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Systemic Resistance Induction by Vascular and Airborne Signaling

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Progress in Botany 71

Part of the book series: Progress in Botany ((BOTANY,volume 71))

Abstract

Plants cannot escape spatially from harmful abiotic conditions or enemy attack. Therefore, they use both constitutive and inducible defense mechanisms to fend off pathogens and herbivores. Resistance induced in response to local attack is often expressed systemically, i.e., in yet undamaged organs. The search for the long-distance signals mediating systemic resistance led to the identification of hormones, such as jasmonic acid (JA), salicylic acid (SA), and ethylene, as well as volatiles and small RNA molecules. This research also revealed that different plant species may use different hormones to mount phenotypically similar resistance responses. Long-distance signals can directly activate defense, or prime for stronger and faster defense induction. Earlier research has focused on vascular transport of signaling metabolites, but volatiles can play a critical role as well. As volatiles move freely through air, they can prime and induce resistance in remote organs of the same individual and in neighboring plants. We compare the advantages and restraints of vascular and airborne signals for the plant and discuss how they can act in synergy to achieve an optimized resistance in distal plant parts.

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References

  • Alborn T, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949

    CAS  Google Scholar 

  • Almeras E, Stolz S, Vollenweider S, Reymond P, Mene-Saffrane L, Farmer EE (2003) Reactive electrophile species activate defense gene expression in Arabidopsis. Plant J 34:202–216

    Google Scholar 

  • Arimura G-I, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defense genes in lima bean leaves. Nature 406:512–515

    PubMed  CAS  Google Scholar 

  • Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 415:977–983

    PubMed  CAS  Google Scholar 

  • Baldwin IT, Schultz JC (1983) Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science 221:277–279

    PubMed  CAS  Google Scholar 

  • Baldwin IT, Zhang Z-P, Diab N, Ohnmeiss TE, McCloud ES, Lynds GY, Schmelz EA (1997) Quantification, correlations and manipulation of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 201:397–404

    CAS  Google Scholar 

  • Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA (2006) Volatile signaling in plant-plant interactions: "Talking trees" in the genomics era. Science 311:812–815

    PubMed  CAS  Google Scholar 

  • BallarĂ© CL (1999) Keeping up with the neighbors: phytochrome sensing and other signaling mechanisms. Trends Plant Sci 4:97–102

    PubMed  Google Scholar 

  • BallarĂ© CL, Scopel AL (1997) Phytochrome signaling in plant canopies: Testing its population-level implications with photoreceptor mutants of Arabidopsis. Funct Ecol 11:441–450

    Google Scholar 

  • Beckers GJ, Conrath U (2007) Priming for stress resistance: from the lab to the field. Curr Opin Plant Biol 10:425–431

    PubMed  Google Scholar 

  • Behnke K, Ehlting B, Teuber M, Bauerfeind M, Louis S, Hasch R, Polle A, Bohlmann J, Schnitzler JP (2007) Transgenic, non-isoprene emitting poplars don't like it hot. Plant J 51:485–499

    PubMed  CAS  Google Scholar 

  • Berenbaum MR, Zangerl AR (1999) Coping with life as a menu option: inducible defenses of the wild parsnip. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 10–32

    Google Scholar 

  • Bezemer TM, van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20:617–624

    PubMed  Google Scholar 

  • Blossey B, Hunt-Joshi TR (2003) Belowground herbivory by insects: influence on plants and aboveground herbivores. Annu Rev Entomol 48:521–547

    PubMed  CAS  Google Scholar 

  • Bose JC (1902) Electric response in ordinary plants under mechanical stimulus. Bot J Linn Soc 35:275–304

    Google Scholar 

  • Bose JC (1913) Researches on irritability of plants. Longmans & Green, London

    Google Scholar 

  • Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43:545–580

    PubMed  CAS  Google Scholar 

  • Brenner ED, Stahlberg R, Mancuso S, Vivanco J, Baluska F, Van Volkenburgh E (2006) Plant neurobiology: an integrated view of plant signaling. Trends Plant Sci 11:413–419

