an amplifier of resistance, possibly during infections by pathogens as well as during responses to herbivore attack and other wounding events.
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Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gómez-Gómez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983
Blein JP, Coutos-Thevenot P, Marion D, Ponchet M (2002) From elicitins to lipid-transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends Plant Sci 7:293–296
Boller T (1995) Chemoperception of microbial signals in plant cells. Annu Rev Plant Physiol Mol Biol 46:189–214
Boller T (2005) Peptide signalling in plant development and self/non-self perception. Curr Opin Cell Biol 17:116–122
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
Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744
Boudsocq M, Willmann MR, McCormack M, Lee H, Shan LB, He P, Bush J, Cheng SH, Sheen J (2010) Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464:418–422
Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, Zipfel C, Rathjen JP (2010) Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci USA 107:14502–14507
Brunner F, Rosahl S, Lee J, Rudd JJ, Geiler C, Kauppinen S, Rasmussen G, Scheel D, Nürnberger T (2002) Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO J 21:6681–6688
Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA 107:9452–9457
Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465–476
Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500
Chinchilla D, Shan L, He P, de Vries S, Kemmerling B (2009) One for all: the receptor-associated kinase BAK1. Trends Plant Sci 14:535–541
Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95–101
D’Ovidio R, Mattei B, Roberti S, Bellincampi D (2004) Polygalacturonases, polygalacturonase-inhibiting proteins and pectic oligomers in plant-pathogen interactions. Biochim Biophys Acta Protein Proteomics 1696:237–244
Dardick C, Ronald P (2006) Plant and animal pathogen recognition receptors signal through non-RD kinases. PLos Pathog 2:14–28
Felix G, Boller T (1995) Systemin induces rapid ion fluxes and ethylene biosynthesis in Lycopersicon peruvianum cells. Plant J 7:381–389
Felix G, Boller T (2003) Molecular sensing of bacteria in plants – the highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J Biol Chem 278:6201–6208
Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–276
Gaulin E, Dramé N, Lafitte C, Torto-Alalibo T, Martinez Y, Ameline-Torregrosa C, Khatib M, Mazarguil H, Villalba-Mateos F, Kamoun S, Mazars C, Dumas B, Bottin A, Esquerre-Tugaye MT, Rickauer M (2006) Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell 18:1766–1777
Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011
Greenberg JT, Yao N (2004) The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol 6:201–211
Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099–1103
He P, Shan L, Sheen J (2007) Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant-microbe interactions. Cell Microbiol 9:1385–1396
Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104:12217–12222
Holton N, Caño-Delgado A, Harrison K, Montoya T, Chory J, Bishop GJ (2007) Tomato BRASSINOSTEROID INSENSITIVE1 is required for systemin-induced root elongation in Solanum pimpinellifolium but is not essential for wound signaling. Plant Cell 19:1709–1717
Huffaker A, Ryan CA (2007) Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. Proc Natl Acad Sci USA 104:10732–10736
Huffaker A, Pearce G, Ryan CA (2006) An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci USA 103:10098–10103
Huffaker A, Dafoe NJ, Schmelz EA (2011) ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance. Plant Physiol 155:1325–1338
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329
Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080
Krol E, Mentzel T, Chinchilla D, Boller T, Felix G, Kemmerling B, Postel S, Arents M, Jeworutzki E, Al-Rasheid KAS, Becker D, Hedrich R (2010) Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J Biol Chem 285:13471–13479
Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–3507
Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, van Esse HP, Smoker M, Rallapalli G, Thomma B, Staskawicz B, Jones JDG, Zipfel C (2010) Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat Biotechnol 28:365–369
Lanfermeijer FC, Staal M, Malinowski R, Stratmann JW, Elzenga JTM (2008) Micro-electrode flux estimation confirms that the Solanum pimpinellifolium cu3 mutant still responds to systemin. Plant Physiol 146:129–139
Lecourieux D, Raneva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171:249–269
Lee H, Chah O-K, Sheen J (2011) Stem-cell-triggered immunity through CLV3p-FLS2 signalling. Nature 473:376–379
Li J, Wen JQ, Lease KA, Doke JT, Tax FE, Walker JC (2002a) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–222
Li L, Li CY, Lee GI, Howe GA (2002b) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci USA 99:6416–6421
Mackey D, McFall AJ (2006) MAMPs and MIMPs: proposed classifications for inducers of innate immunity. Mol Microbiol 61:1365–1371
Matzinger P (2002) The danger model: a renewed sense of self. Science 296:301–305