    PubMed  CAS  Google Scholar 

  • Bruce TJA, Matthes MC, Napier JA, Pickett JA (2007) Stressful ‘‘memories’’ of plants: Evidence and possible mechanisms. Plant Sci 173:603–608

    CAS  Google Scholar 

  • Cao H, Bowling SA, Gordon AS, Dong XN (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592

    PubMed  CAS  Google Scholar 

  • Cao H, Glazebrook J, Clarke JD, Volko S, Dong XN (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63

    PubMed  CAS  Google Scholar 

  • Cao H, Li X, Dong X (1998) Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc Natl Acad Sci USA 95:6531–6536

    PubMed  CAS  Google Scholar 

  • Chaturvedi R, Krothapalli K, Makandar R, Nandi A, Sparks AA, Roth MR, Welti R, Shah J (2008) Plastid omega 3-fatty acid desaturase-dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant J 54:106–117

    PubMed  CAS  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signaling. Nature 448:666–672

    PubMed  CAS  Google Scholar 

  • Cipollini DF (2004) Stretching the limits of plasticity: Can a plant defend against both competitors and herbivores? Ecology 85:28–37

    Google Scholar 

  • Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071

    PubMed  CAS  Google Scholar 

  • Creelman RA, Mullet JE (1997) Oligosaccharins, brassinolides, and jasmonates: Nontraditional regulators of plant growth, development, and gene expression. Plant Cell 9:1211–1223

    PubMed  CAS  Google Scholar 

  • Cui J, Bahrami AK, Pringle EG, Hernandez-Guzman G, Bender CL, Pierce NE, Ausubel FM (2005) Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc Natl Acad Sci USA 102:1791–1796

    PubMed  CAS  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defense responses to infection. Nature 411:826–833

    PubMed  CAS  Google Scholar 

  • Davis MA, Gordon MP, Smit BA (1991) Assimilate movement dictates remote sites of wound-induced gene expression in poplar leaves. Proc Natl Acad Sci USA 88:2393–2396

    PubMed  CAS  Google Scholar 

  • De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580

    PubMed  Google Scholar 

  • De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Metraux JP, Van Loon LC, Dicke M, Pieterse CMJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18:923–937

    PubMed  Google Scholar 

  • Delaney TP, Friedrich L, Ryals JA (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci USA 92:6602–6606

    PubMed  CAS  Google Scholar 

  • Dicke M, Van Poecke RMP, De Boer JG (2003) Inducible indirect defense of plants: from mechanisms to ecological functions. Basic Appl Ecol 4:27–42

    CAS  Google Scholar 

  • Doares SH, Syrovets T, Weiler EW, Ryan CA (1995) Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proc Natl Acad Sci USA 92:4095–4098

    PubMed  CAS  Google Scholar 

  • Dong WX (2004) NPR1, all things considered. Curr Opin Plant Biol 7:547–552

    PubMed  CAS  Google Scholar 

  • Doss RP (2005) Treatment of pea pods with bruchin B results in up-regulation of a gene similar to MtN19. Plant Physiol Biochem 43:225–231

    PubMed  CAS  Google Scholar 

  • Doss RP, Oliver JE, Proebsting WM, Potter SW, Kuy SR, Clement SL, Williamson RT, Carney JR, DeVilbiss ED (2000) Bruchins: Insect-derived plant regulators that stimulate neoplasm formation. Proc Natl Acad Sci USA 97:6218–6223

    PubMed  CAS  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    PubMed  CAS  Google Scholar 

  • Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785

    PubMed  CAS  Google Scholar 

  • Erb M, Ton J, Degenhardt J, Turlings TCJ (2008) Interactions between arthropod-induced aboveground and belowground defenses in plants. Plant Physiol 146:867–874

    PubMed  CAS  Google Scholar 

  • Erb M, Flors V, Karlen D, De Lange E, Planchamp C, D'Alessandro M, Turlings T, Ton J (2009) Signal signature of aboveground induced resistance upon belowground herbivory in maize. Plant J 59:292–302

    Google Scholar 

  • Farmer EE (2001) Surface-to-air signals. Nature 411:854–856

    PubMed  CAS  Google Scholar 

  • Farmer EE, AlmĂ©ras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6:372–378

    PubMed  CAS  Google Scholar 

  • Felton GW, Tumlinson JH (2008) Plant–insect dialogs: complex interactions at the plant–insect interface. Curr Opin Plant Biol 11:457–462

    PubMed  CAS  Google Scholar 

  • Frost C, Appel H, Carlson J, De Moraes C, Mescher M, Schultz J (2007) Within-plant signaling by volatiles overcomes vascular constraints on systemic signaling and primes responses against herbivores. Ecol Lett 10:490–498

    PubMed  Google Scholar 

  • Geigenberger P (2003) Response of plant metabolism to too little oxygen. Curr Opin Plant Biol 6:247–256

    PubMed  CAS  Google Scholar 

  • Glazebrook J, Chen WJ, Estes B, Chang HS, Nawrath C, Metraux JP, Zhu T, Katagiri F (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 34:217–228

    PubMed  CAS  Google Scholar 

  • Godard KA, White R, Bohlmann J (2008) Monoterpene-induced molecular responses in Arabidopsis thaliana. Phytochemistry 69:1838–1849

    PubMed  CAS  Google Scholar 

  • GĂ³mez S, Stuefer JF (2006) Members only: induced systemic resistance to herbivory in a clonal plant network. Oecologia 147:461–468

    PubMed  Google Scholar 

  • Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–777

    PubMed  CAS  Google Scholar 

  • Guedes MEM, Richmond S, Kuc J (1980) Induced systemic resistance to anthracnose in cucumber as influenced by the location of the inducer inoculation with Colletotrichum lagenarium and the onset of flowering and fruiting. Physiol Plant Pathol 17:229–233

    Google Scholar 

  • Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125:711–717

    PubMed  CAS  Google Scholar 

  • Heil M (2008) Indirect defense via tritrophic interactions. New Phytol 178:41–61

    PubMed  CAS  Google Scholar 

  • Heil M, Baldwin IT (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci 7:61–67

    PubMed  CAS  Google Scholar 

  • Heil M, Bostock RM (2002) Induced systemic resistance (ISR) in the context of induced plant defenses. Ann Bot 89:503–512

    PubMed  CAS  Google Scholar 

  • Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472

    PubMed  CAS  Google Scholar 

  • Heil M, Ton J (2008) Long-distance signaling in plant defense. Trends Plant Sci 13:264–272

    PubMed  CAS  Google Scholar 

  • Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE (2001) Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proc Natl Acad Sci USA 98:1083–1088

    PubMed  CAS  Google Scholar 

  • Heil M, Greiner S, Meimberg H, KrĂ¼ger R, Noyer J-L, Heubl G, Linsenmair KE, Boland W (2004) Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430:205–208

    PubMed  CAS  Google Scholar 

  • Heil M, Lion U, Boland W (2008) Defense-inducing volatiles: in search for the active motif. J Chem Ecol 34:601–604

    PubMed  CAS  Google Scholar 

  • Iniguez AL, Dong Y, Carter HD, Ahmer BM, Stone JM, Triplett EW (2005) Regulation of enteric endophytic bacterial colonization by plant defenses. Mol Plant Microbe Interact 18:169–178

    PubMed  CAS  Google Scholar 

  • Izaguirre MM, Mazza CA, Biondini M, Baldwin IT, BallarĂ© CL (2006) Remote sensing of future competitors: Impacts on plant defenses. Proc Natl Acad Sci USA 103:7170–7174

    PubMed  CAS  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    PubMed  CAS  Google Scholar 

  • Kahl J, Siemens DH, Aerts RJ, Gäbler R, KĂ¼hnemann F, Preston CA, Baldwin IT (2000) Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210:336–342

    PubMed  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Google Scholar 

  • Karban R, Baldwin I, Baxter K, Laue G, Felton G (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125:66–71

    Google Scholar 

  • Karban R, Shiojiri K, Huntzinger M, McCall AC (2006) Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87:922–930

    PubMed  Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144

    PubMed  CAS  Google Scholar 

  • Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: The emerging molecular analysis. Annu Rev Plant Biol 53:299–328