McGurl B, Ryan CA (1992) The organization of the prosystemin gene. Plant Mol Biol 20:405–409
Meindl T, Boller T, Felix G (1998) The plant wound hormone systemin binds with the N-terminal part to its receptor but needs the C-terminal part to activate it. Plant Cell 10:1561–1570
Mersmann S, Bourdais G, Rietz S, Robatzek S (2010) Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol 154:391–400
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309
Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104:19613–19618
Morillo SA, Tax FE (2006) Functional analysis of receptor-like kinases in monocots and dicots. Curr Opin Plant Biol 9:460–469
Nam KH, Li JM (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110:203–212
Nühse TS, Peck SC, Hirt H, Boller T (2000) Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK 6. J Biol Chem 275:7521–7526
Nürnberger T, Nennstiel D, Jabs T, Sacks WR, Hahlbrock K, Scheel D (1994) High affinity binding of a binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78:449–460
Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces woun-inducible proteinase-inhibitor proteins. Science 253:895–898
Pearce G, Moura DS, Stratmann J, Ryan CA (2001a) Production of multiple plant hormones from a single polyprotein precursor. Nature 411:817–820
Pearce G, Moura DS, Stratmann J, Ryan CA (2001b) RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc Natl Acad Sci USA 98:12843–12847
Pearce G, Yamaguchi Y, Munske G, Ryan CA (2008) Structure-activity studies of AtPep1, a plant peptide signal involved in the innate immune response. Peptides 29:2083–2089
Pearce G, Yamaguchi Y, Barona G, Ryan CA (2010) A subtilisin-like protein from soybean contains an embedded, cryptic signal that activates defense-related genes. Proc Natl Acad Sci USA 107:14921–14925
Qi Z, Verma R, Gehring C, Yamaguchi Y, Zhao YC, Ryan CA, Berkowitz GA (2010) Ca(2+) signaling by plant Arabidopsis thaliana Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca(2+) channels. Proc Natl Acad Sci USA 107:21193–21198
Rodriguez MCS, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649
Ronald PC, Beutler B (2010) Plant and animal sensors of conserved microbial signatures. Science 330:1061–1064
Ryan CA, Pearce G (2003) Systemins: a functionally defined family of peptide signal that regulate defensive genes in Solanaceae species. Proc Natl Acad Sci USA 100:14577–14580
Ryan CA, Huffaker A, Yamaguchi Y (2007) New insights into innate immunity in Arabidopsis. Cell Microbiol 9:1902–1908
Schulze B, Mentzel T, Jehle AK, Mueller K, Beeler S, Boller T, Felix G, Chinchilla D (2010) Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem 285:9444–9451
Segonzac C, Zipfel C (2011) Activation of plant pattern-recognition receptors by bacteria. Curr Opin Microbiol 14:54–61
Shah J (2009) Plants under attack: systemic signals in defence. Curr Opin Plant Biol 12:459–464
Shiu SH, Karlowski WM, Pan RS, Tzeng YH, Mayer KFX, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234
Spanu P, Grosskopf DG, Felix G, Boller T (1994) The apparent turnover of 1-aminocyclopropane-1-carboxylate synthase in tomato cells is regulated by protein phosphorylation and dephosphorylation. Plant Physiol 106:529–535
Stepanova AN, Alonso JM (2009) Ethylene signaling and response: where different regulatory modules meet. Curr Opin Plant Biol 12:548–555
Tör M, Lotze MT, Holton N (2009) Receptor-mediated signalling in plants: molecular patterns and programmes. J Exp Bot 60:3645–3654
Torres MA (2010) ROS in biotic interactions. Physiol Plant 138:414–429
Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The botany array resource: e-Northerns, expression angling, and promoter analyses. Plant J 43:153–163
Wang ZY, He JX (2004) Brassinosteroid signal transduction – choices of signals and receptors. Trends Plant Sci 9:91–96
Xia YJ, Suzuki H, Borevitz J, Blount J, Guo ZJ, Patel K, Dixon RA, Lamb C (2004) An extracellular aspartic protease functions in Arabidopsis disease resistance signaling. EMBO J 23:980–988
Yamaguchi Y, Huffaker A (2011) Endogenous peptide elicitors in higher plants. Curr Opin Plant Biol 14:351–357
Yamaguchi Y, Pearce G, Ryan CA (2006) The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc Natl Acad Sci USA 103:10104–10109
Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA (2010) PEPR2 Is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22:508–522
Yamaguchi Y, Barona G, Ryan CA, Pearce G (2011) GmPep914, an eight-amino acid peptide isolated from soybean leaves, activates defense-related genes. Plant Physiol 156:932–942
Zhang SQ, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6:520–527
Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767
Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760
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Boller, T., Flury, P. (2012). Peptides as Danger Signals: MAMPs and DAMPs. In: Irving, H., Gehring, C. (eds) Plant Signaling Peptides. Signaling and Communication in Plants, vol 16. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-27603-3_9
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DOI: https://doi.org/10.1007/978-3-642-27603-3_9
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