    PubMed  CAS  Google Scholar 

  • Kessler A, Halitschke R, Diezel C, Baldwin IT (2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148:280–292

    PubMed  Google Scholar 

  • Kiefer IW, Slusarenko AJ (2003) The pattern of systemic acquired resistance induction within the Arabidopsis rosette in relation to the pattern of translocation. Plant Physiol 132:840–847

    PubMed  CAS  Google Scholar 

  • Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2005) Volatile C6-aldehydes and allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46:1093–1102

    PubMed  CAS  Google Scholar 

  • Koch T, Krumm T, Jung V, Engelberth J, Boland W (1999) Differential induction of plant volatile biosynthesis in the lima bean by early and late intermediates of the octadecanoid-signaling pathway. Plant Physiol 121:153–162

    PubMed  CAS  Google Scholar 

  • Korneef A, Pieterse CM (2008) Cross talk in defense signaling. Plant Physiol 146:839–844

    Google Scholar 

  • Kost C, Heil M (2006) Herbivore-induced plant volatiles induce an indirect defense in neighboring plants. J Ecol 94:619–628

    CAS  Google Scholar 

  • Kumar D, Klessig DF (2003) High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proc Natl Acad Sci USA 100:16101–16106

    PubMed  CAS  Google Scholar 

  • Laudert D, Schaller F, Weiler EW (2000) Transgenic Nicotiana tabacum and Arabidopsis thaliana plants overexpressing allene oxide synthase. Planta 211:163–165

    PubMed  CAS  Google Scholar 

  • Lee GI, Howe GA (2003) The tomato mutant spr1 is defective in systemin perception and the production of a systemic wound signal for defense gene expression. Plant J 33:567–576

    PubMed  CAS  Google Scholar 

  • Li C, Schilmiller AL, Liu GH, Lee GI, Jayanty S, Sagemann C, Vrebalov J, Giovannoni JJ, Yagi K, Kobayashi Y, Howe GA (2005) Role of ĂŸ-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17:971–986

    PubMed  CAS  Google Scholar 

  • Maffei ME, Mithöfer A, Boland W (2007a) Before gene expression: early events in plant-insect interaction. Trends Plant Sci 12:310–316

    PubMed  CAS  Google Scholar 

  • Maffei ME, Mithöfer A, Boland W (2007b) Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68:22–24

    Google Scholar 

  • Major IT, Constabel CP (2006) Molecular analysis of poplar defense against herbivory: comparison of wound- and insect elicitor-induced gene expression. New Phytol 172:617–635

    PubMed  CAS  Google Scholar 

  • Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002–1004

    PubMed  CAS  Google Scholar 

  • Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signaling in Arabidopsis. Nature 419:399–403

    PubMed  CAS  Google Scholar 

  • Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant–pathogen interactions. Curr Opin Plant Biol 8:409–414

    PubMed  CAS  Google Scholar 

  • McGurl B, Pearce G, Orozco-Cardenas ML, Ryan CA (1992) Structure, expression, and antisense inhibition of the systemin precursor gene. Science 255:1570–1573

    PubMed  CAS  Google Scholar 

  • MĂ©traux J-P, Signer H, Ryals J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W, Inverardi B (1990) Increase in salicylic acid at the onset of systemic acquired resistance. Science 250:1004–1006

    PubMed  Google Scholar 

  • Mishina TE, Zeier J (2007) Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J 50:500–513

    PubMed  CAS  Google Scholar 

  • Mithöfer A, Wanner G, Boland W (2005) Effects of feeding Spodoptera littoralis on Lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137:1160–1168

    PubMed  Google Scholar 

  • Mölders W, Buchala A, MĂ©traux JP (1996) Transport of salicylic acid in tobacco necrosis virus-infected cucumber plants. Plant Physiol 112:787–792

    PubMed  Google Scholar 

  • Mou Z, Fan W, Dong X (2003) nducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

    PubMed  CAS  Google Scholar 

  • Mur LA, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262

    PubMed  CAS  Google Scholar 

  • Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Herbivory: caterpillar saliva beats plant defenses. Nature 416:599–600

    PubMed  CAS  Google Scholar 

  • Mutikainen P, Walls M, Ovaska J (1996) Herbivore-induced resistance in Betula pendula: the role of plant vascular architecture. Oecologia 108:723–727

    Google Scholar 

  • Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, Sekimata K, Takatsuto S, Yamaguchi I, Yoshida S (2003) Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J 33:887–898

    PubMed  CAS  Google Scholar 

  • NarvĂ¡ez-VĂ¡squez J, Pearce G, Orozco-Cardenas ML, Franceschi VR, Ryan CA (1995) Autoradiographic and biochemical evidence for the systemic translocation of systemin in tomato plants. Planta 195:593–600

    Google Scholar 

  • NarvĂ¡ez-VĂ¡squez J, Pearce G, Ryan CA (2005) The plant cell wall matrix harbors a precursor of defense signaling peptides. Proc Natl Acad Sci USA 102:12974–12977

    PubMed  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    PubMed  CAS  Google Scholar 

  • Orians C (2005) Herbivores, vascular pathways, and systemic induction: facts and artifacts. J Chem Ecol 31:2231–2242

    PubMed  CAS  Google Scholar 

  • Orians CM, Pomerleau J, Rico R (2000) Vascular architecture generates fine scale variation in the systemic induction of proteinase inhibitors in tomato. J Chem Ecol 26:471–485

    CAS  Google Scholar 

  • ParĂ© PW, Alborn HT, Tumlinson JH (1998) Concerted biosynthesis of an insect elicitor of plant volatiles. Proc Natl Acad Sci USA 95:13971–13975

    PubMed  Google Scholar 

  • Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–116

    PubMed  CAS  Google Scholar 

  • Pearce G, Ryan CA (2003) Systemic signaling in tomato plants for defense against herbivores – Isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene. J Biol Chem 278:30044–30050

    PubMed  CAS  Google Scholar 

  • Peck SC (2003) Early phosphorylation events in biotic stress. Curr Opin Plant Biol 6:334–338

    PubMed  CAS  Google Scholar 

  • Peña-CortĂ©s H, Barrios P, Dorta F, Polanco V, SĂ¡chez C, SĂ¡nchez E, RamĂ­rez I (2005) Involvement of jasmonic acid and derivatives in plant responses to pathogens and insects and in fruit ripening. J Plant Growth Regul 23:246–260

    Google Scholar 

  • Peñuelas J, LlusiĂ¡ J (2004) Plant VOC emissions: making use of the unavoidable. Trends Ecol Evol 19:402–404

    PubMed  Google Scholar 

  • Pieterse CMJ, van Wees SCM, van Pelt JA, Knoester M, Laan R, Gerrits N, Weisbeek PJ, van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580

    PubMed  CAS  Google Scholar 

  • Rasmussen JB, Hammerschmidt R, Zook MN (1991) Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiol 97:1342–1347

    PubMed  CAS  Google Scholar 

  • Rhoades DF (1983) Responses of alder and willow to attack by tent caterpillars and webworms: evidence for pheromonal sensitivity of willows. In: Hedin PA (ed) Plant resistance to insects. American Chemical Society, Washington DC, USA, pp 55–68

    Google Scholar 

  • Robatzek S (2007) Vesicle trafficking in plant immune responses. Cell Microbiol 9:1–8

    PubMed  CAS  Google Scholar 

  • Ross AF (1961) Systemic acquired resistance induced by localized virus infection in plants. Virology 14:340–358

    PubMed  CAS  Google Scholar 

  • Ruther J, FĂ¼rstenau B (2005) Emission of herbivore-induced volatiles in absence of a herbivore – Response of Zea mays to green leaf volatiles and terpenoids. Z Naturforsch C Biosci 60:743–756

    CAS  Google Scholar 

  • Ruther J, Kleier S (2005) Plant-plant signaling: Ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-Hexen-1-ol. J Chem Ecol 31:2217–2222

    PubMed  CAS  Google Scholar 

  • Ryals J, Neuenschwander U, Willits M, Molina A, Steiner H, Hunt M (1996) Systemic acquired resistance. Plant Cell 8:1809–1819

    PubMed  CAS  Google Scholar 

  • Ryan CA (1974) Assay and biochemical properties of the proteinase inhibitor inducing factor, a wound hormone. Plant Physiol 54:328–332

    PubMed  CAS  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932

    PubMed  CAS  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

    PubMed  CAS  Google Scholar 

  • Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377

    PubMed  CAS  Google Scholar 

  • Schittko U, Baldwin IT (2003) Constraints to herbivore-induced systemic responses: Bidirectional signaling along orthostichies in Nicotiana attenuata. J Chem Ecol 29:763–770

    PubMed  CAS  Google Scholar 

  • Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, Chourey PS, Alborn HT, Teal PEA (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci USA 103:8894–8899

    PubMed  CAS  Google Scholar 

  • Schmidt S, Baldwin IT (2006) Systemin in Solanum nigrum. The tomato-homologous polypeptide does not mediate direct defense responses. Plant Physiol 142:1751–1758

    PubMed  CAS  Google Scholar 

  • Schwessinger B, Zipfel C (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11:389–395

    PubMed  CAS  Google Scholar 

  • Shah J, Tsui F, Klessig DF (1997) Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol Plant Microbe Interact 10:69–78

    PubMed  CAS  Google Scholar 

  • Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G, Horiuchi J, Nishioka T, Matsui K, Takabayashi J (2006) Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc Natl Acad Sci USA 103:16672–16676

    PubMed  CAS  Google Scholar 

  • Shulaev V, Leon J, Raskin I (1995) Is salicylic acid a translocated signal of systemic acquired resistance in tobacco. Plant Cell 7:1691–1701

    PubMed  CAS  Google Scholar 

  • Shulaev V, Silverman P, Raskin I (1997) Airborne signaling by methyl salicylate in plant pathogen resistance. Nature 385:718–721

    CAS  Google Scholar 

  • Skibbe M, Qu N, Galis I, Baldwin IT (2008) Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20:1984–2000

    PubMed  CAS  Google Scholar 

  • Smith-Becker J, Marois E, Huguet EJ, Midland SL, Sims J, Keen NT (1998) Accumulation of salicylic acid and 4-hydroxybenzoic acid in phloem fluids of cucumber during systemic acquired resistance is preceded by a transient increase in phenylalanine ammonia-lyase activity in petioles and stems. Plant Physiol 116:231–238

    PubMed  CAS  Google Scholar 

  • Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, van Pelt JA, Mueller MJ, Buchala AJ, MĂ©traux J-P, Brown R, Kazan K, van Loon LC, Dong XN, Pieterse CMJ (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770

    PubMed  CAS  Google Scholar 

  • Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci USA 104:18842–18847

    PubMed  CAS  Google Scholar 

  • Stankovic B, Davies E (1996) Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato. FEBS Lett 390:275–279

    PubMed  CAS  Google Scholar 

  • Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13:66–71

    PubMed  CAS  Google Scholar 

  • Stenzel I, Hause B, Maucher H, Pitzschke A, Miersch O, Ziegler J, Ryan CA, Wasternack C (2003) Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato – amplification in wound-signaling. Plant J 33:577–589

    PubMed  CAS  Google Scholar 

  • Stratmann JW (2003) Long distance run in the wound response – jasmonic acid is pulling ahead. Trends Plant Sci 8:247–250

    PubMed  CAS  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu GH, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signaling. Nature 448:661–666

    PubMed  CAS  Google Scholar 

  • Thorpe MR, Ferrieri AP, Herth MM, Ferrieri RA (2007) 11C-imaging: methyl jasmonate moves in both phloem and xylem, promotes transport of jasmonate, and of photoassimilate even after proton transport is decoupled. Planta 226:541–551

    PubMed  CAS  Google Scholar 

  • Ton J, Van Pelt JA, Van Loon LC, Pieterse CMJ (2002) Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Mol Plant Microbe Interact 15:27–34

    PubMed  CAS  Google Scholar 

  • Ton J, D'Allesandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TCJ (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26

    PubMed  CAS  Google Scholar 

  • Truman W, Bennettt MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci USA 104:1075–1080

    PubMed  CAS  Google Scholar 

  • Tscharntke T, Thiessen S, Dolch R, Boland W (2001) Herbivory, induced resistance, and interplant signal transfer in Alnus glutinosa. Biochem Syst Ecol 29:1025–1047

    CAS  Google Scholar 

  • Turlings TCJ, Ton J (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Curr Opin Plant Biol 9:421–427

    PubMed  Google Scholar 

  • Turlings TCJ, Wäckers FL (2004) Recruitment of predators and parasitoids by herbivore-injured plants. In: CardĂ©s RT, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 21–75

    Google Scholar 

  • Van Bel AJE, Gaupels F (2004) Pathogen-induced resistance and alarm signals in the phloem. Mol Plant Pathol 5:495–504

    Google Scholar 

  • Van der Ent S (2008) Transcriptional regulators of rhizobacteria-induced systemic resistance. Utrecht University, Utrecht, pp 181

    Google Scholar 

  • Van Dongen JT, Frohlich A, Ramirez-Aguilar SJ, Schauer N, Fernie AR, Erban A, Kopka J, Clark J, Langer A, Geigenberger P (2008) Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of Arabidopsis plants. Ann Bot 103:269–280

    PubMed  Google Scholar 

  • Van Loon LC (1997) Induced resistance in plants and the role of pathogenesis-related proteins. Eur J Plant Pathol 103:753–765

    Google Scholar 

  • Van Loon LC, Geraats BPJ, Linthorst HJM (2006) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11:184–191

    PubMed  Google Scholar 

  • Van Poecke RMP, Dicke M (2003) Signal transduction downstream of salicylic and jasmonic acid in herbivory-induced parasitoid attraction by Arabidopsis is independent of JAR1 and NPR1. Plant Cell Environ 26:1541–1548

    Google Scholar 

  • Van Wees SCM, De Swart EAM, Van Pelt JA, Van Loon LC, Pieterse CMJ (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:8711–8716

    PubMed  Google Scholar 

  • Velikova V, Pinelli P, Pasqualini S, Reale L, Ferranti F, Loreto F (2005) Isoprene decreases the concentration of nitric oxide in leaves exposed to elevated ozone. New Phytol 166:419–426

    PubMed  CAS  Google Scholar 

  • Vernooij B, Friedrich L, Morse A, Reist R, Kolditz-Jawhar R, Ward E, Uknes S, Kessmann H, Ryals J (1994) Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6:959–965

    PubMed  CAS  Google Scholar 

  • von Dahl CC, Baldwin IT (2007) Deciphering the role of ethylene in plant-herbivore interactions. J Plant Growth Regul 26:201–209

    CAS  Google Scholar 

  • Wang CX, Avdiushko S, Hildebrand DF (1999) Overexpression of a cytoplasm-localized allene oxide synthase promotes the wound-induced accumulation of jasmonic acid in transgenic tobacco. Plant Mol Biol 40:783–793

    PubMed  CAS  Google Scholar 

  • Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–1040

    PubMed  CAS  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setala H, Van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    PubMed  CAS  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    PubMed  CAS  Google Scholar 

  • Wasternack C, Stenzel I, Hause B, Hause G, Kutter C, Maucher H, Neumerkel J, Feussner I, Miersch O (2006) The wound response in tomato – role of jasmonic acid. J Plant Physiol 163:297–306

    PubMed  CAS  Google Scholar 

  • Xu Y, Chang PFL, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM, Bressan RA (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6:1077–1085

    PubMed  CAS  Google Scholar 

  • Zhang Z-P, Baldwin IT (1997) Transport of [2–14C]jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris. Planta 203:436–441

    CAS  Google Scholar 

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Heil, M., Ton, J. (2010). Systemic Resistance Induction by Vascular and Airborne Signaling. In: LĂ¼ttge, U., Beyschlag, W., BĂ¼del, B., Francis, D. (eds) Progress in Botany 71. Progress in Botany, vol 71. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02167-1_11

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